Skip to main content
Log in

Molecular identification of Crimean-Congo haemorrhagic fever virus in Hyalomma rufipes and Amblyomma variegatum in the Upper East Region of Ghana

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Sampled ticks were screened for Crimean-Congo haemorrhagic fever virus (CCHFV) using an assay that targets the nucleoprotein gene region of the S segment, a conserved region of the CCHFV genome. Minimum infection rates of 0.34% and 0.10% were obtained when testing pools of Hyalomma rufipes and Amblyomma variegatum, respectively. Next-generation sequencing and phylogenetic analysis showed that the S and L segments of the CCHFV isolate clustered with those of similar isolates of genotype III. However, analysis of the M segment showed that reassortment had occurred, causing this segment to cluster with those of isolates of genotype I, providing the first evidence of such an occurrence in Ghana.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Data availability

All of the data supporting this study are included in the article.

References

  1. Akuffo R, Brandful JAM, Zayed A, Adjei A, Watany N, Fahmy NT, Hughes R, Doman B, Voegborlo SV, Aziati D, Pratt D, Awuni JA, Adams N, Dueger E (2016) Crimean-Congo hemorrhagic fever virus in livestock ticks and animal handler seroprevalence at an abattoir in Ghana. BMC Infect Dis 16(1):1–5. https://doi.org/10.1186/s12879-016-1660-6

    Article  Google Scholar 

  2. Atkinson B, Chamberlain J, Logue CH, Cook N, Bruce C, Dowall SD, Hewson R (2012) Development of a real-time RT-PCR assay for the detection of Crimean-Congo hemorrhagic fever virus. Vector-Borne Zoonot Dis 12(9):786–793. https://doi.org/10.1089/vbz.2011.0770

    Article  Google Scholar 

  3. Bell-Sakyi L, Koney EBM, Dogbey O, Walker AR (2004) Incidence and prevalence of tick-borne haemoparasites in domestic ruminants in Ghana. Vet Parasitol 124(1–2):25–42. https://doi.org/10.1016/j.vetpar.2004.05.027

    Article  CAS  PubMed  Google Scholar 

  4. Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA, Bray M (2013) Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res 100(1):159–189. https://doi.org/10.1016/j.antiviral.2013.07.006

    Article  CAS  PubMed  Google Scholar 

  5. Bentil RE, Addo SO, Mosore M, Kumordjie S, Yeboah C, Agbodzi B, Behene E, Tagoe J, Baako BOA, Asoala V, Ampadu RO, Mingle DL, Nyarko EO, Fox AT, Letizia AG, Diclaro JW, Sanders T, Oduro D, Nimo-Paintsil SC et al (2023) First whole genome sequencing of Crimean-Congo hemorrhagic fever virus (CCHFV) in tick species within Ghana. Transbound Emerg Dis. https://doi.org/10.1155/2023/2063317

    Article  Google Scholar 

  6. Black WC IV, Piesman J (1994) Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci USA 91(21):10034–10038. https://doi.org/10.1073/pnas.91.21.10034

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bukbuk DN, Dowall SD, Lewandowski K, Bosworth A, Baba SS, Varghese A, Watson RJ, Bell A, Atkinson B, Hewson R (2016) Serological and virological evidence of crimean-congo haemorrhagic fever virus circulation in the human population of Borno State, Northeastern Nigeria. PLoS Neglect Trop Dis 10(12):1–12. https://doi.org/10.1371/journal.pntd.0005126

    Article  Google Scholar 

  8. Burt FJ, Paweska JT, Ashkettle B, Swanepoel R (2009) Genetic relationship in southern African Crimean-Congo haemorrhagic fever virus isolates: evidence for occurrence of reassortment. Epidemiol Infect 137(9):1302–1308. https://doi.org/10.1017/S0950268808001878

    Article  CAS  PubMed  Google Scholar 

  9. Chisholm K, Dueger E, Fahmy NT, Samaha HAT, Zayed A, Abdel-Dayem M, Villinski JT (2012) Crimean-congo hemorrhagic fever virus in ticks from imported livestock, Egypt. Emerg Infect Dis 18(1):181–182. https://doi.org/10.3201/eid1801.111071

    Article  PubMed  PubMed Central  Google Scholar 

  10. Crowder CD, Matthews HE, Schutzer S, Rounds MA, Luft BJ, Nolte O, Campbell SR, Phillipson CA, Li F, Sampath R, Ecker DJ, Eshoo MW (2010) Genotypic variation and mixtures of lyme borrelia in ixodes ticks from North America and Europe. PLoS ONE. https://doi.org/10.1371/journal.pone.0010650

    Article  PubMed  PubMed Central  Google Scholar 

  11. Deyde VM, Khristova ML, Rollin PE, Ksiazek TG, Nichol ST (2006) Crimean-Congo hemorrhagic fever virus genomics and global diversity. J Virol 80(17):8834–8842. https://doi.org/10.1128/JVI.00752-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Estrada-Peña A, De La Fuente J (2014) The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Res 108(1):104–128. https://doi.org/10.1016/j.antiviral.2014.05.016

    Article  CAS  PubMed  Google Scholar 

  13. Gargili A, Estrada-Peña A, Spengler JR, Lukashev A, Nuttall PA, Bente DA (2017) The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies. Antiviral Res 144:93–119. https://doi.org/10.1016/j.antiviral.2017.05.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gonzalez JP, Camicas JL, Cornet JP, Faye O, Wilson ML (1992) Sexual and transovarian transmission of Crimean-Congo haemorrhagic fever virus in Hyalomma truncatum ticks. Res Virol 143(1):23–28. https://doi.org/10.1016/S0923-2516(06)80073-7

    Article  CAS  PubMed  Google Scholar 

  15. Han N, Rayner S (2011) Epidemiology and mutational analysis of global strains of Crimean-Congo haemorrhagic fever virus. Virol Sin 26(4):229–244. https://doi.org/10.1007/s12250-011-3211-z

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hasle G (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect Microbiol 4(48):1–6. https://doi.org/10.3389/fcimb.2013.00048

    Article  ADS  Google Scholar 

  17. Hawman DW, Feldmann H (2023) Crimean-Congo haemorrhagic fever virus. Nat Rev Microbiol 21(July):463–477. https://doi.org/10.1038/s41579-023-00871-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hewson R, Gmyl A, Gmyl L, Smirnova SE, Karganova G, Jamil B, Hasan R, Chamberlain J, Clegg C (2004) Evidence of segment reassortment in Crimean-Congo haemorrhagic fever virus. J Gen Virol 85(10):3059–3070. https://doi.org/10.1099/vir.0.80121-0

    Article  CAS  PubMed  Google Scholar 

  19. Jaenson TGT, Talleklint L, Lundqvist L, Olsen B, Chirico J, Mejlon H (1994) Geographical distribution, host associations, and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden. J Med Entomol 31(2):240–256. https://doi.org/10.1093/jmedent/31.2.240

    Article  CAS  PubMed  Google Scholar 

  20. Jameson LJ, Morgan PJ, Medlock JM, Watola G, Vaux AGC (2012) Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks Tick-Borne Dis 3(2):95–99. https://doi.org/10.1016/j.ttbdis.2011.12.002

    Article  PubMed  Google Scholar 

  21. Kalkan-Yazıcı M, Karaaslan E, Çetin NS, Hasano S, Güney F, Zeybek Ü, Doymaz MZ (2021) Cross-reactive anti-nucleocapsid protein immunity against Crimean-Congo hemorrhagic fever virus and hazara virus in multiple species. J Virol. https://doi.org/10.1128/JVI.02156-20

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lule SA, Gibb R, Kizito D, Nakanjako G, Mutyaba J, Balinandi S, Owen L, Jones KE, Abubakar I, Lutwama JJ, Field N (2022) Widespread exposure to Crimean-Congo haemorrhagic fever in Uganda might be driven by transmission from Rhipicephalus ticks: evidence from cross-sectional and modelling studies. J Infect 85(6):683–692. https://doi.org/10.1016/j.jinf.2022.09.016

    Article  CAS  PubMed  Google Scholar 

  23. Mamman AH, Lorusso V, Adam BM, Dogo GA, Bown KJ, Birtles RJ (2021) First report of Theileria annulata in Nigeria: findings from cattle ticks in Zamfara and Sokoto States. Parasit Vect 14(1):1–9. https://doi.org/10.1186/s13071-021-04731-4

    Article  CAS  Google Scholar 

  24. Morikawa S, Saijo M, Kurane I (2007) Recent progress in molecular biology of Crimean-Congo hemorrhagic fever. Comp Immunol Microbiol Infect Dis 30(5–6):375–389. https://doi.org/10.1016/j.cimid.2007.07.001

    Article  PubMed  Google Scholar 

  25. Nimo-Paintsil SC, Mosore M, Addo SO, Lura T, Tagoe J, Ladzekpo D, Addae C, Bentil RE, Behene E, Dafeamekpor C, Asoala V, Fox A, Watters CM, Koehler JW, Schoepp RJ, Arimoto H, Dadzie S, Letizia A, Ii JWD (2022) Ticks and prevalence of tick-borne pathogens from domestic animals in Ghana. Parasit Vect. https://doi.org/10.1186/s13071-022-05208-8

    Article  Google Scholar 

  26. Okely M, Anan R, Gad-Allah S, Samy AM (2020) Mapping the environmental suitability of etiological agent and tick vectors of Crimean-Congo hemorrhagic fever. Acta Trop 203:105319. https://doi.org/10.1016/j.actatropica.2019.105319

    Article  CAS  PubMed  Google Scholar 

  27. Ramírez de Arellano E, Hernández L, Goyanes MJ, Arsuaga M, Fernández Cruz A, Negredo A, Paz Sánchez-Seco M (2017) Phylogenetic characterization of Crimean-Congo hemorrhagic fever virus, Spain. Emerg Infect Dis 23(12):2078–2080. https://doi.org/10.3201/EID2312.171002

    Article  PubMed  PubMed Central  Google Scholar 

  28. Schulz A, Barry Y, Stoek F, Pickin MJ, Ba A, Chitimia-Dobler L, Haki ML, Doumbia BA, Eisenbarth A, Diambar A, Bah MY, Eiden M, Groschup MH (2021) Detection of Crimean-Congo hemorrhagic fever virus in blood-fed Hyalomma ticks collected from Mauritanian livestock. Parasit Vect 14(1):1–10. https://doi.org/10.1186/s13071-021-04819-x

    Article  CAS  Google Scholar 

  29. Sharifinia N, Rafinejad J, Hanafi-Bojd AA, Chinikar S, Piazak N, Baniardalan M, Biglarian A, Sharifinia F (2015) Hard ticks (Ixodidae) and Crimean-Congo hemorrhagic fever virus in south west of Iran. Acta Med Iran 53(3):177–181. http://acta.tums.ac.ir/index.php/acta/article/view/4913

  30. Walker ARARR, Koney EBMBMEBM (1999) Distribution of ticks (Acari: Ixodida) infesting domestic ruminants in Ghana. Bull Entomol Res 89(5):473–479. https://doi.org/10.1017/s0007485399000619

    Article  Google Scholar 

  31. Walker A, Bouattour A, Camicas J, Estrada-Peña A, Horak I, Latif A, Pegram R, Preston P (2003) Ticks of domestic animals in Africa: a guide to identification of species. In: Bioscience Reports University of Edinburgh

  32. Zhou Z, Deng F, Han N, Wang H, Sun S, Zhang Y, Hu Z, Rayner S (2013) Reassortment and migration analysis of Crimean-Congo haemorrhagic fever virus. J Gen Virol 94(11):2536–2548. https://doi.org/10.1099/vir.0.056374-0

    Article  CAS  PubMed  Google Scholar 

  33. Zivcec M, Metcalfe MG, Albariño CG, Guerrero LW, Pegan SD, Spiropoulou CF, Bergeron É (2015) Assessment of inhibitors of pathogenic Crimean-Congo hemorrhagic fever virus strains using Virus-Like particles. PLoS Negl Trop Dis. https://doi.org/10.1371/journal.pntd.0004259

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The Navrongo Health Research Centre and the Parasitology Department of the Noguchi Memorial Institute for Medical Research are acknowledged by the authors for their assistance and contribution. We are also grateful to Suzanne Mate (MAJ) for her support and contribution towards this study.

Funding

The Global Health Engagement Research Initiative (grant number GRANT12767296) of the Uniformed Services University Centre for Global Health Engagement (CGHE) contributed funding for this work.

Author information

Authors and Affiliations

Authors

Contributions

SOA wrote the main manuscript. SOA, REB, CAA, BOAB, KNY, JA, CNLT, BA, SK, and CY conducted the laboratory analysis. SOA and BA analysed the data. SOA, VA, JCD, JAL, PKB, MDW, JWD, and SKD designed the study. JAL, PKB, MDW, and SKD supervised this study. All authors reviewed and approved the final manuscript.

Corresponding authors

Correspondence to Seth Offei Addo or Samuel K. Dadzie.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

The University of Ghana Institutional Animal Care and Use Committee (UG-IACUC; UG-IACUC 001/19-20) granted ethical permission for this study.

Authors’ disclaimer statement

The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, the Department of Defense, or the US Government. Opinions, interpretations, conclusions, and recommendations are those of the authors and are not necessarily endorsed by the US Army. The authors Joseph W. Diclaro II and James C. Dunford are military service members or employees of the US Government. This work was prepared as part of their official duties. Title 17 USC §105 provides that “Copyright protection under this title is not available for any work of the United States Government”. Title 17 USC §101 defines US Government work as work prepared by a military service member or employee of the US Government as part of that person’s official duties.

Additional information

Handling Editor: Patricia Aguilar.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Addo, S.O., Bentil, R.E., Addae, C.A. et al. Molecular identification of Crimean-Congo haemorrhagic fever virus in Hyalomma rufipes and Amblyomma variegatum in the Upper East Region of Ghana. Arch Virol 169, 62 (2024). https://doi.org/10.1007/s00705-024-05983-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00705-024-05983-y

Navigation