Review
Why are there several species of Borrelia burgdorferi sensu lato detected in dogs and humans?

https://doi.org/10.1016/j.meegid.2014.02.014Get rights and content

Highlights

  • Humans and dogs harbor more species of B. burgdorferi s.l. than other animals.

  • Borrelia burgdorferi s.l. as young phylogenetic system.

  • Humans and dogs have not acquired ability to destroy most of the Borrelia genospecies yet.

  • Co-infections with the tick-borne pathogens in dogs.

Abstract

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.

Section snippets

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

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

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, Müller 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 long-term relationships (

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-Faleciak 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

Conclusion

Dogs, as well as humans, can be infected with more species of B. burgdorferi s.l. than other animals from the forest habitat. This is not only because of their relatively lower exposure to ticks or current lifestyle, but also because these bacteria form a young phylogenetic system and the serum of the dog and the human has not acquired thus far the ability to destroy some species of these bacteria. Dogs apart from many genospecies of B. burgdorferi s.l. harbor other tick-borne agents and dual

Declaration of interest

Author has no declaration of interest to report.

References (104)

  • F.D. Smith et al.

    Estimating Lyme disease risk using pet dogs as sentinels

    Comp. Immunol. Microbiol. Infect. Dis.

    (2012)
  • S. Speck et al.

    Canine borreliosis: a laboratory diagnostic trial

    Vet. Microbiol.

    (2007)
  • B.A. Summers et al.

    Histopathological studies of experimental Lyme disease in the dog

    J. Comp. Pathol.

    (2005)
  • R. Welc-Faleciak et al.

    Babesia canis and other tick-borne infections in dogs in Central Poland

    Vet. Parasitol.

    (2009)
  • M.J.G. Appel et al.

    Experimental Lyme disease in dogs produces arthritis and persistent infection

    J. Infect. Dis.

    (1993)
  • C. Barth et al.

    Prevalence of antibodies against Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum and their clinical relevance in dogs in Munich Germany

    Berl. Munch. Tierarztl. Wochenschr.

    (2012)
  • S. Breitner-Ruddock et al.

    Heterogeneity in the complement-dependent bacteriolysis within the species of Borrelia burgdorferi

    Med. Microbiol. Immunol.

    (1997)
  • W. Burgdofer et al.

    Lyme disease – a tick-borne spirochetosis?

    Science

    (1982)
  • S.R. Casjens et al.

    Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate

    J. Bacteriol.

    (2011)
  • C. Chu et al.

    Molecular epidemiological studies on Borrelia burgdorferi in rodents collected in the forest area of several provinces and autonomous regions of China

    Chin. J. Zoon.

    (2006)
  • C.Y. Chu et al.

    Novel genospecies of Borrelia burgdorferi sensu lato from rodents and ticks in southwestern China

    J. Clin. Microbiol.

    (2008)
  • M. Collares-Pereira et al.

    First isolation of Borrelia lusitaniae from a human patient

    J. Clin. Microbiol.

    (2004)
  • N.G. Craine et al.

    Role of grey squirrels and pheasants in the transmission of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete, in the U.K

    Folia Parasitol. (Praha)

    (1997)
  • E. Diza et al.

    Borrelia valaisiana in cerebrospinal fluid

    Emerg. Infect. Dis.

    (2004)
  • L. Dubska et al.

    Differential role of passerine birds in distribution of Borrelia spirochetes, based on data from ticks collected from birds during the postbreeding migration period in Central Europe

    Appl. Environ. Microbiol.

    (2009)
  • V. Dyachenko et al.

    First case of Anaplasma platys infection in a dog from Croatia

    Parasit. Vectors

    (2012)
  • R.C. Falco et al.

    The distribution of canine exposure to Borrelia burgdorferi in Lyme disease endemic area

    Am. J. Public Health

    (1993)
  • B. Gerber et al.

    The dilemma with Lyme borreliosis in the dog with particular consideration of “Lyme nephritis”

    Schweiz. Arch. Tierheilkd.

    (2009)
  • L. Gern

    Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis: life in the wilds

    Parasite

    (2008)
  • L. Gern et al.

    Isolation of Borrelia burgdorferi sensu lato from the skin of the European badger (Meles meles) in Switzerland

    Vector Borne Zoonotic Dis.

    (2009)
  • H.A. Goossens et al.

    Dogs as sentinels for human Lyme borreliosis in the Netherlands

    J. Clin. Microbiol.

    (2001)
  • M. Guerra et al.

    Canine surveillance system for Lyme borreliosis in Wisconsin and Northern Illinois: geographic distribution and risk factor analysis

    Am. J. Trop. Med. Hyg.

    (2001)
  • R. Gustafson

    Epidemiological studies of Lyme borreliosis and tick-borne encephalitis

    Scand. J. Infect. Dis. Suppl.

    (1994)
  • T. Hermanowska-Szpakowicz et al.

    Detecting DNAS of Anaplasma phagocytophilum and Babesia in the blood of patients suspected of Lyme disease

    Ann. Agric. Environ. Med.

    (2004)
  • K.E. Hovius et al.

    Presence and distribution of Borrelia burgdorferi sensu lato species in internal organs and skin of naturally infected symptomatic and asymptomatic dogs, as detected by polymerase chain reaction

    Vet. Q.

    (1999)
  • J. Hovius et al.

    Antibodies against specific proteins of and immobilizing activity against three strains of Borrelia burgdorferi sensu lato can be found in symptomatic but not in infected asymptomatic dogs

    J. Clin. Microbiol.

    (2000)
  • P.F. Humair et al.

    Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland

    J. Med. Entomol.

    (1995)
  • T.G. Jaenson et al.

    Incompetence of roe deer as reservoirs of the Lyme borreliosis spirochete

    J. Med. Entomol.

    (1992)
  • M. Kondrusik et al.

    Molecular and serological diagnosis of Borrelia burgdorferi infection among patients with diagnosed erythema migrans

    Ann. Agric. Environ. Med.

    (2007)
  • S.K. Kordick et al.

    Co-infection with multiple tick-borne pathogens in a walker hound kennel in North Carolina

    J. Clin. Microbiol.

    (1999)
  • P.J. Krause et al.

    Disease-specific diagnosis of coinfecting tickborne zoonoses: babesiosis, human granulocytic ehrlichiosis, and Lyme disease

    Clin. Infect. Dis.

    (2002)
  • M.M. Kuo et al.

    A comparative study of mammalian and reptilian alternative pathway of complement-mediated killing of the lyme disease spirochete (Borrelia burgdorferi)

    J. Parasitol.

    (2000)
  • K. Kurtenbach et al.

    Serum complement sensitivity as a key factor in Lyme disease ecology

    Infect. Immun.

    (1998)
  • K. Kurtenbach et al.

    Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England

    Appl. Environ. Microbiol.

    (1998)
  • K. Kurtenbach et al.

    Fundamental processes in the evolutionary ecology of Lyme borreliosis

    Nat. Rev. Microbiol.

    (2006)
  • K. Kybicowa et al.

    Detection of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in dogs in the Czech Republic

    Vector Borne Zoonotic Dis.

    (2009)
  • R.S. Lane et al.

    Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis)

    J. Parasitol.

    (1998)
  • M.W. Leschnik et al.

    Humoral immune response in dogs naturally infected with Borrelia burgdorferi sensu lato and in dogs after immunization with a Borrelia vaccine

    Clin. Vaccine Immunol.

    (2010)
  • M. Leschnik et al.

    Effect of owner-controlled acaricidal treatment on tick infestation and immune response to tick-borne pathogens in naturally infested dogs from Eastern Austria

    Parasit. Vectors

    (2013)
  • S.A. Levy et al.

    Canine Lyme borreliosis

    Compend. Contin. Educ. Pract. Vet.

    (1993)
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