Elsevier

Acta Tropica

Volume 131, March 2014, Pages 1-10
Acta Tropica

Ecological study of hantavirus infection in wild rodents in an endemic area in Brazil

https://doi.org/10.1016/j.actatropica.2013.11.016Get rights and content

Highlights

  • Antibody reactivity to hantavirus was detected in five sigmodontine species.

  • Hantavirus prevalence dynamics showed a seasonal pattern with higher prevalence in spring/summer.

  • Rodent species presented different descriptive models of hantavirus infection.

  • Spillover infections on secondary hosts were observed for Juquitiba and Jabora viruses.

  • Bamboo blooming during the studied period may have favored the increases in population sizes.

Abstract

A 3-year ecological study of small mammals was carried out in an endemic area for hantavirus pulmonary syndrome in the state of Santa Catarina in Southern Brazil. A total of 994 rodents of 14 different species corresponding to the subfamilies of Sigmodontinae, Murinae, Eumysopinae, and Caviinae were captured during 2004–2006. Oligoryzomys nigripes and Akodon montensis were the most abundant species and showed a clear seasonal pattern with higher population sizes during the winter. Rodent population outbreaks, associated within bamboo mast seeding events, were detected predominantly in areas where hantavirus pulmonary syndrome cases were notified in the state. Antibody reactivity to Hantavirus was detected in five sigmodontine species: O. nigripes (39/435), A. montensis (15/318), Akodon paranaensis (4/37), Thaptomys nigrita (1/86) and Sooretamys angouya (1/12). The highest hantavirus antibody prevalence occurred during the period of highest population size in A. montensis. For O. nigripes, hantavirus prevalence was higher in late spring, when reproduction was more frequent. Co-circulation of Juquitiba (JUQV) and Jabora (JABV) viruses was observed – JABV in A. paranaensis and A. montensis; JUQV in O. nigripes and T. nigrita. JABV occurrence was associated to gender and population size of the rodent while JUQV was related to gender, season, temperature, and locality.

Graphical abstract

The present paper reports a 3-year population dynamic study of the hantavirus rodents’ reservoirs in an endemic area of hantavirus pulmonary syndrome, Southern Brazil.

  1. Download : Download full-size image

Introduction

The genus Hantavirus (family Bunyaviridae), a group of rodent/insectivore-borne RNA viruses, is widely distributed in the world and includes a variety of strains recognized as human pathogens (Hjelle and Torres-Pérez, 2010, Jonsson et al., 2010, Schmaljohn and Hjelle, 1997). Rodents of the families Muridae and Cricetidae were described as the primary zoonotic reservoirs of these viruses, but distinct hantaviruses have also been discovered in several species of shrews and moles (Arai et al., 2007, Kang et al., 2009, Klempa et al., 2007, Yadav et al., 2007). Transmission is assumed to occur through human inhalation of aerosolized virus from rodents’ urine and/or feces, direct (agonistic encounters), or indirect (contaminated food or environment) contact among rodents (Sauvage et al., 2003).

Hantavirus cardiopulmonary syndrome (HCPS) is considered as one of the major emerging diseases in Brazil, mainly owing to its high mortality rate (∼40%). Since 1993, over 1600 cases of HCPS have been reported and at present, there are eight hantavirus described in Brazil related to Sigmodontinae rodents: Juquitiba/Araucaria, Araraquara, Castelo dos Sonhos, Anajatuba, Laguna Negra, Rio Mearim, Jabora, and Rio Mamore viruses carried by Oligoryzomys nigripes, Necromys lasiurus, Oligoryzomys utiaritensis, Oligoryzomys fornesi, Calomys callidus, Holochilus sciureus, Akodon montensis, and Oligoryzomys microtis, respectively (Oliveira et al., 2011, Firth et al., 2012, Johnson et al., 1999, Raboni et al., 2009, Raboni et al., 2005, Rosa et al., 2005, Suzuki et al., 2004, Travassos Da Rosa et al., 2012, Travassos da Rosa et al., 2011, Travassos da Rosa et al., 2010), the latest three were not described as causing human HCPS.

Outbreaks of different genotypes of Hantavirus in Brazil have often been related to periods of high population sizes of sigmodontine rodents that are commonly associated to agricultural and peridomestic rural environments (Mills and Childs, 1998, Suzuki et al., 2004). These rodents have predominantly granivorous feeding habits and opportunistic reproductive strategies (Gentile et al., 2000). These features allow them to reach high population sizes in certain periods, mainly in productive cropland areas responding quickly to environmental changes. Both the abundance of hantavirus reservoir species and the serostatus within the reservoir population are associated with a suite of biotic and abiotic environmental variables, such as precipitation, habitat quality, and food availability (Mills, 2005).

Ecological studies of hantaviruses are still lacking in Brazil. Little is known about the ecology and temporal dynamics of hantavirus infection in host populations, since most of the studies were punctual in space and time (Oliveira et al., 2009, Raboni et al., 2009, Suzuki et al., 2004, Travassos da Rosa et al., 2010). In the Municipality of Jaborá, an endemic area of HCPS in Southern Brazil, we observed the co-circulation of Juquitiba and Jabora viruses in O. nigripes and A. montensis and recently described the genetic characterization of these two hantaviruses in this region (Oliveira et al., 2011). The present paper reports a population dynamic study of the hantavirus rodents’ reservoirs in this area, investigating the factors related to the hantavirus infection and transmission in the rodent populations during three years.

Section snippets

Study area and sampling

An ecological study of small mammals was carried out in the municipality of Jaborá located in the mid-western region of Santa Catarina State, in Southern Brazil (Fig. 1). Jaborá has 4041 inhabitants (IBGE – Brazilian Institute of Geography and Statistics) and most of them (60.28%) live in rural areas. The economic development of this region is based on farming and cattle raising (agricultural activities). The study area presents a mixed ombrophilous forest that is a vegetation type in the

Population dynamics

From March 2004 to December 2006, we captured 994 individuals of 14 rodent species: A. montensis (n = 323), Akodon paranaensis (n = 39), Brucepattersonius iheringi (n = 18), Delomys dorsalis (n = 1), N. lasiurus (n = 8), Nectomys squamipes (n = 17), O. nigripes (n = 437), Oxymycterus judex (n = 21), Sooretamys angouya (n = 12), Thaptomys nigrita (n = 89) (Rodentia, Sigmodontinae), Mus musculus (n = 15), Rattus rattus (n = 10) (Rodentia, Murinae), Euryzygomatomys spinosus (n = 3) (Rodentia, Echimyidae), Cavia aperea (n = 

Discussion

More than 18 years have passed since HCPS was first described in the American continent. Since then, hantavirus studies, predominantly ecological studies on wild reservoirs, were conducted in many regions (Mills et al., 2010, Palma et al., 2012). In Brazil, most of the studies concerning hantavirus reservoirs were either virus descriptions or short-term local investigations (Oliveira et al., 2009, Raboni et al., 2009, Suzuki et al., 2004, Travassos da Rosa et al., 2010). In this study, we thus

Conflict of interest statement

No competing financial interests exist.

Acknowledgments

We thank the Jaborá Municipal Health Secretary, the Santa Catarina Health Secretary, and the Secretary of Health Surveillance for assistance during the development of our studies in Jaborá. We are grateful to the field team of the Laboratory of Biology and Parasitology of Wild Mammal Reservoirs, IOC/FIOCRUZ, who participated in the Jaborá expeditions. We thank Dr. Helena Bergallo (UERJ/RJ) and Dr. Sotiris Missailidis for time spent on reviewing the manuscript. We thank Raphael Gomes for

References (67)

  • J.E. Childs et al.

    Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States

    J. Infect. Dis.

    (1994)
  • Y.K. Chu et al.

    Sympatry of 2 hantavirus strains, Paraguay, 2003–2007

    Emerg. Infect. Dis.

    (2009)
  • A.P. Dobson et al.

    Microparasites: observed patterns in wild animal populations

  • R.J. Douglass et al.

    Longitudinal studies of Sin Nombre virus in deer mouse-dominated ecosystems of Montana

    Am. J. Trop. Med. Hyg.

    (2001)
  • J.D. Easterbrook et al.

    Immunological mechanisms mediating hantavirus persistence in rodent reservoirs

    PLoS Pathog.

    (2008)
  • D.M. Engelthaler et al.

    Climatic and environmental patterns associated with hantavirus pulmonary syndrome, four corners region, United States

    Emerg. Infect. Dis.

    (1999)
  • C. Firth et al.

    Diversity and distribution of hantaviruses in South America

    J. Virol.

    (2012)
  • W.L. Gannon et al.

    Guidelines of the American society of mammalogists for the use of wild mammals in research

    J. Mammal.

    (2007)
  • R. Gentile et al.

    Population dynamics and reproduction of marsupials and rodents in a Brazilian rural area: a five-year study

    Stud. Neotrop. Fauna Environ.

    (2000)
  • R. Gentile et al.

    Home ranges of Philander frenata and Akodon cursor in a Brazilian restinga (coastal shrubland)

    Mastozool. Neotrop.

    (1997)
  • M. Giovannoni et al.

    Sobre as “ratadas” do primeiro planalto paranaense

    Arq. Biol. Tecnol.

    (1946)
  • D.J. Gubler et al.

    Climate variability and change in the United States: potential impacts on vector- and rodent-borne diseases

    Environ. Health Perspect.

    (2001)
  • B. Hjelle et al.

    Hantaviruses in the Americas and their role as emerging pathogens

    Viruses

    (2010)
  • F.M. Jaksic et al.

    Myths and facts on ratadas: bamboo blooms, rainfall peaks and rodent outbreaks in South America

    Austral Ecol.

    (2003)
  • A.M. Johnson et al.

    Genetic investigation of novel hantaviruses causing fatal HPS in Brazil

    J. Med. Virol.

    (1999)
  • C.B. Jonsson et al.

    A global perspective on hantavirus ecology, epidemiology, and disease

    Clin. Microbiol. Rev.

    (2010)
  • E.R. Kallio et al.

    Hantavirus infections in fluctuating host populations: the role of maternal antibodies

    Proc. R. Soc. B: Biol. Sci.

    (2010)
  • E.R. Kallio et al.

    Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment

    J. Gen. Virol.

    (2006)
  • H.J. Kang et al.

    Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole (Talpa europaea)

    PLoS ONE

    (2009)
  • B. Klempa et al.

    Novel hantavirus sequences in shrew, Guinea

    Emerg. Infect. Dis.

    (2007)
  • E.M. Lehmer et al.

    Differential resource allocation in deer mice exposed to sin nombre virus

    Physiol. Biochem. Zool.

    (2007)
  • N.K. Madhav et al.

    Delayed density-dependent prevalence of Sin Nombre virus antibody in Montana deer mice (Peromyscus maniculatus) and implications for human disease risk

    Vector Borne Zoonotic Dis. (Larchmont, NY)

    (2007)
  • S. Miller et al.

    Guía Para el Reconocimiento de Mamíferos Chilenos

    (1976)
  • Cited by (0)

    View full text