Abstract
This study aimed to determine the seroprevalence and geographical distribution of Ehrlichia spp., Anaplasma spp., Borrelia burgdorferi and Dirofilaria immitis in dogs in Mexico, including owned dogs from veterinary clinics with regular medical care and shelter dogs. The Mexican territory was divided into eight geographical regions; 22 out of 32 states were included; 110 veterinary clinics and 53 dog shelters participated. SNAP® 4Dx Plus® (IDEXX® Laboratories) was used to detect antibodies against Ehrlichia spp., Anaplasma spp., Borrelia burgdorferi and Dirofilaria immitis antigens. A total of 3522 apparently healthy dogs were tested, 1648 from clinics and 1874 from shelters. The highest seroprevalence of infection/exposure was found for Ehrlichia spp. (30.9%), followed by Anaplasma spp. (14.6%), D. immitis (5.3%) and B. burgdorferi (0.1%). Significantly more positive dogs were older than 3 years. Regarding differences between facility types, there were only differences for D. immitis which was more prevalent in clinics than in shelters (OR = 1.97; 95% CI: 1.45–2.69; P < 0.0001). Co-infections were detected in 38.4% of the positive samples. Dogs from Mexican states located on the Atlantic and the Pacific coast were significantly more at risk for Ehrlichia spp. and Anaplasma spp. infections than dogs from interior states. Dogs in Atlantic coastal states were more at risk for Dirofilaria immitis infection.
Keywords: Canine vector-borne diseases, Dogs, ELISA rapid test, Geographical distribution, Mexico
Graphical abstract
Highlights
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Seroprevalence of infection/exposure to vector-borne pathogens in 3522 dogs all over Mexico.
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Analysis of geographical distribution of Ehrlichia, Anaplasma, Borrelia and Dirofilaria infections.
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Highest seroprevalence for Ehrlichia spp. (30.9%), and lowest for Borrelia burgdorferi (0.1%).
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Significantly higher seroprevalence in coastal states compared to inner states.
1. Introduction
Vector-borne diseases of companion animals are caused by parasites, bacteria, or viruses transmitted by the bite of hematophagous arthropods (mainly ticks and mosquitoes) (Beugnet & Marié, 2009). Worldwide, the most important canine vector-borne diseases (CVBD) include anaplasmosis, ehrlichiosis, borreliosis and dirofilariosis (Baneth et al., 2012). In North America, dirofilariosis, or heartworm disease caused by Dirofilaria immitis, is the most critical helminthosis affecting dogs due to its clinical severity (Bowman et al., 2009). The spirochete Borrelia burgdorferi, the causative agent of Lyme disease, is endemic in North America, with the main clinical manifestations in dogs being arthritis and nephritis (Littman et al., 2018). Anaplasmosis and ehrlichiosis (caused by Anaplasma spp. and Ehrlichia spp., respectively) are infections that can cause fever, hemorrhages, depression, myalgia, anorexia, and thrombocytopenia in affected dogs (Rikihisa, 1991). Regarding Anaplasma spp. pathogens, two species commonly infect dogs, Anaplasma phagocytophilum, the agent of the granulocytic anaplasmosis, transmitted by Ixodes spp. ticks, and Anaplasma platys, the agent of the thrombocytic anaplasmosis, transmitted by Rhipicephalus sanguineus (Snellgrove et al., 2020). Regarding Ehrlichia spp., three species are described in North America, Ehrlichia canis transmitted by Rhipicephalus sanguineus and Ehrlichia ewingii and Ehrlichia chaffeensis transmitted by Amblyomma spp. ticks. The serological tests cross-react between the Anaplasma and Ehrlichia species, respectively, and without a PCR identification, it is not possible to conclude on the species based on serology (Chandrashekar et al., 2010).
Nationwide Mexican prevalences of E. canis, Anaplasma spp., B. burgdorferi and D. immitis were reported by Ochoa (2003), Nuñez (2003) and Movilla et al. (2016). The seropositivity of dogs to Anaplasma spp. and E. canis was reported in Campeche (Rojero-Vázquez et al., 2017) and in Yucatán (Rodriguez-Vivas et al., 2005; Ojeda-Chi et al., 2019) while B. burgdorferi was serologically reported in dogs in Mexicali (García et al., 2008). Regarding D. immitis, there are some reports on its prevalence in dogs in Yucatán Peninsula from 2007 to 2018 (Bolio-Gonzalez et al., 2007; Caro-Gonzalez et al., 2011; Torres-Chable et al., 2018).
This survey aimed to determine the seroprevalence of Ehrlichia spp., Anaplasma spp., B. burgdorferi and D. immitis in dogs in veterinary clinics and shelters in different states of Mexico during 2019–2020 including a larger number of dogs than the previous surveys.
2. Materials and methods
2.1. Source of data
One hundred and ten veterinary clinics and 53 dog shelters located in 22 out of the 32 Mexican states were included in this study. The sites were recruited in states from the eight national geo-economic regions, according to the methodology applied by Movilla et al. (2016): northwestern (Baja California, Baja California Sur, Sinaloa and Sonora), northeastern (Nuevo León and Tamaulipas), western (Colima, Jalisco and Nayarit), eastern (Puebla, Tlaxcala and Veracruz), northcentral (Aguascalientes and San Luis Potosi), southcentral (State of Mexico, Mexico City and Morelos), southeastern (Campeche, Quintana Roo, Tabasco and Yucatán) and southwestern (Guerrero) (Fig. 1). The 22 states included in the survey were distributed within the four quartiles of the distribution of annual rainfall by state, including the most dry (Baja California Sur, 179 mm/year) and the most wet (Tabasco, 4050 mm/year) states, based on the records on mean annual precipitation by states collected from 2000 to 2017 (SEMARNAT, 2019).
Fig. 1.
Mexican geo-economic regions and states included in the study. Abbreviations: Cd. de México, Mexico City; Edo. México, State of Mexico.
From December 2019 to February 2020, personnel at participating locations were instructed to test dogs meeting the following inclusion criteria: apparently healthy; older than 1 year; owned dogs with a history of regular outdoor activity and not having received anthelminthic treatments with macrocyclic lactones in 2 months nor ectoparasiticide treatments 1 month before collecting samples; shelter dogs should not have received anthelminthic treatments with macrocyclic lactones 2 months before or ectoparasiticide treatments 1 month before collecting the sample; consent from the owner to collect the sample, and, for care centers, the consent of the corresponding authority.
2.2. Diagnostic testing
Peripheral blood (0.5–1.0 ml) was collected from a vessel on dog’s arm in EDTA tubes. According to the instructions by the manufacturer, whole blood samples from dogs were tested with the ELISA kit SNAP® 4Dx® Plus from IDEXX® (Westbrook, Maine, USA). The SNAP tests were performed on site immediately after blood sampling. This assay screens for the simultaneous qualitative detection of a circulating carbohydrate of D. immitis adult female antigen, and antibodies, both IgG and IgM, against proteins from Ehrlichia spp., Anaplasma spp. and B. burgdorferi. Reported sensitivity and specificity of in-clinic ELISA for detection of antibodies are 96.2 and 100% for Ehrlichia spp., 99.1 and 100% for Anaplasma spp., and 98.8 and 100% for B. burgdorferi. Reported sensitivity and specificity for detection of heartworm antigens are 99.2 and 100%, respectively (Chandrashekar et al., 2010). The tests were read visually.
2.3. Statistical analysis
Data from the participating veterinary clinics and dog shelters were organized by state and regional groups (northwest, northeast, west, east, northcentral, southcentral, southeast and southwest) along with information on age (> 1 to < 3, ≥ 3-year-old) (Evason et al., 2019) and sex of the patients. Chi-square test and logistic regression were applied using Minitab 18 (Minitab, Inc. State College, Pennsylvania, USA). The level of significance for differences between variables in the analysis was set at P < 0.05. Maps on the seroprevalence by region and state for each of the four pathogens in the study were generated using ArcMap 10.7.1 (ESRI. Redlands, California, USA).
3. Results
A total of 3522 diagnostic test results from the 110 clinics and the 53 dog shelters from 22 Mexican states were performed, which is the largest seroprevalence survey conducted in Mexico.
The presence of Ehrlichia spp. and Anaplasma spp. antibodies was detected in every region. The presence of B. burgdorferi antibodies was only detected in four states. Dirofilaria immitis antigen was identified in four regions, except the northcentral and southwestern ones (Table 1, Table 2).
Table 1.
Percent positive test results in dogs by regions and states for Ehrlichia spp., Anaplasma spp., Borrelia burgdorferi and Dirofilaria immitis.
| State |
Ehrlichia spp. |
Anaplasma. spp. |
Borrelia burgdorferi |
Dirofilaria immitis |
|---|---|---|---|---|
| (n/N) | (n/N) | (n/N) | (n/N) | |
| Northwest | ||||
| Baja California | 51.3 (81/158) | 32.9 (52/158) | 0 (0/158) | 0 (0/158) |
| Baja Califonia Sur | 40.2 (68/169) | 18.9 (32/169) | 0 (0/169) | 3.0 (5/169) |
| Sinaloa | 52.3 (68/130) | 16.9 (22/130) | 0 (0/130) | 9.2 (12/130) |
| Sonora | 32.7 (52/159) | 8.8 (14/159) | 0 (0/159) | 3.8 (6/159) |
| Regional mean | 43.7 (269/616) | 19.5 (120/616) | 0 (0/616) | 3.7 (23/616) |
| Northeast | ||||
| Nuevo León | 25.8 (40/155) | 7.1 (11/155) | 0 (0/155) | 1.3 (2/155) |
| Tamaulipas | 33.5 (57/170) | 11.8 (20/170) | 1.2 (2/170) | 37.1 (63/170) |
| Regional mean | 29.8 (97/325) | 9.5 (31/325) | 0.6 (2/325) | 20.0 (65/325) |
| West | ||||
| Colima | 47.3 (79/167) | 27.5 (46/167) | 0.6 (1/167) | 0 (0/167) |
| Jalisco | 19.4 (32/165) | 6.1 (10/165) | 0 (0/165) | 0 (0/165) |
| Nayarit | 32.7 (53/162) | 17.9 (29/162) | 0 (0/162) | 0.6 (1/162) |
| Regional mean | 33.2 (164/494) | 17.2 (85/494) | 0.2 (1/494) | 0.2 (1/494) |
| East | ||||
| Puebla | 0 (0/145) | 0 (0/145) | 0 (0/145) | 0 (0/145) |
| Tlaxcala | 0 (0/114) | 0 (0/114) | 0 (0/114) | 0 (0/114) |
| Veracruz | 39.2 (65/166) | 19.3 (32/166) | 0 (0/166) | 12.0 (20/166) |
| Regional mean | 15.3 (65/425) | 7.5 (32/425) | 0 (0/425) | 4.7 (20/425) |
| Northcentral | ||||
| Aguascalientes | 4.0 (6/149) | 0.7 (1/149) | 0 (0/149) | 0 (0/149) |
| San Luis Potosí | 10.1 (16/158) | 10.8 (17/158) | 0 (0/158) | 0 (0/158) |
| Regional mean | 7.2 (22/307) | 5.9 (18/307) | 0 (0/307) | 0 (0/307) |
| Southcentral | ||||
| Ciudad de México | 3.1 (5/163) | 0 (0/163) | 0 (0/163) | 0 (0/163) |
| México | 0.9 (2/231) | 0 (0/231) | 0 (0/231) | 0 (0/231) |
| Morelos | 21.8 (36/165) | 6.7 (11/165) | 0 (0/165) | 0.6 (1/165) |
| Regional mean | 7.7 (43/559) | 2.0 (11/559) | 0 (0/559) | 0.2 (1/559) |
| Southeast | ||||
| Campeche | 66.0 (103/156) | 39.7 (62/156) | 0 (0/156) | 10.9 (17/156) |
| Quintana Roo | 37.7 (63/167) | 24.6 (41/167) | 0 (0/167) | 12.0 (20/167) |
| Tabasco | 55.3 (94/170) | 19.4 (33/170) | 0.7 (1/170) | 16.5 (28/170) |
| Yucatán | 47.0 (78/166) | 22.9 (38/166) | 0 (0/166) | 4.2 (7/166) |
| Regional mean | 51.3 (338/659) | 26.4 (174/659) | 0.2 (1/659) | 10.9 (72/659) |
| Southwest | ||||
| Guerrero | 67.2 (92/137) | 32.1 (44/137) | 0.7 (1/137) | 0 (0/137) |
| Country mean | 30.9 (1090/3522) | 14.6 (515/3522) | 0.1 (5/3522) | 5.2 (182/3522) |
Abbreviations: n, number positive; N, number tested.
Table 2.
Percent positive test results in dogs by age, sex, and dog origin for Ehrlichia spp., Anaplasma spp., Borrelia burgdorferi and Dirofilaria immitis.
| Variable | No. of seropositive dogs (%) |
||||
|---|---|---|---|---|---|
| Total | Ehrlichia spp. | Anaplasma spp. | B. burgdorferi | D. immitis | |
| Age | |||||
| < 3 years (n = 915) | 276 (30.2)a | 233 (25.5)a | 131 (14.3)a | 3 (0.3)a | 49 (3.9)a |
| ≥ 3 years (n = 2241) | 829 (37.0)b | 720 (32.1)b | 320 (14.3)a | 2 (0.1)a | 133 (5.9)b |
| Sex | |||||
| Female (n = 1939) | 682 (35.2)a | 508 (29.9)a | 286 (14.7)a | 1 (0.1)a | 91 (4.7)a |
| Male (n = 1489) | 552 (37.1)a | 480 (32.2)a | 217 (14.6)a | 4 (0.3)a | 86 (5.8)a |
| Facility type | |||||
| Clinic (n = 1648) | 596 (36.2)a | 488 (29.6)a | 221 (13.4)a | 4 (0.2)a | 114 (6.9)a |
| Shelter (n = 1874) | 676 (36.1)a | 602 (32.1)a | 294 (15.7)a | 1 (0.1)a | 68 (3.6)b |
Note: Different superscript letters indicate significant differences between variable states, P < 0.05.
3.1. Ehrlichia spp. infection
The seroprevalence to Ehrlichia spp. was 30.9% (1090/3522), nationwide. At the regional level it was ranked as follows: southwest (67.2%), southeast (51.3%), northwest (43.7%), west and northeast (33.2% and 29.8%, respectively), east (15.3%), and southcentral and northcentral (7.7% and 7.2%, respectively) (Table 1, Fig. 2).
Fig. 2.
Seroprevalence of Ehrlichia spp. in dogs grouped according to the percentage of positive tests by region (A) and state (B).
The states with >30% of seropositive tests to Ehrlichia spp. were located in the Atlantic and Pacific coasts, while the states from the interior resulted in < 30% of positive tests (Fig. 2). The 8 states from the interior averaged 8.2% (105/1280) of positive tests, which is significantly different from the average of 46.2% (460/995) for the Atlantic states (χ2 = 433, P < 0.0001) and the average of 42.1% (525/1247) for the Pacific states (χ2 = 387, P < 0.0001).
Dogs 3-year-old or older presented a significantly higher percentage of positive results to Ehrlichia spp. (χ2 = 13.7, P < 0.0001) compared to dog under 3-year-old, 32.1% (720/2241) vs 25.5% (233/915), respectively (Table 2). Neither sex nor origin of the dogs (veterinary clinics vs shelters) appeared to be risk factors (Table 3).
Table 3.
Risk factors for positivity to CVBD agents.
| Dependent variable risk factor | OR | 95% CI | P-value |
|---|---|---|---|
| Seropositivityto one of the tested CVBD agents | |||
| Age | 1.36 | 1.15–1.60 | <0.0001 |
| Sex | 1.09 | 0.94–1.25 | 0.251 |
| Veterinary clinic vs dog shelter | 1.00 | 0.87–1.15 | 0.955 |
| Positivity toEhrlichiaspp. | |||
| Age | 1.39 | 1.17–1.65 | <0.0001 |
| Sex | 1.11 | 0.96–1.29 | 0.145 |
| Veterinary clinic vs dog shelter | 0.89 | 0.77–1.03 | 0.108 |
| Positivity toAnaplasmaspp. | |||
| Age | 1.00 | 0.80–1.24 | 0.980 |
| Sex | 0.99 | 0.81–1.19 | 0.885 |
| Veterinary clinic vs dog shelter | 0.83 | 0.69–1.01 | 0.056 |
| Positivity toB. burgdorferi | |||
| Age | 0.27 | 0.05–1.63 | 0.154 |
| Sex | 5.22 | 0.58–6.75 | 0.140 |
| Veterinary clinic vs dog shelter | 4.56 | 0.51–0.81 | 0.175 |
| Positivity toD. immitis | |||
| Age | 1.80 | 1.21–2.68 | 0.004 |
| Sex | 1.24 | 0.92–1.69 | 0.156 |
| Veterinary clinic vs dog shelter | 1.97 | 1.45–2.69 | 0.0001 |
Notes: Levels by factor: Age (≥ 3-year-old vs < 3-year-old); Sex (male vs female); Facility type (clinic vs shelter).
Abbreviations: OR, odds ratio; CI, confidence interval.
3.2. Anaplasma infection
The seroprevalence for Anaplasma spp. in Mexico was 14.6% (515/3522), being highest in the southeast and southwest (26.4% and 32.1%, respectively) (Table 1). In contrast, the lowest seroprevalence was detected in the southcentral region (2.0%) (Fig. 3).
Fig. 3.
Seroprevalence of Anaplasma spp. in dogs grouped according to the percentage of positive tests by region (A) and state (B).
The states with > 11% of positive tests to Anaplasma spp. were located in the Atlantic and Pacific coasts of the country (Fig. 3). The eight interior states averaged 3.13% (40/1280) of positive tests to Anaplasma spp., significantly different from the 22.7% (226/995) of Atlantic states (χ2 = 208, P < 0.0001) and from the 19.9% (249/1247) of Pacific states (χ2 = 177, P < 0.0001).
No age effect and no sex effect were observed. The origin of dogs, veterinary clinics vs shelters, did not appear to be a risk factor (Table 3).
3.3. Borrelia burgdorferi infection
Percent positive test results to B. burgdorferi were reported for only five cases out of 3522 samples (0.1%) (Table 1). There were two cases in the northeastern (2/325; 0.6%), one in the western (1/494; 0.2%), one in the southeastern (1/659; 0.1%), and one in the southwestern (1/137; 0.7%) regions (Fig. 4). Due to the low seroprevalence, no risk factor was found (Table 3).
Fig. 4.
Seroprevalence of Borrelia burgdorferi in dogs grouped according to the percentage of positive tests by region (A) and state (B).
3.4. Dirofilaria immitis infection
For D. immitis, the nationwide seroprevalence was 5.2% (182/3522) (Table 1). The percent of positive test results were highest in the northeast (20.0%) compared to the other regions. The lowest percentage was detected in the southcentral (0.2%) and western (0.2%) regions. No positive results were reported for the northcentral (0.0%) and southwestern (0.0%) regions (Fig. 5).
Fig. 5.
Seroprevalence of Dirofilaria immitis in dogs grouped according to the percentage of positive tests by region (A) and state (B).
The states with > 10% of positive tests to D. immitis were located in the Atlantic coast (Fig. 5). The six Atlantic states averaged 15.5% (155/995) of positive tests to D. immitis, significantly different from the average of 1.0% (27/2527) from the other 16 states in the study (χ2 = 306.7, P < 0.0001).
Animals 3 years-old or older presented a significantly higher percentage of positive results to D. immitis when compared to dogs under 3 years-old, 5.9% (133/2251) vs 3.9% (49/1271), respectively (χ2 = 6.9, P = 0.008). Dogs tested at clinics presented a significantly higher percentage of positive results when compared to those tested at shelters, 6.9% (114/1648) vs 3.6% (68/1874) (Table 2) (χ2 = 19.35, P < 0.0001) (see also Table 3).
3.5. Co-infections
Co-infections, defined as a positive result to two or more agents in the same sample (Evason et al., 2019), were detected in 38.4% (488) of the 1272 positive samples. The following co-infections were detected: Anaplasma spp. and B. burgdorferi (n = 3); Anaplasma spp. and D. immitis (n = 36); Anaplasma spp. and E. canis (n = 420); B. burgdorferi and D. immitis (n = 1); B. burgdorferi and E. canis (n = 3); E. canis and D. immitis (n = 89). There were a few cases including 3 different pathogens: Anaplasma spp., B. burgdorferi and D. immitis (n = 1); Anaplasma spp., B. burgdorferi and E. canis (n = 2); Anaplasma spp., E. canis and D. immitis (n = 29).
4. Discussion
This survey provides an assessment of the geographical distribution of four CVBD in Mexico. To the best of our knowledge, it is the largest survey including apparently healthy dogs conducted in Mexico. Seroprevalence of Anaplasma spp. was 14.6% (515/3522) compared to 9.9% (169/1706) observed by Movilla et al. (2016). It was similar for Ehrlichia spp. (most likely E. canis) in the present study (i.e. 30.9% (1090/3522)) compared to Movilla et al. (2016) (30.8% (526/1706)), as well as for B. burgdorferi, 0.1% (5/3522) compared to 0.2% (4/1702) and D. immitis, 5.2% (182/3522) compared to 5.3% (91/1706). The close similarity in the findings from these two studies, conducted several years apart shows the stability of the prevalences of dog infections since at least 5 years. Based on molecular demonstrations of the presence of E. canis in Mexico, the authors considered that the seroconversions observed in dogs were due to E. canis infection.
The seroprevalences of Ehrlichia spp. and Anaplasma spp. observed in this study show significant differences between coastal and inner states, which is consistent with conditions that favor the survival and reproduction of the vector R. sanguineus (Pujalte et al., 2018).
The percent of positive test results to B. burgdorferi was extremely low, with only five positive cases out of 3522 samples tested nationwide (0.1%). Lyme borreliosis is endemic in temperate and cold climates where the Ixodes vector ticks are prevalent, whereas hot climates like in Mexico are less suitable for Ixodes spp.
Regarding D. immitis, northwestern, northeastern, eastern, and southeastern regions presented higher seroprevalence than the other regions. Another study performed in the Yucatán Peninsula, in the southeastern region, determined a prevalence of 8.3% for D. immitis (Bolio-Gonzalez et al., 2007), like the 7.9% reported by Movilla et al. (2016) for the southeastern region and the 10.9% from the present study. When analyzing the data at a state level, this study found that the six Atlantic states averaged 15.6% of positive tests to D. immitis, much higher than the average of 1.0% from the other 16 states. Previous studies have shown a higher prevalence in dogs sampled in the Gulf of Mexico’s area than in those tested in other Mexican regions, a potential explanation being the abundance of certain mosquito vectors in this specific region (Movilla et al., 2016).
Regarding age, 3-year or older dogs presented a significantly different percentage of positive results for E. canis and D. immitis than younger animals. In previous surveys conducted in Mexico, older age was also reported as a risk factor for a higher E. canis and D. immitis prevalence, indicating that older dogs have been exposed for more extended periods to mosquito or tick bites (Bolio-Gonzalez et al., 2007; Caro-Gonzalez et al., 2011; Movilla et al., 2016; Torres-Chable et al., 2018).
The co-infection between Anaplasma spp. and Ehrlichia spp. was significantly more common than the others, which is in favor of a common vector, R. sanguineus, and is an indirect proof that the species is Anaplasma platys (Snellgrove et al., 2020). Dirofilaria immitis was the only pathogen showing significantly higher seroprevalence in dogs sampled in veterinary clinics (6.9%) when compared to shelter dogs (3.6%), contrary to the general assumption that dogs under clinical supervision would present a lower prevalence (Self et al., 2019). It may be related to higher mosquito control measures in shelters, but further research is needed to investigate this unexpected result.
5. Conclusions
The overall trends in this survey were consistent with previous studies conducted in Mexico. The regional distribution indicated a significantly higher risk of being infected on the Atlantic and Pacific coastal states than in the center of the country. It is most probably related to climatic conditions most favorable to tick vectors and mosquitoes on the coasts when the interior part seems too hot and dry.
Funding
This work was supported by Boehringer Ingelheim Animal Health, Mexico. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Ethical approval
Blood samples were collected according to protocols approved by the Boehringer Ingelheim Animal Health Institutional Animal Care and Use Committee. Those responsible for the animals were informed about these protocols. All owners and care centers read and approved the study protocol and the inclusion of their animals.
CRediT author statement
Felipe Bedoya: Conceptualization, Writing - original draft, Writing - review & editing. Frederic Beugnet: Conceptualization, Writing - original draft, Writing - review & editing. Emilia Tobias: Conceptualization, Writing - original draft, Formal analysis, Writing - review & editing. Erick Garcia-Mendizabal: Conceptualization, Writing - original draft, Investigation, Writing - review & editing. Samantha Hay-Parker: Conceptualization, Writing - original draft, Investigation, Writing - review & editing. Nancy Montes: Conceptualization, Writing - original draft, Investigation, Writing - review & editing. Jose Uribe: Conceptualization, Investigation, Writing - review & editing. Enrique Mondaca: Conceptualization, Data curation, Formal analysis, Writing - original draft, Writing - review & editing. All authors read and approved the final manuscript.
Declaration of competing interests
The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: this research was funded by Boehringer Ingelheim Animal Health, Mexico, of which all the authors were employees or under contract.
Acknowledgements
Special thanks to Vianey Suarez who managed laboratory samples, classification and storage, performed rapid test as well as coordinating the logistics of shipments of materials and samples and to Juan Pablo Martínez Labat for their invaluable contributions. The authors acknowledge and appreciate the contribution of the veterinarians and managers of the animal control centers who made its possible to carry out the present study.
Data availability
All data generated or analyzed during this study are included in this published article. Raw data are available from the corresponding author upon reasonable request with no time embargo.
References
- Baneth G., Bourdeau P., Bourdoiseau G., Bowman D., Breitschwerdt E., Capelli G., et al. Vector-Borne Diseases - constant challenge for practicing veterinarians: recommendations from the CVBD World Forum. Parasites Vectors. 2012;5:55. doi: 10.1186/1756-3305-5-55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beugnet F., Marié J.-L. Emerging arthropod-borne diseases of companion animals in Europe. Vet. Parasitol. 2009;163:298–305. doi: 10.1016/j.vetpar.2009.03.028. [DOI] [PubMed] [Google Scholar]
- Bolio-Gonzalez M.E., Rodriguez-Vivas R.I., Sauri-Arceo C.H., Gutierrez-Blanco E., Ortega-Pacheco A., Colin-Flores R.F. Prevalence of the Dirofilaria immitis infection in dogs from Merida, Yucatan, Mexico. Vet. Parasitol. 2007;148:166–169. doi: 10.1016/j.vetpar.2007.05.019. [DOI] [PubMed] [Google Scholar]
- Bowman D., Little S.E., Lorentzen L., Shields J., Sullivan M.P., Carlin E.P. Prevalence and geographic distribution of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis, and Anaplasma phagocytophilum in dogs in the United States: Results of a national clinic-based serologic survey. Vet. Parasitol. 2009;160:138–148. doi: 10.1016/j.vetpar.2008.10.093. [DOI] [PubMed] [Google Scholar]
- Caro-Gonzalez J.A., Bolio-Gonzalez M.E., Escobedo-Ortegón F.J., Manrique-Saide P., Rodriguez-Vivas R.I., Rodriguez-Buenfil J.C., Sauri-Arceo C.H. Prevalence of Dirofilaria immitis infection in dogs from Celestun, Mexico, using polymerase chain reaction test. Vector Borne Zoonotic Dis. 2011;11:193–196. doi: 10.1089/vbz.2009.0171. [DOI] [PubMed] [Google Scholar]
- Chandrashekar R., Mainville C.A., Beall M.J., O’Connor T., Eberts M.D., Alleman A.R., et al. Performance of a commercially available in-clinic ELISA for the detection of antibodies against Anaplasma phagocytophilum, Ehrlichia canis, and Borrelia burgdorferi and Dirofilaria immitis antigen in dogs. Am. J. Vet. Res. 2010;71:1443–1450. doi: 10.2460/ajvr.71.12.1443. [DOI] [PubMed] [Google Scholar]
- Evason M., Stull J.W., Pearl D.L., Peregrine A.S., Jardine C., Buch J.S., et al. Prevalence of Borrelia burgdorferi, Anaplasma spp., Ehrlichia spp. and Dirofilaria immitis in Canadian dogs, 2008 to 2015: A repeat cross-sectional study. Parasites Vectors. 2019;12:64. doi: 10.1186/s13071-019-3299-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- García L.T., Romero H.Q., Martínez M.T.Q., Evangelista T.B.R., Serrano A.B., Oshima S.H., et al. Prevalence and risk factors for Borrelia burgdorferi infection in Mexicali, Baja California, a Mexico-US border city. Intern. J. Appl. Res. Vet. Med. 2008;6:161–165. [Google Scholar]
- Littman M.P., Gerber B., Goldstein R.E., Labato M.A., Lappin M.R., Moore G.E. ACVIM consensus update on Lyme borreliosis in dogs and cats. J. Vet. Intern. Med. 2018;32:887–903. doi: 10.1111/jvim.15085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Movilla R., García C., Siebert S., Roura X. Countrywide serological evaluation of canine prevalence for Anaplasma spp., Borrelia burgdorferi (sensu lato), Dirofilaria immitis and Ehrlichia canis in Mexico. Parasites Vectors. 2016;9:421. doi: 10.1186/s13071-016-1686-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nuñez O.L. Estudio de la seroprevalencia de Ehrlichia canis en México. Revista AMMVEPE. 2003;14:83–85. [Google Scholar]
- Ochoa L.N. Estudio de la seroprevalencia de Ehrlichia canis en Mexico. AMMVEPE. 2003;14:83–85. [Google Scholar]
- Ojeda-Chi M.M., Rodriguez-Vivas R.I., Esteve-Gasent M.D., León A.A.P. de, Modarelli J.J., Villegas-Perez S.L. Ehrlichia canis in dogs of Mexico: Prevalence, incidence, co-infection and factors associated. Comp. Immunol. Microbiol. Infect. Dis. 2019;67 doi: 10.1016/j.cimid.2019.101351. [DOI] [PubMed] [Google Scholar]
- Pujalte G.G.A., Marberry S.T., Libertin C.R. Tick-borne illnesses in the United States. Prim. Care Clin. Off. Pract. 2018;45:379–391. doi: 10.1016/j.pop.2018.05.011. [DOI] [PubMed] [Google Scholar]
- Rikihisa Y. The tribe Ehrlichieae and ehrlichial diseases. Clin. Microbiol. Rev. 1991;4:286–308. doi: 10.1128/cmr.4.3.286. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rodriguez-Vivas R.I., Albornoz R.E.F., Bolio G.M.E. Ehrlichia canis in dogs in Yucatan, Mexico: Seroprevalence, prevalence of infection and associated factors. Vet. Parasitol. 2005;127:75–79. doi: 10.1016/j.vetpar.2004.08.022. [DOI] [PubMed] [Google Scholar]
- Rojero-Vázquez E., Gordillo-Pérez G., Weber M. Infection of Anaplasma phagocytophilum and Ehrlichia spp. in opossums and dogs in Campeche, Mexico: The role of tick infestation. Frontiers Ecol. Evol. 5, 2017;161 doi: 10.3389/fevo.2017.00161. [DOI] [Google Scholar]
- Self S.W., Pulaski C.N., McMahan C.S., Brown D.A., Yabsley M.J., Gettings J.R. Regional and local temporal trends in the prevalence of canine heartworm infection in the contiguous United States: 2012–2018. Parasites Vectors. 2019;12:380. doi: 10.1186/s13071-019-3633-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SEMARNAT, 2019. Precipitación media histórica por entidad federativa (milímetros). http://dgeiawf.semarnat.gob.mx:8080/ibi_apps/WFServlet?IBIF_ex=D3_AGUA01_01&IBIC_user=dgeia_mce&IBIC_pass=dgeia_mce&NOMBREENTIDAD=∗&NOMBREANIO=∗. (Accessed 8 August 2019).
- Snellgrove A.N., Krapiunaya I., Ford S.L., Stanley H.M., Wickson A.G., Hartzer K.L., Levin M.L. Vector competence of Rhipicephalus sanguineus sensu stricto for Anaplasma platys. Ticks Tick Borne Dis. 2020;11 doi: 10.1016/j.ttbdis.2020.101517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torres-Chable O.M., Baak-Baak C.M., Cigarroa-Toledo N., Blitvich B.J., Brito-Argaez L.G., Alvarado-Kantun Y.N., et al. Molecular detection of Dirofilaria immitis in dogs and mosquitoes in Tabasco, Mexico. J. Vector Borne Dis. 2018;55:151–158. doi: 10.4103/0972-9062.242563. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All data generated or analyzed during this study are included in this published article. Raw data are available from the corresponding author upon reasonable request with no time embargo.