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Volume 20, Number 3—March 2014

Crimean-Congo Hemorrhagic Fever among Health Care Workers, Turkey

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Aysel Kocagul Celikbas, Başak Dokuzoğuz, Nurcam Baykam, Sebnem Eren Gok, Mustafa Necati Eroğlu, Kenan Midilli, Herve Zeller, and Onder ErgonulComments to Author 
Author affiliations: Ankara Numune Training and Research Hospital, Ankara, Turkey (A.K. Celikbas, B. Dokuzoğuz, N. Baykam, S.E. Gok, M.N. Eroğlu); Istanbul University, Istanbul, Turkey (K. Midilli); Institut Pasteur, Lyon, France (H. Zeller); Koç University, Istanbul (O. Ergonul)

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We investigated 9 cases of Crimean-Congo hemorrhagic fever (1 fatal, 2 asymptomatic) among health care workers in Turkey. Needlestick injuries were reported for 4 workers. Eight received ribavirin. In addition to standard precautions, airborne infection isolation precautions are essential during aerosol-generating procedures. For postexposure prophylaxis and therapy, ribavirin should be given.

Crimean-Congo hemorrhagic fever (CCHF) has been described from Africa, Asia, southeastern Europe, and the Middle East (1). The CCHF virus (CCHFV) belongs to the family Bunyaviridae, genus Nairovirus, and causes severe disease in humans; the reported case-fatality rate is 3%–30% (1). Humans become infected through the bites of ticks, contact with infected patients' body fluids, or contact with blood or tissues from viremic livestock. Health care workers (HCWs) are at occupational risk for CCHFV infection. Health care–related CCHFV infections have been reported in Pakistan (25), the United Arab Emirates (6), South Africa (7), Iran (8), India (9), Tajikistan (10), and Turkey (11). We describe the outcomes of 9 HCWs in Turkey who had occupational exposure to CCHFV.

The Cases

The 9 HCWs and all CCHF patients under their care were admitted to the Infectious Diseases and Clinical Microbiology clinic (IDCM) of Ankara Numune Education and Research Hospital (Ankara, Turkey) during 2004–2011 with confirmed CCHF. All 9 HCWs were aware of possible or confirmed CCHFV infection in their patients. During this period, ≈7,000 confirmed CCHF cases were recorded in Turkey; nearly 300 of these patients were hospitalized in IDCM. Acute- and convalescent-phase serum samples from the index patients were sent to the national reference laboratory of Turkey. CCHFV infection was confirmed through IgM positivity by ELISA and/or positive PCR results for CCHFV in blood. After episode 1, the HCWs’ serum samples were sent to the Pasteur Institute (Lyon, France) for contact tracing. The HCWs’ infections were scored according to a severity score index (12). In episode 3, to investigate the source of infection, molecular techniques were used. Oral ribavirin for treatment was administered at the dosage recommended by the World Health Organization (4 g/d for 4 d, 2.4 g/d for 6 d), and for prophylaxis (2g/4×/d for 7 d). The index patients and the HCWs were given erythrocyte, fresh frozen plasma, and total blood preparations depending on their homeostasis.

Episode 1

In 2005, CCHFV infection was diagnosed in a woman on the day of delivery by cesarean section. She was transferred to IDCM, and her baby was transferred to the newborn service at the Dr. Sami Ulus Children's Hospital (Ankara, Turkey). A nurse in IDCM, who had fever and myalgia, was later found to have CCHFV infection (Table 1). Transmission was related to the improper use of gloves during the care of the mother’s surgical wound. The mother recovered, but the infant died 5 days after birth. A nurse in the neonatal clinic in the children’s hospital also acquired CCHFV infection, which was attributed to the intubation and aspiration of bloody secretions from the baby without proper use of gloves and mask. For both HCWs, the incubation period was 2 days. The first HCW was given ribavirin at symptom onset. The second nurse’s illness was mild; because she had a potential for getting pregnant, ribavirin was not started. Both nurses recovered completely (Table 2).

After this episode, the index patient’s contacts were traced. Serum samples from 37 HCWs at IDCM and the obstetrics and newborn clinics at the children’s hospital who were at risk for infection were investigated for CCHF. In addition to the 2 nurses, 2 nurses from the neonatal clinic were CCHF IgM positive but were asymptomatic.

Episode 2

In 2006, a nurse received a needlestick injury during a phlebotomy of a CCHFV-infected patient. She was using gloves but no gown, and the needle stuck to her forearm. The infected patient died. The nurse’s symptoms began 2 days after the incident, and she was transferred to IDCM 4 days after the incident. At admission, her severity score index was high. She had ecchymosis, epistaxis, hematemesis, melena, vaginal bleeding, and somnolence (Table 1). She received oral ribavirin 5 days after the incident, which possibly had limited effect because her illness already had progressed to confusion and gastrointestinal bleeding. She died on the second day after hospital admission.

Episode 3

In 2008, a patient with CCHFV infection and a high viral load (108 copies/mL) was hospitalized with hemoptysis, hematemesis, melena, epistaxis, and intraalveolar bleeding. He died 3 days after admission. One infectious diseases resident and 2 otorhinolaryngology residents acquired CCHFV infection. All HCWs had worn personal protective equipment during the intervention. One otorhinolaryngology resident performed nasal tamponade. After the intervention, the other otorhinolaryngology resident handled and cleaned a head mirror without using gloves, although he was not in face-to-face contact with the patient. The infectious diseases resident resuscitated the patient without apparent direct contact with the patient’s bloody secretions. For the 3 residents, fever, malaise, and myalgia developed 2–5 days after exposure. Ribavirin was started at symptom onset. No contact was observed between the patient and the HCWs, but the RNA sequences from the patients and HCWs were identical by molecular techniques. All of the HCWs recovered.

The transmission of CCHFV could have resulted from indirect contact with contaminated devices, such as the head mirror; the improper removal of gowns, masks, gloves; inadequate hand hygiene; or failure to use N95 masks during aerosolizing procedures. During the procedures that could generate aerosols, HCWs should wear an N95 mask or FFP2 respirator (13). The patients with higher viral load were reported to be more severe disease (14).

Episode 4

In 2008, a phlebotomist working in a children’s hospital had a needlestick injury during phlebotomy of a CCHFV-infected child. He was hospitalized 1 day after symptom onset, and ribavirin was started. His severity score index was moderate, and he recovered.

Episodes 5 and 6

A nurse in 2007 and a pediatric resident in 2008 incurred needlestick injuries during phlebotomy of a CCHFV-infected patient. Postexposure prophylaxis with ribavirin was started immediately after the injuries, and no infections developed.


Six of the 9 CCHF-infected HCWs reported here had histories of needlestick injuries or contact with contaminated blood without adequate barrier precautions. An integrated strategy for controlling accidental exposure to body fluids was developed to protect HCWs against CCHFV infection. All personnel, including cleaning staff in health care units on all shifts were informed and trained about the transmission risks, protection, and clinical symptoms of CCHF (13). The standard, contact, and droplet precautions were usually sufficient to protect against CCHFV infection during the routine care of CCHF patients. In addition to the practices of previous years, the airborne infection isolation precautions during aerosol-generating procedures were performed. The number of HCWs caring for patients with severe CCHF was limited. After all of these measures were enforced, occupational CCHFV infection did not occur in IDCM.

Ribavirin is an effective treatment for CCHFV infection (12) and beneficial for postexposure prophylaxis (13,15). Therapy should be started as early as possible. In the 2 HCWs reported here who received ribavirin for postexposure prophylaxis, no symptoms developed; similar reports will be useful for increasing the power of this conclusion. We used a ribavirin dosage of 2g/day, but no consensus exists about the dosage for postexposure prophylaxis.

Dr Celikbas is an infectious disease and clinical microbiology specialist at the Ankara Numune Training and Education Hospital in Ankara, Turkey. Her primary research interests include emerging infections and brucellosis.



  1. Ergonul  O. Crimean-Congo hemorrhagic fever virus: new outbreaks, new discoveries. Curr Opin Virol. 2012;2:215–20.PubMedGoogle Scholar
  2. Athar  MN, Khalid  MA, Ahmad  AM, Bashir  N, Baqai  HZ, Ahmad  M, Crimean-Congo hemorrhagic fever outbreak in Rawalpindi, Pakistan, February 2002: contact tracing and risk assessment. Am J Trop Med Hyg. 2005;72:4713 .PubMedGoogle Scholar
  3. Altaf  A, Luby  S, Ahmed  AJ, Zaidi  N, Khan  AJ, Mirza  S, Outbreak of Crimean-Congo haemorrhagic fever in Quetta, Pakistan: contact tracing and risk assessment. Trop Med Int Health. 1998;3:87882 . DOIPubMedGoogle Scholar
  4. Fisher-Hoch  SP, McCormick  JB, Swanepoel  R, Van Middlekoop  A, Harvey  S, Kustner  HG. Risk of human infections with Crimean-Congo hemorrhagic fever virus in a South African rural community. Am J Trop Med Hyg. 1992;47:33745 .PubMedGoogle Scholar
  5. Burney  MI, Ghafoor  A, Saleen  M, Webb  PA, Casals  J. Nosocomial outbreak of viral hemorrhagic fever caused by Crimean hemorrhagic fever–Congo virus in Pakistan, January 1976. Am J Trop Med Hyg. 1980;29:9417 .PubMedGoogle Scholar
  6. Suleiman  MN, Muscat-Baron  JM, Harries  JR, Satti  AG, Platt  GS, Bowen  ET, Congo/Crimean haemorrhagic fever in Dubai. An outbreak at the Rashid Hospital. Lancet. 1980;2:93941 . DOIPubMedGoogle Scholar
  7. van de Wal  BW, Joubert  JR, van Eeden  PJ, King  JB. A nosocomial outbreak of Crimean-Congo haemorrhagic fever at Tygerberg Hospital. Part IV. Preventive and prophylactic measures. S Afr Med J. 1985;68:72932 .PubMedGoogle Scholar
  8. Mardani  M, Rahnavardi  M, Rajaeinejad  M, Naini  KH, Chinikar  S, Pourmalek  F, Crimean-Congo hemorrhagic fever among health care workers in Iran: a seroprevalence study in two endemic regions. Am J Trop Med Hyg. 2007;76:4435 .PubMedGoogle Scholar
  9. Mishra  AC, Mehta  M, Mourya  DT, Gandhi  S. Crimean-Congo haemorrhagic fever in India. Lancet. 2011;378:372 . DOIPubMedGoogle Scholar
  10. Tishkova  FH, Belobrova  EA, Valikhodzhaeva  M, Atkinson  B, Hewson  R, Mullojonova  M. Crimean-Congo hemorrhagic fever in Tajikistan. Vector Borne Zoonotic Dis. 2012;12:7226 . DOIPubMedGoogle Scholar
  11. Tütüncü  EE, Gurbuz  Y, Ozturk  B, Kuscu  F, Sencan  I. Crimean Congo haemorrhagic fever, precautions and ribavirin prophylaxis: a case report. Scand J Infect Dis. 2009;41:37880 . DOIPubMedGoogle Scholar
  12. Dokuzoguz  B, Celikbas  A, Eren  S, Baykam  N, Eroglu  MN, Ergonul  O. Severity scoring index for Crimean Congo hemorrhagic fever virus infection and the impact of ribavirin and corticosteroids on fatality. Clin Infect Dis. 2013;57:12704 . DOIPubMedGoogle Scholar
  13. Tarantola  A, Ergonul  O, Tattevin  P. Estimates and prevention of Crimean Congo hemorrhagic fever risks for health care workers. In: Ergonul O, Whitehouse CA, editors. Crimean-Congo hemorrhagic fever: a global perspective. Dordrecht (the Netherlands): Springer; 2007. p. 281–94.
  14. Duh  D, Saksida  A, Petrovec  M, Ahmeti  S, Dedushaj  I, Panning  M, Viral load as predictor of Crimean-Congo hemorrhagic fever outcome. Emerg Infect Dis. 2007;13:176972. DOIPubMedGoogle Scholar
  15. Ergonul  O. Treatment of Crimean-Congo hemorrhagic fever. Antiviral Res. 2008;78:12531. DOIPubMedGoogle Scholar




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DOI: 10.3201/eid2003.131353

Table of Contents – Volume 20, Number 3—March 2014

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Onder Ergonul, Koç University, School of Medicine, Infectious Diseases Department, Istanbul, TurkeyOnder Ergonul, Koç University, School of Medicine, Infectious Diseases Department, Istanbul, Turkey

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