Abstract
Knowledge on the epidemiology of parasitic and vector-borne infections is still very limited for Albania, a country located in the Balkan Peninsula in southeast Europe. Recent publications indicated prevalence rates of up to 52 % for vector-borne infections in less-cared dogs in Albania. To provide data on the epidemiological situation in dogs under veterinary care, a total of 602 client-owned dogs presented to four small animal clinics between March 2010 and April 2011 in Tirana, Albania, were screened by examination of Giemsa-stained blood smears, PCR, and serological methods for the presence of arthropod-borne infections, as well as Neospora caninum and Toxoplasma gondii. Eight different pathogens, namely Babesia vogeli, Hepatozoon canis, Leishmania infantum, Dirofilaria immitis, Anaplasma phagocytophilum, Anaplasma platys, Ehrlichia canis, and Mycoplasma haemocanis, were detected by direct methods with prevalence rates ranging from 1 to 9 %. Seroprevalence for Babesia spp., L. infantum, Anaplasma spp., and E. canis were 6.6, 5.1, 24.1, and 20.8 %, respectively. Dogs >1 year of age were positive for vector-borne infections significantly more often than younger dogs (p = 0.003). More than half (51.7 %) of the dogs were seroreactive to T. gondii and 18.3 % to N. caninum. This is the first report on the detection of A. phagocytophilum, A. platys, E. canis, and M. haemocanis by PCR as well as the serological confirmation of exposure of dogs to N. caninum and T. gondii in Albania. The spectrum of pathogens and the seroprevalences for N. caninum and T. gondii in client-owned dogs from Tirana, Albania, are comparable to that reported in other countries in the Mediterranean Basin. The prevalence rates of vector-borne pathogens are at the lower range of that reported in studies from this geographical region. This is probably due to increased awareness of the owners of pet dogs, including better husbandry conditions and ectoparasiticidal treatment, thus limiting exposure of dogs to vectors.
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Introduction
Knowledge on the epidemiology of parasitic infections in companion animals in general and vector-borne infections in particular is still very limited for the formerly remote and politically isolated country of Albania. A more comprehensive picture on parasitic (e.g., gastrointestinal helminths, lungworms, and ectoparasites) infections in dogs and cats including vector-borne pathogens (e.g., Babesia canis, Leishmania infantum, Dirofilaria immitis, and Ehrlichia canis) has been established only very recently (Cicko and Cani 1998; Cicko et al. 1999; Dhamo et al. 2006; Lazri et al. 2008; Hamel et al. 2009; Xhaxhiu et al. 2009, 2011; Rapti and Rehbein 2010; Knaus et al. 2011a, b, 2012, 2014; Silaghi et al. 2012, 2013, 2014; Bizhga et al. 2013; Sommer et al. 2015). Previous studies mostly in less well-cared dogs reported on the presence of Babesia spp., Hepatozoon canis, filarial infections, as well as E. canis in PCR, serological and/or microscopical examinations (Lazri et al. 2008; Hamel et al. 2009). In order to corroborate previously published findings and to provide updated information on parasitic and vector-borne infections in dogs, a survey was conducted from March 2010 to April 2011 to assess the status of client-owned dogs receiving veterinary care presented to four small animal clinics in Tirana, Albania. This paper presents the results of the microscopical, serological, and molecular biological screening of blood smears, serum, and whole blood samples for vector-borne infections, as well as from a serosurvey on Neospora caninum and Toxoplasma gondii. Results of the examination and identification of parasitic stages in fecal samples and ectoparasites collected from these dogs are reported elsewhere (Shukullari et al. 2015; Shukullari et al. Parasites and vector-borne diseases in client-owned dogs in Albania. Infestation with arthropod ectoparasites, in preperation).
Materials and methods
Sample collection and animal data
At total of 602 dogs presented between March 2010 and April 2011 in Tirana, Albania, to four small animal clinics were sampled with the informed consent of their owners. Whole blood (EDTA anticoagulant) and serum samples were obtained from all animals. Blood smears were prepared, air-dried, and stored at room temperature until further processing. Blood and serum samples were stored at −18 °C. Basic demographic data of the sampled animals with the parameters of interest is presented in Table 1. Additional information retrieved from a questionnaire answered by the owners of each dog is given elsewhere (Shukullari et al. Parasites and vector-borne diseases in client-owned dogs in Albania. Infestation with arthropod ectoparasites, in preperation).
Laboratory diagnostics
Blood smears were Giemsa-stained and examined with a light microscope at 500-fold magnification for pathogens in the blood. Whole blood samples were screened by PCR for DNA of the following pathogens: Babesia spp., L. infantum, E. canis, Anaplasma phagocytophilum, Anaplasma platys, and Mycoplasma spp. (Table 2). DNA extraction was performed from 200 μl blood with the QIAamp DNA MiniKit (Qiagen, Hilden, Germany) following the manufacturer’s instructions. Quality and quantity of extracted DNA were checked with the spectrophotometer NanoDrop ND-1000 (Peqlab, Erlangen, Germany). Conventional PCR was used for the detection of Babesia spp. and Mycoplasma spp. DNA (Watanabe et al. 2003; Casati et al. 2006). Species identification was performed on the species-specific length of the PCR products. Primers and PCR conditions used are summarized in Table 2. The HotMaster Taq DNA Polymerase Kit (5PRIME, Darmstadt, Germany) was used. Real-time PCR was used for the detection of L. infantum, A. phagocytophilum, A. platys, and E. canis DNA (Courtney et al. 2004; Mary et al. 2004; Teglas et al. 2005; Silaghi et al. 2011a; Ionita et al. 2013). Real-time PCR was carried out in an AB7500 (Applied Biosystems, Darmstadt, Germany) using the TaqMan® Gene Expression MasterMix (Applied Biosystems, Darmstadt, Germany), according to the manufacturer’s instructions and with primers and probes under conditions listed in Table 2. Positive and negative controls were included in each PCR run. An 2 % agarose-gel electrophoresis of amplification products of conventional PCRs was performed, and products were visualized under UV light with GelRed™ (Biotium, Hayward, USA). PCR products of the partial Babesia spp. 18srRNA gene were purified (QIAquick PCR Purification Kit, Qiagen, Hilden, Germany), and sequenced to Eurofins MWG Operon (Martinsried, Germany), and obtained sequences were analyzed as described (Silaghi et al. 2011b).
The DiroChek® Canine/Feline Antigen Test Kit (Synbiotics Corp., San Diego, USA) was used for screening for the circulating antigens of female D. immitis. Antibodies to Babesia spp., L. infantum, Anaplasma spp., E. canis, N. caninum and T. gondii were detected using commercial IFA-testkits (MegaCor, Hörbranz, Austria) and an in-house L. infantum-IFAT (cf. Mancianti et al. 1995). Antibody titers ≥1:40 to E. canis, ≥1:50 to N. caninum and T. gondii, and ≥1:64 to Babesia spp., L. infantum, and Anaplasma spp. were considered as seropositive. No endpoint titers were assessed in this survey.
Statistical analysis
The statistical analysis including calculation of the 95 % Clopper-Pearson confidence intervals for prevalence was performed with software package R version 2.13.1 (R Development Core Team 2010). Associations between presence of/exposure to pathogens and dog management factors or age (≤1 and >1 year) of the animals were also analyzed. Factors with p values of less than 0.2 and cofounders (sex, age, season of sampling [winter, spring, summer, fall]), use (pet dog, hunting dog, working dog), habitat [city, suburban, rural], husbandry [indoors, kennel, yard], feed [raw, cooked/dry, both]) were forced into a multiple linear regression model to evaluate the adjusted effects of the associated factors. Level of significance for all analyses was set at p < 0.05.
Results
A total of 151 out of 602 dogs (25.1 %) were positive for vector-borne pathogens by direct methods (Giemsa-stained blood smear, PCR) including samples analyzed using the DiroChek®-ELISA and 237 dogs (39.3 %) by indirect methods (IFATs for detection of antibodies against Babesia spp., L. infantum, E. canis, and Anaplasma spp.). Furthermore, 311 (51.7 %) samples were seropositive for T. gondii and 110 (18.3 %) for N. caninum. Combining all IFAT results 390 (64.8 %) of all dogs were seropositive. Seven different vector-borne pathogens, namely Babesia vogeli, Hepatozoon canis, L. infantum, D. immitis, E. canis, A. phagocytophilum, A. platys, and M. haemocanis were identified by direct methods and in the DiroChek®-ELISA. Six (1.0 %) dogs were demonstrated to be positive for H. canis gamonts, three for microfilariae (0.5 %), and one for large Babesia (0.2 %) in the Giemsa-stained blood smears. The DiroChek®-ELISA was positive for D. immitis antigen in 13 dogs (2.2 %), and one of the seropositive dogs was also microfilaraemic in the Giemsa-stained blood smear. Serum samples were seropositive (IFAT) for Babesia spp. (6.6 %), L. infantum (5.1 %), E. canis (20.8 %), and Anaplasma spp. (24.1 %). Results from microscopical, PCR, and serological testing are summarized in Table 3.
Single infections as well as double and triple mixed infections of vector-borne agents were detected in 118 (19.6 %, 95 % CI 16.5–23.0), 30 (5.0 %, 95 % CI 3.4–7.0), and 3 (0.5 %, 95 % CI 0.12–1.6), respectively, of the dogs by direct methods including DiroChek®-ELISA (Table 4). By IFAT (Babesia spp., L. infantum, E. canis, Anaplasma spp.), 86 (14.3 %, 95 % CI 11.6–17.3) dogs were seropositive to two pathogens, 18 (3.0 %, 95 % CI 1.8–4.7) to three pathogens, and 4 (0.7 %, 95 % CI 0.2–1.7) animals to four pathogens (Table 5).
Multivariate logistic regression models for risk factors for the presence of or exposure to pathogens showed that increasing age of the dogs was the greatest risk factor (Table 6).
Discussion
The overall spectrum of pathogens detected in the present study is similar to the findings of previous reports on the occurrence of some important vector-transmitted pathogens in ticks and in Albanian dogs (Adhami and Murati 1977; Cicko and Cani 1999; Cicko et al. 1999; Christova et al. 2003; Dhamo et al. 2006; Lazri et al. 2008; Hamel et al. 2009; Rapti and Rehbein 2010; Xhaxhiu et al. 2011; Bizhga et al. 2013). To the authors’ knowledge, this study presents the first record of detection of E. canis, A. phagocytophilum, A. platys, and M. haemocanis by PCR and of antibodies against T. gondii and N. caninum in dogs from Albania.
Babesia spp.
Whole blood samples of two dogs harbored DNA of B. vogeli. In previous studies, babesias have been detected microscopically in blood smears from dogs in Albania and neighboring Greece (Diakou 2000; Dhamo et al. 2006). B. vogeli has been identified by PCR in dogs from Albania as well as in dogs from close-by Croatia and Slovenia for instance (Cacciò et al. 2002; Duh et al. 2004; Beck et al. 2009; Hamel et al. 2009). In contrast to the latter studies, neither B. canis nor B. vulpes sp. nov (syn. Theileria annae; Baneth et al. 2015) and B. gibsoni were detected, although these species are present on the Balkan Peninsula (Duh et al. 2004; Beck et al. 2009). The seroprevalence of anti-Babesia antibodies in 6.6 % of the client-owned dogs is within the range of approximately 2 to 10 % previously reported in dogs from Albania, Kosovo, and neighboring Greece (Jensen et al. 2003; Lazri et al. 2008; Hamel et al. 2009). Similar to a previous study from Spain, no risk factors for canine Babesia infection were identified (Solano-Gallego et al. 2006). In contrast, Adaszek et al. (2011) identified young age and originating in rural areas as risk factors in Poland. Similarly, use as hunting dog was identified as a risk factor in a study from Romania (Imre et al. 2013). However, the Babesia species in these studies was B. canis.
Leishmania infantum
Canine leishmaniosisis is a widespread infection in the Mediterranean region, and canids play a major role in the epidemiology of this disease as they act as primary reservoir hosts for human disease (Solano-Gallego et al. 2011). The prevalence rates of 5.1 % by serology and 4.7 % by PCR found in this study are lower than those determined in previous serology-based surveys from Albania (Cicko et al. 1998; Cicko and Cani 1999; Bizgha et al. 2013), neighboring northwestern Greece, and the former Yugoslav Republic of Macedonia (Diakou 2000; Papadopoulou et al. 2005; Athanasiou et al. 2012; Stefanovska et al. 2012) or in dogs imported into Germany from this region (Röhrig et al. 2011). However, serological test methods may underestimate the true number of infected animals as asymptomatic carriers often remain seronegative (Solano-Gallego et al. 2011). Considering risk factors, male dogs were described as being at higher risk of infection (Zaffaroni et al. 1999; Živičnjak et al. 2005; Miranda et al. 2008), which was also the case in the present study. Increasing age and being kept outdoors also have been identified as risks (Zaffaroni et al. 1999; Cardoso et al. 2004; Solano-Gallego et al. 2006; Cortes et al. 2012). This was not observed in the present study.
Hepatozoon canis
Two Hepatozoon spp. are recognized in dogs with H. canis being the only species present in dogs in Europe, while H. americanum only occurs in the Americas (Baneth et al. 2003). Gamonts of H. canis were present in six (1 %) Giemsa-stained blood smears. Hepatozoon canis has been identified in previous studies in Albania applying more sensitive methods with prevalences of approximately 17 % in Giemsa-stained buffy smears and 52 % by PCR (Lazri et al. 2008; Hamel et al. 2009). H. canis has also been reported in case reports or larger surveys in other countries in southeast Europe, e.g., Croatia (Vojta et al., 2009), Greece (Kontos and Koutinas 1990; Diakou 2000; Jensen et al. 2003), or Bulgaria (Ivanov and Kanakov 2003; Tsachev et al. 2008). No risk factor for H. canis was identified in this study, probably due to the low number of positive cases detected by blood-smear examination.
Filarioidea
Several filarial nematodes parasitize canids worldwide with D. immitis and Dirofilaria repens as the two most common and important species in the Mediterranean region (Simón et al. 2012). Approximately 2 % of the dogs tested positive for D. immitis antigen with the DiroChek®-ELISA. Although the Knott’s test was not performed, three microfilaremic dogs were detected in Giemsa-stained blood smears, indicating a high microfilaremia. Previous studies in Albania reported detection rates of 1.8 to 13.5 % for D. immitis and up to 11.5 % for D. repens applying various tests, i.e., detection post-mortem, Knott’s test followed by PCR in the case of D. repens, or serological methods for the detection of D. immitis antigen (Lazri et al. 2008; Hamel et al. 2009, Rapti and Rehbein 2010; Xhaxhiu et al. 2011). The prevalence rate of 2.2 % in dogs under veterinary care from Albania is at the lower range of 2.8 to 37 % reported in dogs from Greece, the former Yugoslav Republic of Macedonia, Serbia, and Bulgaria (Diakou 2000; Dimitrijević et al. 2007; Kirkova et al. 2008; Stefanovska et al. 2012; Morchón et al. 2012). Similar to results reported by Rapti and Rehbein (2010), increasing age was not identified as a risk factor in the present study. Nevertheless, results from other studies indicate that keeping dogs outdoors, male gender, and higher age are risk factors for D. immitis infection (Yildirim et al. 2007; Cardoso et al. 2012; Mircean et al. 2012).
Ehrlichia canis
Ehrlichia canis, the agent of canine monocytic ehrlichiosis, is a widespread tick-borne pathogen in the Mediterranean region and southeast Europe, associated with the presence of the vector tick Rhipicephalus sanguineus (Dantas-Torres 2010). This is the first record of E. canis by PCR in dogs from Albania. The seroprevalence of 20.8 % is within the range of prevalence rates of 17 and 50 % in semi-domesticated dogs from Albania (Lazri et al. 2008; Hamel et al. 2009). Generally, data on E. canis is limited for Southeast Europe, with few reports available from neighboring Bulgaria, Greece, the former Yugoslav Republic of Macedonia, and Serbia (Mylonakis et al. 2004a, b; Pavlovic et al. 2012; Tsachev et al. 2008; Stefanovska et al. 2012). Although increasing age was identified as risk factor in this study, age was not identified as a risk factor study from Spain (Solano-Gallego et al. 2006). In contrast, younger dogs were tested positive more often than older dogs in a multicenter study performed in Spain (Miró et al. 2013).
Anaplasma spp.
A. platys causes canine cyclic thrombocytopenia (Harvey et al. 1978). R. sanguineus has been incriminated as a vector, although not yet confirmed (Sanogo et al. 2003). A. platys-DNA was detected by PCR in 20 (3.3 %) blood samples. To the authors’ knowledge, this is the first report of A. platys from Albania. There is basically no information available on A. platys on the Balkan Peninsula with only one case report describing an infection in a dog imported into Germany from Croatia (Dyachenko et al. 2012) Another single case report is available from Romania (Andersson et al. 2013). Reports on A. platys are available from several countries in the Mediterranean region including Spain, Portugal, Italy, France, and Greece (Kontos and Koutinas 1990; Kontos et al. 1991; Sainz et al. 1999; Beaufils et al. 2002; Mylonakis et al. 2004b; Cardoso et al. 2010; Otranto et al. 2010).
A total of six (1.0 %) of the sampled dogs were positive for A. phagocytophilum-DNA by PCR. A. phagocytophilum is one of the most common tick-borne pathogens in Europe, associated with the occurrence of Ixodes ricinus ticks (Carrade et al. 2009). This study presents the first record of A. phagocytophilum DNA in dogs from Albania.
More than 24 % of the dogs were seropositive to Anaplasma spp. in IFAT. A previous small-scale study reported a seroprevalence rate of 40 % although none of the dogs were positive for A. phagocytophilum DNA by PCR (Hamel et al. 2009). Lower seroprevalence rates of approximately 8 % have been reported in surveys from the former Yugoslav Republic of Macedonia and Serbia (Pavlović et al. 2012a; Stefanovska et al. 2012). Serum/plasma from A. platys-infected dogs may cross-react to A. phagocytophilum antigen in IFAT as well as in SNAP 4dx tests (Beaufils et al. 2002; Santos et al. 2009; Gaunt et al. 2010). Thus, antibodies against Anaplasma spp. detected in this study and, possibly, in the previous study from Albania (Hamel et al. 2009), may also be attributed to exposure to A. platys, which is probably the predominant Anaplasma species in Albania when considering incidence rates detected by PCR in the current study. This is supported by the predominance of R. sanguineus ticks collected from these dogs (Shukullari et al. 2015). Considering the results of the Anaplasma-IFAT, increasing age was identified as a risk factor in the present study, while other authors identified male gender and being kept outdoors as risks (Solano-Gallego et al. 2006; Kybicova et al. 2009), or no risk factors were identified (Jensen et al. 2003).
Mycoplasma haemocanis
PCR-identified DNA of M. haemocanis in 8.8 % of the blood samples of the dogs. This represents the first report of this pathogen in dogs from Albania. A comparable prevalence has been reported in a study in privately owned dogs from North Macedonia in Greece, a region neighboring Albania in the East (Tennant et al. 2011). M. haemocanis infections have also been detected in Italy, Portugal, Spain, Hungary, and Romania with prevalence rates of more than 40 % reported in dogs from Portugal (Novacco et al. 2010; Hamel et al. 2012). Although dogs are usually asymptomatic carriers of M. haemocanis, sporadic cases with severe anemia have been described, primarily in immune-compromised or kenneled dogs (Kemming et al. 2004; Novacco et al. 2010; Willi et al. 2010).
Mixed infections
Mixed infections with as many as three vector-borne pathogens, based on PCR, blood smear evaluation, and detection of D. immitis antigen by ELISA, have been observed in this study, involving Babesia spp., H. canis, L. infantum, E. canis, Anaplasma spp., M. haemocanis, and/or D. immitis. Similar results have been reported in other studies of the Mediterranean region (Kontos and Koutinas 1990; Heyman et al. 2007; Mylonakis et al. 2004a, 2004b; Tsachev et al. 2008; Sasanelli et al. 2009; Cardoso et al. 2010, Otranto et al. 2010; Andersson et al. 2013; De Tommasi et al. 2013). Mixed infections are of considerable importance as they may alter clinical signs as well as disease progression (Sasanelli et al. 2009; De Tommasi et al. 2013).
Neospora caninum
About 18 % of the dogs in this study were seropositive to N. caninum. Dogs are definitive hosts of N. caninum and play an important role in the horizontal transmission of this protozoan parasite to other animals. It is considered the major parasitic cause for abortion in cattle with estimated losses in cattle production exceeding US$ 1200 million per year worldwide (Reichel et al. 2013). Clinical manifestation in dogs is rare, although transplacentally infected puppies may develop neuromuscular symptoms (cf. Dubey et al. 2007). Seropositivity indicates exposure to this pathogen but not necessarily infection. Identification of N. caninum oocysts by coproscopy is hampered by transient excretion and the occurrence of morphologically indistinguishable Hammondia heydorni oocysts. Therefore, usually, only a few dogs are identified shedding N. caninum-like oocysts, e.g., 4.9 % of 386 dogs surveyed in Romania and only 0.2 % of more than 24,000 dogs screened in Germany (Schares et al. 2005; Mitrea et al. 2012a). To the authors’ knowledge, there are no studies on N. caninum available from Albania. Seroprevalence rates range from 20 to over 32 % in dogs from Romania and from 5 to 60 % in livestock from Serbia, Croatia, Greece, Bulgaria, and Romania (Beck et al. 2010; Prelezov et al. 2008; Sotiraki et al. 2008; Gavrea et al. 2011, 2012; Mitrea et al. 2012a, b; Gavrilović et al. 2013). As described in other studies, increasing age was associated with infection due to an increasing chance of acquiring infection with age (Dubey et al. 2007; Mitrea et al. 2012b). This is also indicative for infection of the animals post gestation and, therefore, environmental or feed-borne infections are most likely route of transmission in animals in this study.
Toxoplasma gondii
Toxoplasmosis affects various warm-blooded species worldwide as intermediate hosts and felids act as definitive hosts (Dubey 2008). Approximately 52 % of the dogs were seropositive to T. gondii in this study. To date, there is only limited data on toxoplasmosis in Albania, and there is no data available in dogs. In neighboring Greece, studies identified antibodies to T. gondii in 21 to 34 % of canine blood samples (Chambouris et al. 1989; Diakou 2000). A recent publication reported almost 50 % of 496 pregnant Albanian women were positive for anti-T. gondii IgG, and 55 % out of 61 Albanian migrants were positive in Italy (Ventura et al. 2004; Maggi et al. 2009). Prevalence rates in humans in countries of the Balkan Peninsula and neighboring Greece range from 20 to 50 %, regardless of test-specific variations (cf. Bobić et al. 2011). Seroprevalence rates of 28.9 to 84.5 % have been reported in livestock (sheep, goat, cattle, and pigs) from the region (Klun et al. 2006; Prezelov et al. 2008). As confirmed in previous studies (Azevedo et al. 2005; Gennari et al. 2006; Dubey et al. 2007), lifestyle, and husbandry conditions, including access to T. gondii cysts, were also the most important factors affecting seropositivity in dogs in this study.
Conclusion
The results of this investigation revealed a wide range of vector-borne pathogens in blood samples from client-owned dogs in Tirana, Albania, including the first reports on A. platys, A. phagocytophilum, and M. haemocanis. The prevalence rates for vector-borne infections in dogs under veterinary care were lower than those in less well-cared dogs from this area. This was probably due to increased owner awareness indicated by better husbandry conditions and ectoparasiticidal treatment (Shukullari et al. Parasites and vector-borne diseases in client-owned dogs in Albania. Infestation with arthropod ectoparasites, in preperation), thus limiting vector exposure. Additionally, serological screening gave first evidence for N. caninum and T. gondii exposure in dogs from Albania.
References
Adaszek Ł, Martinez AC, Winiarczyk S (2011) The factors affecting the distribution of babesiosis in dogs in Poland. Vet Parasitol 181:160–165
Adhami J, Murati N (1977) Leishmanioza e qenit dhe rezervuari i leishmaniozës viscerale në vendin tonë. Bul Shkencave Mjekësore 17:69–74
Andersson M, Turcitu MA, Stefanache M, Tamba P, Barbuceanu F, Chitima L (2013) First evidence of Anaplasma platys and Hepatozoon canis co-infection in a dog from Romania—a case report. Ticks Tick Borne Dis 4:317–319
Athanasiou LV, Kontos VI, Saridomichelakis MN, Rallis TS, Diakou A (2012) A cross-sectional sero-epidemiological study of canine leishmaniasis in Greek mainland. Acta Trop 122:291–295
Azevedo SS, Batista CS, Vasconcellos SA, Aguiar DM, Ragozo AM, Rodrigues AA, Alves CJ, Gennari SM (2005) Seroepidemiology of Toxoplasma gondii and Neospora caninum in dogs from the state of Paraíba, Northeast region of Brazil. Res Vet Sci 79:51–56
Baneth G, Mathew JS, Shkap V, Macintire DK, Barta JR, Ewing SA (2003) Canine hepatozoonosis: two disease syndromes caused by separate Hepatozoon spp. Trends Parasitol 19:27–31
Baneth G, Florin-Christensen M, Cardoso L, Schnittger L (2015) Reclassification of Theileria annae as Babesia vulpes sp. nov. Parasites & Vectors 8:207.
Beaufils JP, Inokuma H, Martin-Granel J, Jumelle P, Barbault-Jumelle M, Brouqui P (2002) Anaplasma platys (Ehrlichia platys) infection in a dog in France: description of the case, and characterization of the agent. Rev Méd Vét 153:85–90
Beck R, Vojta L, Mrljak V, Marinculic A, Beck A, Zivicnjak T, Cacciò SM (2009) Diversity of Babesia and Theileria species in symptomatic and asymptomatic dogs in Croatia. Int J Parasitol 39:843–848
Beck R, Marinculić A, Mihaljević Ž, Benić M, Martinković F (2010) Seroprevalence and potential risk factors of Neospora caninum infection in dairy cattle in Croatia. Vet Arhiv 80:163–171
Bizhga B, Laci D, Dhamo G, Keci R, Belegu K, Bakiasi I, Turmalaj L (2013) Survey for canine leishmaniosis. J Anim Vet Adv 12:442–446
Bobić B, Nikolić A, Klun I, Djurković-Djaković O (2011) Kinetics of Toxoplasma infection in the Balkans. Wien Klin Wochenschr 123(Suppl 1):2–6
Cacciò SM, Antunović B, Moretti A, Mangili V, Marinculić A, Barić RR, Slemenda SB, Pieniazek NJ (2002) Molecular characterisation of Babesia canis canis and Babesia canis vogeli from naturally infected European dogs. Vet Parasitol 106:285–292
Cardoso L, Rodrigues M, Santos H, Schoone GJ, Carreta P, Varejão E, van Benthem B, Afonso MO, Alves-Pires C, Semião-Santos SJ, Rodrigues J, Schallig HD (2004) Sero-epidemiological study of canine Leishmania spp. infection in the municipality of Alijó (Alto Douro, Portugal). Vet Parasitol 121:21–32
Cardoso L, Tuna J, Vieira L, Yisaschar-Mekuzas Y, Baneth G (2010) Molecular detection of Anaplasma platys and Ehrlichia canis in dogs from the North of Portugal. Vet J 183:232–233
Cardoso L, Mendão C, Madeira de Carvalho L (2012) Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp. and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal - a national serological study. Parasites Vectors 5:62
Carrade DD, Foley JE, Borjesson DL, Sykes JE (2009) Canine granulocytic anaplasmosis: a review. J Vet Intern Med 23:1129–1141
Casati S, Sager H, Gern L, Piffaretti JC (2006) Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med 13:65–70
Chambouris R, Stünzner D, Sebek Z, Sixl W, Köck M (1989) Zur Toxoplasmose der Hunde in Griechenland. Geographica Medica 3:19–22
Christova I, Van De Pol J, Yazar S, Velo E, Schouls L (2003) Identification of Borrelia burgdorferi sensu lato, Anaplasma and Ehrlichia species, and spotted fever group Rickettsiae in ticks from Southeastern Europe. Eur J Clin Microbiol Infect Dis 22:535–542
Cicko Z, Cani E (1998) Te dhena paraprake mbi studimin “Seroprevalenca e Leishmaniozes kanine dhe identifimi i shkaktarit ne Shqiperi”. Rev Vet Instituti i Kërkimeve Veterinare Tiranë 1:112–115 [in Albanian]
Cicko Z, Zanaj S, Kusi I, Cani E (1999) Kërkime mbi leishmaniozën kanine në Shqipëri. Buletini i Shkencave Bujqësore 3:109–113 [in Albanian]
Cortes S, Vaz Y, Neves R, Maia C, Cardoso L, Campino L (2012) Risk factors for canine leishmaniasis in an endemic Mediterranean region. Vet Parasitol 189:189–196
Courtney JW, Kostelnik LM, Zeidner NS, Massung RF (2004) Multiplex Real-Time PCR for Detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 42:3164–3168
Dantas-Torres F (2010) Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasites Vectors 3:26
De Tommasi AS, Otranto D, Dantas-Torres F, Capelli G, Breitschwerdt EB, de Caprariis D (2013) Are vector-borne pathogen co-infections complicating the clinical presentation in dogs? Parasites Vectors 6:97
Development Core Team R (2010) R: A language and environment for statistical computing. Austria. R foundation for Statistical Computing, Vienna, Retrieved from http://www.R-project.org
Dhamo G, Rapti D, Bizhga B, Llazari A (2006) Kërkime hematologjike paraprake mbi babezionën e qene. Rev Shqiptare e Shkencave Bujqesore 5:114–119 [in Albanian]
Diakou A (2000) Epidemiological study of the dog parasitosis diagnosed by blood and serological examinations. Anima 8:9–15 [in Greek]
Dimitrijević S, Tasić A, Tasić S, Adamović V, Ilić T, Miladinović-Tasić N (2007) Filariosis in dogs in Serbia. In: Genchi C, Rinaldi L, Cringoli G (eds), Dirofilaria immitis and D. repens in dog and cat and human infections. Mappa Parassitologiche 8:201
Dubey JP (2008) The history of Toxoplasma gondii - the first 100 years. J Eukaryot Microbiol 55:467–675
Dubey JP, Alvarado-Esquivel C, Liesenfeld O, Herrera-Flores RG, Ramírez-Sánchez BE, González-Herrera A, Martínez-García SA, Bandini LA, Kwok OC (2007) Neospora caninum and Toxoplasma gondii antibodies in dogs from Durango City, Mexico. J Parasitol 93:1033–1035
Duh D, Tozon NŠ, Petrovec M, Strašek K, Avšić-Županc T (2004) Canine babesiosis in Slovenia: molecular evidence of Babesia canis canis and Babesia canis vogeli. Vet Res 35:363–368
Dyachenko V, Pantchev N, Balzer HJ, Meyersen A, Straubinger RK (2012) First case of Anaplasma platys infection in a dog from Croatia. Parasites Vectors 5:49
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. Parasites Vectors 3:33
Gavrea RR, Iovu A, Losson B, Cozma V (2011) Seroprevalence of Neospora caninum in dairy cattle from north-west and centre of Romania. Parasite 18:349–351
Gavrea R, Mircean V, Pastiu A, Cozma V (2012) Epidemiological survey of Neospora caninum infection in dogs from Romania. Vet Parasitol 188:382–385
Gavrilović P, Živuli A, Todorović I, Jovanović M, Parunović J (2013) Investigation of importance of Neospora caninum in aetiology of abortion in dairy cows in Serbia. Rev Méd Vét 164:100–104
Gennari SM, Franco WAC, Feitosa MM, Ikeda FA, Lima VMF, Amaku M (2006) Presence of anti-Neospora caninum and Toxoplasma gondii antibodies in dogs with visceral leishmaniosis from the region of Araçatuba, São Paulo, Brazil. Braz J Vet Res Anim Sci 43:613–619
Hamel D, Silaghi C, Knaus M, Visser M, Kusi I, Rapti D, Rehbein S, Pfister K (2009) Detection of Babesia canis subspecies and other arthropod-borne diseases in dogs from Tirana, Albania. Wien Klin Wochenschr 121(Suppl 3):42–45
Hamel D, Silaghi C, Lescai D, Pfister K (2012) Epidemiological aspects on vector-borne infections in stray and pet dogs from Romania and Hungary with focus on Babesia spp. Parasitol Res 110:1537–1545
Harvey JW, Simpson CF, Gaskin JM (1978) Cyclic thrombocytopenia induced by a Rickettsia-like agent in dogs. J Infect Dis 137:182–188
Heyman P, Duh D, Van Der Kuylen B, Cochez C, Van Esbroeck M, Vandenvelde C, Avšić-Županc T (2007) Molecular and serological evidence for Anaplasma platys and Babesia sp. infection in a dog, imported in Belgium, from Southern Spain. J Vet Med A Physiol Pathol Clin Med 54:276–279
Imre M, Farkas R, Ilie M, Imre K, Hotea I, Morariu S, Morar D, Dărăbuş G (2013) Seroprevalence of Babesia canis infection in clinically healthy dogs from western Romania. J Parasitol 99:161–163
Ionita M, Mitrea IL, Pfister K, Hamel D, Silaghi C (2013) Molecular evidence for bacterial and protozoan pathogens in hard ticks from Romania. Vet Parasitol 196:71–76
Ivanov A, Kanakov D (2003) First case of canine hepatozoonosis in Bulgaria. Bulg J Vet Med 6:43–46
Jensen J, Müller E, Daugschies A (2003) Für die Reisetiermedizin bedeutungsvolle arthropoden-übertragene Infektionen bei Hunden in Griechenland. Prakt Tierarzt 84:430–438 [in German]
Kemming GI, Messick JB, Enders G, Boros M, Lorenz B, Muenzing S, Kisch-Wedel H, Mueller W, Hahmann-Mueller A, Messmer K, Thein E (2004) Mycoplasma haemocanis infection—a kennel disease? Comp Med 54:404–409
Kirkova Z, Ivanov A, Georgiva D, Prelesov P (2008) An update on dirofilariosis in dogs and wild canines in Bulgaria. Sbornik dokladi ot nauchnata konferentsiya: Traditsii i s'vremenhost v'v veterinarnata meditsina, Sofia, Bulgaria, pp 247–252 [in Bulgarian]
Klun I, Djurković-Djaković O, Katić-Radivojević S, Nikolić A (2006) Cross-sectional survey on Toxoplasma gondii infection in cattle, sheep and pigs in Serbia: seroprevalence and risk factors. Vet Parasitol 135:121–131
Knaus M, Kusi I, Rapti D, Xhaxhiu D, Winter R, Visser M, Rehbein S (2011a) Endoparasites of cats from the Tirana area and the first report on Aelurostrongylus abstrusus (Railliet, 1898) in Albania. Wien Klin Wochenschr 123(Suppl 1):31–35
Knaus M, Rapti D, Kusi I, Shukulari E, Postoli R, Xhaxhiu D, Winter R, Visser M, Rehbein S (2011b) Survey of endo- and ectoparasites of cats from Tirana, Albania. In: Abstr 23rd. Int Conf World Assoc Adv Vet Parasitol (WAAVP), Buenos Aires, Argentina, p 232.
Knaus M, Postoli R, Rapti D, Xhaxhiu D, Visser M, Winter R, Dimitrova Z, Rehbein S (2012) Helminthen bei Katzen aus dem Großraum Tirana. In: Abstr Tag Dtsch Ges Vet Med (DVG). Fachgr Parasitologie und parasitäre Krankheiten, Hannover, Germany, p 22
Knaus M, Rapti D, Shukullari E, Kusi I, Postoli R, Xhaxhiu D, Silaghi C, Hamel D, Visser M, Winter R, Rehbein S (2014) Characterisation of ecto- and endoparasites in domestic cats from Tirana, Albania. Parasitol Res 113:3361–3371
Kontos V, Koutinas A (1990) Canine hepatozoonosis: a review of 11 naturally occurring cases. Bull Hell Vet Med Soc 41:73–81 [in Greek]
Kontos VI, Papadopoulos O, French TW (1991) Natural and experimental canine infections with a Greek strain of Ehrlichia platys. Vet Clin Pathol 20:101–105
Kybicova K, Schanilec P, Hulinska D, Uherkova L, Kurzova Z, Spejchalova S (2009) Detection of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in dogs in the Czech Republic. Vector Borne Zoonotic Dis 9:655–661
Lazri T, Duscher G, Edelhofer R, Bytyci B, Gjino P, Joachim A (2008) Infektion mit arthropodenübertragenen Parasiten bei Hunden im Kosovo und in Albanien unter besonderer Berücksichtigung der Leishmanieninfektionen. Wien Klin Wochenschr 120(Suppl 4):54–58
Maggi P, Volpe A, Carito V, Schinaia N, Bino S, Basho M, Dentico P (2009) Surveillance of toxoplasmosis in pregnant women in Albania. New Microbiol 32:89–92
Mancianti F, Falcone ML, Giannelli C, Poli A (1995) Comparison between an enzyme-linked immunosorbent assay using a detergent-soluble Leishmania infantum antigen and indirect immunofluorescence for the diagnosis of canine leishmaniosis. Vet Parasitol 59:13–21
Mary C, Faraut F, Lascombe L, Dumon H (2004) Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity. J Clin Microbiol 42:5249–5255
Miranda S, Roura X, Picado A, Ferrer L, Ramis A (2008) Characterization of sex, age, and breed for a population of canine leishmaniosis diseased dogs. Res Vet Sci 85:35–38
Mircean V, Dumitrache MO, Györke A, Pantchev N, Jodies R, Mihalca AD, Cozma V (2012) Seroprevalence and geographic distribution of Dirofilaria immitis and tick-borne infections (Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, and Ehrlichia canis) in dogs from Romania. Vector Borne Zoonotic Dis 12:595–604
Miró G, Montoya A, Roura X, Gálvez R, Sainz A (2013) Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study. Parasites Vectors 6:117
Mitrea IL, Enachescu V, Ionita M (2012a) Neospora caninum Infection in Dogs From Southern Romania: Coproparasitological Study and Serological Follow-Up. J Parasitol 99:365–367
Mitrea IL, Enachescu V, Radulescu R, Ionita M (2012b) Seroprevalence of Neospora caninum infection on dairy cattle in farms from southern Romania. J Parasitol 98:69–72
Morchón R, Carretón E, González-Miguel J, Mellado-Hernández I (2012) Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends. Front Physiol 3:196
Mylonakis ME, Koutinas AF, Baneth G, Polizopoulou Z, Fytianou A (2004a) Mixed Ehrlichia canis, Hepatozoon canis, and presumptive Anaplasma phagocytophilum infection in a dog. Vet Clin Pathol 33:249–251
Mylonakis ME, Koutinas AF, Breitschwerdt EB, Hegarty BC, Billinis CD, Leontides LS, Kontos VS (2004b) Chronic canine ehrlichiosis (Ehrlichia canis): a retrospective study of 19 natural cases. J Am Anim Hosp Assoc 40:174–184
Novacco M, Meli ML, Gentilini F, Marsilio F, Ceci C, Pennisi MG, Lombardo G, Lloret A, Santos L, Carrapiço T, Willi B, Wolf G, Lutz H, Hofmann-Lehmann R (2010) Prevalence and geographical distribution of canine hemotropic mycoplasma infections in Mediterranean countries and analysis of risk factors for infection. Vet Microbiol 142:276–284
Otranto D, Testini G, Dantas-Torres F, Latrofa MS, Diniz PP, de Caprariis D, Lia RP, Mencke N, Stanneck D, Capelli G, Breitschwerdt EB (2010) Diagnosis of canine vector-borne diseases in young dogs: a longitudinal study. J Clin Microbiol 48:3316–3324
Papadopoulou C, Kostoula A, Dimitriou D, Panagiou A, Bobojianni C, Antoniades G (2005) Human and canine leishmaniasis in asymptomatic and symptomatic population in Northwestern Greece. J Infect 50:53–60
Pavlovic I, Milojkovic N, Curcin L, Kovacevic M, Novak N, Ivanovic O (2012) Prevalence of ehrlichiosis, anaplasmosis and boreliosis. In: Program & Abstract Book EMOP XI, 25-29 July 2012, Cluj, Romania, p 330
Prezelov P, Koinarski V, Georgiva D (2008) Seroprevalence of Toxoplasma gondii infection in sheep and goats in the Stara Zagora region. Bulg J Vet Med 11:113–119
Rapti D, Rehbein S (2010) Seroprevalence of canine heartworm (Dirofilaria immitis) infection in Albania. Parasitol Res 107:481–485
Reichel MP, Alejandra Ayanegui-Alcérreca M, Gondim LF, Ellis JT (2013) What is the global economic impact of Neospora caninum in cattle - The billion dollar question. Int J Parasitol 43:133–142
Röhrig E, Hamel D, Pfister K (2011) Retrospective evaluation of laboratory data on canine vector-borne infections from the years 2004-2008. Berl Münch Tierärztl Wochenschr 124:411–418
Sainz A, Amusategui I, Tesouro MA (1999) Ehrlichia platys infection and disease in dogs in Spain. J Vet Diagn Invest 11:382–384
Sanogo YO, Davoust B, Inokuma H, Camicas JL, Parola P, Brouqui P (2003) First evidence of Anaplasma platys in Rhipicephalus sanguineus (Acari: Ixodida) collected from dogs in Africa. Onderstepoort J Vet Res 70:205–212
Santos AS, Alexandre N, Sousa R, Nuncio MS, Bacellar F, Dumler JS (2009) Serological and molecular survey of Anaplasma species infection in dogs with suspected tickborne disease in Portugal. Vet Rec 164:168–171
Sasanelli M, Paradies P, Lubas G, Otranto D, de Caprariis D (2009) Atypical clinical presentation of coinfection with Ehrlichia, Babesia and Hepatozoon species in a dog. Vet Rec 164:22–23
Schares G, Pantchev N, Barutzki D, Heydorn AO, Bauer C, Conraths FJ (2005) Oocysts of Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi in faeces collected from dogs in Germany. Int J Parasitol 35:1525–1537
Shukullari E, Rapti D, Visser M, Hamel D, Pfister K, Rehbein S (2015) Parasites and vector-borne diseases in client-owned dogs in Albania. Intestinal and pulmonary endoparasite infections. Parasitol Res. doi:10.1007/s00436-015-4704-8
Silaghi C, Kauffmann M, Passos LM, Pfister K, Zweygarth E (2011a) Isolation, propagation and preliminary characterisation of Anaplasma phagocytophilum from roe deer (Capreolus capreolus) in the tick cell line IDE8. Ticks Tick Borne Dis 2:204–208
Silaghi C, Liebisch G, Pfister K (2011b) Genetic variants of Anaplasma phagocytophilum from 14 equine granulocytic anaplasmosis cases. Parasites Vectors 4:161
Silaghi C, Knaus M, Rapti D, Shukullari E, Pfister K, Rehbein S (2012) Rickettsia felis and Bartonella spp. in fleas from cats in Albania. Vector Borne Zoonotic Dis 12:76–77
Silaghi C, Knaus M, Hamel D, Rapti D, Pfister K, Rehbein S (2013) Molecular detection of pathogens in ticks and fleas infesting dogs in Albania. In: Abstract 12th International Symposium on Ectoparasites in Pets, 25–29 July 2012. European Multicolloquium of Parasitology, Program & Abstract Book EMOP XI, Cluj-Napoca, Romania, p 35
Silaghi C, Knaus M, Rapti D, Kusi I, Shukullari E, Hamel D, Pfister K, Rehbein S (2014) Survey of Toxoplasma gondii and Neospora caninum, haemotropic mycoplasmas and other arthropod-borne pathogens in cats from Albania. Parasites Vectors 7:62
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
Solano-Gallego L, Llull J, Osso M, Hegarty B, Breitschwerdt E (2006) A serological study of exposure to arthropod-borne pathogens in dogs from northeastern Spain. Vet Res 37:231–244
Solano-Gallego L, Miró G, Koutinas A, Cardoso L, Pennisi MG, Ferrer L, Bourdeau P, Oliva G, Baneth G, The LeishVet Group (2011) LeishVet guidelines for the practical management of canine leishmaniosis. Parasites Vectors 4:86
Sommer MF, Beck R, Ionita M, Stefanovska J, Vasić A, Zdravković N, Hamel D, Rehbein S, Knaus M, Mitrea IL, Shukullari E, Kirkova Z, Rapti D, Capári B, Silaghi C (2015) Multilocus sequence typing of canine Giardia duodenalis from South Eastern European countries. Parasitol Res 114:2165–2174
Sotiraki S, Brozos C, Samartzi F, Schares G, Kiossis E, Conraths FJ (2008) Neospora caninum infection in Greek dairy cattle herds detected by two antibody assays in individual milk samples. Vet Parasitol 152:79–84
Stefanovska J, Farkas R, Kochevski Z (2012) Pevalence of some vector borne diseases in dogs in R. Macedonia. In: Program & Abstract Book EMOP XI, 25-29 July 2012, Cluj, Romania: pp 328–329.
Teglas M, Matern E, Lein S, Foley P, Mahan SM, Foley J (2005) Ticks and tick-borne disease in Guatemalan cattle and horses. Vet Parasitol 131:119–127
Tennant KV, Barker EN, Polizopoulou Z, Helps CR, Tasker S (2011) Real-time quantitative polymerase chain reaction detection of haemoplasmas in healthy and unhealthy dogs from Central Macedonia, Greece. J Small Anim Pract 52:645–649
Tsachev I, Ivanov A, Dinev I, Simeonova G, Kanakov D (2008) Clinical Ehrlichia canis and Hepatozoon canis co-infection in a dog in Bulgaria. Rev Méd Vét 159:68–73
Ventura MT, Munno G, Giannoccaro F, Accettura F, Chironna M, Lama R, Hoxha M, Panetta V, Ferrigno L, Rosmini F, Matricardi PM, Barbuti S, Priftanji A, Bonini S, Tursi A (2004) Allergy, asthma and markers of infections among Albanian migrants to Southern Italy. Allergy 59:632–636
Vojta L, Mrljak V, Curković S, Živičnjak T, Marinculić A, Beck R (2009) Molecular epizootiology of canine hepatozoonosis in Croatia. Int J Parasitol 39:1129–1136
Watanabe M, Hisasue M, Hashizaki K, Furuichi M, Ogata M, Hisamatsu S, Ogi E, Hasegawa M, Tsuchiya R, Yamada T (2003) Molecular detection and characterization of Haemobartonella felis in domestic cats in Japan employing sequence-specific polymerase chain reaction (SS-PCR). J Vet Med Sci 65:1111–1114
Willi B, Novacco M, Meli M, Wolf-Jäckel G, Boretti F, Wengi N, Lutz H, Hofmann-Lehmann R (2010) Haemotropic mycoplasmas of cats and dogs: transmission, diagnosis, prevalence and importance in Europe. Schweiz Arch Tierheilkd 152:237–244
Xhaxhiu D, Kusi I, Rapti D, Visser M, Knaus M, Lindner T, Rehbein S (2009) Ectoparasites of dogs and cats in Albania. Parasitol Res 105:1577–1587
Xhaxhiu D, Kusi I, Rapti D, Kondi E, Postoli R, Rinaldi L, Dimitrova ZM, Visser M, Knaus M, Rehbein S (2011) Principal intestinal parasites of dogs in Tirana, Albania. Parasitol Res 108:341–353
Yildirim A, Ica A, Atalay O, Duzlu O, Inci A (2007) Prevalence and epidemiological aspects of Dirofilaria immitis in dogs from Kayseri Province, Turkey. Res Vet Sci 82:358–363
Zaffaroni E, Rubaudo L, Lanfranchi P, Mignone W (1999) Epidemiological patterns of canine leishmaniasis in Western Liguria (Italy). Vet Parasitol 81:11–19
Živičnjak T, Martinković F, Marinculić A, Mrljak V, Kučer N, Matijatko V, Mihaljević Z, Barić-Rafaj R (2005) A seroepidemiologic survey of canine visceral leishmaniosis among apparently healthy dogs in Croatia. Vet Parasitol 131:35–43
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The authors gratefully acknowledge the technical assistance of the laboratory staff of the Diagnostic Unit of the Institute of Comparative Tropical Medicine and Parasitology. The authors also acknowledge the support of Sanisys SA, Switzerland, for statistical analysis.
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Hamel, D., Shukullari, E., Rapti, D. et al. Parasites and vector-borne pathogens in client-owned dogs in Albania. Blood pathogens and seroprevalences of parasitic and other infectious agents. Parasitol Res 115, 489–499 (2016). https://doi.org/10.1007/s00436-015-4765-8
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DOI: https://doi.org/10.1007/s00436-015-4765-8