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    Fatal Zika virus disease in adults: A critical reappraisal of an under-recognized clinical entity
    (Elsevier BV, 2019) Alfonso J. Rodríguez‐Morales; Eduardo Ramírez-Vallejo; Lucia Elena Alvarado-Arnez; Alberto Paniz‐Mondolfi; Lysien I. Zambrano; Albert I. Ko
    Zika virus (ZIKV) is a flavivirus that was most likely introduced into Latin America back in 2013 (Rodriguez-Morales, 2015Rodriguez-Morales A.J. Zika: the new arbovirus threat for Latin America.J Infect Dev Ctries. 2015; 9: 684-685Crossref PubMed Scopus (99) Google Scholar), but did not cause identifiable outbreaks until its massive emergence in Brazil in 2015, when it rapidly spread across the Americas and the Caribbean (Weaver et al., 2016Weaver S.C. Costa F. Garcia-Blanco M.A. Ko A.I. Ribeiro G.S. Saade G. et al.Zika virus: history, emergence, biology, and prospects for control.Antiviral Res. 2016; 130: 69-80Crossref PubMed Scopus (474) Google Scholar). The World Health Organization (WHO) declared the ZIKV epidemic a public health emergency of international concern (PHEC) at the height of the pandemic in 2016 (Rodriguez-Morales, 2015Rodriguez-Morales A.J. Zika: the new arbovirus threat for Latin America.J Infect Dev Ctries. 2015; 9: 684-685Crossref PubMed Scopus (99) Google Scholar, Rodriguez-Morales, 2018Rodriguez-Morales A.J. Severe, atypical and fatal cases of Zika virus infection: experience in Colombia.Int J Infect Dis. 2018; 73: 71Abstract Full Text Full Text PDF Google Scholar), after identifying clusters of ZIKV-associated Guillain–Barré syndrome (GBS) (do Rosario et al., 2016do Rosario M.S. de Jesus P.A. Vasilakis N. Farias D.S. Novaes M.A. Rodrigues S.G. et al.Guillain–Barre syndrome after Zika virus infection in Brazil.Am J Trop Med Hyg. 2016; 95: 1157-1160Crossref PubMed Scopus (77) Google Scholar), and more significantly due to its association with outbreaks of microcephaly among newborn infants in which a causal link between ZIKV infection and birth defects was reliably demonstrated (Rasmussen et al., 2016Rasmussen S.A. Jamieson D.J. Honein M.A. Petersen L.R. Zika virus and birth defects—reviewing the evidence for causality.N Engl J Med. 2016; 374: 1981-1987Crossref PubMed Scopus (1336) Google Scholar). The clinical manifestations of congenital ZIKV infection extend beyond microcephaly and comprise a distinct constellation of birth defects and manifestations known as the congenital Zika syndrome (CZS) (Nogueira et al., 2018Nogueira M.L. Nery Junior, N.R.R. Estofolete C.F. Bernardes Terzian A.C. Guimaraes G.F. Zini N. et al.Adverse birth outcomes associated with Zika virus exposure during pregnancy in Sao Jose do Rio Preto, Brazil.Clin Microbiol Infect. 2018; 24: 646-652Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, Moore et al., 2017Moore C.A. Staples J.E. Dobyns W.B. Pessoa A. Ventura C.V. Fonseca E.B. et al.Characterizing the pattern of anomalies in congenital Zika syndrome for pediatric clinicians.JAMA Pediatr. 2017; 171: 288-295Crossref PubMed Scopus (578) Google Scholar). The ZIKV pandemic in the Americas and Caribbean was known to cause over one million cases and there were reports in which the virus was found to cause severe, life-threatening complications in addition to GBS and CZS, especially among patients with associated comorbidities (Rodriguez-Morales, 2018Rodriguez-Morales A.J. Severe, atypical and fatal cases of Zika virus infection: experience in Colombia.Int J Infect Dis. 2018; 73: 71Abstract Full Text Full Text PDF Google Scholar). From a clinical standpoint, until 2013, ZIKV was generally considered to cause a mild, self-limiting illness, which did not pose a serious public health threat (Rodriguez-Morales, 2015Rodriguez-Morales A.J. Zika: the new arbovirus threat for Latin America.J Infect Dev Ctries. 2015; 9: 684-685Crossref PubMed Scopus (99) Google Scholar, Rodriguez-Morales, 2018Rodriguez-Morales A.J. Severe, atypical and fatal cases of Zika virus infection: experience in Colombia.Int J Infect Dis. 2018; 73: 71Abstract Full Text Full Text PDF Google Scholar, Martinez-Pulgarin et al., 2016Martinez-Pulgarin D.F. Acevedo-Mendoza W.F. Cardona-Ospina J.A. Rodriguez-Morales A.J. Paniz-Mondolfi A.E. A bibliometric analysis of global Zika research.Travel Med Infect Dis. 2016; 14: 55-57Crossref PubMed Scopus (56) Google Scholar). However, it was not until the first non-perinatal death was identified in a 15-year-old girl from northern Colombia in October 2015, (Arzuza-Ortega et al., 2016Arzuza-Ortega L. Polo A. Perez-Tatis G. Lopez-Garcia H. Parra E. Pardo-Herrera L.C. et al.Fatal sickle cell disease and Zika virus infection in girl from colombia.Emerg Infect Dis. 2016; 22: 925-927Crossref PubMed Scopus (76) Google Scholar) that an increasing number of ZIKV-associated fatalities were reported in the literature. The case from Malaysia reported by Rajahram et al., 2019Rajahram G.S. Hale G. Bhatnagar J. Hiu J. Thayan R. William T. et al.Postmortem evidence of disseminated Zika virus infection in an adult patient.Int J Infect Dis. 2019; https://doi.org/10.1016/j.ijid.2019.01.047Abstract Full Text Full Text PDF Scopus (5) Google Scholar in the current issue of the International Journal of Infectious Diseases, confirms that ZIKV infection can result in atypical disease and lead to severe and even fatal outcomes (Rodriguez-Morales, 2018Rodriguez-Morales A.J. Severe, atypical and fatal cases of Zika virus infection: experience in Colombia.Int J Infect Dis. 2018; 73: 71Abstract Full Text Full Text PDF Google Scholar). It also demonstrates, as seen in other studies (Sarmiento-Ospina et al., 2016Sarmiento-Ospina A. Vasquez-Serna H. Jimenez-Canizales C.E. Villamil-Gomez W.E. Rodriguez-Morales A.J. Zika virus associated deaths in Colombia.Lancet Infect Dis. 2016; 16: 523-524Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar, Soares et al., 2016Soares C.N. Brasil P. Carrera R.M. Sequeira P. de Filippis A.B. Borges V.A. et al.Fatal encephalitis associated with Zika virus infection in an adult.J Clin Virol. 2016; 83: 63-65Crossref PubMed Scopus (93) Google Scholar, Zonneveld et al., 2016Zonneveld R. Roosblad J. Staveren J.W. Wilschut J.C. Vreden S.G. Codrington J. Three atypical lethal cases associated with acute Zika virus infection in Suriname.IDCases. 2016; 5: 49-53Crossref PubMed Scopus (19) Google Scholar, Azevedo et al., 2016Azevedo R.S. Araujo M.T. Martins Filho A.J. Oliveira C.S. Nunes B.T. Cruz A.C. et al.Zika virus epidemic in Brazil. I. Fatal disease in adults: clinical and laboratorial aspects.J Clin Virol. 2016; 85: 56-64Crossref PubMed Scopus (58) Google Scholar), that this neurotropic virus can disseminate to multiple organs and tissues, in addition to the central nervous system, while inflicting pathological effects. Previous to this report, the majority of fatalities associated with ZIKV infection were almost invariably linked to acute neurological complications (Sarmiento-Ospina et al., 2016Sarmiento-Ospina A. Vasquez-Serna H. Jimenez-Canizales C.E. Villamil-Gomez W.E. Rodriguez-Morales A.J. Zika virus associated deaths in Colombia.Lancet Infect Dis. 2016; 16: 523-524Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar, Soares et al., 2016Soares C.N. Brasil P. Carrera R.M. Sequeira P. de Filippis A.B. Borges V.A. et al.Fatal encephalitis associated with Zika virus infection in an adult.J Clin Virol. 2016; 83: 63-65Crossref PubMed Scopus (93) Google Scholar, Azevedo et al., 2016Azevedo R.S. Araujo M.T. Martins Filho A.J. Oliveira C.S. Nunes B.T. Cruz A.C. et al.Zika virus epidemic in Brazil. I. Fatal disease in adults: clinical and laboratorial aspects.J Clin Virol. 2016; 85: 56-64Crossref PubMed Scopus (58) Google Scholar). However, amongst those exceptional fatalities without neurological involvement, the question was raised as to whether ZIKV could cause renal and cardiac involvement, as was observed on autopsy examinations of the case described in this issue. Renal and cardiac complications have been reported in atypical, severe (Villamil-Gomez et al., 2016aVillamil-Gomez W.E. Ramirez-Vallejo E. Cardona-Ospina J.A. Silvera L.A. Rodriguez-Morales A.J. Electrocardiographic alterations in patients with chikungunya fever from Sucre, Colombia: a 42-case series.Travel Med Infect Dis. 2016; 14: 510-512Crossref PubMed Scopus (12) Google Scholar, Alvarez et al., 2017Alvarez M.F. Bolivar-Mejia A. Rodriguez-Morales A.J. Ramirez-Vallejo E. Cardiovascular involvement and manifestations of systemic Chikungunya virus infection: a systematic review.F1000Res. 2017; 6: 390Crossref PubMed Scopus (40) Google Scholar), and fatal cases (Hoz et al., 2015Hoz J.M. Bayona B. Viloria S. Accini J.L. Juan-Vergara H.S. Viasus D. Fatal cases of Chikungunya virus infection in Colombia: diagnostic and treatment challenges.J Clin Virol. 2015; 69: 27-29Crossref PubMed Scopus (49) Google Scholar, Mercado et al., 2018Mercado M. Acosta-Reyes J. Parra E. Guzman L. Beltran M. Gasque P. et al.Renal involvement in fatal cases of Chikungunya virus infection.J Clin Virol. 2018; 103: 16-18Crossref PubMed Scopus (25) Google Scholar) of chikungunya virus (CHIKV) infection. Conversely, cases of ZIKV infection with documented renal or cardiac complications have been reported on rarely and have usually lacked detailed histopathological evaluation as well as molecular confirmation of the presence of viral RNA within the renal or cardiac tissues during routine autopsy of fatal cases (Mercado-Reyes et al., 2019Mercado-Reyes M. Acosta-Reyes J. Navarro-Lechuga E. Corchuelo S. Rico A. Parra E. et al.Dengue, Chikungunya and Zika virus coinfection: results of the national surveillance during the Zika epidemic in Colombia.Epidemiol Infect. 2019; 147: e77Crossref PubMed Scopus (43) Google Scholar). ZIKV infection has previously been reported to cause cardiovascular compromise as a consequence of systemic infection, as revealed by electrocardiographic and echocardiographic alterations (Villamil-Gomez et al., 2018Villamil-Gomez W.E. Ramirez-Vallejo E. Rodriguez-Morales A.J. Cardiac compromise in Zika virus infection.Mayo Clin Proc. 2018; 93: 393-394Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar, Schwartzmann et al., 2017Schwartzmann P.V. Ramalho L.N. Neder L. Vilar F.C. Ayub-Ferreira S.M. Romeiro M.F. et al.Zika virus meningoencephalitis in an immunocompromised patient.Mayo Clin Proc. 2017; 92: 460-466Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar), even including venous thromboembolism (in ZIKV and CHIKV infections) (Ramacciotti et al., 2019Ramacciotti E. Agati L.B. Aguiar V.C.R. Wolosker N. Guerra J.C. de Almeida R.P. et al.Zika and Chikungunya virus and risk for venous thromboembolism.Clin Appl Thromb Hemost. 2019; 25Crossref Scopus (37) Google Scholar), as well as demonstrating myocardial inflammation secondary to viral infection (Villamil-Gomez et al., 2018Villamil-Gomez W.E. Ramirez-Vallejo E. Rodriguez-Morales A.J. Cardiac compromise in Zika virus infection.Mayo Clin Proc. 2018; 93: 393-394Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar). Autopsy examinations of a heart transplant recipient who developed ZIKV infection revealed plasma cell infiltrates in the myocardial tissue, along with perivascular and endovascular damage (Schwartzmann et al., 2017Schwartzmann P.V. Ramalho L.N. Neder L. Vilar F.C. Ayub-Ferreira S.M. Romeiro M.F. et al.Zika virus meningoencephalitis in an immunocompromised patient.Mayo Clin Proc. 2017; 92: 460-466Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar). Nevertheless, publications in the literature on cardiovascular manifestations in adult patients with ZIKV infection are scarce, and the case report by Rajahram et al., 2019Rajahram G.S. Hale G. Bhatnagar J. Hiu J. Thayan R. William T. et al.Postmortem evidence of disseminated Zika virus infection in an adult patient.Int J Infect Dis. 2019; https://doi.org/10.1016/j.ijid.2019.01.047Abstract Full Text Full Text PDF Scopus (5) Google Scholar is timely in underscoring how this arboviral infection can produce unexpected clinical complications with renal and cardiovascular involvement. Previous reports have suggested an association between cardiovascular complications and ZIKV during the acute phase of the infection (Villamil-Gomez et al., 2018Villamil-Gomez W.E. Ramirez-Vallejo E. Rodriguez-Morales A.J. Cardiac compromise in Zika virus infection.Mayo Clin Proc. 2018; 93: 393-394Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar, Li et al., 2016Li X.F. Dong H.L. Huang X.Y. Qiu Y.F. Wang H.J. Deng Y.Q. et al.Characterization of a 2016 clinical isolate of Zika virus in non-human primates.EBioMedicine. 2016; : 170-177Google Scholar, Minhas et al., 2017Minhas A.M. Nayab A. Iyer S. Narmeen M. Fatima K. Khan M.S. et al.Association of Zika virus with myocarditis, heart failure, and arrhythmias: a literature review.Cureus. 2017; 9: e1399PubMed Google Scholar). However, only a limited number of studies have addressed this potential association (Martinez-Pulgarin et al., 2016Martinez-Pulgarin D.F. Acevedo-Mendoza W.F. Cardona-Ospina J.A. Rodriguez-Morales A.J. Paniz-Mondolfi A.E. A bibliometric analysis of global Zika research.Travel Med Infect Dis. 2016; 14: 55-57Crossref PubMed Scopus (56) Google Scholar, Minhas et al., 2017Minhas A.M. Nayab A. Iyer S. Narmeen M. Fatima K. Khan M.S. et al.Association of Zika virus with myocarditis, heart failure, and arrhythmias: a literature review.Cureus. 2017; 9: e1399PubMed Google Scholar). Findings in patients (Abdalla et al., 2018Abdalla L.F. Santos J.H.A. Barreto R.T.J. Souza E.M.E. D'Assuncao F.F. Borges M.A. et al.Atrial fibrillation in a patient with Zika virus infection.Virol J. 2018; 15: 23Crossref PubMed Scopus (15) Google Scholar) and non-human primates (Li et al., 2016Li X.F. Dong H.L. Huang X.Y. Qiu Y.F. Wang H.J. Deng Y.Q. et al.Characterization of a 2016 clinical isolate of Zika virus in non-human primates.EBioMedicine. 2016; : 170-177Google Scholar) have provided evidence that ZIKV has a broad tissue tropism, which includes renal and heart tissues (Rajahram et al., 2019Rajahram G.S. Hale G. Bhatnagar J. Hiu J. Thayan R. William T. et al.Postmortem evidence of disseminated Zika virus infection in an adult patient.Int J Infect Dis. 2019; https://doi.org/10.1016/j.ijid.2019.01.047Abstract Full Text Full Text PDF Scopus (5) Google Scholar, Li et al., 2016Li X.F. Dong H.L. Huang X.Y. Qiu Y.F. Wang H.J. Deng Y.Q. et al.Characterization of a 2016 clinical isolate of Zika virus in non-human primates.EBioMedicine. 2016; : 170-177Google Scholar). Nevertheless, further investigations are needed in order to delineate the underlying pathogenic processes in which ZIKV affects myocardial tissue and to characterize the spectrum of cardiovascular manifestations caused by this emerging arboviral infection (Musso et al., 2018Musso D. Rodriguez-Morales A.J. Levi J.E. Cao-Lormeau V.M. Gubler D.J. Unexpected outbreaks of arbovirus infections: lessons learned from the Pacific and tropical America.Lancet Infect Dis. 2018; 18: e355-e361Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar). A review of the literature identified a total of 84 fatal cases of ZIKV infection during the recent pandemic in the Americas (Rodriguez-Morales et al., 2018Rodriguez-Morales A.J. Acevedo-Mendoza W.F. Nasner-Posso K.M. Martínez-Pulgarín D.F. Restrepo-López A. Cardona-Ospina J.A. Postnatal acquired fatal Zika virus infection in the Americas: a systematic review.Int J Infect Dis. 2018; 73: 195Abstract Full Text Full Text PDF Google Scholar). However, few of these reported cases underwent an in-depth tissue assessment and molecular characterization during autopsy, as was performed in the case report by Rajahram et al., 2019Rajahram G.S. Hale G. Bhatnagar J. Hiu J. Thayan R. William T. et al.Postmortem evidence of disseminated Zika virus infection in an adult patient.Int J Infect Dis. 2019; https://doi.org/10.1016/j.ijid.2019.01.047Abstract Full Text Full Text PDF Scopus (5) Google Scholar. It should be emphasized that the pathogenesis of severe ZIKV infection remains poorly understood. In vitro and experimental animal models have provided evidence that antibody-dependent enhancement (ADE) may play a role, but clinical correlates for this phenomenon still need to be confirmed in human ZIKV infection (Ngono and Shresta, 2018Ngono A.E. Shresta S. Immune response to dengue and Zika.Annu Rev Immunol. 2018; 36: 279-308Crossref PubMed Scopus (128) Google Scholar, Andrade et al., 2019Andrade P. Gimblet-Ochieng C. Modirian F. Collins M. Cardenas M. Katzelnick L.C. et al.Impact of pre-existing dengue immunity on human antibody and memory B cell responses to Zika.Nat Commun. 2019; 10: 938Crossref PubMed Scopus (31) Google Scholar). Recent studies suggested that preexisting high antibody titers to dengue virus were associated with a reduced risk of acquiring ZIKV infection and disease. In this sense, the landscape of ZIKV immunity that now exists may affect the risks of future transmission (Rodriguez-Barraquer et al., 2019Rodriguez-Barraquer I. Costa F. Nascimento E.J.M. Nery N.J. Castanha P.M.S. Sacramento G.A. et al.Impact of preexisting dengue immunity on Zika virus emergence in a dengue endemic region.Science. 2019; 363: 607-610Crossref PubMed Scopus (155) Google Scholar). Additionally, cases with arboviral co-infections/co-detection (dengue and chikungunya) have been reported in Colombia and Brazil (Villamil-Gomez et al., 2016bVillamil-Gomez W.E. Rodriguez-Morales A.J. Uribe-Garcia A.M. Gonzalez-Arismendy E. Castellanos J.E. Calvo E.P. et al.Zika, dengue, and chikungunya co-infection in a pregnant woman from Colombia.Int J Infect Dis. 2016; 51: 135-138Abstract Full Text Full Text PDF PubMed Scopus (79) Google Scholar, Sardi et al., 2016Sardi S.I. Somasekar S. Naccache S.N. Bandeira A.C. Tauro L.B. Campos G.S. et al.Coinfections of Zika and Chikungunya viruses in Bahia, Brazil, identified by metagenomic next-generation sequencing.J Clin Microbiol. 2016; 54: 2348-2353Crossref PubMed Scopus (89) Google Scholar), as well as concurrent infections with other microorganisms such as Leptospira (Neaterour et al., 2017Neaterour P. Rivera A. Galloway R.L. Negron M.G. Rivera-Garcia B. Sharp T.M. Fatal Leptospira spp./Zika virus coinfection-Puerto Rico, 2016.Am J Trop Med Hyg. 2017; 97: 1085-1087Google Scholar) and co-infections with other arboviruses (Mercado-Reyes et al., 2019Mercado-Reyes M. Acosta-Reyes J. Navarro-Lechuga E. Corchuelo S. Rico A. Parra E. et al.Dengue, Chikungunya and Zika virus coinfection: results of the national surveillance during the Zika epidemic in Colombia.Epidemiol Infect. 2019; 147: e77Crossref PubMed Scopus (43) Google Scholar). Co-circulation with other arboviruses and ADE pose a challenge for physicians and public health authorities, given the potential to confound and delay diagnosis and possibly influence poorer outcomes in patients with previous exposure to other flaviviruses (Ngono and Shresta, 2018Ngono A.E. Shresta S. Immune response to dengue and Zika.Annu Rev Immunol. 2018; 36: 279-308Crossref PubMed Scopus (128) Google Scholar). As a result, multiple research networks on ZIKV and arboviruses in general have been established, which can leverage protocols, methodologies, and multidisciplinary approaches to inform treatment, prevention, and control strategies. Although recent advances have greatly contributed to our understanding of ZIKV pathogenesis, systemic involvement and the expanding tissue tropism of this virus and its potential relationship to different lineages highlight important aspects for future investigation. Finally, it is worth considering the setting for vaccine development and preparedness for other emerging arboviruses in Latin America and the Asia-Pacific region, such as Ross River, Mayaro, Oropouche, Madariaga, West Nile, and the Venezuelan equine encephalitis and Eastern equine encephalitis viruses. None. All authors report no potential conflicts. All authors have submitted the ICMJE Disclosure Form for Potential Conflicts of Interest. AJRM conceived the idea of the Editorial and performed a review of the literature on the related topic. All authors read the case that is being editorialized. AJRM developed the first draft of the manuscript. All authors consequently contributed to revisions. All authors approved the final version submitted. This article was presented in part at the 18th International Congress of Infectious Diseases (18th ICID) and the XVIII Congress of the Argentine Society for Infectious Diseases (SADI), Buenos Aires, Argentina, March 1–4, 2018 (Conference of A.J. Rodriguez-Morales at Session 48: Zika: Regional Experiences in Neurological Diseases and Severe Cases). The Faculty of Health Sciences of the Universidad Tecnológica de Pereira, the Colombian Association of Infectious Diseases (ACIN) (Coffee-Triangle Region chapter), and the International Society for Infectious Disease (ISID) supported A.J. Rodriguez-Morales in his participation at the ICID/SADI meetings where this article was initially presented.
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    Guillain–Barré syndrome associated with Zika virus infection in Honduras, 2016–2017
    (Elsevier BV, 2019) Lysien I. Zambrano; Itzel Carolina Fuentes-Barahona; Ramon Jeremías Soto-Fernández; Concepción Zúñiga; José Cláudio da Silva; Alfonso J. Rodríguez‐Morales
    Despite the enormous magnitude of Zika virus (ZIKV) infection epidemics in the Americas (Musso et al., 2018Musso D. Rodriguez-Morales A.J. Levi J.E. Cao-Lormeau V.M. Gubler D.J. Unexpected outbreaks of arbovirus infections: lessons learned from the Pacific and tropical America.Lancet Infect Dis. 2018; 18: e355-e361Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar), studies describing its many consequences, such as congenital Zika syndrome (CZS) (Alvarado-Socarras et al., 2018Alvarado-Socarras J.L. Idrovo A.J. Contreras-Garcia G.A. Rodriguez-Morales A.J. Audcent T.A. Mogollon-Mendoza A.C. et al.Congenital microcephaly: a diagnostic challenge during Zika epidemics.Travel Med Infect Dis. 2018; 23: 14-20Crossref PubMed Scopus (23) Google Scholar) and Guillain–Barré syndrome (GBS) (Villamil-Gomez et al., 2017Villamil-Gomez W.E. Sanchez-Herrera A.R. Hernandez H. Hernandez-Iriarte J. Diaz-Ricardo K. Castellanos J. et al.Guillain-Barre syndrome during the Zika virus outbreak in Sucre, Colombia, 2016.Travel Med Infect Dis. 2017; 16: 62-63Crossref PubMed Scopus (20) Google Scholar), are lacking for many countries across the region. This mainly concerns reports from the countries of Central America, such as Honduras. Honduras was affected by a ZIKV epidemic during the years 2016–2017 (Zambrano et al., 2019Zambrano L.I. Vasquez-Bonilla W.O. Fuentes-Barahona I.C. Claudio da Silva J. Valle-Reconco J.A. Medina M.T. et al.Spatial distribution of Zika in Honduras during 2016-2017 using geographic information systems (GIS) — implications for public health and travel medicine.Travel Med Infect Dis. 2019; Crossref Scopus (7) Google Scholar). This study was performed to assess the clinical profiles and the frequency of GBS associated with ZIKV during the outbreak in Honduras in 2016–2017. A retrospective observational study was performed. Data from patients who met the diagnostic criteria for GBS, according to the Brighton Collaboration (levels 1 or 2), with recent ZIKV infection and screening for other etiologies of GBS, were retrieved and recorded. Cases of ZIKV were clinically and laboratory-confirmed (RT-PCR). A total of 108 cases of GBS were studied. During the same period, 32 607 cases of ZIKV (0.3% of them) diagnosed by clinical surveillance and 326 confirmed by RT-PCR (33.1% of them) occurred. The mean age of the patients was 34.9 years and 58.9% were male. These patients were from the capital area, Francisco Morazán Province (35.2%), Choluteca (11.1%), and Comayagua (11.11%), among other areas of the country. Electrophysiological tests were consistent with the primary demyelinating form of the disease. Of the total patients, 10.2% were positive for dengue virus (DENV), chikungunya virus (CHIKV), or ZIKV (Table 1), including six (5.6%) cases due to ZIKV infection and one (0.9%) due to ZIKV–DENV co-infection, among other etiologies (Table 1). Among those with ZIKV GBS, the mean age of the patients was 35.4 years and 67% were male. These ZIKV patients presented fever and rash among other clinical manifestations (Table 1).Table 1Clinical characteristics of patients with GBS, Honduras, 2016–2017.VariablesMeanSD Age (years)34.3523.2 Delay between symptoms and diagnosis (days)4.382.72 Mean time in the ICU (days)14.513.06Number% Male6458.9 EtiologyZIKV RT-PCR-positive65.6ZIKV/DENV RT-PCR-positive10.9CHIKV RT-PCR-positive10.9DENV IgM-positive (RT-PCR-negative)10.9CHIKV IgM-positive (RT-PCR-negative)10.9ZIKV/DENV/CHIKV RT-PCR-negative/IgM-negative9789.8 Clinical manifestations of ZIKV RT-PCR-positive patients (n = 6)Fever3/6Paresthesia3/6Rash2/6Asthenia1/6Myalgia1/6CHIKV, chikungunya virus; DENV, dengue virus; GBS, Guillain–Barré syndrome; ICU, intensive care unit; IgM, immunoglobulin M; RT-PCR, reverse transcriptase polymerase chain reaction test; SD, standard deviation; ZIKV, Zika virus. Open table in a new tab CHIKV, chikungunya virus; DENV, dengue virus; GBS, Guillain–Barré syndrome; ICU, intensive care unit; IgM, immunoglobulin M; RT-PCR, reverse transcriptase polymerase chain reaction test; SD, standard deviation; ZIKV, Zika virus. The delay between symptom onset and diagnosis was a mean of 4.38 ± 2.72 days; the mean time in the ICU was 14.5 ± 13.06 days (Table 1). Treatment comprised intravenous immunoglobulin (IVIG) in all patients. Twenty-four patients required intubation and assisted ventilation (22.2%). Eleven fatal cases occurred (case fatality rate 10%). The remaining cases had made a satisfactory recovery at the 1-year follow-up. Since 2017, cases of ZIKV have been seen sporadically in Honduras, as well as associated GBS cases. Previous ecological analyses in the Americas, including data from Honduras, have found that ZIKV (Dos Santos et al., 2016Dos Santos T. Rodriguez A. Almiron M. Sanhueza A. Ramon P. de Oliveira W.K. et al.Zika Virus and the Guillain-Barre Syndrome — case series from seven countries.N Engl J Med. 2016; 375: 1598-1601Crossref PubMed Scopus (231) Google Scholar), in addition to other arboviruses (Villamil-Gomez et al., 2016Villamil-Gomez W. Silvera L.A. Paez-Castellanos J. Rodriguez-Morales A.J. Guillain-Barre syndrome after Chikungunya infection: a case in Colombia.Enferm Infecc Microbiol Clin. 2016; 34: 140-141Crossref PubMed Scopus (17) Google Scholar), is associated with GBS. Although ZIKV infection is usually benign, the clinical evolution can even be fatal in non-GBS cases (Arzuza-Ortega et al., 2016Arzuza-Ortega L. Polo A. Perez-Tatis G. Lopez-Garcia H. Parra E. Pardo-Herrera L.C. et al.Fatal sickle cell disease and Zika virus infection in girl from Colombia.Emerg Infect Dis. 2016; 22: 925-927Crossref PubMed Scopus (76) Google Scholar, Sarmiento-Ospina et al., 2016Sarmiento-Ospina A. Vasquez-Serna H. Jimenez-Canizales C.E. Villamil-Gomez W.E. Rodriguez-Morales A.J. Zika virus associated deaths in Colombia.Lancet Infect Dis. 2016; 16: 523-524Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar, Rodriguez-Morales et al., 2019Rodriguez-Morales A.J. Ramirez-Vallejo E. Alvarado-Arnez L.E. Paniz-Mondolfi A. Zambrano L.I. Ko A.I. Fatal Zika virus disease in adults: a critical reappraisal of an under-recognized clinical entity.Int J Infect Dis. 2019; Abstract Full Text Full Text PDF Scopus (7) Google Scholar). In the context of GBS, countries at risk of ZIKV epidemics require adequate intensive care bed capacity for the management of severe cases (Villamil-Gomez et al., 2017Villamil-Gomez W.E. Sanchez-Herrera A.R. Hernandez H. Hernandez-Iriarte J. Diaz-Ricardo K. Castellanos J. et al.Guillain-Barre syndrome during the Zika virus outbreak in Sucre, Colombia, 2016.Travel Med Infect Dis. 2017; 16: 62-63Crossref PubMed Scopus (20) Google Scholar, Dos Santos et al., 2016Dos Santos T. Rodriguez A. Almiron M. Sanhueza A. Ramon P. de Oliveira W.K. et al.Zika Virus and the Guillain-Barre Syndrome — case series from seven countries.N Engl J Med. 2016; 375: 1598-1601Crossref PubMed Scopus (231) Google Scholar, Villamil-Gomez et al., 2016Villamil-Gomez W. Silvera L.A. Paez-Castellanos J. Rodriguez-Morales A.J. Guillain-Barre syndrome after Chikungunya infection: a case in Colombia.Enferm Infecc Microbiol Clin. 2016; 34: 140-141Crossref PubMed Scopus (17) Google Scholar). In fact, the GBS cases in the present study were from areas affected by ZIKV epidemics (Zambrano et al., 2019Zambrano L.I. Vasquez-Bonilla W.O. Fuentes-Barahona I.C. Claudio da Silva J. Valle-Reconco J.A. Medina M.T. et al.Spatial distribution of Zika in Honduras during 2016-2017 using geographic information systems (GIS) — implications for public health and travel medicine.Travel Med Infect Dis. 2019; Crossref Scopus (7) Google Scholar), as well as previous DENV and CHIKV (Zambrano et al., 2017Zambrano L.I. Sierra M. Lara B. Rodriguez-Nunez I. Medina M.T. Lozada-Riascos C.O. et al.Estimating and mapping the incidence of dengue and chikungunya in Honduras during 2015 using Geographic Information Systems (GIS).J Infect Public Health. 2017; 10: 446-456Crossref PubMed Scopus (34) Google Scholar). It can be argued that arbovirus RNA detection by RT-PCR should be part of the study of GBS cases. Most studies have suggested that the numbers of cases of GBS were significantly increased in the Americas during the ZIKV epidemics of 2016 (Dos Santos et al., 2016Dos Santos T. Rodriguez A. Almiron M. Sanhueza A. Ramon P. de Oliveira W.K. et al.Zika Virus and the Guillain-Barre Syndrome — case series from seven countries.N Engl J Med. 2016; 375: 1598-1601Crossref PubMed Scopus (231) Google Scholar). Adherence to protocols for the care of patients with acute neurological syndromes in ZIKV endemic areas is clearly vital, and the training and education of healthcare workers, including travel medicine practitioners dealing with people visiting endemic areas, particularly in Latin America, should be prioritized. Finally, in addition to GBS, the spectrum of the neurological consequences of ZIKV include not only CZS and GBS, but also encephalitis, meningoencephalitis, myelitis, sensory neuropathies, optic neuropathy, seizures, and epilepsy, among other reported complications (Medina and Medina-Montoya, 2017Medina M.T. Medina-Montoya M. New spectrum of the neurologic consequences of Zika.J Neurol Sci. 2017; 383: 214-215Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar). Dirección de Investigación Científica (DICU), Universidad Nacional Autonoma de Honduras.
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    Perception of COVID-19 Vaccination Amongst Physicians in Colombia
    (Multidisciplinary Digital Publishing Institute, 2021) Jorge L. Alvarado-Socarrás; Andrea Liliana Vesga-Varela; Doris Cristina Quintero-Lesmes; Marcela M. Fama-Pereira; Norma C. Serrano; Mauricio Vasco; Virgil Carballo-Zárate; Lysien I. Zambrano; Alberto Paniz‐Mondolfi; Alfonso J. Rodríguez‐Morales
    <i>Introduction</i>: The SARS-CoV-2/COVID-19 pandemic has triggered the need to develop rapidly effective and safe vaccines to prevent infection, particularly in those at-risk populations such as medical personnel. This study's objective was to assess the perception of COVID-19 vaccination amongst Colombian physicians featuring two different scenarios of COVID-19 vaccination. <i>Methods</i>: A cross-sectional analytical study was carried out through an online survey directed at medical staff in several cities in Colombia. The percentage of physicians who have a positive perception to be vaccinated and the associated factors that determine that decision were determined. A binomial regression analysis adjusted for age and sex was carried out, taking as a dependent variable the acceptance of free vaccination with an effectiveness of 60 and 80%. The most significant factors were determined in the non-acceptance of vaccination. <i>Results</i>: Between 77.0% and 90.7% of physicians in Colombia accept COVID-19 vaccination, according to the scenario evaluated where the vaccine's effectiveness was 60 or 80%, respectively. Medical specialty, having never paid for a vaccine, recommending the administration of the vaccine to their parents or people over 70 years, and dispensing the vaccine to their children, were the factors to consider to be vaccinated for free with an effectiveness of 60% and 80%. <i>Conclusions</i>: There is a high perception of the intention to vaccinate physicians in Colombia against COVID-19, and this is very similar to that of the general population.
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    Perception of COVID-19 Vaccination Amongst Physicians in Colombia, January 2021
    (2021) Jorge L. Alvarado-Socarrás; Andrea Liliana Vesga-Varela; Doris Cristina Quintero-Lesmes; Marcela M. Fama-Pereira; Norma C. Serrano; Mauricio Vasco; Virgil Carballo-Zárate; Lysien I. Zambrano; Alberto Paniz‐Mondolfi; Alfonso J. Rodríguez‐Morales
    Introduction: The SARS-CoV-2/COVID-19 pandemic has triggered the need for developing rapidly effective and safety vaccines to prevent infection, particularly in those at-risk populations such as medical personnel. The objective of this study was to assess perception of COVID-19 vaccination amongst Colombian physicians featuring two different sceneries of COVID-19 vaccination. Methods: A cross-sectional analytical study was carried out through an online survey, directed at medical staff in several cities in Colombia. The percentage of physicians who have a positive perception to be vaccinated and the associated factors that determine that decision were determined. A binomial regression analysis adjusted for age and sex was carried out, taking as a dependent variable the acceptance of free vaccination with an effectiveness of 60 and 80%. The most significant factors were determined in the non-acceptance of vaccination. Results: Between 77.1% and 90.8% of physicians in Colombia, accept COVID-19 vaccination, according to the scenario evaluated where the effectiveness of the vaccine was 60 or 80%, respectively. Medical specialty, have ever paid for a vaccine, recommend administrating the vaccine to their parents or people over 70 years and dispense the vaccine to their children were the factors to be vaccinated for free with an effectiveness of 60% and 80%. Conclusions: There is a high perception of the intention to vaccinate physicians in Colombia against COVID-19. But it is very similar to that of the general population, according to results reported in other studies.
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    SARS-CoV-2 natural infection in animals: a systematic review of studies and case reports and series
    (Taylor & Francis, 2021) D. Katterine Bonilla‐Aldana; Alejandra García-Barco; S. Daniela Jiménez-Diaz; Jorge Luis Bonilla-Aldana; María C. Cardona-Trujillo; Fausto Muñoz‐Lara; Lysien I. Zambrano; Luis Andrés Salas-Matta; Alfonso J. Rodríguez‐Morales
    COVID-19 pandemic is essentially a zoonotic disease. In this context, early in 2020, transmission from humans to certain animals began reporting; the number of studies has grown since. To estimate the pooled prevalence of SARS-CoV-2 natural infection in animals and to determine differences in prevalence between countries, years, animal types and diagnostic methods (RT-PCR or serological tests). A systematic literature review with meta-analysis using eight databases. Observational studies were included but analyzed separately. We performed a random-effects model meta-analysis to calculate the pooled prevalence and 95% confidence interval (95% CI) for prevalence studies and case series. After the screening, 65 reports were selected for full-text assessment and included for qualitative and quantitative analyses. A total of 24 reports assessed SARS-CoV-2 infection by RT-PCR, combining a total of 321,785 animals, yielding a pooled prevalence of 12.3% (95% CI 11.6%-13.0%). Also, a total of 17 studies additionally assessed serological response against SARS-CoV-2, including nine by ELISA, four by PRTN, one by MIA, one by immunochromatography (rest, two studies, the method was not specified), combining a total of 5319 animals, yielding a pooled prevalence of 29.4% (95% CI 22.9%-35.9%). A considerable proportion of animals resulted infected by SARS-CoV-2, ranking minks among the highest value, followed by dogs and cats. Further studies in other animals are required to define the extent and importance of natural infection due to SARS-CoV-2. These findings have multiple implications for public human and animal health. One Health approach in this context is critical for prevention and control.
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    Spatial distribution of dengue in Honduras during 2016–2019 using a geographic information systems (GIS)–Dengue epidemic implications for public health and travel medicine
    (Elsevier BV, 2019) Lysien I. Zambrano; Edith Rodríguez; Iván Alfonso Espinoza-Salvadó; Itzel Carolina Fuentes-Barahona; Tales Lyra de Oliveira; Gláucia Luciano da Veiga; José Cláudio da Silva; Jorge Alberto Valle-Reconco; Alfonso J. Rodríguez‐Morales
    The pattern and evolution of DENV epidemic in 2019 in Honduras has been similar to that which occurred for in 2015. As previously reported, this epidemic involved the north and central areas of the country predominantly, reaching municipality incidences there >1000 cases/100,000 population (or 1%). Studies using geographical information systems linked with clinical disease characteristics are necessary to obtain accurate epidemiological data for public health systems. Such information is also useful for assessment of risk for travelers who visit specific areas in a destination country.
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    Spatial Distribution of Dengue in Honduras during 2016-2019 Using Geographic Information Systems (GIS) &amp;ndash; Implications During Epidemic for Public Health and Travel Medicine
    (2019) Lysien I. Zambrano; Edith Rodríguez; Iván Alfonso Espinoza-Salvadó; Itzel Carolina Fuentes-Barahona; Tales Lyra de Oliveira; Gláucia Luciano da Veiga; José Cláudio da Silva; Jorge Alberto Valle-Reconco; Alfonso J. Rodríguez‐Morales
    Background: After serious epidemics of chikungunya (CHIKV) and Zika (ZIKV) in the Americas, dengue (DENV) have reemerged in most countries. We analyzed the incidence, incidence rates, and evolution of DENV cases in Honduras from 2015-2018 and the ongoing 2019 epidemic. Methods: Using epidemiological weeks (EW) surveillance data on the DENV in Honduras, we estimated incidence rates (cases/100,000 population), and developed maps at national, departmental, and municipal levels. Results: From 1 January 2016 to 21 July 2019, a total of 109,557 cases of DENV were reported, 28,603 in 2019, for an incidence rate of 312.32 cases/100,000 pop this year; 0.13% laboratory-confirmed. The highest peak was reached on the EW 28&amp;deg;, 2019 (5,299 cases; 57.89 cases/100,000 pop). The department with the highest number of cases and incidence rate was Cortes (8,404 cases, 479.68 cases/100,000 pop in 2019). Discussion: The pattern and evolution of DENV epidemic in 2019 in Honduras has been similar to that which occurred for in 2015. As previously reported, this epidemic involved the north and central areas of the country predominantly, reaching municipality incidences there &amp;gt;1,000 cases/100,000 pop (1%). Studies using geographical information systems linked with clinical disease characteristics are necessary to attain accurate epidemiological data for public health systems. Such information is also useful for assessment of risk for travelers who visit specific areas in a destination country.
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    Spatial Distribution of Zika in Honduras during 2016&amp;ndash;2017 Using Geographic Information Systems (GIS)&amp;mdash;Implications in Public Health and Travel Medicine
    (2018) Lysien I. Zambrano; Walter O. Vasquez-Bonilla; Itzel Carolina Fuentes-Barahona; José Cláudio da Silva; Jorge Alberto Valle-Reconco; Marco Tulio Medina; John D. England; Jorge A. Sánchez‐Duque; Alfonso J. Rodríguez‐Morales
    Background: Zika virus (ZIKV) infection has affected significantly Latin America in 2015&amp;ndash;2017. However, most studies have been reported from Brazil and Colombia, but few of them in Central America. For these reasons we analyzed the incidence, incidence rates and evolution of cases of Honduras during 2016&amp;ndash;2017. Methods: Using epidemiological weeks (EW) surveillance data on the ZIKV epidemics in Honduras, we estimated incidence rates (cases/100,000 population), and developed maps at national, departments and municipal levels. Results: From January 1, 2016 to December 31, 2017, a total of 32,607 cases of Zika were reported (98.5% in 2016 for an incidence rate of 36.85 cases/100,000 pop; 1% confirmed by RT-PCR). The highest peak was reached on the EW 6&amp;deg;, 2016 (2,559 cases; 29.34 cases/100,000 pop). The department with the highest number of cases and incidence rate was Cort&amp;eacute;s (13,128 cases, 791.08 cases/100,000 pop in 2016). Discussion: Pattern and evolution of Zika in Honduras has been like those that occurred for chikungunya in 2015, that we analyzed and previously reported, affecting predominantly the central and capital area of the country, reaching also high incidences there &amp;gt;750 cases/100,000 pop. Studies using geographical information systems, to map its epidemiology, as well on the clinical aspects linked to, are necessary in this country, as well for the assessment of risk for travelers who visit specific areas in a destination country.
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    Spatial Distribution of Zika in Honduras during 2016&amp;ndash;2017 Using Geographic Information Systems (GIS)&amp;mdash;Implications in Public Health and Travel Medicine
    (2019) Lysien I. Zambrano; Walter O. Vasquez-Bonilla; Itzel Carolina Fuentes-Barahona; José Cláudio da Silva; Jorge Alberto Valle-Reconco; Marco Tulio Medina; John D. England; Jorge A. Sánchez‐Duque; Alfonso J. Rodríguez‐Morales
    Background: Zika virus (ZIKV) infection has significantly affected Latin America in 2015&amp;ndash;2017. Most studies have been reported from Brazil and Colombia, and only a few from Central America. For these reasons we analyzed the incidence, incidence rates and evolution of cases in Honduras from 2016&amp;ndash;2017. Methods: Using epidemiological weeks (EW) surveillance data on the ZIKV epidemics in Honduras, we estimated incidence rates (cases/100,000 population), and developed maps at national, departmental and municipal levels. Results: From 1 January 2016 to 31 December 2017, a total of 32,607 cases of ZIKV were reported (98.5% in 2016 for an incidence rate of 36.85 cases/100,000 pop; 1% confirmed by RT-PCR). The highest peak was reached on the EW 6&amp;deg;, 2016 (2,559 cases; 29.34 cases/100,000 pop). The department with the highest number of cases and incidence rate was Cort&amp;eacute;s (13,128 cases, 791.08 cases/100,000 pop in 2016). Discussion: The pattern and evolution of ZIKV infection in Honduras has been similar to that which occurred for chikungunya in 2015. As previously reported, infection with chikungunya involved predominantly the central and capital area of the country, reaching incidences there &amp;gt;750 cases/100,000 pop. &amp;nbsp;Studies using geographical information systems linked with clinical disease characteristics are necessary to attain accurate epidemiological data for public health systems. Such information is also useful for assessment of risk for travelers who visit specific areas in a destination country.
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    Spatial distribution of Zika in Honduras during 2016–2017 using geographic information systems (GIS) – Implications for public health and travel medicine
    (Elsevier BV, 2019) Lysien I. Zambrano; Walter O. Vasquez-Bonilla; Itzel Carolina Fuentes-Barahona; José Cláudio da Silva; Jorge Alberto Valle-Reconco; Marco T. Medina; John D. England; Jorge A. Sánchez‐Duque; Alfonso J. Rodríguez‐Morales