Abstract
Canine vector-borne pathogens (CVBPs) comprise a group of disease agents mainly transmitted by ticks, fleas, mosquitoes and sand flies. In this study, we assessed the presence of CVBPs in an Afro-descendent community (Quilombola) of northeastern, Brazil. Dog blood samples (n = 201) were collected and analyzed by rapid test for the detection of antibodies against Leishmania spp., Anaplasma spp., Ehrlichia spp. and Borrelia burgdorferi sensu lato (s.l.), and antigens of Dirofilaria immitis. In addition, polymerase chain reactions were performed for Anaplasmataceae, Babesia spp., Hepatozoon spp., Rickettsia spp. and B. burgdorferi s.l. Overall, 66.7% of the dogs scored positive to at least one pathogen at serological and/or molecular methods. Antibodies against Ehrlichia spp. were the most frequently detected (57.2%; n = 115/201), followed by Anaplasma spp. (8.5%; n = 17/201), Leishmania spp. (8.5%; n = 17/201) and B. burgdorferi s.l. (0.5%; n = 1/201). For D. immitis, 11 out of 201 (5.5%) animals scored positive. At the molecular analysis, 10.4% (n = 21/201) of the samples scored positive for Babesia spp./Hepatozoon spp., followed by Anaplasmataceae (5.0%; n = 10/201) and Rickettsia spp. (3.0%; n = 6/201). All samples were negative for B. burgdorferi s.l. Our data demonstrated the presence of CVBPs in the studied population, with a high seropositivity for Ehrlichia spp. In addition, considering the detection of zoonotic pathogens in dogs and their relationship with people from Quilombola communities, effective control strategies are advocated for minimizing the risk of infection in this socially vulnerable human population and their pets.
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Introduction
Canine vector-borne diseases (CVBDs) are caused by a group of pathogens mainly transmitted by ticks (e.g., Babesia spp., Ehrlichia spp., Anaplasma spp., Rickettsia spp.), fleas (e.g., Rickettsia felis, Dipylidium caninum), mosquitoes (e.g., Dirofilaria spp.) and sand flies (e.g., Leishmania spp.) (Otranto 2018; Maggi and Krämer 2019; Alhassan et al. 2021). The zoonotic potential of some CVBD-causing agents represents a threat to human health, especially in the tropics and subtropics, as the climatic conditions of these areas are conducive to the growth and proliferation of arthropod vectors (Dantas-Torres 2008; Maggi and Krämer 2019). The CVBDs of major veterinary and public health concern are leishmaniasis and heartworm disease (HWD), followed by anaplasmosis, ehrlichiosis and babesiosis (Dantas-Torres et al. 2020; Borges et al. 2021). In Brazil, dogs can be infected by zoonotic Leishmania spp., including Leishmania infantum, Leishmania amazonensis and Leishmania braziliensis (Belo et al. 2013; Souza et al. 2019). Leishmania spp. infection occurs mostly through the bites of infected female phlebotomine sand flies (Alvar et al. 2012). Leishmaniases are still predominantly rural diseases, with wildlife species (e.g., foxes, opossums and rodents) acting as principal hosts of the parasites (Roque and Jansen 2014; Bezerra-Santos et al. 2021). However, dogs are considered the main reservoirs of L. infantum and source of infection to the vectors in both rural and urban areas (Dantas-Torres 2007). Another important parasite of zoonotic potential in Brazil is Dirofilaria immitis, the agent of HWD, often characterized by severe cardiopulmonary disorders which may be fatal. The distribution of D. immitis overlaps that of mosquito vectors of the genera Culex, Aedes, Ochlerotatus and Anopheles (Ahid and Lourenço-Oliveira 1999; Simón et al. 2012; Ramos et al. 2016; Maggi and Krämer 2019; Brianti et al. 2021; Mendoza-Roldan et al., 2021). For example, a previous study demonstrated the presence of competent vectors of D. immitis (e.g., Ochlerotatus scapularis and Ochlerotatus taeniorhynchus) occurring throughout the year in an endemic area of Brazil (Labarthe et al. 1998), with a correlation between the high populations of arthropod vectors and the odds of infection in dogs and humans (Bendas et al. 2019).
Anaplasma platys, Ehrlichia canis and Babesia vogeli are the major causative agents of canine anaplasmosis, ehrlichiosis and babesiosis in Brazil (Dantas-Torres 2008), which are characterized by a variety of clinical signs (e.g., pyrexia, lethargy, weight loss, lymphadenopathy, bleeding tendencies, hemoglobinuria, petechiae, jaundice and even death) (Ybañez et al. 2018) and hematological alterations (e.g., anemia and thrombocytopenia) in infected animals. The main biological vector of these hemoparasites is the brown dog tick (i.e., the recently proposed Rhipicephalus linneai, also referred to as the tropical lineage of Rhipicephalus sanguineus sensu lato by Šlapeta et al. 2021), which has also been associated with the transmission of other pathogens, such as Hepatozoon canis and bacterial species belonging to the spotted fever group rickettsiae (SFGR) (Ramos et al. 2014; Santos et al. 2018; Alhassan et al. 2021). Animals coinfected by multiple CVBD-causing pathogens are at higher risk of developing severe clinical signs (de Caprariis et al. 2011). For example, a study estimated that dogs with leishmaniasis are 12 times more likely to be coinfected with E. canis compared to healthy ones, with increased severity of clinical presentation, and potential reduction in the efficacy of the treatment (Attipa et al. 2018).
In Brazil, there are an estimated number of about 3,000 Quilombola communities composed by descendants of slaves of African origin, usually located in remote rural areas (Conde et al. 2020). People from these communities commonly live from agriculture and/or use of forest resources (Conde et al. 2020). In these areas wandering dogs, as well as owned restricted and semi-restricted ones are usually part of the domestic fauna. Data on canine zoonotic pathogens from these communities are scarce, with a single report recording a prevalence of 8.4% for L. infantum in skin samples from dogs (Silva et al. 2017). Nevertheless, the presence of wandering dogs, vectors and deficient sanitary conditions suggest that other pathogens of veterinary and public health concern may occur in these areas. Thus, the present study was aimed to assess the occurrence of CVBD-causing pathogens in a Quilombola community in the northeastern region of Brazil.
Material and methods
Study area
This study was conducted in a Quilombola community in the municipality of Garanhuns (08°53′25" S, 36°29′34" W; 896 m above sea level), Pernambuco, Northeastern Brazil. Semi-restricted or unrestricted dogs are frequently present in the study area and live in contact with other domestic animals (e.g., cats, birds and domestic ruminants) and wildlife (e.g., opossums, rodents and birds). The study area has a tropical savanna climate with dry-summer characteristics, which corresponds to the Köppen climate classification category “Aw,” presenting a mean annual temperature of 20 ºC (range, 16–30 ºC), relative humidity of 76% (38–100%) and precipitation of 873 mm (751–1000 mm) (Barbosa et al. 2016), with rains concentrated from April to July (Andrade et al. 2008).
Sample collection and laboratory analysis
From July 2021 to January 2022, blood samples (1.5–5 ml) were collected from cephalic vein of 201 dogs. Samples were divided into two aliquots: one stored in tubes containing EDTA, and the other in tubes without anticoagulant, for molecular and serological analysis, respectively. Data on sex, dog categories (i.e., restricted and semi-restricted according to Otranto et al. 2017), overnight stay and the presence of ectoparasites were recorded for each dog. The serum samples were tested by an immunochromatographic assay (DPP® CVL, BioManguinhos) for anti-Leishmania spp. antibodies and by an ELISA rapid test (SNAP® 4Dx Plus, Idexx), which detects antibodies to Anaplasma spp. (A. platys/A. phagocytophilum), Ehrlichia spp. (E. canis/E. ewingii), B. burgdorferi s.l. and antigens of D. immitis. All tests were performed according to the manufacturer’s instructions.
Genomic DNA was extracted from 200 μl aliquots of EDTA-treated blood samples using GenUP DNA Kit (Biotechrabbit, Berlin, Germany) following the manufacturer’s instructions. All samples were tested for the presence of Anaplasmataceae, Borrelia spp., Rickettsia spp., Babesia spp. and Hepatozoon spp. by conventional PCR, using the primers reported in Table 1.
PCR products were purified (Thermo Scientific™ FastAP™ Thermosensitive Alkaline Phosphatase) and sequenced using the same forward and reverse primer sets reported in Table 1 for each pathogen, employing the Big DyeTerminator v.3.1 chemistry in a 3130 Genetic analyzer (Applied Biosystems, California, USA) in an automated sequencer (ABI-PRISM 377). Nucleotide sequences were edited, aligned and analyzed using Mega 7.0 software and compared with reference sequences available on GenBank database using Basic Local Alignment Search Tool (BLAST; http://blast.ncbi.nlm.nih.gov/Blast.cgi).
Data analysis
Descriptive statistics were used to calculate relative and absolute frequencies. Exact binominal 95% confidence intervals (CIs) were established for proportions. The chi-square with Yates correction was used to compare proportions with a p value < 0.05 regarded as statistically significant. Analyses were performed using Epitools-Epidemiological Calculators (https://epitools.ausvet.com.au/).
Results
Out of 201 examined dogs, 134 (66.7%; 95% CI = 59.9–72.8%) tested serologically or molecularly positive to at least one vector-borne pathogen. Particularly, Ehrlichia spp. was the most frequently detected by serology in 115 (57.2%; 95% CI = 50.3–63.9%), followed by Anaplasma spp. 17 (8.5%; 95% CI = 5.3–13.1%), Leishmania spp. 17 (8.5; 95% CI = 5.3–13.1%) and D. immitis 11 (5.5%; 95% CI = 3.1–9.5%). In addition, simultaneous positivity was observed in 16.9% (n = 34) of dogs, mostly by Ehrlichia spp. with other pathogens (Table 2). Only one female dog was seropositive for B. burgdorferi s.l. with co-positivity to Ehrlichia spp. Data on sex, dog category, overnight stay and the presence of ectoparasites are reported in Table 3, along with the percentage of dogs positive for each pathogen.
At the molecular analysis, the dog blood samples showed PCR-positive results for Babesia spp./Hepatozoon spp. in 21 (10.4%; 95% CI = 6.9–15.4%), Anaplasmataceae in 10 (5.0%; 95% CI 2.7–8.9%) and Rickettsia spp. in 6 (3.0%; 95% CI 1.4–6.4%). All samples were PCR-negative for the presence B. burgdorferi s.l., and for the rickettsial ompA gene.
According to BLAST analysis, two samples positive for the 18S rRNA gene revealed 100% nucleotide identity with B. vogeli (accession number: MN700646), and 19 samples presented 97.2–100% nucleotide identity with H. canis (accession numbers: MK673842; MK645969; MN791089; MK673839). For the 16S rRNA gene sequences, two samples revealed 100% nucleotide identity with A. platys (accession numbers: MN922611; MN994338; MN922609; MN922608) and eight samples revealed 99.1–100% nucleotide identity with E. canis (accession numbers: MN922610; MN227484; MN227484; MK507008). A single A. platys positive sample was also reagent at serological examination, whereas five E. canis positive samples were detected at both molecular and serological tests.
Finally, four samples positive for the gltA gene had 100% nucleotide identity with R. felis sequences (accession numbers: MN817141; MN817140; MT499363).
Sequences herein obtained were submitted to GenBank under the accession numbers: OP084684 for Babesia vogeli; OP084681 to OP084683 for Hepatozoon canis; OP082323 for Anaplasma spp.; OP082324 to OP082328 for Ehrlichia spp.; and OP099835 for Rickettsia felis.
Discussion
Data presented herein indicated a high overall level of exposure to vector-borne pathogens in dogs from the Quilombola community in northeastern Brazil. In particular, over 50% of the dogs were seropositive to Ehrlichia spp., which is in line with previous studies conducted in the same region (Figueredo et al. 2017; Dantas-Torres et al. 2020). This may be partly explained by the high prevalence of the brown dog tick on dogs in the study area (Santos et al. 2017; 2018). The seropositivity to other pathogens (i.e., Anaplasma spp., Leishmania spp. and D. immitis) was lower as compared with a recent study conducted in an urban area of Pernambuco (Dantas-Torres et al. 2020). Differences may be related to many eco-epidemiological factors, including the level of exposure to the vectors and climatic factors. For example, in the same area a low occurrence and diversity in sand fly species throughout a one-year sampling period has been demonstrated, with Lutzomyia evandroi being the only species identified (Ubirajara Filho et al. 2020).
Among the vector-borne protozoa, H. canis was the most frequently detected molecularly (i.e., n = 19 dogs were infected by H. canis, while only two dogs by B. vogeli). This may be due to the shorter time of circulation of B. vogeli in the blood of infected animals. Epidemiological data from previous studies demonstrated that B. vogeli is highly prevalent in Brazil, with up to 8.2% molecularly positive dogs in Pernambuco (Ramos et al. 2010; Dantas-Torres et al. 2021), 8.0% in São Paulo (O’Dwyer et al. 2009), 10.0% in Paraíba (Rotondano et al. 2015), 15.0% in Ceará (Fonsêca et al. 2022), 30.6% in Minas Gerais (Barbosa et al. 2020) and 14.1% in Rio de Janeiro (Paulino et al. 2018; Camilo et al. 2021). Conversely, H. canis has been reported with lower prevalence (i.e., 0.4% to 5.4%) in Northeastern Brazil (Ramos et al. 2010; Dantas-Torres et al. 2021), differently from the Southeastern region, in which higher prevalence values (i.e., 58.7–79.2%) were reported (Miranda et al. 2014; Spolidorio et al. 2009).
The simultaneous detection of Ehrlichia spp. and Anaplasma spp. (6.5%) at PCR and serological tests agrees with previous reports in Pernambuco state in which both pathogens were the most frequently diagnosed molecularly (Ramos et al. 2010). The above picture is probably due to the high abundance of brown dog ticks, which may transmit multiple pathogens simultaneously (Shaw et al. 2001). Similarly, the positivity to both Ehrlichia spp. and Leishmania spp. is of importance due to the implications those pathogens may have in the pathogenesis of CVBD, mainly their clinical presentation, and response to therapy (de Caprariis et al. 2011; Attipa et al. 2018). For example, a study on the experimental infection of E. canis and A. platys in dogs demonstrated that these pathogens cause various changes in pathophysiological parameters (i.e., more pronounced anemia and thrombocytopenia). Therefore, raising awareness of the risks of simultaneous positivity when animals are exposed to multiple tick-borne pathogens (Gaunt et al. 2010).
Rickettsia felis, a zoonotic rickettsia belonging to the SFG, previously described infecting human patients from Kenya (Richards et al. 2010) and Serbia (Banović et al. 2021), was molecularly detected for the first time in the dogs herein assessed. This pathogen was also detected in fleas (Ctenocephalides felis) and ticks (Dermacentor nitens) collected from dogs and horses from the same study area (Oliveira et al. 2020). Rickettsia felis is widespread in Brazil, and its distribution overlaps that of C. felis, its main biological vector (Horta et al. 2014). This finding is particularly important from a One Health perspective, considering that the local circulation of zoonotic pathogens may represent an eminent risk for the Quilombola community.
Conclusion
Data herein presented demonstrated that different pathogens (i.e., B. vogeli, A. platys, E. canis, H. canis and R. felis) are prevalent in dogs from the studied Quilombola community in northeastern, Brazil. Considering the occurrence of zoonotic pathogens in dogs and their close relationship with humans living in these communities, increased awareness and effective control strategies are advocated for minimizing the risk of infection in animals and humans from Quilombola communities, where the access to veterinary services is generally limited.
Data availability
The authors declare that data supporting the findings of this study are available within the article.
References
Ahid SMM, Lourenço-de-Oliveira R (1999) Mosquitos vetores potenciais da dirofilariose canina no Nordeste do Brasil. Rev Saú Públ 33:560–565. https://doi.org/10.1590/S0034-89101999000600007
Alhassan A, Hove P, Sharma B, Matthew-Belmar V, Karasek I, Lanza-Perea M, Werners AH, Wilkerson MJ, Ganta RR (2021) Molecular detection and characterization of Anaplasma platys and Ehrlichia canis in dogs from the Caribbean. Ticks Tick Borne Dis 12:101727. https://doi.org/10.1016/j.ttbdis.2021.101727
Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, Boer M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7:e35671. https://doi.org/10.1371/journal.pone.0035671
Andrade ARS, Paixão FJR, Azevedo CAV, Gouveia JPG, Oliveira JAS Jr (2008) Estudo do comportamento de períodos secos e chuvosos no município Garanhuns, PE, para fins de planejamento agrícola. PA&T 1:54–61
Attipa C, Solano-Gallego L, Papasouliotis K, Soutter F, Morris D, Helps C, Carver S, Tasker S (2018) Association between canine leishmaniosis and Ehrlichia canis co-infection: a prospective case-control study. Parasit Vectors 11:1–9. https://doi.org/10.1186/s13071-018-2717-8
Banović P, Díaz-Sánchez AA, Galon C, Simin V, Mijatović D, Obregón D, Moutailler S, Cabezas-Cruz A (2021) Humans infested with Ixodes ricinus are exposed to a diverse array of tick-borne pathogens in Serbia. Ticks Tick Borne Dis 12:101609. https://doi.org/10.1016/j.ttbdis.2020.101609
Barbosa COS, Garcia JR, Fava NMN, Pereira DA, Cunha MJR, Nachum-Biala Y, Cury MC, Baneth G (2020) Babesiosis caused by Babesia vogeli in dogs from Uberlândia State of Minas Gerais, Brazil. Parasitol Res 119:1173–1176. https://doi.org/10.1007/s00436-019-06515-3
Barbosa VV, Souza WM, Galvinício JD (2016) Análise da variabilidade climática do município de Garanhuns, Pernambuco–Brasil. Rev Bras Geogr Fís 9:353–367. https://doi.org/10.26848/rbgf.v9.2.p353-367
Belo VS, Struchiner CJ, Werneck GL, Barbosa DS, Oliveira RB, Neto RG, Silva ES (2013) A systematic review and meta-analysis of the factors associated with Leishmania infantum infection in dogs in Brazil. Vet Parasitol 195:1–13. https://doi.org/10.1016/j.vetpar.2013.03.010
Bendas AJR, Branco AS, Silva BRSA, Paiva JP, Miranda MGN, Mendes-de-Almeida F, Labarthe NV (2019) Mosquito abundance in a Dirofilaria immitis hotspot in the eastern state of Rio de Janeiro. Brazil Vet Parasitol Reg Stud Reports 18:100320. https://doi.org/10.1016/j.vprsr.2019.100320
Bezerra-Santos MA, Ramos RAN, Campos AK, Dantas-Torres F, Otranto D (2021) Didelphis spp. opossums and their parasites in the Americas: A One Health perspective. Parasitol Res 120:4091–4111. https://doi.org/10.1007/s00436-021-07072-4
Borges LM, Oliveira AG, Mateus NLF, Oliveira EF, Arrua AEC, Infran JOM, Taketa LB, Monteiro PEO, Fernandes CEDS, Piranda EM (2021) Canine visceral leishmaniasis in an area of sporadic transmission in Brazil. Vector Borne Zoonotic Dis 21:539–545. https://doi.org/10.1089/vbz.2020.2701
Brianti E, Panarese R, Napoli E, Benedetto G, Gaglio G, Bezerra-Santos MA, Mendoza-Roldan JA, Otranto D (2021) Dirofilaria immitis infection in the Pelagie archipelago: The southernmost hyperendemic focus in Europe. Transbound Emerg Dis 00:1–7. https://doi.org/10.1111/tbed.14089
Camilo TA, Mendonça LP, Santos DM, Ramirez LH, Senne NA, Paulino PG, Oliveira PA, Peixoto MP, Massard CL, Angelo IDC, Santos HA (2021) Spatial distribution and molecular epidemiology of Babesia vogeli in household dogs from municipalities with different altitude gradients in the state of Rio de Janeiro. Brazil Ticks Tick Borne Dis 12:101785. https://doi.org/10.1016/j.ttbdis.2021.101785
Conde BE, Aragaki S, Ticktin T, Surerus Fonseca A, Yazbek PB, Sauini T, Rodrigues E (2020) Evaluation of conservation status of plants in Brazil’s Atlantic forest: an ethnoecological approach with Quilombola communities in Serra do Mar State Park. PLoS ONE 15:e0238914. https://doi.org/10.1371/journal.pone.0238914
Dantas-Torres F (2007) The role of dogs as reservoirs of Leishmania parasites, with emphasis on Leishmania (Leishmania) infantum and Leishmania (Viannia) braziliensis. Vet Parasitol 149:139–146. https://doi.org/10.1016/j.vetpar.2007.07.007
Dantas-Torres F (2008) Canine vector-borne diseases in Brazil. Parasit Vectors 1:1–17. https://doi.org/10.1186/1756-3305-1-25
Dantas-Torres F, Figueredo LA, Sales K, Miranda D, Alexandre J, Silva YY, Silva LG, Valle GR, Ribeiro VM, Otranto D, Deuster K, Pollmeier M, Altreuther G (2020) Prevalence and incidence of vector-borne pathogens in unprotected dogs in two Brazilian regions. Parasit Vectors 13:1–7. https://doi.org/10.1186/s13071-020-04056-8
Dantas-Torres F, Alexandre J, Miranda DEO, Figueredo LA, Sales KGDS, Sousa-Paula LC, Silva LG, Valle GR, Ribeiro VM, Otranto D, Deuster K, Pollmeier M, Altreuther G (2021) Molecular epidemiology and prevalence of babesial infections in dogs in two hyperendemic foci in Brazil. Parasitol Res 120:2681–2687. https://doi.org/10.1007/s00436-021-07195-8
de Caprariis D, Dantas-Torres F, Capelli G, Mencke N, Stanneck D, Breitschwerdt EB, Otranto D (2011) Evolution of clinical, haematological and biochemical findings in young dogs naturally infected by vector-borne pathogens. Vet Microbiol 21:206–212. https://doi.org/10.1016/j.vetmic.2010.10.006
Figueredo LA, Sales KGDS, Deuster K, Pollmeier M, Otranto D, Dantas-Torres F (2017) Exposure to vector-borne pathogens in privately owned dogs living in different socioeconomic settings in Brazil. Vet Parasitol 243:18–23. https://doi.org/10.1016/j.vetpar.2017.05.020
Fonsêca ADV, Oliveira LMB, Jorge FR, Cavalcante RO, Bevilaqua CML, Pinto FJM, Santos JMLD, Teixeira BM, Rodrigues AKPP, Braz GF, Viana GA, Costa EC, Serpa MCA, Weck BC, Labruna MB (2022) Occurrence of tick-borne pathogens in dogs in a coastal region of the state of Ceará, northeastern Brazil. Rev Bras Parasitol Vet 31:e021321. https://doi.org/10.1590/S1984-29612022010
Gaunt S, Beall M, Stillman B, Lorentzen L, Diniz P, Chandrashekar R, Breitschwerdt E (2010) Experimental infection and co-infection of dogs with Anaplasma platys and Ehrlichia canis: hematologic, serologic and molecular findings. Parasit Vectors 3:1–10. https://doi.org/10.1186/1756-3305-3-33
Horta MC, Ogrzewalska M, Azevedo MC, Costa FB, Ferreira F, Labruna MB (2014) Rickettsia felis in Ctenocephalides felis felis from five geographic regions of Brazil. Am J Trop Med Hyg 91:96–100. https://doi.org/10.4269/ajtmh.13-0699
Labarthe N, Serrão ML, Melo YF, Oliveira SJ, Lourenço-de-Oliveira R (1998) Mosquito frequency and feeding habits in an enzootic canine dirofilariasis area in Niterói, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 93:145–154. https://doi.org/10.1590/S0074-02761998000200002
Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42:90–98. https://doi.org/10.1128/jcm.42.1.90-98.2004
Maggi RG, Krämer F (2019) A review on the occurrence of companion vector-borne diseases in pet animals in Latin America. Parasit Vectors 12:1–37. https://doi.org/10.1186/s13071-019-3407-x
Mendoza-Roldan JA, Gabrielli S, Cascio A, Manoj RRS, Bezerra-Santos MA, Benelli G, Brianti E, Latrofa MS, Otranto D (2021) Zoonotic Dirofilaria immitis and Dirofilaria repens infection in humans and an integrative approach to the diagnosis. Acta Trop 223:106083. https://doi.org/10.1016/j.actatropica.2021.106083
Miranda RL, O’Dwyer LH, Castro JR, Metzger B, Rubini AS, Mundim AV, Eyal O, Talmi-Frank D, Cury MC, Baneth G (2014) Prevalence and molecular characterization of Hepatozoon canis in dogs from urban and rural areas in Southeast Brazil. Res Vet Sci 97:325–328
O’Dwyer LH, Lopes VV, Rubini AS, Paduan KS, Ribolla PE (2009) Babesia spp. infection in dogs from rural areas of São Paulo State. Brazil Rev Bras Parasitol Vet 18:23–26. https://doi.org/10.4322/rbpv.01802005
Oliveira JCP, Reckziegel GH, Ramos CAN, Giannelli A, Alves LC, Carvalho GA, Ramos RAN (2020) Detection of Rickettsia felis in ectoparasites collected from domestic animals. Exp Appl Acarol 81:255–264. https://doi.org/10.1007/s10493-020-00505-2
Otranto D (2018) Arthropod-borne pathogens of dogs and cats: From pathways and times of transmission to disease control. Vet Parasitol 15:68–77. https://doi.org/10.1016/j.vetpar.2017.12.021
Otranto D, Dantas-Torres F, Mihalca AD, Traub RJ, Lappin M, Baneth G (2017) Zoonotic parasites of sheltered and stray dogs in the era of the global economic and political crisis. Trends Parasitol 33:813–825. https://doi.org/10.1016/j.pt.2017.05.013
Parola P, Roux V, Camicas JL, Baradji I, Brouqui P, Raoult D (2000) Detection of ehrlichiae in African ticks by polymerase chain reaction. Trans R Soc Trop Med Hyg 94:707–708. https://doi.org/10.1016/s0035-9203(00)90243-8
Paulino PG, Pires MS, Silva CB, Peckle M, Costa RL, Vitari GLV, Abreu APM, Massard CL, Santos HA (2018) Molecular epidemiology of Babesia vogeli in dogs from the southeastern region of Rio de Janeiro, Brazil. Vet Parasitol Reg Stud Reports 13:160–165. https://doi.org/10.1016/j.vprsr.2018.06.004
Ramos R, Ramos C, Araújo F, Oliveira R, Souza I, Pimentel D, Galindo M, Santana M, Rosas E, Faustino M, Alves L (2010) Molecular survey and genetic characterization of tick-borne pathogens in dogs in metropolitan Recife (north-eastern Brazil). Parasitol Res 107:1115–1120. https://doi.org/10.1007/s00436-010-1979-7
Ramos RAN, Latrofa MS, Giannelli A, Lacasella V, Campbell BE, Dantas-Torres F, Otranto D (2014) Detection of Anaplasma platys in dogs and Rhipicephalus sanguineus group ticks by a quantitative real-time PCR. Vet Parasitol 205:285–288. https://doi.org/10.1016/j.vetpar.2014.06.023
Ramos RAN, Rêgo AGO, Firmino EDF, Ramos CAN, Carvalho GA, Dantas-Torres F, Otranto D, Alves LC (2016) Filarioids infecting dogs in northeastern Brazil. Vet Parasitol 15:26–29. https://doi.org/10.1016/j.vetpar.2016.06.025
Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol 173:1576–1589. https://doi.org/10.1128/jb.173.5.1576-1589.1991
Richards AL, Jiang J, Omulo S, Dare R, Abdirahman K, Ali A, Sharif SK, Feikin DR, Breiman RF, Njenga MK (2010) Human Infection with Rickettsia felis, Kenya. Emerg Infect Dis 16:1081–1086. https://doi.org/10.3201/eid1607.091885
Roque AL, Jansen AM (2014) Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl 3:251–262. https://doi.org/10.1016/j.ijppaw.2014.08.004
Rotondano TE, Almeida HK, Krawczak FS, Santana VL, Vidal IF, Labruna MB, Azevedo SS, Almeida AM, Melo MA (2015) Survey of Ehrlichia canis, Babesia spp. and Hepatozoon spp. in dogs from a semiarid region of Brazil. Rev Bras Parasitol 24:52–58. https://doi.org/10.1590/S1984-29612015011
Santos MAB, Souza IB, Macedo LO, Ramos CAN, Rego AGO, Alves LC, Ramos RAN, Carvalho GA (2017) Cercopithifilaria bainae in Rhipicephalus sanguineus sensu lato ticks from dogs in Brazil. Ticks Tick Borne Dis 8:623–625. https://doi.org/10.1016/j.ttbdis.2017.04.007
Santos MAB, Macedo LO, Otranto D, Ramos CAN, Rêgo AGOD, Giannelli A, Alves LC, Carvalho GA, Ramos RAN (2018) Screening of Cercopithifilaria bainae and Hepatozoon canis in ticks collected from dogs of Northeastern Brazil. Acta Parasitol 25:605–608. https://doi.org/10.1515/ap-2018-0069
Shaw SE, Day MJ, Birtles RJ, Breitschwerdt EB (2001) Tick-borne infectious diseases of dogs. Trends Parasitol 2:74–80. https://doi.org/10.1016/s1471-4922(00)01856-0
Silva AF, Damasceno ARA, Prado WS, Caldeira RD, Sampaio-Junior FD, Farias DM, Silva LCO, Guimarães RJPS, Góes-Cavalcante G, Scofield A (2017) Leishmania infantum infection in dogs from maroon communities in the Eastern Amazon. Ciênc Rural 47:e20160025. https://doi.org/10.1590/0103-8478cr20160025
Simón F, Siles-Lucas M, Morchón R, González-Miguel J, Mellado I, Carretón E, Montoya-Alonso JA (2012) Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev 25:507–544. https://doi.org/10.1128/CMR.00012-12
Skotarczak B, Wodecka B, Hermanowska-Szpakowicz T (2002) Sensitivity of PCR method for detection of DNA of Borrelia burgdorferi sensu lato in different isolates. Przegl Epidemiol 56:73–79
Šlapeta J, Chandra S, Halliday B (2021) The “tropical lineage” of the brown dog tick Rhipicephalus sanguineus sensu lato identified as Rhipicephalus linnaei (Audouin, 1826). Int J Parasitol 51:431–436. https://doi.org/10.1016/j.ijpara.2021.02.001
Souza NA, Leite RS, Silva SO, Penna MG, Vilela LFF, Melo MN, Andrade ASR (2019) Detection of mixed Leishmania infections in dogs from an endemic area in southeastern Brazil. Acta Trop 193:12–17. https://doi.org/10.1016/j.actatropica.2019.02.016
Spolidorio MG, Labruna MB, Zago AM, Donatele DM, Caliari KM, Yoshinari NH (2009) Hepatozoon canis infecting dogs in the State of Espírito Santo, southeastern Brazil. Vet Parasitol 163:357–361. https://doi.org/10.1016/j.vetpar.2009.05.002
Tabar MD, Altet L, Francino O, Sánchez A, Ferrer L, Roura X (2008) Vector-borne infections in cats: molecular study in Barcelona area (Spain). Vet Parasitol 151:332–336. https://doi.org/10.1016/j.vetpar.2007.10.019
Ubirajara Filho CRC, Sales KGS, Lima TARF, Dantas-Torres F, Alves LC, Carvalho GA, Ramos RAN (2020) Lutzomyia evandroi in a New Area of Occurrence of Leishmaniasis. Acta Parasitol 65:716–722. https://doi.org/10.2478/s11686-020-00215-0
Ybañez R, Ybañez AP, Arnado L, Belarmino L, Malingin K, Cabilete P, Amores Z, Talle MG, Liu M, Xuan X (2018) Detection of Ehrlichia, Anaplasma, and Babesia spp. in dogs of Cebu. Philippines Vet World 11:14–19. https://doi.org/10.14202/vetworld.2018.14-19
Acknowledgments
This article is based on the development of activities carried out during the Programa Institucional de Internacionalização (CAPES-PRINT) sandwich doctoral period at the Department of Veterinary Medicine, University of Bari, Italy, with support from a fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
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Lucia Oliveira de Macedo: methodology and first draft of the manuscript; Marcos Antonio Bezerra-Santos: methodology, review and editing; Carlos Roberto Cruz Ubirajara Filho: methodology; Kamila Gaudêncio da Silva Sales: methodology; Lucas C. de Sousa-Paula: methodology; Lidiane Gomes da Silva: methodology; Filipe Dantas-Torres: review and editing; Rafael Antonio do Nascimento Ramos: methodology, review and editing; Domenico Otranto: supervision, review and editing. All authors reviewed and agreed with the last version of the manuscript.
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The Ethics Committee for Animal Experimentation (ECAE) of Federal Rural University of Pernambuco approved all study procedures (approval number: 1041060520).
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de Macedo, L.O., Bezerra-Santos, M.A., Filho, C.R.C.U. et al. Vector-borne pathogens of zoonotic concern in dogs from a Quilombola community in northeastern Brazil. Parasitol Res 121, 3305–3311 (2022). https://doi.org/10.1007/s00436-022-07661-x
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DOI: https://doi.org/10.1007/s00436-022-07661-x