1,058
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Distinguishing host responses, extensive viral dissemination and long-term viral RNA persistence in domestic sheep experimentally infected with Crimean-Congo haemorrhagic fever virus Kosovo Hoti

, , , , , , & show all
Article: 2302103 | Received 19 Oct 2023, Accepted 31 Dec 2023, Published online: 22 Jan 2024

References

  • Bente DA, Forrester NL, Watts DM, et al. Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res. 2013;100(1):159–189. doi:10.1016/j.antiviral.2013.07.006
  • Fels JM, Maurer DP, Herbert AS, et al. Protective neutralizing antibodies from human survivors of Crimean-Congo hemorrhagic fever. Cell. 2021;184(13):3486–3501.e21. doi:10.1016/j.cell.2021.05.001
  • Spengler JR, Bente DA, Bray M, et al. Second international conference on Crimean-Congo hemorrhagic fever. Antiviral Res. 2018;150:137–147. doi:10.1016/j.antiviral.2017.11.019
  • Spengler JR, Bergeron E, Spiropoulou CF. Crimean-Congo hemorrhagic fever and expansion from endemic regions. Curr Opin Virol. 2019;34:70–78. doi:10.1016/j.coviro.2018.12.002
  • Sweileh WM. Global research trends of World Health Organization's top eight emerging pathogens. Global Health. 2017;13(1):9–27. doi:10.1186/s12992-017-0233-9
  • Mehand MS, Millett P, Al-Shorbaji F, et al. World Health Organization methodology to prioritize emerging infectious diseases in need of research and development. Emerg Infect Dis. 2018;24(9):e171427. doi:10.3201/eid2409.171427
  • Abudurexiti A, Adkins S, Alioto D, et al. Taxonomy of the order Bunyavirales: update 2019. Arch Virol. 2019;164(7):1949–1965. doi:10.1007/s00705-019-04253-6
  • Hoogstraal H. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol. 1979;15(4):307–417. doi:10.1093/jmedent/15.4.307
  • Spengler JR, Estrada-Pena A, Garrison AR, et al. A chronological review of experimental infection studies of the role of wild animals and livestock in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus. Antiviral Res. 2016;135:31–47. doi:10.1016/j.antiviral.2016.09.013
  • Fajs L, Jakupi X, Ahmeti S, et al. Molecular epidemiology of Crimean-Congo hemorrhagic fever virus in Kosovo. PLoS Negl Trop Dis. 2014;8(1):e2647. doi:10.1371/journal.pntd.0002647
  • Duh D, Nichol ST, Khristova ML, et al. The complete genome sequence of a Crimean-Congo hemorrhagic fever virus isolated from an endemic region in Kosovo. Virol J. 2008;5:7. doi:10.1186/1743-422X-5-7
  • Haddock E, Feldmann F, Hawman DW, et al. A cynomolgus macaque model for Crimean-Congo haemorrhagic fever. Nat Microbiol. 2018;3(5):556–562. doi:10.1038/s41564-018-0141-7
  • Smith DR, Shoemaker CJ, Zeng X, et al. Persistent Crimean-Congo hemorrhagic fever virus infection in the testes and within granulomas of non-human primates with latent tuberculosis. PLoS Pathog. 2019;15(9):e1008050. doi:10.1371/journal.ppat.1008050
  • Cross RW, Prasad AN, Borisevich V, et al. Crimean-Congo hemorrhagic fever virus strains Hoti and Afghanistan cause viremia and mild clinical disease in cynomolgus monkeys. PLoS Negl Trop Dis. 2020;14(8):e0008637. doi:10.1371/journal.pntd.0008637
  • Golden JW, Zeng X, Cline CR, et al. The host inflammatory response contributes to disease severity in Crimean-Congo hemorrhagic fever virus infected mice. PLoS Pathog. 2022;18(5):e1010485. doi:10.1371/journal.ppat.1010485
  • Kohn MA, Senyak J. Sample Size Calculators [website]. [accessed 2023-08-03]. UCSF CTSI. 2021. Available from: https://sample-size.net/sample-size-proportions/
  • Wilson ML, LeGuenno B, Guillaud M, et al. Distribution of Crimean-Congo hemorrhagic fever viral antibody in Senegal: environmental and vectorial correlates. Am J Trop Med Hyg. 1990;43(5):557–566. doi:10.4269/ajtmh.1990.43.557
  • Papa A, Sidira P, Kallia S, et al. Factors associated with IgG positivity to Crimean-Congo hemorrhagic fever virus in the area with the highest seroprevalence in Greece. Ticks Tick Borne Dis. 2013;4(5):417–420. doi:10.1016/j.ttbdis.2013.04.003
  • Fisher-Hoch SP, McCormick JB, Swanepoel R, et al. Risk of human infections with Crimean-Congo hemorrhagic fever virus in a South African rural community. Am J Trop Med Hyg. 1992;47(3):337–345. doi:10.4269/ajtmh.1992.47.337
  • Ibrahim AM, Adam IA, Osman BT, et al. Epidemiological survey of Crimean Congo hemorrhagic fever virus in cattle in East Darfur State, Sudan. Ticks Tick Borne Dis. 2015;6(4):439–444. doi:10.1016/j.ttbdis.2015.03.002
  • Barthel R, Mohareb E, Younan R, et al. Seroprevalance of Crimean-Congo haemorrhagic fever in Bulgarian livestock. Biotechnol Biotechnol Equip. 2014;28(3):540–542. doi:10.1080/13102818.2014.931685
  • Lotfollahzadeh S, Nikbakht Boroujeni GR, Mokhber Dezfouli MR, et al. A serosurvey of Crimean-Congo haemorrhagic fever virus in dairy cattle in Iran. Zoonoses Public Health. 2011;58(1):54–59. doi:10.1111/j.1863-2378.2009.01269.x
  • Adam IA, Mahmoud MA, Aradaib IE. A seroepidemiological survey of Crimean Congo hemorrhagic fever among cattle in North Kordufan State, Sudan. Virol J. 2013;10:178. doi:10.1186/1743-422X-10-178
  • Mostafavi E, Chinikar S, Esmaeili S, et al. Seroepidemiological survey of Crimean-Congo hemorrhagic fever among sheep in Mazandaran province, northern Iran. Vector Borne Zoonotic Dis. 2012;12(9):739–742. doi:10.1089/vbz.2011.0958
  • Garcia S, Chinikar S, Coudrier D, et al. Evaluation of a Crimean-Congo hemorrhagic fever virus recombinant antigen expressed by Semliki Forest suicide virus for IgM and IgG antibody detection in human and animal sera collected in Iran. J Clin Virol. 2006;35(2):154–159. doi:10.1016/j.jcv.2005.02.016
  • Mohamed M, Said AR, Murad A, et al. A serological survey of Crimean-Congo haemorrhagic fever in animals in the Sharkia Governorate of Egypt. Vet Ital. 2008;44(3):513–517.
  • Bodur H, Akinci E, Ascioglu S, et al. Subclinical infections with Crimean-Congo hemorrhagic fever virus, Turkey. Emerg Infect Dis. 2012;18(4):640–642. doi:10.3201/eid1804.111374
  • merckvetmanual.com. Normal Rectal Temperature Ranges. [accessed 2023-08-03]. MERCK veterinary manual; 2023. Available from: https://www.merckvetmanual.com/multimedia/table/normal-rectal-temperature-ranges
  • Clawson AB. Normal rectal temperatures of sheep. Am J Physiol Legacy Content. 1928;85(2):251–270. doi:10.1152/ajplegacy.1928.85.2.251
  • Oygar PD, Gurlevik SL, Sag E, et al. Changing disease course of Crimean-Congo hemorrhagic fever in children, Turkey. Emerg Infect Dis. 2023;29(2):268–277. doi:10.3201/eid2902.220976
  • Bente DA, Alimonti JB, Shieh WJ, et al. Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J Virol. 2010;84(21):11089–11100. doi:10.1128/JVI.01383-10
  • Saksida A, Duh D, Wraber B, et al. Interacting roles of immune mechanisms and viral load in the pathogenesis of Crimean-Congo hemorrhagic fever. Clin Vaccine Immunol. 2010;17(7):1086–1093. doi:10.1128/CVI.00530-09
  • Ergonul O. Crimean-Congo haemorrhagic fever. Lancet Infect Dis. 2006;6(4):203–214. doi:10.1016/S1473-3099(06)70435-2
  • Weber F, Mirazimi A. Interferon and cytokine responses to Crimean Congo hemorrhagic fever virus; an emerging and neglected viral zonoosis. Cytokine Growth Factor Rev. 2008;19(5-6):395–404. doi:10.1016/j.cytogfr.2008.11.001
  • Papa A, Tsergouli K, Caglayik DY, et al. Cytokines as biomarkers of Crimean-Congo hemorrhagic fever. J Med Virol. 2016;88(1):21–27. doi:10.1002/jmv.24312
  • Ergonul O, Tuncbilek S, Baykam N, et al. Evaluation of serum levels of interleukin (IL)-6, IL-10, and tumor necrosis factor-alpha in patients with Crimean-Congo hemorrhagic fever. J Infect Dis. 2006;193(7):941–944. doi:10.1086/500836
  • Papa A, Bino S, Velo E, et al. Cytokine levels in Crimean-Congo hemorrhagic fever. J Clin Virol. 2006;36(4):272–276. doi:10.1016/j.jcv.2006.04.007
  • Ozturk B, Kuscu F, Tutuncu E, et al. Evaluation of the association of serum levels of hyaluronic acid, sICAM-1, sVCAM-1, and VEGF-A with mortality and prognosis in patients with Crimean-Congo hemorrhagic fever. J Clin Virol. 2010;47(2):115–119. doi:10.1016/j.jcv.2009.10.015
  • Papa A, Dalla V, Papadimitriou E, et al. Emergence of Crimean-Congo haemorrhagic fever in Greece. Clin Microbiol Infect. 2010;16(7):843–847. doi:10.1111/j.1469-0691.2009.02996.x
  • Ergonul O, Seref C, Eren S, et al. Cytokine response in Crimean-Congo hemorrhagic fever virus infection. J Med Virol. 2017;89(10):1707–1713. doi:10.1002/jmv.24864
  • Connolly-Andersen AM, Moll G, Andersson C, et al. Crimean-Congo hemorrhagic fever virus activates endothelial cells. J Virol. 2011;85(15):7766–7774. doi:10.1128/JVI.02469-10
  • Sawant DA, Tharakan B, Wilson RL, et al. Regulation of tumor necrosis factor-alpha-induced microvascular endothelial cell hyperpermeability by recombinant B-cell lymphoma-extra large. J Surg Res. 2013;184(1):628–637. doi:10.1016/j.jss.2013.04.079
  • Zhang Y, Han Y, Zhao Y, et al. DT-13 Ameliorates TNF-alpha-induced vascular endothelial hyperpermeability via non-muscle myosin IIA and the Src/PI3 K/Akt signaling pathway. Front Immunol. 2017;8:925. doi:10.3389/fimmu.2017.00925
  • Friedl J, Puhlmann M, Bartlett DL, et al. Induction of permeability across endothelial cell monolayers by tumor necrosis factor (TNF) occurs via a tissue factor-dependent mechanism: relationship between the procoagulant and permeability effects of TNF. Blood. 2002;100(4):1334–1339. doi:10.1182/blood.V100.4.1334.h81602001334_1334_1339
  • Rodrigues R, Paranhos-Baccala G, Vernet G, et al. Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS One. 2012;7(1):e29712. doi:10.1371/journal.pone.0029712
  • Biffl WL, Moore EE, Moore FA, et al. Interleukin-8 increases endothelial permeability independent of neutrophils. J Trauma. 1995;39(1):98–102; discussion -3. doi:10.1097/00005373-199507000-00013
  • Yu H, Huang X, Ma Y, et al. Interleukin-8 regulates endothelial permeability by down-regulation of tight junction but not dependent on integrins induced focal adhesions. Int J Biol Sci. 2013;9(9):966–979. doi:10.7150/ijbs.6996
  • Bates DO. Vascular endothelial growth factors and vascular permeability. Cardiovasc Res. 2010;87(2):262–271. doi:10.1093/cvr/cvq105
  • Sukriti S, Tauseef M, Yazbeck P, et al. Mechanisms regulating endothelial permeability. Pulm Circ. 2014;4(4):535–551. doi:10.1086/677356
  • Smith RO, Ninchoji T, Gordon E, et al. Vascular permeability in retinopathy is regulated by VEGFR2 Y949 signaling to VE-cadherin. Elife. 2020;9:e54056.
  • Puhlmann M, Weinreich DM, Farma JM, et al. Interleukin-1beta induced vascular permeability is dependent on induction of endothelial tissue factor (TF) activity. J Transl Med. 2005;3:37. doi:10.1186/1479-5876-3-37
  • Du L, Dong F, Guo L, et al. Interleukin-1beta increases permeability and upregulates the expression of vascular endothelial-cadherin in human renal glomerular endothelial cells. Mol Med Rep. 2015;11(5):3708–3714. doi:10.3892/mmr.2015.3172
  • Kotowicz K, Callard RE, Klein NJ, et al. Interleukin-4 increases the permeability of human endothelial cells in culture. Clin Exp Allergy. 2004;34(3):445–449. doi:10.1111/j.1365-2222.2004.01902.x
  • Skaria T, Burgener J, Bachli E, et al. IL-4 causes hyperpermeability of vascular endothelial cells through Wnt5A signaling. PLoS One. 2016;11(5):e0156002. doi:10.1371/journal.pone.0156002
  • Whitehouse CA. Crimean-Congo hemorrhagic fever. Antiviral Res. 2004;64(3):145–160. doi:10.1016/j.antiviral.2004.08.001
  • Zivcec M, Safronetz D, Scott D, et al. Lethal Crimean-Congo hemorrhagic fever virus infection in interferon alpha/beta receptor knockout mice is associated with high viral loads, proinflammatory responses, and coagulopathy. J Infect Dis. 2013;207(12):1909–1921. doi:10.1093/infdis/jit061
  • Bosteen MH, Tritsaris K, Hansen AJ, et al. IL-17A potentiates TNFalpha-induced secretion from human endothelial cells and alters barrier functions controlling neutrophils rights of passage. Pflugers Arch. 2014;466(5):961–972. doi:10.1007/s00424-013-1354-5
  • Hawman DW, Meade-White K, Leventhal S, et al. T-Cells and interferon gamma are necessary for survival following Crimean-Congo hemorrhagic fever virus infection in mice. Microorganisms. 2021;9(2):279. doi:10.3390/microorganisms9020279
  • Griffin DE. Why does viral RNA sometimes persist after recovery from acute infections? PLoS Biol. 2022;20(6):e3001687. doi:10.1371/journal.pbio.3001687
  • Chen B, Julg B, Mohandas S, et al. Viral persistence, reactivation, and mechanisms of long COVID. Elife. 2023;12:e86015.