Evidence of Crimean-Congo Haemorrhagic Fever Virus Occurrence in Ixodidae Ticks of Armenia
-
Hasmik Gevorgyan
,
Gohar G. Grigoryan
,
Hripsime A. Atoyan
,
Martin Rukhkyan
,
Astghik Hakobyan
,
Hovakim Zakaryan
,
Sargis A. Aghayan
Abstract
Background: Crimean-Congo hemorrhagic fever (CCHF) causes serious health problems in humans. Though ticks of the genera Hyalomma play a significant role in the CCHF transmission it was also found in 31 other thick species.
Methods: Totally, 1412 ticks from 8 remote sites in Armenia during 2016 were sampled, pooled (3-5 ticks per pool) and tested for the presence of CCHFV antigen using ELISA test.
Results: From 359 tick pools, 132 were CCHF virus antigen-positive. From 6 tick species, four species (Rhipicephalus sanguineus, R. annulatus, R. bursa, Hyalomma marginatum) were positive for the virus antigen and R. sanguineus was the most prevalent (37.9%). Dermacentor marginatus and Ixodes ricinus revealed no positive pools, but both revealed delectable but very low virus antigen titers. The highest infection rate (50%) was observed in R. sanguineus, whereas H. marginatus rate of infection was 1 out 17.
Conclusion: For the first time in the last four decades CCHF virus antigen was detected in Ixodid ticks of Armenia. This finding substantiates the role of R. sanguineus in the disease epidemiology; however, the role of H. marginatum in the CCHF virus circulation in the country could not be excluded.
1. Gonzalez JP, Souris M, Valdivia-Granda W (2018) Global Spread of Hemorrhagic Fever Viruses: Predicting Pandemics. In: Methods in Molecular Biology. Meth-ods Mol Biol. 1604: 3–31.
2. Ohimain EI (2017) Emerging Pathogens of Global Significance, Priorities for Atten-tion and Control. EC Microbiol. 56: 215–240.
3. Pshenichnaya NY, Sydenko IS, Klinovaya EP, Romanova EB, Zhuravlev AS (2016) Possible sexual transmission of Crime-an-Congo hemorrhagic fever. Int J In-fect Dis. 45: 109–11.
4. Eckerle I, Briciu VT, Ergönül Ö, Lupşe M, Papa A, Radulescu A, Tsiodras S, Tsitou C, Drosten C, Nussenblatt VR, Reusken CB, Sigfrid LA, Beeching NJ (2018) Emerging souvenirs-clinical presentation of the returning traveller with imported arbovirus infections in Europe. Clin Mi-crobiol Infect. 24(3): 240–245.
5. Maltezou HC, Andonova L, Andraghetti R, Bouloy M, Ergonul O, Jongejan F, Kal-vatchev N, Nichol S, Niedrig M, Pla-tonov A, Thomson G, Leitmeyer K, Zeller H (2010) Crimean-Congo hem-orrhagic fever in Europe: current situa-tion calls for preparedness. Euro Surveill. 15(10): 19504.
6. Sharififard M, Alavi SM, Salmanzadeh S, Safdari F, Kamali A (2016) Epidemio-logical Survey of Crimean-Congo Hem-orrhagic Fever (CCHF), a Fatal Infectious Disease in Khuzestan Province, South-west Iran, During 1999–2015. Jundisha-pur J Microbiol. 9(5): e30883.
7. Leblebicioglu H, Eroglu C, Erciyas-Yavuz K, Hokelek M, Acici M, Yilmaz H (2014) Role of Migratory Birds in Spread-ing Crimean-Congo Hemorrhagic Fever, Turkey. Emerg Infect Dis. 20(8): 1331–1334.
8. Metanat M, Sharifi-Mood B, Fathollah-zadeh N, Rezaei Kahkha L, Bahremand F, Sharifi R (2018) Report of a Family with Crimean-Congo Hemorrhagic Fever Following Contact with Frozen Meat: A Case Seires Study. Arch Clin Infect Dis. In Press.
9. Ahmadkhani M, Alesheikh AA, Khakifirouz S, Salehi-Vaziri M (2018) Space-time epidemiology of Crimean-Congo hemor-rhagic fever (CCHF) in Iran. Ticks Tick Borne Dis. 9(2): 207–216.
10. Ergonul O, Celikbas A, Dokuzoguz B, Eren S, Baykam N, Esener H (2004) Charac-teristics of Patients with Crimean-Con-go Hemorrhagic Fever in a Recent Out-break in Turkey and Impact of Oral Rib-avirin Therapy. Clin Infect Dis. 39(2): 284–287.
11. Papa A, Mirazimi A, Köksal I, Estrada-Pena A, Feldmann H (2015) Recent ad-vances in research on Crimean-Congo hemorrhagic fever. J Clin Virol. 64: 137–143.
12. Whitehouse C (2004) Crimean-Congo hem-orrhagic fever. Antiviral Res. 64(3): 145–160.
13. Mourya DT, Yadav PD, Shete AM, Gurav YK, Raut CG, Jadi RS, Pawar SD, Nichol ST, Mishra AC (2012) Detection, Iso-lation and Confirmation of Crimean-Con-go Hemorrhagic Fever Virus in Human, Ticks and Animals in Ahmadabad, India, 2010–2011. PLoS Negl Trop Dis. 6(5): e1653.
14. Tuncer P, Yesilbag K, Alpay G, Dincer E, Girisgin AO, Aydin L, Yavuz Uyar, Aykut Ozkul (2014) Crimean-Congo Hemorrhagic Fever infection in domes-tic animals in Marmara region, Western Turkey. Ankara Univ Vet Fak Derg. 61 (19): 49–53.
15. Hoogstraal H (1979) The epidemiology of tick-borne Crimean-Congo hemorrhag-ic fever in Asia, Europe, and Africa. J Med Entomol. 15(4): 307–417.
16. Yesilbag K, Aydin L, Dincer E, Alpay G, Girisgin AO, Tuncer P, Ozkul A (2013) Tick survey and detection of Crimean-Congo hemorrhagic fever virus in tick species from a non-endemic area, South Marmara region, Turkey. Exp Appl Ac-arol. 60(2): 253–261.
17. Ergonul O, Whitehouse CA (2007) Intro-duction. In: Ergonul O, Whitehouse CA. Crimean-Congo hemorrhagic fever. A global perspective. Dordrecht, Springer Science and Business Media 2007, p. 3–11.
18. Anderson JF, Magnarelli LA (2008) Biol-ogy of Ticks. Infect Dis Clin North Am. 22(2): 195–215.
19. Melik-Andreasyan GG, Keshishyan AS, Manukyan DV, Harutyunova KV, Harutyunova MV, Voskanyan LS (2013) A study of certain territories in Armenia for the presence of natural foci of tick-borne encephalitis and West Nile fever (in Russian). Med Sci Armen. 52(4): 52–58.
20. Semashko IV, Chumakov PM, Karapetyan MR (1974) First isolation of the CHF virus in Armenia from the blood of the patient with Crimean hemorrhagic fever. Sb Tr Inst Polio Virusn Encef Akad Med Nauk USSR. 7: 271–278.
21. Hekimoglu O, Ozer N, Ergunay K, Ozkul A (2012) Species distribution and de-tection of Crimean Congo Hemorrhag-ic Fever Virus (CCHFV) in field-col-lected ticks in Ankara Province, Central Anatolia, Turkey. Exp Appl Acarol. 56 (1): 75–84.
22. Leblebicioglu H, Ozaras R, Irmak H, Sen-can I (2016) Crimean-Congo hemor-rhagic fever in Turkey: Current status and future challenges. Antiviral Res. 126: 21–34.
23. Salehi-Vaziri M, Salmanzadeh S, Ban-iasadi V, Jalali T, Mohammadi T, Azad-Manjiri S, Jamshidi Y, Khakifirouz S, Fazlalipour M (2017) An Outbreak of Crimean-Congo Hemorrhagic Fever in the South West of Iran. Jundishapur J Microbiol. 10(1): e41735.
24. Shahhosseini N, Chinikar S, Shams E, Nowotny N, Fooks AR (2017) Crimean-Congo hemorrhagic fever cases in the North of Iran have three distinct origins. Virus Disease. 28(1): 50–53.
25. Wilder-Smith A, Gubler DJ, Weaver SC, Monath TP, Heymann DL, Scott TW (2017) Epidemic arboviral diseases: pri-orities for research and public health. Lancet Infect Dis. 17(3): 101–106.
26. Vardanyan MV, Gevorgyan H (2009) The study of the epidemiological peculiari- ties of piroplasmosis in the lowland zone of Armenia. The National Scientific-prac-tical Conference on Infectious Disease Epidemiology, 2009 September 22–26, National Institute of Epidemiology, Vi-rology and Medical Parsitology, Yerevan, Armenia, pp. 37–38.
27. Failloux AB, Bouattour A, Faraj C, Gunay F, Haddad N, Harrat Z, Jancheska E, Kanani K, Kenawy MA, Kota M, Pa-jovic I, Paronyan L, Petric D, Sarih M, Sawalha S, Shaibi T, Sherifi K, Sulesco T, Velo E, Gaayeb L, Victoir K, Robert V (2017) Surveillance of Arthropod-Borne Viruses and Their Vectors in the Mediterranean and Black Sea Regions Within the MediLabSecure Network. Curr Trop Med Rep. 41(1): 27–39.
28. Estrada-Peña A, Bouattour A, Camicas J, Walker A (2004) Ticks of domestic an-imals in the mediterranean region. p. 131.
29. Dedkov VG, Shchelkanov MY, Bushkieva BT, Rudenko TA, Kurdyukova OV, Galkina IV, Sapotsky MV, Blinova EA, Dzhambinov SD, Shipulin GA (2017) A neonatal death associated with Crime-an-Congo hemorrhagic fever (Republic of Kalmykia, Russia, June 2016). An-tiviral Res. 146: 146–148.
30. Biggerstaff BJ (2009) Mosquito Surveil- lance Software. Fort Collins, CO, USA: Center for Disease Control and Preven-tion. Avaliable at: www. cdc.gov/ncidod/dvbid/westnile/softwar e.htm.
31. Matevosyan K, Semashko I, Rubin S, Chu-makov M (1974) Antibodies to CHF virus in human and cattle blood sera from Armenia SSR (NAMRU-T939). Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 22: 173–175.
32. Semashko IV, Chumakov MP, Matev- osyan KSh, Safarov RK, Marutyan EM, Postoyan SR, Karapetyan RM, Bashkirtsev VN, Tkachenko EA, Chunikhin SP (1975) Results from the 1972–1974 works on isolation and investigation of CHF-Congo, Dhori, and Bhanja viruses in Azerbaijan and Armenia. 1975 October 21–23, Aca-demy of Medical Sciences, Moscow, USSR. pp. 354–355 (In Russian).
34. Dilbaryan KP, Hovhannisyan VS (2016) Arthropods (Arthropoda) of Armenia of medical importance, their biological and ecological peculiarities. Med Sci Armen. 6(1): 81–89 (in Russian).
35. Dilbaryan KP (2015) Blood-sucking ticks (family Ixodidae Murray, 1887, genus Dermacentor Koch, 1844) of Armenia being the transmitters of human and an-imal diseases. Theory Pract Parasitol Dis. 16: 120–122 (in Russian).
2. Ohimain EI (2017) Emerging Pathogens of Global Significance, Priorities for Atten-tion and Control. EC Microbiol. 56: 215–240.
3. Pshenichnaya NY, Sydenko IS, Klinovaya EP, Romanova EB, Zhuravlev AS (2016) Possible sexual transmission of Crime-an-Congo hemorrhagic fever. Int J In-fect Dis. 45: 109–11.
4. Eckerle I, Briciu VT, Ergönül Ö, Lupşe M, Papa A, Radulescu A, Tsiodras S, Tsitou C, Drosten C, Nussenblatt VR, Reusken CB, Sigfrid LA, Beeching NJ (2018) Emerging souvenirs-clinical presentation of the returning traveller with imported arbovirus infections in Europe. Clin Mi-crobiol Infect. 24(3): 240–245.
5. Maltezou HC, Andonova L, Andraghetti R, Bouloy M, Ergonul O, Jongejan F, Kal-vatchev N, Nichol S, Niedrig M, Pla-tonov A, Thomson G, Leitmeyer K, Zeller H (2010) Crimean-Congo hem-orrhagic fever in Europe: current situa-tion calls for preparedness. Euro Surveill. 15(10): 19504.
6. Sharififard M, Alavi SM, Salmanzadeh S, Safdari F, Kamali A (2016) Epidemio-logical Survey of Crimean-Congo Hem-orrhagic Fever (CCHF), a Fatal Infectious Disease in Khuzestan Province, South-west Iran, During 1999–2015. Jundisha-pur J Microbiol. 9(5): e30883.
7. Leblebicioglu H, Eroglu C, Erciyas-Yavuz K, Hokelek M, Acici M, Yilmaz H (2014) Role of Migratory Birds in Spread-ing Crimean-Congo Hemorrhagic Fever, Turkey. Emerg Infect Dis. 20(8): 1331–1334.
8. Metanat M, Sharifi-Mood B, Fathollah-zadeh N, Rezaei Kahkha L, Bahremand F, Sharifi R (2018) Report of a Family with Crimean-Congo Hemorrhagic Fever Following Contact with Frozen Meat: A Case Seires Study. Arch Clin Infect Dis. In Press.
9. Ahmadkhani M, Alesheikh AA, Khakifirouz S, Salehi-Vaziri M (2018) Space-time epidemiology of Crimean-Congo hemor-rhagic fever (CCHF) in Iran. Ticks Tick Borne Dis. 9(2): 207–216.
10. Ergonul O, Celikbas A, Dokuzoguz B, Eren S, Baykam N, Esener H (2004) Charac-teristics of Patients with Crimean-Con-go Hemorrhagic Fever in a Recent Out-break in Turkey and Impact of Oral Rib-avirin Therapy. Clin Infect Dis. 39(2): 284–287.
11. Papa A, Mirazimi A, Köksal I, Estrada-Pena A, Feldmann H (2015) Recent ad-vances in research on Crimean-Congo hemorrhagic fever. J Clin Virol. 64: 137–143.
12. Whitehouse C (2004) Crimean-Congo hem-orrhagic fever. Antiviral Res. 64(3): 145–160.
13. Mourya DT, Yadav PD, Shete AM, Gurav YK, Raut CG, Jadi RS, Pawar SD, Nichol ST, Mishra AC (2012) Detection, Iso-lation and Confirmation of Crimean-Con-go Hemorrhagic Fever Virus in Human, Ticks and Animals in Ahmadabad, India, 2010–2011. PLoS Negl Trop Dis. 6(5): e1653.
14. Tuncer P, Yesilbag K, Alpay G, Dincer E, Girisgin AO, Aydin L, Yavuz Uyar, Aykut Ozkul (2014) Crimean-Congo Hemorrhagic Fever infection in domes-tic animals in Marmara region, Western Turkey. Ankara Univ Vet Fak Derg. 61 (19): 49–53.
15. Hoogstraal H (1979) The epidemiology of tick-borne Crimean-Congo hemorrhag-ic fever in Asia, Europe, and Africa. J Med Entomol. 15(4): 307–417.
16. Yesilbag K, Aydin L, Dincer E, Alpay G, Girisgin AO, Tuncer P, Ozkul A (2013) Tick survey and detection of Crimean-Congo hemorrhagic fever virus in tick species from a non-endemic area, South Marmara region, Turkey. Exp Appl Ac-arol. 60(2): 253–261.
17. Ergonul O, Whitehouse CA (2007) Intro-duction. In: Ergonul O, Whitehouse CA. Crimean-Congo hemorrhagic fever. A global perspective. Dordrecht, Springer Science and Business Media 2007, p. 3–11.
18. Anderson JF, Magnarelli LA (2008) Biol-ogy of Ticks. Infect Dis Clin North Am. 22(2): 195–215.
19. Melik-Andreasyan GG, Keshishyan AS, Manukyan DV, Harutyunova KV, Harutyunova MV, Voskanyan LS (2013) A study of certain territories in Armenia for the presence of natural foci of tick-borne encephalitis and West Nile fever (in Russian). Med Sci Armen. 52(4): 52–58.
20. Semashko IV, Chumakov PM, Karapetyan MR (1974) First isolation of the CHF virus in Armenia from the blood of the patient with Crimean hemorrhagic fever. Sb Tr Inst Polio Virusn Encef Akad Med Nauk USSR. 7: 271–278.
21. Hekimoglu O, Ozer N, Ergunay K, Ozkul A (2012) Species distribution and de-tection of Crimean Congo Hemorrhag-ic Fever Virus (CCHFV) in field-col-lected ticks in Ankara Province, Central Anatolia, Turkey. Exp Appl Acarol. 56 (1): 75–84.
22. Leblebicioglu H, Ozaras R, Irmak H, Sen-can I (2016) Crimean-Congo hemor-rhagic fever in Turkey: Current status and future challenges. Antiviral Res. 126: 21–34.
23. Salehi-Vaziri M, Salmanzadeh S, Ban-iasadi V, Jalali T, Mohammadi T, Azad-Manjiri S, Jamshidi Y, Khakifirouz S, Fazlalipour M (2017) An Outbreak of Crimean-Congo Hemorrhagic Fever in the South West of Iran. Jundishapur J Microbiol. 10(1): e41735.
24. Shahhosseini N, Chinikar S, Shams E, Nowotny N, Fooks AR (2017) Crimean-Congo hemorrhagic fever cases in the North of Iran have three distinct origins. Virus Disease. 28(1): 50–53.
25. Wilder-Smith A, Gubler DJ, Weaver SC, Monath TP, Heymann DL, Scott TW (2017) Epidemic arboviral diseases: pri-orities for research and public health. Lancet Infect Dis. 17(3): 101–106.
26. Vardanyan MV, Gevorgyan H (2009) The study of the epidemiological peculiari- ties of piroplasmosis in the lowland zone of Armenia. The National Scientific-prac-tical Conference on Infectious Disease Epidemiology, 2009 September 22–26, National Institute of Epidemiology, Vi-rology and Medical Parsitology, Yerevan, Armenia, pp. 37–38.
27. Failloux AB, Bouattour A, Faraj C, Gunay F, Haddad N, Harrat Z, Jancheska E, Kanani K, Kenawy MA, Kota M, Pa-jovic I, Paronyan L, Petric D, Sarih M, Sawalha S, Shaibi T, Sherifi K, Sulesco T, Velo E, Gaayeb L, Victoir K, Robert V (2017) Surveillance of Arthropod-Borne Viruses and Their Vectors in the Mediterranean and Black Sea Regions Within the MediLabSecure Network. Curr Trop Med Rep. 41(1): 27–39.
28. Estrada-Peña A, Bouattour A, Camicas J, Walker A (2004) Ticks of domestic an-imals in the mediterranean region. p. 131.
29. Dedkov VG, Shchelkanov MY, Bushkieva BT, Rudenko TA, Kurdyukova OV, Galkina IV, Sapotsky MV, Blinova EA, Dzhambinov SD, Shipulin GA (2017) A neonatal death associated with Crime-an-Congo hemorrhagic fever (Republic of Kalmykia, Russia, June 2016). An-tiviral Res. 146: 146–148.
30. Biggerstaff BJ (2009) Mosquito Surveil- lance Software. Fort Collins, CO, USA: Center for Disease Control and Preven-tion. Avaliable at: www. cdc.gov/ncidod/dvbid/westnile/softwar e.htm.
31. Matevosyan K, Semashko I, Rubin S, Chu-makov M (1974) Antibodies to CHF virus in human and cattle blood sera from Armenia SSR (NAMRU-T939). Tr Inst Polio Virus Entsef Akad Med Nauk SSSR. 22: 173–175.
32. Semashko IV, Chumakov MP, Matev- osyan KSh, Safarov RK, Marutyan EM, Postoyan SR, Karapetyan RM, Bashkirtsev VN, Tkachenko EA, Chunikhin SP (1975) Results from the 1972–1974 works on isolation and investigation of CHF-Congo, Dhori, and Bhanja viruses in Azerbaijan and Armenia. 1975 October 21–23, Aca-demy of Medical Sciences, Moscow, USSR. pp. 354–355 (In Russian).
34. Dilbaryan KP, Hovhannisyan VS (2016) Arthropods (Arthropoda) of Armenia of medical importance, their biological and ecological peculiarities. Med Sci Armen. 6(1): 81–89 (in Russian).
35. Dilbaryan KP (2015) Blood-sucking ticks (family Ixodidae Murray, 1887, genus Dermacentor Koch, 1844) of Armenia being the transmitters of human and an-imal diseases. Theory Pract Parasitol Dis. 16: 120–122 (in Russian).
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| Issue | Vol 13 No 1 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i1.928 | |
| Keywords | ||
| CCHF Ixodid ticks Armenia ELISA Infection rate | ||
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How to Cite
1.
Gevorgyan H, Grigoryan GG, Atoyan HA, Rukhkyan M, Hakobyan A, Zakaryan H, Aghayan SA. Evidence of Crimean-Congo Haemorrhagic Fever Virus Occurrence in Ixodidae Ticks of Armenia. J Arthropod Borne Dis. 2018;13(1):9.
