Advertisement

EcoHealth

, Volume 16, Issue 3, pp 558–569 | Cite as

Hantavirus Pulmonary Syndrome Risk in Entre Ríos, Argentina

  • María Victoria Vadell
  • Aníbal Eduardo Carbajo
  • Carolina Massa
  • Gerardo Rubén Cueto
  • Isabel Elisa Gómez VillafañeEmail author
Original Contribution
First Online:

Abstract

Hantavirus pulmonary syndrome (HPS) is a severe emerging endemic disease of the Americas. Because hantavirus reservoirs are sylvatic rodents, HPS risk has been associated with occupational and recreational activities in natural and rural environments. The aim of this study was to analyze the risk of HPS in an endemic province of Argentina. For this, we explored the relationship between HPS cases occurring in Entre Ríos province between 2004 and 2015 and climate, vegetation, landscape, reservoir population, and rodent community characteristics by means of generalized linear models. We modeled HPS occurrence at each site, and both the incidence and number of cases grouped by department. The resulting best model of each analysis was applied in a GIS to build HPS risk maps. Risk of occurrence of HPS increased with tree cover and decreased with distance to rivers. We identified the south of Entre Ríos as the area with higher HPS risk, and therefore, where HPS prevention measures should be more urgently applied. Risk maps based on data available in the public domain are a useful tool that should be used by decision makers to concentrate surveillance and control efforts in those areas with highest HPS risk.

Keywords

Hantavirus pulmonary syndrome Disease Epidemiology Risk Zoonosis Public health 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We are thankful to the National Health Ministry of Argentina (Ministerio de Salud de la Nación) for providing the data on confirmed HPS cases and, to the anonymous reviewers for improving the manuscript with their comments and suggestions.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10393_2019_1425_MOESM1_ESM.doc (268 kb)
Supplementary material 1 (DOC 268 kb)
10393_2019_1425_MOESM2_ESM.doc (40 kb)
Supplementary material 2 (DOC 39 kb)

References

  1. Adams MJ, Lefkowitz EJ, King AM, Harrach B, Harrison RL, Knowles NJ, et al. (2017) Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Archives of Virology 162:2505-2538PubMedGoogle Scholar
  2. Amaral CD, Costa GB, de Souza WM, Alves PA, Borges IA, Tolardo AL, et al. (2018) Silent Orthohantavirus circulation among humans and small mammals from Central Minas Gerais, Brazil. EcoHealth 15:577-589PubMedGoogle Scholar
  3. Andreo V, Neteler M, Rocchini D, Provensal C, Levis S, Porcasi X, et al. (2014) Estimating hantavirus risk in Southern Argentina: a GIS-based approach combining human cases and host distribution. Viruses 6:201-222PubMedPubMedCentralGoogle Scholar
  4. Avenant N (2005) Barn owl pellets: a useful tool for monitoring small mammal communities. Belgian Journal of Zoology 135:39-43Google Scholar
  5. Bonvicino CR, Bezerra AMR (2003) Use of regurgitated pellets of barn owl (Tyto alba) for inventorying small mammals in the Cerrado of Central Brazil. Studies on Neotropical Fauna and Environment 38:1-5Google Scholar
  6. Boone JD, Otteson EW, McGwire KC, Villard P, Rowe JE, St Jeor S (1998). Ecology and demographics of hantavirus infections in rodent populations in the Walker River Basin of Nevada and California. The American Journal of Tropical Medicine and Hygiene 59:445-451PubMedGoogle Scholar
  7. Brown JH, Ernest SM (2002) Rain and rodents: complex dynamics of desert consumers. Bioscience 52:979–987Google Scholar
  8. Brown AD, Pacheco S (2006) Propuesta de actualización del mapa ecorregional de la Argentina. Pages 587 In: Brown A, Martinez Ortíz U, Acerbi M, Corcuera J (editors), La situación ambiental argentina, Buenos Aires: Fundación Vida Silvestre ArgentinaGoogle Scholar
  9. Busch M, Kravetz FO (1992) Competitive interactions among rodents (Akodon azarae, Calomys laucha, C. musculinus and Oligoryzomys flavescens) in a two-habitat system. I. Spatial and numerical relationships. Mammalia 56:45-56Google Scholar
  10. Busch M, Alvarez MR, Cittadino EA, Kravetz FO (1997) Habitat selection and interspecific competition in rodents in pampean agroecosystems. Mammalia 1:167-184Google Scholar
  11. Busch M, Cavia R, Carbajo A, Bellomo C, Gonzalez Capria S, Padula P (2004) Spatial and temporal analysis of the distribution of Hantavirus Pulmonary Syndrome (HPS) in Buenos Aires Province, and its relation to rodent distribution, agricultural and demographic variables. Tropical Medicine & International Health 9:508-519Google Scholar
  12. Calisher CH, Root JJ, Mills JN, Beaty BJ (2002) Assessment of ecologic and biologic factors leading to hantavirus pulmonary syndrome, Colorado, USA. Croatian Medical Journal 43:330-337PubMedGoogle Scholar
  13. Carver S, Mills JN, Parmenter CA, Parmenter RR, Richardson KS, Harris RL, et al. (2015). Toward a Mechanistic Understanding of Environmentally Forced Zoonotic Disease Emergence: Sin Nombre Hantavirus. Bioscience 65:651-666PubMedPubMedCentralGoogle Scholar
  14. Carvalho de Oliveira R, Guterres A, Fernandes J, D’Andrea PS, Bonvicino CR, de Lemos ERS (2014a). Hantavirus reservoirs: current status with an emphasis on data from Brazil. Viruses 6:1929-1973PubMedCentralGoogle Scholar
  15. Carvalho de Oliveira R, Gentile R, Guterres A, Fernandes J, Teixeira BR, Vaz V, et al. (2014) Ecological study of hantavirus infection in wild rodents in an endemic area in Brazil. Acta Tropica 131:1-10Google Scholar
  16. Cavia R, Cueto GR, Suárez OV (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landscape and Urban Planning 90:11-19Google Scholar
  17. Crawley MJ (2012) The R book, West Sussex: John Wiley & SonsGoogle Scholar
  18. Colombo VC, Brignone J, Sen C, Previtali MA, Martin ML, Levis S, et al. (2018) Orthohantavirus genotype Lechiguanas in Oligoryzomys nigripes (Rodentia: Cricetidae): new evidence of host-switching. Acta Tropica 191:133-138PubMedGoogle Scholar
  19. de Oliveira SV, Fonseca LX, de Araújo Vilges KM, Maniglia FV, Pereira SV, de Caldas EP, et al. (2015) Vulnerability of Brazilian municipalities to hantavirus infections based on multi-criteria decision analysis. Emerging Themes in Epidemiology 12:1-8.  https://doi.org/10.1186/s12982-015-0036-5 CrossRefGoogle Scholar
  20. Donalisio MR, Peterson AT (2011) Environmental factors affecting transmission risk for hantaviruses in forested portions of southern Brazil. Acta Tropica 119:125-130PubMedGoogle Scholar
  21. Eisen L, Eisen RJ (2007) Need for improved methods to collect and present spatial epidemiologic data for vectorborne diseases. Emerging Infectious Diseases 13:1816-1820PubMedPubMedCentralGoogle Scholar
  22. Engler P, Rodríguez M, Cancio R, Handloser M, Vera L (2008) Zonas Agro Económicas Homogéneas: Entre Ríos. Estudios socioeconómicos de la sustentabilidad de los sistemas de producción y recursos. Instituto Nacional de Tecnología Agropecuaria, Buenos Aires Available: https://inta.gob.ar/sites/default/files/script-tmp-inta_zonas_agroeconmicas_homogneas__entre_rios.pdf [accessed December 12, 2016]
  23. Estrada-Peña A, Ostfeld RS, Peterson AT, Poulin R, de la Fuente J (2014) Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30:205-214PubMedGoogle Scholar
  24. Forbes KM, Sironen T,Plyusnin A (2018). Hantavirus maintenance and transmission in reservoir host populations. Current opinion in virology 28:1-6PubMedGoogle Scholar
  25. Glass GE, Cheek JE, Patz JA, Shields TM, Doyle TJ, Thoroughman DA, et al. (2000) Using remotely sensed data to identify areas at risk for hantavirus pulmonary syndrome. Emerging Infectious Diseases 6:238-247PubMedPubMedCentralGoogle Scholar
  26. Glass GE, Shields T, Cai B, Yates TL, Parmenter R (2007). Persistently highest risk areas for hantavirus pulmonary syndrome: potential sites for refugia. Ecological Applications 17:129-139PubMedGoogle Scholar
  27. Gómez Villafañe IE, Miñarro F, Valenzuela L, Bilenca D (2009) Experimental assessment of rodent control on two poultry farms of central Argentina. Journal of Applied Poultry Research 18:622-629Google Scholar
  28. Gómez Villafañe IE, Expósito Y, San Martín Á, Picca P, Busch M (2012) Rodent diversity and habitat use in a protected area of Buenos Aires province, Argentina. Revista Mexicana de Biodiversidad 83:762-771Google Scholar
  29. Gorosito IL, Douglass RJ (2017) A damped precipitation‐driven, bottom‐up model for deer mouse population abundance in the northwestern United States. Ecology and Evolution 7:11113-11123PubMedPubMedCentralGoogle Scholar
  30. Happold D, Happold M (1986) Small mammals of Zomba Plateau, Malawi, as assessed by their presence in pellets of the grass owl, Tyto capensis, and by live‐trapping. African Journal of Ecology 24:77-87Google Scholar
  31. Heisler LM, Somers CM, Poulin RG (2016) Owl pellets: a more effective alternative to conventional trapping for broad‐scale studies of small mammal communities. Methods in Ecology and Evolution 7:96-103Google Scholar
  32. Hijmans RJ, Cameron S, Parra J, Jones P, Jarvis A, Richardson K (2005) WorldClim version 1. Available:http://www.worldclim.org/version1 [accessed December 1, 2016]
  33. IGN (2013) GIS layers. Available: http://ign.gob.ar/NuestrasActividades//InformacionGeoespacial/CapasSIG [accessed March 2, 2015]
  34. INDEC (Argentina´s National Institute of Statistics and Censuses; 2010) National Census of population, homes and dwellings 2010. Available: http://www.indec.gov.ar [accessed June 6, 2016]
  35. Jahangir E, Irazola V, Rubinstein A (2012) Need, enabling, predisposing, and behavioral determinants of access to preventative care in Argentina: analysis of the national survey of risk factors. PloS One 7:1-6. https://doi.org/10.1371/journal.pone.0045053CrossRefGoogle Scholar
  36. Jonsson CB, Figueiredo LTM, Vapalahti O (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clinical Microbiology Reviews 23:412-441PubMedPubMedCentralGoogle Scholar
  37. Kallio E, Klingstrom J, Gustafsson E, Manni T, Vaheri A, Henttonen H, et al. (2006) Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. Journal of General Virology 87:2127–2134PubMedGoogle Scholar
  38. Kruger DH, Figueiredo LTM, Song J-W, Klempa B (2015) Hantaviruses—Globally emerging pathogens. Journal of Clinical Virology 64:128-136PubMedGoogle Scholar
  39. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159-174Google Scholar
  40. Lovera R, Fernandez SM, Cavia R (2015) Wild small mammals in intensive milk cattle and swine production systems. Agriculture, Ecosystems & Environment 202:251-259Google Scholar
  41. Luis AD, Douglass RJ, Mills JN, Bjørnstad ON (2010). The effect of seasonality, density and climate on the population dynamics of Montana deer mice, important reservoir hosts for Sin Nombre hantavirus. Journal of Animal Ecology 79:462-470PubMedGoogle Scholar
  42. Maroli M, Vadell MV, Iglesias A, Padula PJ, Gómez Villafañe IE (2015) Daily movements and microhabitat selection of hantavirus reservoirs and other sigmodontinae rodent species that inhabit a protected natural area of Argentina. EcoHealth 12:421–431PubMedGoogle Scholar
  43. Maroli M, Vadell MV, Padula P, Gómez Villafañe IE (2018) Rodent Abundance and Hantavirus Infection in Protected Area, East-Central Argentina. Emerging Infectious Diseases 24:131-134PubMedPubMedCentralGoogle Scholar
  44. Martinez VP, Bellomo C, San Juan J, Pinna D, Forlenza R, Elder M, Padula PJ (2005) Person-to-person transmission of Andes virus. Emerging infectious diseases 11:1848-1853PubMedPubMedCentralGoogle Scholar
  45. Martinez VP, Bellomo CM, Cacace ML, Suárez P, Bogni L, Padula PJ (2010) Hantavirus pulmonary syndrome in Argentina, 1995–2008. Emerging Infectious Diseases 16: 1853–1860PubMedPubMedCentralGoogle Scholar
  46. Massa C, Teta P, Cueto GR (2013) Effects of regional context and landscape composition on diversity and composition of small rodent assemblages in Argentinian temperate grasslands and wetlands. Mammalia 78:371-382Google Scholar
  47. Massa C, Gabelli FM, Cueto GR (2015) Using GPS tracking to determine movement patterns and foraging habitat selection of the common barn-owl (Tyto alba). El hornero 30:7-12Google Scholar
  48. Maurice AdS, Ervin E, Schumacher M, Yaglom H, VinHatton E, Melman S, et al. (2017) Exposure characteristics of hantavirus pulmonary syndrome patients, United States, 1993–2015. Emerging Infectious Diseases 23:733-739Google Scholar
  49. Mills JN, Ellis BA, McKee KT, Maiztegui JI, Childs JE (1991) Habitat associations and relative densities of rodent populations in cultivated areas of central Argentina. Journal of Mammalogy 72: 470-479Google Scholar
  50. Mills JN, Amman BR, Glass GE (2010). Ecology of hantaviruses and their hosts in North America. Vector-Borne and Zoonotic Diseases 10:563-574PubMedGoogle Scholar
  51. Moons KG, Kengne AP, Woodward M, Royston P, Vergouwe Y, Altman DG, et al. (2012) Risk prediction models: I. Development, internal validation, and assessing the incremental value of a new (bio) marker. Heart 98:683-690INDEC (National Institute of Statistics and Censuses) 2010)National Census of population, homes and dwellings 2010. Available: http://www.indec.gov.ar [accessed June 6, 2016]
  52. Núñez JJ, Fritz CL, Knust B, Buttke D, Enge B, Novak MG, et al. (2014) Hantavirus infections among overnight visitors to Yosemite National Park, California, USA, 2012. Emerging Infectious Diseases 20:386-393PubMedPubMedCentralGoogle Scholar
  53. Nsoesie EO, Mekaru SR, Ramakrishnan N, Marathe MV, Brownstein JS (2014) Modeling to predict cases of hantavirus pulmonary syndrome in Chile. PLoS Neglected Tropical Diseases 8:1-10. 10.1371/journal.pntd.0002779CrossRefGoogle Scholar
  54. O´Donnell O (2007) Access to health care in developing countries: breaking down demand side barriers. Cadernos Saúde Pública 23:2820-2834Google Scholar
  55. Padula P J, Edelstein A, Miguel SDL, Lopez N M, Rossi CM, Rabinovich RD (1998) Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241: 323-330PubMedGoogle Scholar
  56. Parmenter RR, Brunt JW, Moore DI, Ernest S (1993) The hantavirus epidemic in the southwest: rodent population dynamics and the implications for transmission of hantavirus-associated adult respiratory distress syndrome (HARDS) in the four corners region. Sevilleta LTER report #41 for the Federal Centers for Disease Control and Prevention 1-10Google Scholar
  57. Peters CJ, Khan AS (2002) Hantavirus pulmonary syndrome: the new American hemorrhagic fever. Clinical Infectious Diseases 34:1224-1231PubMedGoogle Scholar
  58. Peters DH, Garg A, Bloom G, Walker DG, Brieger WR, Rahman MH (2008) Poverty and access to health care in developing countries. Annals of the New York Academy of Sciences 1136:161-171PubMedGoogle Scholar
  59. Prist PR, Uriarte M, Tambosi LR, Prado A, Pardini R, Metzger JP (2016) Landscape, environmental and social predictors of Hantavirus risk in São Paulo, Brazil. PLoS ONE 11:1-18. https://doi.org/10.1371/journal.pone.0163459CrossRefGoogle Scholar
  60. Prist PR, D’Andrea PS, Metzger JP (2017). Landscape, climate and hantavirus cardiopulmonary syndrome outbreaks. EcoHealth 14:614-629PubMedGoogle Scholar
  61. R-Core-Team (2013) R: A Language and Environment for Statistical Computing. Vienna. Available at: http://www.r-project.org
  62. Scheibler DR, Christoff AU (2007) Habitat associations of small mammals in southern Brazil and use of regurgitated pellets of birds of prey for inventorying a local fauna Brazilian Journal of Biology 67:619-625Google Scholar
  63. Steyerberg EW, Harrell Jr FE, Borsboom GJ, Eijkemans M, Vergouwe Y, Habbema JDF (2001) Internal validation of predictive models: efficiency of some procedures for logistic regression analysis. Journal of Clinical Epidemiology 54:774-781PubMedGoogle Scholar
  64. Townshend J, Hansen M, Carroll M, DiMiceli C, Sohlberg R, Huang C (2011) User Guide for the MODIS Vegetation Continuous Fields product Collection 5 Version 1. Available:http://glcf.umd.edu/library/guide/VCF_C5_UserGuide_Dec2011.pdf [accessed May 11, 2015]
  65. Udrizar Sauthier WO, Abba AM, Udrizar Sauthier DE (2010) Nests of Oligoryzomys sp. and Holochilus brasiliensis (Rodentia, Cricetidae) in eastern Entre Ríos Province, Argentina. Mastozoología Neotropical 17:207-211Google Scholar
  66. Vadell MV, Bellomo C, San Martín A, Padula P, Gómez Villafañe IE (2011). Hantavirus ecology in rodent populations in three protected areas of Argentina. Tropical Medicine & International Health 16:1342–1352Google Scholar
  67. Vadell MV, García Erize F, Gómez Villafañe IE (2017) Evaluation of habitat requirements of small rodents and effectiveness of an ecologically-based management in a hantavirus-endemic natural protected area in Argentina. Integrative Zoology 12:77–94PubMedGoogle Scholar
  68. Vadell MV, Gómez Villafañe IE (2016). Environmental Variables Associated with Hantavirus Reservoirs and Other Small Rodent Species in Two National Parks in the Paraná Delta, Argentina: Implications for Disease Prevention. EcoHealth 13: 248-260PubMedGoogle Scholar
  69. Verner D (2006) Rural poor in rich rural areas: poverty in rural Argentina. World Bank. Available:http://econ.worldbank.org [accessed January 28, 2017]
  70. Vial PA, Valdivieso F, Mertz G, Castillo C, Belmar E, Delgado I, et al. (2006) Incubation period of hantavirus cardiopulmonary syndrome. Emerging Infectious Diseases 12:1271-1273PubMedPubMedCentralGoogle Scholar
  71. Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, et al. (2002) The ecology and evolutionary history of an emergent disease: Hantavirus Pulmonary Syndrome. Bioscience 52: 989-998Google Scholar
  72. Young JC, Hansen GR, Graves TK, Deasy MP, Humphreys JG, Fritz CL, et al. (2000) The incubation period of hantavirus pulmonary syndrome. The American Journal of Tropical Medicine and Hygiene 62:714-717PubMedGoogle Scholar
  73. Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data, Nueva York: SpringerGoogle Scholar
  74. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1:3-14Google Scholar

Copyright information

© EcoHealth Alliance 2019

Authors and Affiliations

  • María Victoria Vadell
    • 1
    • 2
  • Aníbal Eduardo Carbajo
    • 1
    • 2
  • Carolina Massa
    • 3
  • Gerardo Rubén Cueto
    • 2
    • 3
  • Isabel Elisa Gómez Villafañe
    • 2
    • 3
    Email author
  1. 1.Instituto Nacional de Investigación e Ingeniería AmbientalUniversidad de San MartínSan MartínArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y TécnicasBuenos AiresArgentina
  3. 3.Departamento de Ecología, Genética y Evolución - IEGEBA, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160Buenos AiresArgentina

Personalised recommendations

Cite article

Buy options