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Table 1.  

Characteristic Patient no. and source
1 (10) 2 (10) 3 (12) 4 (13) 5 6 7 8 (11) 9 10
Age, y 62 50 74 53 70 54 69 32 59 30
Sex M F M M M M M F M F
Rural location No No No Yes Yes Yes Yes No Yes No
Date 2016 Aug 2016 Aug 2018 Jul 2018 Aug 2020 Jun 2020 Jul 2020 Aug 2013 May 2021 Apr 2021 Jun
Risk factors† Leisure Nurse Hunting Ag Ag Ag Leisure Leisure Ag Leisure
Comorbidities HTN, OSA None None Hepatic steatosis, active drinker Tongue cancer TB,
HTN None Diabetes mellitus, dyslipemia Diabetes mellitus
Bakir scale at admission 7 0 7 6 6 4 8 5 2 5
Outcome Died Good Died Good Good Good Died Good Good Good

Table 1. Main epidemiologic data of patients with Crimean-Congo hemorrhagic fever, Spain, 2013–2021*

*Source is indicated if other than this study. Ag, agriculture; HTN, hypertension; OSA, obstructive sleep apnea. †Risk factors include high-risk occupations; agriculture includes shepherding activities.

Table 2.  

Characteristic Patient no. and source
1 (10) 2 (10) 3 (12) 4 (13) 5 6 7 8 (11) 9 10
Main clinical data                    
   Tick bite Y N Y N Y Y Y Y Y Y
   First symptom Fever Fever Fever Fever Fever Fever Fever Fever Fever Fever
   Fever duration, d 4 5 6 6 9 5 4 4 4 5
   Days from first symptom to admission 3 2 4 5 9 7 3 2 4 12
   Digestive symptoms Y Y Y N Y N Y Y Y Y
   Any bleeding Y Y Y N Y N Y Y N Y
Laboratory data†                    
   Hemoglobin, g/dL 13.4 13.9 13.5 14.1 14.6 15.5 13.4 14.4 17 17
   Leukocytes, × 103 cells/mm3 13.9 6.2 10.7 3.1 2.4 2.3 5.5 1.5 2.8 11.1
   Neutrophils, % 85.5 83 90 62 33 66.4 69 63 68.5 90
   Lymphocytes, % 7.9 10.2 5 27 38 26.1 25 31 24.4 4
   Platelets, × 103/mm3 30 174 229 41 44 32 7 44 76 159
   Glucose, mg/d 80 102 83 135 110 134 280 106 116 491
   Creatinine, mg/dL 1.69 1.24 0.83 1.33 0.92 0.75 4.8 0.67 0.85 1.1
   CRP, mg/L 87.6 2.9 ND 15.2 0.3 0.65 3.72 0.6 0.55 52
   AST, U/L 203 24 20 347 273 273 1,305 494 107 72
   ALT, U/L 88 37 9 161 281 135 347 171 141 70
   Ferritin, ng/mL ND ND >40,000‡ 15,718 34,044 28,393 60,000 ND 7,878 1,147
   Bilirubin, mg/dL 0.9 0.5 0.5 0.7 0.43 0.35 1.4 0.29 0.58 ND
   GGT, U/L ND ND ND 425 272 132 1,420 77 136 ND
   ALP, U/L ND ND ND 103 84 59 239 58 72 91
   LDH, U/L ND ND 172 721 358 589 2,311 1,085 341 272
   Triglycerides, mg/dL ND ND ND ND ND 407‡ ND ND 164‡ ND
   Prothrombin time, s 18.1 15.6 10.7 10.2 10 12 13 12 11 ND
   Prothrombin activity, % 52.8 62 104 106 123 99 86 81 102 84
   Partial thromboplastin time, s 18.1 48.7 26.2 43.8 30.2 52.7 61.4 128 ND 29
   Functional fibrinogen, mg/dL ND 265.9 320 605 281 304 156 141 272 325
   D-dimer, ng/mL ND 35,200 ND ND ND 1.3 5.5 3.48 ND ND
   Genotype III III IV V III III III ND V ND
Treatment DOX; support DOX; Ribavirin ev/orally for 9 d DOX; support DOX DOX; ribavirin orally for 10 d§ DOX; ribavirin orally for 10 d§ DOX support DOX; support DOX DOX; support
Length of stay, d 9 23 8 6 22 9 2 17 9 8

Table 2. Main clinical and laboratory data of patients with Crimean-Congo hemorrhagic fever, Spain, 2013–2021*

*Source is indicated if other than this study. ALP, alkaline phosphatase; ALT, alanine aminotransferase; AST, aspartate aminotransferase; CRP, C-reactive protein; DOX, doxycycline; GGT, gamma-glutamyl transferase; LDH, lactate dehydrogenase; ND, no data. †Analysis upon admission or during the first 24 hours. ‡Analysis performed during hospital admission. §In accordance with World Health Organization guidelines.

CME / ABIM MOC

Crimean-Congo Hemorrhagic Fever, Spain, 2013–2021

  • Authors: Helena Miriam Lorenzo Juanes, PharmD, PhD Student; Cristina Carbonell, MD, PhD; Begoña Febrer Sendra, BSc, PhD Student; Amparo López-Bernus, MD, PhD; Alberto Bahamonde, MD, PhD; Alberto Orfao, MD, PhD; Carmen Viera Lista, BSc, PhD Student; María Sánchez Ledesma, MD, PhD; Ana Isabel Negredo, PhD; Beatriz Rodríguez Alonso, MD, PhD; Beatriz Rey Bua, MD; María Paz Sánchez-Seco, PhD; Juan Luis Muñoz Bellido, MD, PhD; Antonio Muro, MD, PhD; Moncef Belhassen-García, MD, PhD
  • CME / ABIM MOC Released: 1/23/2023
  • Valid for credit through: 1/23/2024, 11:59 PM EST
Start Activity

  • Credits Available

    Physicians - maximum of 1.00 AMA PRA Category 1 Credit(s)™

    ABIM Diplomates - maximum of 1.00 ABIM MOC points

    You Are Eligible For

    • Letter of Completion
    • ABIM MOC points

Target Audience and Goal Statement

This activity is intended for infectious disease specialists and other clinicians who take care of patients who may develop Crimean-Congo hemorrhagic fever.

The goal of this activity is for learners to be better able to evaluate the clinical presentation and common genotypes of Crimean-Congo hemorrhagic fever.

Upon completion of this activity, participants will:

  • Analyze the disease condition of Crimean-Congo hemorrhagic fever
  • Assess the epidemiology of Crimean-Congo hemorrhagic fever in the current study
  • Assess the clinical presentation of Crimean-Congo hemorrhagic fever in the current study
  • Distinguish the most common genotype of Crimean-Congo hemorrhagic fever in the current study


Disclosures

Medscape, LLC requires every individual in a position to control educational content to disclose all financial relationships with ineligible companies that have occurred within the past 24 months. Ineligible companies are organizations whose primary business is producing, marketing, selling, re-selling, or distributing healthcare products used by or on patients.

All relevant financial relationships for anyone with the ability to control the content of this educational activity are listed below and have been mitigated. Others involved in the planning of this activity have no relevant financial relationships.


Faculty

  • Helena Miriam Lorenzo Juanes, PharmD, PhD Student

    Servicio de Microbiología y Parasitología
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Universidad de Salamanca, Salamanca, Spain

  • Cristina Carbonell, MD, PhD

    Servicio de Medicina Interna
    Unidad de Infecciosas
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Universidad de Salamanca
    Salamanca, Spain

  • Begoña Febrer Sendra, BSc, PhD Student

    Grupo Enfermedades Infecciosas y Tropicales
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Facultad de Farmacia
    Universidad de Salamanca
    Salamanca, Spain

  • Amparo López-Bernus, MD, PhD

    Servicio de Medicina Interna
    Unidad de Infecciosas
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Universidad de Salamanca
    Salamanca, Spain

  • Alberto Bahamonde, MD, PhD

    Servicio de Medicina Interna
    Hospital El Bierzo
    Ponferrada, Spain

  • Alberto Orfao, MD, PhD

    Centro de Investigación del Cancer
    Servicio de Citometría
    Centro de Investigación Biomédica en Red de Cáncer
    Instituto de Investigación Biomédica de Salamanca
    Universidad de Salamanca
    Salamanca, Spain

  • Carmen Viera Lista, BSc, PhD Student

    Grupo Enfermedades Infecciosas y Tropicales
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Facultad de Farmacia
    Universidad de Salamanca
    Salamanca, Spain

  • María Sánchez Ledesma, MD, PhD

    Servicio de Medicina Interna
    Unidad de Infecciosas
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Universidad de Salamanca
    Salamanca, Spain

  • Ana Isabel Negredo, PhD

    Arbovirus and Imported Viral Diseases Unit
    Centro Nacional de Microbiología
    Instituto de Salud Carlos III
    Red de Investigación Colaborativa en Enfermedades Tropicales
    Madrid, Spain

  • Beatriz Rodríguez Alonso, MD, PhD

    Servicio de Medicina Interna
    Unidad de Infecciosas
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Universidad de Salamanca
    Salamanca, Spain

  • Beatriz Rey Bua, MD

    Servicio de Haematología
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Universidad de Salamanca
    Salamanca, Spain

  • María Paz Sánchez-Seco, PhD

    Arbovirus and Imported Viral Diseases Unit
    Centro Nacional de Microbiología
    Instituto de Salud Carlos III
    Red de Investigación Colaborativa en Enfermedades Tropicales
    Madrid, Spain

  • Juan Luis Muñoz Bellido, MD, PhD

    Servicio de Microbiología y Parasitología
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Departamento de Ciencias Biomédicas y del Diagnóstico
    Universidad de Salamanca
    Salamanca, Spain

  • Antonio Muro, MD, PhD

    Grupo Enfermedades Infecciosas y Tropicales
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Universidad de Salamanca
    Salamanca, Spain

  • Moncef Belhassen-García, MD, PhD

    Servicio de Medicina Interna
    Unidad de Infecciosas
    Hospital Universitario de Salamanca
    Instituto de Investigación Biomédica de Salamanca
    Centro de Investigación en Enfermedades Tropicales
    Grupo Enfermedades Infecciosas y Tropicales
    Universidad de Salamanca
    Salamanca, Spain

CME Author

  • Charles P. Vega, MD

    Health Sciences Clinical Professor of Family Medicine
    University of California, Irvine School of Medicine

    Disclosures

    Charles P. Vega, MD, has the following relevant financial relationships:
    Consultant or advisor for: GlaxoSmithKline; Johnson & Johnson Pharmaceutical Research & Development, L.L.C.

Editor

  • Dana C. Dolan, BS

    Copyeditor 
    Emerging Infectious Diseases

Compliance Reviewer

  • Amanda Jett, PharmD, BCACP

    Associate Director, Accreditation and Compliance, Medscape, LLC

    Disclosures

    Amanda Jett, PharmD, BCACP, has no relevant financial relationships.

Peer Reviewer

This activity has been peer reviewed and the reviewer has no relevant financial relationships.


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Interprofessional Continuing Education

In support of improving patient care, this activity has been planned and implemented by Medscape, LLC and Emerging Infectious Diseases. Medscape, LLC is jointly accredited with commendation by the Accreditation Council for Continuing Medical Education (ACCME), the Accreditation Council for Pharmacy Education (ACPE), and the American Nurses Credentialing Center (ANCC), to provide continuing education for the healthcare team.

    For Physicians

  • Medscape, LLC designates this Journal-based CME activity for a maximum of 1.0 AMA PRA Category 1 Credit(s)™ . Physicians should claim only the credit commensurate with the extent of their participation in the activity.

    Successful completion of this CME activity, which includes participation in the evaluation component, enables the participant to earn up to 1.0 MOC points in the American Board of Internal Medicine’s (ABIM) Maintenance of Certification (MOC) program. Participants will earn MOC points equivalent to the amount of CME credits claimed for the activity. It is the CME activity provider’s responsibility to submit participant completion information to ACCME for the purpose of granting ABIM MOC credit.

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CME / ABIM MOC

Crimean-Congo Hemorrhagic Fever, Spain, 2013–2021

Authors: Helena Miriam Lorenzo Juanes, PharmD, PhD Student; Cristina Carbonell, MD, PhD; Begoña Febrer Sendra, BSc, PhD Student; Amparo López-Bernus, MD, PhD; Alberto Bahamonde, MD, PhD; Alberto Orfao, MD, PhD; Carmen Viera Lista, BSc, PhD Student; María Sánchez Ledesma, MD, PhD; Ana Isabel Negredo, PhD; Beatriz Rodríguez Alonso, MD, PhD; Beatriz Rey Bua, MD; María Paz Sánchez-Seco, PhD; Juan Luis Muñoz Bellido, MD, PhD; Antonio Muro, MD, PhD; Moncef Belhassen-García, MD, PhDFaculty and Disclosures

CME / ABIM MOC Released: 1/23/2023

Valid for credit through: 1/23/2024, 11:59 PM EST

processing....

Abstract

Crimean-Congo hemorrhagic fever (CCHF) is a viral infectious disease for which distribution of the main vector, Hyalomma spp. ticks, is expanding. We analyzed all 10 cases of CCHF diagnosed in Spain during 2013–2021; case-patient median age was 56.5 years, and 7 were men. We identified CCHF virus genotypes III and V. Six case-patients acquired the infection in urban areas. Sixty percent of patients were infected in summer and 40% in spring. Two patients met criteria for hemophagocytic syndrome. Seven patients survived. The epidemiologic pattern of CCHF in Spain is based on occasional cases with an elevated mortality rate. Genotype III and, to a less extent also genotype V, CCHF circulates in humans in a common geographic area in Spain. Those data suggest that the expansion pathways are complex and may change over time. Physicians should remain alert to the possibility of new CCHF cases.

Introduction

Crimean-Congo hemorrhagic fever (CCHF) is a tickborne viral disease caused by the CCHF virus (CCHFV), a negative single-stranded RNA virus of the genus Orthonairovirus in the Nairoviridae family[1]. CCHF is considered an emerging infectious disease because of the expanding distribution of its main vector, ticks of the genus Hyalomma. Consequently, CCHF is listed by the World Health Organization as one of the top-priority diseases for research and development in public health emergency contexts (https://www.who.int/activities/prioritizingdiseases-for-research-and-development-in-emergency-contexts)[2].

The spectrum of clinical manifestations of CCHF ranges from subclinical illness (including fever, headache, malaise, myalgia, sore throat, dizziness, abdominal pain, nausea, vomiting, conjunctivitis, and photophobia)[3] to acute infection with hemorrhage, multiorgan failure, and death[4]. Laboratory findings are frequently remarkable, including leukopenia, thrombocytopenia, and elevated liver transaminases in serum[5]. Some studies have suggested the relevance of the innate immune system in limiting the spread of the virus, but the specific mechanisms leading to asymptomatic versus severe disease remain unknown.

In recent years, the epidemiology of CCHFV has changed; climate change has been identified as one of the factors driving the circulation of the virus. CCHFV has been identified in Africa, Asia, and Europe, in territories located south of the 50th North parallel, the area inhabited by its main vector[6–8]. CCHFV has caused major outbreaks in eastern Europe[9]. In turn, CCHF is considered endemic in areas of southwestern Europe.

Our group identified the first human cases in western Spain in summer 2013[10–13]. In Spain, the CCHFV genotype identified from patients in 2016 and 2018 belonged to the African genotype III, the European genotype V, and the Asian genotype IV where the group Africa 4 is placed[10,12,13]. A strong clinical suspicion is required to obtain fast and accurate diagnosis, initiate supportive treatment if needed, and activate biosafety measures to prevent nosocomial transmission[10]. Herein, we report on the clinical and epidemiologic pattern and the genotype of the virus identified in all patients with CCHF investigated in Spain from 2013 through May 2022.

The Clinical Research Ethics Committee of Investigation with Drugs of the Hospital Universitario de Salamanca (Salamanca, Spain) approved the study protocol (CEIMC PI 91 09/2017). All procedures described were carried out in accordance with the ethical standards described in the Revised Declaration of Helsinki of 2013. All clinical and epidemiologic data were anonymized.