Spatial and risk factor analyses of vector-borne pathogens among shelter dogs in the eastern United States

doi:10.21203/rs.3.rs-2757163/v1

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Research Article

Spatial and risk factor analyses of vector-borne pathogens among shelter dogs in the eastern United States

https://doi.org/10.21203/rs.3.rs-2757163/v1

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published 10 Jun, 2023

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Background

Vector-borne infections pose significant health risks to humans, domestic animals, and wildlife. Domestic dogs (Canis lupus familiaris) in the United States may be infected with and serve as sentinel hosts for several zoonotic vector-borne pathogens. In this study, we analyzed the geographic distribution, risk factors, and co-infections associated with infection with Ehrlichia spp., Anaplasma spp., Borrelia burgdorferi, and Dirofilaria immitis in shelter dogs in the eastern United States.

Methods

From 2016–2020, blood samples from 3,750 shelter dogs from 19 states were examined with IDEXX SNAP® 4Dx® Plus tests to determine prevalence of infection with tick-borne pathogens and infection with D. immitis. We assessed the impact of factors including age, sex, intact status, breed group, and location on infection using logistic regression.

Results

Regional variation in detection prevalence was noted: D. immitis (17.4%, n = 355/2,036) and Ehrlichia spp. (10.7%, n = 217/2,036) were highest in the Southeast while prevalence for B. burgdorferi (19.3%, n = 143/740) and Anaplasma spp. (5.7%, n = 42/740) were highest in the Northeast. Overall, 4.8% (n = 179/3,750) of dogs had co-infections, the most common of which were D. immitis/Ehrlichia spp. (1.6%, n = 59/3,750), B. burgdorferi/Anaplasma spp. (1.5%, n = 55/3,750), and B. burgdorferi/Ehrlichia spp. (1.2%, n = 46/3,750). Risk factors significantly influenced infection across the evaluated pathogens were location and breed group. All evaluated risk factors were significant for the prevalence of D. immitis antigens.

Conclusions

Our results demonstrate a regionally variable risk of infection with vector-borne pathogens in shelter dogs throughout the eastern United States, likely due to varying distributions of vectors. However, as many vectors are undergoing range expansions or other changes in distribution associated with climate and landscape change, continued vector-borne pathogen surveillance is important for maintaining reliable risk assessment.

co-infections

heartworm

tick-borne disease

vector-borne disease

Vector-borne infections pose significant health risks to humans, domestic species, and wildlife. Domestic dogs (Canis lupus familiaris) are susceptible to many vector-borne pathogens (VBP) of veterinary and public health concern [1–6] with some of the most studied pathogens being Dirofilaria immitis (heartworm), Borrelia burgdorferi (Lyme disease), Anaplasma spp. (anaplasmosis), and Ehrlichia spp. (ehrlichiosis) [7, 8]. Importantly, several of these pathogens are significant pathogens of domestic dogs [9]. Finally, because several of these pathogens are zoonotic, dogs can serve as sentinel hosts. Using Lyme disease as an example, seroprevalence of B. burgdorferi infections in dogs is associated with counties where human infections occur [6, 10]. Because of these reasons, understanding the epidemiology of vector-borne infections in dogs is important for both human and veterinary health.

Origin and history of individual dogs is key to effective surveillance of canine VBP. Generally, the domestic dog population can be divided into groups such as owned dogs with veterinary care, owned dogs without veterinary care, stray dogs, and shelter dogs. The assumption is that many owned dogs under veterinary care would receive a combination of preventatives specific to VBP and intestinal parasites [9, 11, 12]. Dogs without veterinary care (owned or not) and those that enter shelters (generally > 50% of which are strays) are likely to be at a higher risk of infection with VBP through increased environmental exposure and/or lack of preventatives [7, 13, 14]. Other potential risk factors associated with an increased likelihood of VBP infection include age and body condition [15]. Older dogs will have a higher probability of being exposed during their lifetime, and dogs in poor body condition may be immunologically compromised, increasing infection risk.

Co-infections of vertebrate hosts are common which may complicate diagnosis and treatment or increase the risk of severe disease [4, 16–18]. In general, co-infections occur with pathogens with a common vector and/or overlapping geographic ranges [4, 7, 9, 11, 12]. For the pathogens of interest in our study, D. immitis is a mosquito-borne parasite while the most common vector of B. burgdorferi and A. phagocytophilum is Ixodes scapularis, the most common vector of Ehrlichia canis is Rhipicephalus sanguineus and presumptively Anaplasma platys, and Amblyomma americanum is a common vector of Ehrlichia chaffeensis and Ehrilicia ewingii [7, 19].

The geographical distribution of tick species is changing, and thus the risk of co-infections is changing. This is reflected in the changes in the distribution and prevalence of canine VBP, highlighting the need for contemporary data [5, 8, 20–23]. In the southeastern United States, co-infections between D. immitis and Ehrlichia spp. have been common while co-infections with B. burgdorferi and A. phagocytophilum are more common in the upper Midwest and Northeast [1, 9, 11, 12]. The increasing detection of A. americanum in northeastern states could increase the risk of Ehrlichia infections in dogs in that region [24, 25]. Infection with many tick-borne pathogens cause similar clinical signs and presentations, but may require different treatments (e.g., Babesia spp.), thus knowing the risk of co-infections is important. The purpose of this study is to evaluate the prevalence of select VBP (D. immitis, Ehrlichia spp., Anaplasma spp., and B. burgdorferi) in shelter dog populations in the eastern United States and evaluate risk factors associated with detection and co-infections.

Sample Collections

From 2016–2020, we recruited shelters in 19 states to participate in the study. Focal areas included 97 counties in the eastern half of the United States and were selected due to known geographic ranges of the focal pathogens (Fig. 1). Participating shelters were either asked to test dogs that met the inclusion criteria or provide data that was collected using the same methods and inclusion criteria. To be included, dogs had to be 6 months of age or older and had to originate from the county or neighboring counties around the shelter. Dogs that were too young or under bite quarantine were excluded. Dog blood samples were tested using SNAP® 4Dx® Plus tests which were provided by IDEXX Laboratories and shipped directly to the shelter or to the University of Georgia (UGA) for sample testing. We requested shelters test between 50 and 200 dogs. Furthermore, SNAP® 4Dx® Plus data was provided by investigators from a related shelter study in Mississippi which included data collected from June 2016 through February 2017 [15]. The approximate age, location, date of when the sample was collected, estimated breed and the corresponding American Kennel Club (AKC) breed group, sex, and intact status were collected for each dog.

Data Analysis

Variables assessed as risk factors included age (< 1-year-old or ≥ 1-year-old), location, breed group, intact status, and sex. Dogs were classified into AKC breed groups based off dominant breed features because many of the dogs were of mixed breed. Each pathogen and co-infection combination were evaluated using binomial generalized linear models (GLMs) to assess the relationship between the risk factor and the SNAP® 4Dx® Plus test outcome (positive, negative). Significant results from the GLMs were further analyzed through pairwise comparison to calculate the odds ratio, confidence interval, and P-value using the lsmeans package [26]. All pathogens were assessed on an individual basis per pathogen and further analyzed through observed co-infection combinations, excluding dogs with not applicable values for the variable being analyzed. Statistical analyses were performed in R version 4.1.1 [27] and factors with P-values ≥ 0.05 were considered significant.

Population Data

The study included 3,750 dogs from 19 states and 97 counties with dogs per county ranging from 2 to 226. The demographic data of the dogs in our study population can be found in Table 1. Most dogs were ≥ 1 year and intact; similar numbers of males and females were sampled (Table 1). The AKC breed group with the largest representation was the terrier breed group (n = 1,185/3,750, 31.6%) (Table 1). Nearly half (n = 2,036/3,750, 54.3%) of the dogs were from the Southeast with the remaining were from the Midwest (n = 974/3,750, 26.0%) and Northeast (n = 740/3,750, 19.7%) (Table 1).

Table 1

Demographic data and prevalence of infection with vector-borne pathogens among 3,750 dogs from shelters in 19 states in the eastern United States
	No. of samples	Number of dogs positive (%)
	No. of samples	Dirofilaria immitis	Anaplasma spp.	Ehrlichia spp.	Borrelia burgdorferi
Total Sample	3750	419 (11.2)	90 (2.4)	299 (8.0)	332 (8.9)
Age group
< 1 years old	492	6 (1.2)	8 (1.6)	13 (2.6)	15 (3.0)
≥ 1 years old	3100	405 (13.1)	75 (2.4)	283 (9.1)	305 (9.8)
Unknown	158	8 (5.1)	7 (4.4)	3 (1.9)	12 (7.6)
Sex
Female	1938	202 (10.4)	47 (2.4)	154 (7.9)	178 (9.2)
Male	1686	213 (12.6)	39 (2.3)	143 (8.5)	145 (8.6)
Unknown	126	4 (3.2)	4 (3.2)	2 (1.6)	9 (7.1)
Intact Status
Intact	2163	312 (14.4)	47 (2.2)	191 (8.8)	180 (8.3)
Not-intact	1274	100 (7.8)	34 (2.7)	95 (7.5)	107 (8.4)
Unknown	313	7 (2.2)	9 (2.9)	13 (4.2)	45 (14.4)
AKC Breed Group
Herding	391	42 (10.7)	14 (3.6)	37 (9.5)	40 (10.2)
Hound	503	54 (10.7)	14 (2.8)	91 (18.1)	78 (15.5)
Non-Sporting	159	18 (11.3)	3 (1.9)	9 (5.7)	9 (5.7)
Sporting	466	60 (12.9)	26 (5.6)	32 (6.9)	52 (11.2)
Terrier	1185	169 (14.3)	17 (1.4)	71 (6.0)	86 (7.3)
Toy	418	15 (3.6)	1 (0.2)	13 (3.1)	12 (2.9)
Working	268	21 (7.8)	6 (2.2)	19 (7.1)	31 (11.6)
Unknown	360	40 (11.1)	9 (2.5)	27 (7.5)	24 (6.7)
Region/State
Northeast	740	12 (1.6)	42 (5.7)	34 (4.6)	143 (19.3)
Maine	189	2 (1.1)	22 (11.6)	4 (2.1)	44 (23.3)
Maryland	202	10 (5.0)	2 (1.0)	29 (14.4)	39 (19.3)
New Hampshire	37	0 (0)	2 (5.4)	1 (2.7)	5 (13.5)
New York	171	0 (0)	14 (8.2)	0 (0)	42 (24.6)
Pennsylvania	141	0 (0)	2 (1.4)	0 (0)	13 (9.2)
Midwest	974	52 (5.3)	19 (2.0)	48 (4.9)	66 (6.8)
Kansas	16	0 (0)	0 (0)	1 (6.3)	0 (0)
Minnesota	97	3 (3.1)	11 (11.3)	3 (3.1)	28 (28.9)
Missouri	335	36 (10.7)	2 (0.6)	37 (11.0)	1 (0.3)
North Dakota	2	0 (0)	0 (0)	0 (0)	0 (0)
Ohio	352	13 (3.7)	1 (0.3)	5 (1.4)	22 (6.3)
Wisconsin	172	0 (0)	5 (2.9)	2 (1.2)	15 (8.7)
Southeast	2036	355 (17.4)	29 (1.4)	217 (10.7)	123 (6.0)
Florida	372	59 (15.9)	0 (0)	18 (4.8)	3 (0.8)
Georgia	200	31(15.5)	0 (0)	9 (4.5)	1 (0.5)
Louisiana	177	59 (33.3)	1 (0.6)	4 (2.3)	0 (0)
Mississippi	116	35 (30.2)^a	0 (0)	21 (18.1)	0 (0)
North Carolina	197	56 (28.4)	0 (0)	52 (26.4)	7 (3.6)
Oklahoma	200	26 (13.0)	0 (0)	18 (9.0)	0 (0)
Tennessee	382	75 (19.6)	4 (1.0)	13 (3.4)	1 (0.3)
Virginia	392	14 (3.6)	24 (6.1)	82 (20.9)	111 (28.3)
^aHeartworm data from Mississippi is published (Donnett et al. 2018).

Dirofilaria immitis Antigen Prevalence

A total of 419 (11.2%, n = 3,750) dogs were positive for D. immitis antigens (Table 1, Fig. 2). Dogs < 1 year of age had a lower prevalence and were 12.2 times less likely to have D. immitis antigens detected compared with dogs ≥ 1 year of age (Tables 1 and 2). A higher prevalence was noted for males compared with females (Tables 1 and 2). Dogs that were intact were 2 times more likely to be positive compared to not-intact dogs (Tables 1 and 2). The prevalence of D. immitis antigens was lower in the toy breed group compared to the herding, hound, non-sporting, sporting, and terrier breed groups (Table 1, Table 2).

Table 2

Significant results of bivariable generalized linear model and pairwise comparison analysis of potential risk factors for seropositive status for vector-borne pathogens among 3,750 dogs from shelters in 19 states in the eastern United States
Pathogens and pairs of risk factor	OR	95% CI	P value
Dirofilaria immitis
Age Group
≥ 1 years old – <1 years old	12.2	5.4–27.4	< 0.0001
Sex
Male – Female	1.2	1.0–1.5	0.0418
Intact Status
Intact – Not-intact	2.0	1.6–2.5	< 0.0001
Breed Group
Herding – Toy	3.2	1.7–5.9	0.0032
Hound – Toy	3.2	1.8–5.8	0.0020
Non-Sporting – Toy	3.4	1.7–7.0	0.0120
Sporting – Toy	4.0	2.2–7.1	0.0001
Terrier – Toy	4.4	2.6–7.6	< 0.0001
Region
Midwest – Northeast	3.4	1.8–6.4	0.0005
Southeast – Midwest	3.7	2.8–5.1	< 0.0001
Southeast – Northeast	12.7	7.1–22.7	< 0.0001
Ehrlichiaspp.
Age Group
≥ 1 years old – <1 years old	3.7	2.1–6.5	< 0.0001
Breed Group
Herding – Toy	3.2	1.7–6.2	0.0073
Hound – Herding	2.1	1.4–3.2	0.0060
Hound – Non-Sporting	3.6	1.8–7.4	0.0067
Hound – Sporting	3.0	1.9–4.6	< 0.0001
Hound – Terrier	3.5	2.5–4.8	< 0.0001
Hound – Toy	6.8	3.7–12.4	< 0.0001
Hound – Working	2.9	1.7–4.8	0.0013
Region
Southeast – Midwest	2.3	1.7–3.2	< 0.0001
Southeast – Northeast	2.5	1.7–3.6	< 0.0001
Anaplasmaspp.
Breed Group
Sporting – Terrier	4.1	2.2–7.6	0.0002
Sporting – Toy	24.5	3.3–181.3	0.0288
Region
Northeast – Midwest	3.1	1.8–5.3	0.0002
Northeast – Southeast	4.2	2.6–6.8	< 0.0001
Borrelia burgdorferi
Age Group
≥ 1 years old – <1 years old	3.5	2.0–5.9	< 0.0001
Breed Group
Herding – Toy	3.8	2.0–7.4	0.0014
Hound – Non-Sporting	3.0	1.5–6.2	0.0388
Hound – Terrier	2.3	1.7–3.2	< 0.0001
Hound – Toy	6.1	3.3–11.5	< 0.0001
Sporting – Toy	4.2	2.2–8.0	0.0002
Terrier – Toy	2.6	1.4–4.9	0.0336
Working – Toy	4.4	2.2–8.8	0.0004
Region
Northeast – Midwest	3.3	2.4–4.5	< 0.0001
Northeast – Southeast	3.8	2.9–4.9	< 0.0001
OR = odds ratio; CI = confidence interval

Dirofilaria immitis antigen detection was highest in the Southeast (17.4%, n = 355/2,036) followed by the Midwest (5.3%, n = 52/974) and the Northeast (1.6%, n = 12/740) (Table 1, Fig. 1). The Midwest was 3.4 times more likely to have D. immitis antigen detection than the Northeast (Table 2). The Southeast was 3.7 times more likely to have D. immitis antigen detection than the Midwest and 12.7 times more likely than the Northeast (Table 2). An analysis of state vs. state comparisons is provided in Additional File 1: Text S1 and Table S1.

Ehrlichia spp. Antibody Prevalence

Ehrlichia spp. antibodies were detected in 8.0% (n = 299/3,750) of the dogs (Table 1, Fig. 2). Analyzed risk factors in relation to detection of Ehrlichia spp. antibodies of significance were age, breed group, and location (Table 2). Dogs ≥ 1 year of age were 3.7 times more likely to have Ehrlichia spp. antibody prevalence than dogs < 1 year of age (Table 2). The hound breed group had the highest prevalence of Ehrlichia spp. antibodies (Table 1). The hound group was at an increased risk of Ehrlichia spp. antibody detection compared to the other analyzed breed groups (Table 2). The herding breed group was found to be 3.2 times more likely to have Ehrlichia spp. antibody detected than the toy breed group (Table 2).

The highest prevalence of Ehrlichia spp. antibodies was documented in the Southeast (10.7%, n = 217/2,036) (Table 1, Fig. 1). The lowest prevalence was documented in the Northeast (4.6%, n = 34/740) and the Midwest had a prevalence of 4.9% (n = 48/974) (Table 1). The Southeast had a statistically higher risk of Ehrlichia spp. antibody prevalence (Table 4). The Southeast was 2.5 times more likely to have Ehrlichia spp. antibody prevalence than the Northeast and 2.3 times more likely than the Midwest (Table 2). An analysis of state vs. state comparisons is provided in Additional File 1: Text S2 and Table S2.

Table 4

Demographic data and prevalence of infection with the three most prevalent co-infection combinations (*Borrelia burgdorferi + Anaplasma* spp., *B. burgdorferi + Ehrlichia* spp., and *Dirofilaria immitis + Ehrlichia*) pathogens among 3,750 dogs from shelters in 19 states in the eastern United States
	n	Dirofilaria immitis + Ehrlichia spp. (%)	Borrelia burgdorferi + Ehrlichia spp. (%)	Borrelia burgdorferi + Anaplasma spp. (%)
Age group
< 1 years old	492	1 (0.20)	1 (0.20)	4 (0.81)
≥ 1 years old	3100	58 (1.87)	44 (1.42)	47 (1.52)
Unknown	158	0(0)	1 (0.63)	4 (2.53)
Sex
Female	1938	32 (1.65)	22 (1.14)	25 (1.29)
Male	1686	27 (1.60)	23 (1.36)	27 (1.60)
Unknown	126	0 (0)	1 (0.79)	3 (2.38)
Intact Status
Intact	2163	46 (2.13)	28 (1.29)	34 (1.57)
Not-intact	1274	13 (1.02)	13 (1.02)	16 (1.26)
Unknown	313	0 (0)	5 (1.60)	5 (1.60)
AKC Breed Group
Herding	391	6 (1.53)	4 (1.02)	10 (2.56)
Hound	503	12 (2.39)	22 (4.37)	9 (1.79)
Non-Sporting	159	3 (1.89)	1 (0.63)	0 (0)
Sporting	466	9 (1.93)	3 (0.64)	16 (3.43)
Terrier	1185	16 (1.35)	13 (1.10)	11 (0.93)
Toy	418	1 (0.24)	1 (0.24)	0 (0)
Working	268	3 (1.12)	1 (0.37)	2 (0.75)
Unknown	360	9 (2.50)	1 (0.28)	7 (1.94)
Region
Northeast	740	0 (0)	13 (1.76)	20 (2.70)
Maine	189	0 (0)	0 (0)	7 (3.70)
Maryland	202	0 (0)	13 (6.44)	1 (0.50)
New Hampshire	37	0 (0)	0 (0)	2 (5.41)
New York	171	0 (0)	0 (0)	9 (5.26)
Pennsylvania	141	0 (0)	0 (0)	1 (0.71)
Midwest	974	7 (0.72)	4 (0.41)	13 (1.33)
Kansas	16	0 (0)	0 (0)	0 (0)
Minnesota	97	0 (0)	1 (1.03)	9 (9.28)
Missouri	335	7 (2.09)	0 (0)	0 (0)
North Dakota	2	0 (0)	0 (0)	0 (0)
Ohio	352	0 (0)	3 (0.85)	1 (0.28)
Wisconsin	172	0 (0)	0 (0)	3 (1.74)
Southeast	2036	52 (2.55)	29 (1.42)	22 (1.08)
Florida	372	7 (1.88)	1 (0.27)	0 (0)
Georgia	200	3 (1.50)	0 (0)	0 (0)
Louisiana	177	4 (2.26)	0 (0)	0 (0)
Mississippi	116	9 (7.76)	0 (0)	0 (0)
North Carolina	197	22 (11.17)	2 (1.02)	0 (0)
Oklahoma	200	2 (1.00)	0 (0)	0 (0)
Tennessee	382	1 (0.26)	0 (0)	0 (0)
Virginia	392	4 (1.02)	26 (6.63)	22 (5.61)
n = total number of samples

Anaplasma spp. Antibody Prevalence

Anaplasma spp. antibodies were detected in 2.4% (n = 90/3,750) of the dogs (Table 1, Fig. 2). Risk factors that were significant in relation to Anaplasma spp. antibody prevalence included breed group and location (Table 2). The sporting breed group had the highest prevalence of Anaplasma spp. antibodies of 5.6% (n = 26/466) (Table 1). The sporting breed group was at an increased risk of Anaplasma spp. antibody prevalence compared to the terrier and toy breed groups (Table 2). The sporting breed group was 4.1 times more likely to have Anaplasma spp. antibodies detected than the terrier breed group (Table 2). The sporting breed group was 24.5 times more likely to have Anaplasma spp. antibodies detected than the toy breed group (Table 2).

The highest detection prevalence of Anaplasma spp. antibodies was documented in the Northeast (5.7%, n = 42/740) (Table 1, Fig. 1) followed by the Midwest (2.0%, n = 19/974) and the Southeast (1.4%, n = 29/2,036) (Table 1, Fig. 1). The Northeast was 4.2 times and 3.1 times more likely to have Anaplasma spp. antibodies compared with the Southeast and Midwest, respectively (Table 2). An analysis of state vs. state comparisons is provided in Additional File 1: Text S3 and Table S3.

Borrelia burgdorferi Antibody Prevalence

Borrelia burgdorferi antibodies were detected in 8.9% (n = 332/3,750) of dogs (Table 1, Fig. 2). Analyzed risk factors in relation to detection of B. burgdorferi antibodies of significance were age, breed group, and location (Table 2). Dogs ≥ 1 year of age were 3.5 times more likely to have B. burgdorferi antibodies compared with dogs < 1 year of age (Tables 1 and 2). The hound breed group had the highest prevalence of B. burgdorferi antibodies (15.5%, n = 78/503) (Table 1). The herding, hound, sporting, terrier, and working breed groups had a significantly higher prevalence of B. burgdorferi compared to the other analyzed breed groups (Table 2). Additionally, the toy breed group (2.9%, n = 12/418) had a decreased risk of B. burgdorferi antibody detection (Table 2).

The highest B. burgdorferi antibody prevalence was documented in the Northeast (19.3%, n = 143/740) followed by the Midwest (6.8%, n = 66/974) and the Southeast (6.0%, n = 123/2,036) (Table 1, Fig. 1). The Northeast had an increased risk of B. burgdorferi antibody detection which was 3.3 times more likely than the Midwest and 3.8 times more likely than the Southeast (Table 2, Fig. 1). An analysis of state vs. state comparisons is provided in Additional File 1: Text S4 and Table S4.

Co-infections

There were nine different co-infection combinations observed in 179 dogs (Table 3, Fig. 2). The three most prevalent co-infections were B. burgdorferi + Anaplasma spp. (1.47%, n = 55/3,750), B. burgdorferi + Ehrlichia spp. (1.23%, n = 46/3,750), and D. immitis + Ehrlichia spp. (1.57%, n = 59/3,750) (Table 3, Table 4, Fig. 2, Fig. 3).

Table 3

Co-infections among 3,750 dogs from shelters in 19 states in the eastern United States
Pathogens			No. of co-infections	Location	Prevalence (%)
Dirofilaria immitis	Borrelia burgdorferi	Ehrlichia spp.	4	NC, VA	0.11
D. immitis	B. burgdorferi	Anaplasma spp.	2	ME	0.05
B. burgdorferi	Anaplasma spp.	Ehrlichia spp.	5	ME, MD, MN, VA	0.13
D. immitis	Ehrlichia spp.		59	FL, GA, LA, MS, MO, NC, OK, TN, VA	1.57
D. immitis	Anaplasma spp.		1	TN	0.03
D. immitis	B. burgdorferi		6	FL, MD, MO, OH	0.16
B. burgdorferi	Ehrlichia spp.		46	FL, MD, MN, NC, OH, VA	1.23
B. burgdorferi	Anaplasma spp.		55	MD, ME, MN, NH, NY, OH, PA, VA, WI	1.47
Anaplasma spp.	Ehrlichia spp.		1	MO	0.03
Total Co-infections			179		4.77

For all three of these co-infection pairs, location was a significant risk factor (Table 5). The B. burgdorferi + Anaplasma spp. pair was more likely to be detected in the Northeast compared the Southeast (Tables 4 and 5, Fig. 3). The co-infection combination between B. burgdorferi + Ehrlichia spp. was mostly observed in the Northeast and was significantly more likely to be detected in the Northeast versus the Midwest, although all of the Northeast positives were from Maryland (Table 5, Fig. 3). The co-infection pair of D. immitis + Ehrlichia spp. was significantly more likely to occur in the Southeast compared with the Midwest and no cases were noted in the Northeast (Tables 4 and 5, Fig. 3).

Table 5

Significant results of binomial generalized linear model and pairwise comparison analysis of potential risk factors for positive status for the three most common coinfections noted in this study among 3,750 dogs from shelters in 19 states in the eastern United States
Pairs and Risk Factors	OR	95% CI	P value
Dirofilaria immitis + Ehrlichia spp.
Age Group
≥ 1 years old – <1 years old	9.3	1.3–67.3	0.0269
Intact Status
Intact – Not-intact	2.1	1.1–3.9	0.0185
Region
Southeast – Midwest	3.6	1.2–11.1	0.0042
Borrelia burgdorferi + Ehrlichiaspp.
Breed Group
Hound – Sporting	7.0	2.1–23.6	0.0272
Hound – Terrier	4.1	2.1–8.2	0.0013
Region
Northeast – Midwest	4.4	1.4–13.5	0.0275
Borrelia burgdorferi + Anaplasmaspp.
Breed Group
Sporting – Terrier	3.8	1.8–8.3	0.0131
Region
Northeast – Southeast	2.6	1.4–4.7	0.0072
OR = odds ratio; CI = confidence interval

There were also significant associations for breed group for co-infections B. burgdorferi + Anaplasma spp. and B. burgdorferi + Ehrlichia spp. (Table 5). The sporting breed group was 3.8 times more likely to have co-infections with B. burgdorferi + Anaplasma spp. than the terrier breed group (Table 5). The hound breed group was 7.0 times more likely to have co-infections with B. burgdorferi + Ehrlichia spp. than the sporting breed group and 4.1 times more likely than the terrier breed group (Table 5).

Additional risk factors for co-infections with D. immitis + Ehrlichia spp. were age group and intact status (Table 5). Dogs that were ≥ 1 year of age were 9.3 times more likely to have a co-infection with D. immitis + Ehrlichia spp. compared with dogs < 1 year of age (Table 5). Dogs that were intact were 2.1 times more likely to have co-infections with D. immitis + Ehrlichia spp. than dogs that were not intact (Table 5).

In the present study, we investigated the prevalence of VBP (D. immitis, Ehrlichia spp., Anaplasma spp., and B. burgdorferi) in shelter dogs in the eastern United States from 2016 to 2020. We found regional prevalence variation of all pathogens and several risk factors (age, sex, breed group, and intact status) were associated with infection. We also observed several different co-infection combinations with B. burgdorferi + Anaplasma spp., B. burgdorferi + Ehrlichia spp., and D. immitis + Ehrlichia spp. being the most frequently detected. This study provides contemporary data on the prevalence of these pathogens in a group of dogs that are expected to have limited veterinary care or preventive use. High prevalence and detection outside of known endemic regions highlights the need for continued monitoring.

Knowledge on the accurate distribution of pathogens is critically important for veterinarians and clients to gauge the risk of disease in dogs and other possible hosts. In general, the geographic distributions for the VBP were consistent with the known geographic ranges reported in previous studies for both the pathogens and vectors [1, 4, 5, 9, 11, 12, 15, 16, 22, 28]. However, there were some notable findings. We detected a low prevalence (1.1%, n = 2/189) of D. immitis in Maine which historically has few heartworm detections (< 0.5%) [11]. Detection of D. immitis outside the known endemic range is often assumed to be related to travel or translocated dogs from heartworm endemic regions. However, the inclusion criteria of this study should have excluded most translocated dogs, and our findings are supported by increasing heartworm prevalence trends in the far Northeast and other regions (e.g., Colorado) [11, 21, 29, 30]. The potential for local transmission in non-endemic regions highlights the need for heartworm preventative use. In addition, we noted a higher prevalence of B. burgorferi infection in dogs from Virginia compared to past studies [11] which corresponds with reported changes in the distribution of this pathogen in dogs and people and its vector in Virginia [8, 31–34]. Continued studies on the distribution of VBP are warranted as changes in the distribution and density of vectors and their associated pathogens has been noted in recent years which may be related to several factors such as climate or habitat changes [5, 8, 20–23, 35]. Additionally, novel vectors (e.g., Asian longhorned tick, Haemaphysalis longicornis) have been introduced into the United States and this tick may alter the native pathogen transmission dynamics [36–38].

Consistent with previous studies, dogs that were ≥ 1 year of age had an increased risk of being positive [7, 15]. Tick-borne pathogen infection was assessed with the detection of antibodies which may be persistent; older dogs have an increased time at risk of exposure, increasing the likelihood of infection to the vector and pathogen. Heartworm infections also typically occur in older dogs as this parasite has a long-life cycle and older dogs have increased time for mosquito exposure [39]. We also found that intact dogs were more likely to be infected with D. immitis compared with non-intact dogs, who may be more likely to have previous access to veterinary care or preventative medications. Other studies have also noted that intact dogs had higher rates of VBP infection [40, 41] and tick exposure [42].

Interestingly, we found that, breed group was associated with changes in infection risk. Our findings indicate that the toy breed group specifically had a lower risk of infection for all pathogens which is consistent with a previous study on ticks [42]. The decreased risk of infection for the toy breed group may be due to the popularity of these dogs in urban settings or that smaller dogs likely spend less time outdoors. Similarly, larger breed groups (e.g., hound, herding, sporting) had higher prevalence of infection which may be related to more time spent outdoors. There may also be spatial differences in breed distribution because of different trends in owner popularity and dog utility. For example, both D. immitis and Ehrlichia were more common in large breed groups that are popular outdoor dogs in Southern states. Although this study focused on VBP, similar results (increased risk of parasitic infections for large breed groups) has been noted in other parasite systems (e.g., Dracunculus) [43, 44].

In general, the prevalence of pathogens included in this study were comparable to previous shelter-based studies conducted in the same regions using similar methods (e.g., 16.0% D. immitis prevalence in Texas) [7]. However, our prevalence rates for D. immitis, B. burgdorferi, and Ehrlichia spp. were higher than other studies primarily conducted on owned dogs and public data available on the Companion Animal Parasite Council (CAPC) website [11, 28]. Our observed higher prevalence rates most likely were because our sample collection was from shelter dogs and > 50% of the dogs that enter a shelter are considered strays [13]. These dogs are expected to have decreased access to veterinary care and therefore preventative medications. Further analysis of this association is reported separately [45].

Dogs are not exposed to vectors or pathogens in isolation and most geographic regions have multiple vectors and pathogens co-circulating. Many large serosurvey studies on dogs and pathogen infection are unable to examine co-infections because testing data are not associated with individual cases [11, 21]. However, prospective studies, such as this one, provide opportunities to examine patterns of co-infections [7]. Although we detected nine co-infections groups, including 11 dogs with infection with three pathogens, the most common pairs were B. burgdorferi + Anaplasma spp., B. burgdorferi + Ehrlichia spp., and D. immitis + Ehrlichia spp. The most likely explanation for the increased frequency between these three combinations is because of the pathogens shared ranges and vectors. Anaplasma phagocytophilum and B. burgdorferi have overlapping ranges in the Northeast, which was the region of highest prevalence documented in our study and share the same vector (I. scapularis) [9, 46]. Co-infections between B. burgdorferi and Ehrlichia spp., and D. immitis and Ehrlichia spp. were most likely more common due to overlapping ranges. The most likely Ehrlichia spp. that was detected most is the E. canis species due to a strong documented prevalence in the South [9].

In this study, we analyzed seroprevalence data for VBP in 3,750 dogs sampled in shelters from 97 counties in 19 states in the eastern United States. In general, we found D. immitis and Ehrlichia spp. prevalence to be highest in the Southeast and Anaplasma spp. and B. burgdorferi prevalence to be highest in the Northeast which is consistent with previous studies and expected vector ranges. Co-infections that were most common were between B. burgdorferi + Anaplasma spp., B. burgdorferi + Ehrlichia spp., and D. immitis + Ehrlichia spp. We found decreased risks of infection in dogs that were less than one year of age, in toy breed group, and dogs that had been spayed or neutered. In general, we found increased risks of infection in dogs that were greater than one age and in the hound breed group. However, some pathogens were detected outside their typical range so these data support previous studies that show an expanding range for these pathogens and/or vector species highlighting the need for continued surveillance and assessment of risk factors in both owned and unowned dogs.

Acknowledgements

With much gratitude, we thank IDEXX Laboratories Inc. for sharing data from their database that was collected from shelters and for providing the SNAP® 4Dx® Plus tests that were used by the shelters that participated in this study.

Funding

JRG was funded by the Companion Animal Parasite Council (CAPC). The funders had no role in any part of the study or manuscript.

Availability of data and materials

Aggregated data from shelters is provided in the manuscript and available from the corresponding author on reasonable request.

Authors’ contributions

JRG, CMH, CAC, and MJY designed this study and contributed to the interpretation of the results. CMH, CAC, and MJY wrote the manuscript. AVS and KH provided data from Mississippi for the analysis. CMH, JRG, CAC, MJY, AVS, AAM, KH, KWB, and MJY reviewed and edited. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable (prospective shelter data were obtained during routine testing of dogs under shelter guidelines).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Spatial and risk factor analyses of vector-borne pathogens among shelter dogs in the eastern United States

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