Gerardo Suzán

Bats are a major natural reservoir for hepaciviruses and pegiviruses

Although there are over 1,150 bat species worldwide, the diversity of viruses harbored by bats has only recently come into focus as a result of expanded wildlife surveillance. Such surveys are of importance in determining the potential for novel viruses to emerge in humans, and for optimal management of bats and their habitats. To enhance our knowledge of the viral diversity present in bats, we initially surveyed 415 sera from African and Central American bats. Unbiased high-throughput sequencing revealed the presence of a highly diverse group of bat-derived viruses related to hepaciviruses and pegiviruses within the family Flaviridae. Subsequent PCR screening of 1,258 bat specimens collected worldwide indicated the presence of these viruses also in North America and Asia. A total of 83 bat-derived viruses were identified, representing an infection rate of nearly 5%. Evolutionary analyses revealed that all known hepaciviruses and pegiviruses, including those previously documented in humans and other primates, fall within the phylogenetic diversity of the bat-derived viruses described here. The prevalence, unprecedented viral biodiversity, phylogenetic divergence, and worldwide distribution of the bat-derived viruses suggest that bats are a major and ancient natural reservoir for both hepaciviruses and pegiviruses and provide insights into the evolutionary history of hepatitis C virus and the human GB viruses.

Experimental Evidence for Reduced Rodent Diversity Causing Increased Hantavirus Prevalence

Emerging and re-emerging infectious diseases have become a major global environmental problem with important public health, economic, and political consequences. The etiologic agents of most emerging infectious diseases are zoonotic, and anthropogenic environmental changes that affect wildlife communities are increasingly implicated in disease emergence and spread. Although increased disease incidence has been correlated with biodiversity loss for several zoonoses, experimental tests in these systems are lacking. We manipulated small-mammal biodiversity by removing non-reservoir species in replicated field plots in Panama, where zoonotic hantaviruses are endemic. Both infection prevalence of hantaviruses in wild reservoir (rodent) populations and reservoir population density increased where small-mammal species diversity was reduced. Regardless of other variables that affect the prevalence of directly transmitted infections in natural communities, high biodiversity is important in reducing transmission of zoonotic pathogens among wildlife hosts. Our results have wide applications in both conservation biology and infectious disease management.

Coronaviruses in bats from Mexico

Bats are reservoirs for a wide range of human pathogens including Nipah, Hendra, rabies, Ebola, Marburg and severe acute respiratory syndrome coronavirus (CoV). The recent implication of a novel beta (β)-CoV as the cause of fatal respiratory disease in the Middle East emphasizes the importance of surveillance for CoVs that have potential to move from bats into the human population. In a screen of 606 bats from 42 different species in Campeche, Chiapas and Mexico City we identified 13 distinct CoVs. Nine were alpha (α)-CoVs; four were β-CoVs. Twelve were novel. Analyses of these viruses in the context of their hosts and ecological habitat indicated that host species is a strong selective driver in CoV evolution, even in allopatric populations separated by significant geographical distance; and that a single species/genus of bat can contain multiple CoVs. A β-CoV with 96.5 % amino acid identity to the β-CoV associated with human disease in the Middle East was found in a Nyctinomops laticaudatus bat, suggesting that efforts to identify the viral reservoir should include surveillance of the bat families Molossidae/Vespertilionidae, or the closely related Nycteridae/Emballonuridae. While it is important to investigate unknown viral diversity in bats, it is also important to remember that the majority of viruses they carry will not pose any clinical risk, and bats should not be stigmatized ubiquitously as significant threats to public health.

Epidemiological considerations of rodent community composition in fragmented landscapes in Panama

Abstract We predicted that more-fragmented habitats are associated with lower diversity of small mammals and higher densities of populations of rodents that are hosts of hantaviruses. We compared diversity and distribution of small mammals that are either hosts or nonhosts of hantaviruses in 6 Panamanian national parks and adjacent areas with varying degree of human impacts. We sampled forest, edge, and anthropogenically disturbed habitats. The generalist rodents Oligoryzomys fulvescens (reservoir of Choclo virus) and Zygodontomys brevicauda (reservoir of Calabazo virus) were more abundant in disturbed habitats, especially in smaller and more isolated patches, where population density and diversity of other rodent species was lowest. In contrast, these 2 species had lower abundances in larger forested areas with more nonreservoir species of small mammals. Our results suggest that the change in the natural environment resulting from tropical deforestation is increasing the abundance and distribution of species that are reservoirs for hantaviruses. Therefore, it is likely that forest fragmentation has contributed to recent outbreaks of hantavirus pulmonary syndrome in tropical areas. Conservation of natural resources becomes all the more imperative, not only for protecting fauna and flora but also for human health.

The Effect of Habitat Fragmentation and Species Diversity Loss on Hantavirus Prevalence in Panama

Habitat fragmentation and diversity loss due to increased conversion of natural habitats to agricultural uses influence the distribution and abundance of wildlife species and thus may change the ecology of pathogen transmission. We used hantaviruses in Panama as a research model to determine whether anthropogenic environmental change is associated with changes in the dynamics of viral transmission. Specifically, we wanted to determine whether hantavirus infection was correlated with spatial attributes of the landscape at both large and small scales or whether these changes are mediated by changes in community composition. When analyzed at coarse spatial scales, hantavirus reservoirs were more commonly found in disturbed habitats and edge habitats than in forested areas. At local scales, reservoir species dominance was significantly correlated with the slope of the terrain. To evaluate the effect of small‐mammal diversity loss on infection dynamics, we implemented an experiment with selective species removal at experimental sites. Seroprevalence of hantavirus was higher in the community of small mammals and increased through time in the experimental sites. The higher seroprevalence in experimental plots suggests that greater diversity likely reduces encounter rates between infected and susceptible hosts. Our studies suggest that habitat loss and fragmentation and species diversity loss are altering hantavirus infection dynamics in Panama. Our work represents a multidisciplinary approach toward disease research that includes biodiversity concerns such as environmental change and degradation, human settlement patterns, and the ecology of host and nonhost species, work that may be especially important in tropical countries.

Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space

The potential for disease transmission at the interface of wildlife, domestic animals and humans has become a major concern for public health and conservation biology. Research in this subject is commonly conducted at local scales while the regional context is neglected. We argue that prevalence of infection at local and regional levels is influenced by three mechanisms occurring at the landscape level in a metacommunity context. First, (1) dispersal, colonization, and extinction of pathogens, reservoir or vector hosts, and nonreservoir hosts, may be due to stochastic and niche-based processes, thus determining distribution of all species, and then their potential interactions, across local communities (metacommunity structure). Second, (2) anthropogenic processes may drive environmental filtering of hosts, nonhosts, and pathogens. Finally, (3) phylogenetic diversity relative to reservoir or vector host(s), within and between local communities may facilitate pathogen persistence and circulation. Using a metacommunity approach, public heath scientists may better evaluate the factors that predispose certain times and places for the origin and emergence of infectious diseases. The multidisciplinary approach we describe fits within a comprehensive One Health and Ecohealth framework addressing zoonotic infectious disease outbreaks and their relationship to their hosts, other animals, humans, and the environment.

Serologic Evidence of Hantavirus Infection in Sigmodontine Rodents in Mexico

Antibodies to hantaviruses in two species of sigmodontine rodents (Peromyscus maniculatus and Reithrodontomys sumichrasti) collected in central Mexico are reported. Peromyscus maniculatus, a common species throughout much of Mexico, is the reservoir of Sin Nombre virus (SNV), the etiologic agent of the great majority of cases of hantavirus pulmonary syndrome (HPS) in North America. Although the identity of the virus detected in P. maniculatus in Mexico could not be determined by these serologic results, our findings suggest that SNV may occur throughout the range of P. maniculatus in North America. If true, the failure to identify HPS in Mexico is not due to the absence of pathogenic hantaviruses in Mexico.

Serosurvey of Wild Rodents for Hantaviruses in Panama, 2000–2002

Five hundred fifty-six samples representing 24 species of small mammals (two species of marsupials and 22 rodents) were collected in Panama between February 2000 and July 2002. The samples were examined for antibodies to hantaviruses by means of enzyme-linked immunosorbent assay or immunoblot assays. The serologic results indicated that several rodent species might act as hantaviral reservoirs in Panama: Costa Rican pygmy rice rat (Oligoryzomys fulvescens costaricensis), four positive of 72 tested (5.6%); Cherries cane rat (Zygodontomys brevicauda cherriei), five of 108 (4.6%); Mexican deer mouse (Peromyscus mexicanus), one of 22 (5%); Mexican harvest mouse (Reithrodontomys mexicanus), one of seven (14%); Chiriquí harvest mouse (Reithrodontomys creper), one of two (50%); and Sumichrasts harvest mouse (Reithrodontomys sumichrasti), three of four (75%). Hantavirus infection in Peromyscus mexicanus and the three species of Reithrodontomys was caused by Rio Segundo hantavirus, a species of virus not previously reported from Panama. At least three hantaviruses, therefore, are known to infect populations of wild rodents in the country. However, given the total number of animals tested, the role of these rodent species in the epidemiology and epizootiology of hantavirus infections remains unclear.

Dengue virus in bats from southeastern Mexico.

To identify the relationship between landscape use and dengue virus (DENV) occurrence in bats, we investigated the presence of DENV from anthropogenically changed and unaltered landscapes in two Biosphere Reserves: Calakmul (Campeche) and Montes Azules (Chiapas) in southern Mexico. Spleen samples of 146 bats, belonging to 16 species, were tested for four DENV serotypes with standard reverse transcriptase polymerase chain reaction (RT-PCR) protocols. Six bats (4.1%) tested positive for DENV-2: four bats in Calakmul (two Glossophaga soricina, one Artibeus jamaicensis, and one A. lituratus) and two bats in Montes Azules (both A. lituratus). No effect of anthropogenic disturbance on the occurrence of DENV was detected; however, all three RT-PCR-positive bat species are considered abundant species in the Neotropics and well-adapted to disturbed habitats. To our knowledge, this study is the first study conducted in southeastern Mexico to identify DENV-2 in bats by a widely accepted RT-PCR protocol. The role that bats play on DENVs ecology remains undetermined.

Survey for antibody to hantaviruses in Tamaulipas, Mexico.

Wild rodents (n=248) were trapped in two ecologically distinct sites at El Cielo Biosphere Reserve in the state of Tamaulipas, Mexico, during the summer of 2003. Samples from 199 individuals were tested for Hantavirus antibodies by an indirect enzyme-linked immunosorbent assay (ELISA). Hantavirus antibodies to recombinant Sin Nombre virus nucleocapsid protein were found in seven rodents (3.5%) of a single species, Peromyscus levipes. Antibody-positive rodents were found only in the Cloud Forest site, which had lower rodent species diversity than the Tropical Subdecidous Forest site. Although the identity of the virus in P. levipes remains to be determined, our study provides further evidence that Hantavirus antibody–positive individuals are prevalent in the rodent fauna of Mexico. This is the first survey for Hantavirus antibodies in the rodent fauna of Tamaulipas and the first report of P. levipes as a potential host for a Hantavirus.