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

Aníbal G. Armién Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Blas Armién Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Frederick Koster Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Juan M. Pascale Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Mario Avila Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Publio Gonzalez Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Manuel de la Cruz Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Yamitzel Zaldivar Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Yaxelis Mendoza Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Fernando Gracia Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Brian Hjelle Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Sang-Joon Lee Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Terry L. Yates Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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Jorge Salazar-Bravo Department of Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minnesota, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama; Ministry of Health, Herrera Province, Panama; Lovelace Respiratory Research Institute, Albuquerque, New Mexico; Hospital Santo Tomas, Panama City, Panama; Department of Pathology, School of Medicine, University of New Mexico, Albuquerque, New Mexico; Division of Epidemiology and Biostatistics, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Center for Epidemiology and Zoonoses, Texas Tech University, Lubbock, Texas

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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.

Author Notes

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