Robert B Tesh

University of Texas Medical Branch at Galveston, Galveston, Texas, United States

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Publications (352)1433.41 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: The Orbivirus genus of the family Reoviridae is comprised of 22 virus species including the Changuinola virus (CGLV) serogroup. The complete genome sequences of 13 CGLV serotypes isolated between 1961 and 1988 from distinct geographic areas of the Brazilian Amazon region were obtained. All viral sequences were obtained from single-passaged CGLV strains grown in Vero cells. CGLVs are the only orbiviruses known to be transmitted by phlebotomine sandflies. Ultrastructure and molecular analyses by electron microscopy and gel electrophoresis, respectively revealed viral particles with typical orbivirus size and morphology, as well as the presence of a segmented genome with 10 segments. Full-length nucleotide sequencing of each of the ten RNA segments of the 13 CGLV serotypes provided basic information regarding the genome organization, encoded proteins and genetic traits. Segment 2 (encoding VP2) of the CGLV is uncommonly larger in comparison to those found in other orbiviruses and shows varying sizes even among different CGLV serotypes. Phylogenetic analyses support previous serologic findings, which indicated that CGLV constitutes a separate serogroup within the genus Orbivirus. In addition, 6 out of 13 analyzed CGLV serotypes show reassortment of their genome segments.
    Journal of General Virology 07/2014; · 3.13 Impact Factor
  • Xue-Jie Yu, Robert B Tesh
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    ABSTRACT: This review examines the evidence indicating a role for parasitic mites in the transmission and maintenance of Hantaan virus in nature. The available data, much of it from recent studies in China, indicate that both trombiculid and gamasid mites are naturally infected with Hantaan virus and that infected mites can transmit the virus by bite to laboratory mice and transovarially (vertically) through eggs to their offspring. Collectively, these findings challenge the current paradigm of hantavirus transmission, namely that rodents serve as the reservoir of human pathogenic hantaviruses in nature and that humans are infected with these viruses by inhalation of aerosols of infectious rodent excreta. Further research is needed to confirm the mite-hantavirus association and to determine if parasitic mites are in fact the major source and principal vectors of human pathogenic hantaviruses, such as Hantaan. If the mite hypothesis is correct, then it will significantly alter current concepts about the epidemiology, prevention and control of human hantavirus infection.
    The Journal of infectious diseases. 06/2014;
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    ABSTRACT: The genus Negevirus consists of insect-only viruses isolated from mosquitoes and sandflies. Here, we report the successful construction of a full-length infectious cDNA clone of Negev virus strain M30957. Viral RNA was transcribed in vitro and virus was readily rescued with or without the use of a cap analog. These results strongly suggest that Negev virus, and likely other members within the genus, is a non-segmented, single stranded, positive sense RNA virus.
    Journal of General Virology 05/2014; · 3.13 Impact Factor
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    ABSTRACT: BACKGROUND: The family Mesoniviridae (order Nidovirales) comprises of a group of positive-sense, single-stranded RNA ([+]ssRNA) viruses isolated from mosquitoes. FINDINGS: Thirteen novel insect-specific virus isolates were obtained from mosquitoes collected in Indonesia, Thailand and the USA. By electron microscopy, the virions appeared as spherical particles with a diameter of ~50 nm. Their 20,129 nt to 20,777 nt genomes consist of positive-sense, single-stranded RNA with a poly-A tail. Four isolates from Houston, Texas, and one isolate from Java, Indonesia, were identified as variants of the species Alphamesonivirus-1 which also includes Nam Dinh virus (NDiV) from Vietnam and Cavally virus (CavV) from Cote d'Ivoire. The eight other isolates were identified as variants of three new mesoniviruses, based on genome organization and pairwise evolutionary distances: Karang Sari virus (KSaV) from Java, Bontag Baru virus (BBaV) from Java and Kalimantan, and Kamphaeng Phet virus (KPhV) from Thailand. In comparison with NDiV, the three new mesoniviruses each contained a long insertion (180 - 588 nt) of unknown function in the 5' region of ORF1a, which accounted for much of the difference in genome size. The insertions contained various short imperfect repeats and may have arisen by recombination or sequence duplication. CONCLUSIONS: In summary, based on their genome organizations and phylogenetic relationships, thirteen new viruses were identified as members of the family Mesoniviridae, order Nidovirales. Species demarcation criteria employed previously for mesoniviruses would place five of these isolates in the same species as NDiV and CavV (Alphamesonivirus-1) and the other eight isolates would represent three new mesonivirus species (Alphamesonivirus-5, Alphamesonivirus-6 and Alphamesonivirus-7). The observed spatiotemporal distribution over widespread geographic regions and broad species host range in mosquitoes suggests that mesoniviruses may be common in mosquito populations worldwide.
    Virology Journal 05/2014; 11(1):97. · 2.09 Impact Factor
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    ABSTRACT: A novel mononegavirus was isolated in 1975 from ticks (Ornithodoros coriaceus) collected during investigation of an outbreak of epizootic bovine abortion (EBA) in northern California. It was originally designated "bovine abortion-tick virus" (BA-T virus). The EBA is now known to be associated with a deltaproteobacterium infection, and not a virus. The BA-T virus had remained uncharacterized until now. We have determined by electron microscopy, serology, and genome sequencing that the BA-T virus is a fourth member of the newly proposed family Nyamiviridae, and we have renamed it Sierra Nevada virus (SNVV). Although antigenically distinct, phylogenetically SNVV is basal to Nyamanini virus (NYMV) and Midway virus (MIDWV), two other tick-borne agents. Although NYMV was found to infect land birds, and MIDWV seabirds, it is presently unknown whether SNVV naturally infects birds or mammals.
    The American journal of tropical medicine and hygiene 04/2014; · 2.53 Impact Factor
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    ABSTRACT: A novel mononegavirus was isolated in 1975 from ticks (Ornithodoros coriaceus) collected during investigation of an outbreak of epizootic bovine abortion (EBA) in northern California. It was originally designated "bovine abortion-tick virus" (BA-T virus). The EBA is now known to be associated with a deltaproteobacterium infection, and not a virus. The BA-T virus had remained uncharacterized until now. We have determined by electron microscopy, serology, and genome sequencing that the BA-T virus is a fourth member of the newly proposed family Nyamiviridae, and we have renamed it Sierra Nevada virus (SNVV). Although antigenically distinct, phylogenetically SNVV is basal to Nyamanini virus (NYMV) and Midway virus (MIDWV), two other tick-borne agents. Although NYMV was found to infect land birds, and MIDWV seabirds, it is presently unknown whether SNVV naturally infects birds or mammals.
    The American journal of tropical medicine and hygiene 04/2014; · 2.53 Impact Factor
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    ABSTRACT: A serosurvey of antibodies against selected flaviviruses and alphaviruses in 384 bats (representing 10 genera and 14 species) was conducted in the Caribbean island of Trinidad. Sera were analysed using epitope-blocking enzyme-linked immunosorbent assays (ELISAs) specific for antibodies against West Nile virus (WNV), Venezuelan equine encephalitis virus (VEEV) and eastern equine encephalitis virus (EEEV), all of which are zoonotic viruses of public health significance in the region. Overall, the ELISAs resulted in the detection of VEEV-specific antibodies in 11 (2.9%) of 384 bats. Antibodies to WNV and EEEV were not detected in any sera. Of the 384 sera, 308 were also screened using hemagglutination inhibition assay (HIA) for antibodies to the aforementioned viruses as well as St. Louis encephalitis virus (SLEV; which also causes epidemic disease in humans), Rio Bravo virus (RBV), Tamana bat virus (TABV) and western equine encephalitis virus (WEEV). Using this approach, antibodies to TABV and RBV were detected in 47 (15.3%) and 3 (1.0%) bats, respectively. HIA results also suggest the presence of antibodies to an undetermined flavivirus(es) in 8 (2.6%) bats. Seropositivity for TABV was significantly (P < 0.05; χ(2) ) associated with bat species, location and feeding preference, and for VEEV with roost type and location. Differences in prevalence rates between urban and rural locations were statistically significant (P < 0.05; χ(2) ) for TABV only. None of the aforementioned factors was significantly associated with RBV seropositivity rates.
    Zoonoses and Public Health 04/2014; · 2.09 Impact Factor
  • Journal of Virology 03/2014; 88(5):3054. · 5.08 Impact Factor
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    ABSTRACT: Emerging and zoonotic pathogens pose continuing threats to human health and ongoing challenges to diagnostics. As nucleic acid tests are playing increasingly prominent roles in diagnostics, the genetic characterization of molecularly uncharacterized agents is expected to significantly enhance detection and surveillance capabilities. We report the identification of two previously unrecognized members of the family Orthomyxoviridae, which includes the influenza viruses and the tick-transmitted Thogoto and Dhori viruses. We provide morphologic, serologic and genetic evidence that Upolu virus (UPOV) from Australia and Aransas Bay virus (ABV) from North America, both previously considered potential bunyaviruses based on electron microscopy and physicochemical features, are orthomyxoviruses instead. Their genomes show up to 68% nucleotide sequence conservation to Thogoto virus (segment 2; ∼74% at amino acid level) and a more distant relationship to Dhori virus, the two prototype viruses of the recognized species in the genus Thogotovirus. Despite sequence similarity, the coding potential of UPOV and ABV differed from Thogoto virus, being instead like that of Dhori virus. Our findings suggest that the tick-transmitted UPOV and ABV represent geographically distinct viruses in the genus Thogotovirus of the family Orthomyxoviridae that do not fit in the two currently recognized species of that genus. Upolu virus (UPOV) and Aransas Bay virus (ABV) are shown to be orthomyxoviruses instead of bunyaviruses as previously thought. Genetic characterization and adequate classification of agents is paramount in this molecular age to devise appropriate surveillance and diagnostics. Although closer to Thogoto virus by sequence, UPOV and ABV differ in their coding potential by lacking a proposed pathogenicity factor. In this respect they are similar to Dhori virus, which despite this lack can cause disease. These findings enable further studies into the evolution and pathogenicity of orthomyxoviruses.
    Journal of Virology 02/2014; · 5.08 Impact Factor
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    ABSTRACT: A thorough characterization of the genetic diversity of viruses present in vector and vertebrate host populations is essential for the early detection of and response to emerging pathogenic viruses, yet genetic characterization of many important viral groups remains incomplete. The Simbu serogroup of the genus Orthobunyavirus, family Bunyaviridae is an example. The Simbu serogroup currently consists of a highly diverse group of related arboviruses that infect both humans and economically important livestock species. Here, we report complete genome sequences for 11 viruses within this group, with a focus on the large and poorly characterized Manzanilla and Oropouche species complexes. Phylogenetic and pairwise divergence analyses indicate the presence of high-levels of genetic diversity within these two species complexes, on par with that seen among the five other species complexes in the Simbu serogroup. Based on previously reported divergence thresholds between species, the data suggest that these two complexes should actually be divided into at least five species. Together these five species form a distinct phylogenetic clade apart from the rest of the Simbu serogroup. Pairwise sequence divergences among viruses of this clade and viruses in other Simbu serogroup species complexes are similar to levels of divergence among the other orthobunyavirus serogroups. The genetic data also suggest relatively high levels of natural reassortment, with three potential reassortment events present, including two well-supported events involving viruses known to infect humans.
    Journal of General Virology 02/2014; · 3.13 Impact Factor
  • Charles H Calisher, Robert B Tesh
    Archives of Virology 02/2014; · 2.03 Impact Factor
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    ABSTRACT: Arboretum (ABTV) and Puerto Almendras (PTAMV) are two mosquito-associated rhabdoviruses isolated from pools of Psorophora albigenu and Ochlerotattus fulvus mosquitoes, respectively, collected in the Department of Loreto, Peru, in 2009. Initial tests suggested that both viruses were novel rhabdoviruses and this was confirmed by complete genome sequencing. Analysis of their 11,482 nt (ABTV) and 11,876 (PTAMV) genomes indicates that they encode the five canonical rhabdovirus structural proteins (N, P, M, G and L) with an additional gene (U1) encoding a small hydrophobic protein. Evolutionary analysis of the L protein indicates that ABTV and PTAMV are novel and phylogenetically distinct rhabdoviruses that cannot be classified as members of any of the eight currently recognized genera within the family Rhabdoviridae, highlighting the vast diversity of this virus family.
    Journal of General Virology 01/2014; · 3.13 Impact Factor
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    ABSTRACT: Flanders virus (FLAV) and Hart Park virus (HPV) are rhabdoviruses that circulate in mosquito-bird cycles in the eastern and western United States, respectively, and constitute the only two North American representatives of the Hart Park serogroup. Previously, it was suggested that FLAV is unique among the rhabdoviruses in that it contains two pseudogenes located between the P and M genes, while the cognate sequence for HPV has been lacking. Herein, we demonstrate that FLAV and HPV do not contain pseudogenes in this region, but encode three small functional proteins designated as U1-U3 that apparently arose by gene duplication. To further investigate the U1-U3 region, we conducted the first large-scale evolutionary analysis of a member of the Hart Park serogroup by analyzing over 100 spatially and temporally distinct FLAV isolates. Our phylogeographic analysis demonstrates that although FLAV appears to be slowly evolving, phylogenetically divergent lineages co-circulate sympatrically.
    Virology 01/2014; 448C:284-292. · 3.35 Impact Factor
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    ABSTRACT: The complete genomes of Orungo virus (ORUV), Lebombo virus (LEBV) and Changuinola virus (CGLV) were sequenced, confirming that they each encode 11 distinct proteins (VP1-VP7 and NS1-NS4). Phylogenetic analyses of cell-attachment protein 'outer-capsid protein 1' (OC1), show that orbiviruses fall into three large groups, identified as: VP2(OC1), in which OC1 is the 2nd largest protein, including the Culicoides transmitted orbiviruses; VP3(OC1), which includes the mosquito transmitted orbiviruses; and VP4(OC1) which includes the tick transmitted viruses. Differences in the size of OC1 between these groups, places the T2 'subcore-shell protein' as the third largest protein 'VP3(T2)' in the first of these groups, but the second largest protein 'VP3(T2)' in the other two groups. ORUV, LEBV and CGLV all group with the Culicoides-borne VP2(OC1)/VP3(T2) viruses. The G+C content of the ORUV, LEBV and CGLV genomes is also similar to that of the Culicoides-borne, rather than the mosquito-borne, or tick borne orbiviruses. These data suggest that ORUV and LEBV are Culicoides- rather than mosquito-borne. Multiple isolations of CGLV from sand flies suggest that they are its primary vector. OC1 of the insect-borne orbiviruses is approximately twice the size of the equivalent protein of the tick borne viruses. Together with internal sequence similarities, this suggests its origin by duplication (concatermerisation) of a smaller OC1 from an ancestral tick-borne orbivirus. Phylogenetic comparisons showing linear relationships between the dates of evolutionary-separation of their vector species, and genetic-distances between tick-, mosquito- or Culicoides-borne virus-groups, provide evidence for co-evolution of the orbiviruses with their arthropod vectors.
    PLoS ONE 01/2014; 9(1):e86392. · 3.73 Impact Factor
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    ABSTRACT: Pools of mosquitoes were tested for insect-specific viruses using cytopathic effect (CPE) assays on Aedes albopictus (C6/36) cells. Illumina sequencing of RNA from pool TR7094, which produced extensive CPE two days post-infection, yielded the complete genome sequences of a previously unknown Bunyavirus, designated Cumuto virus (CUMV), and a second virus designated Wallerfield virus (WALV). WALV shared highest amino acid identity (60.1%) with Dezidougou virus from Cote d'Ivoire, a positive-sense, single-strand RNA, insect-specific virus belonging to the newly proposed Negevirus genus associated with mosquitoes and phlebotomine sandflies. The S, M and L segments of CUMV were most closely related to those of Gouleako virus, also from Cote d'Ivoire (amino acid identities = 36%, 38% and 54% respectively). Neither virus produced CPE on vertebrate cells, or illness in newborn mice. Isolation and characterization of these viruses increases our knowledge of the geographic distribution, diversity and host range of mosquito-specific bunyaviruses and negeviruses.
    Journal of General Virology 11/2013; · 3.13 Impact Factor
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    ABSTRACT: Severe fever with thrombocytopenia syndrome virus (SFTSV) is a newly discovered Phlebovirus causing an emerging hemorrhagic fever in East Asia with reported case fatality rates up to 30%. Despite the high case fatality rate and large number of persons at risk of infection, the pathobiology of the disease is unknown, and no effective animal model has been available for investigating the pathogenesis of the disease. We have studied mice and hamsters as potential small animal models of SFTSV infection following subcutaneous, intraperitoneal or intracerebral inoculation. Animal tissues were processed for viral load, histopathology, immunohistochemistry, confocal and electron microscopic studies. We found that immunocompetent adult mice and hamsters did not become ill after SFTSV infection. However, alpha/beta interferon receptor (IFNAR(-/-)) knockout mice were highly susceptible to SFTSV infection, and all mice died within 3-4 days after subcutaneous inoculation of 10(6) ffu of SFTSV. Histologic examination of tissues of IFNAR(-/-)mice infected with SFTSV showed no detectable lesions. In contrast, by immunohistochemistry virus antigen was found in liver, intestine, kidney, spleen, lymphoid tissue, and brain, but not in the lungs. Mesenteric lymph nodes and spleen were the most heavily infected tissues. Quantitative RT-PCR confirmed the presence of virus in these same tissues. Confocal microscopy showed that SFTSV colocalized with reticular cells, but did not colocalize with dendritic cells, monocytes/macrophages, neutrophils or endothelium. Our results indicate that SFTSV multiplied in all organs except for lungs and that mesenteric lymph nodes and spleen were the most heavily infected tissues. The major target cells of SFTSV appear to be reticular cells in lymphoid tissues of intestine and spleen.
    Journal of Virology 11/2013; · 5.08 Impact Factor
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    ABSTRACT: Background. The first comparison of a live RNA virus vaccine to its wild-type parental strain by deep sequencing is presented, using as a model the yellow fever virus (YFV) live vaccine strain 17D-204 and its wild-type parental strain, Asibi.Methods. The YFV 17D-204 vaccine genome was compared to that of the parental strain Asibi by massively parallel methods. Variability was compared on multiple scales of the viral genomes. A modeled exploration of small frequency variants was performed to reconstruct plausible regions of mutational plasticity.Results. Overt quasispecies diversity is a feature of the parental strain, whereas the live vaccine strain by contrast lacks diversity by multiple independent measurements. A lack of attenuating mutations in the Asibi population relative to that of 17D-204 was observed, demonstrating that the vaccine strain was derived by discrete mutation of Asibi and not by selection of genomes in the wild-type population.Conclusions. Relative quasispecies structure is a plausible correlate of attenuation for live viral vaccines. Analyses such as these of attenuated viruses improve our understanding of the molecular basis of vaccine attenuation and provide critical information on the stability of live vaccines and the risk of reversion to virulence.
    The Journal of Infectious Diseases 10/2013; · 5.85 Impact Factor
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    ABSTRACT: Genomic and antigenic characterization of members of the Sandfly fever Naples virus (SFNV) complex reveals the presence of five clades that differ in their geographic distribution. Saint Floris and Gordil viruses, both found in Africa, form one clade; Punique, Granada and Massila viruses, all isolated in the western Mediterranean, constitute a second; Toscana virus, a third; Sandfly fever Naples virus isolates from Italy, Cyprus, Egypt and India form a fourth; while Tehran virus and a Serbian isolate Yu 8/76, represent a fifth. Interestingly, this last clade appears not to express the NSs open reading frame. Karimabad virus, previously classified as a member of the SFNV complex, and Gabek Forest virus are distinct and form a new species complex (named Karimabad) in the Phlebovirus genus. In contrast with the high reassortment frequency observed in some South American phleboviruses, the only virus of the SFNV complex with evidence of reassortment was Granada virus.
    Journal of General Virology 10/2013; · 3.13 Impact Factor
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    ABSTRACT: Kolente virus (KOLEV) is a rhabdovirus originally isolated from ticks and a bat in Guinea, West Africa, in 1985. Although tests at the time of isolation suggested that KOLEV was a novel rhabdovirus, it has remained largely uncharacterized. We assembled the complete genome sequence of the prototype strain DakAr K7292, which was found to encode the five canonical rhabdovirus structural proteins (N, P, M, G and L) with alternative ORFs (> 180 nt) in the P and L genes. Serologically, KOLEV exhibits a weak antigenic relationship with the Barur and Fukuoka viruses in the Kern Canyon group. Phylogenetic analysis revealed that KOLEV represents a distinct and divergent lineage that shows no clear relationship to any rhabdovirus except Oita virus (OITAV), although with limited phylogenetic resolution. In sum, KOLEV represents new species in the family Rhabdoviridae.
    Journal of General Virology 09/2013; · 3.13 Impact Factor
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    ABSTRACT: We investigated the genetics and evolution of West Nile virus (WNV) since initial detection in the United States in 1999 on the basis of continual surveillance studies in the Houston, Texas, USA, metropolitan area (Harris County) as a surrogate model for WNV evolution on a national scale. Full-length genomic sequencing of 14 novel 2010-2012 WNV isolates collected from resident birds in Harris County demonstrates emergence of 4 independent genetic groups distinct from historical strains circulating in the greater Houston region since 2002. Phylogenetic and geospatial analyses of the 2012 WNV isolates indicate closer genetic relationship with 2003-2006 Harris County isolates than more recent 2007-2011 isolates. Inferred monophyletic relationships of these groups with several 2006-2009 northeastern US isolates supports potential introduction of a novel WNV strain in Texas since 2010. These results emphasize the need to maintain WNV surveillance activities to better understand WNV transmission dynamics in the United States.
    Emerging Infectious Diseases 09/2013; 19(9):1418-27. · 6.79 Impact Factor

Publication Stats

7k Citations
1,433.41 Total Impact Points

Institutions

  • 1996–2014
    • University of Texas Medical Branch at Galveston
      • • Department of Pathology
      • • Center for Biodefense and Emerging Infectious Diseases
      • • Center for Tropical Diseases
      Galveston, Texas, United States
  • 2013
    • The Gorgas Memorial Institute for Health Studies (GMI)
      Ciudad de Panamá, Panamá, Panama
    • The Pirbright Institute
      • Vector-borne Viral Diseases (VVD) Programme
      Woking, ENG, United Kingdom
    • Johns Hopkins Bloomberg School of Public Health
      • Department of International Health
      Baltimore, MD, United States
    • United States Army Medical Research Institute for Infectious Diseases
      Maryland, United States
    • University of Pittsburgh
      Pittsburgh, Pennsylvania, United States
  • 2005–2013
    • Columbia University
      • • Center for Infection and Immunity
      • • Department of Epidemiology
      New York City, New York, United States
    • Autonomous University of Nuevo León
      San Nicolás de los Garza, Nuevo León, Mexico
    • University of Queensland
      Brisbane, Queensland, Australia
  • 2012
    • University of Florida
      • Department of Small Animal Clinical Sciences
      Gainesville, FL, United States
  • 2009–2012
    • Washington University in St. Louis
      • Department of Molecular Microbiology
      San Luis, Missouri, United States
    • Institute of Research for Development
      • 190 - Emerging Viral Diseases (EPV)
      Marseille, Provence-Alpes-Cote d'Azur, France
    • Biotechnology and Biological Sciences Research Council
      Swindon, England, United Kingdom
    • University of Washington Seattle
      • Department of Medicine
      Seattle, WA, United States
  • 2011
    • University of Victoria
      • Department of Biochemistry and Microbiology
      Victoria, British Columbia, Canada
  • 2009–2011
    • University of South Florida
      • Department of Global Health
      Tampa, FL, United States
  • 1993–2011
    • Colorado State University
      • • Microbiology, Immunology & Pathology
      • • College of Agricultural Sciences
      Fort Collins, CO, United States
    • Fundação Oswaldo Cruz
      • Departamento de Imunologia
      Rio de Janeiro, Rio de Janeiro, Brazil
  • 1992–2011
    • University of Georgia
      • Southeastern Cooperative Wildlife Disease Study
      Athens, GA, United States
    • University of Maryland, College Park
      • Department of Entomology
      College Park, MD, United States
  • 2010
    • University of Strasbourg
      Strasburg, Alsace, France
    • University of Buea
      • Department of Plant and Animal Science
      Buea, South-West Region, Cameroon
  • 2008
    • New York City Department of Health and Mental Hygiene
      New York, United States
  • 1995–2007
    • Connecticut Agricultural Experiment Station
      New Haven, Connecticut, United States
  • 2006
    • Centers for Disease Control and Prevention
      • Division of Vector-Borne Diseases
      Druid Hills, GA, United States
    • University of Houston
      Houston, Texas, United States
  • 2004–2006
    • Instituto Evandro Chagas
      Ananindeua, Pará, Brazil
    • University of Texas Health Science Center at Houston
      • Center for Infectious Diseases
      Houston, TX, United States
    • Tulane University
      New Orleans, Louisiana, United States
  • 2003
    • University of Rhode Island
      Kingston, Rhode Island, United States
    • Wisconsin National Primate Research Center
      Madison, Wisconsin, United States
  • 1988–2003
    • Yale-New Haven Hospital
      New Haven, Connecticut, United States
  • 1998
    • Instituto Nacional de Higiene "Rafael Rangel"
      Caracas, Distrito Federal, Venezuela
  • 1989–1995
    • University of Alaska Fairbanks
      • Institute of Arctic Biology
      Fairbanks, AK, United States
    • Harvard Medical School
      Boston, Massachusetts, United States
  • 1994
    • Instituto Adolfo Lutz
      San Paulo, São Paulo, Brazil
  • 1991
    • Youngstown State University
      Youngstown, Ohio, United States