Panamericana de Salud Publica  2020 44, 03

COVID-19 pandemic in Panama: lessons of the unique risks and research opportunities for Latin America.

Jose R. Loaiza, Rao Kosagisharaf, Gilberto A. Eskildsen, Eduardo Ortega-Barria, Matthew J. Miller y Rolando A. Gittens.


The Republic of Panama has the second most unequally distrib-uted wealth in Central America, has recently entered the list of countries affected by the COVID-19 pandemic, and has one of the largest testing rate per inhabitant in the region and consequently the highest incidence rate of COVID-19, making it an ideal loca-tion to discuss potential scenarios for assessing epidemic pre-paredness, and to outline research opportunities in the Region of the Americas. We address two timely important questions: What are the unique risks of COVID-19 in Panama that could help other countries in the Region be better prepared? And what kind of scientific knowledge can Panama contribute to the regional and global study of COVID-19? This paper provides suggestions about how the research community could support local health authori-ties plan for different scenarios and decrease public anxiety. It also presents basic scientific opportunities about emerging pandemic pathogens towards promoting global health from the perspective of a middle income country.





Microbiology Resource Announcements 2020 16;9(16):e00230-20

Genome Sequences of Chikungunya Virus Isolates from Bolivia

Caio M. França, Roxana Loayza, Yelin Roca, Ana Maria Montaño Arias, Freddy Tinajeros, Loaiza JR., Anshule Takyar, Robert H. Gilman,

Matthew J. Miller.


We generated nine coding-complete chikungunya virus genome sequences from blood samples collected during the early 2015 outbreak in Bolivia. Relative to other publicly available chikungu-nya sequences, the Bolivian samples represent a monophyletic group, suggesting that a single lineage was widely circulating in the country between February and May 2015.





BMC Public Health (2018) 18:1261

Socioeconomic and demographic predictors of resident knowledge,

attitude, and practice regarding arthropod-borne viruses in Panama

A. Whiteman, A. Mejia, I. Hernandez, J. R. Loaiza.


Background: We sought to identify if socioeconomic and demographic factors play a role in resident knowledge, attitude, and practice regarding Dengue, Chikungunya, and Zika in order to inform effective management procedures for disease prevention in Panama, a middle-income tropical country in Central America. All three are arthropod-borne viruses transmitted by Aedes mosquito vectors present in the focal region of Panama City, the largest city in Central America and an urban region of extreme socioeconomic polarization.

Methods: Between November 2017 and February 2018, we administered standardized, anonymous knowledge, attitude, and practice surveys to 263 residents split between two neighborhoods of high socioeconomic status (SES) and two neighborhoods of low SES. We then summed the knowledge, attitude, and practice scores respectively, and used linear and logistic regressions to quantify relationships with socioeconomic and demographic factors.

Results: Low-SES neighborhoods with high proportions of low income residents, residents over 70 years old had lower mean knowledge scores compared to other groups. Furthermore, residents in neighborhoods of low SES reported more mosquito biting relative to residents in neighborhoods of high SES, yet comparably lower level of concerns for disease transmission. Additionally, knowledge was lower for the more novel emergent threats of Chikungunya and Zika, compared to the endemic Dengue.

Conclusion: Findings suggest that low-SES neighborhoods with high proportions of low income, low education, and elderly residents should be targeted for outreach programs designed to prevent DENV, CHIKV, or ZIKV in Panama City. These outcomes support our initial hypotheses as lower relative knowledge and fewer practices related to the prevention of Dengue, Chikungunya, and Zika were found in low-SES neighborhoods. There is also a widespread lack of adequate knowledge regarding these diseases as well as low levels of concern in areas of highly reported mosquito biting. We provide suggestions for taking neighborhood socioeconomic status and specific aspects resident health literacy and attitude into account for creating more effective outreach campaigns as both endemic and novel arthropod-borne disease rates continue to increase throughout Latin America.





PLOS ONE 2018;13(3):e0194874

Maternal invasion history of Aedes aegypti and Aedes albopictus into the Isthmus of Panama: Implications for the control of emergent viral disease agents

Gilberto A. Eskildsen, Jose R. Rovira, Octavio Smith, Matthew J. Miller, Kelly L. Bennett, W. Owen McMillan, Jose Loaiza.


Despite an increase in dengue outbreaks and the arrival of chikungunya and Zika disease in Panama, studies on the demographic history of the invasive Aedes mosquitoes that are the principle vectors of these diseases are still lacking in this region. Here, we assess the genetic diversity of these mosquitoes in order to decipher their invasion histories into the Isthmus of Panama. DNA sequences from the mitochondrial cytochrome C oxidase I gene obtained from 30 localities in 10 provinces confirmed the presence of more than one mito- chondrial haplogroup (i.e., maternal lineage) in each species. The invasion of Aedes albopictus was likely from temperate European countries, as the most frequent and widespread haplogroup in Panama harbored variants that are uncommon elsewhere in the Americas. Two infrequent and geographically restricted Ae. albopictus haplotypes appear to have subsequently invaded Panama from neighboring Costa Rica and the USA, respectively. In addition, we recovered two deeply divergent mitochondrial clades in Panamanian Aedes aegypti. The geographic origins of these clades is unknown, given that divergence in the mitochondrial genome is probably due to ancient population processes within the native range of Ae. aegypti, rather than due to its global expansion out of Africa. However, Panamanian Ae. aegypti mitochondrial sequences within the first clade were closely related to others from Colombia, Bolivia, Brazil, Mexico and the USA, suggesting two separate invasions from Western Hemisphere source populations. The pattern of increased genetic diversity in Aedes mosquitoes in Panama is likely facilitated by the numerous land and water inter-connections across the country, which allows them to enter via sea- and land-transportation from Europe, North, Central and South America. Our results here should be considered in disease mitigation programs if emergent arboviruses are to be effectively diminished in Panama through vector suppression.




Biological Journal of the Linnean Society, 2018, XX, 1–12

Historical and contemporary forces combine to shape patterns of genetic differentiation in two species of Mesoamerican Anopheles mosquitoes

Jose R. Loaiza, Matthew J. Miller.


Pleistocene environmental changes were important drivers of species- and population-level diversification in Anopheles mosquitoes. However, Anopheles species have different ecologies, so their response to Pleistocene climate oscillations should have differed. We investigate whether genetic diversification in Anopheles punctimacula s.s. (a forest specialist and secondary vector of Plasmodium vivax) and Anopheles albimanus (a habitat colonist and primary vector of P. vivax and P. falciparum) is due to: (1) historical population processes, (2) contemporary population processes or (3) a combination of both. Differences in the degree of refugial isolation during the Last Glacial Maximum (LGM) and the degree to which isolated populations evolved habitat niche differences appear to explain differences in the phylogeographical patterns between A. punctimacula s.s. and A. albimanus in Lower Middle America (Mesoamerica). Refugial isolation during the LGM and subsequent niche diversification shaped the phylogeographical history of A. punctimacula s.s. During the LGM, the genetic pool of this species was fragmented into extremely narrow and scattered habitat refugia, resulting in two discrete mitochondrial lineages. Subsequently, these lineages appear to have further evolved distinct niche preferences and diversified due to different climatic conditions between populations, which may have contributed to the lack of introgression or range overlap among mitochondrial lineages. While A. albimanus also experienced range contraction, recovery was more rapid, and we find no evidence of niche evolution among lineages. This appears to explain the broad mitochondrial introgression in this species. Greater resilience to climatic instability by A. albimanus might contribute to its principal transmission role for human Plasmodium parasites across the Neotropics.




Malaria Journal 2019;18(1):95

Application of matrix-assisted laser desorption/ionization mass spectrometry

to identify species of Neotropical Anopheles vectors of malaria

Jose R. Loaiza, Alejandro Almanza, Juan C. Rojas, Luis Mejía, Norma D. Cervantes, Javier E. Sanchez-Galan, Fernando Merchán,

Arnaud Grillet, Matthew J. Miller, Luis F. De León, Rolando A. Gittens.


Background: Malaria control in Panama is problematic due to the high diversity of morphologically similar Anopheles mosquito species, which makes identification of vectors of human Plasmodium challenging. Strategies by Panama- nian health authorities to bring malaria under control targeting Anopheles vectors could be ineffective if they tackle a misidentified species.

Methods: A rapid mass spectrometry identification procedure was developed to accurately and timely sort out field-collected Neotropical Anopheles mosquitoes into vector and non-vector species. Matrix-assisted laser desorption/ionization (MALDI) mass spectra of highly-abundant proteins were generated from laboratory-reared mosquitoes using different extraction protocols, body parts, and sexes to minimize the amount of material from specimen vouchers needed and optimize the protocol for taxonomic identification. Subsequently, the mass spectra of field-collected Neotropical Anopheles mosquito species were classified using a combination of custom-made unsupervised (i.e., Principal component analysis—PCA) and supervised (i.e., Linear discriminant analysis—LDA) classification algorithms.

Results: Regardless of the protocol used or the mosquito species and sex, the legs contained the least intra-specific variability with enough well-preserved proteins to differentiate among distinct biological species, consistent with previous literature. After minimizing the amount of material needed from the voucher, one leg was enough to produce reliable spectra between specimens. Further, both PCA and LDA were able to classify up to 12 mosquito species, from different subgenera and seven geographically spread localities across Panama using mass spectra from one leg pair. LDA demonstrated high discriminatory power and consistency, with validation and cross-validation positive identification rates above 93% at the species level.

Conclusion: The selected sample processing procedure can be used to identify field-collected Anopheles species, including vectors of Plasmodium, in a short period of time, with a minimal amount of tissue and without the need of an expert mosquito taxonomist. This strategy to analyse protein spectra overcomes the drawbacks of working with out a reference library to classify unknown samples. Finally, this MALDI approach can aid ongoing malaria eradication efforts in Panama and other countries with large number of mosquito’s species by improving vector surveillance in epidemic-prone sites such as indigenous Comarcas.




Journal of General Virology DOI 10.1099/jgv.0.001260

Diverse novel phleboviruses in sandflies from the Panama Canal area,

Central Panama

Marco Marklewitz, Larissa C. Dutari, Sofia Paraskevopoulou, Rachel A. Page, Jose R. Loaiza, Sandra Junglen.


The genus Phlebovirus (order Bunyavirales, family Phenuiviridae) comprises 57 viruses that are grouped into nine species complexes. Sandfly-transmitted phleboviruses are found in Europe, Africa and the Americas and are responsible for febrile illness and infections of the nervous system in humans. The aim of this study was to assess the genetic diversity of sandfly- transmitted phleboviruses in connected and isolated forest habitats throughout the Panama Canal area in Central Panama. In total, we collected 13 807 sandflies comprising eight phlebotomine species. We detected several strains pertaining to five previously unknown viruses showing maximum pairwise identities of 45–78 % to the RNA-dependent RNA polymerase genes of phleboviruses. Entire coding regions were directly sequenced from infected sandflies as virus isolation in cell culture was not successful. The viruses were tentatively named La Gloria virus (LAGV), Mona Grita virus (MOGV), Peña Blanca virus (PEBV), Tico virus (TICV) and Tres Almendras virus (TRAV). Inferred phylogenies and p-distance-based analyses revealed that PEBV groups with the Bujaru phlebovirus speciescomplex, TRAV with the Candiru phlebovirus species- complex and MOGV belongs to the proposed Icoarci phlebovirus speciescomplex, whereas LAGV and TICV seem to be distant members of the Bujaru phlebovirus species-complex. No specific vector or habitat association was found for any of the five viruses. Relative abundance of sandflies was similar over habitat types. Our study shows that blood-feeding insects originating from remote and biodiverse habitats harbour multiple previously unknown phleboviruses. These viruses should be included in future surveillance studies to assess their geographic distribution and to elucidate if these viruses cause symptoms of disease in animals or humans.





Parasites and Vectors, 2019;12(1):264

High infestation of invasive Aedes mosquitoes in used-tyres

along the local transport network of Panama.

Bennett KL, Carmelo Gómez-Martínez, Alejandro Almanza, Jose R. Rovira, W. Owen McMillan, Vanessa Enriquez, Elia Barraza,

Marcela Díaz, Javier Sanchez Galan, Ari Whiteman, Rolando A. Gittens, Loaiza JR..


Background: The long-distance dispersal of the invasive disease vectors Aedes aegypti and Aedes albopictus has introduced arthropod-borne viruses into new geographical regions, causing a significant medical and economic burden. The used-tire industry is an effective means of Aedes dispersal, yet studies to determine Aedes occurrence and the factors influencing their distribution along local transport networks are lacking. To assess infestation along the primary transport network of Panama we documented all existing garages that trade used tires on the highway and surveyed a subset for Ae. aegypti and Ae. albopictus. We also assess the ability of a mass spectrometry approach to classify mosquito eggs by comparing our findings to those based on traditional larval surveillance.

Results: Both Aedes species had a high infestation rate in garages trading used tires along the highways, providing a conduit for rapid dispersal across Panama. However, generalized linear models revealed that the presence of Ae. aegypti is associated with an increase in road density by a log-odds of 0.44 (0.73 ± 0.16; P = 0.002), while the presence of Ae. albopictus is associated with a decrease in road density by a log-odds of 0.36 (0.09 ± 0.63; P = 0.008). Identification of mosquito eggs by mass spectrometry depicted similar

occurrence patterns for both Aedes species as that obtained with traditional rearing methods.





EcoHealth, 2019; 16(2):210-221.

Aedes mosquito infestation in socioeconomically contrasting

neighborhoods of Panama City.

Ari Whiteman, Carmelo Gomez, Jose Rovira, Gang Chen, W. Owen McMillan, Jose Loaiza.


The global expansion and proliferation of Aedes aegypti and Aedes albopictus represents a growing public health threat due to their capacity to transmit a variety of arboviruses to humans, including dengue, chikungunya, and Zika. Particularly important in urban regions, where these species have evolved to breed in man-made containers and feed nearly exclusively on human hosts, the threat of vector-borne disease has risen in recent decades due to the growth of cities, progression of climate change, and increase in globalization. While the dynamics of Aedes populations in urban settings have been well studied in relation to ecological features of the landscape, relatively less is known about the relationship between neighborhood socioeconomic status and Aedes infestation. Here, we compare infestation levels of both A. aegypti and A. albopictus in four socioeconomically contrasting neighborhoods of urban Panama City, Panama. Our results indicate that infestation levels for both Aedes species vary between neighborhoods of contrasting socioeconomic status, being higher in neighborhoods having lower percentage of residents with bachelor degrees and lower monthly household income. Additionally, we find that proximity between socioeconomically contrasting neighborhoods can predict infestation levels by species, with A. aegypti increasing and A. albopictus decreasing with proximity between neighborhoods. These findings hold key implications for the control and prevention of dengue, chikungunya, and Zika in Panama, a region with ongoing arbovirus outbreaks and high economic inequity.





Tropical Medicine & International Health, 2019 24(7): 849-861. doi.org/10.1111/tmi.13244.

Forest disturbance and vector transmitted diseases in the lowland tropical rainforest of central Panama

Jose R. Loaiza, Jose R. Rovira, Oris I. Sanjur, Jesus Altagracia Zepeda, James E. Pecor, Desmond H. Foley, Larissa Dutari, Meghan Radtke,

Montira J. Pongsiri, Octavio Smith Molinar, Gabriel Z. Laporta.


Objective To explore possible changes in the community attributes of haematophagous insects as a function of forest disturbance. We compare the patterns of diversity and abundance, plus the behavioural responses of three epidemiologically distinct vector assemblages across sites depicting various levels of forest cover.

Methods Over a 3-year period, we sampled mosquitoes, sandflies and biting-midges in forested habitats of central Panama. We placed CDC light traps in the forest canopy and in the understorey to gather blood-seeking females.

Results We collected 168 405 adult haematophagous dipterans in total, including 26 genera and 86 species. Pristine forest settings were always more taxonomically diverse than the disturbed forest sites, confirming that disturbance has a negative impact on species richness. Species of Phlebotominae and Culicoides were mainly classified as climax (i.e. forest specialist) or disturbance-generalist, which tend to decrease in abundance along with rising levels of disturbance. In contrast, a significant portion of mosquito species, including primary and secondary disease vectors, was classified as colonists (i.e. disturbed-areas specialists), which tend to increase in numbers towards more disturbed forest habitats. At pristine forest, the most prevalent species of Phlebotominae and Culicoides partitioned the vertical niche by being active at the forest canopy or in the understorey; yet this pattern was less clear in disturbed habitats. Most mosquito species were not vertically stratified in their habitat preference. conclusion We posit that entomological risk and related pathogen exposure to humans is higher in pristine forest scenarios for Culicoides and Phlebotominae transmitted diseases, whereas forest disturbance poses a higher entomological risk for mosquito-borne infections. This suggests that the Dilution Effect Hypothesis (DEH) does not apply in tropical rainforests where highly abundant, yet unrecognised insect vectors and neglected zoonotic diseases occur. Comprehensive, community level entomological surveillance is, therefore, the key for predicting potential disease spill over in scenarios of pristine forest intermixed with anthropogenic habitats. We suggest that changes in forest quality should also be considered when assessing arthropod-borne disease transmission risk.





Tropical Medicine & International Health 2019; 24(7): 849-861. doi.org/10.1111/tmi.13244.

Molecular validation of anthropophilic Phlebotominae sandflies

(Diptera: Psychodidae) in Central Panama

Larissa Dutari, Jose R Loaiza.


Six Phlebotominae sand fly species are incriminated as biological vectors of human pathogens in Panama, but molecular corroboration is still needed. We aim at confirming the identity of Phlebotominae species documented as anthropophilic in Panama. Adult sandflies were collected from August 2010 to February 2012 in Central Panama using CDC light traps. Species confirmation was accomplished through molecular barcodes and allied sequences from GenBank. A total of 53,366 sand fly specimens representing 18 species were collected. Five species were validated molecularly as single phylogenetic clusters, but Psychodopygus thula depicted two genetically divergent lineages, which may be indicative of cryptic speciation.




Scientific Reports, 2019; 9:12160

Dynamics and diversity of bacteria associated with the disease vectors

Aedes aegypti and Aedes albopictus

Kelly L. Bennett, Carmelo Gómez-Martínez, Yamileth Chin, Kristin Saltonstall, W. Owen McMillan, Jose R. Rovira, Jose R. Loaiza.


Aedes aegypti and Aedes albopictus develop in the same aquatic sites where they encounter microorganisms that influence their life history and capacity to transmit human arboviruses. Some bacteria such as Wolbachia are currently being considered for the control of Dengue, chikungunya and Zika. Yet little is known about the dynamics and diversity of Aedes-associated bacteria, including larval habitat features that shape their tempo-spatial distribution. We applied large-scale 16S rRNA amplicon sequencing to 960 adults and larvae of both Ae. aegypti and Ae. albopictus mosquitoes from 59 sampling sites widely distributed across nine provinces of Panama. We find both species share a limited, yet highly variable core microbiota, reflecting high stochasticity within their oviposition habitats. Despite sharing a large proportion of microbiota, Ae. aegypti harbours higher bacterial diversity than Ae. albopictus, primarily due to rarer bacterial groups at the larval stage. We find significant differences between the bacterial communities of larvae and adult mosquitoes, and among samples from metal and ceramic containers. However, we find little support for geography, water temperature and pH as predictors of bacterial associates. We report a low incidence of natural Wolbachia infection for both Aedes and its geographical distribution. this baseline information provides a foundation for studies on the functions and interactions of Aedes-associated bacteria with consequences for bio-control within panama.




Plos One 2019; 14(9): e0222145

Habitat disturbance and the organization of bacterial communities in Neotropical hematophagous arthropods

Kelly L. Bennett, Alejandro Almanza, W. Owen McMillan, Kristin Saltonstall, Evangelina Lo´ pez Vdovenko, Jorge S. VindaI, Luis Mejia,

Kaitlin Driesse, Luis F. De Leo´n, Jose R. Loaiza.


The microbiome plays a key role in the biology, ecology and evolution of arthropod vectors of human pathogens. Vector-bacterial interactions could alter disease transmission dynamics through modulating pathogen replication and/or vector fitness. Nonetheless, our understanding of the factors shaping the bacterial community in arthropod vectors is incomplete.

Using large-scale 16S amplicon sequencing, we examine how habitat disturbance structures the bacterial assemblages of field-collected whole-body hematophagous arthropods that vector human pathogens including mosquitoes (Culicidae), sand flies (Psychodidae), biting midges (Ceratopogonidae) and hard ticks (Ixodidae). We found that all comparisons of the bacterial community among species yielded statistically significant differences, but a difference was not observed between adults and nymphs of the hard tick, Haemaphysalis juxtakochi. While Culicoides species had the most distinct bacterial community among dipterans, tick species were composed of entirely different bacterial OTU’s. We observed differences in the proportions of some bacterial types between pristine and disturbed habitats for Coquillettidia mosquitoes, Culex mosquitoes, and Lutzomyia sand flies, but their associations differed within and among arthropod assemblages. In contrast, habitat quality was a poor predictor of differences in bacterial classes for Culicoides biting midges and hard tick species. In general, similarities in the bacterial communities among hematophagous arthropods could be explained by their phylogenetic relatedness, although intraspecific variation seems influenced by habitat disturbance.




 Journal of General Virology. 2019, doi: 10.1099/jgv.0.001344

Agua Salud alphavirus defines a novel lineage of insect-specific alphaviruses

discovered in the New World

Kyra Hermanns, Marco Marklewitz, Florian Zirkel, Gijs J. Overheul, Rachel A. Page, Jose R. Loaiza, Christian Drosten,

Ronald P. van Rij, Sandra Junglen.


The genus Alphavirus harbours mostly insect-transmitted viruses that cause severe disease in humans, livestock and wildlife.

Thus far, only three alphaviruses with a host range restricted to insects have been found in mosquitoes from the Old

World, namely Eilat virus (EILV), Taï Forest alphavirus (TALV) and Mwinilunga alphavirus (MWAV). In this study, we found a

novel alphavirus in one Culex declarator mosquito sampled in Panama. The virus was isolated in C6/36 mosquito cells, and

full genome sequencing revealed an 11 468 nt long genome with maximum pairwise nucleotide identity of 62.7 % to Sindbis

virus. Phylogenetic analyses placed the virus as a solitary deep rooting lineage in a basal relationship to the Western equine

encephalitis antigenic complex and to the clade comprising EILV, TALV and MWAV, indicating the detection of a novel alphavirus,

tentatively named Agua Salud alphavirus (ASALV). No growth of ASALV was detected in vertebrate cell lines, including cell lines

derived from ectothermic animals, and replication of ASALV was strongly impaired above 31 °C, suggesting that ASALV represents

the first insect-restricted alphavirus of the New World.



Plos Neglected Tropical Diseases 2019; 13 (9): e0007266

Detecting space-time clusters of dengue fever in Panama after adjusting for vector surveillance data

Ari Whiteman, Michael R. Desjardins, Gilberto A. Eskildsen, Jose R. Loaiza.


Long term surveillance of vectors and arboviruses is an integral aspect of disease prevention and control systems in countries

affected by increasing risk. Yet, little effort has been made to adjust space-time risk estimation by integrating disease case counts with vector surveillance data, which may result in inaccurate risk projection when several vector species are present, and when little is known about their likely role in local transmission. Here, we integrate 13 years of dengue case surveillance and associated Aedes occurrence data across 462 localities in 63 districts to estimate the risk of infection in the Republic of Panama. Our exploratory space-time modelling approach detected the presence of five clusters, which varied by duration, relative risk, and spatial extent after incorporating vector species as covariates. The Ae. aegypti model contained the highest number of districts with more dengue cases than would be expected given baseline population levels, followed by the model accounting for both Ae. aegypti and Ae. albopictus. This implies that arbovirus case surveillance coupled with entomological surveillance can affect cluster detection and risk estimation, potentially improving efforts to understand outbreak dynamics at national scales.




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