Epidemiology of Camelpox: New Aspects

After the abolition of the mandatory smallpox vaccination, the humanity lost the immunity not only to smallpox, but also to infections caused by pathogens of this family (Orthopoxvirus): monkeypox, cowpox, buffalo pox, camelpox. Since the camelpox and African gerbil viruses are the closest to the variola virus (genomic homology is 97%) in phylogenetic and genetic terms, it cannot be ruled out that a mutation in a small fragment of the genome of one of these viruses will lead to the replacement of a relatively safe virus with an epidemically dangerous pathogen. The purpose of is article is to summarize materials on the study of camelpox virus. The sources for this research is scientific articles and other English-language literature available via the Internet. The research method is an analysis of scientific sources on camelpox from the general to the specific. The authors considered the epizootic danger of the virus, its virulence for humans, phylogenetic relationship with other orthopoxviruses, means of specific prevention and treatment of camel pox in camels. The discussion and the results. The causative agent of camelpox causes a nodular-pastular rash on the skin and mucous membranes in Camelus dromedaries and Camelus bactrianus. The disease is contagious, and its epizootics lead to significant economic damage. From December 2008 to May 2009, several laboratory-confirmed cases of camelpox in humans were reported in India, Somalia and eastern Sudan. Nowadays for the identification of the camelpox virus, a RT-PCR test system with primers for the C18L gene is usually offered, which detects only this virus. The established host range of the virus is limited to one animal - the camel. To treat sick camels, chemotherapy drugs are used: cidofovir and tocoverimate (ST-246). For immunoprophylaxis, live and inactivated vaccines are used. The conclusion. Camelpox virus poses a risk to humans in regions where people raise camels and are in close contact with them. The immunodeficient populations of people may serve as an additional «window» for the penetration of this virus into human society. The genetic variability of the virus and the plasticity of its genome make it possible to obtain virus strains with altered properties. Synthetic biology methods create a risk, through small substitutions in the genome of the virus, of turning it into an epidemic danger for humans. Constant monitoring of this disease is necessary, since there is a danger of the transmission of camelpox from Kazakhstan to areas bordering the Russian Federation.

1. Duraffour S, Meyer H, Andrei G, Snoeck R. Camelpox virus. Antiviral Res. 2011;92(2):167–86. https://doi.org/10.1016/j.antiviral.2011.09.003

2. Joseph S, Kinne J, Nagy P, Juhász J, Barua R, Patteril NAG, et al. Outbreak of a systemic form of camelpox in a dromedary herd (Camelusdromedarius) in the United Arab Emirates. Viruses. 2021;13(10):1940. https://doi.org/10.3390/v13101940

3. Afonso CL, Tulman ER, Lu Z, Zsak L, Sandybaev NT, Kerembekova UZ, et al. The genome of camelpox virus. Virology. 2002;295(1):1–9. https://doi.org/10.1006/viro.2001.1343

4. Султанкулова КТ, Строчков ВМ, Тайлакова ЭТ, Червякова ОВ, Сандыбаев НТ, Щедрова АВ и др. Филогенетический анализ генома вируса оспы верблюдов, штамма «М-96». Вестник науки КазАТУ им. С. Сейфуллина. 2012;(1). Sultankukova KT, Strochcov VM, Tailakova ET, Chervyakova OV, Sandybaev NT, Shchedrova AV, et al. Phylogenetic analysis of genome camelpox virus, strain «М-96». Herald of Science S Seifulin Kazkh Agrotechnical Research University. 2012;(1).

5. Bera BC, Shanmugasundaram K, Barua S, Venkatesan G, Virmani N, Riyesh T, et al. Zoonotic cases of camelpox infection in India. Vet Microbiol. 2011;152(1-2):29–38. https://doi.org/10.1016/j.vetmic.2011.04.010

6. Bhanuprakash V, Prabhu M, Venkatesan G, Balamuragan V, Hosamani M, Pathak KM, Singh RK. Camelpox: epidemiology, diagnosis and control measures. Expert Rev Anti Infect Ther. 2010;8(10):1187–201. https://doi.org/10.1586/eri.10.105

7. Жугунисов КД, Мамбеталиев МА, Азанбекова МА, Кенжебаева МК, Килибаев СС, Туысканова МС и др. Выделение нового штамма М-2020 вируса оспы верблюдов (Poxviridae: Orthopoxvirus: Camelpox virus) в Республике Казахстан и изучение его репродукции на различных биологических системах. Вопросы ви- русологии. 2022;67(1):77–86. Zhugunissov KD, Mambetaliyev MA, Azanbekova MA, Kenzhebaeva МК, Kilibayev SS, Tuyskanova MS, et al. Isolation of a new strain М-2020 of the camelpox virus (Poxviridae: Orthopoxvirus: Camelpox virus) in Republic of Kazakhstan and study of its reproduction in various biological systems. Problems of Virology (Voprosy Virusologii). 2022;67(1):77–86 (in Russian). https://doi.org/10.36233/0507-4088-100

8. Al-Bayati HAM, Albadry MAS, Al-Safi ZH. Detection and isolation of camelpoxvirus in Wasitprovince, Iraq Arch Razi Institute. 2022;77(3):1133–8. https://doi.org/10.22092/ARI.2022.357388.2028

9. Narnaware SD, Ranjan R, Dahiya SS, Panchbuddhe A, Bajpai D, Tuteja FC, et al. Pathological and molecular investigations of systemic form of camelpox in naturally infected adult male dromedary camels in India. Нeliyon. 2021;7(2):e06186. https://doi.org/10.1016/j.heliyon.2021.e06186

10. Булатов ЕА, Мамадалиев СМ, Мамбеталиев М, Битов НТ. О циркуляции вируса оспы верблюдов в Мангыстауской области Республики Казахстан в скрытой форме. Актуальные вопросы ветеринарной биологии. 2010;3(7):10–3. Bulatov YA, Mamadaliyev SM, Mambetaliyev M, Bitov NT. Circulation of the camel pox virus in Manghystauskaya region, republic of Kazakhstan, in the latent form. Actual Question in Veterinary Biology. 2010;3(7):10–3 (in Russian).

11. Israeli O, Cohen-Gihon I, Zvi A, Shifman O, Melamed S, Paran N, et al. Complete genome sequence of the first camelpox virus case diagnosed in Israel. Microbiol Resour Announc. 2019;8(34):e00671-19. https://doi.org/10.1128/MRA.00671-19

12. Mirkena T, Walelign E, Tewolde N, Gari G, Abebe G, Newman S. Camel production sуstems in Ethiopia: a revive of literature with notes on MERS-CoV risk factors. Pastoralism. 2018;8(1):30. https://doi.org/10.1186/s13570-018-0135-3

13. Leese AS. Two diseases of young camels. J Trop Vet Sci. 1989;4:1.

14. Balamurugan V, Venkatesan G, Bhanuprakash V, Singh RK. Camelpox, an emerging orthopox viral disease Indian. J Virol. 2013;24(3):295–305. https://doi.org/10.1007/s13337-013-0145-0

15. Росляков АА, Садыков РГ. Электронно-микроскопическое изучение вируса оспы верблюдов. Труды Алма-Атинского зооветеринарного института. Серия клинико-эпизоотологическая. 1969;15(4):23–6. Roslyakov AA, Sadykov RG. Electron microscopic study of camel pox virus. Proceedings of the Alma-Ata Veterinary Institute. Series is clinical and epizootological. 1969;15(4):23–6 (in Russian).

16. Samartsev AA, Praxein ST. A study of camel smallpox. Proceeding of KazNIVI. 1950; P. 198.

17. Ramya RH, Hessam IM. Isolation, cultivation and characterization of camel poxvirus. Zentralbl Veterinarmed B. 1972;19(3):182–9. https://doi.org/10.1111/j.1439-0450.1972.tb00393.x

18. Mosadeghhesari M, Oryan A, Zibaee S, Varshovi HR. Molecular investigation cultivation of camelpox virus in Iran. Arch Virol. 2014;159(11):3005–11. https://doi.org/10.1007/s00705-014-2169-1

19. Davies FG, Mungai JN, Shaw T. Characteristics of Kenyan camelpox virus. J Hyg (Lond). 1975;75(3):381–5. https://doi.org/10.1017/s002217240002444x

20. Gitao CG. An investigation of camelpox outbreaks in two principal camel (Camelus dromedaries) rearing areas of Kenya. Rev Sci Tech. 1997;16(3):841–7. https://doi.org/10.20506/rst.16.3.1077

21. Falluji MM, Tantawi HH, Shony MO. Isolation, identification and characterization of camelpox virus in Iraq. J Hyg (Lond). 1979;83(2):267–72. https://doi.org/10.1017/s002217240002605x

22. Pfeffer M, Meyer H, Wernery U, Kaaden OR. Comparison of camelpox viruses isolated in Dubai. Vet Microbiol. 1996;49(1-2):135–46. https://doi.org/10.1016/0378-1135(95)00181-6

23. Kinne J, Cooper JE, Wernery U. Pathological studies on camelpox lesion of the respiratory system in the United Arab Emirates (UAE). J Comp Pathol. 1986;118(4):257–66. https://doi.org/10.1016/s0021-9975(07)80002-8

24. Abu Elzein EM, Gameel AA, Ramadan RO, Housawi FM. An eruptive moderate form of camelpox infection in dromedary camels (Camelus dromedaries) in Saudi Arabia. Rev Sci Tech. 1999;18(3):749–52. https://doi.org/10.20506/rst.18.3.1194

25. Al-Zi'abi O, Nishikawa H, Meyer H. The first outbreak of camelpox in Syria. J Vet Med Sci. 2007;69(5):541– 43. https://doi.org/10.1292/jvms.69.541

26. Bera BC, Shanmugasundaram K, Barua S, Venkatesan G, Virmani N, Riyesh T, et al. Zoonotic cases of camelpox infection in India. Vet Microbiol. 2011;152(1-2):29–38. https://doi.org/10.1016/j.vetmic.2011.04.010

27. Erster O, Melamed S, Paran N, Weiss S, Khinich Y, Gelman B, et al. First Diagnosed Case of Camelpox virus in Israel. Viruses. 2018;10(2):78. https://doi.org/10.3390/v10020078

28. Venkatesan G, Bhanuprakash V, Balamuragan V, Singh RK, Pandey AB. Development of loop-mediated isothermal amplification assay for specific and rapid detection of camelpox virus in clinical samples. J Virol Methods. 2012;183(1):34–9. https://doi.org/10.1016/j.jviromet.2012.03.019

29. Duraffour S, Matthys P, van den Oord JJ, De Schutter T, Mitera T, Snoeck R, Andrei G. Study of camelpox virus pathogenesis in athymic nude mice. PLoS One. 2011;6(6):e21561. https://doi.org/10.1371/journal.pone.0021561

30. Kriz B. A study of camelpox in Somalia. J Comp Pathol. 1982;92(1):1–8. https://doi.org/10.1016/0021-9975(82)90037-8

31. Kfalafalla AI, Abdelazim F. Human and dromedary camel infection with camelpox virus in Eastern Sudan. Vector Borne Zoonotic Dis. 2017;17(4):281–84. https://doi.org/10.1089/vbz.2016.2070

32. Shchelkunov SN. An increasing danger of zoonotic orthopoxvirus infections. PLoS Pathog. 2013;9(12):e1003756. https://doi.org/10.1371/journal.ppat.1003756

33. Zhugunissov K, Kilibayev S, Mambetaliyev M, Zakarya K, Kassenov M, Abduraimov Y, et al. Development and evaluation of a live attenuated egg-based camelpox vaccine. Front Vet Sci. 2021;8:721023. https://doi.org/10.3389/fvets.2021.721023

34. Bulatov ЕK, Mamadaliev SM, Mambetaliyev M, et al. Studying of cultural properties of camelpox virus. In: Quarantine and zoonotic infection in Kazakhstan Intern Conf. Is. 3. Alma-Ata; 2001. P. 79–82.

35. Marcacci M, Khalafalla AI, Al Hammad ZM, Monaco F, Cammà C, Yusof MF, et al. Genome sequencing of a camelpox vaccine reveals close similarity to modified vaccinia virus Ankara (MVA). Viruses. 2020;12(8):786. https://doi.org/10.3390/v12080786

36. Afonso CL, Tulman ER, Lu Z, Zsak L, Sandybaev NT, Kerembekova UZ, et al. The genome of camelpox virus. Virology. 2002;295(1):1–9. https://doi.org/10.1006/viro.2001.1343

37. Gubser C, Smith GL. The sequence of camelpox virus shows it is most closely related to variola virus, the cause of smallpox. J Gen Virol. 2002;83(Pt 4):855–72. https://doi.org/10.1099/0022-1317-83-4-855

38. Renner-Muller IC, Meyer H, Munz E. Characterization isolates from Africa and Asia. Vet Microbiol. 1995;45(4):371–81. https://doi.org/10.1016/0378-1135(94)00143-k

39. Wernery U. Viral infections in camels – a review. J Camel Pract Res. 1995;2(1):1–12.

40. Ropp SL, Jin Q, Knight JC, Massung RF, Esposito JJ. PCR strategy for identification and differentiation ofsmall pox and other orthopoxviruses. J Clin Microbiol. 1995;33(8):2069–76. https://doi.org/10.1128/jcm.33.8.2069-2076

41. Kfalafalla AI, Al-Busada KA, El-Sabagh IM. Multiplexs PCR for rapid diagnosis and differentiation o pox and pox-like diseases in dromedary camels. Virol J. 2015;12:102. https://doi.org/10.1186/s12985-015-0329-x

42. Meyer H, Pfeffer M, Rziha HJ. Sequence alterations within and downstream of the A-type inclusion protein genes allow of Orthopoxvirus species by polymerase chain reaction. J Gen Virol. 1994;75:1975–81. https://doi.org/10.1099/0022-1317-75-8-1975

43. Abdellatif MM, Salim B, Ibrahim AA, Asil T, Khalafalla AI. Analysis of TK and C18L genes of wild-type culture passaged camelpox virus. Virol Sin. 2013;28(4):239–41. https://doi.org/10.1007/s12250-013-3329-2

44. Balamurugan V, Bhanuprakash V, Hosamani M, Jayappa KD, Venkatesan G, Chauhan B, Singh RK. A polymerase chain reaction strategy for the diagnosis of camelpox. J Vet Diagn Invest. 2009;21:231–7. https://doi.org/10.1177/104063870902100209

45. Bhanuprakash V, Prabhu M, Venkatesan G, Balamurugan V, Hosamani M, Pathak KM, Singh RK. Camelpox: epidemiology, diagnosis and control measures. Expert Rev Anti Infect Ther. 2010;8(10):1187–201. https://doi.org/10.1586/eri.10.105

46. Venkatesan G, Bhanuprakash V, Balamurugan V, Prabhu M, Pandey AB. TagMan hydrolysis probe based real time PCR for detection and quantitation of camelpox virus in skin scabs. J Virol Methods. 2012;181(2):192–6. https://doi.org/10.1016/j.jviromet.2012.02.002

47. Zhugunissov K, Kilibayev S, Mambetaliyev M, Zakarya K, Kassenov M, Abduraimov Y, et al. Development and evaluation of a live attenuated egg-based camelpox vaccine. Front Vet Sci. 2021;8:721023. https://doi.org/10.3389/fvets.2021.721023

48. Hafes SM, al-Sukayran A, dela Cruz D, Mazloum KS, al-Bokmy AM, al-Mukayel A, Amjad AM. Development of a live cell culture camelpox vaccine. Vaccine. 1992;10:533–9. https://doi.org/10.1016/0264-410x(92)90353-l

49. Abdellatif MM, Ibrahim AA, Khalafalla AI. Development and evaluation of a live attenuated camelpox vaccine from a local field isolate of the virus. Rev Sci Tech. 2014;33(3) 831–8. https://doi.org/10.20506/rst.33.3.2321

50. Khalafalla AI, Hosani MA, Ishag HZA, Muhairi SSA. More cell culture passaged Camelpox virus sequences found resembling those of vaccinia virus. Open Veterinary J. 2020;10(2):144–56. https://doi.org/10.4314/ovj.v10i2.4

51. Saud Z, Butt M. Another case of mistaken identity? Vaccinia virus in another live Camelpox vaccine. Biologicals. 2020;65:36–41. https://doi.org/10.1016/j.biologicals.2020.04.002

52. Saud Z, Hitchings MD, Butt TM. Nanopore sequencing and de novo assembly of a misidentified Camelpox vaccine reveals putative epigenetic modificationsand alternate protein signal peptides. Sci Rep. 2021;11(1):17758. https://doi.org/10.1038/s41598-021-97158-x

53. Noyce RS, Lederman S, Evans DH. Construction of an infectious horsepox virus vaccine from chemically synthesized DNA fragments. PLoS ONE. 2018;13(1):e0188453. https://doi.org/10.1371/journal.pone.0188453