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Anaplasma phagocytophilum infection in small mammal hosts of Ixodes ticks, Western United States.

A total of 2,121 small mammals in California were assessed for Anaplasma phagocytophilum from 2006 through 2008. Odds ratios were >1 for 4 sciurids species and dusky-footed woodrats. High seroprevalence was observed in northern sites. Ten tick species were identified. Heavily infested rodent species included meadow voles, woodrats, deer mice, and redwood chipmunks.

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Anaplasma phagocytophilum is a tick-transmitted pathogen that causes granulocytic anaplasmosis in humans, horses, and dogs (1-3). A. phagocytophilum is maintained in rodent-Ixodes spp. tick cycles, including the western blacklegged tick (Indopacetus pacificus) in the western United States (4). Transovarial transmission does not occur, and I. pacificus feeds only 1 time per stage, so infection must be acquired by a juvenile tick feeding on an infected mammal. Suggested reservoirs in the West include the dusky-footed woodrat (Neotoma fuscipes), for which chronic infection has been observed, and the western gray squirrel (Sciurus griseus), which are frequently infected in nature (5,6). The northern coast range and Sierra Nevada foothills of California (4,7), where abundant rodents include deer mice (Peromyscus spp.), woodrats, and chipmunks (Tamias spp.), have moderate to high levels of granulocytic anaplasmosis. We sought to evaluate granulocytic anaplasmosis exposure and infection and describe the Ixodes spp. tick fauna in small mammals from central and northern coastal California.

The Study

Small mammals were caught in live traps (HB Sherman, Tallahassee, FL, USA, and Tomahawk Live Trap, Tomahawk, WI, USA) at 9 sites or collected as carcasses on roads (online Technical Appendix, available from www. cdc.gov/EID/content/14/7/l147-Techapp.pdf) from 2006 to 2008. Traps were set at locations of observed active rodent use or dens and baited with peanut butter and oats or corn, oats, and barley. Rodents were anesthetized with ketamine and xylazine delivered subcutaneously, examined for ectoparasites, and bled by retro-orbital abrasion or femoral venipuncture. The blood was anticoagulated with EDTA. Shrew (Sorex spp.) carcasses were retrieved when found in traps, kept cold, and then sampled in the laboratory. Live shrews were examined for ticks but released without further processing. All carcasses were identified to species, age, and sex; examined for ectoparasites; and then dissected for coagulated heart blood and spleen. Ectoparasites were preserved in 70% ethanol for identification. Data were included for animals from 3 previous studies (5,8,9).

Plasma anti-A, phagocytophilum immunoglobulin G (Ig) was assayed by an indirect immunofluorescent antibody assay (3), by using A. phagocytophilum-infected HL-60 cells as substrate and fluorescein isothiocyanate-labeled goat anti-rat heavy and light chain IgG (Kirkegaard and Perry, Gaithersburg, MD, USA). This assay does not distinguish exposure to A. phagocytophilum from A. platys, but the PCR was specific for A. phagocytophilum. PCR was performed for all fying (Glaucomys sabrinus), Douglas (Tamiasciuris douglasii), and gray squirrels; all chipmunks from Santa Cruz and Marin Counties; a random subset of chipmunks from Humboldt Redwoods State Park and Hendy Woods State Park; and a random subset of individual mammals of other species. DNA was extracted from whole blood by using a kit (DNeasy Tissue kit, QIAGEN, Valencia, CA, USA), and real-time PCR was performed as described previously (5).

Data were analyzed with "R" (www.r-project.org), with a cutoff for statistical significance of p = 0.05. Differences in seroprevalence among small mammal species and between sexes were assessed by [chi square] test. Individual small mammals' risk for A. phagocytophilum exposure and infection were assessed as a function of sex, species, and location by calculating odds ratios (OR) and 95% confidence intervals (CI). Multivariate logistic regression was performed to evaluate seropositivity as a function of site, host species, and interactions to evaluate possible interaction and confounding between the variables.

A total of 2,121 small mammals, including 2,100 rodents, 20 shrews, and 1 lagomorph, were evaluated for exposure to and infection with A. phagocytophilum and infestation with Ixodes spp. ticks (Table 1). The overall seroprevalence was 15.2% (95% CI 13.6-16.9). Highest values and ORs >1 occurred in dusky-footed woodrats, tree squirrels, and some chipmunk species (Table 1; online Technical Appendix). The PCR prevalence among rodents tested was 3.8% (N = 652, 95% CI 2.9-5.3); highest values were reported in tree squirrels and some chipmunk species (Table 1). Although deer mice have been reported to be exposed to A. phagocytophilum (10,11), we found little evidence of this in our study. Woodrats at northern sites tended to be infected, while sciurids (excluding ground squirrels) showed high rates of exposure at multiple sites, consistent with previous reports (5). A total of 60% of eastern gray squirrels from Connecticut were seropositive with reservoir competence documented by producing PCR-positive ticks after feeding on infected squirrels (12). A PCR-positive eastern chipmunk (Tamias striatus) was reported from Minnesota (13).

Location was an important determinant of exposure to infection, with high seroprevalence in the Hoopa Valley Indian Reservation and Hendy Woods State Park (Table 2). ORs significantly <1 were observed for Samuel P. Taylor State Park and the Morro Bay area, and 5 sites in the far northern coast range and Quincy in the Sierra Nevada had ORs >1 (online Technical Appendix). Statistical analysis failed to document a significant interaction between site and host species, but confounding was apparent, with overrepresentation of gray squirrels and woodrats in some high prevalence sites (online Technical Appendix). PCR prevalence was high at Sutter Buttes State Park and Siskiyou County (both with low sample size) and Big Basin State Park and Hendy Woods State Park, each [approximately equal to]12% (Table 2). Results are consistent with prior reports for horses and dogs (4). Previous spatial analysis documented increased A. phagocytophilum risk in redwood, montane hardwood, and blue oak/foothill pine habitats (14). In our dataset, obvious habitat differences would not account for differences in disease exposure, given the presence of live oak, tanoak, redwood, and Douglas fir at many sites. Further ecologic studies to identify differing ecologic factors among these sites would be useful.

Tick species observed in our study sites include possible enzootic vectors and several human-biting species, including I. pacificus and I. angustus (online Technical Appendix). Host species from which relatively large collections were obtained included meadow voles, woodrats, deer mice, tree squirrels, and redwood chipmunks (T. ochrogenys). Tick diversity was highest on redwood chipmunks and in more northerly sites (online Technical Appendix). L angustus, primarily a nidicolous tick of rodents but occasionally bites humans and is a competent vector for Borrelia burgdorferi sensu stricto (15), occurred on most rodent species. I. spinipalpis, which occurred on woodrats, deer mice, squirrels, and chipmunks, functions as a primary vector for B. bissettii in a woodrat enzootic cycle (16), and Neotoma mexicana and I. spinipalpis have an enzootic cycle in Colorado for A. phagocytophilum.

Conclusions

We show that a strong distinction can be made in possible reservoir capacity among rodent species, with many, such as deer mice and voles, only contributing to the ecology of granulocytic anaplasmosis through their support of ticks but not A. phagocytophilum infection. Others, including tree squirrels and woodrats, are frequently infected, in addition to supporting ticks. Considerable similarities exist between the ecology of A. phagocytophilum and B. burgdorferi in the West, although the large diversity of genospecies that exists for B. burgdorferi has not been reported for A. phagocytophilum. These data provide a starting point for future work to clarify the reservoir competence of small mammals for A. phagocytophilum and to determine how ecologic interactions among small mammals, other vertebrate hosts, multiple possible vectors, and both B. burgdorferi and A. phagocytophilum could affect the enzootic persistence of these pathogens and risk to humans and animals.

DOI: 10.3201/eid1407.071599

Acknowledgments

We thank Niki Drazenovich, Elizabeth Holmes, Bernadette Clueit, Michael Adjemian, Jamie Bettaso, Greta Wengert, and Edwin Saada for field and laboratory assistance; and Patrick Foley for suggestions for analysis. Personnel at each of the study sites (Hoopa Valley Indian Tribe, UC Reserve System, California State Parks, Bureau of Land Management, and private land owners) provided invaluable access and logistic support.

Financial support was provided by the UC Davis Center for Vectorborne Diseases and the Committee on Research.

Dr Foley is a disease ecologist at the University of California, Davis, Department of Medicine and Epidemiology. She is also a veterinarian. Her major research focus is the ecology of tick-borne diseases.

References

(1.) Greig B, Asanovich KM, Armstrong PJ, Dumler JS. Geographic, clinical, serologic, and molecular evidence of granulocytic ehrlichiosis, a likely zoonotic disease, in Minnesota and Wisconsin dogs. J Clin Microbiol. 1996;34:44-8.

(2.) Madigan JE. Equine ehrlichiosis. Vet Clin North Am Equine Pract. 1993;9:423-8.

(3.) Dumler JS, Asanovich KM, Bakken JS, Richter P, Kimsey R, Madigan JE. Serologic cross-reactions among Ehrlichia equi, Ehrlichia phagocytophila, and human granulocytic ehrlichia. J Clin Microbiol. 1995;33:1098-103.

(4.) Foley JE, Foley P, Brown RN, Lane RS, Dumler JS, Madigan JE. Ecology of granulocytic ehrlichiosis and Lyme disease in the western United States.. J Vector Ecol. 2004;29:41-50.

(5.) Nieto NC, Foley J. Evaluation of squirrels as ecologically significant hosts for Anaplasma phagocytophilum in California. J Med Entomol. In press.

(6.) Foley JE, Kramer VL, Weber D. Experimental ehrlichiosis in dusky footed woodrats (Neotoma fuscipes). J Wildl Dis. 2002;38:194-8.

(7.) California Department of Health Service. Vector-borne diseases in California. 2004 annual report. Sacramento (CA): The Department; 2006.

(8.) Foley J, Clueit S, Brown RN. Differential exposure to Anaplasma phagocytophilum in rodent species in northern California. Vector Borne Zoonotic Dis. 2008;8:49-55. DOI: 10.1089/vbz.2007.0175

(9.) Nieto NC, Foley P, Calder L, Dabritz H, Adjemian J, Conrad PA, et al. Ectoparasite diversity and exposure to vector-borne disease agents in wild rodents in central coastal California. J Med Entomol. 2007;44:328-35. DOI: 10.1603/0022-2585 (2007)44[328:EDAETV]2.0.CO;2

(10.) Zeidner NS, Burkot TR, Massung R, Nicholson WL, Dolan MC, Rutherford JS, et al. Transmission of the agent of human granulocytic ehrlichiosis by Ixodes spinipalpis ticks: evidence of an enzootic cycle of dual infection with Borrelia burgdorferi in Northern Colorado. J Infect Dis. 2000;182:616-9. DOI: 10.1086/315715

(11.) Nicholson WL, Muir S, Sumner JW, Childs JE. Serologic evidence of infection with Ehrlichia spp. in wild rodents (Muridae: Sigmodontinae) in the United States. J Clin Microbiol. 1998;36:695-700.

(12.) Levin ML, Nicholson WL, Massung RE Sumner JW, Fish D. Comparison of the reservoir competence of medium-sized mammals and Peromyscus leucopus for Anaplasma phagocvtophilum in Connecticut. Vector Borne Zoonotic Dis. 2002;2:125-36. DOI: 10.1089/15303660260613693

(13.) Walls JJ, Greig B, Neitzel D, Dumler J. Natural infection of small mammal species in Minnesota with the agent of human granulocytic ehrlichiosis. J Clin Microbiol. 1997;35:853-5.

(14.) Foley JE, Queen E, Sacks B, Foley P. GIS-facilitated spatial epidemiology of tick-borne diseases in coyotes (Canis latrans) in northern and coastal California. Comp Immunol Microbiol Infect Dis. 2005;28:197-212. DOI: 10.1016/j.cimid.2005.01.006

(15.) Peavey CA, Lane RS, Damrow T. Vector competence of Ixodes angustus (Acari: Ixodidae) for Borrelia burgdorferi sensu stricto. Exp Appl Acarol. 2000;24:77-84. DOI: 10.1023/A:1006331311070

(16.) Brown RN, Peot MA, Lane RS. Sylvatic maintenance of Borrelia burgdorferi (Spirochaetales) in Northern California: untangling the web of transmission. J Med Entomol. 2006;43:743-51. DOI: 10.1603/0022-2585(2006)43[743:SMOBBS]2.0.CO;2

Address for correspondence: Janet E. Foley, Department of Medicine and Epidemiology, University of California, Davis, California 95616, USA; email: jefoley@ucdavis.edu

Janet E. Foley, * Nathan C. Nieto, * Jennifer Adjemian, * Haydee Dabritz, ([dagger]) and Richard N. Brown ([double dagger])

* University of California, Davis, California, USA; ([dagger]) California Department of Public Health, Richmond, California, USA; and ([double dagger]) Humboldt State University, Arcata, California, USA
Table 1. Seroprevalence and PCR prevalence of Anaplasma
phagocytophilum among small mammal species, northern and
central coastal California *

 A. phagocytophilum IFA

Mammal species Seropositive Seroprevalence

Clethrionomys californicus 1 12.50
Glaucomys sabrinus 2 14.29
Mus musculus 0 0.00
Microtus californicus 2 5.88
Neotoma cinerea 0 0.00
N. fuscipes 167 50.15
N. macrotis 2 3.03
All Neotoma 169 42.25
Peromyscus boylii 3 8.82
P. californicus 2 0.67
P. maniculatus 18 3.46
P. truei 1 2.56
Peromyscus spp. 0 0.00
All Peromyscus 24 2.68
Rattus rattus 0 0.00
Reithrodontomys megalotis 0 0.00
Spermophilus beecheyi 0 0.00
S.lateralis 2 22.22
Sciurus carolinensis 11 57.89
S. griseus 34 70.83
S. niger 1 100.00
All Sciurus 46 47.83
Sorex spp. 0 0.00
Sylvilagus bachmani 0 0.00
Tamias amoenus 6 6.82
T. merriami 0 0.00
T. minimus 0 0.00
T. senex 5 4.81
T. speciosus 4 33.33
T. sonomae 1 14.29
T. ochrogenys 30 27.52
Tamias spp. 2 8.33
All Tamias 48 13.45
Tamiasciurus douglasii 6 40
Total 300 15.24

 A. phagocytophilum A. phagocytophilum
 IFA msp2 PCR

 PCR
Mammal species 95% CI positive

Clethrionomys californicus 0.6-53.3 0
Glaucomys sabrinus 2.5-43.9 1
Mus musculus 0-25.3 0
Microtus californicus 1.0-21.1 0
Neotoma cinerea 0-94.5 0
N. fuscipes 44.7-55.6 8
N. macrotis 5.3-11.5 1
All Neotoma 37.4-47.3 9
Peromyscus boylii 2.3-24.8 1
P. californicus 0.1-2.7 0
P. maniculatus 2.1-5.5 0
P. truei 0.1-15.1 NT
Peromyscus spp. 0-53.7 NT
All Peromyscus 1.8-4.0 1
Rattus rattus 0-37 0
Reithrodontomys megalotis 0-17.2 1
Spermophilus beecheyi 0-4.2 0
S.lateralis 3.9-59.9 NT
Sciurus carolinensis 34.0-78.9 3
S. griseus 55.7-82.6 6
S. niger 55.0-100.0 0
All Sciurus 33.1-62.9 9
Sorex spp. 0-37.0 0
Sylvilagus bachmani 0-94.5 NT
Tamias amoenus 2.8-14.8 NT
T. merriami 0-48.3 0
T. minimus 0-4.9 NT
T. senex 1.8-11.4 NT
T. speciosus 11.3-64.6 NT
T. sonomae 0.7-58.0 2
T. ochrogenys 19.6-37.0 2
Tamias spp. 1.5-28.5 NT
All Tamias 10.2-17.5 4
Tamiasciurus douglasii 17.5-67.1 0
Total 13.7-16.9 33

 A. phagocytophilum
 msp2 PCR

 PCR
Mammal species prevalence 95% CI

Clethrionomys californicus 0 0-53.7
Glaucomys sabrinus 16.70 0.8-63.5
Mus musculus 0 0-34.4
Microtus californicus 0 0-17.8
Neotoma cinerea 0 0-94.5
N. fuscipes 4.30 2.0-8.6
N. macrotis 1.80 0.09-10.6
All Neotoma 3.70 1.8-7.1
Peromyscus boylii 4.00 0.2-22.3
P. californicus 0 0-3.8
P. maniculatus 0 0-6.6
P. truei
Peromyscus spp.
All Peromyscus 0.45 0.02-2.9
Rattus rattus 0 0-37.1
Reithrodontomys megalotis 6.30 0.3-32.3
Spermophilus beecheyi 0 0-20.0
S.lateralis
Sciurus carolinensis 18.80 5.0-46.3
S. griseus 15.80 6.6-31.9
S. niger 0 0-94.5
All Sciurus 16.40 8.2-29.3
Sorex spp. 0 0-94.5
Sylvilagus bachmani
Tamias amoenus
T. merriami 0 0-40.2
T. minimus
T. senex
T. speciosus
T. sonomae 50.00 15.0-85.0
T. ochrogenys 6.90 1.2-24.2
Tamias spp.
All Tamias 34.00 3.2-24.1
Tamiasciurus douglasii 0 0-60.4
Total 3.80 2.9-5.3

* IFA, immunofluorescence assay; CI, confidence interval;
NT, not tested.

Table 2. Regional seroprevelance and PCR prevalence rates for
exposure to Anaplasma phagocytophilum in small mammals in
various sites, northern and central California *

 A. phagocytophilum IFA

Site Seropositive Seroprevalence

Big Basin State Park 16 6.30
Humboldt Redwoods State Park 24 16.90
Hoopa Valley Indian Reservation 173 36.19
Hendy Woods State Park 43 22.51
King Range National 1 3.45
Conservation Area
Mendocino County (roadside 0 0.00
only)
Morro Bay regional communities 5 1.23
Placerville City region (roadside 1 1.00
only)
Quincy City region (roadside 2 50.00
only)
Sutter Buttes State Park 3 7.50
Sagehen Research Station 17 7.69
Siskiyou County (roadside only) 3 1.00
Sonoma 1 1.00
Samuel P. Taylor State Park 3 1.75
Trinity County (roadside only) 2 40.00
Sacramento River Valley 3 1.00
(roadside only)
Willow Creek Town (roadside 3 0.30
only)
Yolo County 1 6.67

 A. phagocy-
 A. phagocytophilum tophilum msp2
 IFA PCR

 PCR
Site 95% CI positive

Big Basin State Park 3.76-10.22 5
Humboldt Redwoods State Park 11.33-24.31 2
Hoopa Valley Indian Reservation 31.91-40.70 6
Hendy Woods State Park 16.93-29.22 5
King Range National 0.18-19.63 0
Conservation Area
Mendocino County (roadside 0.00-94.53 0
only)
Morro Bay regional communities 0.45-3.01 2
Placerville City region (roadside 5.46-1.00 1
only)
Quincy City region (roadside 15.00-84.99 0
only)
Sutter Buttes State Park 1.96-21.48 1
Sagehen Research Station 4.68-12.24 0
Siskiyou County (roadside only) 30.99-1.00 1
Sonoma 5.46-1.00 0
Samuel P. Taylor State Park 0.42-5.45 2
Trinity County (roadside only) 7.26-82.96 0
Sacramento River Valley 30.99-1.00 0
(roadside only)
Willow Creek Town (roadside 8.09-64.63 0
only)
Yolo County 0.35-33.97 0

 A. phagocytophilum msp2 PCR

 PCR
Site prevalence 95% CI

Big Basin State Park 12.20 4.58-27.00
Humboldt Redwoods State Park 6.06 1.06-21.62
Hoopa Valley Indian Reservation 4.14 1.69-9.18
Hendy Woods State Park 12.19 4.58-27.00
King Range National 0.00 0.00-80.21
Conservation Area
Mendocino County (roadside 0.00 0.00-94.54
only)
Morro Bay regional communities 0.67 0.12-2.65
Placerville City region (roadside 1.00 5.46-1.00
only)
Quincy City region (roadside 0.00 0.00-60.42
only)
Sutter Buttes State Park 50.00 9.45-90.55
Sagehen Research Station 0.00 0.00-60.42
Siskiyou County (roadside only) 33.33 1.76-87.47
Sonoma 0.00 0.00-94.54
Samuel P. Taylor State Park 4.26 0.74-15.73
Trinity County (roadside only) 0.00 0.00-53.71
Sacramento River Valley 0.00 0.00-69.00
(roadside only)
Willow Creek Town (roadside 0.00 0.00-60.42
only)
Yolo County 0.00 0.00-25.35

* IFA, immunofluorescence assay; CI, confidence interval.
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Article Details
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Title Annotation:DISPATCHES
Author:Foley, Janet E.; Nieto, Nathan C.; Adjemian, Jennifer; Dabritz, Haydee; Brown, Richard N.
Publication:Emerging Infectious Diseases
Article Type:Disease/Disorder overview
Geographic Code:1USA
Date:Jul 1, 2008
Words:3034
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