Spatial and temporal patterns of Leptospira infection in dogs from northern California: 67 cases (2001–2010)

Janemarie H. Hennebelle Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Jane E. Sykes Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Tim E. Carpenter Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Janet Foley Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Abstract

Objective—To conduct an epidemiological analysis of the spatial and temporal distribution of canine leptospirosis cases in northern California and detect spatial clustering in any region.

Design—Retrospective case-control study.

Animals—67 dogs with leptospirosis and 271 control dogs.

Procedures—Medical records of case and control dogs were reviewed. Spatial coordinates of home addresses of the study population were analyzed visually and statistically via a Cuzick-Edwards test and spatial, temporal, and space-time permutation scan statistics.

Results—Cases were distributed around the San Francisco Bay region as well as in the Sierra Nevada foothills near Sacramento, Calif, whereas controls were principally distributed along route I-80 between San Francisco and Sacramento, Calif. Clustering was found for the second through sixth nearest neighboring cases via the global spatial cluster test. A local spatial cluster of 30 cases was identified in San Francisco (95% confidence interval, 1.3 to 7.0), and a temporal cluster of 18 cases was identified from May 2003 through May 2004 (95% confidence interval, 1.4 to 6.5). No significant space-time cluster was identified.

Conclusions and Clinical Relevance—The use of geographic information systems provided a visual representation of the results of statistical analysis for the location and time at which leptospirosis cases occurred. This useful tool can be used to educate veterinary practitioners and the public about a potentially fatal zoonotic disease and direct vaccination strategies to help prevent disease occurrence.

Abstract

Objective—To conduct an epidemiological analysis of the spatial and temporal distribution of canine leptospirosis cases in northern California and detect spatial clustering in any region.

Design—Retrospective case-control study.

Animals—67 dogs with leptospirosis and 271 control dogs.

Procedures—Medical records of case and control dogs were reviewed. Spatial coordinates of home addresses of the study population were analyzed visually and statistically via a Cuzick-Edwards test and spatial, temporal, and space-time permutation scan statistics.

Results—Cases were distributed around the San Francisco Bay region as well as in the Sierra Nevada foothills near Sacramento, Calif, whereas controls were principally distributed along route I-80 between San Francisco and Sacramento, Calif. Clustering was found for the second through sixth nearest neighboring cases via the global spatial cluster test. A local spatial cluster of 30 cases was identified in San Francisco (95% confidence interval, 1.3 to 7.0), and a temporal cluster of 18 cases was identified from May 2003 through May 2004 (95% confidence interval, 1.4 to 6.5). No significant space-time cluster was identified.

Conclusions and Clinical Relevance—The use of geographic information systems provided a visual representation of the results of statistical analysis for the location and time at which leptospirosis cases occurred. This useful tool can be used to educate veterinary practitioners and the public about a potentially fatal zoonotic disease and direct vaccination strategies to help prevent disease occurrence.

Leptospirosis is a zoonotic disease of humans and animals that is caused by aquatic spirochetes of the genus Leptospira, which includes Leptospira interrogans and Leptospira kirschneri.1 Leptospirosis is endemic at a high level in various geographic locations worldwide, with numerous human cases reported annually in tropical locations such as Hawaii.2,3 In dogs, leptospirosis can cause life-threatening hepatic and renal failure.4 Numerous serovars are capable of causing disease in dogs, and although each serovar has an enzootic maintenance host in nature, domestic and feral species are capable of serving as reservoir or incidental hosts for multiple serovars; such wildlife cycles are poorly understood.2,4,a Leptospirosis is diagnosed in as many as 5 to 10 dogs/y at the William R. Pritchard Veterinary Medical Teaching Hospital at the University of California-Davis. However, the proximal source of infection for these dogs is rarely known, nor is it known what features of the dogs' biotic and abiotic environments increase the dogs' risk. To better understand and manage that risk, identification of spatial and temporal patterns of disease is needed. Two previous studies5,6 that used spatial cluster analysis to map canine seroreactivity across the United States and California identified clusters in northern and eastern California. One study5 identified 43 cases from 1998 through 2000 around the San Francisco Bay Area as well as in Sacramento, Calif. The second study by Gautam et al6 examined seroreactivity across the United States; those authors identified space-time clusters of Leptospira seroreactivity in eastern and northern California during 2006 and 2007 as well as a specific cluster of cases located in central California during 2005 associated with seroconversion to serovar Pomona.

Temporal and spatial scan statistics assist identification of the location and time at which disease clusters occur.7,8 The purpose of the study reported here was to analyze a large number of canine leptospirosis cases that occurred over an extended period to determine the spatial locations, possible clustering, and spatial and temporal statistics associated with such clusters of cases in northern California.

Materials and Methods

Data description—Data were extracted electronically from records of dogs with confirmed cases of leptospirosis and a group of control dogs evaluated at the Veterinary Medical Teaching Hospital. Records from dogs with leptospirosis diagnosed from March 2001 through November 2010 at the Veterinary Medical Teaching Hospital were identified through an electronic search for leptospir*, pulmonary hemorrhage, acute renal failure, kidney failure, liver failure, and acute hepatic failure. Inclusion criteria for cases were dogs that lived in California with clinicopathologic abnormalities consistent with leptospirosis and that had at least 1 positive serologic MAT result with a reciprocal titer ≥ 800 for at least 1 Leptospira serovar or positive results of renal immunohistochemical staining. The entire medical record was reviewed by 2 of the authors (JHH and JES), including a board-certified internal medicine specialist, to ensure the clinicopathologic findings were consistent with leptospirosis for each case. The results of acute and, where available, convalescent Leptospira serologic testing were compiled. Leptospira serologic testing was performed with the MAT at the California Animal Health and Food Safety Laboratory, Davis, Calif, for antibodies against serovars Pomona, Grippotyphosa, Bratislava, Canicola, Icterohaemorrhagiae, and Hardjo. Vaccine status among case dogs was evaluated and defined as leptospirosis vaccine administered within 12 months prior to evaluation, leptospirosis vaccine administered > 12 months prior to evaluation, leptospirosis vaccine not administered, or vaccination history unknown.

At least 4 controls were selected for every case with a freely available random number generator.b Controls were dogs evaluated at the Veterinary Medical Teaching Hospital during the same time period with no evidence of clinicopathologic or serologic test results consistent with leptospirosis; serologic testing to rule out Leptospira spp infection in this group was not generally performed because leptospirosis was not suspected as a diagnosis by the attending clinician. For both case and control dogs, data extracted from records included the date of evaluation, home address with 5-digit ZIP code, and home environment, including whether the dog was predominantly indoors or outdoors and had exposure to wildlife, livestock, or bodies of water. Additional information examined during medical record review included signalment, history of vaccination for leptospirosis, clinical signs, laboratory abnormalities, and outcome (survival to discharge or death). When not available in the record, information on vaccination history was obtained by follow-up calls to referring veterinary clinics.

Data analysis—For all dogs, the home address with a 5-digit ZIP code was used as the identifier; home addresses and ZIP codes were transformed to latitude and longitude coordinates with freely available geocoding software.c Data were compiled with map features, and maps were produced with standard geographic information system software.d,e

Cluster analysis was performed to evaluate spatial, temporal, and space-time clustering of confirmed cases. Spatial clustering was evaluated at the global and local levels to account for different patterns clustering can take.7,8 Global tests may identify an overall pattern of clustering without determining the specific location of the cluster, whereas local area testing may identify the specific location of clusters in a population, which may have only a limited number of clusters.7,9 Both tests adjust for the nonhomogeneous distribution of a population on the basis of the number and proportion of cases in a case-control sample.8 The Cuzick-Edwards test, a global test, was used to determine whether more cases among their first 6 nearest neighboring cases occurred than were expected if cases and controls were randomly distributed and was performed with statistical software.10,f

Local area clustering of cases in space, time, and space-time interactions was evaluated with spatial scan statistic software.g The spatial model uses a Bernoulli likelihood function to evaluate the probability of cases being within overlapping spatial circles.11–13 An additional spatial scan was performed by comparing cases with the 67 controls that had the highest costs incurred during the first visit to the Veterinary Medical Teaching Hospital to determine whether referral bias contributed significantly to the distribution of cases. The scan test evaluates an ordered time series of events (case data in this study) by use of intervals (windows) to determine the maximum number of events that occur within a fixed window or time period.11 The maximum temporal window was evaluated in 2 ways: via 50% of the time period or a maximum of a 30-day time period.

Space-time cluster analysis involves thousands of overlapping cylinders that each have a base corresponding to geographic area and height that corresponds to time.14,15 The space-time permutation test was used to calculate an expected number of cases within any section of a cylinder under the null hypothesis that given a Poisson distribution, spatial, and temporal randomness were expected. A maximum spatial window of 50% of the study area and a maximum temporal window of 50% of the time period were used according to published recommendations.7,15

Clusters were identified and assessed by comparing the number of expected cases with the number of observed cases within a scanning window. P values were computed via a Monte Carlo simulation of 999 replications under the null hypothesis of a random distribution in space and time; values of P < 0.05 were considered significant. Additionally, significant clusters were evaluated via a χ2 or Fisher exact test to determine whether there was a significant difference in the pattern of seroreactivity within the cluster compared with cases outside the cluster.

Results

Eighty-one dogs with leptospirosis were identified; 67 of these dogs met the inclusion criteria and had sufficient data for further analysis. A total of 271 dogs met the criteria for the control group, resulting in a control-to-case ratio of 4.05:1. All 338 dogs in the study group had primary home addresses in California. Among case dogs, 44 (66%) dogs had paired MAT titer results reported (Table 1). All 44 dogs had a 4-fold change in titer to at least 1 Leptospira serovar.

Table 1—

Serologic test results for 66 dogs in which leptospirosis was diagnosed at the University of California-Davis Veterinary Medical Teaching Hospital in northern California from March 2001 through November 2010.

VariableVaccine not given (n = 42)Vaccine given ≤ 12 months (n = 8)Vaccine given > 12 months (n = 7)Vaccination unknown (n = 9)
Paired reciprocal titers reported (No. of dogs)27845
Interval between paired specimen collection (d)10 (4–44)9 (5–12)13 (7–21)21 (6–43)
Highest acute reciprocal titer (median [range {GMT}])100 (100–6,400 [2.00])400 (100–3,200 [2.60])100 (100–6,400 [2.00])100 (100–6,400 [2.00])
Highest convalescent reciprocal titer (median [range {GMT}])6,400 (800–102,400 [3.81])3,200 (3,200–51,200 [3.51])9,600 (1,600–25,600 [3.98])2,400 (1,600–51,200 [3.38])
Single reciprocal titer reported (No. of dogs)15*034
 Time (d) after onset of illness (median [range])7 (4–27)7 (4–10)11 (5–126)
 Highest reciprocal titer (median [range {GMT}])2,400 (400*–25,600 [3.38])12,800 (1,600–25,600 [4.10])6,400 (6,400–25,600 [3.81])

One dog had positive results of immunohistochemical staining and a reciprocal titer of 400; all other titers were ≥ 800.

— = Not applicable. GMT = Geometric mean titer.

Twenty-one (31%) dogs had only a single titer reported that was ≥ 1,600; 6 dogs had a reciprocal titer of 1,600, and the remaining 15 dogs had a reciprocal titer ≥ 3,200. Two of these 21 dogs also had positive PCR assay results for urine or blood specimens. Two of the 67 dogs (including the dog with the lowest seroreactivity) also had positive test results for Leptospira via renal immunohistochemical staining, one of which did not have available serologic test results.

Among control dogs, 2 of 271 dogs were tested for leptospirosis via a serologic MAT; the remaining 269 dogs were not tested for leptospirosis with any of the described diagnostic tests. The 2 dogs that were tested were seronegative.

The primary serovar to which seroreactivity occurred was Pomona in 44 of 67 (66%) case dogs, followed by Bratislava in 6 (9%) cases; 7 of 67 (10%) case dogs had highest seroreactivity to both Pomona and Bratislava. The remaining case dogs either had positive results of renal immunohistochemical staining or had highest seroreactivity to a combination of serovars. There were no case dogs with highest seroreactivity to Grippotyphosa, Canicola, or Hardjo alone. Vaccination for leptospirosis within a 12-month period prior to evaluation was reported in 8 of 67 (12%) case dogs (Table 1). Vaccination for leptospirosis > 12 months prior to evaluation was reported in 7 of 67 (10%) case dogs. The vaccine type administered was known for 5 dogs, and in all case dogs, a bivalent Icterohaemorrhagiae and Canicola vaccine was administered. Vaccination for leptospirosis was not present in the history of 42 of 67 (63%) case dogs, and 9 (13%) dogs had an unknown vaccination status. Among 24 dogs that were either vaccinated or had an unknown vaccination status, the results for paired serologic testing were available for 17. A ≥ 4-fold change in titer to at least 1 serovar occurred in all 17 dogs. Among the 7 remaining dogs, 1 had positive results of renal immunohistochemical staining and all 7 had a single reciprocal titer reported. Three of 7 case dogs received a leptospirosis vaccination > 12 months prior to evaluation (median, 3 years; range, 2 to 3 years). Among 4 dogs with an unknown vaccination status, 1 dog also had a positive Leptospira urine PCR assay result.

The distribution of case and control dogs was mapped to provide a visual representation of where case and control dogs resided (Figure 1). Preliminary observation suggested geographic clustering occurring among case dogs, relative to control dogs. Specific cluster locations appeared in San Francisco and the Bay Area and along route I-80 from Davis, Calif, to the foothills of the Sierra Nevada Mountains. Results of the Cuzick-Edwards test were significant (P = 0.01) for the nearest neighbors 2 through 6. Spatial scan statistical analysis revealed 1 significant (P = 0.001) spatial cluster for Leptospira seroreactivity (95% CI, 1.3 to 7.0; Figure 2). The cluster population included 30 case and 41 control dogs within a radius of 40.4 km that covered an area in San Francisco and the Bay Area. Within this primary spatial cluster, seroreactivity to several serovars was identified: 20 of 30 (67%) case dogs had the highest titer to serovar Pomona, followed by Bratislava (n = 2 dogs) and Icterohaemorrhagiae (2), and 6 had the highest titers to different combinations of serovars. Results of a χ2 test used to compare the distribution of seroreactivity to Pomona within the spatial cluster with case dogs outside the spatial cluster indicated there was no significant (P = 0.888) difference between the 2 populations (95% CI, 0.62 to 1.5). A Fisher exact test used to compare case dogs within the cluster to case dogs outside the cluster with the highest seroreactivity to Bratislava indicated there was no significant (P = 0.44) difference between the 2 groups (95% CI, 0.82 to 1.1).

Figure 1—
Figure 1—

Map of the spatial location in northern California of 67 case dogs with leptospirosis and 271 control dogs evaluated at the University of California-Davis Veterinary Medical Teaching Hospital (VMTH) from March 2001 through November 2010, identified by home address coordinates. Geographic coordinate system: GCS_North_American_1983_CRSC. Projection: Mercator auxiliary sphere.

Citation: Journal of the American Veterinary Medical Association 242, 7; 10.2460/javma.242.7.941

Figure 2—
Figure 2—

Map of spatial location and spatial cluster in northern California of case and control dogs in Figure 1, identified by home address coordinates. Inset—County map of California; rectangle indicates area of interest. See Figure 1 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 242, 7; 10.2460/javma.242.7.941

Time series data indicated that there appeared to be temporal clustering among cases (Figures 3–5). Temporal clustering was identified during 2003 through 2004 with a marginally nonsignificant (P = 0.058) cluster of 18 cases occurring from May through the following May (95% CI, 1.4 to 6.5). Seroreactivity identified among case dogs in the temporal cluster included the highest titer to Pomona (n = 13 dogs), Bratislava (2), and multiple serovars (2); the remaining case dog had positive results of renal immunohistochemical staining, and serologic test results were not reported. On the basis of the results of a χ2 test, there was no significant (P = 0.49) difference between the distributions of seroreactivity to Pomona inside the temporal cluster, compared with outside the cluster (95% CI, 0.33 to 1.7). Results of a Fisher exact test used to compare case dogs within the temporal cluster with case dogs outside the cluster with highest seroreactivity to Bratislava indicated there was no significant (P = 0.52) difference (95% CI, 0.15 to 3.7). No significant clusters were found for either the space-time scan (P = 0.325) among case and control dogs or among case dogs relative to control dogs (P = 0.446) with the highest costs on the first visit.

Figure 3—
Figure 3—

Yearly distribution of dogs with leptospirosis evaluated at the University of California-Davis Veterinary Medical Teaching Hospital from 2001 through 2010.

Citation: Journal of the American Veterinary Medical Association 242, 7; 10.2460/javma.242.7.941

Figure 4—
Figure 4—

Frequency of diagnosis of leptospirosis in dogs evaluated at the University of California-Davis Veterinary Medical Teaching Hospital by month and mean monthly rainfall (solid line) in northern California from 2001 through 2010.

Citation: Journal of the American Veterinary Medical Association 242, 7; 10.2460/javma.242.7.941

Figure 5—
Figure 5—

Yearly frequency of diagnosis of leptospirosis in dogs evaluated at the University of California-Davis Veterinary Medical Teaching Hospital and mean yearly rainfall (solid line) in northern California from 2001 through 2010.

Citation: Journal of the American Veterinary Medical Association 242, 7; 10.2460/javma.242.7.941

Discussion

Infection with pathogenic leptospires causes febrile illness and hepatic and renal disease in dogs and humans in the United States.16 During the period from 1982 through 2001, 23 cases of human leptospirosis were reported in California.17 To more clearly understand and control leptospirosis in dogs, proper identification and quantification of regional disease occurrence and temporal trends are required.

In the present study, local and global clustering tests were used and identified spatial and temporal clustering among case dogs, compared with results for control dogs from March 2001 through November 2010. In performing the spatial analyses, several assumptions were made. A case dog was considered seropositive if a single titer was ≥ 800 or if positive identification of leptospires was made on immunohistochemical staining of renal tissue. Although a 2-fold change in titer during a 4-week period is considered a definitive indication of active leptospiral infection, a single reciprocal titer ≥ 800 in conjunction with clinical signs is widely accepted as an indicator of current or recent infection with Leptospira spp in both dogs and humans.4,16,18–21 Case selection could have been affected by vaccine- or exposure-induced seroreactivity; however, in all case dogs, the history and clinical signs documented in the medical records were strongly suggestive of this diagnosis and the clinical diagnosis made by the attending clinician was leptospirosis; clinical diagnoses were only used to corroborate the epidemiological data that were available. In addition, paired serologic test results were available for most case dogs included in the study. Among those case dogs for which only a single titer was available, none had received a leptospirosis vaccine within the previous 12 months, and all dogs had either a reciprocal titer ≥ 1,600 or a combination of diagnostic tests with results suggestive of leptospirosis. Likewise, the use of statistical software can have limited power for detecting spatial clusters; however, the use of a global area test such as the Cuzick-Edwards test first can help mitigate these effects by determining whether relative spatial clustering is occurring.

Spatial clustering was identified globally among dogs with leptospirosis via the Cuzick-Edwards test, which has not been previously used to analyze human or canine leptospirosis cases in northern California. Given the expected nonrandom distribution of both case and control dogs, the Cuzick-Edwards test is a way to clarify the relative position of case and control animals.10 The significant clustering among case dogs from the second- through the sixth-order nearest neighbor means that case dogs were relatively close to each other, compared with control dogs. This correlated well with where case and control dogs resided and suggested that an independent test for clarification of specific locations of clusters could be beneficial.

On the basis of the spatial scan statistic, cases were identified throughout the San Francisco Bay Area and around Sacramento, Calif, with a significant spatial cluster identified in San Francisco, with a radius of 40.4 km. The moderate climate of coastal northern California is ideal for the proliferation of leptospires during certain times of the year. Additionally, the dense human population and urbanization around the entire San Francisco Bay region could be a contributing factor to spatial clustering of cases, given that this has been associated with an increased prevalence of leptospirosis cases in humans.22 After severe flooding in Rio de Janeiro during 2006, clusters of leptospirosis cases in humans were identified approximately 3 to 5 weeks after peak flooding among residents living near areas of solid waste accumulation and within the most severely flooded parts of the city.23 The specific cluster locations were areas of the city where vectors and humans would have an opportunity to overlap; in particular, dogs and rats were cited as the main reservoirs of leptospirosis during this outbreak.23 Similarly, the locations identified in the study reported here could be correlated not only to climate, but also to an overlap of vectors. Sea lions are abundant along the coast of northern California. An epidemic-endemic cycle of leptospirosis caused by serovar Pomona has been identified in California sea lions (Zalophus californianus), and sea lions have been identified as suspected reservoir or incidental hosts for this serovar.24–26 It is unclear how dogs and humans are affected by this cycle and to what degree sea lions contribute to zoonotic transmission of leptospirosis. Another possibility is that referral bias contributed to the distribution of cases, considering that 45% of case dogs referred to the Veterinary Medical Teaching Hospital in the present study received hemodialysis, an expensive but effective treatment modality for severe canine leptospirosis.27 The use of control dogs was important to mitigate the effects of possible referral bias; the results of the spatial scan comparing case and control dogs that incurred the highest costs did not identify significant clustering among case dogs, suggesting that such bias was not a contributing factor. These data were also consistent with that of previous studies5,6,27 in northern California. One of those studies27 found that 77% of cases occurring from 1990 through 1998 originated from coastal regions of the San Francisco Bay Area, whereas 14% of cases occurred in regions surrounding Sacramento, Calif. Given the large human population in San Francisco (> 776,773) and Sacramento (> 1.2 million) counties, it is possible that the distribution described for canine leptospirosis is related to human population density.h

A potential limitation of the study was the fact that we were unable to rule out the possibility that the control dogs were infected with leptospires. A serologic MAT was not performed on each control dog because the clinical signs in those dogs were not consistent with leptospirosis and this was a retrospective study. An ideal control group would consist of dogs with 2 negative serologic test results in samples taken 7 to 14 days apart together with negative results of another diagnostic test, such as PCR assay or immunohistochemical staining. However, the decision to use a randomly selected group of control dogs was made on the basis of a lack of available control dogs with negative test results for active leptospirosis during the same time period. During the period from 2001 to 2010, only 18 dogs had negative paired serologic MAT results reported, and 2 of those 18 dogs also underwent an additional diagnostic test for leptospirosis (PCR assay), the results of which were also negative. Performing the same statistical tests with these 18 dogs as part of the control group did not affect the outcome. Certainly, the problem of false-negative results for controls exists in any case-control study; however, given the likelihood that only a few potentially misclassified dogs were included as controls, the outcome would not be significantly affected. Prospective studies over a 10-year time period would be necessary to overcome this limitation.

Increased prevalence of leptospirosis is commonly reported in association with excessive rain, especially flooding, which creates environmental conditions appropriate to the survival and transmission of aquatic Leptospira spirochetes.4,18,28 In the present study, temporal clustering of 18 of 67 cases was identified during 13 of the 117 study months (May 2003 through May 2004). The remaining cases were evenly distributed across all months, excluding November and December 2003 and April 2004, when no cases were reported. The rainy season in northern California typically starts in October and extends through April.i Over the entire study period, most cases did occur during the rainiest time of the year; however, cases that were part of the 2003–2004 cluster occurred outside of the rainy season. This may be explained by weather patterns; from 2002 to 2006, and particularly during April 2003, greater precipitation than is typical was recorded.j The phenomenon of a delay between increased rainfall and case occurrence has been reported and is not understood completely, but a correlation between heavy rainfall and canine leptospirosis occurring 3 months later has been documented,29 and this may also have been the situation in the present study.

Leptospirosis is a potentially fatal zoonotic disease in dogs and occurs in densely populated, urban areas of northern California. Recent literature7,27 that indicated clusters of Leptospira seroreactivity in California was further quantified in the present study. Additionally, the most common serovar to which seroreactivity occurred in dogs from northern California was identified as Pomona, which differs from nationwide studies5,30 in which the highest titers reported among dogs were to serovar Grippotyphosa. Spatial and temporal analyses of leptospirosis in northern California helps fill in the current gaps in knowledge for public health practitioners by providing information that can inform vaccination strategies for dogs. Further information is necessary to provide the most complete epidemiological representation of this reemerging threat in humans and other species.

ABBREVIATIONS

CI

Confidence interval

MAT

Microscopic agglutination test

a.

Goldstein RE. Canine leptospirosis 2010: update on diagnosis, treatment, and prevention (abstr), in Proceedings. 82nd Annu West Vet Conf 2010.

b.

RANDOM.ORG. True random number service. Available at: www.random.org. Accessed Jan 1, 2011.

c.

GPS Visualizer. Available at: www.gpsvisualizer.com. Accessed Jan 1, 2011.

d.

California Spatial Information Library. Cal-Atlas geospatial clearinghouse. Available at: www.atlas.ca.gov. Accessed Jan 1, 2011.

e.

ArcGis, version 10.0, Environmental System Research Institute, Redland, Calif.

f.

SSTAT, version 4.70, University of California-Davis, Davis, Calif.

g.

SaTScan, version 9.1.1, M Kulldorff and Information Management Services Inc, Boston, Mass.

h.

US Census Bureau. 2000 California census. Available at: factfinder. census.gov/servlet/GCTTable?_bm=y&-geo_id=04000US06&-_box_head_nbr=GCT-PH1&-ds_name=DEC_2000_SF1_U&-format=ST-2. Accessed Aug 1, 2011.

i.

Western Regional Climate Center. California Climate. Available at: www.wrcc.dri.edu. Accessed Jun 1, 2011.

j.

Golden Gate Weather. Golden Gate Weather services links. Available at: ggweather.com/links.html. Accessed Jun 1, 2011.

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