Printer Friendly

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

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[degrees]30'00"N and longitude 87[degrees]44'49 W (Figure 1) [29]. The climate is warm and humid, with an annual average temperature of 26.5[degrees]C, a minimum of 18[degrees]C, and a maximum of 34[degrees]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[R] tubes with and without EDTA anticoagulant. Tubes without anticoagulant were centrifuged for 5 min at 800 xg to separate the serum, which was then transferred to 1.5 mL Eppendorf tubes and stored at -20[degrees]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[R] 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[degrees]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[degrees]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[R] 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, >3y.o.), ticks (presence, absence), anemia (yes, no), leucopenia (yes, no), thrombocytopenia (yes, no), and hemorrhage (yes, no). Contingency tables (2 x K) were obtained with these variables. Variables with a p value [less than or equal to] 0.20 were analyzed in SPSS[R] 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 p 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 p [less than or equal to] 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.sub.95%] = 2.23-27.04, and p = 0.001) and >3y.o. (OR = 15.39, [CI.sub.95%] = 4.13-57.40, and p [less than or equal to] 0.001); presence of ticks (OR = 3.13, [CI.sub.95%] = 1.17-8.44, and p = 0.023); and thrombocytopenia (OR = 3.36, [CI.sub.95%] = 1.28-8.83, and p = 0.013) 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 beenreportedinIran [11];inAfrica, 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, Nimez [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 >3y.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, p = 0.005; >4 y.o.: OR =4.24, p = 0.043), and Brazil (25 y.o.: OR = 2.20, p [less than or equal to] 0.05; >5 y.o.: OR = 2.96, p [less than or equal to] 0.01), 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 p = 0.023), similar to the report by Costa et al. [37] (OR = 2.1, p [less than or equal to] 0.01) 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. Nunez [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-Nahetal. [56] foundinYucatan, 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.


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


[1] 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.

[2] 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.

[3] 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.

[4] C. N. Gutierrez, M. Martinez, E. Senchez 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.

[5] 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.

[6] S. Harrus and T. Waner, "Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): an overview," Veterinary Journal, vol. 187, no. 3, pp. 292-296, 2011.

[7] R. I. Rodriguez-Vivas, M. E. Bolio-Gonzelez, and M. M. OjedaChi, "Diagnestico de la ehrlichiosis monocitica canina: una revisien actualizada," Ciencia y Agricultura, vol. 12, no. 1, pp. 83-98, 2015.

[8] 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.

[9] 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.

[10] 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.

[11] 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.

[12] 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.

[13] 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.

[14] 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.

[15] 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.

[16] 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.

[17] 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.

[18] 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.

[19] 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.

[20] B. Skotarczak, "Canine ehrlichiosis," Annals of Agriculture and Environmental Medicine, vol. 10, no. 2, pp. 137-141, 2003.

[21] 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.

[22] 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.

[23] 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.

[24] 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.

[25] F. Dantas-Torres, "Biology and ecology of the brown dog tick, Rhipicephalus sanguineus," Parasites & Vectors, vol. 3, article no. 26, 2010.

[26] A. C. Garcia and O. L. Nunez, "Pancitopenia tropical en un perro," Revista AMMVEPE, vol. 7, pp. 235-236, 1996.

[27] 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.

[28] M. Jimenez-Coello, C. Perez-Osorio, I. Vado-Solis, J. C. Rodriguez-Buenfil, and A. Ortega-Pacheco, "Serological survey of Ehrlichia canis in stray dogs from Yucaten, Mexico, using two different diagnostic tests," Vector-Borne and Zoonotic Diseases, vol. 9, no. 2, pp. 209-211, 2009.

[29] Google-INEGI, Xcalak, Quintana-Roo, Mexico map in Google maps, October 2016, Xcalak,+Quintana+Roo/@18.2708536,-88.3961858,9z/data= !4m5!3m4!1s0x8f5b428a800da7ff:0xb2f5ac6748959c7d!8m2!3d18 .2713888!4d-87.8358333?hl=en.

[30] Comisien Nacional de Areas Naturales Protegidas (CONANP), Programa de Manejo. Parque Nacional Arrecifes de Xcalak, Comisien Nacional de Areas Naturales Protegidas, Mexico City, Meexico, 2004.

[31] R. I. Rodriguez-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.

[32] L. G. Voight and L. S. Shannon, Hematology Techniques & Concepts for Veterinary Technicians, Wiley-Blackwell, Iowa, IA, USA, 2nd edition, 2011.

[33] 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.

[34] 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.

[35] M. Thrusfield, Veterinary Epidemiology, Blackwell, Iowa, IA, USA, 3rd edition, 2007.

[36] A. Seinz, S. Delgado, I. Amusategui, M. A. Tesouro, and P. Caermenes, "Seroprevalence of canine ehrlichiosis in CastillaLeen (north-west Spain)," Preventive Veterinary Medicine, vol. 29, no. 1, pp. 1-7, 1996.

[37] 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.

[38] 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.

[39] A. Egenvall, B. N. Bonnett, A. Gunnarsson et al., "Seroprevalence of granulocytic Ehrlichia spp. and Borrelia burgdorferi sensulato in Swedish dogs 1991-1994," Scandinavian Journal of Infectious Diseases, vol. 32, no. 1, pp. 19-25, 2000.

[40] 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.

[41] 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.

[42] 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.

[43] A. C. H. Nakaghi, R. Z. Machado, M. T. Costa, M. R. Andre, and C. D. Baldani, "Canine ehrlichiosis: clinical, hematological, serological and molecular aspects," Ciencia Rural, vol. 38, no. 3, pp. 766-770, 2008.

[44] O. L. Nufiez, "Estudio de la seroprevalencia de Ehrlichia canis en Mexico," Revista AMMVEPE, vol. 14, pp. 83-85, 2003.

[45] R. I. Rodriguez-Vivas, M. E. Bolio-Gonzelez, and M. M. OjedaChi, "Diagnostico de la ehrlichiosis monocitica canina: una revision actualizada," Ciencia y Agricultura, vol. 12, no. 1, pp. 83-96, 2015.

[46] 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.

[47] C. S. Gaxiola, I. F. Obregen, M. M. Quintero, and R. M. Cabrera Rubio, Prevalencia de Rhipicephalus Sanguineus en Canideos de dos Colonias de Diferente Nivel Socio-Economico de Culiacan Sinaloa, Memorias del 13 Congreso Latinoamericano de Parasitologia, 1997.

[48] C. Cruz-Vazquez and Z. Garcia-Vazquez, "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.

[49] L. Tinoco-Gracia, H. Quiroz-Romero, M. T. Quintero-Martinez 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.

[50] C. Bulla, R. Kiomi Takahira, J. Pessoa Araujo 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.

[51] 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.

[52] 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.

[53] 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.

[54] 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.

[55] 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.

[56] 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.

Pedro Pablo Martinez-Vega, (1) Manuel Emilio Bolio-Gonzalez, (2) Roger Ivan Rodriguez-Vivas, (2) Eduardo Gutierrez-Blanco, (2) Carlos Perez- Osorio, (3) Sandra Luz Villegas-Perez, (2) and Carlos Humberto Sauri-Arceo (2)

(1) Laboratorio de Parasitologia, Centro de Investigaciones Regionales "Dr. Hideyo Noguchi" Unidad Inalambrica, Universidad Autonoma de Yucatan, Calle 96 S/N Cruzamientos Av. Jacinto Canek y Calle 47, 97225 Merida, YUC, Mexico

(2) Departamento de Salud Animal y Medicina Preventiva, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autonoma de Yucatan, Km. 15.5 Carr. Morida-Xmatkuil, AP 4-116 Itzimna, Merida, YUC, Mexico

(3) Unidad de Investigacion Clinica y Epidemiologia, FacultaddeMedicina, Universidad Autonoma de Yucatan, Av. Itzaes No. 498, 97000 Merida, YUC, Mexico

Correspondence should be addressed to Eduardo Gutierrez-Blanco;

Received 19 August 2016; Revised 31 October 2016; Accepted 13 November 2016

Academic Editor: Carlos E. P. Corbett

Caption: Figure 1: Map showing the geographical position of the studied area.
Table 1: Logistic regression analysis to detect associated factors
to anti-Ehrlichia spp. antibody response in 118 dogs from Xcalak,
Quintana Roo, Mexico.

Variable             Total   Positive    Prevalence (%)     OR

  <1 year             29         8             28
  1-3 years           42        30             71          7.77
  > 3 years           47        37             78          15.39
  No                  57        31             54
  Yes                 61        44             72          3.13
  No                  35        15             43
  Yes                 83        60             72          3.36
  No                  75        52             69
  Yes                 43        23             53          0.93

Variable             [CI.sub.95%]    p value

  <1 year
  1-3 years           2.23-27.04      0.001
  > 3 years           4.13-57.40      <0.001
  Yes                  1.17-8.41      0.023
  Yes                  1.28-8.83      0.013
  Yes                  0.32-2.70      0.891

OR: odds ratio; [CI.sub.95%]: confidence interval (95%); p value:
COPYRIGHT 2017 Hindawi Limited
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2017 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Research Article
Author:Martinez-Vega, Pedro Pablo; Bolio-Gonzalez, Manuel Emilio; Rodriguez-Vivas, Roger Ivan; Gutierrez-Bl
Publication:Journal of Tropical Medicine
Article Type:Report
Geographic Code:1MEX
Date:Jan 1, 2017
Previous Article:Diversity of Leptospira spp. in Rats and Environment from Urban Areas of Sarawak, Malaysia.
Next Article:Performance Evaluation of Commercial Dengue Diagnostic Tests for Early Detection of Dengue in Clinical Samples.

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters