Multi-antigen serology and a diagnostic algorithm for the detection of arbovirus infections as novel tools for arbovirus preparedness in southeast Europe (MERMAIDS-ARBO): a prospective observational study
Arboviruses are increasingly affecting Europe, partly due to the effects of climate change. This increase in range and impact emphasises the need to improve preparedness for emerging arboviral infections that often co-circulate and might have overlapping clinical syndromes. We aimed to strengthen su...
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| Published in | The Lancet infectious diseases Vol. 25; no. 6; pp. 678 - 689 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Ltd
01.06.2025
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1473-3099 1474-4457 1474-4457 |
| DOI | 10.1016/S1473-3099(24)00654-6 |
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| Abstract | Arboviruses are increasingly affecting Europe, partly due to the effects of climate change. This increase in range and impact emphasises the need to improve preparedness for emerging arboviral infections that often co-circulate and might have overlapping clinical syndromes. We aimed to strengthen surveillance networks for four clinically relevant arboviruses in southeast Europe.
This study reports an in-depth analysis of the MERMAIDS-ARBO prospective observational study in adults (ie, aged ≥18 years) hospitalised with an arbovirus-compatible disease syndrome in 21 hospitals in seven countries in southeast Europe over four arbovirus seasons (May 1–Oct 31, 2016–19) to obtain arbovirus prevalence outcomes. The main objectives of the MERMAIDS-ARBO study, describing the clinical management and outcomes of four arboviruses endemic to southeast Europe, including Crimean–Congo haemorrhagic fever virus (CCHFV), tick-borne encephalitis virus (TBEV), Toscana virus, and West Nile virus (WNV), are reported elsewhere. In this analysis, given the challenges associated with arbovirus diagnostics, we developed a diagnostic algorithm accounting for serology outcomes and sample timing to study arbovirus prevalence in southeast Europe. Serum samples were collected on days 0, 7, 28, and 60 after hospital admission and tested for anti-CCHFV IgG and IgM antibodies with ELISAs (confirmed with an indirect immunofluorescence test) and for IgG and IgM antibodies specific to TBEV, Toscana virus, and WNV with custom-printed protein microarrays (confirmed with virus neutralisation tests). All acute-phase samples were tested by PCR for all four viruses. Descriptive analyses were performed for virus-reactive cases by geography and year, and possible factors (eg, age, sex, and insect bites) associated with virus reactivity were assessed.
Of 2896 individuals screened, 913 were eligible for inclusion, of whom 863 (514 men, 332 women, and 17 unknown) had samples sent to the study reference laboratories and were included in molecular and serological analyses. Some individuals had insufficient clinical data to be included in the clinical analysis, but met the eligibility criteria for and were included here. Serum sampling was incomplete (eg, samples missing from one or more timepoints or no data on time since symptom onset) for 602 (70%) patients, and the timing of collection was often heterogeneous after symptom onset up to 40 days (average median delay of 5–6 days across all timepoints), affecting the ability to diagnose arbovirus infection by serology. By use of an interpretation table incorporating timing and completeness of sampling, one (<1%) participant had a confirmed recent infection with CCHFV, ten (1%) with TBEV, 40 (5%) with Toscana virus, and 52 (6%) with WNV. Most acute confirmed infections of Toscana virus were found in Albania (25 [63%] of 40), whereas WNV was primarily identified in Romania (36 [69%] of 52). Albania also had the highest overall Toscana virus seropositivity (168 [60%] of 282), mainly explained by patients confirmed to be exposed or previously exposed (104 [62%] of 168). Patients without antibodies to WNV or Toscana virus were significantly younger than patients with antibodies (mean difference –8·48 years [95% CI –12·31 to –4·64] for WNV, and –6·97 years [–9·59 to –4·35] for Toscana virus). We found higher odds of Toscana virus reactivity in men (odds ratio 1·56 [95% CI 1·15 to 2·11]; p=0·0055), WNV reactivity with mosquito bites versus no mosquito bites (2·47 [1·54 to 3·97]; p=0·0002), and TBEV reactivity with tick bites versus no tick bites (2·21 [1·19 to 4·11]; p=0·018).
This study shows that despite incomplete and heterogeneous data, differential diagnosis of suspected arbovirus infections is possible, and the diagnostic interpretation algorithm we propose could potentially be used to strengthen routine diagnostics in clinical settings in areas at risk for arboviral diseases. Our data highlight potential hotspots for arbovirus surveillance and risk factors associated with these particular arbovirus infections.
European Commission and Versatile Emerging infectious disease Observatory.
For the Greek, Albanian, Romanian, Bosnian, Serbian, and Croatian translation of the summary see Supplementary Materials section. |
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| AbstractList | Arboviruses are increasingly affecting Europe, partly due to the effects of climate change. This increase in range and impact emphasises the need to improve preparedness for emerging arboviral infections that often co-circulate and might have overlapping clinical syndromes. We aimed to strengthen surveillance networks for four clinically relevant arboviruses in southeast Europe.BACKGROUNDArboviruses are increasingly affecting Europe, partly due to the effects of climate change. This increase in range and impact emphasises the need to improve preparedness for emerging arboviral infections that often co-circulate and might have overlapping clinical syndromes. We aimed to strengthen surveillance networks for four clinically relevant arboviruses in southeast Europe.This study reports an in-depth analysis of the MERMAIDS-ARBO prospective observational study in adults (ie, aged ≥18 years) hospitalised with an arbovirus-compatible disease syndrome in 21 hospitals in seven countries in southeast Europe over four arbovirus seasons (May 1-Oct 31, 2016-19) to obtain arbovirus prevalence outcomes. The main objectives of the MERMAIDS-ARBO study, describing the clinical management and outcomes of four arboviruses endemic to southeast Europe, including Crimean-Congo haemorrhagic fever virus (CCHFV), tick-borne encephalitis virus (TBEV), Toscana virus, and West Nile virus (WNV), are reported elsewhere. In this analysis, given the challenges associated with arbovirus diagnostics, we developed a diagnostic algorithm accounting for serology outcomes and sample timing to study arbovirus prevalence in southeast Europe. Serum samples were collected on days 0, 7, 28, and 60 after hospital admission and tested for anti-CCHFV IgG and IgM antibodies with ELISAs (confirmed with an indirect immunofluorescence test) and for IgG and IgM antibodies specific to TBEV, Toscana virus, and WNV with custom-printed protein microarrays (confirmed with virus neutralisation tests). All acute-phase samples were tested by PCR for all four viruses. Descriptive analyses were performed for virus-reactive cases by geography and year, and possible factors (eg, age, sex, and insect bites) associated with virus reactivity were assessed.METHODSThis study reports an in-depth analysis of the MERMAIDS-ARBO prospective observational study in adults (ie, aged ≥18 years) hospitalised with an arbovirus-compatible disease syndrome in 21 hospitals in seven countries in southeast Europe over four arbovirus seasons (May 1-Oct 31, 2016-19) to obtain arbovirus prevalence outcomes. The main objectives of the MERMAIDS-ARBO study, describing the clinical management and outcomes of four arboviruses endemic to southeast Europe, including Crimean-Congo haemorrhagic fever virus (CCHFV), tick-borne encephalitis virus (TBEV), Toscana virus, and West Nile virus (WNV), are reported elsewhere. In this analysis, given the challenges associated with arbovirus diagnostics, we developed a diagnostic algorithm accounting for serology outcomes and sample timing to study arbovirus prevalence in southeast Europe. Serum samples were collected on days 0, 7, 28, and 60 after hospital admission and tested for anti-CCHFV IgG and IgM antibodies with ELISAs (confirmed with an indirect immunofluorescence test) and for IgG and IgM antibodies specific to TBEV, Toscana virus, and WNV with custom-printed protein microarrays (confirmed with virus neutralisation tests). All acute-phase samples were tested by PCR for all four viruses. Descriptive analyses were performed for virus-reactive cases by geography and year, and possible factors (eg, age, sex, and insect bites) associated with virus reactivity were assessed.Of 2896 individuals screened, 913 were eligible for inclusion, of whom 863 (514 men, 332 women, and 17 unknown) had samples sent to the study reference laboratories and were included in molecular and serological analyses. Some individuals had insufficient clinical data to be included in the clinical analysis, but met the eligibility criteria for and were included here. Serum sampling was incomplete (eg, samples missing from one or more timepoints or no data on time since symptom onset) for 602 (70%) patients, and the timing of collection was often heterogeneous after symptom onset up to 40 days (average median delay of 5-6 days across all timepoints), affecting the ability to diagnose arbovirus infection by serology. By use of an interpretation table incorporating timing and completeness of sampling, one (<1%) participant had a confirmed recent infection with CCHFV, ten (1%) with TBEV, 40 (5%) with Toscana virus, and 52 (6%) with WNV. Most acute confirmed infections of Toscana virus were found in Albania (25 [63%] of 40), whereas WNV was primarily identified in Romania (36 [69%] of 52). Albania also had the highest overall Toscana virus seropositivity (168 [60%] of 282), mainly explained by patients confirmed to be exposed or previously exposed (104 [62%] of 168). Patients without antibodies to WNV or Toscana virus were significantly younger than patients with antibodies (mean difference -8·48 years [95% CI -12·31 to -4·64] for WNV, and -6·97 years [-9·59 to -4·35] for Toscana virus). We found higher odds of Toscana virus reactivity in men (odds ratio 1·56 [95% CI 1·15 to 2·11]; p=0·0055), WNV reactivity with mosquito bites versus no mosquito bites (2·47 [1·54 to 3·97]; p=0·0002), and TBEV reactivity with tick bites versus no tick bites (2·21 [1·19 to 4·11]; p=0·018).FINDINGSOf 2896 individuals screened, 913 were eligible for inclusion, of whom 863 (514 men, 332 women, and 17 unknown) had samples sent to the study reference laboratories and were included in molecular and serological analyses. Some individuals had insufficient clinical data to be included in the clinical analysis, but met the eligibility criteria for and were included here. Serum sampling was incomplete (eg, samples missing from one or more timepoints or no data on time since symptom onset) for 602 (70%) patients, and the timing of collection was often heterogeneous after symptom onset up to 40 days (average median delay of 5-6 days across all timepoints), affecting the ability to diagnose arbovirus infection by serology. By use of an interpretation table incorporating timing and completeness of sampling, one (<1%) participant had a confirmed recent infection with CCHFV, ten (1%) with TBEV, 40 (5%) with Toscana virus, and 52 (6%) with WNV. Most acute confirmed infections of Toscana virus were found in Albania (25 [63%] of 40), whereas WNV was primarily identified in Romania (36 [69%] of 52). Albania also had the highest overall Toscana virus seropositivity (168 [60%] of 282), mainly explained by patients confirmed to be exposed or previously exposed (104 [62%] of 168). Patients without antibodies to WNV or Toscana virus were significantly younger than patients with antibodies (mean difference -8·48 years [95% CI -12·31 to -4·64] for WNV, and -6·97 years [-9·59 to -4·35] for Toscana virus). We found higher odds of Toscana virus reactivity in men (odds ratio 1·56 [95% CI 1·15 to 2·11]; p=0·0055), WNV reactivity with mosquito bites versus no mosquito bites (2·47 [1·54 to 3·97]; p=0·0002), and TBEV reactivity with tick bites versus no tick bites (2·21 [1·19 to 4·11]; p=0·018).This study shows that despite incomplete and heterogeneous data, differential diagnosis of suspected arbovirus infections is possible, and the diagnostic interpretation algorithm we propose could potentially be used to strengthen routine diagnostics in clinical settings in areas at risk for arboviral diseases. Our data highlight potential hotspots for arbovirus surveillance and risk factors associated with these particular arbovirus infections.INTERPRETATIONThis study shows that despite incomplete and heterogeneous data, differential diagnosis of suspected arbovirus infections is possible, and the diagnostic interpretation algorithm we propose could potentially be used to strengthen routine diagnostics in clinical settings in areas at risk for arboviral diseases. Our data highlight potential hotspots for arbovirus surveillance and risk factors associated with these particular arbovirus infections.European Commission and Versatile Emerging infectious disease Observatory.FUNDINGEuropean Commission and Versatile Emerging infectious disease Observatory.For the Greek, Albanian, Romanian, Bosnian, Serbian, and Croatian translation of the summary see Supplementary Materials section.TRANSLATIONSFor the Greek, Albanian, Romanian, Bosnian, Serbian, and Croatian translation of the summary see Supplementary Materials section. Summary Background Arboviruses are increasingly affecting Europe, partly due to the effects of climate change. This increase in range and impact emphasises the need to improve preparedness for emerging arboviral infections that often co-circulate and might have overlapping clinical syndromes. We aimed to strengthen surveillance networks for four clinically relevant arboviruses in southeast Europe. Methods This study reports an in-depth analysis of the MERMAIDS-ARBO prospective observational study in adults (ie, aged ≥18 years) hospitalised with an arbovirus-compatible disease syndrome in 21 hospitals in seven countries in southeast Europe over four arbovirus seasons (May 1–Oct 31, 2016–19) to obtain arbovirus prevalence outcomes. The main objectives of the MERMAIDS-ARBO study, describing the clinical management and outcomes of four arboviruses endemic to southeast Europe, including Crimean–Congo haemorrhagic fever virus (CCHFV), tick-borne encephalitis virus (TBEV), Toscana virus, and West Nile virus (WNV), are reported elsewhere. In this analysis, given the challenges associated with arbovirus diagnostics, we developed a diagnostic algorithm accounting for serology outcomes and sample timing to study arbovirus prevalence in southeast Europe. Serum samples were collected on days 0, 7, 28, and 60 after hospital admission and tested for anti-CCHFV IgG and IgM antibodies with ELISAs (confirmed with an indirect immunofluorescence test) and for IgG and IgM antibodies specific to TBEV, Toscana virus, and WNV with custom-printed protein microarrays (confirmed with virus neutralisation tests). All acute-phase samples were tested by PCR for all four viruses. Descriptive analyses were performed for virus-reactive cases by geography and year, and possible factors (eg, age, sex, and insect bites) associated with virus reactivity were assessed. Findings Of 2896 individuals screened, 913 were eligible for inclusion, of whom 863 (514 men, 332 women, and 17 unknown) had samples sent to the study reference laboratories and were included in molecular and serological analyses. Some individuals had insufficient clinical data to be included in the clinical analysis, but met the eligibility criteria for and were included here. Serum sampling was incomplete (eg, samples missing from one or more timepoints or no data on time since symptom onset) for 602 (70%) patients, and the timing of collection was often heterogeneous after symptom onset up to 40 days (average median delay of 5–6 days across all timepoints), affecting the ability to diagnose arbovirus infection by serology. By use of an interpretation table incorporating timing and completeness of sampling, one (<1%) participant had a confirmed recent infection with CCHFV, ten (1%) with TBEV, 40 (5%) with Toscana virus, and 52 (6%) with WNV. Most acute confirmed infections of Toscana virus were found in Albania (25 [63%] of 40), whereas WNV was primarily identified in Romania (36 [69%] of 52). Albania also had the highest overall Toscana virus seropositivity (168 [60%] of 282), mainly explained by patients confirmed to be exposed or previously exposed (104 [62%] of 168). Patients without antibodies to WNV or Toscana virus were significantly younger than patients with antibodies (mean difference –8·48 years [95% CI –12·31 to –4·64] for WNV, and –6·97 years [–9·59 to –4·35] for Toscana virus). We found higher odds of Toscana virus reactivity in men (odds ratio 1·56 [95% CI 1·15 to 2·11]; p=0·0055), WNV reactivity with mosquito bites versus no mosquito bites (2·47 [1·54 to 3·97]; p=0·0002), and TBEV reactivity with tick bites versus no tick bites (2·21 [1·19 to 4·11]; p=0·018). Interpretation This study shows that despite incomplete and heterogeneous data, differential diagnosis of suspected arbovirus infections is possible, and the diagnostic interpretation algorithm we propose could potentially be used to strengthen routine diagnostics in clinical settings in areas at risk for arboviral diseases. Our data highlight potential hotspots for arbovirus surveillance and risk factors associated with these particular arbovirus infections. Funding European Commission and Versatile Emerging infectious disease Observatory. Translations For the Greek, Albanian, Romanian, Bosnian, Serbian, and Croatian translation of the summary see Supplementary Materials section. Arboviruses are increasingly affecting Europe, partly due to the effects of climate change. This increase in range and impact emphasises the need to improve preparedness for emerging arboviral infections that often co-circulate and might have overlapping clinical syndromes. We aimed to strengthen surveillance networks for four clinically relevant arboviruses in southeast Europe. This study reports an in-depth analysis of the MERMAIDS-ARBO prospective observational study in adults (ie, aged ≥18 years) hospitalised with an arbovirus-compatible disease syndrome in 21 hospitals in seven countries in southeast Europe over four arbovirus seasons (May 1–Oct 31, 2016–19) to obtain arbovirus prevalence outcomes. The main objectives of the MERMAIDS-ARBO study, describing the clinical management and outcomes of four arboviruses endemic to southeast Europe, including Crimean–Congo haemorrhagic fever virus (CCHFV), tick-borne encephalitis virus (TBEV), Toscana virus, and West Nile virus (WNV), are reported elsewhere. In this analysis, given the challenges associated with arbovirus diagnostics, we developed a diagnostic algorithm accounting for serology outcomes and sample timing to study arbovirus prevalence in southeast Europe. Serum samples were collected on days 0, 7, 28, and 60 after hospital admission and tested for anti-CCHFV IgG and IgM antibodies with ELISAs (confirmed with an indirect immunofluorescence test) and for IgG and IgM antibodies specific to TBEV, Toscana virus, and WNV with custom-printed protein microarrays (confirmed with virus neutralisation tests). All acute-phase samples were tested by PCR for all four viruses. Descriptive analyses were performed for virus-reactive cases by geography and year, and possible factors (eg, age, sex, and insect bites) associated with virus reactivity were assessed. Of 2896 individuals screened, 913 were eligible for inclusion, of whom 863 (514 men, 332 women, and 17 unknown) had samples sent to the study reference laboratories and were included in molecular and serological analyses. Some individuals had insufficient clinical data to be included in the clinical analysis, but met the eligibility criteria for and were included here. Serum sampling was incomplete (eg, samples missing from one or more timepoints or no data on time since symptom onset) for 602 (70%) patients, and the timing of collection was often heterogeneous after symptom onset up to 40 days (average median delay of 5–6 days across all timepoints), affecting the ability to diagnose arbovirus infection by serology. By use of an interpretation table incorporating timing and completeness of sampling, one (<1%) participant had a confirmed recent infection with CCHFV, ten (1%) with TBEV, 40 (5%) with Toscana virus, and 52 (6%) with WNV. Most acute confirmed infections of Toscana virus were found in Albania (25 [63%] of 40), whereas WNV was primarily identified in Romania (36 [69%] of 52). Albania also had the highest overall Toscana virus seropositivity (168 [60%] of 282), mainly explained by patients confirmed to be exposed or previously exposed (104 [62%] of 168). Patients without antibodies to WNV or Toscana virus were significantly younger than patients with antibodies (mean difference –8·48 years [95% CI –12·31 to –4·64] for WNV, and –6·97 years [–9·59 to –4·35] for Toscana virus). We found higher odds of Toscana virus reactivity in men (odds ratio 1·56 [95% CI 1·15 to 2·11]; p=0·0055), WNV reactivity with mosquito bites versus no mosquito bites (2·47 [1·54 to 3·97]; p=0·0002), and TBEV reactivity with tick bites versus no tick bites (2·21 [1·19 to 4·11]; p=0·018). This study shows that despite incomplete and heterogeneous data, differential diagnosis of suspected arbovirus infections is possible, and the diagnostic interpretation algorithm we propose could potentially be used to strengthen routine diagnostics in clinical settings in areas at risk for arboviral diseases. Our data highlight potential hotspots for arbovirus surveillance and risk factors associated with these particular arbovirus infections. European Commission and Versatile Emerging infectious disease Observatory. For the Greek, Albanian, Romanian, Bosnian, Serbian, and Croatian translation of the summary see Supplementary Materials section. |
| Author | Radić, Ljiljana Betica Biçaku, Albina Ponosheci Chandler, Felicity Jacobs, Kevin Dumitru, Irina M Andrianopoulos, Ioannis Scherbeijn, Sandra Cleton, Natalie Hrisca, Raluca M Lupse, Mihaela Moroti, Ruxandra Kuijstermans, Mandy Markotić, Alemka Kasbergen, Louella M R Birlutiu, Victoria Vrkic, Ivana Kurti, Arsim Tardei, Gratiela Mrdjen, Visnja Goossens, Herman Ledina, Dragan Arapović, Jurica Marincu, Iosif Željka, Mačak Šafranko Hristea, Adriana Chen, Siyu Pandak, Nenad Corman, Victor M Turtle, Lance Baljic, Rusmir Văsieşiu, Anca Meda Raka, Lul Halichidis, Stela Papanikolaou, Metaxia N Charrel, Remi N Loens, Katherine Sigfrid, Louise Codreanu, Daniel Harxhi, Arjan Vasiesiu, Anca Meda Betica Radić, Ljiljana Drosten, Christian Sikkema, Reina S Ieven, Margareta Koshovari, Iris Sulaver, Željana Galal, Ushma Reusken, Chantal Travar, Maja Koulouras, Vasilios Puca, Edmond Ostojić, Maja Melchert, Julia Marija, Santini Denis, Emmanuelle Hookham, Lauren Verhaz, Antonija Chan, Xin Hui S Grbeša, Đurđica Cekinović Wei, Jia Bino, Silvia Barac, Aleksandra Ponoshec |
| Author_xml | – sequence: 1 givenname: Louella M R surname: Kasbergen fullname: Kasbergen, Louella M R email: l.kasbergen@erasmusmc.nl organization: Department of Viroscience, Erasmus University Medical Center, Rotterdam, Netherlands – sequence: 2 givenname: Erwin surname: de Bruin fullname: de Bruin, Erwin organization: Department of Viroscience, Erasmus University Medical Center, Rotterdam, Netherlands – sequence: 3 givenname: Felicity surname: Chandler fullname: Chandler, Felicity organization: Department of Viroscience, Erasmus University Medical Center, Rotterdam, Netherlands – sequence: 4 givenname: Louise surname: Sigfrid fullname: Sigfrid, Louise organization: ERGO, Pandemic Sciences Institute, University of Oxford, Oxford, UK – sequence: 5 givenname: Xin Hui S surname: Chan fullname: Chan, Xin Hui S organization: Nuffield Department of Medicine, University of Oxford, Oxford, UK – sequence: 6 givenname: Lauren surname: Hookham fullname: Hookham, Lauren organization: Nuffield Department of Medicine, University of Oxford, Oxford, UK – sequence: 7 givenname: Jia surname: Wei fullname: Wei, Jia organization: Nuffield Department of Medicine, University of Oxford, Oxford, UK – sequence: 8 givenname: Siyu surname: Chen fullname: Chen, Siyu organization: Nuffield Department of Medicine, University of Oxford, Oxford, UK – sequence: 11 givenname: Remi N surname: Charrel fullname: Charrel, Remi N organization: Unite des Virus Emergents, Aix-Marseille Université, Universita di Corsica, IRD 190, Inserm 1207, IRBA, Marseille, France – sequence: 14 givenname: Victor M surname: Corman fullname: Corman, Victor M organization: Institute of Virology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany – sequence: 15 givenname: Chantal surname: Reusken fullname: Reusken, Chantal organization: Department of Viroscience, Erasmus University Medical Center, Rotterdam, Netherlands – sequence: 16 givenname: Katherine surname: Loens fullname: Loens, Katherine organization: Department of Medical Microbiology, University of Antwerp UIA, Antwerp, Belgium – sequence: 17 givenname: Corneliu Petru surname: Popescu fullname: Popescu, Corneliu Petru organization: Carol Davila University of Medicine and Pharmacy, Bucharest, Romania – sequence: 18 givenname: Mihaela surname: Lupse fullname: Lupse, Mihaela organization: Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania – sequence: 19 givenname: Violeta surname: Briciu fullname: Briciu, Violeta organization: Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania – sequence: 20 givenname: Anca Meda surname: Văsieşiu fullname: Văsieşiu, Anca Meda organization: Department of Infectious Diseases, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Târgu Mureş, Târgu Mureş, Romania – sequence: 22 givenname: Arjan surname: Harxhi fullname: Harxhi, Arjan organization: Faculty of Medicine, Medical University of Tirana, Tirana, Albania – sequence: 23 givenname: Edmond surname: Puca fullname: Puca, Edmond organization: Department of Infectious Diseases, Mother Teresa University Hospital Center, Tirana, Albania – sequence: 25 givenname: Maja surname: Travar fullname: Travar, Maja organization: Department of Microbiology, Faculty of Medicine, University of Banja Luka, Banja Luka, Bosnia and Herzegovina – sequence: 26 givenname: Maja surname: Ostojić fullname: Ostojić, Maja organization: School of Medicine, University of Mostar, Mostar, Bosnia and Herzegovina – sequence: 27 givenname: Rusmir surname: Baljic fullname: Baljic, Rusmir organization: Unit for Infectious Disease, Clinical Center of the University of Sarajevo, Sarajevo, Bosnia and Herzegovina – sequence: 28 givenname: Jurica surname: Arapović fullname: Arapović, Jurica organization: School of Medicine, University of Mostar, Mostar, Bosnia and Herzegovina – sequence: 29 givenname: Dragan surname: Ledina fullname: Ledina, Dragan organization: Department of Infectious Diseases, University Hospital Split, Split, Croatia – sequence: 30 givenname: Đurđica surname: Cekinović Grbeša fullname: Cekinović Grbeša, Đurđica organization: Clinic for Infectious Diseases, Clinical Hospital Center Rijeka, Rijeka, Croatia – sequence: 31 givenname: Ivica surname: Čabraja fullname: Čabraja, Ivica organization: Department of Infectious Diseases, Dr Josip Benčević General Hospital, Slavonski Brod, Croatia – sequence: 32 givenname: Ivan-Christian surname: Kurolt fullname: Kurolt, Ivan-Christian organization: Dr Fran Mihaljević University Hospital for Infectious Diseases, Zagreb, Croatia – sequence: 33 givenname: Stela surname: Halichidis fullname: Halichidis, Stela organization: Clinical Infectious Diseases Hospital, Constanța, Romania – sequence: 34 givenname: Victoria surname: Birlutiu fullname: Birlutiu, Victoria organization: Faculty of Medicine, Lucian Blaga University of Sibiu, Sibiu, Romania – sequence: 35 givenname: Irina M surname: Dumitru fullname: Dumitru, Irina M organization: Ovidius University of Constanța, Clinical Hospital of Infectious Diseases, Academy of Romanian Scientists, Bucharest, Romania – sequence: 36 givenname: Ruxandra surname: Moroti fullname: Moroti, Ruxandra organization: Carol Davila University of Medicine and Pharmacy, Bucharest, Romania – sequence: 37 givenname: Aleksandra surname: Barac fullname: Barac, Aleksandra organization: Clinic for Infectious and Tropical Diseases, University Clinical Center of Serbia, Belgrade, Serbia – sequence: 39 givenname: Athina surname: Pyrpasopoulou fullname: Pyrpasopoulou, Athina organization: Infectious Diseases Unit, Hippokration General Hospital, Thessaloniki, Greece – sequence: 40 givenname: Vasilios surname: Koulouras fullname: Koulouras, Vasilios organization: Intensive Care Unit, University Hospital of Ioannina, University of Ioannina, Ioannina, Greece – sequence: 42 givenname: Metaxia N surname: Papanikolaou fullname: Papanikolaou, Metaxia N organization: Intensive Care Unit, Ippokrateion Athens General Hospital, Athens, Greece – sequence: 43 givenname: Emmanuel surname: Roilides fullname: Roilides, Emmanuel organization: Infectious Diseases Unit, Hippokration General Hospital, Thessaloniki, Greece – sequence: 44 givenname: Alemka surname: Markotić fullname: Markotić, Alemka organization: Dr Fran Mihaljević University Hospital for Infectious Diseases, Zagreb, Croatia – sequence: 45 givenname: Ushma surname: Galal fullname: Galal, Ushma organization: Nuffield Department of Primary Care Health Sciences, Clinical Trials Unit, University of Oxford, Oxford, UK – sequence: 47 givenname: Lynsey surname: Goodwin fullname: Goodwin, Lynsey organization: NIHR Health Protection Research Unit for Emerging Zoonotic Infections, University of Liverpool, Liverpool, UK – sequence: 48 givenname: Lance surname: Turtle fullname: Turtle, Lance organization: NIHR Health Protection Research Unit for Emerging Zoonotic Infections, University of Liverpool, Liverpool, UK – sequence: 50 givenname: Hamdi surname: Ramadani fullname: Ramadani, Hamdi organization: Clinic of Infectious Diseases, University Clinical Center of Kosovo, Prishtina, Kosovo – sequence: 52 givenname: Margareta surname: Ieven fullname: Ieven, Margareta organization: Department of Medical Microbiology, University of Antwerp UIA, Antwerp, Belgium – sequence: 53 givenname: Christian surname: Drosten fullname: Drosten, Christian organization: Institute of Virology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany – sequence: 54 givenname: Peter W surname: Horby fullname: Horby, Peter W organization: ERGO, Pandemic Sciences Institute, University of Oxford, Oxford, UK – sequence: 55 givenname: Reina S surname: Sikkema fullname: Sikkema, Reina S organization: Department of Viroscience, Erasmus 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| Copyright | 2025 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license Copyright © 2025 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Published by Elsevier Ltd.. All rights reserved. 2025. The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. This work is published under https://creativecommons.org/licenses/by/3.0/ (theLicense”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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