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Hantavirus Infection and Habitat Associations among Rodent Populations in Agroecosystems of Panama: Implications for Human Disease Risk

Aníbal G. Armién^*, Blas Armién, Frederick Koster, Juan M. Pascale, Mario Avila, Publio Gonzalez, Manuel de la Cruz, Yamitzel Zaldivar, Yaxelis Mendoza, Fernando Gracia, Brian Hjelle, Sang-Joon Lee, Terry L. Yates, AND Jorge Salazar-Bravo

Hantavirus cardiopulmonary syndrome (HCPS), which is caused by infection with Choclo virus, is uncommon in Panama, yet seropositivity among rural residents is as high as 60%. To clarify the environmental risk factors favoring rodent-to-human transmission, we tested serum from 3,067 rodents captured over a five-year period for antibodies against recombinant N protein of hantavirus by enzyme immunoassay and strip immunoblot. Among 220 seropositive rodents, Oligoryzomys fulvescens, the reservoir of Choclo virus, had the highest overall seroprevalence (23.5%); more abundant rodents (Zygodontomys brevicauda and Sigmodon hirsutus) had lower seroprevalences. In the mixed (combined modern and traditional) productive agroecosystem, the highest seroprevalence was among O. fulvescens captured in residences and in crops grown within 40 meters of a residence, with significantly lower seroprevalence in adjacent pasture and non-productive vegetation. Thus, crop habitats may serve as refugia for invasion into adjacent human residences and suggests several interventions to reduce human infection.

Received December 8, 2007. Accepted for publication March 27, 2009.

Acknowledgments: We thank the International Centers for Infectious Diseases Research (ICIDR) program of the National Institutes of Health, Ministry of Health, the University of New Mexico, the Gorgas Memorial Institute of Studies of Health, the Panamanian Institute of Livestock and Agricultural Research, and the National Environment Authority for their support. We also thank persons from the communities, several state organizations, the rodent ecology team of the Ministry of Health, and especially Dr. Eustiquio Brose, Dr. Carlos Falcon, Omar Vargas, Francisco Crespo, and Nelson Rios for support during fieldwork. The ELISA reagents were provided by Special Pathogens Branch, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention (Atlanta, GA).

We dedicate this paper to the memory of Terry L. Yates

Financial support: This study was supported by an Opportunity Pool award and supplement from the International Centers for Infectious Diseases Research program of the National Institutes of Health (U19-AI 45452); funds from the Instituto Conmemorativo Gorgas de Estudios de la Salud, Hantavirus Research Project No. 04-90-0075-8; the Ministry of Health, Panama; and the Secretaria Nacional de Ciencia y Tecnología, Innovation and Technology Program no. ftd06-089, Panama.

^* Address correspondence to Aníbal G. Armién, Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108. E-mail: armie001{at}umn.edu

Deceased.

Note: Supplemental tables 3 and 4 and supplemental figure 5 appear online at www.ajtmh.org.

Authors’ addresses: Aníbal G. Armién, Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108, E-mail: armie001{at}umn.edu. Blas Armién, Juan M. Pascale, Publio Gonzalez, Manuel de la Cruz, Yamizel Zaldivar, and Yaxelis Mendoza, Instituto Conmemorativo Gorgas de Estudios de la Salud, Avenida Justo Arosemena, Apartado 6991, Zona 5, Panama, E-mail: barmien{at}gorgas.gob.pa. Mario Avila, Instituto Conmemorativo Gorgas de Estudios de la Salud, Avenida Justo Arosemena, Apartado 6991, Zona 5, Panama and Ministry of Health, Herrera Province, Panama. Frederick Koster, Lovelace Respiratory Research Institute, Albuquerque, NM 87108. Fernando Gracia, Hospital Santo Tomas, Panama City, Panama. Brian Hjelle, SOM Pathology Department, 08 4640, University of New Mexico Health Sciences Center, Albuquerque, NM 87131-0001. Sang-Joon Lee, Department of Internal Medicine, MSC 10 555, University of New Mexico Health Sciences Center, Albuquerque, NM 87131-0001. Jorge Salazar-Bravo, Center for Epidemiology and Zoonoses, Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409.

Reprint requests: Blas Armién, Instituto Conmemorativo Gorgas de Estudios de la Salud, Avenida Justo Arosemena, Apartado 6991, Zona 5, Panama, E-mail: barmien{at}gorgas.gob.pa.