Review: Capripoxvirus Diseases: Current Status and Opportunities for Control

Transboundary and Emerging Diseases

Volumn 64, Issue 3, 2017, Pages 729-745

  Tuppurainen, E S M ^a   Venter, E H ^b   Shisler, J L ^c   Gari, G ^d   Mekonnen, G A ^d   Juleff, N ^e   Lyons, N A ^f,g   De Clercq, K ^h   Upton, C ⁱ   Bowden, T R ^j   Babiuk, S ^k   Babiuk, L A ^l  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d National Animal Health Diagnostics and Investigation Center (NAHDIC)   (Ethiopia)

^e BILL AND MELINDA GATES FOUNDATION   (United States)

^f INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^g FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS   (Italy)

^h VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

ⁱ UNIVERSITY OF VICTORIA   (Canada)

^j CSIRO   (Australia)

^k CANADIAN FOOD INSPECTION AGENCY   (Canada)

^l UNIVERSITY OF ALBERTA   (Canada)

more..

Author keywords

control; goatpox; immunity; lumpy skin disease; sheeppox; vaccines

Indexed keywords

MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; SMALLPOX VACCINE; VIRUS VECTOR;

CAPRIPOXVIRUS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DISEASE PREDISPOSITION; DISEASE SEVERITY; GEOGRAPHIC DISTRIBUTION; GOATPOX; IMMUNITY; LUMPY SKIN DISEASE; MORTALITY RATE; NONHUMAN; REVIEW; SHEEPPOX; VACCINATION; VIRUS INFECTION; VIRUS TRANSMISSION; ANIMAL; DISEASE OUTBREAKS; IMMUNOLOGY; POXVIRUS INFECTION; VETERINARY;

ANIMALS; CAPRIPOXVIRUS; DISEASE OUTBREAKS; POXVIRIDAE INFECTIONS;

EID: 85018713448     PISSN: 18651674     EISSN: 18651682     Source Type: Journal    
DOI: 10.1111/tbed.12444     Document Type: Review

References (117)

1. Abutarbush, S. M., 2014: Efficacy of vaccination against lumpy skin disease in Jordanian cattle. Vet. Rec. 175, 302.
2. Abutarbush, S. M., M. M. Ababneh, I. G. Al Zoubi, O. M. Al Sheyab, M. G. Al Zoubi, M. O. Alekish, and R. J. Al Gharabat, 2013: Lumpy skin disease in Jordan: disease emergence, clinical signs, complications and preliminary-associated economic losses. Transbound. Emerg. Dis. 62, 549–554.
3. Abutarbush, S. M., W. M. Hananeh, W. Ramadan, O. M. Al Sheyab, A. R. Alnajjar, I. G. Al Zoubi, N. J. Knowles, K. Bachanek-Bankowska, and E. S. Tuppurainen, 2016: Adverse reactions to field vaccination against lumpy skin disease in Jordan. Transbound. Emerg. Dis. 63, e213–e219.
4. Ali, B. H., and H. M. Obeid, 1977: Investigation of the first outbreaks of lumpy skin disease in Sudan. Br. Vet. J. 133, 184–189.
5. Al-Salihi, K. A., and I. Q. Hassan, 2015: Lumpy skin disease in iraq: study of the disease emergence. Transbound. Emerg. Dis. 62, 457–462.
6. Annandale, C. H., P. C. Irons, V. P. Bagla, U. I. Osuagwuh, and E. H. Venter, 2010: Sites of persistence of lumpy skin disease virus in the genital tract of experimentally infected bulls. Reprod. Domest. Anim. 45, 250–255.
7. Annandale, C. H., D. E. Holm, K. Ebersohn, and E. H. Venter, 2013: Seminal transmission of lumpy skin disease virus in heifers. Transbound. Emerg. Dis. 61, 443–448.
8. Antoine, G., F. Scheiflinger, F. Dorner, and F. G. Falkner, 1998: The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244, 365–396.
9. Ayelet, G., Y. Abate, T. Sisay, H. Nigussie, E. Gelaye, S. Jemberie, and K. Asmare, 2013: Lumpy skin disease: preliminary vaccine efficacy assessment and overview on outbreak impact in dairy cattle at Debre Zeit, central Ethiopia. Antiviral Res. 98, 261–265.
10. Ayelet, G., R. Haftu, S. Jemberie, A. Belay, E. Gelaye, B. Sibhat, E. Skjerve, and K. Asmare, 2014: Lumpy skin disease in cattle in central Ethiopia: outbreak investigation and isolation and molecular detection of the virus. Rev. Sci. Tech. 33, 877–887.
11. Babiuk, S., G. Parkyn, J. Copps, J. E. Larence, M. I. Sabara, T. R. Bowden, D. B. Boyle, and R. P. Kitching, 2007: Evaluation of an ovine testis cell line (OA3.Ts) for propagation of capripoxvirus isolates and development of an immunostaining technique for viral plaque visualization. J. Vet. Diagn. Invest. 19, 486–491.
12. Babiuk, S., T. R. Bowden, G. Parkyn, B. Dalman, L. Manning, J. Neufeld, C. Embury-Hyatt, J. Copps, and D. B. Boyle, 2008: Quantification of lumpy skin disease virus following experimental infection in cattle. Transbound. Emerg. Dis. 55, 299–307.
13. Bagla, V. P., U. I. Osuagwuh, C. H. Annandale, P. C. Irons, and E. H. Venter, 2006: Elimination of toxicity and enhanced detection of lumpy skin disease virus on cell culture from experimentally infected bovine semen samples. Onderstepoort J. Vet. Res. 73, 263–268.
14. Balinsky, C. A., G. Delhon, C. L. Afonso, G. R. Risatti, M. V. Borca, R. A. French, E. R. Tulman, S. J. Geary, and D. L. Rock, 2007: Sheeppox virus kelch-like gene SPPV-019 affects virus virulence. J. Virol. 81, 11392–11401.
15. Banerjee, A., E. Duflo, N. Goldberg, D. Karlan, R. Osei, W. Pariente, J. Shapiro, B. Thuysbaert, and C. Udry, 2015: A multifaceted program causes lasting progress for the very poor: evidence from six countries. Science 80, 348, 1260799.
16. Barnard, B. J. H., 1997: Antibodies against some viruses of domestic animals in South African wild animals. Onderstepoort J. Vet. Res. 64, 95–110.
17. Ben-Gera, J., E. Klement, E. Khinich, Y. Stram, and N. Y. Shpigel, 2015: Comparison of the efficacy of Neethling lumpy skin disease virus and x10RM65 sheep-pox live attenuated vaccines for the prevention of lumpy skin disease – The results of a randomized controlled field study. Vaccine 33, 4837–4842.
18. Berhe, G., C. Minet, C. Le Goff, T. Barrett, A. Ngangnou, C. Grillet, G. Libeau, M. Fleming, D. N. Black, and A. Diallo, 2003: Development of a dual recombinant vaccine to protect small ruminants against peste-des-petits-ruminants virus and capripoxvirus infections. J. Virol. 77, 1571–1577.
19. Bhanot, V., V. Balamurugan, V. Bhanuprakash, G. Venkatesan, A. Sen, V. Yadav, R. Yogisharadhya, and R. K. Singh, 2009: Expression of P32 protein of goatpox virus in Pichia pastoris and its potential use as a diagnostic antigen in ELISA. J. Virol. Methods 162, 251–257.
20. Bhanuprakash, V., B. K. Indrani, M. Hosamani, and R. K. Singh, 2006: The current status of sheep pox disease. Comp. Immunol. Microbiol. Infect. Dis. 29, 27–60.
21. Bielanski, A., 2007: Disinfection procedures for controlling microorganism in the semen and embryos of humens and farm animals. Theriogenology 68, 1–22.
22. Boshra, H., T. Truong, C. Nfon, V. Gerdts, S. Tikoo, L. A. Babiuk, P. Kara, A. Mather, D. Wallace, and S. Babiuk, 2013: Capripoxvirus-vectored vaccines against livestock diseases in Africa. Antivir. Res. 98, 217–227.
23. Boulter, E. A., and G. Appleyard, 1973: Differences between extracellular and intracellular forms of poxvirus and their implications. Prog. Med. Virol. 16, 86–108.
24. Bowden, T. R., S. L. Babiuk, G. R. Parkyn, J. S. Copps, and D. B. Boyle, 2008: Capripoxvirus tissue tropism and shedding: a quantitative study in experimentally infected sheep and goats. Virology 371, 380–393.
25. Bowden, T. R., B. E. Coupar, S. L. Babiuk, J. R. White, V. Boyd, C. J. Duch, B. J. Shiell, N. Ueda, G. R. Parkyn, J. S. Copps, and D. B. Boyle, 2009: Detection of antibodies specific for sheeppox and goatpox viruses using recombinant capripoxvirus antigens in an indirect enzyme-linked immunosorbent assay. J. Virol. Methods 161, 19–29.
26. Brenner, J., M. Bellaiche, E. Gross, D. Elad, Z. Oved, M. Haimovitz, A. Wasserman, O. Friedgut, Y. Stram, V. Bumbarov, and H. Yadin, 2009: Appearance of skin lesions in cattle populations vaccinated against lumpy skin disease: statutory challenge. Vaccine 27, 1500–1503.
27. Carn, V. M., and R. P. Kitching, 1995a: The clinical response of cattle experimentally infected with lumpy skin disease (Neethling) virus. Arch. Virol. 140, 503–513.
28. Carn, V. M., and R. P. Kitching, 1995b: An investigation of possible routes of transmission of lumpy skin disease virus (Neethling). Epidemiol. Infect. 114, 219–226.
29. Carn, V. M., R. P. Kitching, J. M. Hammond, and P. Chand, 1994: Use of a recombinant antigen in an indirect ELISA for detecting bovine antibody to capripoxvirus. J. Virol. Methods 49, 285–294.
30. Caufour, P., T. Rufael, C. E. Lamien, R. Lancelot, M. Kidane, D. Awel, T. Sertse, O. Kwiatek, G. Libeau, M. Sahle, A. Diallo, and E. Albina, 2014: Protective efficacy of a single immunization with capripoxvirus-vectored recombinant peste des petits ruminants vaccines in presence of pre-existing immunity. Vaccine 32, 3772–3779.
31. Chen, W., S. Hu, L. Qu, Q. Hu, Q. Zhang, H. Zhi, K. Huang, and Z. Bu, 2010: A goat poxvirus-vectored peste-des-petits-ruminants vaccine induces long-lasting neutralization antibody to high levels in goats and sheep. Vaccine 28, 4742–4750.
32. Chihota, C. M., L. F. Rennie, R. P. Kitching, and P. S. Mellor, 2001: Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera : Culicidae). Epidemiol. Infect. 126, 317–321.
33. Chihota, C. M., L. F. Rennie, R. P. Kitching, and P. S. Mellor, 2003: Attempted mechanical transmission of lumpy skin disease virus by biting insects. Med. Vet. Entomol. 17, 294–300.
34. Coetzer, J. A. W., 2004: Lumpy skin disease. In: Coetzer, J. A. W. and R. C. Tustin (eds), Infectious Diseases of Livestock, pp. 1268–1276. University Press Southern Africa, Oxford.
35. Davies, F. G., 1982: Observations on the epidemiology of lumpy skin disease in Kenya. J. Hyg. (Lond) 88, 95–102.
36. Davies, F. G., 1991a: Lumpy skin disease of cattle: a growing problem in Africa and the Near East. World Anim. Rev. 68, 37–42.
37. Davies, F. G., 1991b: Lumpy skin disease, an African capripox virus disease of cattle. Br. Vet. J. 147, 489–503.
38. Diallo, A., C. Minet, G. Berhe, C. Le Goff, D. N. Black, M. Fleming, T. Barrett, C. Grillet, and G. Libeau, 2002: Goat immune response to capripox vaccine expressing the hemagglutinin protein of peste des petits ruminants. Ann. N. Y. Acad. Sci. 969, 88–91.
39. Downie, A. W., and C. K. McCarthy, 1958: The antibody response in man following infection with viruses of the pox group. III. Antibody response in smallpox. J. Hyg. 56, 479–487.
40. El-Nahas, E. M., A. S. El-Habbaa, G. F. El-Bagoury, and M. E. I. Radwan, 2011: Isolation and identification of lumpy skin disease virus from naturally infected buffaloes at Kaluobia. Egypt. Glob. Vet. 7, 234–237.
41. Embury-Hyatt, C., S. Babiuk, L. Manning, S. Ganske, T. R. Bowden, D. B. Boyle, and J. Copps, 2012: Pathology and viral antigen distribution following experimental infection of sheep and goats with capripoxvirus. J. Comp. Pathol. 146, 106–115.
42. Fagbo, S., J. A. W. Coetzer, and E. H. Venter, 2014: Seroprevalence of Rift Valley fever and lumpy skin disease in African buffalo (Syncerus caffer) in the Kruger National Park and Hluhluwe-iMfolozi Park, South Africa. J. S. Afr. Vet. Assoc. 85, 1075.
43. Galasso, G. J., M. J. Mattheis, J. D. Cherry, J. D. Connor, K. McIntosh, A. S. Benenson, and D. W. Alling, 1977: Clinical and serologic study of four smallpox vaccines comparing variations of dose and route of administration. Summary. J. Infect. Dis. 135, 183–186.
44. Galmiche, M. C., J. Goenaga, R. Wittek, and L. Rindisbacher, 1999: Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254, 71–80.
45. Gari, G., P. Bonnet, F. Roger, and A. Waret-Szkuta, 2011: Epidemiological aspects and financial impact of lumpy skin disease in Ethiopia. Prev. Vet. Med. 102, 274–283.
46. Gari, G., G. Abie, D. Gizaw, A. Wubete, M. Kidane, H. Asgedom, B. Bayissa, G. Ayelet, C. A. L. Oura, F. Roger, and E. S. M. Tuppurainen, 2015: Evaluation of the safety, immunogenicity and efficacy of three capripoxvirus vaccine strains against lumpy skin disease virus. Vaccine 33, 3256–3261.
47. Garner, M. G., and M. B. Lack, 1995: An evaluation of alternate control strategies for foot and mouth disease in Australia – A regional approach. Prev. Vet. Med. 23, 9–32.
48. Gates, M. F., 2014: Putting women and girls at the center of development. Science 345, 1273–1275.
49. Gelaye, E., A. Belay, G. Ayelet, S. Jenberie, M. Yami, A. Loitsch, E. Tuppurainen, R. Grabherr, A. Diallo, and C. E. Lamien, 2015: Capripox disease in Ethiopia: genetic differences between field isolates and vaccine strain, and implications for vaccination failure. Antiviral Res. 119, 28–35.
50. Golden, J. W., and J. W. Hooper, 2008: Heterogeneity in the A33 protein impacts the cross-protective efficacy of a candidate smallpox DNA vaccine. Virology 377, 19–29.
51. Gordon, J., A. Mohandas, S. Wilton, and S. Dales, 1991: A prominent antigenic surface polypeptide involved in the biogenesis and function of the vaccinia virus envelope. Virology 181, 671–686.
52. Green, H. F., 1959: Lumpy skin disease: its effect on hides and leather and a comparison on this respect with some other skin diseases. Bull. Epizoot. Dis. Afr. 7, 63–74.
53. Haig, D. A., 1957: Lumpy skin disease. Bull. Epizoot. Dis. Afr. 5, 421–430.
54. Halloran, M. E., M. Haber, I. M. J. Longini, and C. J. Struchiner, 1991: Direct and indirect effects in vaccine efficacy and effectiveness. Am. J. Epidemiol. 133, 323–331.
55. Halloran, M. E., I. M. Longini, and C. J. Struchiner, 1999: Design and interpretation of vaccine field studies. Epidemiol. Rev. 21, 73–88.
56. Heine, H. G., M. P. Stevens, A. J. Foord, and D. B. Boyle, 1999: A capripoxvirus detection PCR and antibody ELISA based on the major antigen P32, the homolog of the vaccinia Virus H3L gene. J. Immunol. Methods 227, 187–196.
57. Heraud, J. M., Y. Edghill-Smith, V. Ayala, I. Kalisz, J. Parrino, V. S. Kalyanaraman, J. Manischewitz, L. R. King, A. Hryniewicz, C. J. Trindade, M. Hassett, W. P. Tsai, D. Venzon, A. Nalca, M. Vaccari, P. Silvera, M. Bray, B. S. Graham, H. Golding, J. W. Hooper, and G. Franchini, 2006: Subunit recombinant vaccine protects against monkeypox. J. Immunol. 177, 2552–2564.
58. Hooper, J. W., D. M. Custer, and E. Thompson, 2003: Four-gene-combination DNA vaccine protects mice against a lethal vaccinia virus challenge and elicits appropriate antibody responses in nonhuman primates. Virology 306, 181–195.
59. Hsiao, J. C., C. S. Chung, and W. Chang, 1999: Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J. Virol. 73, 8750–8761.
60. Hunter, P., and D. Wallace, 2001: Lumpy skin disease in southern Africa: a review of the disease and aspects of control. J. S. Afr. Vet. Assoc. 72, 68–71.
61. Irons, P. C., E. S. M. Tuppurainen, and E. H. Venter, 2005: Excretion of lumpy skin disease virus in bull semen. Theriogenology 63, 1290–1297.
62. Jing, L., T. M. Chong, C. L. McClurkan, J. Huang, B. T. Story, and D. M. Koelle, 2005: Diversity in the acute CD8 T cell response to vaccinia virus in humans. J. Immunol. 175, 7550–7559.
63. Kara, P. D., C. L. Afonso, D. B. Wallace, G. F. Kutish, C. Abolnik, Z. Lu, F. T. Vreede, L. C. F. Taljaard, A. Zsak, G. J. Viljoen, and D. L. Rock, 2003: Comparative sequence analysis of the South African vaccine strain and two virulent field isolates of lumpy skin disease virus. Arch. Virol. 148, 1335–1356.
64. Khalafalla, A. I., M. A. Gaffar Elamin, and Z. Abbas, 1993: Lumpy skin disease: observations on the recent outbreaks of the disease in the Sudan. Rev. Elev. Med. Vet. Pays Trop. 46, 548–550.
65. Kitching, R. P., 1986a: The control of sheep and goat pox. Rev. Sci. Tech. Off. Int. des Epizoot. 5, 503–511.
66. Kitching, R. P., 1986b: Passive protection of sheep against capripoxvirus. Res. Vet. Sci. 41, 247–250.
67. Kitching, R. P., 2003: Vaccines for lumpy skin disease, sheep pox and goat pox. Dev. Biol. 114, 161–167.
68. Kitching, R. P., and P. S. Mellor, 1986: Insect transmission of capripoxvirus. Res. Vet. Sci. 40, 255–258.
69. Kitching, R. P., J. M. Hammond, and W. P. Taylor, 1987: A single vaccine for the control of capripox infection in sheep and goats. Res. Vet. Sci. 42, 53–60.
70. Klausner, Z., E. Fattal, and E. Klement, 2017: Using synoptic systems’ typical wind trajectories for the analysis of potential atmospheric long-distance dispersal of lumpy skin disease virus. Transbound. Emerg. Dis. 64, 398–410.
71. Knight-Jones, T. J. D., K. Edmond, S. Gubbins, and D. J. Paton, 2014: Veterinary and human vaccine evaluation methods. Proc. Biol. Sci. 281, 20132839.
72. Lamien, C. E., C. Le Goff, R. Silber, D. B. Wallace, V. Gulyaz, E. Tuppurainen, H. Madani, P. Caufour, T. Adam, M. El Harrak, A. G. Luckins, E. Albina, and A. Diallo, 2011a: Use of the Capripoxvirus homologue of Vaccinia virus 30 kDa RNA polymerase subunit (RPO30) gene as a novel diagnostic and genotyping target: Development of a classical PCR method to differentiate goat poxvirus from sheep poxvirus. Vet. Microbiol. 149, 30–39.
73. Lamien, C. E., M. Lelenta, W. Goger, R. Silber, E. Tuppurainen, M. Matijevic, A. G. Luckins, and A. Diallo, 2011b: Real time PCR method for simultaneous detection, quantitation and differentiation of capripoxviruses. J. Virol. Methods 171, 134–140.
74. Le Goff, C., C. E. Lamien, E. Fakhfakh, A. Chadeyras, E. Aba-Adulugba, G. Libeau, E. Tuppurainen, D. B. Wallace, T. Adam, R. Silber, V. Gulyaz, H. Madani, P. Caufour, S. Hammami, A. Diallo, and E. Albina, 2009: Capripoxvirus G-protein-coupled chemokine receptor: a host-range gene suitable for virus animal origin discrimination. J. Gen. Virol. 90, 1967–1977.
75. Lubinga, J. C., E. S. M. Tuppurainen, W. H. Stoltsz, K. Ebersohn, J. A. W. Coetzer, and E. H. Venter, 2013: Detection of lumpy skin disease virus in saliva of ticks fed on lumpy skin disease virus-infected cattle. Exp. Appl. Acarol. 61, 129–138.
76. Lubinga, J. C., E. S. M. Tuppurainen, J. A. W. Coetzer, W. H. Stoltsz, and E. H. Venter, 2014: Evidence of lumpy skin disease virus over-wintering by transstadial persistence in Amblyomma hebraeum and transovarial persistence in Rhipicephalus decoloratus ticks. Exp. Appl. Acarol. 62, 77–90.
77. Mack, T. M., J. Jr Noble, and D. B. Thomas, 1972: A prospective study of serum antibody and protection against smallpox. Am. J. Trop. Med. Hyg. 21, 214–218.
78. Mayr, A., V. Hochstein-Mintzel, and H. Stickl, 1975: Creation of an attenuated strain of Ankara, MVA. Infection 3, 6–14.
79. McClain, D. J., S. Harrison, C. L. Yeager, J. Cruz, F. A. Ennis, P. Gibbs, M. S. Wright, P. L. Summers, J. D. Arthur, and J. A. Graham, 1997: Immunologic responses to vaccinia vaccines administered by different parenteral routes. J. Infect. Dis. 175, 756–763.
80. Moss, B., 2011: Smallpox vaccines: targets of protective immunity. Immunol. Rev. 239, 8–26.
81. Moutaftsi, M., D. C. Tscharke, K. Vaughan, D. M. Koelle, L. Stern, M. Calvo-Calle, F. Ennis, M. Terajima, G. Sutter, S. Crotty, I. Drexler, G. Franchini, J. W. Yewdell, S. R. Head, J. Blum, B. Peters, and A. Sette, 2010: Uncovering the interplay between CD8, CD4 and antibody responses to complex pathogens. Future Microbiol. 5, 221–239.
82. Nawathe, D. R., M. O. Asagba, A. Abegunde, S. A. Ajayi, and L. Durkwa, 1982: Some observations on the occurrence of lumpy skin disease in Nigeria. Zentralbl Veterinarmed B. 29, 31–36.
83. Ngichabe, C. K., H. M. Wamwayi, E. K. Ndungu, P. K. Mirangi, C. J. Bostock, D. N. Black, and T. Barrett, 2002: Long term immunity in African cattle vaccinated with a recombinant capripox-rinderpest virus vaccine. Epidemiol. Infect. 128, 343–349.
84. Osuagwuh, U. I., V. Bagla, E. H. Venter, C. H. Annandale, and P. C. Irons, 2007: Absence of lumpy skin disease virus in semen of vaccinated bulls following vaccination and subsequent experimental infection. Vaccine 25, 2238–2243.
85. Pasick, J., 2004: Application of DIVA vaccines and their companion diagnostic tests to foreign animal disease eradication. Anim. Health Res. Rev. 5, 257–262.
86. Perrin, A., E. Albina, E. Breard, C. Sailleau, S. Prome, C. Grillet, O. Kwiatek, P. Russo, R. Thiery, S. Zientara, and C. Cetre-Sossah, 2007: Recombinant capripoxviruses expressing proteins of bluetongue virus: evaluation of immune responses and protection in small ruminants. Vaccine 25, 6774–6783.
87. Perry, B., and D. Grace, 2009: The impacts of livestock diseases and their control on growth and development processes that are pro-poor. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2643–2655.
88. Rao, T. V., and S. K. Bandyopadhyay, 2000: A comprehensive review of goat pox and sheep pox and their diagnosis. Anim. Health Res. Rev. 1, 127–136.
89. Rodriguez, J. F., R. Janeczko, and M. Esteban, 1985: Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. J. Virol. 56, 482–488.
90. Romero, C. H., T. Barrett, R. W. Chamberlain, R. P. Kitching, M. Fleming, and D. N. Black, 1994: Recombinant capripoxvirus expressing the hemagglutinin protein gene of Rinderpest virus protection of cattle against Rinderpest and Lumpy skin disease viruses. Virology 204, 425–429.
91. Romero, C. H., T. Barrett, R. P. Kitching, C. Bostock, and D. N. Black, 1995: Protection of goats against peste-des-petits-ruminants with recombinant capripoxviruses expressing the fusion and haemagglutinin protein genes of rinderpest virus. Vaccine 13, 36–40.
92. Salib, F. A., and A. H. Osman, 2011: Incidence of lumpy skin disease among Egyptian cattle in Giza Governorate, Egypt. Vet. World 4, 162–167.
93. Sette, A., H. Grey, C. Oseroff, B. Peters, M. Moutaftsi, S. Crotty, E. Assarsson, J. Greenbaum, Y. Kim, R. Kolla, D. Tscharke, D. Koelle, R. P. Johnson, J. Blum, S. Head, and J. Sidney, 2009: Definition of epitopes and antigens recognized by vaccinia specific immune responses: their conservation in variola virus sequences, and use as a model system to study complex pathogens. Vaccine 27(Suppl 6), G21–G26.
94. Soi, R. K., F. R. Rurangirwa, T. C. McGuire, P. M. Rwambo, J. C. DeMartini, and T. B. Crawford, 2010: Protection of sheep against Rift Valley fever virus and sheep poxvirus with a recombinant capripoxvirus vaccine. Clin. Vaccine Immunol. 17, 1842–1849.
95. Somasundaram, M. K., 2011: An outbreak of lumpy skin disease in a Holstein Dairy Herd in Oman: a clinical report. Asian J. Anim. Vet. Adv. 6, 851–859.
96. Tageldin, M. H., D. B. Wallace, G. H. Gerdes, J. F. Putterill, R. R. Greyling, M. N. Phosiwa, R. M. Al Busaidy, and S. I. Al Ismaaily, 2014: Lumpy skin disease of cattle: an emerging problem in the Sultanate of Oman. Trop. Anim. Health Prod. 46, 241–246.
97. Tscharke, D. C., G. Karupiah, J. Zhou, T. Palmore, K. R. Irvine, S. M. Haeryfar, S. Williams, J. Sidney, A. Sette, J. R. Bennink, and J. W. Yewdell, 2005: Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 201, 95–104.
98. Tulman, E. R., C. L. Afonso, Z. Lu, L. Zsak, G. F. Kutish, and D. L. Rock, 2001: Genome of lumpy skin disease virus. J. Virol. 75, 7122–7130.
99. Tulman, E. R., C. L. Afonso, Z. Lu, L. Zsak, J. H. Sur, N. T. Sandybaev, U. Z. Kerembekova, V. L. Zaitsev, G. F. Kutish, and D. L. Rock, 2002: The genomes of sheeppox and goatpox viruses. J. Virol. 76, 6054–6061.
100. Tuppurainen, E., and C. Oura, 2014: Lumpy skin disease: an African cattle disease getting closer to the EU. Vet. Rec. 175, 300–301.
101. Tuppurainen, E. S. M., E. H. Venter, and J. A. W. Coetzer, 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.
102. Tuppurainen, E. S. M., W. H. Stoltsz, M. Troskie, D. B. Wallace, C. A. L. Oura, P. S. Mellor, J. A. W. Coetzer, and E. H. Venter, 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.
103. Tuppurainen, E. S. M., J. C. Lubinga, W. H. Stoltsz, M. Troskie, S. T. Carpenter, J. A. W. Coetzer, E. H. Venter, and C. A. L. Oura, 2013a: Mechanical transmission of lumpy skin disease virus by Rhipicephalus appendiculatus male ticks. Epidemiol. Infect. 141, 425–430.
104. Tuppurainen, E. S. M., J. C. Lubinga, W. H. Stoltsz, M. Troskie, S. T. Carpenter, J. A. W. Coetzer, E. H. Venter, and C. A. L. Oura, 2013b: Evidence of vertical transmission of lumpy skin disease virus in Rhipicephalus decoloratus ticks. Ticks Tick. Borne. Dis. 4, 329–333.
105. Tuppurainen, E. S., C. R. Pearson, K. Bachanek-Bankowska, N. J. Knowles, S. Amareen, L. Frost, M. R. Henstock, C. E. Lamien, A. Diallo, and P. P. Mertens, 2014: Characterization of sheep pox virus vaccine for cattle against lumpy skin disease virus. Antiviral Res. 109, 1–6.
106. Uttenthal, A., S. Parida, T. B. Rasmussen, D. J. Paton, B. Haas, and W. G. Dundon, 2010: Strategies for differentiating infection in vaccinated animals (DIVA) for foot-and-mouth disease, classical swine fever and avian influenza. Expert. Rev. Vaccines 9, 73–87.
107. Van Oirschot, J. T., H. J. Rziha, P. J. Moonen, J. M. Pol, and D. van Zaane, 1986: Differentiation of serum antibodies from pigs vaccinated or infected with Aujeszky's disease virus by a competitive enzyme immunoassay. J. Gen. Virol. 67(6), 1179–1182.
108. Vannie, P., I. Capua, M. F. Le Potier, D. K. J. Mackay, B. Muylkens, S. Parida, D. J. Paton, and E. Thiry, 2007: Marker vaccines and the impact of their use on diagnosis and prophylactic measures. Rev. Sci. Tech. 26, 351–372.
109. Vaucher, P., 2009: Designing phase III or IV trials for vaccines: choosing between individual or cluster randomised trial designs. Vaccine 27, 1928–1931.
110. Wade-Evans, A. M., C. H. Romero, P. Mellor, H. Takamatsu, J. Anderson, J. Thevasagayam, M. J. Fleming, P. P. Mertens, and D. N. Black, 1996: Expression of the major core structural protein (VP7) of bluetongue virus, by a recombinant capripox virus, provides partial protection of sheep against a virulent heterotypic bluetongue virus challenge. Virology 220, 227–231.
111. Wallace, D. B., and G. J. Viljoen, 2005: Immune responses to recombinants of the South African vaccine strain of lumpy skin disease virus generated by using thymidine kinase gene insertion. Vaccine 23, 3061–3067.
112. Wallace, D. B., C. E. Ellis, A. Espach, S. J. Smith, R. R. Greylinga, and G. J. Viljoen, 2006: Protective immune responses induced by different recombinant vaccine regimes to Rift Valley fever. Vaccine 24, 7181–7189.
113. Wallace, D. B., J. Weyer, L. H. Nel, and G. J. Viljoen, 2007: Improved method for the generation and selection of homogeneous lumpy skin disease virus (SA-Neethling) recombinants. J. Virol. Methods 146, 52–60.
114. Weiss, K. E., 1968: Lumpy skin disease virus. Virol. Monogr. 3, 111–131.
115. Wolffe, E. J., S. Vijaya, and B. Moss, 1995: A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies. Virology 211, 53–63.
116. Yeruham, I., S. Perl, A. Nyska, A. Abraham, M. Davidson, M. Haymovitch, O. Zamir, and H. Grinstein, 1994: Adverse reactions in cattle to a capripox vaccine. Vet. Rec. 135, 330–332.
117. Young, E., P. A. Basson, and K. E. Weiss, 1970: Experimental infection of game animals with lumpy skin disease virus prototype strain Neethling. Onderstepoort J. Vet. Res. 37, 79–87.