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Article

Mapping Eastern (EEE) and Venezuelan Equine Encephalitides (VEE) among Equines Using Geographical Information Systems, Colombia, 2008–2019

by
D. Katterine Bonilla-Aldana
1,
Christian David Bonilla Carvajal
2,3,
Emilly Moreno-Ramos
4,
Joshuan J. Barboza
5,* and
Alfonso J. Rodriguez-Morales
3,6,7,8
1
Research Unit, Universidad Continental, Huancayo 12000, Peru
2
Faculty of Veterinary Medicine, Fundación Universitaria Autónoma de las Américas, Pereira 660003, Colombia
3
Faculties of Veterinary Medicina and Medicine, Institución Universitaria Visión de las Américas, Pereira 660003, Colombia
4
Universidad San Ignacio de Loyola, Lima 13008, Peru
5
Vicerrectorado de Investigacion, Universidad Norbert Wiener, Lima 15046, Peru
6
Faculty of Health Sciences, Universidad Científica del Sur, Lima 15067, Peru
7
Grupo de Investigación Biomedicina, Faculty of Medicine, Fundación Universitaria Autónoma de las Américas, Pereira 660003, Colombia
8
Gilbert and Rose-Marie Chagoury School of Medicine, Lebanese American University, Beirut 1102, Lebanon
*
Author to whom correspondence should be addressed.
Viruses 2023, 15(3), 707; https://doi.org/10.3390/v15030707
Submission received: 8 November 2022 / Revised: 6 January 2023 / Accepted: 9 January 2023 / Published: 8 March 2023
(This article belongs to the Special Issue Chikungunya Virus and Emerging Alphaviruses)
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Abstract

:
Introduction: Eastern equine encephalitis virus (EEEV) and Venezuelan equine encephalitis virus (VEEV) viruses are zoonotic pathogens affecting humans, particularly equines. These neuroarboviruses compromise the central nervous system and can be fatal in different hosts. Both have significantly influenced Colombia; however, few studies analyse its behaviour, and none develop maps using geographic information systems to characterise it. Objective: To describe the temporal-spatial distribution of those viruses in Colombia between 2008 and 2019. Methods: Retrospective cross-sectional descriptive study, based on weekly reports by municipalities of the ICA, of the surveillance of both arboviruses in equines, in Colombia, from 2008 to 2019. The data were converted into databases in Microsoft Access 365®, and multiple epidemiological maps were generated with the Kosmo RC1®3.0 software coupled to shape files of all municipalities in the country. Results: In the study period, 96 cases of EEE and 70 of VEE were reported, with 58% of EEE cases occurring in 2016 and 20% of EEV cases in 2013. The most affected municipalities for EEE corresponded to the department of Casanare: Yopal (20), Aguazul (16), and Tauramena (10). In total, 40 municipalities in the country reported ≥1 case of EEE. Conclusions: The maps allow a quick appreciation of groups of neighbouring municipalities in different departments (1° political division) and regions of the country affected by those viruses, which helps consider the expansion of the disease associated with mobility and transport of equines between other municipalities, also including international borders, such as is the case with Venezuela. In that country, especially for EEV, municipalities in the department of Cesar are bordering and at risk for that arboviral infection. there is a high risk of equine encephalitis outbreaks, especially for VEE. This poses a risk also, for municipalities in the department of Cesar, bordering with Venezuela.

1. Introduction

Vector-borne diseases remain a significant public health problem in tropical and subtropical regions, especially those of viral aetiology. Beyond dengue, chikungunya, and Zika, other particularly zoonotic arboviruses, such as the case of equine encephalitides, are especially relevant in the Americas [1]. Venezuelan Equine Encephalitis virus (VEEV) has been especially important after the large outbreak across the Venezuelan-Colombian border in 1995; this led to approximately ~75,000 cases in humans, ~4% with neurological consequences and a case fatality rate of 0.4% (4 per 1000 cases), just in the La Guajira State of Colombia. In that area, ~50,000 horses were infected, with 4000 fatal outcomes (~8%) [2,3].
The Venezuelan equine encephalitis virus causes Venezuelan equine encephalomyelitis. Mosquito vectors, such as Culex spp. (involved in the enzootic cycle), Ochlerotatus, and Psorophora spp., transmit the virus. Culex serves as amplifying vector, and Ochleratatus and Psorophora as bridge vectors. It mainly affects different species of equids, humans, and wild animals. However, the enzootic cycle of VEEV is complex and involves many other species of mammals. Some of the enzootic viral species within the alphavirus genus are Mosso das Pedras virus, Everglades virus, Mucambo virus, Tonate virus, Pixuna virus, Cabassou virus, and Río Negro virus, among others [1].
Besides VEEV, a related alphavirus is eastern equine encephalitis (EEE). EEE is one of the most severe arboviral encephalitides that occurs in different countries in the Americas. It has been reported in northern and southern countries, including Canada, the United States of America (USA), Belize, Costa Rica, Panama, Colombia, Venezuela, Ecuador, Guyana, Suriname, Brazil, and Bolivia [1].
EEE is considered an emerging viral disease and is showing a steady increase in incidence in a broader population. In the USA, six to eight cases are reported annually, predominantly between May and October, primarily in Florida, Georgia, Maryland, Wisconsin, and New Jersey. This virus has also been considered a potential bioterrorism weapon, given its airborne transmission. According to the Centers for Disease Control and Prevention (CDC), EEEV and VEEV are considered bioterrorism agents in category B, the second highest priority pathogens, including those that are moderately easy to spread, led to moderate fatality rates and low mortality rates, and require specific enhancements of CDC’s diagnostic capacity and enhanced disease surveillance (www.cdc.gov, accessed on 1 October 2022). The fatality rate of EEE is 30%, with neurological sequelae observed in approximately 50% of survivors [4].
EEEV virus was initially isolated from dead horses in Delaware, Maryland, and Virginia in 1933. However, it continues to circulate among Culiseta melanura mosquitoes and birds that serve as amplifying hosts in freshwater hardwood swamps [5]. Notably, C. melanura feeds almost exclusively on birds. Hence, the spread of the EEE virus to humans and other mammalian hosts (e.g., horses) requires invertebrate hosts such as Aedes, Coquillettidia, or Culex that feed on both birds and mammals [6]. Culex pedroi (enzootic cycle) and Aedes taeniorhynchus (epizootic cycle) are considered the main vectors of EEEV [1,7,8]. In the eastern United States, especially following the 2019 season, New England states (north of New Jersey) were also heavily affected by the virus [9].
Following the 1967–68 epizootic of VEE in areas of low and moderate seasonal rainfall in Colombia, a strain of the VEE virus was sought in the high-rainfall region of the Pacific lowlands, where previous serological studies had shown past VEE activity. VEE virus in humans without indication of clinical disease manifests in epidemic form. A total of 20 sentinel hamsters, in two groups, were exposed for 2-week periods, one in July and one in August and September 1969, along the margins of a grassy freshwater swamp area 50 km inland from the port of Tumaco, department of Nariño, near the north Ecuadorian border. In Colombia, departments are the first political divisions of the territory (e.g., analogous to states in the United States). One hamster developed an infection from the VEE virus, and two others from the EEE virus [8,10,11]. EEE virus isolates were the first from Colombia, the first from the west coast of South America, and the first from sentinel hamsters [12]. The circulation of the EEE virus in Colombia has been reported since 1957, and species such as Culex bidens were suspected to be this virus’s vector during an epizootic in Argentina in 1988. In 2016, C. bidens was identified in the municipality of Santa Cruz de Lorica, Córdoba, on the north Caribbean coast of Colombia [13].
Both viral pathologies (EEE and VEE) can cause severe compromise of the central nervous system and death, both in animals and in humans, with the ability to persist over time due to having multiple vertebrate hosts. Despite all of the above, there are few studies on VEE [14,15,16,17,18] and even more on EEE in Colombia [19,20]. The objective of the current study is to characterise the temporal-spatial distribution of EEE and VEE in Colombia between 2008 and 2019.

2. Methods

2.1. Type of Study

A retrospective cross-sectional descriptive observational study was conducted to assess the incidence of EEE and VEE in horses in Colombia. Their incidence per year for the Colombian departments was estimated, and epidemiological maps of the diseases were developed covering the years 2008 to 2019. Additionally, for 2016 to 2019, the annual number of equines per department was obtained. For that period, the incidence rate of EEE and VEE was estimated by calculating the number of cases per 100,000 equines per department per year, confirmed by RT-PCR, by the accredited ICA central reference laboratories.
This is a study of secondary sources where bulletins from the Columbian Agricultural Institute (ICA) were used to obtain local sociodemographic data and records of disease occurrences and their locations, including disease diagnosis. In addition, the total number of cases and their regional location were taken for the geographical characterisation of the incidence of VEE-EEE in the departments of Colombia.
For the respective geographical characterisation, the free access software Kosmo 3.1 was used, which comes with preloaded tools for the geographical analyses. For this investigation, West Bogotá (West Bogotá) (Magna SIRGAS) was used as a reference system (EPSG 21896) of the geographic coordinate system. The mapping was carried out (at a scale of 1: 1,365,207) for which two types of layers were used; the first layer was the departments, to which colours of greater and lesser intensity were added, defined by the epidemiological data layer, classified by ranges established by quartiles, which made it possible to differentiate the areas with a higher incidence of the disease from those with a lower incidence.

2.2. Population

Horses from Colombia between the periods 2008–2019 that were diagnosed positive for EEE and VEE, according to the ICA databases.

2.3. Sample

The sample was a census taken from the ICA databases, from which registered data will be taken from cases of diagnosis of EEE and VEE in horses in Colombia between 2008 and 2019, confirmed by molecular testing, RT-PCR, by the accredited ICA central reference laboratories.

2.4. Analyses

Descriptive statistics were performed on Stata IC® version 14. The summary of cases per year and departments and the median number and their interquartile (IQR) cases per year for specific periods were calculated.

3. Results

In the study period (2008–2019), 96 cases of EEE (median 2 cases/year, IQR 0–7) and 70 of VEE were reported (median 6 cases/year, IQR 3–8), with 58% of EEE cases occurring in 2016 (Figure 1) and 20% of VEE cases in 2013 (Figure 2).
The most affected municipalities for EEE corresponded to the department of Casanare: Yopal (20), Aguazul (16) and Tauramena (10) (Figure 3, Figure 4, Figure 5, Figure 6 and Figure 7). A total of 40 municipalities in the country reported ≥1 case of EEE in the period (Figure 3). For VEE, the cases were less concentrated, with Montelíbano, Córdoba being the municipality with the most reported cases (4) (Figure 8, Figure 9, Figure 10 and Figure 11). A total of 44 municipalities reported ≥1 case of VEE in the period (Figure 8).
During the first six years (2008–2013), a smaller number of cases and affected municipalities was observed for EEV (Figure 3) compared with the following six years (2014–2019) (Figure 3, Figure 4, Figure 5, Figure 6 and Figure 7). On the other hand, the highest concentration of cases and affected municipalities in VEE occurred from 2013 to 2016 (Figure 8, Figure 9, Figure 10 and Figure 11).
In 2016, there was a concentration of cases in the neighbouring municipalities in the Casanare department, amounting to 93% of the annual cases for that year (Figure 5). In 2017, municipalities such as Cumaribo, La Primavera, and Arauca, which border Venezuela, reported cases of EEE (Figure 6). In 2013, 2014, and 2016, a similar situation occurred for Tibú, Agustin Codazzi, Becerril, and Curumaní municipalities, which also border with that country and reported cases of VEE (Figure 9, Figure 10 and Figure 11). In addition, one capital municipality reported cases of VEE in 2014 and 2016, Valledupar.
For 2016–2019, the highest incidence rates of VEE (cases per 100,000 animals) were observed in 2016, 0.829 cases per 100,000 animals (8.29 cases per 1,000,000 animals) (Table 1).
In 2016, the department with the highest incidence rate was Cesar (14.165 cases per 100,000 animals). However, the national rates decreased in the following years to 0.346 cases per 100,000 animals (3.46 cases per 1,000,000 animals) in 2017, to 0.269 cases per 100,000 animals (2.69 cases per 1,000,000 animals) in 2018, and 0 cases per 100,000 animals in 2019 (Table 1). For 2017, the department with the highest incidence rate was Cordoba (1.842 cases per 100,000 animals). In 2018, at Chocó, the incidence rate was 18.150 cases per 100,000 animals. In 2019 no cases were reported (Table 1).
For 2016–2019, the highest incidence rates of EEE (cases per 100,000 animals) were observed in 2016, 3.870 cases per 100,000 animals (38.7 cases per 1,000,000 animals) (Table 2). In 2016, the department with the highest incidence rate was Casanare (62.999 cases per 100,000 animals). However, the national rates decreased in the following years to 1.176 cases per 100,000 animals (11.76 cases per 1,000,000 animals) in 2017, to 0.269 cases per 100,000 animals (2.69 cases per 1,000,000 animals) in 2018, and 0 cases per 100,000 animals in 2019 (Table 2). For 2017, the department with the highest incidence rate was Vichada (56.417 cases per 100,000 animals). In 2018, at Guaviare, the incidence rate was 9.708 cases per 100,000 animals. In 2019 only Meta reported cases with an incidence rate of 3.159 per 100,000 animals (Table 2). On the border with Venezuela, the Cesar department (Figure 11) had 2016 high incidence rates of VEE (Table 3).

4. Discussion

Zoonotic arboviruses may be considered even more complex than those that are only anthroponotic or are predominantly anthroponotic [21]. Equine encephalitides are suitable examples of that. These arboviruses include many flavi and alphaviruses and have a wide range of animal hosts and humans. Birds and horses, specifically, are key animals in their enzootic cycles [21]. In the case of horses, these are animals that may serve as sentinels for these vector-borne diseases, as well as for others, mainly due to the ease of access to them, given their proximity to human beings. Regarding birds, the fact that many of them are migratory is a matter of concern for international spreading in countries related to migration routes.
Equine encephalitides such as EEE and VEE are still significant zoonotic arboviral threats in Colombia, Venezuela, and other countries of Latin America and probably the Caribbean islands [1,22,23,24]. In the current study, a wide distribution during the study period was observed in both alphavirus infections. Nevertheless, with higher variations in EEE (0 to 56 cases in a year), reaching a peak of cases in 2016, without significant variations in the number of cases per year for VEE (0 to 14 cases per year) were observed.
As expected, circulation in municipalities bordering Venezuela was observed in both infections, which may create concern given the sanitary crisis in the country. Over the last few years, the sanitary crisis in Venezuela has implied the reemergence of multiple infectious diseases in humans, animals, zoonotic diseases, and a decrease in vaccination and control programmes, which have led to a complex situation. That may be related to vaccination problems and the critical situation and especially given the healthcare crisis in Venezuela [25], where there are no vaccination programmes for animals or humans (lack of immunisation for measles, mumps, yellow fever and multiple other vaccine-preventable diseases), and where numerous infectious diseases have re-emerged, including foot-and-mouth disease that was reintroduced to Colombia from Venezuela [25,26,27,28,29,30,31]. Furthermore, the border crossing of human beings from Venezuela to Colombia has been documented among patients with imported infections, that in some cases, try to reach other borders, such as the one between Colombia and Ecuador in the South or between Colombia and Panama trying to reach the “American dream” after crossing the Darién gap [32,33,34,35]. Although humans are not important reservoir hosts for VEE or EEE, they may cross borders infected and may be diagnosed in other territories and countries.
Additionally, although they may not be a suitable source for transmission, they may impact the health system, care, and disease burden in destination areas. Domestic, farm and wild animals, including equines and birds, may cross the borders (in areas without border controls), sometimes even with their owners, with multiple implications, including EEE and VEE. Therefore, more controls and regulations regarding equines, including vaccination, should be considered, as they may add an additional burden to the healthcare systems of destination countries. In the case of VEE, live-attenuated vaccines have been used in the U.S. military and laboratory workers, and formalin-inactivated vaccines are available for use in horses [36]. One such live-attenuated vaccine is TC-83, developed initially by the U.S. army for vaccine use [37]. TC-83 was created by serially passaging the Trinidad Donkey VEEV strain in guinea pig heart cells [38]. In recent years, new vaccines for horses have been investigated [39], but even a phase 1, open-label, dose-escalation, randomised clinical trial, assessing the safety and immunogenicity of a trivalent virus-like particle vaccine against Western, Eastern, and Venezuelan Equine Encephalitis viruses in humans found a favourable safety profile and neutralising antibody responses including high response against VEE and EE. Along with pressing public health needs, evidence supports further evaluation of the vaccine in advanced-phase clinical trials [40]. In this context, especially vaccination against VEE plays a key role in control. However, the enhancement in the vaccination programme against eastern and Venezuelan equine encephalitis viruses should be performed not only in Colombia but across the border to Venezuela. Given the current sociopolitical situation, cooperation between both governments should be held in order to improve the disease control and vaccination programmes in both countries and specifically on the border. Such arboviral diseases may add an additional burden to the healthcare systems of destination countries.
In the case of EEE, this neuroarbovirus has been scarcely investigated in Colombia, with municipalities of the department of Casanare, such as Yopal, Aguazul, San Luis de Palenque, Trinidad, Orocué, Mani, and Tauramena, affected in 2016. Additionally, in 2017, many municipalities of the eastern plains or lowlands presented cases of EEE in the departments of Meta, Guaviare, Arauca, and Vichada. The maps developed show a clear circulation corridor that goes from the municipality of La Primavera (Vichada) on the border with Venezuela, passing through Cumaribo (Vichada), San José del Guaviare (Guaviare), Puerto Rico (Meta) and Puerto Lleras (Meta) (Figure 6). Surveillance for eastern and Venezuelan equine encephalitis viruses needs to be increased in the country in humans and horses, as well as studies in birds are also crucial for understanding its transmission. In addition, entomological surveillance is critical in studying such cycles [41], including the study of the mosquito’s host preference, which may be helpful in understanding vector feeding [16].
VEE is a persistent zoonosis in Colombia through long periods of apparent epidemiological silence in horses and humans [41,42,43]. In addition to equine studies, it is essential to know the behaviour of rodents as well as bats [24,44], which could have a potential role as dispersing hosts of this virus. Therefore, equine surveillance is helpful as a predictive or sentinel indicator to prevent human cases. Similarly, EEE, to date, has not been reported in Colombia in humans. Nevertheless, a member of the eastern equine encephalitis virus (EEEV) complex, Madariaga virus (MADV) is currently registered in multiple countries of Latin America [45], such as Brazil, Panama [46], Haiti [47], Venezuela [48], among others and in addition to Argentina [49], where it was described.

5. Conclusions

The developed GIS-based maps generated have allowed us to quickly appreciate groups of neighbouring municipalities in different departments and regions of the country affected by EEE and VEE, helps to appreciate the expansion of the disease associated with mobility and transportation of equines between different municipalities, also including international borders, as it is the case with Venezuela, especially for VEE, with municipalities of the department of Cesar among others. Furthermore, these results have implications for public health in planning and surveillance, especially in those municipalities close to those historically affected in the study period. Future assessments of equine encephalitides should extend to other potential threats, including MADV, Western Equine Encephalitis virus, West Nile Virus, Saint Louis encephalitis virus, reported in Brazil [18,50,51,52], Rocio virus [53,54], among others, that may even be considered neglected arboviruses in Latin America [55].

Author Contributions

Conceptualization; methodology; software; validation; formal analysis; investigation; resources; data curation; writing—original draft preparation; writing—review and editing; visualization; project administration; funding acquisition: D.K.B.-A.; C.D.B.C.; E.M.-R.; J.J.B.; A.J.R.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Therefore, The Animal Ethics Committee (CICUA) at the Fundación Universitaria Autónoma de las Américas, Colombia, approved and endorsed this study (Acta No. 34 de 2021).

Informed Consent Statement

Not applicable.

Data Availability Statement

Available upon reasonable request.

Acknowledgments

Semillero de investigación en Zoonosis (ZISOO) for their support. In addition, to the Instituto Colombiano Agropecuario (ICA) (Colombian Agriculture Institute) for providing us with the epidemiological bulletins, the primary data source. This study was presented in part as a thesis on Veterinary Medicine of CDBC, under the direction of DKBA, at Institución Universitaria Visión de las Américas, Colombia.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Guzmán-Terán, C.; Calderón-Rangel, A.; Rodriguez-Morales, A.; Mattar, S. Venezuelan equine encephalitis virus: The problem is not over for tropical America. Ann. Clin. Microbiol. Antimicrob. 2020, 19, 19. [Google Scholar] [CrossRef] [PubMed]
  2. Rivas, F.; Diaz, L.A.; Cardenas, V.; Daza, E.; Bruzon, L.; Alcala, A.; De La Hoz, O.; Caceres, F.M.; Aristizabal, G.; Martinez, J.W.; et al. Epidemic Venezuelan Equine Encephalitis in La Guajira, Colombia, 1995. J. Infect. Dis. 1997, 175, 828–832. [Google Scholar] [CrossRef] [PubMed]
  3. Navarro, J.C.; Medina, G.; Vasquez, C.; Coffey, L.L.; Wang, E.; Suárez, A.; Biord, H.; Salas, M.; Weaver, S.C. Postepizootic persistence of Venezuelan equine en-cephalitis virus, Venezuela. Emerg. Infect. Dis. 2005, 11, 1907–1915. [Google Scholar] [CrossRef] [PubMed]
  4. Banda, C.; Samanta, D. Eastern Equine Encephalitis. StatPearls. In Treasure Island (FL); StatPearls Publishing LLC: Tampa, FL, USA, 2022. [Google Scholar]
  5. Mackay, A.J.; Cara, C.; Kim, C.-H.; Stone, C.M. Update on the distribution of Culiseta melanura in regions of Illinois with prior eastern equine encephalitis virus activity. J. Vector Ecol. 2022, 47, 230–234. [Google Scholar] [CrossRef] [PubMed]
  6. Gill, C.M.; Beckham, J.D.; Piquet, A.L.; Tyler, K.L.; Pastula, D.M. Five Emerging Neuroinvasive Arboviral Diseases: Cache Valley, Eastern Equine Encephalitis, Jamestown Canyon, Powassan, and Usutu. Skull Base 2019, 39, 419–427. [Google Scholar] [CrossRef] [PubMed]
  7. Figueiredo, L.T.M. The Brazilian flaviviruses. Microbes Infect. 2000, 2, 1643–1649. [Google Scholar] [CrossRef]
  8. Carrera, J.-P.; Forrester, N.; Wang, E.; Vittor, A.Y.; Haddow, A.D.; López-Vergès, S.; Abadía, I.; Castaño, E.; Sosa, N.; Báez, C.; et al. Eastern Equine Encephalitis in Latin America. New Engl. J. Med. 2013, 369, 732–744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Armstrong, P.M.; Andreadis, T.G. Ecology and Epidemiology of Eastern Equine Encephalitis Virus in the Northeastern United States: An Historical Perspective. J. Med. Èntomol. 2021, 59, 1–13. [Google Scholar] [CrossRef]
  10. Aréchiga-Ceballos, N.; Aguilar-Setién, A. Alphaviral equine encephalomyelitis (Eastern, Western and Venezuelan). Rev. Sci. Technol. (Int. Off. Epizoot.) 2015, 34, 491–501. [Google Scholar] [CrossRef]
  11. Petrov, A.A.; Lebedev, V.N.; Kulish, V.S.; Pyshnaya, N.S.; Stovba, L.F.; Borisevich, S. Epidemiologic Analysis of Outbreaks of Diseases Caused by American Equine Encephalitis Causative Agents in Endemic Regions. J. Microbiol. Epidemiol. Immunobiol. 2015, 5, 103–110. [Google Scholar]
  12. Sanmartín, C.; Trapido, H.; Barreto, P.; Lesmes, C.I. Isolations of Venezuelan and Eastern Equine Encephalomyelitis Viruses from Sentinel Hamsters Exposed in the Pacific Lowlands of Colombia. Am. J. Trop. Med. Hyg. 1971, 20, 469–473. [Google Scholar] [CrossRef] [PubMed]
  13. Laurito, M.; Hoyos-Lopez, R. First record of Culex (Culex) bidens (Diptera: Culicidae) in Colombia: Taxonomic and epidemio-logical implications. Acta Trop. 2018, 188, 251–257. [Google Scholar] [CrossRef] [PubMed]
  14. Torres-Gutierrez, C.; Bergo, E.S.; Emerson, K.J.; de Oliveira, T.M.; Greni, S.; Sallum, M.A.M. Mitochondrial COI gene as a tool in the taxonomy of mosquitoes Culex subgenus Melanoconion. Acta Trop. 2016, 164, 137–149. [Google Scholar] [CrossRef] [PubMed]
  15. Mendenhall, I.H.; Bahl, J.; Blum, M.J.; Wesson, D.M. Genetic Structure of Culex erraticus Populations Across the Americas. J. Med. Èntomol. 2012, 49, 522–534. [Google Scholar] [CrossRef] [PubMed]
  16. Mendenhall, I.H.; Tello, S.A.; Neira, L.A.; Castillo, L.F.; Ocampo, C.B.; Wesson, D.M. Host preference of the arbovirus vector Culex erraticus (Diptera: Culicidae) at Sonso Lake, Cauca Valley Department, Colombia. J. Med. Entomol. 2012, 49, 1092–1102. [Google Scholar] [CrossRef] [Green Version]
  17. Kumar, B.; Manuja, A.; Gulati, B.R.; Virmani, N.; Tripathi, B. Zoonotic Viral Diseases of Equines and Their Impact on Human and Animal Health. Open Virol. J. 2018, 12, 80–98. [Google Scholar] [CrossRef] [Green Version]
  18. Komar, N.; Clark, G.G. West Nile virus activity in Latin America and the Caribbean. Rev. Panam. Salud Pública 2006, 19, 112–117. [Google Scholar] [CrossRef] [Green Version]
  19. Guzmán, C.; Calderón, A.; Martinez, C.; Oviedo, M.; Mattar, S. Eco-epidemiology of the Venezuelan equine encephalitis virus in bats of Córdoba and Sucre, Colombia. Acta Trop. 2018, 191, 178–184. [Google Scholar] [CrossRef]
  20. Guzmán, C.; Calderón, A.; Oviedo, T.; Mattar, S.; Castañeda, J.; Rodriguez, V.; Figueiredo, L.T.M. Molecular and cellular evidence of natural Venezuelan equine encephalitis virus infection in frugivorous bats in Colombia. Veter-World 2020, 13, 495–501. [Google Scholar] [CrossRef] [Green Version]
  21. Weaver, S.C. Prediction and prevention of urban arbovirus epidemics: A challenge for the global virology community. Antivir. Res. 2018, 156, 80–84. [Google Scholar] [CrossRef]
  22. Crosby, B.; Crespo, M.E. Venezuelan Equine Encephalitis. StatPearls. In Treasure Island (FL); StatPearls Publishing LLC: Tampa, FL, USA, 2022. [Google Scholar]
  23. Garcia-Rejon, J.E.; Navarro, J.C.; Cigarroa-Toledo, N.; Baak-Baak, C.M. An Updated Review of the Invasive Aedes albopictus in the Americas; Geographical Distribution, Host Feeding Patterns, Arbovirus Infection, and the Potential for Vertical Transmission of Dengue Virus. Insects 2021, 12, 967. [Google Scholar] [CrossRef] [PubMed]
  24. Bonilla-Aldana, D.K.; Jimenez-Diaz, S.D.; Arango-Duque, J.S.; Aguirre-Florez, M.; Balbin-Ramon, G.J.; Paniz-Mondolfi, A.; Suárez, J.A.; Pachar, M.R.; Perez-Garcia, L.A.; Delgado-Noguera, L.A.; et al. Bats in ecosystems and their Wide spectrum of viral infectious potential threats: SARS-CoV-2 and other emerging viruses. Int. J. Infect. Dis. IJID Off. Publ. Int. Soc. Infect. Dis. 2021, 102, 87–96. [Google Scholar] [CrossRef] [PubMed]
  25. Rodríguez-Morales, A.J.; Suárez, J.A.; Risquez, A.; Delgado-Noguera, L.; Paniz-Mondolfi, A. The current syndemic in Venezuela: Measles, malaria and more co-infections coupled with a breakdown of social and healthcare infrastructure. Quo vadis? Travel Med. Infect. Dis. 2018, 27, 5–8. [Google Scholar] [CrossRef] [PubMed]
  26. Paniz-Mondolfi, A.E.; Sordillo, E.M.; Marquez-Colmenarez, M.C.; Delgado-Noguera, L.A.; Rodriguez-Morales, A.J. The arrival of SARS-CoV-2 in Venezuela. Lancet 2020, 395, e85–e86. [Google Scholar] [CrossRef] [PubMed]
  27. Rodríguez-Morales, A.J.; Bonilla-Aldana, D.K.; Morales, M.; Suárez, J.A.; Martínez-Buitrago, E. Migration crisis in Venezuela and its impact on HIV in other countries: The case of Colombia. Ann. Clin. Microbiol. Antimicrob. 2019, 18, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Rodriguez-Morales, A.J.; Bonilla-Aldana, D.K.; Risquez, A.; Paniz-Mondolfi, A.; Suarez, J.A. Should we be concerned about Vene-zuelan hemorrhagic fever?—A reflection on its current situation in Venezuela and potential impact in Latin America amid the migration crisis. New Microbes New Infect. 2021, 44, 100945. [Google Scholar] [CrossRef]
  29. Rodríguez-Morales, A.J.; Bonilla-Aldana, D.K.; Suárez, J.A.; Franco-Paredes, C.; Forero-Peña, D.A.; Mattar, S.; Villamil-Gómez, W.E.; Ruíz-Sáenz, J.; Cardona-Ospina, J.A.; Figuera, M.E.; et al. Yellow fever reemergence in Venezuela—Implications for international travelers and Latin American countries during the COVID-19 pandemic. Travel Med. Infect. Dis. 2021, 44, 102192. [Google Scholar] [CrossRef]
  30. Rodriguez-Morales, A.J.; Figuera, M.E. COVID-19 in Colombia and Venezuela: Two Sides of the Coin. Am. J. Public Health 2022, 112, S581–S584. [Google Scholar] [CrossRef]
  31. Malirat, V.; Bergmann, I.E.; Campos, R.D.M.; Conde, F.; Quiroga, J.L.; Villamil, M.; Salgado, G.; Ortiz, S. Molecular epidemiology of foot-and-mouth disease virus type A in South America. Veter. Microbiol. 2012, 158, 82–94. [Google Scholar] [CrossRef]
  32. Rodriguez-Morales, A.J.; Suarez, J.A.; Risquez, A.; Cimerman, S.; Valero-Cedeno, N.; Cabrera, M.; Grobusch, M.P.; Paniz-Mondolfi, A. In the eye of the storm: Infec-tious disease challenges for border countries receiving Venezuelan migrants. Travel Med. Infect. Dis. 2019, 30, 4–6. [Google Scholar] [CrossRef]
  33. Rodriguez-Morales, A.J.; Suarez, J.A.; Risquez, A.; Villamil-Gomez, W.E.; Paniz-Mondolfi, A. Consequences of Venezuela’s massive migration crisis on imported malaria in Colombia, 2016-2018. Travel Med. Infect. Dis. 2019, 28, 98–99. [Google Scholar] [CrossRef] [PubMed]
  34. Tobon-Giraldo, M.; Salazar, M.I.; Aguirre-Florez, M.; Montilla-Trejos, C.A.; Suárez, J.A.; Rodriguez-Morales, A.J. The dilemmas and care challenges of Venezuelan pregnant migrants presenting in Colombia. Travel Med. Infect. Dis. 2019, 32, 101409. [Google Scholar] [CrossRef] [PubMed]
  35. Higuita, N.A.; Suarez, J.A.; Millender, E.; Creighton, E.G.; Corbisiero, M.F.; Freites, C.O.; Cordero, J.H.; Kousari, A.; Unterborn, R.; Marcos, L.A.; et al. U.S. bound journey of migrant peoples InTransit across Dante’s Inferno and Purgatory in the Americas. Travel Med. Infect. Dis. 2022, 47, 102317. [Google Scholar] [CrossRef]
  36. Taylor, K.; Kolokoltsova, O.; Ronca, S.E.; Estes, M.; Paessler, S. Live, Attenuated Venezuelan Equine Encephalitis Virus Vaccine (TC83) Causes Persistent Brain Infection in Mice with Non-functional αβ T-Cells. Front. Microbiol. 2017, 8, 81. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Pittman, P.R.; Makuch, R.S.; Mangiafico, J.A.; Cannon, T.L.; Gibbs, P.H.; Peters, C.J. Long-term duration of detectable neutralising an-tibodies after administration of live-attenuated VEE vaccine and following booster vaccination with inactivated VEE vaccine. Vaccine 1996, 14, 337–343. [Google Scholar] [CrossRef]
  38. Alevizatos, A.C.; McKinney, R.W.; Feigin, R.D. Live, attenuated Venezuelan equine encephalomyelitis virus vaccine. I. Clinical effects in man. Am. J. Trop. Med. Hyg. 1967, 16, 762–768. [Google Scholar] [CrossRef] [PubMed]
  39. Fine, D.L.; Roberts, B.A.; Teehee, M.L.; Terpening, S.J.; Kelly, C.L.; Raetz, J.L.; Baker, D.C.; Powers, A.M.; Bowen, R.A. Venezuelan equine encephalitis virus vaccine can-didate (V3526) safety, immunogenicity and efficacy in horses. Vaccine 2007, 25, 1868–1876. [Google Scholar] [CrossRef]
  40. Coates, E.E.; Edupuganti, S.; Chen, G.L.; Happe, M.; Strom, L.; Widge, A.; Florez, M.B.; Cox, J.H.; Gordon, I.; Plummer, S.; et al. Safety and immunogenicity of a trivalent virus-like particle vaccine against western, eastern, and Venezuelan equine encephalitis viruses: A phase 1, open-label, dose-escalation, randomised clinical trial. Lancet Infect. Dis. 2022, 22, 1210–1220. [Google Scholar] [CrossRef]
  41. Paniz-Mondolfi, A.E.; Blohm, G.; Piñero, R.; Rondon-Cadenas, C.; Rodríguez-Morales, A.J. Venezuelan equine encephalitis: How likely are we to see the next epidemic? Travel Med. Infect. Dis. 2017, 17, 67–68. [Google Scholar] [CrossRef]
  42. Rodríguez-Morales, A.J.; Paniz-Mondolfi, A.E.; Villamil-Gómez, W.E.; Navarro, J.C. Mayaro, Oropouche and Venezuelan Equine Encephalitis viruses: Following in the footsteps of Zika? Travel Med. Infect. Dis. 2017, 15, 72–73. [Google Scholar] [CrossRef]
  43. Ortiz-Martinez, Y.; Villamil-Gómez, W.E.; Rodríguez-Morales, A.J. Bibliometric assessment of global research on Venezuelan Equine Encephalitis: A latent threat for the Americas. Travel Med. Infect. Dis. 2016, 15, 78–79. [Google Scholar] [CrossRef]
  44. Forrester, N.L.; Wertheim, J.O.; Dugan, V.G.; Auguste, A.J.; Lin, D.; Adams, A.P.; Chen, R.; Gorchakov, R.; Leal, G.; Estrada-Franco, J.G.; et al. Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas. PLoS Negl. Trop. Dis. 2017, 11, e0005693. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Gil, L.; Magalhaes, T.; Santos, B.; Oliveira, L.; Oliveira-Filho, E.; Cunha, J.; Fraiha, A.; Rocha, B.; Longo, B.; Ecco, R.; et al. Active Circulation of Madariaga Virus, a Member of the Eastern Equine Encephalitis Virus Complex, in Northeast Brazil. Pathogens 2021, 10, 983. [Google Scholar] [CrossRef] [PubMed]
  46. Carrera, J.-P.; Pittí, Y.; Molares-Martínez, J.C.; Casal, E.; Pereyra-Elias, R.; Saenz, L.; Guerrero, I.; Galué, J.; Rodriguez-Alvarez, F.; Jackman, C.; et al. Clinical and Serological Findings of Madariaga and Venezuelan Equine Encephalitis Viral Infections: A Follow-up Study 5 Years After an Outbreak in Panama. Open Forum Infect. Dis. 2020, 7, ofaa359. [Google Scholar] [CrossRef] [PubMed]
  47. Lednicky, J.A.; White, S.K.; Mavian, C.N.; El Badry, M.A.; Telisma, T.; Salemi, M.; Okech, B.A.; De Rochars, V.M.B.; Morris, J.G. Emergence of Madariaga virus as a cause of acute febrile illness in children, Haiti, 2015-2016. PLoS Negl. Trop. Dis. 2019, 13, e0006972. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Blohm, G.M.; Lednicky, J.A.; White, S.K.; Mavian, C.N.; Márquez, M.C.; González-García, K.P.; Salemi, M.; Morris, J.G.; Paniz-Mondolfi, A.E. Madariaga Virus: Identification of a Lineage III Strain in a Venezuelan Child With Acute Undifferentiated Febrile Illness, in the Setting of a Possible Equine Epizootic. Clin. Infect. Dis. 2018, 67, 619–621. [Google Scholar] [CrossRef]
  49. Stechina, O.S.; Oria, G.I.; Torres, C.; Diaz, L.A.; Contigiani, M.; Stein, M. First Detection of Madariaga virus in Mosquitoes Collected in a Wild Environment of Northeastern Argentina. Am. J. Trop. Med. Hyg. 2019, 101, 916–918. [Google Scholar] [CrossRef]
  50. Batallán, G.P.; Konigheim, B.S.; Quaglia, A.I.; Rivarola, M.E.; Beranek, M.D.; Tauro, L.B.; Flores, S.F.; Laurito, M.; Almirón, W.R.; Contigiani, M.S.; et al. Autochthonous circulation of Saint Louis encephalitis and West Nile viruses in the Province of La Rioja, Argentina. Rev. Argent. Microbiol. 2021, 53, 154–161. [Google Scholar] [CrossRef]
  51. Burgueño, A.; Spinsanti, L.; Díaz, L.A.; Rivarola, M.E.; Arbiza, J.; Contigiani, M.; Delfraro, A. Seroprevalence of St. Louis encephalitis virus and West Nile virus (Flavivirus, Flaviviridae) in horses, Uruguay. BioMed Res. Int. 2013, 2013, 582957. [Google Scholar] [CrossRef] [Green Version]
  52. Mansilla, A.P.; Grande, J.M.; Diaz, A. Effect of Agroecosystems on Seroprevalence of St. Louis Encephalitis and West Nile Viruses in Birds, La Pampa, Argentina, 2017–2019. Emerg. Infect. Dis. 2022, 28, 1393–1402. [Google Scholar] [CrossRef]
  53. Saivish, M.V.; Da Costa, V.G.; Rodrigues, R.L.; Féres, V.C.R.; Montoya-Diaz, E.; Moreli, M.L. Detection of Rocio Virus SPH 34675 during Dengue Epidemics, Brazil, 2011–2013. Emerg. Infect. Dis. 2020, 26, 797–799. [Google Scholar] [CrossRef] [PubMed]
  54. Saivish, M.V.; Gomes da Costa, V.; de Lima Menezes, G.; Alves da Silva, R.; Dutra da Silva, G.C.; Moreli, M.L.; Sacchetto, L.; Pacca, C.C.; Vasilakis, N.; Nogueira, M.L. Rocio Virus: An Updated View on an Elusive Flavivirus. Viruses 2021, 13, 2293. [Google Scholar] [CrossRef] [PubMed]
  55. Rodriguez-Morales, A.J.; Bonilla-Aldana, D.K. Neglected Arboviruses in Latin America. In New Advances in Neglected Tropical Diseases; Rijeka, D.M.A.S., Ed.; IntechOpen: London, UK, 2022; p. 1. [Google Scholar]
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Figure 1. Yearly cases of EEE among equines in Colombia from 2008 to 2019.
Figure 1. Yearly cases of EEE among equines in Colombia from 2008 to 2019.
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Figure 2. Yearly cases of VEE among equines in Colombia from 2008 to 2019.
Figure 2. Yearly cases of VEE among equines in Colombia from 2008 to 2019.
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Figure 3. Distribution maps of EEE among equines, Colombia, 2008–2019.
Figure 3. Distribution maps of EEE among equines, Colombia, 2008–2019.
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Figure 4. EEE among equines in affected municipalities of Colombia, 2011 and 2014.
Figure 4. EEE among equines in affected municipalities of Colombia, 2011 and 2014.
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Figure 5. EEE among equines in affected municipalities of Colombia, 2015 and 2016.
Figure 5. EEE among equines in affected municipalities of Colombia, 2015 and 2016.
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Figure 6. EEE among equines in affected municipalities of Colombia, 2017.
Figure 6. EEE among equines in affected municipalities of Colombia, 2017.
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Figure 7. EEE among equines in affected municipalities of Colombia, 2018 and 2019.
Figure 7. EEE among equines in affected municipalities of Colombia, 2018 and 2019.
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Figure 8. Distribution maps of VEE among equines, Colombia, 2008–2019.
Figure 8. Distribution maps of VEE among equines, Colombia, 2008–2019.
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Figure 9. VEE among equines in affected municipalities of Colombia, 2013.
Figure 9. VEE among equines in affected municipalities of Colombia, 2013.
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Figure 10. VEE among equines in affected municipalities of Colombia, 2014.
Figure 10. VEE among equines in affected municipalities of Colombia, 2014.
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Figure 11. VEE among equines in affected municipalities of Colombia, 2016.
Figure 11. VEE among equines in affected municipalities of Colombia, 2016.
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Table
Table 1. VEE cases, equine population, and equine VEE annual incidence per department, Colombia, 2016–2019.
Table 1. VEE cases, equine population, and equine VEE annual incidence per department, Colombia, 2016–2019.
DepartmentCases per YearPopulation per YearAnnual Incidence
(Cases/100,000 Animals)
201620172018201920162017201820192016201720182019
Amazonas000005250650.0000.0000.0000.000
Antioquia0100153,970165,213178,018221,4630.0000.6050.0000.000
Arauca000049,80055,40258,17052,0530.0000.0000.0000.000
Atlantico000012,70010,66399421990.0000.0000.0000.000
Bolivar000053,80853,35657,07110,1010.0000.0000.0000.000
Boyaca000048,26848,26846,86857,3860.0000.0000.0000.000
Caldas0000873118,95621,11052,9260.0000.0000.0000.000
Caqueta000048,34948,34954,56341,0140.0000.0000.0000.000
Casanare000082,54199,20890,04963,6390.0000.0000.0000.000
Cauca000081,76482,48386,83497,0800.0000.0000.0000.000
Cesar800056,47758,43761,09189,25614.1650.0000.0000.000
Choco002011,35910,57811,01960,9960.0000.00018.1500.000
Cordoba1200106,829108,604115,47311,0690.9361.8420.0000.000
Cundinamarca0000109,077109,077108,455112,8050.0000.0000.0000.000
Guainia000012,19012,190154110,7790.0000.0000.0000.000
Guaviare000011,130856110,3011050.0000.0000.0000.000
Huila000064,84156,31056,31011,0150.0000.0000.0000.000
La-Guajira000021,27614,02521,03845,6030.0000.0000.0000.000
Magdalena010062,54456,34460,28921,0500.0001.7750.0000.000
Meta200066,03772,18477,41563,3073.0290.0000.0000.000
Narino000054,20955,30552,32379,9980.0000.0000.0000.000
Norte de Santander001026,50117,54824,53747,6610.0000.0004.0750.000
Putumayo000011,59611,98211,61426,6210.0000.0000.0000.000
Quindio000031236995699513,5050.0000.0000.0000.000
Risaralda0000910011,670626763830.0000.0000.0000.000
San Andres000015815516656910.0000.0000.0000.000
Santander100077,20057,79758,42559,1971.2950.0000.0000.000
Sucre010056,87954,37154,70362,9080.0001.8390.0000.000
Tolima0010118,214118,590118,590146,6310.0000.0000.8430.000
Valle000019,96119,77720,74724,3150.0000.0000.0000.000
Vaupes0000282191400.0000.0000.0000.000
Vichada000084363545754481530.0000.0000.0000.000
Total125401,447,0961,446,0161,486,2221,603,0140.8290.3460.2690.000
Table
Table 2. EEE cases, equine population, and equine EEE annual incidence per department, Colombia, 2016–2019.
Table 2. EEE cases, equine population, and equine EEE annual incidence per department, Colombia, 2016–2019.
DepartmentCases per YearPopulation per YearAnnual Incidence
(Cases/100,000 Animals)
201620172018201920162017201820192016201720182019
Amazonas000005250650.0000.0000.0000.000
Antioquia1300153,970165,213178,018221,4630.6491.8160.0000.000
Arauca020049,80055,40258,17052,0530.0003.6100.0000.000
Atlantico000012,70010,66399421990.0000.0000.0000.000
Bolivar010053,80853,35657,07110,1010.0001.8740.0000.000
Boyaca010048,26848,26846,86857,3860.0002.0720.0000.000
Caldas0000873118,95621,11052,9260.0000.0000.0000.000
Caqueta010048,34948,34954,56341,0140.0002.0680.0000.000
Casanare5201082,54199,20890,04963,63962.9990.0001.1110.000
Cauca000081,76482,48386,83497,0800.0000.0000.0000.000
Cesar000056,47758,43761,09189,2560.0000.0000.0000.000
Choco010011,35910,57811,01960,9960.0009.4540.0000.000
Cordoba2100106,829108,604115,47311,0691.8720.9210.0000.000
Cundinamarca0000109,077109,077108,455112,8050.0000.0000.0000.000
Guainia000012,19012,190154110,7790.0000.0000.0000.000
Guaviare011011,130856110,3011050.00011.6819.7080.000
Huila000064,84156,31056,31011,0150.0000.0000.0000.000
La-Guajira001021,27614,02521,03845,6030.0000.0004.7530.000
Magdalena020062,54456,34460,28921,0500.0003.5500.0000.000
Meta121266,03772,18477,41563,3071.5142.7711.2923.159
Narino000054,20955,30552,32379,9980.0000.0000.0000.000
Norte de Santander000026,50117,54824,53747,6610.0000.0000.0000.000
Putumayo000011,59611,98211,61426,6210.0000.0000.0000.000
Quindio000031236995699513,5050.0000.0000.0000.000
Risaralda0000910011,670626763830.0000.0000.0000.000
San Andres000015815516656910.0000.0000.0000.000
Santander000077,20057,79758,42559,1970.0000.0000.0000.000
Sucre000056,87954,37154,70362,9080.0000.0000.0000.000
Tolima0000118,214118,590118,590146,6310.0000.0000.0000.000
Valle000019,96119,77720,74724,3150.0000.0000.0000.000
Vaupes0000282191400.0000.0000.0000.000
Vichada020084363545754481530.00056.4170.0000.000
Total5617421,447,0961,446,0161,486,2221,603,0143.8701.1760.2690.125
Table
Table 3. VEE cases, equine population, and equine EEE annual incidence per municipalities at the department of Cesar, Colombia, 2016–2019.
Table 3. VEE cases, equine population, and equine EEE annual incidence per municipalities at the department of Cesar, Colombia, 2016–2019.
MunicipalityCases per YearPopulation per YearAnnual Incidence
(Cases/100,000 Animals)
201620172018201920162017201820192016201720182019
Aguachica000024392419244324450.0000.0000.0000.000
Agustín Codazzi1000402040314036403524.8760.0000.0000.000
Astrea000025002797291529180.0000.0000.0000.000
Becerril30001200143621712180250.0000.0000.0000.000
Bosconia000023002146216421650.0000.0000.0000.000
Chimichagua000024002681289228930.0000.0000.0000.000
Chiriguaná000020103459436943700.0000.0000.0000.000
Curumaní1000205026043092309448.7800.0000.0000.000
El Copey1000261026852456246038.3140.0000.0000.000
El Paso000018502595304730500.0000.0000.0000.000
Gamarra000013101229129813000.0000.0000.0000.000
González000065058059620.0000.0000.0000.000
La Gloria000023502337231023120.0000.0000.0000.000
La Jagua de Ibirico000016001450125412560.0000.0000.0000.000
La Paz000024002450263526380.0000.0000.0000.000
Manaure00008508502022050.0000.0000.0000.000
Pailitas000018101432142714300.0000.0000.0000.000
Pelaya000020101319138713900.0000.0000.0000.000
Pueblo Bello000012705334274300.0000.0000.0000.000
Río de Oro000016601343148814900.0000.0000.0000.000
San Alberto000017721681166516640.0000.0000.0000.000
San Diego000025502316221621140.0000.0000.0000.000
San Martín000024002100306130550.0000.0000.0000.000
Tamalameque000019131946178617900.0000.0000.0000.000
Valledupar2000855310,01810,29110,25023.3840.0000.0000.000
Total800056,47758,43761,09160,99614.1650.0000.0000.000
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Bonilla-Aldana, D.K.; Bonilla Carvajal, C.D.; Moreno-Ramos, E.; Barboza, J.J.; Rodriguez-Morales, A.J. Mapping Eastern (EEE) and Venezuelan Equine Encephalitides (VEE) among Equines Using Geographical Information Systems, Colombia, 2008–2019. Viruses 2023, 15, 707. https://doi.org/10.3390/v15030707

AMA Style

Bonilla-Aldana DK, Bonilla Carvajal CD, Moreno-Ramos E, Barboza JJ, Rodriguez-Morales AJ. Mapping Eastern (EEE) and Venezuelan Equine Encephalitides (VEE) among Equines Using Geographical Information Systems, Colombia, 2008–2019. Viruses. 2023; 15(3):707. https://doi.org/10.3390/v15030707

Chicago/Turabian Style

Bonilla-Aldana, D. Katterine, Christian David Bonilla Carvajal, Emilly Moreno-Ramos, Joshuan J. Barboza, and Alfonso J. Rodriguez-Morales. 2023. "Mapping Eastern (EEE) and Venezuelan Equine Encephalitides (VEE) among Equines Using Geographical Information Systems, Colombia, 2008–2019" Viruses 15, no. 3: 707. https://doi.org/10.3390/v15030707

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