Associated Factors to Seroprevalence of<i> Ehrlichia</i> spp. in Dogs of Quintana Roo, Mexico

Martínez-Vega, Pedro Pablo; Bolio-Gonzalez, Manuel Emilio; Rodríguez-Vivas, Roger Iván; Gutierrez-Blanco, Eduardo; Pérez-Osorio, Carlos; Villegas-Perez, Sandra Luz; Sauri-Arceo, Carlos Humberto

doi:https://doi.org/10.1155/2016/4109467

Journal of Tropical Medicine

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Research Article | Open Access

Volume 2016 | Article ID 4109467 | https://doi.org/10.1155/2016/4109467

Associated Factors to Seroprevalence of Ehrlichia spp. in Dogs of Quintana Roo, Mexico

Pedro Pablo Martínez-Vega,¹Manuel Emilio Bolio-Gonzalez,²Roger Iván Rodríguez-Vivas,²Eduardo Gutierrez-Blanco,²Carlos Pérez-Osorio,³Sandra Luz Villegas-Perez,²and Carlos Humberto Sauri-Arceo²

Academic Editor: Carlos E. P. Corbett

Received19 Aug 2016

Revised31 Oct 2016

Accepted13 Nov 2016

Published21 Dec 2016

Abstract

The objective of this study was to determine the seroprevalence to Ehrlichia spp. in dogs from Xcalak, Quintana Roo, Mexico, and the associated factors. Serum samples were obtained from 118 dogs and used in an indirect immunofluorescent assay test for the detection of antibodies against Ehrlichia spp. A questionnaire was used to obtain information about possible variables associated with seroprevalence. These variables were analyzed through Chi² test and logistic regression. Dog seroprevalence of antibodies against Ehrlichia spp. was 64% (75/118). Fifty-two percent (61/118) of dogs had tick infestation which was identified as Rhipicephalus sanguineus sensu lato. Anemia was observed in 36% of dogs. Leucopenia (2.5%), thrombocytopenia (70%), and hemorrhage (14%) were also observed. Thirty-one percent (23/75) of dogs with anemia, 4% (3/75) of dogs with leucopenia, 80% (60/75) of dogs with thrombocytopenia, 17% (13/75) of dogs with hemorrhages, and 59% (44/75) of dogs with ticks were positive for Ehrlichia spp. antibodies. The factors associated with seroprevalence were age (1–3 and >3 years old, OR = 7.77 and OR = 15.39, resp.), tick infestation (OR = 3.13), and thrombocytopenia (OR = 3.36). In conclusion, seroprevalence of Ehrlichia spp. was high in the community of Xcalak and its associated factors were age, tick infestation, and thrombocytopenia.

1. Introduction

Ehrlichia canis (E. canis) is the most important species of Ehrlichia found in dogs; however, Ehrlichia chaffeensis (E. chaffeensis) and Ehrlichia ewingii (E. ewingii) may cause a clinical illness on this animal species [1–4]. The disease in dogs is classified as acute, subclinical, or chronic, based on the chronological appearance of clinical signs and pathological findings [5–7]. These three pathogen species belong to Anaplasmataceae family and order Rickettsiales. They have a 97% similarity in their 16S rRNA sequence and they also share similar immunogenic epitopes [8–13]. Therefore, it is not uncommon to observe cross-reactions in serological tests among members of this genogroup [2, 9, 14]. The above observation was demonstrated by several studies in which E. canis antigen was used in serological assays to determine exposure to E. chaffeensis in humans and E. ewingii in dogs [15–18]. The three Ehrlichia species have the potential of zoonotic transmission through vectors (monocytic canine ehrlichiosis, human monocytic ehrlichiosis, and canine granulocytic ehrlichiosis); although the role of the dog is not clear yet in the epidemiology of the disease in humans [2, 19–21]. The distribution of ehrlichiosis correlates with the presence of the vector [20, 22]. The tick Rhipicephalus sanguineus sensu lato is the main vector of E. canis, but E. chaffeensis and E. ewingii DNA have been detected also in this tick species [23, 24]. Ehrlichiosis is considered endemic in tropical and subtropical regions since these areas present adequate climatic conditions for the tick vector growth and development [22, 25]. The disease in dogs has been reported in Mexico since 1996 [26] and there are a few studies in Yucatan reporting seroprevalence in urban and rural areas [27, 28], but little is known about the epidemiology of the disease in coastal zones.

The aim of the present work was to determine the seroprevalence of Ehrlichia spp. through the indirect immunofluorescence assay test (IFAT), as well as identify associated factors to the presence of antibodies to Ehrlichia spp. in dogs from Xcalak, Quintana Roo, Mexico.

2. Materials and Methods

2.1. Study Area

This study was conducted at the National Park of Xcalak Reefs located in the Southern Coast of Quintana Roo, Mexico, located at latitude 18°30′00′′N and longitude 87°44′49′′W (Figure 1) [29]. The climate is warm and humid, with an annual average temperature of 26.5°C, a minimum of 18°C, and a maximum of 34°C. The annual average rainfall is 1,300 mm [30].

2.2. Study Population and Sampling

All population of 118 dogs was sampled in the National Park of Xcalak Reefs, Quintana, Roo, Mexico. Animal handling was performed accordingly to bioethical guidelines to assure their physical integrity. All dogs were physically examined before samples were taken. The owners were interviewed according to a questionnaire in order to obtain information about the dogs. An inspection was done during the physical examination to identify the presence of hemorrhagic signs such as petechiae, ecchymoses, and suffusions, as well as the presence of ticks. Adult ticks were collected from dogs and deposited in plastic containers with 70% ethanol and the tick identification [31] was conducted in the Parasitology Laboratory at the Veterinary Medicine School, UADY, Yucatan, Mexico. Blood samples from each dog were obtained by puncture in the cephalic vein and collected in Vacutainer® tubes with and without EDTA anticoagulant. Tubes without anticoagulant were centrifuged for 5 min at 800 ×g to separate the serum, which was then transferred to 1.5 mL Eppendorf tubes and stored at −20°C until their process in the Laboratory of Immunology at the School of Veterinary Medicine, UADY. A complete cell count, including platelets count and WC counts, was made on the blood samples with EDTA in a semiautomatic impedance analyzer (Sysmex® model KX-21N) at the Small Species Clinic, Veterinary Medicine School, UADY, Yucatan, Mexico.

Less than 200,000 platelets/mL of blood were considered to be thrombocytopenia (26); less than 5.5 million red blood cells/mL, or less than 37% hematocrit, or less than 12 g/dL hemoglobin was considered to be anemia and less than 6,000 white blood cells/mL were considered leucopenia [32].

2.3. Detection of Antibodies to Ehrlichia spp.

An indirect immunofluorescent assay test was used to determine IgG antibody titers from serum samples [33]. This assay is considered the reference serological test with a sensitivity of 82 to 100% and a specificity of 67 and 100% [34]. Glass slides containing DH82 cells infected with the Arkansas strain of E. chaffeensis (kindly provided by David H. Walker, M.D., from the Department of Pathology at The University of Texas Medical Branch) were used as antigen. Serum samples were diluted in PBS 1 : 100 (pH 7.2) and added to the antigen in the slides. Positive and negative controls were included. Positive control was serum from a dog previously diagnosed with clinical ehrlichiosis and a positive IFAT (1 : 400) confirmed by a positive PCR analysis. Negative control was serum from a dog with no clinical evidence of ehrlichiosis and both negative IFAT and PCR analysis. The glass slides were incubated for 30 minutes at 37°C and then washed three times in PBS (5 minutes each). Rabbit anti-dog IgG labeled with fluorescein isothiocyanate (Sigma-Aldrich Germany) was added in a 1 : 50 PBS dilution and slides were incubated for another 30 minutes at 37°C. After the incubation period, the slides were washed three times in PBS (5 minutes each). Evans blue (0.1% (w/v) in water solution, Sigma-Aldrich, Germany) was added to the last wash buffer as a counterstain. The glass slides were air dried and mounted with buffered glycerol (pH 8.7); then, they were transferred to a microscope equipped for fluorescence (Leica® Germany) and observed at 400x.

2.4. Data Analysis

Seroprevalence was calculated using the formula described by Thrusfield [35] for disease occurrence. The independent variables used to determine association with seroprevalence of Ehrlichia spp. were age (<1, 1–3, >3 y.o.), ticks (presence, absence), anemia (yes, no), leucopenia (yes, no), thrombocytopenia (yes, no), and hemorrhage (yes, no). Contingency tables (2 × K) were obtained with these variables. Variables with a value ≤ 0.20 were analyzed in SPSS® v. 15.0 (SPSS Inc. 2006) using a binomial logistic regression model with fixed effect to obtain exact estimations of regression, 95% confidence intervals (CI 95%), odds ratio (OR), and value.

3. Results

Antibodies against Ehrlichia spp. were detected in 64% (75/118) of the dogs. Sixty-one percent of dogs (72/118) were infested with ticks and all ticks were identified as R. sanguineus s.l.

The average and standard deviation number of thrombocytes, red blood cells, hemoglobin, hematocrit, and white blood cells in the population were 123,860 +/− 100,041 (range: 12,000–721,000) platelets/mL of blood, 5.36 +/− 1.01 (range: 2.39–7.59) million cells/mL of blood, 41.07 +/− 8.71 (range: 18.9–58.6) percent, and 13,160 +/− 4,180 (range: 3,300–23,800) cells/mL of blood, respectively.

Anemia was found in 36% (43/118) of the dogs, leucopenia in 2.5% (3/118), and thrombocytopenia in 70% (83/118). However, only 14% (17/118) of the dogs presented hemorrhages. Thirty-one percent (23/75) of dogs with anemia, 4% (3/75) of dogs with leucopenia, 80% (60/75) of dogs with thrombocytopenia, 17% (13/75) of dogs with hemorrhages, and 59% (44/75) of dogs with ticks were positive for Ehrlichia spp. antibodies. The univariate analysis that was used to identify factors associated with seroprevalence of Ehrlichia spp. showed that variables with ≤ 0.20 were age, presence of ticks, thrombocytopenia, and anemia. But the logistic regression indicated a positive association of animals with age 1–3 y.o. (OR = 7.77, CI_95% = 2.23–27.04, and ) and >3 y.o. (OR = 15.39, CI_95% = 4.13–57.40, and ); presence of ticks (OR = 3.13, CI_95% = 1.17–8.44, and ); and thrombocytopenia (OR = 3.36, CI_95% = 1.28–8.83, and ) with seroprevalence of Ehrlichia spp. (Table 1).

4. Discussion

The epidemiology of canine ehrlichiosis is closely related not only to the vector distribution, which is more frequently associated with tropical and subtropical zones, but also to animal behavior, age, and its environment [27, 36, 37]. Consequently, there is a wide diversity of worldwide seroprevalence. In European countries, such as Bulgaria, Spain, Sweden, and Switzerland, seroprevalence of 30% [38], 19% [36], 17.7% [39], and 2.2% [40], respectively, was reported. In Asia, 14.6% has been reported in Iran [11]; in Africa, 67.8% [41] and 54.2% [42] were recorded in Ivory Coast and Tunisia, respectively.

In America, 44.7% [37] and 63.3% [43] seroprevalence was found in Brazil. In Mexico, Núñez [44] described 33.1% seroprevalence; and in Yucatan, 44.1% [27] and 8.7% [28] were reported. In the present study, a 64% seroprevalence to Ehrlichia spp. was found. The wide range of the results reported worldwide might be due to the different serological tests used with different sensitivity and specificity [45]. Also the wide range of seroprevalence found in different countries and regions suggests that environmental conditions associated with the geographical zones play an important role by influencing the tick vector distribution and reproductive cycle [25, 37]. In addition, dogs that are 1–3 and >3 y.o. had 7.77–15.39 chances of being serologically positive. Similar results have been reported in Yucatan, Mexico (2–4 y.o.: OR = 6.77, ; >4 y.o.: OR =4.24, ), and Brazil (2–5 y.o.: OR = 2.20, ≤ 0.05; >5 y.o.: OR = 2.96, ), by Rodriguez-Vivas et al. [27] and Costa et al. [37], respectively. This trend could be explained by the fact that older animals have a bigger chance of being exposed to vectors than younger animals. As a consequence, the chances of being exposed to the etiological agent of ehrlichiosis increase. Baneth et al. [46] have shown a higher susceptibility to ehrlichiosis in adult dogs. On the other hand, antibody titers remain during prolonged periods, even when the patient has a full clinical recovery [3, 5, 6]. The presence of ticks was another factor associated with the seroprevalence (OR = 3.13, CI 95% = 1.17–8.44, and ), similar to the report by Costa et al. [37] (OR = 2.1, ) in Brazil. All the ticks in this study were identified as R. sanguineus and a 61% infestation was observed on the dogs. The presence of the vector is essential for the transmission of the disease in the epidemiology of ehrlichiosis as noted by Harrus et al. [5], Skotarczak [20], and Stich et al. [22]. Several studies have shown that the prevalence of ticks and the seroprevalence to Ehrlichia spp. in Mexico vary accordingly to geographical zones. Núñez [44] reported seroprevalence of 48.3%, 24.1%, and 70.2%, to E. canis in the States of Sinaloa, Morelos, and Baja California Mexico, respectively. Also, 46% [47], 20% [48], and 59.6% [49] prevalence of R. sanguineus has been found in those same states. Herein, dogs presenting thrombocytopenia had 3.36 more chances of having a positive antibody titer. Other authors, such as Rodriguez-Vivas et al. [27], found that dogs had 18.91 more chances of having a positive antibody titer when presenting thrombocytopenia. This evidence confirms that thrombocytopenia is the most common and consistent clinical sign of canine ehrlichiosis [5, 7, 50, 51]. Niwetpathomwat et al. [52] found, in a retrospective study involving 687 cases with a diagnosis of canine ehrlichiosis, that thrombocytopenia was present in 93% of the dogs. In addition, the three species of Ehrlichia spp. (E. canis, E. chaffeensis, and E. ewingii) that can be infecting the studied population produce thrombocytopenia [2, 20, 53, 54].

R. sanguineus s.l. on dogs has a wide distribution in the Yucatan Peninsula [31] and this tropical lineage of R. sanguineus has showed to be a competent vector for E. canis [55]. Pat-Nah et al. [56] found in Yucatan, Mexico, that R. sanguineus s.l. ticks are the vector of E. canis infections in dogs. The high infestations of dogs and the wide distribution of R. sanguineus s.l. on dogs in the Yucatan Peninsula highlight the risk for Ehrlichia transmission [31].

The results in this study show that antibodies to Ehrlichia spp. are present in the dogs of Xcalak, Quintana Roo, Mexico; however, further molecular studies are required to identify which species of the genogroup (E. canis, E. chaffeensis, and E. ewingii) are present in this dog population. This is the first report of dog’s exposure to Ehrlichia spp. in the coastal zone of the Yucatan Peninsula.

5. Conclusion

It is concluded that the seroprevalence of Ehrlichia spp. in the dog population of Quintana Roo coast is high, and therefore the disease can be considered endemic to the region. The associated factors are increased age, tick infestation, and thrombocytopenia.

Competing Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgments

The research reported here was supported by graduate studies scholarships awarded to Pedro Pablo Martinez Vega by the Consejo Nacional de Ciencia y Tecnología of México (CONACYT). The authors acknowledge the National Park of Xcalak Reefs located in the Southern Coast of Quintana Roo, Mexico.

References

G. Baneth, E. B. Breitschwerdt, B. C. Hegarty, B. Pappalardo, and J. Ryan, “A survey of tick-borne bacteria and protozoa in naturally exposed dogs from Israel,” Veterinary Parasitology, vol. 74, no. 2–4, pp. 133–142, 1998.
View at: Publisher Site | Google Scholar
E. B. Breitschwerdt, B. C. Hegarty, and S. I. Hancock, “Sequential evaluation of dogs naturally infected with Ehrlichia canis, Ehrlichia chaffeensis, Ehrlichia equi, Ehrlichia ewingii, or Bartonella vinsonii,” Journal of Clinical Microbiology, vol. 36, pp. 2645–2651, 1998.
View at: Google Scholar
T. Waner, S. Harrus, F. Jongejan, H. Bark, A. Keysary, and A. W. C. A. Cornelissen, “Significance of serological testing for ehrlichial diseases in dogs with special emphasis on the diagnosis of canine monocytic ehrlichiosis caused by Ehrlichia canis,” Veterinary Parasitology, vol. 95, no. 1, pp. 1–15, 2001.
View at: Publisher Site | Google Scholar
C. N. Gutiérrez, M. Martínez, E. Sánchez et al., “Cultivation and molecular identification of Ehrlichia canis and Ehrlichia chaffeensis from a naturally co-infected dog in Venezuela,” Veterinary Clinical Pathology, vol. 37, no. 3, pp. 258–265, 2008.
View at: Publisher Site | Google Scholar
S. Harrus, T. Waner, H. Bark, F. Jongejan, and A. W. C. A. Cornelissen, “Recent advances in determining the pathogenesis of canine monocytic ehrlichiosis,” Journal of Clinical Microbiology, vol. 37, no. 9, pp. 2745–2749, 1999.
View at: Google Scholar
S. Harrus and T. Waner, “Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): an overview,” Veterinary Journal, vol. 187, no. 3, pp. 292–296, 2011.
View at: Publisher Site | Google Scholar
R. I. Rodríguez-Vivas, M. E. Bolio-González, and M. M. Ojeda-Chi, “Diagnóstico de la ehrlichiosis monocítica canina: una revisión actualizada,” Ciencia y Agricultura, vol. 12, no. 1, pp. 83–98, 2015.
View at: Publisher Site | Google Scholar
S.-M. Chen, J. S. Dumler, H.-M. Feng, and D. H. Walker, “Identification of the antigenic constituents of Ehrlichia chaffeensis,” American Journal of Tropical Medicine and Hygiene, vol. 50, no. 1, pp. 52–58, 1994.
View at: Google Scholar
Y. Rikihisa, S. A. Ewing, and J. C. Fox, “Western immunoblot analysis of Ehrlichia chaffeensis, E. canis, or E. ewingii infections in dogs and humans,” Journal of Clinical Microbiology, vol. 32, no. 9, pp. 2107–2112, 1994.
View at: Google Scholar
S.-I. Shibata, M. Kawahara, Y. Rikihisa et al., “New Ehrlichia species closely related to Ehrlichia chaffeensis isolated from Ixodes ovatus ticks in Japan,” Journal of Clinical Microbiology, vol. 38, no. 4, pp. 1331–1338, 2000.
View at: Google Scholar
B. Akhtardanesh, R. Ghanbarpour, and H. Blourizadeh, “Serological evidence of canine monocytic ehrlichiosis in Iran,” Comparative Clinical Pathology, vol. 19, no. 5, pp. 469–474, 2010.
View at: Publisher Site | Google Scholar
J. S. Dumler, A. F. Barbet, C. P. J. Bekker et al., “Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila,” International Journal of Systematic and Evolutionary Microbiology, vol. 51, no. 6, pp. 2145–2165, 2001.
View at: Publisher Site | Google Scholar
V. Singu, L. Peddireddi, K. R. Sirigireddy, C. Cheng, U. Munderloh, and R. R. Ganta, “Unique macrophage and tick cell-specific protein expression from the p28/p30-outer membrane protein multigene locus in Ehrlichia chaffeensis and Ehrlichia canis,” Cellular Microbiology, vol. 8, no. 9, pp. 1475–1487, 2006.
View at: Publisher Site | Google Scholar
M. Perez, Y. Rikihisa, and B. Wen, “Ehrlichia canis-like agent isolated from a man in Venezuela: antigenic and genetic characterization,” Journal of Clinical Microbiology, vol. 34, no. 9, pp. 2133–2139, 1996.
View at: Google Scholar
K. Maeda, N. Markowitz, R. C. Hawley, M. Ristic, D. Cox, and J. E. McDade, “Human infection with Ehrlichia canis, a leukocyte rickettsia,” New England Journal of Medicine, vol. 316, no. 14, pp. 853–856, 1987.
View at: Publisher Site | Google Scholar
J. E. Dawson, Y. Rikihisa, S. A. Ewing, and D. B. Fishbein, “Serologic diagnosis of human ehrlichiosis using two Ehrlichia canis isolates,” Journal of Infectious Diseases, vol. 163, no. 3, pp. 564–567, 1991.
View at: Publisher Site | Google Scholar
A. Unver, Y. Rikihisa, N. Ohashi, L. C. Cullman, R. Buller, and G. A. Storch, “Western and dot blotting analyses of Ehrlichia chaffeensis indirect fluorescent-antibody assay-positive and -negative human sera by using native and recombinant E. chaffeensis and E. canis antigens,” Journal of Clinical Microbiology, vol. 37, no. 12, pp. 3888–3895, 1999.
View at: Google Scholar
T. P. O'Connor, J. L. Hanscom, B. C. Hegarty, R. G. Groat, and E. B. Breitschwerdt, “Comparison of an indirect immunofluorescence assay, western blot analysis, and a commercially available ELISA for detection of Ehrlichia canis antibodies in canine sera,” American Journal of Veterinary Research, vol. 67, no. 2, pp. 206–210, 2006.
View at: Publisher Site | Google Scholar
B. E. Anderson, J. E. Dawson, D. C. Jones, and K. H. Wilson, “Ehrlichia chaffeensis, a new species associated with human ehrlichiosis,” Journal of Clinical Microbiology, vol. 29, no. 12, pp. 2838–2842, 1991.
View at: Google Scholar
B. Skotarczak, “Canine ehrlichiosis,” Annals of Agriculture and Environmental Medicine, vol. 10, no. 2, pp. 137–141, 2003.
View at: Google Scholar
M. Perez, M. Bodor, C. Zhang, Q. Xiong, and Y. Rikihisa, “Human infection with Ehrlichia canis accompanied by clinical signs in Venezuela,” Annals of the New York Academy of Sciences, vol. 1078, pp. 110–117, 2006.
View at: Publisher Site | Google Scholar
R. W. Stich, J. J. Schaefer, W. G. Bremer, G. R. Needham, and S. Jittapalapong, “Host surveys, ixodid tick biology and transmission scenarios as related to the tick-borne pathogen, Ehrlichia canis,” Veterinary Parasitology, vol. 158, no. 4, pp. 256–273, 2008.
View at: Publisher Site | Google Scholar
G. L. Murphy, S. A. Ewing, L. C. Whitworth, J. C. Fox, and A. A. Kocan, “A molecular and serologic survey of Ehrlichia canis, E. chaffeensis, and E. ewingii in dogs and ticks from Oklahoma,” Veterinary Parasitology, vol. 79, no. 4, pp. 325–339, 1998.
View at: Publisher Site | Google Scholar
L. M. Ndip, R. N. Ndip, S. N. Esemu, D. H. Walker, and J. W. McBride, “Predominance of Ehrlichia chaffeensis in Rhipicephalus sanguineus ticks from kennel-confined dogs in Limbe, Cameroon,” Experimental and Applied Acarology, vol. 50, no. 2, pp. 163–168, 2010.
View at: Publisher Site | Google Scholar
F. Dantas-Torres, “Biology and ecology of the brown dog tick, Rhipicephalus sanguineus,” Parasites & Vectors, vol. 3, article no. 26, 2010.
View at: Publisher Site | Google Scholar
A. C. García and O. L. Núñez, “Pancitopenia tropical en un perro,” Revista AMMVEPE, vol. 7, pp. 235–236, 1996.
View at: Google Scholar
R. I. Rodriguez-Vivas, R. E. F. Albornoz, and G. M. E. Bolio, “Ehrlichia canis in dogs in Yucatan, Mexico: seroprevalence, prevalence of infection and associated factors,” Veterinary Parasitology, vol. 127, no. 1, pp. 75–79, 2005.
View at: Publisher Site | Google Scholar
M. Jiménez-Coello, C. Pérez-Osorio, I. Vado-Solís, J. C. Rodríguez-Buenfil, and A. Ortega-Pacheco, “Serological survey of Ehrlichia canis in stray dogs from Yucatán, Mexico, using two different diagnostic tests,” Vector-Borne and Zoonotic Diseases, vol. 9, no. 2, pp. 209–211, 2009.
View at: Publisher Site | Google Scholar
Google-INEGI, Xcalak, Quintana-Roo, Mexico map in Google maps, October 2016, https://www.google.com.mx/maps/place/Xcalak,+Quintana+Roo/@18.2708536,-88.3961858,9z/data=!4m5!3m4!1s0x8f5b428a800da7ff:0xb2f5ac6748959c7d!8m2!3d18.2713888!4d-87.8358333?hl=en.
Comisión Nacional de Áreas Naturales Protegidas (CONANP), Programa de Manejo. Parque Nacional Arrecifes de Xcalak, Comisión Nacional de Áreas Naturales Protegidas, México City, México, 2004.
R. I. Rodríguez-Vivas, D. A. Apanaskevich, M. M. Ojeda-Chi et al., “Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico,” Veterinary Parasitology, vol. 215, pp. 106–113, 2016.
View at: Publisher Site | Google Scholar
L. G. Voight and L. S. Shannon, Hematology Techniques & Concepts for Veterinary Technicians, Wiley-Blackwell, Iowa, IA, USA, 2nd edition, 2011.
M. Ristic, D. L. Huxsoll, R. M. Weisiger, P. K. Hildebrandt, and M. B. Nyindo, “Serological diagnosis of tropical canine pancytopenia by indirect immunofluorescence,” Infection and Immunity, vol. 6, no. 3, pp. 226–231, 1972.
View at: Google Scholar
J. J. Walls, M. Aguero-Rosenfeld, J. S. Bakken et al., “Inter- and intralaboratory comparison of Ehrlichia equi and human granulocytic ehrlichiosis (HGE) agent strains for serodiagnosis of HGE by the immunofluorescent-antibody test,” Journal of Clinical Microbiology, vol. 37, no. 9, pp. 2968–2973, 1999.
View at: Google Scholar
M. Thrusfield, Veterinary Epidemiology, Blackwell, Iowa, IA, USA, 3rd edition, 2007.
A. Sáinz, S. Delgado, I. Amusategui, M. A. Tesouro, and P. Cármenes, “Seroprevalence of canine ehrlichiosis in Castilla-León (north-west Spain),” Preventive Veterinary Medicine, vol. 29, no. 1, pp. 1–7, 1996.
View at: Publisher Site | Google Scholar
L. M. Costa Jr., K. Rembeck, M. F. B. Ribeiro, P. Beelitz, K. Pfister, and L. M. F. Passos, “Sero-prevalence and risk indicators for canine ehrlichiosis in three rural areas of Brazil,” The Veterinary Journal, vol. 174, no. 3, pp. 673–676, 2007.
View at: Publisher Site | Google Scholar
I. Tsachev, V. Kontos, I. Zarkov, and S. Krastev, “Survey of antibodies reactive with Ehrlichia canis among dogs in South Bulgaria,” Revue de Medecine Veterinaire, vol. 157, no. 10, pp. 481–485, 2006.
View at: Google Scholar
A. Egenvall, B. N. Bonnett, A. Gunnarsson et al., “Sero-prevalence of granulocytic Ehrlichia spp. and Borrelia burgdorferi sensu lato in Swedish dogs 1991–1994,” Scandinavian Journal of Infectious Diseases, vol. 32, no. 1, pp. 19–25, 2000.
View at: Publisher Site | Google Scholar
N. Pusterla, J. B. Pusterla, P. Deplazes et al., “Seroprevalence of Ehrlichia canis and of canine granulocytic ehrlichia infection in dogs in Switzerland,” Journal of Clinical Microbiology, vol. 36, no. 12, pp. 3460–3462, 1998.
View at: Google Scholar
B. Davoust, O. Bourry, J. Gomez et al., “Surveys on seroprevalence of canine monocytic ehrlichiosis among dogs living in the Ivory Coast and Gabon and evaluation of a quick commercial test kit Dot-ELISA,” Annals of the New York Academy of Sciences, vol. 1078, pp. 464–469, 2006.
View at: Publisher Site | Google Scholar
Y. M'Ghirbi, A. Ghorbel, M. Amouri, A. Nebaoui, S. Haddad, and A. Bouattour, “Clinical, serological, and molecular evidence of ehrlichiosis and anaplasmosis in dogs in Tunisia,” Parasitology Research, vol. 104, no. 4, pp. 767–774, 2009.
View at: Publisher Site | Google Scholar
A. C. H. Nakaghi, R. Z. Machado, M. T. Costa, M. R. André, and C. D. Baldani, “Canine ehrlichiosis: clinical, hematological, serological and molecular aspects,” Ciencia Rural, vol. 38, no. 3, pp. 766–770, 2008.
View at: Publisher Site | Google Scholar
O. L. Núñez, “Estudio de la seroprevalencia de Ehrlichia canis en México,” Revista AMMVEPE, vol. 14, pp. 83–85, 2003.
View at: Google Scholar
R. I. Rodríguez-Vivas, M. E. Bolio-González, and M. M. Ojeda-Chi, “Diagnóstico de la ehrlichiosis monocítica canina: una revisión actualizada,” Ciencia y Agricultura, vol. 12, no. 1, pp. 83–96, 2015.
View at: Publisher Site | Google Scholar
G. Baneth, T. Waner, A. Koplah, S. Weinstein, and A. Keysary, “Survey of Ehrlichia canis antibodies among dogs in Israel,” Veterinary Record, vol. 138, no. 11, pp. 257–259, 1996.
View at: Publisher Site | Google Scholar
C. S. Gaxiola, I. F. Obregón, M. M. Quintero, and R. M. Cabrera Rubio, Prevalencia de Rhipicephalus Sanguineus en Canideos de dos Colonias de Diferente Nivel Socio-Económico de Culiacán Sinaloa, Memorias del 13 Congreso Latinoamericano de Parasitología, 1997.
C. Cruz-Vázquez and Z. García-Vázquez, “Seasonal distribution of Rhipicephalus sanguineus ticks (Acari: Ixodidae) on dogs in an urban area of Morelos, Mexico,” Experimental and Applied Acarology, vol. 23, no. 3, pp. 277–280, 1999.
View at: Publisher Site | Google Scholar
L. Tinoco-Gracia, H. Quiroz-Romero, M. T. Quintero-Martínez et al., “Prevalence of Rhipicephalus sanguineus ticks on dogs in a region on the Mexico-USA border,” Veterinary Record, vol. 164, no. 2, pp. 59–61, 2009.
View at: Publisher Site | Google Scholar
C. Bulla, R. Kiomi Takahira, J. Pessoa Araújo Jr., L. A. Trinca, R. Souza Lopes, and C. E. Wiedmeyer, “The relationship between the degree of thrombocytopenia and infection with Ehrlichia canis in an endemic area,” Veterinary Research, vol. 35, no. 1, pp. 141–146, 2004.
View at: Publisher Site | Google Scholar
A. Rungsipipat, M. Oda, N. Kumpoosiri et al., “Clinicopathological study of experimentally induced canine monocytic ehrlichiosis,” Comparative Clinical Pathology, vol. 18, no. 1, pp. 13–22, 2009.
View at: Publisher Site | Google Scholar
A. Niwetpathomwat, S. Techangamsuwan, and S. Suvarnavibhaja, “A retrospective study of the clinical hematology and biochemistry of canine ehrlichiosis in an animal hospital population in Bangkok, Thailand,” Comparative Clinical Pathology, vol. 14, no. 4, pp. 217–220, 2006.
View at: Publisher Site | Google Scholar
E. E. Goldman, E. B. Breitschwerdt, C. B. Grindem, B. C. Hegarty, J. J. Walls, and J. S. Dumler, “Granulocytic ehrlichiosis in dogs from North Carolina and Virginia,” Journal of Veterinary Internal Medicine, vol. 12, no. 2, pp. 61–70, 1998.
View at: Publisher Site | Google Scholar
A. M. Liddell, S. L. Stockham, M. A. Scott et al., “Predominance of Ehrlichia ewingii in Missouri dogs,” Journal of Clinical Microbiology, vol. 41, no. 10, pp. 4617–4622, 2003.
View at: Publisher Site | Google Scholar
J. Moraes-Filho, F. S. Krawczak, F. B. Costa, J. F. Soares, and M. B. Labruna, “Comparative evaluation of the vector competence of four South American populations of the rhipicephalus sanguineus group for the bacterium Ehrlichia canis, the agent of canine monocytic ehrlichiosis,” PLoS ONE, vol. 10, no. 9, Article ID e0139386, 2015.
View at: Publisher Site | Google Scholar
H. Pat-Nah, R. I. Rodriguez-Vivas, M. E. Bolio-Gonzalez, S. L. Villegas-Perez, and E. Reyes-Novelo, “Molecular diagnosis of Ehrlichia canis in dogs and ticks Rhipicephalus sanguineus (Acari: Ixodidae) in Yucatan, Mexico,” Journal of Medical Entomology, vol. 52, no. 1, pp. 101–104, 2015.
View at: Publisher Site | Google Scholar

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Copyright © 2016 Pedro Pablo Martínez-Vega et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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