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Assessment of hantavirus and arenavirus antibody prevalence and associated rodent species in Dickens County, Texas.

Abstract.--A trapping program was implemented to sample rodents seasonally in Dickens County, Texas, from June 2008 to April 2009. A total of 292 rodents were collected using live traps (trapping success rate = 20.2%). Blood samples collected from the specimens were tested for evidence of IgG antibodies to New World hantaviruses and arenaviruses. A total of 30 individuals (10.3% of captured rodents) from four species, spanning three genera, tested positive for viral antibodies. Twenty-one individuals (7.2% of captured rodents) tested positive for hantavirus IgG antibodies, and nine individuals (3.1% of captured rodents) tested positive for arenavirus IgG antibodies. A statistically significant, nonrandom distribution of antibody positive rodents was observed between trapping localities.

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Members of the virus genera Hantavirus (family Bunyaviridae) and Arenavirus (family Arenaviridae) are rodent-borne viruses with cosmopolitan distributions, primarily associated with the rodent families Cricetidae (New World) and Muridae (Old World). Both genera of viruses are associated with human illnesses. Seven New World hantaviruses have been associated with Hantavirus Pulmonary Syndrome (HPS--Fulhorst et al. 2007), a rodent-borne viral zoonosis that can cause an array of disease symptoms and is frequently fatal (Nichol et al. 1993; Plyusnin et al. 1996; Schmaljohn & Hjelle 1997). However, the human health implications of arenaviruses are less clear. New World arenaviruses (Tacaribe serocomplex) have been separated into two phylogeographic clades: South American arenaviruses, a number of which have been associated with severe human disease (Peters 2002), and North American arenaviruses, whose human health impact has not been rigorously assessed (Fulhorst et al. 2007). Arenaviruses and hantaviruses occur over widespread geographic areas, however, little is known about the distribution of individual viruses across most of their range, though it has been documented that multiple viruses (at both the generic and specific levels) can occur in geographic sympatry (Mantooth et al. 2001; Milazzo et al. 2010).

The 17 hantavirus species known to occur in North America are associated with 10 species of rodents spanning five rodent genera (Nichol et al. 2005; Mills et al. 2010). Six hantavirus-associated rodent species occur in Texas, including Microtus ochrogaster, Oryzomys palustris, Peromyscus leucopus, P. maniculatus, Reithrodontomys megalotis, and Sigmodon hispidus (Nichol et al. 2005). Three of these rodent species are associated with viruses that are causally associated with HPS (Fulhorst et al. 2007).

The eight arenaviruses known to occur in North America are associated with seven rodent species, spanning three genera (Salvato et al. 2005; Inizan et al. 2010), with Neotoma micropus, N. leucodon, N. mexicana, O. palustris, and S. hispidus occurring in Texas (Schmidly 2004). In addition to the recognized arenavirus hosts, other Texas rodent genera (Onychomys, Baiomys, Peromyscus, Dipodomys, and Chaetodipus) have tested positive for arenavirus antibodies (Milazzo et al. 2010). Though no host relationship has been established in Texas from these genera, Peromyscus californicus is a recognized natural host of Bear Canyon virus (BCNV) in California (Fulhorst et al. 2002).

This study was conducted in Dickens Co., Texas (Figure 1), at a topographic transition from the Llano Estacado to the Rolling Plains. This ecotone offers increased diversity in terms of habitat structure and composition, providing for multispecies occurrences across various habitat niches, particularly by rodents known to harbor hantaviruses and arenaviruses.

All hantavirus-associated rodent species known to occur in Texas (with the exception of O. palustris) are present in Dickens Co. (Schmidly 2004). Previous studies have detected the presence of hantavirus antibodies in neighboring counties (S. hispidus in Bailey Co.--Rawlings et al. 1996; P. maniculatus, P. leucopus and R. fulvescens in Cottle Co.--Mantooth et al. 2001). All arenavirus-associated rodent species present in Texas (with the exception of N. mexicana) also occur in Dickens Co. (Schmidly 2004). Previous studies have detected the presence of arenavirus antibodies in Dickens Co. and nearby counties (N. micropus and S. hispidus in Dickens Co.; P. leucopus in Hall Co.; N. micropus in Motley Co.--Milazzo et al. 2010). The presence of multiple viral hosts, combined with previously reported virus occurrence in the region (Mantooth et al. 2001; Milazzo et al. 2010) make this locality ideal to study host/virus interactions that have yet to be fully characterized. The primary purposes of this study were 1) to examine antibody/rodent species associations, and 2) to provide a better understanding of hantavirus and arenavirus occurrence in wild rodents within Dickens County, between June 2008 and April 2009.

MATERIALS AND METHODS

Localities.--The study site in Dickens Co., Texas, was split into four localities due to their variable habitat types, which included: pasture land, riparian habitat, caliche arroyos, agriculture fields, grass lawn, man-made pond, marshy wetlands, as well as both maintained and abandoned outbuildings, wood piles, and an occupied house. Locality I (33[degrees]45'35" N, 100[degrees]55'48" W) was a transition zone between the southern plains and the rolling hills of the southern Texas panhandle. It comprised two major habitat types at different elevations. The higher elevation site included an abandoned homestead with corrals, an abandoned bam, and junk pile. The lower elevation comprised a series of caliche arroyos surrounded by juniper grassland. Locality II (33[degrees]45'36" N, 100[degrees]48'44" W) was a mesic area adjacent to a house and small man-made pond, as well as the associated habitat below the dam. Habitat types varied slightly with a grass lawn confined to within 50 m of the house as well as typical tall grass and cattails around the pond. The mesic area transitioned into a drier habitat with scattered outbuildings, as well as idle farm equipment and irrigation supplies. Riparian habitat existed on the dam, whereas juniper/mesquite grassland and a marshy area occurred below the dam. Locality III (33[degrees]45'32" N, 100[degrees]47'42" W) was an irrigated alfalfa field, with sandy plowed soil, bordered by non-irrigated corners consisting of native grasses. A windbreak tree row comprised plums and scrub oak lined the western edge of the locality. Locality IV (33[degrees]46'25" N, 100[degrees]46'8" W--only sampled on Trip 4) was a typical southern rolling plains habitat with bunch grasses, mesquite, sandy soil, and yucca.

Trapping.--Between June 2008 and April 2009, four collecting trips were conducted in Dickens Co., with one conducted per season: Trip 1-Summer (June 2008), Trip 2-Fall (September 2008), Trip 3-Winter (February 2009), and Trip 4-Spring (April 2009). Specimens were collected from a total of four localities of varying habitat types, representing a total of 1,444 trap nights. Sherman live-traps (Sherman Trap Co., Tallahassee, Florida) and Tomahawk live-traps (Tomahawk Live Trap Co., Tomahawk, Wisconsin) were baited with either a scratch grain/rolled oats mixture, or apples. Trapping transects consisted of 50 Sherman live-traps set 5 m apart in straight lines. Tomahawk live-traps were set in pairs at all observed Neotoma middens.

Handling of specimens.--Individual rodents were anesthetized and subsequently euthanized with a 9:1 Ketamine: Xylazine mixture following the Texas Tech University Institutional Animal Care and Use Committee (IACUC) protocols. Following anesthetization, blood samples were drawn via the retro-orbital sinus using approved techniques and were deposited onto Nobuto blood filter strips (ADVANTEC MFS, Inc., Dublin, CA, USA). Following retro-orbital bleeding, animals were euthanized, and immediately given a unique identification number (TK number), sexed, weighed, and measured. In cases where females gave birth in traps, dams and pups were cross-referenced. Tissue samples (heart, kidney, liver, lung, muscle, and spleen) were extracted and voucher specimens (skulls and skins) were prepared and deposited in the Natural Science Research Laboratory, Museum of Texas Tech University for verification of species identification and use in current and future projects.

Antibody Assays.--Blood samples were analyzed at the University of Texas Medical Branch (UTMB), Galveston using ELISA methods previously described (hantaviruses--Fulhorst et al. 1997: arenaviruses--Fulhorst et al. 1996). All samples were tested for IgG antibodies using cell-lysate antigens prepared from Whitewater Arroyo virus strain AV9310135 (WWAV) and Cano Delgadito virus strain VHV-574 (CADV). These antigens are cross-reactive with other known New World arenaviruses and hantaviruses respectively. All samples were screened utilizing ELISA methods, and samples with positive results were screened a second time to ensure consistency.

Statistical.--Chi-squared tests were conducted, utilizing the software package 'R' (R Development Core Team 2005) to examine the distribution of rodents with virus antibodies between localities. Separate Chi-squared tests ([alpha]=0.05) with no corrections were conducted to analyze the distributions of antibody positive rodents: initially for individuals with hantavirus antibodies only, then individuals with arenavirus antibodies only, and ultimately for rodents with all antibodies analyzed jointly (distinguished as 'All'), regardless of generic affiliation of antibodies. An additional Chi-squared test with Yates' continuity correction was conducted to examine if any correlation between rodents positive for antibodies of the different viral genera occurred (distinguished as Corr).

RESULTS

Two hundred ninety-two rodents from 14 species, and nine genera were collected over the course of this study, accounting for a trapping success rate of 20.22% (Table 1). Three genera in the family Heteromyidae and 10 genera within two subfamilies (one in Sigmodontinae, nine in Neotominae) of the family Cricetidae were captured. Utilization of ELISA methods revealed 30 individuals (10.3% of captured individuals) of four species, within three genera, with antibodies reactive to either hantavirus (n=21) or arenavirus (n=9: Table 2).

Hantavirus antibodies were detected in three of the four antibody positive species: P. leucopus (n-19), P. maniculatus (n=1), and S. hispidus (n=1). Arenavirus antibodies were detected in two of the four species: N. micropus (n=1) and S. hispidus (n=2). Although antibodies from both viral genera were detected in S. hispidus, no individuals were found reactive with antigens of both viruses (Table 2). Chi-squared test results are as follows: hantavirus antibodies-[X.sup.2] (3, n=292)=8.73, [P.sub.Hanta]=0.03; arenavirus antibodies- [X.sup.2](3, n=292)=2.69, [P.sub.Arena]-0.4; all antibodies - [X.sup.2](3, n=292)=8.83, [P.sub.All]=0.03; correlation between antibody genera - [X.sup.2](1, n=292)=0.037, [P.sub.Corr] = 0.85.

DISCUSSION

This study provides serologic evidence for geographic sympatry of viruses belonging to the genus Hantavirus and the genus Arenavirus. It is important to note that hantavirus antibodies are highly cross-reactive, thus a positive antibody titer does not necessarily indicate a specific virus species. Attempts to isolate virus by cultivation in monolayers of Vero E6 cells using methods outlined by Fulhorst et al. (1996) were unsuccessful; therefore identification of specific viruses, which were responsible for antibodies detected in these populations, was not possible.

The genus Neotoma has been documented as a host for numerous arenavirus species (Calisher et al. 1970; Fulhorst et al. 1996; Cajimat et al. 2007a, 2007b, 2008; Milazzo et al. 2008). Specifically, isolates of Catarina Virus have been obtained from N. micropus (Cajimat et al. 2007b). In this study, seven out of 40 (17.5 %) N. micropus tested positive for IgG antibodies to WWAV. Arenavirus antibody positive individuals were captured at two localities (II and III) during three (1, 2, and 3) of the four collection trips. Given the natural diversity within Neotoma-hosted arenaviruses, cross-reactivity in EFISA assays, and the fact that attempts to isolate virus were unsuccessful, it is unclear whether the virus antibodies present in this population are indicative of a currently recognized or novel virus.

Multiple Peromyscus species have been reported to possess arenavirus antibodies (Milazzo et al. 2010); however, only a single species, P. californicus, is defined as a natural host for an arenavirus (Fulhorst et al. 2002). It is noteworthy that P. californicus is known to cohabit in the middens of N. macrotis in California, and both species are associated with BCNV (Fulhorst et al. 2002; Cajimat et al. 2007a). Cajimat et al. (2007a) suggest that N. macrotis is the principal host of BCNV, and transmission of the virus to P. californicus occurred through repeated, close contact. A similar behavioral ecology has been observed between P. leucopus and N. micropus in Texas (Suchecki 2003). Although no P. leucopus tested positive for arenavirus antibodies in this study, a previous study (Milazzo et al. 2010) found P. leucopus from neighboring Hall Co., which tested positive for arenavirus antibodies. Therefore, where P. leucopus and N. micropus coexist, it is reasonable to predict they both may act as hosts for the same species of arenavirus. Although P. leucopus currently is not associated with a specific arenavirus strain, it is a known host for two hantavirus species (New York virus--Hjelle et al. 1995b, 1995c; and Sin Nombre virus--Morzunov et al. 1998). Sin Nombre virus (SNV) has been detected in P. leucopus in western Texas (Rawlings et al. 1996). Nineteen individuals of P. leucopus from this study tested positive for IgG antibodies to CADV.

The second species of Peromyscus to test positive for hantavirus antibodies in this study was P. maniculatus. Although arenavirus IgG antibodies have been detected and reported in this species in Texas (Milazzo et al. 2010), in this study it only tested positive for hantavirus. Peromyscus maniculatus is a host for SNV, which was the first New World hantavirus recognized as a human pathogen (Childs et al. 1994; Netski et al. 1999).

Sigmodon hispidus is a known reservoir of multiple hantaviruses (Rollin et al. 1995; Rawlings et al. 1996; Fulhorst et al. 2007), and one arenavirus (Fulhorst et al. 2007). Two individuals from this study tested positive for arenavirus antibodies, and one tested positive for hantavirus antibodies. Antibodies to both viral genera were detected in S. hispidus from Locality III on the same night (Trip 1). Sympatry of antibodies to multiple viral genera (geographical and temporal in nature), combined with the ability of S. hispidus to act as a host to multiple viral species within these genera further reinforce the importance of S. hispidus in future research towards the understanding of virus/host dynamics in North America.

Reithrodontomys are known reservoirs for two species of hantaviruses (Hjelle et al. 1994; Hjelle et al. 1995a), and have tested positive for arenavirus IgG antibodies (Milazzo et al. 2010). In addition, virus antibodies have been detected in both Onychomys (arenavirus- Milazzo et al. 2010) and Baiomys (arenavirus--Milazzo et al. 2010, and hantavirus--McIntyre et al. 2005; Holsomback et al. 2009). In this study, the absence of antibodies in these three genera may be due to the rarity of exposure, in combination with insufficient sampling of individuals for detection of hantavirus or arenavirus antibody positive individuals.

Although arenavirus antibodies have been previously detected in heteromyid rodents (Inizan et al. 2010; Milazzo et al. 2010), no individuals from the three species (Chaetodipus hispidus, Dipodomys ordii, and Perognathus merriami) of the family Heteromyidae captured in this study tested positive for arenavirus antibodies. No prior accounts of arenavirus infections in these species have been published, although related species (Chaetodipus nelsoni and Dipodomys merriami) were reported positive for antibodies in Mexico by Inizan et al. (2010).

The geographic distributions of rodents with hantavirus and arenavirus antibodies were tested independently, and then jointly for nonrandomness using Chi-squared tests ([alpha] = 0.05). The distribution of rodents with arenavirus antibodies between localities ([p.sub.Arena]=0.4418) did not vary significantly from random. Additional Chi-squared tests determined the distribution of hantavirus antibody positive rodents, as well as the distribution of all individuals with antibodies, when analyzed jointly, to be significantly different from random ([p.sub.Hanta]=0.03306; [p.sub.All] = 0.03165). Distributional correlations between rodents with hantavirus and arenavirus antibodies were not found ([p.sub.Corr] = 0.85). Evidence of hantavirus exposure was observed at two of the four trapping localities (localities II and III), locality II had the highest prevalence of hantavirus antibody-positive individuals (16 of 21). This locality is also the most variable in habitat and the most closely associated with active human presence. It is not clear whether anthropogenic factors (i.e. increased water, food, and shelter availability) or habitat variability facilitate the increased prevalence of hantavirus antibody positive rodents, or if this is simply an artifact of an increased rodent population size. It has been suggested that restricted movement of rodents through buildings may lead to concentration of urine and feces in highly traveled areas, increasing likelihood of virus transmission, and that any virus shed indoors may persist longer than in open-air environments, where ultraviolet light would quickly inactivate the virus and air movement could dissipate the aerosols (Kuenzi et al. 2001). Locality II had the largest number of captured rodents with 138 of the 292 animals collected, followed by locality III with 105 animals. Locality II also had the second highest species richness (nine species) behind locality III (11 species). While locality II has the most active human presence, locality III also has experienced habitat modification and human presence. With the nature of the habitat modification and the ecology of peridomestic rodents it is arguable that all factors, including increased population size are anthropogenic, making it difficult to determine the true cause of the increased occurrence of rodents with hantavirus antibodies.

ACKNOWLEDGEMENTS

We thank R.J. Baker, F.A.A. Kahn, S.B. Ayers, R. Duplechin, R.N. Platt, R. Larsen, and C.W. Thompson for assistance with field work, H. Gamer and K. MacDonald for their assistance in procuring blood samples from the Natural Science Research Laboratory at the Museum of Texas Tech University, and R.J. Baker, C.F. Fulhorst, R.D. Bradley, R.E. Strauss, M.N.B. Cajimat, H.M.H.M. Huynh, T.S. Holsomback, A.W. Ferguson, and N. Ordonez-Garza for their assistance on previous versions of this manuscript. We thank the land owner for access to their property. NIH grant AI-41435 provided the financial support for the laboratory work done by Mary Louise Milazzo at the University of Texas Medical Branch, Galveston.

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MRM at: MMauldin@cdc.gov

Matthew R. Mauldin (1,4), Megan S. Keith (1), Mary Louise Milazzo (2) and J. Delton Hanson (3)

(1) Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409-3131

(2) University of Texas Medical Branch, Galveston, TX 77555-0144

(3) Research and Testing Laboratory, Lubbock, TX 79407-2523

(4) Current address: Poxvirus and Rabies Branch Centers for Disease Control and Prevention, Atlanta, GA 30333

Table 1. Individual rodents by species caught by trip (in
chronological order; indicated by date), locality (indicated by
roman numerals), and virus genus for which they tested IgG
antibody positive (A for Arenavirus, H for Hantavirus). Numbers
without letters indicate the total number of individuals captured
from the specified trip or locality. Numbers followed by A or H
indicate number of arenavirus or hantavirus antibody positive
individuals respectively collected at a given locality. Dashes
indicate absence of data. Zeros indicate that no individuals from
a given group tested positive for either genus of virus
antibodies.

                             June 2008            September 2008
                             Locality                Locality

                         I     II      III      I       II       III

Baiomys taylorii         --    0/1      --      --      --       --
Chaeotdipus hispidus     --    0/1     0/1      --      0/2      0/3
Dipodomys ordii          --    --      0/2      --      --       --
Mus musculus             --    0/6      --      --      --       0/2
Neotoma micropus        0/2   3A/8     1A/7    0/2     1A/5     1A/2
Onychomys leucogaster    --    --       --      --      --       --
Perognathus merriami     --    --       --     0/2      --       --
Peromyscus attwateri    0/4    --       --     0/5      --       --
Peromyscus leucopus     0/5    0/6     1H/6    0/3    12H/22     0/1
Peromyscus maniculatus   --    --       --      --      --       --
Reithrodontomys          --    --       --      --      0/1      --
fulvesens
Reithrodontomys          --    --       --      --      --       --
megalotis
Reithrodontomys          --    --       --      --      --       --
montanus
Sigmodon hispidus       0/1   0/15   1A,1H/17   --      0/1     0/21
Total per locality      0/12  3A/37  2A,2H/33  0/12  1A,12H/31  1A/29
Total per trip                   5A,2H/82               2A,12H/72

                            February 2009
                              Locality

                         I       II      III

Baiomys taylorii         --      0/2      --
Chaeotdipus hispidus     --      --       --
Dipodomys ordii          --      --       --
Mus musculus             --      --       --
Neotoma micropus        0/3     1A/5      --
Onychomys leucogaster    --      --       --
Perognathus merriami     --      --       --
Peromyscus attwateri    0/6      --       --
Peromyscus leucopus     0/3     4H/14    0/2
Peromyscus maniculatus   --      --      1H/1
Reithrodontomys          --      0/4     0/1
fulvesens
Reithrodontomys          --      --       --
megalotis
Reithrodontomys         0/1      --       --
montanus
Sigmodon hispidus        --      --       --
Total per locality      0/13  lA,4H/25   1H/4
Total per trip                1A,5H/42

                             April 2009               Total by
                             Locality                 Species

                         I      II      III    IV

Baiomys taylorii        --     0/2      --     --       0/5
Chaeotdipus hispidus    --     0/1      0/2    0/1      0/11
Dipodomys ordii         --      --      0/4    --       0/6
Mus musculus            --     0/3      --     --       0/11
Neotoma micropus        --     0/2      0/4    --      7A/40
Onychomys leucogaster   --      --      0/6    0/1      0/7
Perognathus merriami    --      --      --     --       0/2
Peromyscus attwateri    --      --      --     --       0/15
Peromyscus leucopus     --     0/20    2H/15   0/1     19H/98
Peromyscus maniculatus  --      --      --     --       1H/1
Reithrodontomys         --     0/4      0/2    0/3     0/1 5
fulvesens
Reithrodontomys         --      --      --     --        --
megalotis
Reithrodontomys         --     0/1      0/2    --       0/4
montanus
Sigmodon hispidus       0/1    0/10     0/1   1A/3    2A,1H/70
Total per locality      0/1    0/45    2H/39  1A/11  9A,21H/292
Total per trip               1A,2H/96

Table 2. Individual rodents that tested IgG antibody positive
('H' indicates Hantavirus IgG antibodies, 'A' indicates
Arenavirus IgG antibodies). Includes unique Texas Tech University
(TTU) Catalog number, species, and the antibody type for all
individuals in our study which tested positive.

TTU#            Species           AB+

115407   Peromyscus leucopus       H
115408   Sigmodon hispidus         H
115409   Sigmodon hispidus         A
115410   Neotoma micropus          A
115411   Neotoma micropus          A
115412   Neotoma micropus          A
115413   Neotoma micropus          A
115414   Peromyscus leucopus       H
115415   Peromyscus leucopus       H
115416   Peromyscus leucopus       H
115417   Peromyscus leucopus       H
115418   Peromyscus leucopus       H
115419   Peromyscus leucopus       H
115420   Peromyscus leucopus       H
115421   Peromyscus leucopus       H
115422   Peromyscus leucopus       H
115423   Peromyscus leucopus       H
115424   Neotoma micropus          A
115425   Peromyscus leucopus       H
115426   Peromyscus leucopus       H
115427   Neotoma micropus          A
115428   Neotoma micropus          A
115429   Peromyscus maniculatus    H
115430   Peromyscus leucopus       H
115431   Peromyscus leucopus       H
115432   Peromyscus leucopus       H
115433   Peromyscus leucopus       H
115434   Peromyscus leucopus       H
115435   Peromyscus leucopus       H
115436   Sigmodon hispidus         A
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Author:Mauldin, Matthew R.; Keith, Megan S.; Milazzo, Mary Louise; Hanson, J. Delton
Publication:The Texas Journal of Science
Date:Feb 1, 2012
Words:4889
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