Infection, Genetics and Evolution 23 (2014) 182–188
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Review
Why are there several species of Borrelia burgdorferi sensu lato detected in dogs and humans? Bogumiła Skotarczak ⇑ Department of Genetics, Faculty of Biology, University of Szczecin, Felczaka 3c, 71-412 Szczecin, Poland
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Article history: Received 25 October 2013 Received in revised form 21 January 2014 Accepted 11 February 2014 Available online 5 March 2014 Keywords: Canine borreliosis Genospecies of B. burgdorferi s.l. Borreliacidal ability of serum Co-infections
a b s t r a c t Borrelia burgdorferi sensu lato is a group of spirochete bacteria species some of which cause borreliosis in humans and dogs. Humans and dogs are susceptible to illness from many of the same tick-borne pathogens, including B. burgdorferi s.l. (Bbsl). Little is known about the pathogenic role of the species of Bbsl in canines. The molecular methods which detect and amplify the DNA of borreliae and allow differentiating borreliae species or strains have not been used in canine diagnostics yet. Until now, it has been believed that in European dogs, like in humans, at least three pathogenic species occur but the most frequently described symptoms may be associated with the infection caused by B. burgdorferi sensu stricto species. A dog as well as a human is a host for many species of Bbsl, because borreliacidal ability of serum of dogs and humans is evident only in certain genospecies of Bbsl. Therefore both a dog and a human harbor more species than in case of some wild animal species which create older phylogenetic Bbsl species–host systems and these animals may act even as a non-competent reservoir host. Apart from many genospecies of Bbsl, a dog harbors other tick-borne agents and dual or triple infections may occur. Ó 2014 Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
Short history of the etiological factor of Lyme disease and epidemiology . Pathogenic role of the species of B. burgdorferi s.l. in canines. . . . . . . . . . . Why do human and dog harbor several species of B. burgdorferi s.l.? . . . . Co-infections with the tick-borne pathogens in dogs . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Declaration of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Borrelia burgdorferi sensu lato is a group of spirochete bacteria causing borreliosis (also called Lyme disease or Lyme borreliosis), a multihost and multipathogen disease, a zoonosis transmitted by ticks. In Europe, these bacteria are transmitted to humans and to reservoir hosts by hard ticks – Ixodes ricinus species (Hermanowska-Szpakowicz et al., 2004; Piesman and Gern, 2004; Wodecka et al., 2010). I. ricinus is a parasitic arthropod with three life stages, i.e., larva, nymph and adult (male or female). Excluding the male, in each stage the tick takes one blood meal on a vertebrate host. I. ricinus feeds on many different vertebrate species ⇑ Tel.: +48 0914441521; fax: +48 0914441580. E-mail address: [email protected] http://dx.doi.org/10.1016/j.meegid.2014.02.014 1567-1348/Ó 2014 Elsevier B.V. All rights reserved.
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which can function as a reservoir host of different B. burgdorferi s.l. genospecies. More than 100 vertebrate species have been identified which can act as reservoir hosts for Lyme borreliosis spirochetes including rodents (vole, wood mouse, dormouse, squirrel, chipmunk, wood rat, rat), insectivores (shrew, hedgehog), raccoon and several bird species (Masuzawa, 2004; Michalik et al., 2005; Piesman and Gern, 2004). For other species such as foxes or badgers only limited information is available and it is uncertain whether they constitute reservoir hosts (Gern and Sell, 2009; Matuschka et al., 2000; Miyamoto and Masuzawa, 2002), although domestic dog has been reported to be reservoir competent (Mather et al., 1994; Leschnik et al., 2010; Straubinger, 2000).
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Currently, on the basis of numerous genetic and phylogenetic analyses, at least 19 subdivisions called genospecies or species have been described in the B. burgdorferi sensu lato complex (Mannelli et al., 2012). Several of these have been detected in Europe (B. burgdorferi sensu stricto (s.s.), Borrelia afzelii, Borrelia garinii, Borrelia valaisiana, Borrelia lusitaniae, Borrelia bavariensis (previously Borrelia garinii OspA serotype 4), Borrelia finlandensis and Borrelia spielmanii (Casjens et al., 2011; HermanowskaSzpakowicz et al., 2004; Kondrusik et al., 2007; Margos et al., 2009; Wang et al., 1997; Wodecka and Skotarczak, 2005). Borrelia andersonii and B. burgdorferi s.s. are typical for North America and five for Asia Borrelia japonica, Borrelia turdi, Borrelia tanukii, Borrelia sinica and Borrelia yangete) (Chu et al., 2008). In ticks I. ricinus, B. afzelii, B. garinii and B. burgdorferi s.s. are the most common European circulating genospecies and they are thought to be the etiological agents of Lyme disease, pathogenic for human and dog (Hovius et al., 1999, 2000; Marconi and Garon, 1992; Rauter and Hartung, 2005; Skotarczak and Wodecka, 2003, 2005; Skotarczak et al., 2005; Wilhelmsson et al., 2010; Wodecka et al., 2009). They are characterized by a different organotropic and pathogenic potential, antigen structure and geographic distribution. Several genospecies may be present simultaneously in a vector (Rauter and Hartung, 2005; Skotarczak et al., 2003; Wodecka et al., 2010). B. burgdorferi s.s. is the only established etiologic agent of Lyme borreliosis in dog and human in North America, where Lyme borreliosis differs in dog and human in terms of clinical outcome following the infection, diagnostic approach, prevention strategy and treatment recommendation (Little et al., 2010). Different genospecies are often associated with other clinical manifestations of the disease: B. burgdorferi s.s. is most often associated with arthritis and neuroborreliosis, B. garinii with neuroborreliosis and B. afzelii with acrodermatitis chronica atrophicans. Although, some species, such as B. lusitaniae, are associated with human diseases only occasionally (Collares-Pereira et al., 2004), and B. bavariensis is probably linked to neuroborreliosis (Ornstein et al., 2001). For other species of Bbsl, such as Borrelia valaisiana, the status is unclear because they have a high regional prevalence in Europe, but have not often been isolated from human (Diza et al., 2004) and the recently described B. finlandensis has uncertain pathogenicity (Casjens et al., 2011). It has been suggested that not all strains/genotypes within a species cause disseminated disease in humans (Wormser et al., 2008). Also, the role of B. spielmanii as a causative agent of LB was confirmed by reported cases of patients with erythema migrans in the Netherlands, Germany, Hungary and Slovenia (Maraspin et al., 2006). Much less is known about Lyme disease in these animals than in a human. The most common symptom of Lyme disease in dog is migratory arthritis without divergent radiographic findings, but there is no erythema migrans characteristic for human Lyme disease. Other but less common symptoms reported in dog are carditis, glomerulonephritis, neuritis and renal lesions. Various studies aimed at showing a relation between renal disease and B. burgdorferi infection. ‘‘Lyme nephritis’’ was investigated in dogs with distinctive renal lesions and typical clinical signs, in which antibodies against B. burgdorferi were found (Gerber et al., 2009). However, a causative role of B. burgdorferi in the development of renal disease was not confirmed, and renal lesions were not found in experimentally infected dogs (Summers et al., 2005). Because of the difficulties in finding sufficient indicative clinical signs, additional information about environmental life of dogs is of importance in the clinical diagnosis of canine Lyme borreliosis (Krupka and Straubinger, 2010). Unlike in the case of human infection, however, a typical Lyme disease in dogs is not easy to document, mainly because many of the animals exposed to B. burgdorferi do not develop clinical
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abnormalities (Levy et al., 1993; Leschnik et al., 2013; Littman et al., 2006).
1. Short history of the etiological factor of Lyme disease and epidemiology Symptoms of Lyme disease have been known in medicine for over 100 years, but due to their multifaceted nature, they were at first considered as several separate diseases. The first symptom was described in 1853, when Buchwald reported it as ‘‘idiopathic skin atrophy’’ (Gustafson, 1994). Attention heightened from 1975 after Steere et al. (1983) identified the disease in children and adolescents in Old Lyme, Connecticut (USA). A strange lesion of joint inflammation was observed regularly in this area and was described as Lyme arthritis. The etiology of this condition was at first unknown, but ticks were suspected and intensively studied because of the seasonal nature of infections, coinciding with times of mass tick emergence, and also due to patients complaining of tick bites (Rand et al., 1996; Steere et al., 1983). In 1981, Willy Burgdorfer from Hamilton University isolated spirochete-like bacteria from a culture from gut contents of the tick Ixodes scapularis (Ixodes dammini) collected on Shelter Island N.Y. (Schwan et al., 1993). This isolate was fixed with the symbol B 31 and became the prototype sample of the species of spirochetes called B. burgdorferi by W. Burgdorfer in 1982 (Burgdofer et al., 1982). Less than a decade after reports of a new infectious disease from Lyme, similar symptoms were described in a domestic dog (Lissman et al., 1984). Many studies show that the frequency of B. burgdorferi infection in human and dog is correlated with the density of ticks’ population and the geographic location of their biotope; these indicate the degree of risk for a human and a dog (Guerra et al., 2001). Dog inhabiting tick infested areas in which instances of human Lyme borreliosis are also found produce B. burgdorferi s.l. antibodies (Magnarelli et al., 1995, 2000; Skotarczak et al., 2003; Stefancikova et al., 1998; Straubinger et al., 1997). The results of numerous studies confirm that from an epidemiological point of view, dogs should be considered as risk animals because they accompany people in high risk areas. Dogs provide a good indication of a likely exposure of their owners to infected ticks, since they largely share the same environment and visit the same outdoor areas (Smith et al., 2012). According to Stefancikova et al. (1998), even removing ticks or grooming infested animals constitute an exposure risk. However, opinions differ. Goossens et al. (2001) did not observe any correlation between frequency of antibodies in a hunting dog and its owner’s serum. They concluded that direct transfer of ticks between hunters and hunting dogs was insignificant and that dog did not constitute a borreliosis hazard. People working or vacationing in tick infested areas have higher frequency of B. burgdorferi antibody occurrence than control groups. According to the authors, if the results of serological studies on people with high outdoor activity are taken into account, then a higher frequency of antibodies against B. burgdorferi is expected in hunting dogs compared with control animals. Several authors suggest that the epidemiological profile of borreliosis in dogs is an indicator of the potential risk to people in the area (Falco et al., 1993; Lindenmayer et al., 1991; Merino et al., 2000). Moreover, according to the results of a new study carried out by the Center for Disease Control and Prevention (CDC), the more dogs with Lyme disease, the higher the frequency of this tick-borne illness in humans in the USA. On the basis of data from ‘‘prevalence maps’’ presented by the Companion Animal Parasite Council (www.PetsAndParasites.org), it was established that the humans in areas with a higher than average number of dogs with borreliosis are at a greater risk of contracting the illness. The
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findings of the study emphasize the importance of alerting pet owners and their families to the risk of tick-borne disease as well as the need of its prevention. The Lyme disease research and prevalence maps are crucial in educating human and veterinary health care professionals as well as pet owners as to the importance of about this increasing problem.
B. afzelii comes from Switzerland (Speck et al., 2001). But, subsequent work by the same team (Speck et al., 2007) reported only an incidental positive PCR result for the presence of DNA of B. bugdorferi s.l. in the blood of naturally infected dogs which questions the usefulness of this technique. Leschnik et al. (2013) arrived at the same conclusion. Thus, in a dog as in a human, there are at least the same three species of pathogenic B. burgdorferi s.l.
2. Pathogenic role of the species of B. burgdorferi s.l. in canines In Europe, the three most prevalent species of the B. burgdorferi s.l. are characterized by a different organotropic and pathogenic potential and, as mentioned above, different species are often associated with different clinical manifestations of the diseases in humans. So far, very little is known of the pathogenic role of the species of B. burgdorferi s.l. in canines, because molecular methods are applied for differentiation of Borrelia species or strains, and they are not commonly used in the veterinary diagnostics. For many years combined infections of the most prevalent genospecies have been thought to occur in European canines and in naturally exposed dogs. B. burgdorferi s.s. and B. garinii co-infections are the most frequent (Hovius et al., 1999). A study of B. burgdorferi s.l DNA isolated from canine blood from north western Poland revealed the dominance of B. burgdorferi s.s. (Skotarczak et al., 2005; Wodecka et al., 2009), as in other studies of human and I. ricinus infection (Wodecka and Skotarczak, 2005). The prevalence of Borrelia species infection was determined using nested polymerase chain reaction (nested PCR) and restriction fragment length polymorphism (RFLP) analysis with enzyme Fsp4H I in blood of dogs naturally infested by ticks in endemic region of Poland (Skotarczak and Wodecka, 2005). Blood samples were collected from 98 dogs of various breeds, brought to the Veterinary Clinic in Szczecin (north-western Poland) for various reasons. The PCR-RFLP revealed a single species, B. burgdorferi s.s. in all PCR – positive samples obtained through amplification of the fla gene. Digestion of PCR products gave one band pattern only consistent with the pattern obtained with sequence analysis of the fla gene from a reference isolate of B. burgdorferi s.s. GeHo (X15660) obtained from the GenBank. In all dogs infected by B. burgdorferi s.s. the limb joints were most commonly affected, resulting in lameness, carpal and tarsal arthralgia, joint swelling. In the latest study of dogs from the same locality (Wodecka et al., 2009), which were brought to the Veterinary Clinic, the veterinary surgeons detected clinical form of borreliosis. Blood samples collected from 18 dogs, with clinically detected borreliosis, were used to acquire DNA for PCR. Positive results of PCR, with primers complementary to the fla gene, indicating the presence of DNA of one species only – B. burgdorferi s.s. were found in the blood of 7 dogs. Each of these dogs most commonly manifested symptoms of arthritic pain and/ or arthritic swelling, fever, anorexia and/or lymphadenopathy. In the USA well documented infections of dogs with combination of polyarthritis, fever, anorexia and/or lymphadenopathy were described (Littman et al., 2006). Since in European descriptions of clinical symptoms of canine Lyme disease (but without genospecies identification) the most common symptoms match those above, the conclusion may be that this species (B. burgdorferi s.s.) is dominant in dogs in Europe. However, in other regions of Poland and other parts of Europe, there are cases of dogs infected with B. garinii and B. afzelii, yet these are single cases only. In the Czech Republic, DNA of B. garinii was detected in blood sample from one dog (Kybicova et al., 2009), also infection with B. garinii was detected (with PCR) in one dog with meningoencephalitis (Kybicova et al., 2009; Schanilec et al., 2010). In central Poland 7 cases with B. afzelii were described, but without any information concerning the clinical symptoms in these dogs (Zygner et al., 2009). A documented report of a naturally exposed dog infected with
3. Why do human and dog harbor several species of B. burgdorferi s.l.? In natural circumstances, the clinical form of borreliosis is found only in species from outside the wood biotope, i.e., human, dog, cat, horse and cow, however most often, it affects a dog and a humans (Appel et al., 1993; Magnarelli et al., 2001; May et al., 1994; Muller et al., 2002; Parker and White, 1992; Steere, 1989). Lack of clinical infection symptoms in forest animals implies that a balanced state in this parasite–host system has been reached as a result of longterm relationships (Skotarczak, 2002). Currently, many factors that decide the sensitivity or resistance of host to Borrelia are already known, but the crucial factor that could explain the selective transmission and host association of B. burgdorferi s.l. is the lytic component in serum (Kraiczy and Stevenson, 2013; Kurtenbach et al., 2002). It was identified as the alternative pathway of complement (Breitner-Ruddock et al., 1997; Kurtenbach et al., 1998a; Van Dam et al., 1997). Analyses of resistance or sensitivity patterns to complement are extended to many B. burgdorferi s.l. strains and different vertebrate species, including avian, reptilian, rodent and ruminant hosts (Kurtenbach et al., 1998a; Kuo et al., 2000; Lane and Quistad, 1998; Nelson et al., 2000) which result in an assumption of a connection between B. burgdorferi s.l. species and some vertebrate hosts. In accordance with this theory, B. afzelii and B. bissettii are resistant to this component occurring in rodents, which makes these animals a competent reservoir for both species. Studies of Kurtenbach et al. (2002) revealed that B. garinii and B. valaisiana are also resistant to the above mentioned component of serum present in birds. B. burgdorferi s.s. also shows indirect sensitivity to this component, in both mammals and birds, so it is not detected in both of these vertebrates. B. lusitaniae is associated with lizard (Kurtenbach et al., 1998b; Majlathova et al., 2006; Richter and Matuschka, 2006). B. spielmanii appears to be associated with dormouse and hedgehog. So far, it has been found that big forest mammals (i.e., roe deer, red deer and wild boar) despite being basic hosts for the adult I. ricinus are not a reservoir for the B. burgdorferi s.l. species (Jaenson and Talleklint, 1992; Kurtenbach et al., 2002; Skotarczak et al., 2008), which means they have borreliacidal ability against borrelial infection. Thus, borrelial genospecies associated with a specific host are usually resistant to the abovementioned component of serum of the given host. However, the associations between genospecies and hosts are not absolute and may vary geographically (Gern, 2008). There is evidence that ticks and reservoir hosts can be co-infected with multiple Borrelia spp. Although many studies show that different species of animals which have achieved the status of a reservoir for B. burgdorferi are a harbor only for one or a few more species of B. burgdorferi. For example, the results of a study by Skuballa et al. (2007) indicate that hedgehogs may be a harbor for three B. burgdorferi genospecies, while a few passerine bird species are associated with B. garinii only (Dubska et al., 2009), in grey squirrel (Sciurus carolinensis Gmelin) and pheasant (Phasianus colchicus Linnaeus) two species B. afzelii and B. garinii were found (Pawelczyk et al., 2004) or only one (Michalik et al., 2005). In other studies, the wood mouse (Apodemus sylvaticus) and bank vole (Myodes glareolus, formerly known as Clethrionomys glareolus) were described as specific hosts for B. afzelii only
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(Buffet et al., 2012), one species only, B. burgdorferi s.s. was found in other rodent hosts, such as the red squirrel (Sciurus vulgaris) and brown rat (Rattus norvegicus) (Humair et al., 1995; Margos et al., 2011; Marsot et al., 2011) or in two rodent species (Myodes glareolus, Apodemus flavicollis) B. garinii only (Craine et al., 1997). Generally, in wild animals usually one, two or three species of B. burgdorferi s.l. occur and more species are resistant to serum component of humans and dogs. In Europe, despite the three species considered as the major human pathogens, such species as B. lusitaniae (Collares-Pereira et al., 2004), B. bavariensis, B. spielmanii or B. valaisiana (Diza et al., 2004) were isolated from humans. In dogs, as mentioned above, there are at least three pathogenic genospecies or even more (Bhide et al., 2005), because humans and dogs are susceptible to illnesses caused by many of the same tick-borne pathogens, including B. burgdorferi s.l. Thus, one can hypothesize that unlike the wild animals, human and domestic animals like a dog, as they are occasionally infected, have not acquired borreliacidal ability against most of the Borrelia genospecies yet. However, this hypothesis is only partly confirmed by the studies of Bhide et al. (2005), in which different Borrelia species and serotypes were tested for their sensitivity to serum complement from various animals and humans as potential hosts reservoir. A percentage of sensitivity of different Borrelia species to dog serum indicates that this animal is a reservoir competent host for all examined Borrelia species (except B. lusitanie), particularly for B. afzelii isolates, B. burgdorferi s.s., B. andersonii-21123 and B. bissettii-DN127. Apart from the dog this host may be its direct ancestor – the wolf, in case of the cat – the lynx. Cats and humans can also be infected by different species of B. burgdorferi s.l. Complement-mediated killing of Borrelia in the European bison, red fallow and roe deer, as may be expected, is extensive and it is evident that these animals act as a non-competent reservoir host, which also pertains to breeding animals like cattle. Serum of other breeding animals, like sheep showed intermediate Borrelia species-dependent killing, similarly to wild animals, like the mouflon. Thus, not only the frequency of contact with a tick and current lifestyle of animal-hosts determine the boreliacidal ability but also the duration of the phylogenetic system of the bacteria–host. So, the oldest borrelia–host systems concern cattle and some species from subfamily Capreolinae and Cervinae, whereas younger ones involve rodents or some species of birds and various species from Felinae and Canidae family as well as humans. The results of Marsot et al. (2011) confirm this hypothesis. In their investigation, they examined whether the Siberian chipmunk (Tamias sibiricus barberi), species introduced in France, was potentially a new reservoir host for species of B. burgdorferi s.l. causing Lyme disease and whether chipmunks were infected by all of the B. burgdorferi s.l. genospecies considered to be associated with European rodents. In addition, the prevalence and diversity of B. burgdorferi s.l. in chipmunks was compared with a native reservoir rodent, the bank vole (Myodes glareolus). Chipmunks were infected by the three Borrelia genospecies that infect rodents (B. burgdorferi sensu stricto, B. afzelii, and B. garinii), whereas voles by B. afzelii only. Because chipmunks were twice more frequently infected than voles, the authors concluded that this may be explained by either a higher exposure of chipmunks (they harbour more ticks), or by their higher tolerance of other B. burgdorferi s.l. genospecies than bank voles. Why do these chipmunks have a higher tolerance for the B. burgdorferi s.l. genospecies? This species of a squirrel living as a native species in Korea has never been infected there by the European genospecies because they are not present in this country (Kurtenbach et al., 2006). A few studies of Siberian chipmunks conducted in China, their native area, reveal that they harbour some native B. burgdorferi s.l. genospecies like Eurasian-type B. garinii 20047, and Asian-type B. garinii NT29 (Chu et al., 2006).
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4. Co-infections with the tick-borne pathogens in dogs Ticks may also transmit other pathogens which complicate the diagnosis. Reports of co-infection with multiple tick-borne organisms in humans and dogs were published (Kordick et al., 1999; Krause et al., 2002; Hermanowska-Szpakowicz et al., 2004; Welc-Fale˛ciak et al., 2009; Rymaszewska and Adamska, 2011; Barth et al., 2012). Among those pathogens there are Anaplasma (Ehrlichia) phagocytophilum bacteria and Babesia protozoa, which, as our studies indicate, coexist in north-western Polish populations of I. ricinus (Skotarczak et al., 2002). The aim of the previous studies in 2004 (Skotarczak et al., 2004) was to determine if dogs infested with ticks were a reservoir for E. phagocytophilum and Babesia spp. The purpose of the recent study (Rymaszewska and Adamska, 2011) from north-western Poland was to examine whether co-infection with two or more vector-borne pathogens could appear in three groups of dogs. The first group consisted of dogs with suspected borreliosis, the second of dogs considered healthy and third group of dogs with detected babesiosis. For the detection of DNA of A. phagocytophilum, Rickettsia spp. and Bartonella spp. in the blood of these dogs, polymerase chain reactions were applied. In dogs from the first group (242 individuals), the DNA of both A. phagocytophilum and Bartonella sp. was identified and in less than 1% of them, DNA of A. phagocytophilum or Bartonella sp. with B. burgdorferi s.l. (the presence of antibodies against and/or DNA B. burgdorferi s.l.) as co-infection was revealed. In the second group, only the DNA of A. phagocytophilum was detected, however in the third group no pathogenic agents transmitted by ticks were found. In other studies from Central Poland (Welc-Faleciak et al., 2009) on sled dogs, the occurrence of four vector-borne infections (Babesia canis, Bartonella sp., Anaplasma/Ehrlichia and B. burgdorferi) was assessed with PCR and nested PCR methods. Among 82 dogs, the DNA of B. canis was detected in three dogs undergoing treatment for babesiosis, but the DNAs of other tick-borne pathogens were also found in 22 out of 79 apparently healthy dogs, including 20 cases of B. canis infection, one case of B. burgdorferi s.l. and one case of A. phagocytophilum. No DNA of Bartonella spp. and Ehrlichia canis was detected in any of the examined samples. Sequencing of Babesia fragment of 18S rDNA gene amplified from acute and asymptomatic cases, revealed that it was identical with the B. canis sequence, originally obtained from Dermacentor reticulatus ticks in Poland. Other studies from Central Poland (Zygner et al., 2009) of blood samples from dogs were carried out to investigate the presence of DNA of B. burgdorferi s.l., Anaplasma phagocytophilum, Babesia canis and Hepatozoon canis. Borrelia DNA was detected in seven of 408 dogs (sequencing amplicons indicated only the B. afzelii genospecies), A phagocytophilum DNA was found in two, and B canis DNA was found in 48 (11.8%). The antibodies against tick-borne pathogens like A. phagocytophilum, B. burgdorferi s.l. and E. canis in French dogs were detected by Pantchev et al. (2009). It is established that Anaplasma platys, the contributing causative agent of infectious canine cyclic thrombocytopenia is endemic in countries of the Mediterranean basin. A. platys was detected in a dog from Croatia which was also co-infected by Babesia vogeli (Dyachenko et al., 2012). Thrombocytopenia, anemia and elevated values of C-reactive protein were the laboratory test abnormalities observed in this case. Other studies from Italy (de Caprariis et al., 2011), indicate a significant association between tick infestation of dogs and A. platys or B. vogeli, as single infections, and A. platys and B. vogeli or A. platys and Bartonella spp. as co-infections. The authors underline that this study shows the clinical difficulties associated with assigning a specific clinical sign or haematological abnormality to a particular canine vector-borne disease. The DNAs of E. canis, A. platys, B. vogeli, Hepatozoon canis, and Bartonella sp.
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Review
Why are there several species of Borrelia burgdorferi sensu lato detected in dogs and humans? Bogumiła Skotarczak ⇑ Department of Genetics, Faculty of Biology, University of Szczecin, Felczaka 3c, 71-412 Szczecin, Poland
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Article history: Received 25 October 2013 Received in revised form 21 January 2014 Accepted 11 February 2014 Available online 5 March 2014 Keywords: Canine borreliosis Genospecies of B. burgdorferi s.l. Borreliacidal ability of serum Co-infections
a b s t r a c t Borrelia burgdorferi sensu lato is a group of spirochete bacteria species some of which cause borreliosis in humans and dogs. Humans and dogs are susceptible to illness from many of the same tick-borne pathogens, including B. burgdorferi s.l. (Bbsl). Little is known about the pathogenic role of the species of Bbsl in canines. The molecular methods which detect and amplify the DNA of borreliae and allow differentiating borreliae species or strains have not been used in canine diagnostics yet. Until now, it has been believed that in European dogs, like in humans, at least three pathogenic species occur but the most frequently described symptoms may be associated with the infection caused by B. burgdorferi sensu stricto species. A dog as well as a human is a host for many species of Bbsl, because borreliacidal ability of serum of dogs and humans is evident only in certain genospecies of Bbsl. Therefore both a dog and a human harbor more species than in case of some wild animal species which create older phylogenetic Bbsl species–host systems and these animals may act even as a non-competent reservoir host. Apart from many genospecies of Bbsl, a dog harbors other tick-borne agents and dual or triple infections may occur. Ó 2014 Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
Short history of the etiological factor of Lyme disease and epidemiology . Pathogenic role of the species of B. burgdorferi s.l. in canines. . . . . . . . . . . Why do human and dog harbor several species of B. burgdorferi s.l.? . . . . Co-infections with the tick-borne pathogens in dogs . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Declaration of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Borrelia burgdorferi sensu lato is a group of spirochete bacteria causing borreliosis (also called Lyme disease or Lyme borreliosis), a multihost and multipathogen disease, a zoonosis transmitted by ticks. In Europe, these bacteria are transmitted to humans and to reservoir hosts by hard ticks – Ixodes ricinus species (Hermanowska-Szpakowicz et al., 2004; Piesman and Gern, 2004; Wodecka et al., 2010). I. ricinus is a parasitic arthropod with three life stages, i.e., larva, nymph and adult (male or female). Excluding the male, in each stage the tick takes one blood meal on a vertebrate host. I. ricinus feeds on many different vertebrate species ⇑ Tel.: +48 0914441521; fax: +48 0914441580. E-mail address: [email protected] http://dx.doi.org/10.1016/j.meegid.2014.02.014 1567-1348/Ó 2014 Elsevier B.V. All rights reserved.
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which can function as a reservoir host of different B. burgdorferi s.l. genospecies. More than 100 vertebrate species have been identified which can act as reservoir hosts for Lyme borreliosis spirochetes including rodents (vole, wood mouse, dormouse, squirrel, chipmunk, wood rat, rat), insectivores (shrew, hedgehog), raccoon and several bird species (Masuzawa, 2004; Michalik et al., 2005; Piesman and Gern, 2004). For other species such as foxes or badgers only limited information is available and it is uncertain whether they constitute reservoir hosts (Gern and Sell, 2009; Matuschka et al., 2000; Miyamoto and Masuzawa, 2002), although domestic dog has been reported to be reservoir competent (Mather et al., 1994; Leschnik et al., 2010; Straubinger, 2000).
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Currently, on the basis of numerous genetic and phylogenetic analyses, at least 19 subdivisions called genospecies or species have been described in the B. burgdorferi sensu lato complex (Mannelli et al., 2012). Several of these have been detected in Europe (B. burgdorferi sensu stricto (s.s.), Borrelia afzelii, Borrelia garinii, Borrelia valaisiana, Borrelia lusitaniae, Borrelia bavariensis (previously Borrelia garinii OspA serotype 4), Borrelia finlandensis and Borrelia spielmanii (Casjens et al., 2011; HermanowskaSzpakowicz et al., 2004; Kondrusik et al., 2007; Margos et al., 2009; Wang et al., 1997; Wodecka and Skotarczak, 2005). Borrelia andersonii and B. burgdorferi s.s. are typical for North America and five for Asia Borrelia japonica, Borrelia turdi, Borrelia tanukii, Borrelia sinica and Borrelia yangete) (Chu et al., 2008). In ticks I. ricinus, B. afzelii, B. garinii and B. burgdorferi s.s. are the most common European circulating genospecies and they are thought to be the etiological agents of Lyme disease, pathogenic for human and dog (Hovius et al., 1999, 2000; Marconi and Garon, 1992; Rauter and Hartung, 2005; Skotarczak and Wodecka, 2003, 2005; Skotarczak et al., 2005; Wilhelmsson et al., 2010; Wodecka et al., 2009). They are characterized by a different organotropic and pathogenic potential, antigen structure and geographic distribution. Several genospecies may be present simultaneously in a vector (Rauter and Hartung, 2005; Skotarczak et al., 2003; Wodecka et al., 2010). B. burgdorferi s.s. is the only established etiologic agent of Lyme borreliosis in dog and human in North America, where Lyme borreliosis differs in dog and human in terms of clinical outcome following the infection, diagnostic approach, prevention strategy and treatment recommendation (Little et al., 2010). Different genospecies are often associated with other clinical manifestations of the disease: B. burgdorferi s.s. is most often associated with arthritis and neuroborreliosis, B. garinii with neuroborreliosis and B. afzelii with acrodermatitis chronica atrophicans. Although, some species, such as B. lusitaniae, are associated with human diseases only occasionally (Collares-Pereira et al., 2004), and B. bavariensis is probably linked to neuroborreliosis (Ornstein et al., 2001). For other species of Bbsl, such as Borrelia valaisiana, the status is unclear because they have a high regional prevalence in Europe, but have not often been isolated from human (Diza et al., 2004) and the recently described B. finlandensis has uncertain pathogenicity (Casjens et al., 2011). It has been suggested that not all strains/genotypes within a species cause disseminated disease in humans (Wormser et al., 2008). Also, the role of B. spielmanii as a causative agent of LB was confirmed by reported cases of patients with erythema migrans in the Netherlands, Germany, Hungary and Slovenia (Maraspin et al., 2006). Much less is known about Lyme disease in these animals than in a human. The most common symptom of Lyme disease in dog is migratory arthritis without divergent radiographic findings, but there is no erythema migrans characteristic for human Lyme disease. Other but less common symptoms reported in dog are carditis, glomerulonephritis, neuritis and renal lesions. Various studies aimed at showing a relation between renal disease and B. burgdorferi infection. ‘‘Lyme nephritis’’ was investigated in dogs with distinctive renal lesions and typical clinical signs, in which antibodies against B. burgdorferi were found (Gerber et al., 2009). However, a causative role of B. burgdorferi in the development of renal disease was not confirmed, and renal lesions were not found in experimentally infected dogs (Summers et al., 2005). Because of the difficulties in finding sufficient indicative clinical signs, additional information about environmental life of dogs is of importance in the clinical diagnosis of canine Lyme borreliosis (Krupka and Straubinger, 2010). Unlike in the case of human infection, however, a typical Lyme disease in dogs is not easy to document, mainly because many of the animals exposed to B. burgdorferi do not develop clinical
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abnormalities (Levy et al., 1993; Leschnik et al., 2013; Littman et al., 2006).
1. Short history of the etiological factor of Lyme disease and epidemiology Symptoms of Lyme disease have been known in medicine for over 100 years, but due to their multifaceted nature, they were at first considered as several separate diseases. The first symptom was described in 1853, when Buchwald reported it as ‘‘idiopathic skin atrophy’’ (Gustafson, 1994). Attention heightened from 1975 after Steere et al. (1983) identified the disease in children and adolescents in Old Lyme, Connecticut (USA). A strange lesion of joint inflammation was observed regularly in this area and was described as Lyme arthritis. The etiology of this condition was at first unknown, but ticks were suspected and intensively studied because of the seasonal nature of infections, coinciding with times of mass tick emergence, and also due to patients complaining of tick bites (Rand et al., 1996; Steere et al., 1983). In 1981, Willy Burgdorfer from Hamilton University isolated spirochete-like bacteria from a culture from gut contents of the tick Ixodes scapularis (Ixodes dammini) collected on Shelter Island N.Y. (Schwan et al., 1993). This isolate was fixed with the symbol B 31 and became the prototype sample of the species of spirochetes called B. burgdorferi by W. Burgdorfer in 1982 (Burgdofer et al., 1982). Less than a decade after reports of a new infectious disease from Lyme, similar symptoms were described in a domestic dog (Lissman et al., 1984). Many studies show that the frequency of B. burgdorferi infection in human and dog is correlated with the density of ticks’ population and the geographic location of their biotope; these indicate the degree of risk for a human and a dog (Guerra et al., 2001). Dog inhabiting tick infested areas in which instances of human Lyme borreliosis are also found produce B. burgdorferi s.l. antibodies (Magnarelli et al., 1995, 2000; Skotarczak et al., 2003; Stefancikova et al., 1998; Straubinger et al., 1997). The results of numerous studies confirm that from an epidemiological point of view, dogs should be considered as risk animals because they accompany people in high risk areas. Dogs provide a good indication of a likely exposure of their owners to infected ticks, since they largely share the same environment and visit the same outdoor areas (Smith et al., 2012). According to Stefancikova et al. (1998), even removing ticks or grooming infested animals constitute an exposure risk. However, opinions differ. Goossens et al. (2001) did not observe any correlation between frequency of antibodies in a hunting dog and its owner’s serum. They concluded that direct transfer of ticks between hunters and hunting dogs was insignificant and that dog did not constitute a borreliosis hazard. People working or vacationing in tick infested areas have higher frequency of B. burgdorferi antibody occurrence than control groups. According to the authors, if the results of serological studies on people with high outdoor activity are taken into account, then a higher frequency of antibodies against B. burgdorferi is expected in hunting dogs compared with control animals. Several authors suggest that the epidemiological profile of borreliosis in dogs is an indicator of the potential risk to people in the area (Falco et al., 1993; Lindenmayer et al., 1991; Merino et al., 2000). Moreover, according to the results of a new study carried out by the Center for Disease Control and Prevention (CDC), the more dogs with Lyme disease, the higher the frequency of this tick-borne illness in humans in the USA. On the basis of data from ‘‘prevalence maps’’ presented by the Companion Animal Parasite Council (www.PetsAndParasites.org), it was established that the humans in areas with a higher than average number of dogs with borreliosis are at a greater risk of contracting the illness. The
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findings of the study emphasize the importance of alerting pet owners and their families to the risk of tick-borne disease as well as the need of its prevention. The Lyme disease research and prevalence maps are crucial in educating human and veterinary health care professionals as well as pet owners as to the importance of about this increasing problem.
B. afzelii comes from Switzerland (Speck et al., 2001). But, subsequent work by the same team (Speck et al., 2007) reported only an incidental positive PCR result for the presence of DNA of B. bugdorferi s.l. in the blood of naturally infected dogs which questions the usefulness of this technique. Leschnik et al. (2013) arrived at the same conclusion. Thus, in a dog as in a human, there are at least the same three species of pathogenic B. burgdorferi s.l.
2. Pathogenic role of the species of B. burgdorferi s.l. in canines In Europe, the three most prevalent species of the B. burgdorferi s.l. are characterized by a different organotropic and pathogenic potential and, as mentioned above, different species are often associated with different clinical manifestations of the diseases in humans. So far, very little is known of the pathogenic role of the species of B. burgdorferi s.l. in canines, because molecular methods are applied for differentiation of Borrelia species or strains, and they are not commonly used in the veterinary diagnostics. For many years combined infections of the most prevalent genospecies have been thought to occur in European canines and in naturally exposed dogs. B. burgdorferi s.s. and B. garinii co-infections are the most frequent (Hovius et al., 1999). A study of B. burgdorferi s.l DNA isolated from canine blood from north western Poland revealed the dominance of B. burgdorferi s.s. (Skotarczak et al., 2005; Wodecka et al., 2009), as in other studies of human and I. ricinus infection (Wodecka and Skotarczak, 2005). The prevalence of Borrelia species infection was determined using nested polymerase chain reaction (nested PCR) and restriction fragment length polymorphism (RFLP) analysis with enzyme Fsp4H I in blood of dogs naturally infested by ticks in endemic region of Poland (Skotarczak and Wodecka, 2005). Blood samples were collected from 98 dogs of various breeds, brought to the Veterinary Clinic in Szczecin (north-western Poland) for various reasons. The PCR-RFLP revealed a single species, B. burgdorferi s.s. in all PCR – positive samples obtained through amplification of the fla gene. Digestion of PCR products gave one band pattern only consistent with the pattern obtained with sequence analysis of the fla gene from a reference isolate of B. burgdorferi s.s. GeHo (X15660) obtained from the GenBank. In all dogs infected by B. burgdorferi s.s. the limb joints were most commonly affected, resulting in lameness, carpal and tarsal arthralgia, joint swelling. In the latest study of dogs from the same locality (Wodecka et al., 2009), which were brought to the Veterinary Clinic, the veterinary surgeons detected clinical form of borreliosis. Blood samples collected from 18 dogs, with clinically detected borreliosis, were used to acquire DNA for PCR. Positive results of PCR, with primers complementary to the fla gene, indicating the presence of DNA of one species only – B. burgdorferi s.s. were found in the blood of 7 dogs. Each of these dogs most commonly manifested symptoms of arthritic pain and/ or arthritic swelling, fever, anorexia and/or lymphadenopathy. In the USA well documented infections of dogs with combination of polyarthritis, fever, anorexia and/or lymphadenopathy were described (Littman et al., 2006). Since in European descriptions of clinical symptoms of canine Lyme disease (but without genospecies identification) the most common symptoms match those above, the conclusion may be that this species (B. burgdorferi s.s.) is dominant in dogs in Europe. However, in other regions of Poland and other parts of Europe, there are cases of dogs infected with B. garinii and B. afzelii, yet these are single cases only. In the Czech Republic, DNA of B. garinii was detected in blood sample from one dog (Kybicova et al., 2009), also infection with B. garinii was detected (with PCR) in one dog with meningoencephalitis (Kybicova et al., 2009; Schanilec et al., 2010). In central Poland 7 cases with B. afzelii were described, but without any information concerning the clinical symptoms in these dogs (Zygner et al., 2009). A documented report of a naturally exposed dog infected with
3. Why do human and dog harbor several species of B. burgdorferi s.l.? In natural circumstances, the clinical form of borreliosis is found only in species from outside the wood biotope, i.e., human, dog, cat, horse and cow, however most often, it affects a dog and a humans (Appel et al., 1993; Magnarelli et al., 2001; May et al., 1994; Muller et al., 2002; Parker and White, 1992; Steere, 1989). Lack of clinical infection symptoms in forest animals implies that a balanced state in this parasite–host system has been reached as a result of longterm relationships (Skotarczak, 2002). Currently, many factors that decide the sensitivity or resistance of host to Borrelia are already known, but the crucial factor that could explain the selective transmission and host association of B. burgdorferi s.l. is the lytic component in serum (Kraiczy and Stevenson, 2013; Kurtenbach et al., 2002). It was identified as the alternative pathway of complement (Breitner-Ruddock et al., 1997; Kurtenbach et al., 1998a; Van Dam et al., 1997). Analyses of resistance or sensitivity patterns to complement are extended to many B. burgdorferi s.l. strains and different vertebrate species, including avian, reptilian, rodent and ruminant hosts (Kurtenbach et al., 1998a; Kuo et al., 2000; Lane and Quistad, 1998; Nelson et al., 2000) which result in an assumption of a connection between B. burgdorferi s.l. species and some vertebrate hosts. In accordance with this theory, B. afzelii and B. bissettii are resistant to this component occurring in rodents, which makes these animals a competent reservoir for both species. Studies of Kurtenbach et al. (2002) revealed that B. garinii and B. valaisiana are also resistant to the above mentioned component of serum present in birds. B. burgdorferi s.s. also shows indirect sensitivity to this component, in both mammals and birds, so it is not detected in both of these vertebrates. B. lusitaniae is associated with lizard (Kurtenbach et al., 1998b; Majlathova et al., 2006; Richter and Matuschka, 2006). B. spielmanii appears to be associated with dormouse and hedgehog. So far, it has been found that big forest mammals (i.e., roe deer, red deer and wild boar) despite being basic hosts for the adult I. ricinus are not a reservoir for the B. burgdorferi s.l. species (Jaenson and Talleklint, 1992; Kurtenbach et al., 2002; Skotarczak et al., 2008), which means they have borreliacidal ability against borrelial infection. Thus, borrelial genospecies associated with a specific host are usually resistant to the abovementioned component of serum of the given host. However, the associations between genospecies and hosts are not absolute and may vary geographically (Gern, 2008). There is evidence that ticks and reservoir hosts can be co-infected with multiple Borrelia spp. Although many studies show that different species of animals which have achieved the status of a reservoir for B. burgdorferi are a harbor only for one or a few more species of B. burgdorferi. For example, the results of a study by Skuballa et al. (2007) indicate that hedgehogs may be a harbor for three B. burgdorferi genospecies, while a few passerine bird species are associated with B. garinii only (Dubska et al., 2009), in grey squirrel (Sciurus carolinensis Gmelin) and pheasant (Phasianus colchicus Linnaeus) two species B. afzelii and B. garinii were found (Pawelczyk et al., 2004) or only one (Michalik et al., 2005). In other studies, the wood mouse (Apodemus sylvaticus) and bank vole (Myodes glareolus, formerly known as Clethrionomys glareolus) were described as specific hosts for B. afzelii only
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(Buffet et al., 2012), one species only, B. burgdorferi s.s. was found in other rodent hosts, such as the red squirrel (Sciurus vulgaris) and brown rat (Rattus norvegicus) (Humair et al., 1995; Margos et al., 2011; Marsot et al., 2011) or in two rodent species (Myodes glareolus, Apodemus flavicollis) B. garinii only (Craine et al., 1997). Generally, in wild animals usually one, two or three species of B. burgdorferi s.l. occur and more species are resistant to serum component of humans and dogs. In Europe, despite the three species considered as the major human pathogens, such species as B. lusitaniae (Collares-Pereira et al., 2004), B. bavariensis, B. spielmanii or B. valaisiana (Diza et al., 2004) were isolated from humans. In dogs, as mentioned above, there are at least three pathogenic genospecies or even more (Bhide et al., 2005), because humans and dogs are susceptible to illnesses caused by many of the same tick-borne pathogens, including B. burgdorferi s.l. Thus, one can hypothesize that unlike the wild animals, human and domestic animals like a dog, as they are occasionally infected, have not acquired borreliacidal ability against most of the Borrelia genospecies yet. However, this hypothesis is only partly confirmed by the studies of Bhide et al. (2005), in which different Borrelia species and serotypes were tested for their sensitivity to serum complement from various animals and humans as potential hosts reservoir. A percentage of sensitivity of different Borrelia species to dog serum indicates that this animal is a reservoir competent host for all examined Borrelia species (except B. lusitanie), particularly for B. afzelii isolates, B. burgdorferi s.s., B. andersonii-21123 and B. bissettii-DN127. Apart from the dog this host may be its direct ancestor – the wolf, in case of the cat – the lynx. Cats and humans can also be infected by different species of B. burgdorferi s.l. Complement-mediated killing of Borrelia in the European bison, red fallow and roe deer, as may be expected, is extensive and it is evident that these animals act as a non-competent reservoir host, which also pertains to breeding animals like cattle. Serum of other breeding animals, like sheep showed intermediate Borrelia species-dependent killing, similarly to wild animals, like the mouflon. Thus, not only the frequency of contact with a tick and current lifestyle of animal-hosts determine the boreliacidal ability but also the duration of the phylogenetic system of the bacteria–host. So, the oldest borrelia–host systems concern cattle and some species from subfamily Capreolinae and Cervinae, whereas younger ones involve rodents or some species of birds and various species from Felinae and Canidae family as well as humans. The results of Marsot et al. (2011) confirm this hypothesis. In their investigation, they examined whether the Siberian chipmunk (Tamias sibiricus barberi), species introduced in France, was potentially a new reservoir host for species of B. burgdorferi s.l. causing Lyme disease and whether chipmunks were infected by all of the B. burgdorferi s.l. genospecies considered to be associated with European rodents. In addition, the prevalence and diversity of B. burgdorferi s.l. in chipmunks was compared with a native reservoir rodent, the bank vole (Myodes glareolus). Chipmunks were infected by the three Borrelia genospecies that infect rodents (B. burgdorferi sensu stricto, B. afzelii, and B. garinii), whereas voles by B. afzelii only. Because chipmunks were twice more frequently infected than voles, the authors concluded that this may be explained by either a higher exposure of chipmunks (they harbour more ticks), or by their higher tolerance of other B. burgdorferi s.l. genospecies than bank voles. Why do these chipmunks have a higher tolerance for the B. burgdorferi s.l. genospecies? This species of a squirrel living as a native species in Korea has never been infected there by the European genospecies because they are not present in this country (Kurtenbach et al., 2006). A few studies of Siberian chipmunks conducted in China, their native area, reveal that they harbour some native B. burgdorferi s.l. genospecies like Eurasian-type B. garinii 20047, and Asian-type B. garinii NT29 (Chu et al., 2006).
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4. Co-infections with the tick-borne pathogens in dogs Ticks may also transmit other pathogens which complicate the diagnosis. Reports of co-infection with multiple tick-borne organisms in humans and dogs were published (Kordick et al., 1999; Krause et al., 2002; Hermanowska-Szpakowicz et al., 2004; Welc-Fale˛ciak et al., 2009; Rymaszewska and Adamska, 2011; Barth et al., 2012). Among those pathogens there are Anaplasma (Ehrlichia) phagocytophilum bacteria and Babesia protozoa, which, as our studies indicate, coexist in north-western Polish populations of I. ricinus (Skotarczak et al., 2002). The aim of the previous studies in 2004 (Skotarczak et al., 2004) was to determine if dogs infested with ticks were a reservoir for E. phagocytophilum and Babesia spp. The purpose of the recent study (Rymaszewska and Adamska, 2011) from north-western Poland was to examine whether co-infection with two or more vector-borne pathogens could appear in three groups of dogs. The first group consisted of dogs with suspected borreliosis, the second of dogs considered healthy and third group of dogs with detected babesiosis. For the detection of DNA of A. phagocytophilum, Rickettsia spp. and Bartonella spp. in the blood of these dogs, polymerase chain reactions were applied. In dogs from the first group (242 individuals), the DNA of both A. phagocytophilum and Bartonella sp. was identified and in less than 1% of them, DNA of A. phagocytophilum or Bartonella sp. with B. burgdorferi s.l. (the presence of antibodies against and/or DNA B. burgdorferi s.l.) as co-infection was revealed. In the second group, only the DNA of A. phagocytophilum was detected, however in the third group no pathogenic agents transmitted by ticks were found. In other studies from Central Poland (Welc-Faleciak et al., 2009) on sled dogs, the occurrence of four vector-borne infections (Babesia canis, Bartonella sp., Anaplasma/Ehrlichia and B. burgdorferi) was assessed with PCR and nested PCR methods. Among 82 dogs, the DNA of B. canis was detected in three dogs undergoing treatment for babesiosis, but the DNAs of other tick-borne pathogens were also found in 22 out of 79 apparently healthy dogs, including 20 cases of B. canis infection, one case of B. burgdorferi s.l. and one case of A. phagocytophilum. No DNA of Bartonella spp. and Ehrlichia canis was detected in any of the examined samples. Sequencing of Babesia fragment of 18S rDNA gene amplified from acute and asymptomatic cases, revealed that it was identical with the B. canis sequence, originally obtained from Dermacentor reticulatus ticks in Poland. Other studies from Central Poland (Zygner et al., 2009) of blood samples from dogs were carried out to investigate the presence of DNA of B. burgdorferi s.l., Anaplasma phagocytophilum, Babesia canis and Hepatozoon canis. Borrelia DNA was detected in seven of 408 dogs (sequencing amplicons indicated only the B. afzelii genospecies), A phagocytophilum DNA was found in two, and B canis DNA was found in 48 (11.8%). The antibodies against tick-borne pathogens like A. phagocytophilum, B. burgdorferi s.l. and E. canis in French dogs were detected by Pantchev et al. (2009). It is established that Anaplasma platys, the contributing causative agent of infectious canine cyclic thrombocytopenia is endemic in countries of the Mediterranean basin. A. platys was detected in a dog from Croatia which was also co-infected by Babesia vogeli (Dyachenko et al., 2012). Thrombocytopenia, anemia and elevated values of C-reactive protein were the laboratory test abnormalities observed in this case. Other studies from Italy (de Caprariis et al., 2011), indicate a significant association between tick infestation of dogs and A. platys or B. vogeli, as single infections, and A. platys and B. vogeli or A. platys and Bartonella spp. as co-infections. The authors underline that this study shows the clinical difficulties associated with assigning a specific clinical sign or haematological abnormality to a particular canine vector-borne disease. The DNAs of E. canis, A. platys, B. vogeli, Hepatozoon canis, and Bartonella sp.
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