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    Sampling sites along the study area in Chile (numbers are as in Table 1).

  • 1

    Schmaljohn C, Hjelle B, 1997. Hantaviruses: a global disease problem. Emerg Infect Dis 3 :95–104.

  • 2

    Hart C, Bennet M, 1999. Hantavirus infections: epidemiology and pathogenesis. Microbes Infect 1 :1229–1237.

  • 3

    Duchin JS, Koster FT, Peters CJ, Simpson GL, Tempest B, Zaki SR, Ksiazek TG, Rollin PE, Nichol S, Umland ET, Moolenaar RL, Reef SE, Nolte KB, Gallaher MM, Butler JC, Breiman RF, 1994. Hantavirus pulmonary syndrome: A clinical description of 17 patients with a newly recognized disease. N Engl J Med 330 :949–955.

    • Search Google Scholar
    • Export Citation
  • 4

    Mills J, Childs J, 1998. Ecological studies of rodents reservoirs: their relevance for human health. Emerg Infect Dis 4 :529–537.

  • 5

    Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, Calisher CH, Nichol ST, Abbot KD, Young JC, Morrison ML, Baety BJ, Dunnum JL, Baker RJ, Salazar-Bravo J, Peters CJ, 2002. The ecology and evolutionary history of an emergent disease: hantavirus pulmonary syndrome. BioScience 52 :989–998.

    • Search Google Scholar
    • Export Citation
  • 6

    Lee H, van der Groen G, 1989. Hemorrhagic fever with renal syndrome. Prog Med Virol 36 :62–102.

  • 7

    Botten J, Mirowsky K, Ye C, Gottlieb K, Saavedra M, Ponce L, Hjelle B, 2002. Shedding and intercage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 7 :7587–7594.

    • Search Google Scholar
    • Export Citation
  • 8

    Baró M, Vergara J, Navarrete M, 1999. Hantavirus en Chile: revisión y análisis de casos desde 1975. Rev Med Chil 127 :1513–1523.

  • 9

    Sportorno A, Palma R, Valladares J, 2000. Biología de roedores reservorios de hantavirus en Chile. Rev Chil Infect 17 :197–210.

  • 10

    Pavletic C, 2000. Hantavirus: Su distribución geográfica entre los roedores silvestres de Chile. Rev Chil Infect 17 :186–196.

  • 11

    Levis S, Morzunov S, Rowe J, Enria D, Pini N, Calderon G, Sabattini M, St Jeor SC, 1998. Genetic diversity and epidemiology of hantaviruses in Argentina. J Infect Dis 177 :529–538.

    • Search Google Scholar
    • Export Citation
  • 12

    Mann G, 1978. Los pequeños mamíferos de Chile. Gayana Zool 40 :1–342.

  • 13

    Gallardo M, Palma R, 1990. Systematics of Oryzomys longicaudatus (Rodentia, Muridae) in Chile. J Mammal 71 :333–342.

  • 14

    Murúa R, Gonzáles L, Meserve P, 1986. Population ecology of Oryzomys longicaudatus Philippi (Rodentia: Cricetidae) in southern Chile. J Anim Ecol 55 :281–293.

    • Search Google Scholar
    • Export Citation
  • 15

    Kelt D, 1994. The natural history of small mammals from Aysén Region, southern Chile. Rev Chil Hist Nat 67 :183–207.

  • 16

    Mackelprang R, Dearing D, Jeor S, 2001. High prevalence of Sin Nombre virus in rodent populations, central Utah: A consequence of human disturbance? Emerg Infect Dis 7 :480–481.

    • Search Google Scholar
    • Export Citation
  • 17

    Simonetti J, Agüero T, 1990. Assessing independence of animal movements: spatio-temporal variability in Oryzomys longicaudatus.Mammalia 54 :316–319.

    • Search Google Scholar
    • Export Citation
  • 18

    Calderón G, Pini N, Bolpe J, Levis S, Mills J, Segura E, Guthmann N, Cantoni G, Becker J, Fonollat A, Ripio C, Bortman M, Benedetti R, Sabattini M, Enria D, 1999. Hantavirus reservoir host associated with peridomestic habitats in Argentina. Emerg Infect Dis 5 :792–797.

    • Search Google Scholar
    • Export Citation
  • 19

    Mills J, Childs J, Ksiazek T, Peters C, Velleca W, 1995. Methods for Trapping and Sampling Small Mammals for Virologic Testing. Atlanta, GA: United States Department of Health and Human Services.

  • 20

    Yee J, Wortman IA, Nofchissey R, Bennett SG, Webb JP, Irwin W, Hjelle B, 2003. Rapid and simple method for screening wild rodents for antibodies to Sin Nombre hantavirus. J Wildl Dis 39 :271–277.

    • Search Google Scholar
    • Export Citation
  • 21

    Cantoni G, Padula P, Calderon G, Mills J, Herrero E, Sandoval P, Martínez V, Pini N, Larrieu E, 2001. Seasonal variation in prevalence of antibody to hantaviruses in rodents from southern Argentina. Trop Med Int Health 6 :811–816.

    • Search Google Scholar
    • Export Citation
  • 22

    Yahnke CJ, Meserve PL, Ksiazek TG, Mills JN, 2001. Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan chaco. Am J Trop Med Hyg 65 :768–776.

    • Search Google Scholar
    • Export Citation
  • 23

    Williams RJ, Bryan RT, Mills JN, Palma RE, Vera I, de Velásquez F, Baez E, Schmidt WE, Figueroa RE, Peters CJ, Zaki SR, Khan AS, Ksiazek TG, 1997. An outbreak of hantavirus pulmonary syndrome in western Paraguay. Am J Trop Med Hyg 57 :274–282.

    • Search Google Scholar
    • Export Citation
  • 24

    Toro J, Vega JD, Khan AS, Mills JN, Padula P, Terry W, Yadón Z, Valderrama R, Ellis BA, Pavletic C, Cerda R, Zaki S, Wun-Ju S, Meyer R, Tapia M, Mansilla C, Baro M, Vergara JA, Concha M, Calderon G, Enria D, Peters CJ, Ksiazek TG, 1998. An outbreak of hantavirus pulmonary syndrome, Chile, 1997. Emerg Infect Dis 4 :687–694.

    • Search Google Scholar
    • Export Citation
  • 25

    Redford KH, Eisenberg JF, 1992. Mammals of the Neotropics. The Southern Cone. Chicago: The University Chicago Press.

  • 26

    Padula PJ, Colavecchia SB, Martínez VP, Gonzales MO, Eldelstein A, Miguel DL, Russi J, Mora-Riquelme J, Colucci N, Almirón M, Rabinovich RD, 2000. Genetic diversity, distribution, and serological features of hantavirus infection in five countries in South America. J Clin Microbiol 38 :3029–3035.

    • Search Google Scholar
    • Export Citation
  • 27

    Padula PJ, Sánchez AJ, Edelstein A, Nichol ST, 2002. Complete nucleotide sequence of the M RNA segment of Andes virus and analysis of the variability of the termini of the virus S, M and L RNA segments. J Gen Virol 83 :2117–2122.

    • Search Google Scholar
    • Export Citation
  • 28

    Bohlman MC, Morzunov SP, Meissner J, Beth-Taylor M, Ishibashi K, Rowe J, Levis S, Enria D, St. Jeor SC, 2002. Analysis of hantavirus genetic diversity in Argentina: S segment- derived phylogeny. J Virol 76 :3765–3773.

    • Search Google Scholar
    • Export Citation
  • 29

    Sotomayor V, Aguilera X, 2000. Epidemiología de la infección humana por hantavirus en Chile. Rev Chil Infect 17 :220–232.

  • 30

    Krüger D, Ulrich R, Lundkvist A, 2001. Hantavirus infections and their prevention. Microbes Infect 3 :1129–1144.

 
 
 

 

 
 
 

 

 

 

 

 

 

PERIDOMESTIC SMALL MAMMALS ASSOCIATED WITH CONFIRMED CASES OF HUMAN HANTAVIRUS DISEASE IN SOUTHCENTRAL CHILE

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  • 1 Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile; Centro de Estudios Médicos, Departamento de Enfermedades Infecciosas, Pontificia Universidad Católica de Chile, Santiago, Chile; Centro de Estudios Avanzados en Ecología y Biodiversidad, Pontificia Universidad Católica de Chile, Santiago, Chile; Department of Biology, Museum of Southwestern Biology, and Division of Infectious Diseases, Department of Internal Medicine, University of New Mexico, Albuquerque, New Mexico; Facultad de Ciencias de la Salud, Universidad del Desarrollo, Santiago, Chile

Cases of human hantavirus disease have been reported in Chile since 1995, most of them in people living in rural and periurban areas. We conducted a peridomestic study of small mammals to evaluate the relationships between the presence of rodents with antibodies to Andes virus confirmed human cases of hantavirus pulmonary syndrome in southcentral Chile. The results of 20 sampled sites, which involved the capture of 272 mice over an 18-month period, showed the occurrence of 10 small mammal species, of which Oligoryzomys longicaudatus was the only seropositive species for hantavirus, with an intra-specific serologic rate of 10.4%.

INTRODUCTION

Human diseases caused by hantaviruses (genus Hantavirus, family Bunyaviridae) have been reported in several countries.1,2 In the Americas, this disease is known as hantavirus pulmonary syndrome (HPS)3 and is one of the most dangerous emerging infectious diseases.4 Several rodent species in the Americas constitute the reservoir for distinctive strains of Hantavirus with high levels of species-specificity among them.1,5 The disease is transmitted to humans by inhalation of virus-contaminated aerosols of rodent excreta6 and secretions.7

The first case of HPS reported in Chile was in 1995, although it has been retrospectively reported in 1975.8 To date, five rodents species of the subfamily Sigmodontinae (Muridae) have been identified to be serologically positive for hantavirus in Chile.9,10 Among them, the species Oligoryzomys longicaudatus, the colilargo (tribe Oryzomyni), is one of the major reservoirs for the virus.11 Other sigmodontines that have been found to be positive for the virus in Chile (although at a considerably lower rate) are Abrothrix longipilis (ratón de pelo largo), Abrothrix olivaceus (ratón oliváceo), Phyllotis darwini (ratón orejudo), and Loxodontomys micropus (pericote del sur).9 All of these species have an extensive range of distribution in Chile.12 In fact, O. longicaudatus ranges from Copiapó (28°S) southward to Aysén (48°S), as well as to the southern Patagonian forests of Argentina.13 This species is mainly restricted to forests and bushy areas, showing a preference for humid habitats near rivers and other water sources.14,15 A second species, O. magellanicus, inhabits the forests of region XII.13 However, neither human cases nor seropositive O. magellanicus have been reported in region XII. The other taxa, A. longipilis and A. olivaceus, coexist with O. longicaudatus along most of its distributional range.

The first confirmed human case of HPS reported in Chile was in Llanquihue Province (X region) in 1995. Since then, several other cases have been confirmed along the geographic range of O. longicaudatus. One possible explanation for this emerging disease has been the settlement of human populations in periurban and rural areas near the habitats where wild rodents occur, which would facilitate the exposure of human populations.16 For this reason, rural (inhabiting in the countryside outside cities and towns) and periurban (around villages and towns) human populations are usually considered to be at higher risk of acquiring the disease than people living in cities. In addition, the large home range (320–4,800 m2) and high mobility reported for O. longicaudatus in populations of southern Chile14 increase the probability of contact between wild rodents and people, particularly in rural areas. However, a more restricted home range and mobility has been reported for colilargo populations in central Chile.17

To evaluate the relationships between confirmed cases of HPS and the occurrence of seropositive rodents, we conducted a survey in periurban and rural areas of southcentral Chile to determine which species are involved in the disease. To date, O. longicaudatus has been reported as the sole reservoir for Andes virus in Chile, and no information has been obtained about the participation of others sigmodontine species in the transmission of the disease. In addition, we report the type of human activity that people were conducting at the moment of contracting the disease, as well as the site category and the type of habitat where the cases were confirmed.

MATERIALS AND METHODS

Study area.

Peridomestic trapping was conducted in collaboration with the Ministry of Health. Immediately after serologic confirmation of HPS, Ministry of Health staff interviewed the index case and family members to identify all potential exposure sites where the HPS patient had been in the 45 days prior to symptom onset. In each case, we contacted the local Health Service representative to determine the exact location for small mammal sampling. Trapping was then initiated at all potential exposure sites. Most of the sites sampled were located between regions V and X in Chile (Figure 1) where two ecogeographic zones meet (the Mediterranean and the Temperate Forests regions), and where approximately two-thirds of the Chilean population is concentrated. Infectious sites were defined as periurban and rural as previously described,18 with modifications.

We defined periurban as those areas located between 500 and 3,000 meters from a small town or city (5,000 or more inhabitants). Rural sites are defined as areas that might be close to (approximately 500–1,000 meters) a small village (up to 5,000 habitants) or in the countryside. Periurban sites included yards, adjoining lands, outbuildings, weeds, ponds, modified lands, natural understories, cultivated areas, and fence lines. Rural sites included the countryside such as cultivated areas, ponds, natural or planted forests, modified lands, natural understories, bamboo (e.g., Chusquea sp.), ravines, camping sites, outbuildings, and weeds (Table 1). We also described the most probable kind of human activity that people were conducting when exposed to the virus. We classified these as farmers, resident people (people that live in the area of exposure), and visitors (persons who do not live or work in the area of exposure; e.g., camping, trekking, etc).

Trapping.

Between July 2001 and December 2002 we visited 20 sites (Table 1) where confirmed cases of hantavirus disease were reported. All sampled sites were located between regions V and X (32–42°S) classified in four periurban and 16 rural sites (Figure 1 and Table 1). Trapping was conducted using Sherman traps (8 × 9 × 23 cm; H. B. Sherman Traps, Inc., Tallahassee, FL) for three nights at each site (trappings varied between 225 and 771 traps/night depending on the availability of sites in the area) and the bait used was a mixture of oats and tinned fish. When trapping locations included human buildings (e.g., houses, sheds), traps were set around and below them (when possible). In 11 of the 20 sites studied traps were set around houses and immediate vicinities since not all sites included human constructions. Immediate vicinities are defined as grassy areas, timber, and/or log piles, crops, etc. The number of traps set around houses varied depending on the area of the same, but the numbers varied between 10 and 15 traps. Additional trapping places involved sites far from human buildings where local people previously detected rodents. We followed established safety guidelines for rodent captures and processing according to the Center for Disease Control and Prevention (Atlanta, GA) protocols.19 Animals in the field were anesthetized and blood was drawn from the retro-orbital sinus for further serologic analyses. Blood samples were preserved in liquid nitrogen and brought to the laboratory for analysis. Specimens were identified in the field with further taxonomic confirmation in the laboratory at the species level. In addition, for each specimen the heart, kidney, spleen, liver, and lung were extracted, and stored in liquid nitrogen for further virus detection. Voucher specimens were preserved in 96% ethanol, and deposited in the Colección de Flora y Fauna, Professor Patricio Sánchez Reyes, Pontificia Universidad Católica de Chile (Santiago, Chile) and in the Division of Mammals of the Museum of Southwestern Biology, University of New Mexico (Albuquerque, NM). We evaluated small mammals captures by calculating the relative density, calculated as the number of captures/number of total traps × 100.

Serologic test.

Serologic analyses were performed on all rodent samples. All analyses were performed in the Centro de Investigaciones Médicas, Pontificia Universidad Católica de Chile (Santiago, Chile). Antibodies against Andes virus were detected in blood samples using the strip immunoassay vacuum-blot test.20 Briefly, 5 μL of rodent blood was used to probe a 1.6 × 5-cm nitrocellulose membrane bearing a horizontal ~0.5-mm × 1.6-mm band containing approximately 300 ng of affinity-purified recombinant Andes virus N antigen overnight at room temperature in a volume of 1 mL. After washes in detergent buffer, any bound antibodies to N antigen were detected by incubating the membrane with a 1:1,000 dilution of alkaline phosphatase-conjugated deer mouse anti-Peromyscus leucopus IgG and revealed with the 5-bromo, 4-chloro, 3-indolylphosphate/nitroblue tetrazolium (BCIP/ NBT) phosphatase substrate system (Kirkegaard and Perry Laboratories, Gaithersburg, MD).

RESULTS

In the 18-month study period, 82 human cases were confirmed as positive for HPS in the regions mentioned earlier (information available from the web page of Ministerio de Salud de Chile, http//:epi.minsal.cl). Sampling was conducted in the southcentral area of Chile as human cases were arising. However, in several cases human disease reports occurred almost simultaneously, making it difficult to sample all localities at the same time by a single field team. When more than one case was reported simultaneously, we chose that site that involved more people with the disease. Additionally, we selected localities that were not sampled previously. Of the 20 selected sites, six were located in region V, three in region VI, five in region VII, two in region VIII, one in region IX, two in region X, and one in the Metropolitan region (Santiago). We characterized 16 rural and 4 periurban sites (Figure 1 and Table 1). Oligoryzomys longicaudatus was captured both in periurban and rural sites. Fourteen habitat types were characterized in the sampled areas, including natural forests, cultivated areas, and weeds. The latter was the most prevalent type of habitat, while fence lines and planted forests were the least represented (Table 1). Of the three types of human activities described earlier, 10 cases were farm workers, seven were residents, and five were visitors.

We trapped nine species of rodents and one mouse-opossum of the following species: Sigmodontinae: O. longicaudatus, A. olivaceus, A. longipilis, Abrothrix sanborni, P. darwini, L. micropus; Murinae: Rattus norvegicus, Rattus rattus, Mus musculus; Didelphimorphia: Thylamys elegans. All localities sampled had at least one species that had been reported serologically positive for hantavirus either in this or other studies.9,10 We captured 272 specimens of these 10 species. Nine of the 11 sites where traps were set around houses recorded sigmodontine and murine mice. The species trapped around human buildings were O. longicaudatus, A. olivaceus, and the three murine rodents. Forty-five mice were trapped around houses (of a whole total of 272 specimens), of which 21 were murines, 21 A. olivaceus, and 4 O. longicaudatus. Of these, only one specimen was seropositive for Andes virus (O. longicaudatus); this was from the locality of Longaví (region VII).

Abrothrix olivaceus was the species most frequently trapped (127 individuals, 46.7%), being collected in 18 of the 20 sites, and absent only in the localities of Hijuelas II and San Antonio (both in the V region). The colilargo O. longicaudatus, was found in 14 localities and was the second most frequently captured species (48 individuals, 17.65%). The sigmodontine A. sanborni was the least captured species, being trapped only in Lago Ranco (X Region). The sites of Quillón and Puerto Montt showed the highest species richness (five species), while Lago Ranco and Puerto Montt showed the highest abundance of sigmodontine mice with four species.

Relative density (Table 1) of sigmodontine rodents ranged between 0.1 (L. micropus) to 7.0 (A. olivaceus). Among murine rodents these values ranged between 0.1 (R. rattus) and 2.5 (M. musculus). The highest relative density for O. longicaudatus was in Lago Ranco (3.3). Among sites, the highest mean relative densities were in Tucapel (11.7) and Santo Domingo (11.3), while the lowest density was in San Fernando (1.12).

Five O. longicaudatus were positive for antibodies to Andes virus (seroprevalence rate of 1.87%). All seropositive colilargos were adult males. There was one seropositive mouse in Coya (region VI), one in San Fernando (region VI), and one in Longaví (region VII), and there were two seropositive mice in Tucapel (region VIII).

DISCUSSION

The seroprevalence rate of 1.87% in our study contrasts with other serologic reports in South America, which have shown higher rates (3–7%).10,18,21 Indeed, when these studies considered only sigmodontine rodents, seropositive rates increased to between 3% and 11%.10,18,22–24 When we considered only sigmodontine mice, our rate increased to 2.36%. This rate is similar to that of 2.28% obtained in an ongoing latitudinal study in Chile, which involves a great variety of wild and semi-undisturbed areas, as well as a high trapping density (Palma RE and others, unpublished data). A probable explanation for the lower rate obtained in Chile compared with that of Argentina may be the higher diversity of sigmodontine mice recognized in Argentina.25 The latter rate may increase the probability of potential reservoirs. In fact, several genetic variants26,27 or hantavirus strains28 have been described in Argentina in five species of rodents, with four pathogenic for humans.

Trapping mice success (and serologic results) in our study was related to the type of areas sampled. In fact, there was a high degree of human intervention at many of the sites, particularly those in periurban areas, including poisoning of rodents prior to trapping, manipulation of traps by local residents, and loss of traps. However, the low number of rodents captured and the relative frequencies of trap success were similar to that in other studies that have involved peridomestic studies.18

Seropositive rodents were found mostly in rural sites, which were areas of highest risk in which people could get the disease, thus supporting results of previous studies.10 Four of the 20 sampling sites had O. longicaudatus positive for Andes virus, representing a 20% success rate in detecting seropositive mice in areas where transmission presumptively occurred. In addition, mice were most likely to be found in areas with the presence of weeds (18 sites), cultivated areas (10 sites), and natural understory or forests (7 sites), which are widely developed in the Mediterranean region in Chile. Houses and other human buildings also constituted areas of high risk since a significant number of sigmodontine mice were trapped around them and/or in their vicinities. Interestingly, of the four colilargos trapped in this kind of area, one was seropositive for hantavirus. With respect to human infection, farm workers were a higher risk category. Risk of infection was also high in rural environments for both farmers and residents, as well as for visitors during the spring and summer.29

To date, we have captured the five species reported as seropositive for hantavirus in Chile.9 It is significant that five O. longicaudatus were seropositive since this supports previous publications that suggest that O. longicaudatus is the major reservoir of the virus.11,27,28 The species was captured both in periurban and rural sites (21.4% and 78.6%, respectively), with the highest abundance found in natural (Lago Ranco) and little disturbed areas (e.g., Tucapel). The presence of this species in periurban zones is an indication of high risk for exposure to hantavirus, since considerable numbers of people are moving to periurban areas.30 In addition, at the intra-specific level, we have obtained one of the higher serologic rates for O. longicaudatus (10.4%) compared with other studies in the southern cone of South America. Finally, it is important to mention that at least in this study, O. longicaudatus was the only species found positive for Andes virus even though the most frequently trapped species was A. olivaceus (more than two-fold higher).

Table 1

Sampled sites, location, category of sites, habitat, human activity of affected, and relative density of rodent species captured in the sampling period (July 2001–December 2002)*

Relative density† of species captured
Sampled site (Georeference)Habitat categoryHabitatHuman activity of affectedNight trapsAlAoAsLmOlPdMmRnRrTe
* Al = Abrothrix longipilis; Ao = Abrothrix olivaceus; As = Abrothrix sanborni; Lm = Loxodontomys micropus; Ol = Oligoryzomys longicaudatus; Pd = Phyllotis darwini; Mm = Mus musculus; Rn = Rattus norvegicus; Rr = Rattus rattus; Te = Thylamys elegans; R = rural; P = periurban.
† Assessed as trap success, indicated as the number of captures/number of total traps × 100.
1. Llai Llay V region (32° 51′ S; 70° 55′ W)RCultivated area, weedsFarm worker23700.400002.50.400
2. Villa Alemana V region (33° 4′ S; 70° 21′ W)RCultivated area, weeds, natural understoryVisitor30004.700001.000.30
3. Hijuelas I V region (32° 48′ S; 70° 08′ W)RCultivated area, weedsFarm worker21001.000001.00.500
4. Hijuelas II V region (32° 49′ S; 71° 6′ W)RCultivated area, natural understory, ravinesFarm worker27000000.4001.101.5
5. Santo Domingo V region (33° 44′ S; 71° 39′ W)RCultivated area, ponds, weedsVisitor3004.06.7000000.700
6. San Antonio V region (33° 34′ S; 71° 37′ W)PYards, outbuildings, adjoining lands, fence lines, weedsResident22500000.401.300.90
7. Las Cabras VI region (34° 4′ S; 71° 17′ W)RPonds, modified land, weedsResident3000.31.0002.7000.700
8. Coya VI region (34° 11′ S; 70° 32′ W)ROutbuildings, modified land, weeds, ravinesResident14500.7000.71.403.400
9. San Fernando VI region (34° 46′ S; 70° 46′ W)RPonds, modified land, weedsResident36000.6000.300000.3
10. Romeral VII region (34° 58′ S; 71° 7′ W)PPonds, modifed land, natural understory, weedsResident3000.73.0000.30000.70
11. Rauco VII region (35° 1′ S; 71° 32′ W)RCultivated area, weedsFarm worker27000.7000.4000.400
12. San Clemente VII region (35° 29′ S; 71° 13′ W)RCultivated area, weedsFarm worker30000.70000000.70
13. Longaví VII region (36° 1′ S; 71° 30′ W)RCultivated area, ponds, weeds, ravinesFarm worker3750.31.9000.800000
14. Bullileo VII region (36° 17′ S; 71° 24′ W)RNatural and planted forest, weeds, camping sitesFarm worker, resident and visitors24000.4001.3000.41.30
15. Tucapel VIII region (37° 14′ S; 71° 47′ W)RNatural forest, weeds, camping sites, bambooVisitor3001.37.0003.00000.30
16. Quillón VIII region (36° 43′ S; 72° 33′ W)RCultivated area, ponds, weedsFarm worker28801.4002.1001.01.00
17. Lautaro IX region (38° 31′ S; 72° 25′ W)PYards, outbuildings, adjoining lands, weedsVicitor30002.0000.300.7000
18. Lago Ranco X region (40° 21′ S; 72° 18′ W)RNatural forest, bambooFarm worker2733.61.80.703.300000
19. Puerto Montt X region (41° 25′ S; 73° 11′ W)RNatural forest, modified land, weeds, bambooResident7710.31.300.10.40000.10
20. Talagante Metropolitan region (33° 39′ S; 70° 52′ W)PCultivated area, outbuildings, weedsFarm worker24006.700000.42.100
Figure 1.
Figure 1.

Sampling sites along the study area in Chile (numbers are as in Table 1).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 70, 3; 10.4269/ajtmh.2004.70.305

Authors’ addresses: Fernando Torres-Pérez, Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago 6513677, Chile. Jorge Navarrete-Droguett, Rebeca Aldunate, and Marcela Ferrés, Centro de Estudios Médicos, Departamento de Enfermedades Infecciosas, Pontificia Universidad Católica de Chile, Santiago, Chile. Terry L. Yates, Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque NM 87131. Gregory J. Mertz, Department of Internal Medicine, University of New Mexico School of Medicine, 915 Camino de Salud, BRF-323, Albuquerque, NM 87131-0001. Pablo A. Vial, Facultad de Ciencias de la Salud, Universidad del Desarrollo, Santiago, Chile. Pablo A. Marquet and R. Eduardo Palma, Centro de Estudios Avanzados en Ecología y Biodiversidad and Departamento de Ecología, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago 6513677, Chile.

Acknowledgments: We thank A. Charrier, M. Ehrenfeld, G. Lobos, and P. Godoy for field and laboratory work. We also thank the Servicio Agrícola y Ganadero for trapping permits in periurban and rural areas, and the Ministry of Health and local health services who provided us with information on sampling sites.

Financial support: This work was supported by the grant Hantavirus Ecology and Disease in Chile (NIH-ICIDR 1 U19 AI-45452-01) to the University of New Mexico and to the Pontificia Universidad Católica de Chile.

REFERENCES

  • 1

    Schmaljohn C, Hjelle B, 1997. Hantaviruses: a global disease problem. Emerg Infect Dis 3 :95–104.

  • 2

    Hart C, Bennet M, 1999. Hantavirus infections: epidemiology and pathogenesis. Microbes Infect 1 :1229–1237.

  • 3

    Duchin JS, Koster FT, Peters CJ, Simpson GL, Tempest B, Zaki SR, Ksiazek TG, Rollin PE, Nichol S, Umland ET, Moolenaar RL, Reef SE, Nolte KB, Gallaher MM, Butler JC, Breiman RF, 1994. Hantavirus pulmonary syndrome: A clinical description of 17 patients with a newly recognized disease. N Engl J Med 330 :949–955.

    • Search Google Scholar
    • Export Citation
  • 4

    Mills J, Childs J, 1998. Ecological studies of rodents reservoirs: their relevance for human health. Emerg Infect Dis 4 :529–537.

  • 5

    Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, Calisher CH, Nichol ST, Abbot KD, Young JC, Morrison ML, Baety BJ, Dunnum JL, Baker RJ, Salazar-Bravo J, Peters CJ, 2002. The ecology and evolutionary history of an emergent disease: hantavirus pulmonary syndrome. BioScience 52 :989–998.

    • Search Google Scholar
    • Export Citation
  • 6

    Lee H, van der Groen G, 1989. Hemorrhagic fever with renal syndrome. Prog Med Virol 36 :62–102.

  • 7

    Botten J, Mirowsky K, Ye C, Gottlieb K, Saavedra M, Ponce L, Hjelle B, 2002. Shedding and intercage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 7 :7587–7594.

    • Search Google Scholar
    • Export Citation
  • 8

    Baró M, Vergara J, Navarrete M, 1999. Hantavirus en Chile: revisión y análisis de casos desde 1975. Rev Med Chil 127 :1513–1523.

  • 9

    Sportorno A, Palma R, Valladares J, 2000. Biología de roedores reservorios de hantavirus en Chile. Rev Chil Infect 17 :197–210.

  • 10

    Pavletic C, 2000. Hantavirus: Su distribución geográfica entre los roedores silvestres de Chile. Rev Chil Infect 17 :186–196.

  • 11

    Levis S, Morzunov S, Rowe J, Enria D, Pini N, Calderon G, Sabattini M, St Jeor SC, 1998. Genetic diversity and epidemiology of hantaviruses in Argentina. J Infect Dis 177 :529–538.

    • Search Google Scholar
    • Export Citation
  • 12

    Mann G, 1978. Los pequeños mamíferos de Chile. Gayana Zool 40 :1–342.

  • 13

    Gallardo M, Palma R, 1990. Systematics of Oryzomys longicaudatus (Rodentia, Muridae) in Chile. J Mammal 71 :333–342.

  • 14

    Murúa R, Gonzáles L, Meserve P, 1986. Population ecology of Oryzomys longicaudatus Philippi (Rodentia: Cricetidae) in southern Chile. J Anim Ecol 55 :281–293.

    • Search Google Scholar
    • Export Citation
  • 15

    Kelt D, 1994. The natural history of small mammals from Aysén Region, southern Chile. Rev Chil Hist Nat 67 :183–207.

  • 16

    Mackelprang R, Dearing D, Jeor S, 2001. High prevalence of Sin Nombre virus in rodent populations, central Utah: A consequence of human disturbance? Emerg Infect Dis 7 :480–481.

    • Search Google Scholar
    • Export Citation
  • 17

    Simonetti J, Agüero T, 1990. Assessing independence of animal movements: spatio-temporal variability in Oryzomys longicaudatus.Mammalia 54 :316–319.

    • Search Google Scholar
    • Export Citation
  • 18

    Calderón G, Pini N, Bolpe J, Levis S, Mills J, Segura E, Guthmann N, Cantoni G, Becker J, Fonollat A, Ripio C, Bortman M, Benedetti R, Sabattini M, Enria D, 1999. Hantavirus reservoir host associated with peridomestic habitats in Argentina. Emerg Infect Dis 5 :792–797.

    • Search Google Scholar
    • Export Citation
  • 19

    Mills J, Childs J, Ksiazek T, Peters C, Velleca W, 1995. Methods for Trapping and Sampling Small Mammals for Virologic Testing. Atlanta, GA: United States Department of Health and Human Services.

  • 20

    Yee J, Wortman IA, Nofchissey R, Bennett SG, Webb JP, Irwin W, Hjelle B, 2003. Rapid and simple method for screening wild rodents for antibodies to Sin Nombre hantavirus. J Wildl Dis 39 :271–277.

    • Search Google Scholar
    • Export Citation
  • 21

    Cantoni G, Padula P, Calderon G, Mills J, Herrero E, Sandoval P, Martínez V, Pini N, Larrieu E, 2001. Seasonal variation in prevalence of antibody to hantaviruses in rodents from southern Argentina. Trop Med Int Health 6 :811–816.

    • Search Google Scholar
    • Export Citation
  • 22

    Yahnke CJ, Meserve PL, Ksiazek TG, Mills JN, 2001. Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan chaco. Am J Trop Med Hyg 65 :768–776.

    • Search Google Scholar
    • Export Citation
  • 23

    Williams RJ, Bryan RT, Mills JN, Palma RE, Vera I, de Velásquez F, Baez E, Schmidt WE, Figueroa RE, Peters CJ, Zaki SR, Khan AS, Ksiazek TG, 1997. An outbreak of hantavirus pulmonary syndrome in western Paraguay. Am J Trop Med Hyg 57 :274–282.

    • Search Google Scholar
    • Export Citation
  • 24

    Toro J, Vega JD, Khan AS, Mills JN, Padula P, Terry W, Yadón Z, Valderrama R, Ellis BA, Pavletic C, Cerda R, Zaki S, Wun-Ju S, Meyer R, Tapia M, Mansilla C, Baro M, Vergara JA, Concha M, Calderon G, Enria D, Peters CJ, Ksiazek TG, 1998. An outbreak of hantavirus pulmonary syndrome, Chile, 1997. Emerg Infect Dis 4 :687–694.

    • Search Google Scholar
    • Export Citation
  • 25

    Redford KH, Eisenberg JF, 1992. Mammals of the Neotropics. The Southern Cone. Chicago: The University Chicago Press.

  • 26

    Padula PJ, Colavecchia SB, Martínez VP, Gonzales MO, Eldelstein A, Miguel DL, Russi J, Mora-Riquelme J, Colucci N, Almirón M, Rabinovich RD, 2000. Genetic diversity, distribution, and serological features of hantavirus infection in five countries in South America. J Clin Microbiol 38 :3029–3035.

    • Search Google Scholar
    • Export Citation
  • 27

    Padula PJ, Sánchez AJ, Edelstein A, Nichol ST, 2002. Complete nucleotide sequence of the M RNA segment of Andes virus and analysis of the variability of the termini of the virus S, M and L RNA segments. J Gen Virol 83 :2117–2122.

    • Search Google Scholar
    • Export Citation
  • 28

    Bohlman MC, Morzunov SP, Meissner J, Beth-Taylor M, Ishibashi K, Rowe J, Levis S, Enria D, St. Jeor SC, 2002. Analysis of hantavirus genetic diversity in Argentina: S segment- derived phylogeny. J Virol 76 :3765–3773.

    • Search Google Scholar
    • Export Citation
  • 29

    Sotomayor V, Aguilera X, 2000. Epidemiología de la infección humana por hantavirus en Chile. Rev Chil Infect 17 :220–232.

  • 30

    Krüger D, Ulrich R, Lundkvist A, 2001. Hantavirus infections and their prevention. Microbes Infect 3 :1129–1144.

Author Notes

Reprint requests: R. Eduardo Palma, Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago 6513677, Chile, Fax: 56-2-686-2621, E-mail: epalma@genes.bio.puc.cl.
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