Medical Microbiology and Immunology

, Volume 203, Issue 2, pp 85–91 | Cite as

Comparative microbiological features of Bartonella henselae infection in a dog with fever of unknown origin and granulomatous lymphadenitis

  • Amandine Drut
  • Isabelle Bublot
  • Edward B. Breitschwerdt
  • Luc Chabanne
  • Muriel Vayssier-Taussat
  • Jean-Luc Cadoré
Original Investigation

Abstract

We report the first documented case of Bartonella henselae infection in a dog from France and the first isolation of B. henselae from a dog with fever of unknown origin. This observation contributes to the “One Health” concept focusing on zoonotic pathogens emerging from companion animals. A 1-year-old female German shepherd dog was referred for evaluation of fever of unknown origin of 1 month duration. Diagnostic investigations confirmed diffuse pyogranulomatous lymphadenitis. The dog became afebrile, and lymph node size normalized in response to a 6-week course of doxycycline. Retrospectively, Bartonella DNA was amplified from an EDTA-anticoagulated blood sample obtained before antimicrobial therapy, with the gtlA fragment sharing 99 % identity with the 350-bp gtlA fragment of the B. henselae Houston-1 strain. The same strain was isolated in the blood of three healthy cats from the household. Two months after discontinuation of doxycycline, the dog experienced a febrile relapse. Bartonella DNA was again amplified from blood prior to and immediately after administration of a 6-week course azithromycin therapy. However, without administration of additional medications, PCR was negative 9 months after azithromycin therapy and the dog remains clinically healthy 12 months following the second course of antibiotics. The medical management of this case raises several clinically relevant comparative infectious disease issues, including the extent to which Bartonella spp. contribute to fever of unknown origin and pyogranulomatous inflammatory diseases in dogs and humans, and the potential of doxycycline and azithromycin treatment failures. The possibility that dogs could constitute an underestimated reservoir for B. henselae transmission to people is also discussed.

Keywords

Bartonella henselae Cat-scratch disease Dog Fever of unknown origin Granulomatous lymphadenitis 

References

  1. 1.
    Breitschwerdt EB, Maggi RG, Chomel BB, Lappin MR (2010) Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care 20:8–30CrossRefGoogle Scholar
  2. 2.
    Dietrich F, Schmidgen T, Maggi RG, Richter D, Matuschka FR, Vonthein R, Breitschwerdt EB, Kempf VA (2010) Prevalence of Bartonella henselae and Borrelia burgdorferi sensu lato DNA in Ixodes ricinus ticks in Europe. Appl Environ Microbiol 76:1395–1398PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Mascarelli PE, Maggi RG, Hopkins S, Mozayeni BR, Trull CL, Bradley JM, Hegarty BC, Breitschwerdt EB (2013) Bartonella henselae infection in a family experiencing neurological and neurocognitive abnormalities after woodlouse hunter spider bites. Parasites Vectors 6:98PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Kaiser PO, Riess T, O’Rourke F, Linke D, Kempf VA (2011) Bartonella spp.: throwing light on uncommon human infections. Int J Med Microbiol 301:7–15PubMedCrossRefGoogle Scholar
  5. 5.
    Harms A, Dehio C (2012) Intruders below the radar: molecular pathogenesis of Bartonella spp. Clin Microbiol Rev 25:42–78PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Welch DF, Pickett DA, Slater NL, Steigerwalt AG, Brenner DJ (1992) Rochalimaea henselae sp. nov., a cause of septicaemia, bacillary angiomatosis, and parenchymal bacillary peliosis. J Clin Microbiol 30:275–280PubMedCentralPubMedGoogle Scholar
  7. 7.
    Hadfield TL, Warren R, Kass M, Brun E, Levy C (1993) Endocarditis caused by Rochalimaea henselae. Hum Pathol 24:1140–1141PubMedCrossRefGoogle Scholar
  8. 8.
    Holmes A, Greenough T, Balady G, Regnery R, Anderson B, O’Keane JC, Fonger J, McCrone E (1995) Bartonella henselae endocarditis in an immunocompetent adult. Clin Infect Dis 21:1004–1007PubMedCrossRefGoogle Scholar
  9. 9.
    Ohad DG, Morick D, Avidor B, Harrus S (2010) Molecular detection of Bartonella henselae and Bartonella koehlerae from aortic valves of boxer dogs with infective endocarditis. Vet Microbiol 141:182–185PubMedCrossRefGoogle Scholar
  10. 10.
    Fenimore A, Varanat M, Maggi R, Schultheiss P, Breitschwerdt EB, Lappin MR (2011) Bartonella spp. DNA in cardiac tissues from dogs in Colorado and Wyoming. J Vet Intern Med 25:613–616PubMedCrossRefGoogle Scholar
  11. 11.
    Chomel BB, Kasten RW, Willimas C, Wey AC, Henn JB, Maggi RG, Carrasco S, Mazet J, Boulouis HJ, Maillard R, Breitschwerdt EB (2009) Bartonella endocarditis: a pathology shared by animal reservoirs and patients. Ann NY Acad Sci 1166:120–126PubMedCrossRefGoogle Scholar
  12. 12.
    Chomel BB, Kasten RW (2010) Bartonellosis, an increasingly recognized zoonosis. J Appl Microbiol 109:743–750PubMedCrossRefGoogle Scholar
  13. 13.
    Breitschwerdt EB, Linder KL, Day MJ, Maggi RG, Chomel BB, Kempf VA (2013) Koch’s postulates and the pathogenesis of comparative infectious disease causation associated with Bartonella species. J Comp Pathol 148:115–125PubMedCrossRefGoogle Scholar
  14. 14.
    Jacobs RF, Schutze GE (1998) Bartonella henselae as a cause of prolonged fever and fever of unknown origin in children. Clin Infect Dis 26:80–84PubMedCrossRefGoogle Scholar
  15. 15.
    Tsukahara M, Tsuneoka H, Lino H, Murano I, Takahashi H, Uchida M (2000) Bartonella henselae infection as a cause of fever of unknown origin. J Clin Microbiol 38:1990–1991PubMedCentralPubMedGoogle Scholar
  16. 16.
    Day MJ (2011) One health: the importance of companion animal vector-borne diseases. Parasit Vectors 4:49PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Norman AF, Regnery R, Jameson P, Greene C, Krause DC (1995) Differentiation of Bartonella-like isolates at the species level by PCR–restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol 33:1797–1803PubMedCentralPubMedGoogle Scholar
  18. 18.
    Saunders GK, Monroe WE (2006) Systemic granulomatous disease and sialometaplasia in a dog with Bartonella infection. Vet Pathol 43:391–392PubMedCrossRefGoogle Scholar
  19. 19.
    Morales SC, Breitschwerdt EB, Washabau RJ, Matise I, Maggi RG, Duncan AW (2007) Detection of Bartonella henselae DNA in two dogs with pyogranulomatous lymphadenitis. J Am Vet Med Assoc 230:681–685PubMedCrossRefGoogle Scholar
  20. 20.
    Tabar MD, Maggi RG, Altet L, Vilafranca M, Francino O, Roura X (2011) Gammopathy in a Spanish dog infected with Bartonella henselae. J Small Anim Pract 52:209–212PubMedCrossRefGoogle Scholar
  21. 21.
    Kordick DL, Brown TT, Shin KO, Breitschwerdt EB (1999) Clinical and pathologic evaluation of chronic Bartonella henselae or Bartonella clarridgeiae infection in cats. J Clin Microbiol 37:1536–1547PubMedCentralPubMedGoogle Scholar
  22. 22.
    Varanat M, Broadhurst J, Linder KE, Maggi RG, Breitschwerdt EB (2012) Identification of Bartonella henselae in 2 cats with pyogranulomatous myocarditis and diaphragmatic myositis. Vet Pathol 49:608–611PubMedCrossRefGoogle Scholar
  23. 23.
    Liao HM, Huang FY, Chi H, Wang NL, Chen BF (2006) Systemic cat scratch disease. J Formos Med Assoc 105:674–679PubMedCrossRefGoogle Scholar
  24. 24.
    Vayssier-Taussat M, Le Rhun D, Deng HK, Biville F, Cescau S, Danchin A, Marignac G, Lenaour E, Boulouis HJ, Mavris M, Arnaud L, Yang H, Wang J, Quebatte M, Engel P, Saenz H, Dehio C (2010) The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog 6:e1000946PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Kordick DL, Papich MG, Breitschwerdt EB (1997) Efficacy of enrofloxacin or doxycycline for treatment of Bartonella henselae or Bartonella clarridgeiae infection in cats. Antimicrob Ag Chemother 41:2448–2455Google Scholar
  26. 26.
    Eddlestone SM, Diniz PP, Neer TM, Gaunt SD, Corstvet R, Cho D, Hosgood G, Hegarty B, Breitschwerdt EB (2007) Doxycycline clearance of experimentally induced chronic Ehrlichia canis infection in dogs. J Vet Intern Med 21:1237–1242PubMedCrossRefGoogle Scholar
  27. 27.
    Breitschwerdt EB, Papich MG, Hegarty BC, Gilger B, Hancock SI, Davidson MG (1999) Efficacy of doxycycline, azithromycin, or trovafloxacin for treatment of experimental Rocky Mountain spotted fever in dogs. Antimicrob Agents Chemother 43:813–821PubMedCentralPubMedGoogle Scholar
  28. 28.
    Kordick DL, Breitschwerdt EB (1998) Persistent infection of pets within a household with three Bartonella species. Emerg Infect Dis 4:325–328PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Biswas S, Maggi RG, Papich MG, Breitschwerdt EB (2010) Molecular mechanisms of Bartonella henselae resistance to azithromycin, pradofloxacin and enrofloxacin. J Antimicrob Chemother 65:581–582PubMedCrossRefGoogle Scholar
  30. 30.
    VanderHeyden TR, Yong SL, Breitschwerdt EB, Maggi RG, Mihalik AR, Parada JP, Fimmel CJ (2012) Granulomatous hepatitis due to Bartonella henselae infection in an immunocompetent patient. BMC Infect Dis 12:17PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Diniz PP, Wood M, Maggi RG, Sontakke S, Stepnik M, Breitschwerdt EB (2009) Co-isolation of Bartonella henselae and Bartonella vinsonii subsp. berkhoffi from blood, joint and subcutaneous seroma from two naturally infected dogs. Vet Microbiol 138:368–372PubMedCrossRefGoogle Scholar
  32. 32.
    Sykes JE, Lindsay LL, Maggi RG, Breitschwerdt EB (2010) Human coinfection with Bartonella henselae and two hemotropic mycoplasma variants resembling Mycoplasma ovis. J Clin Microbiol 48:3782–3785PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Breitschwerdt EB, Kordick DL (2010) Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clin Microbiol Rev 13:428–438CrossRefGoogle Scholar
  34. 34.
    Guptill L (2010) Bartonellosis. Vet Microbiol 140:347–359PubMedCrossRefGoogle Scholar
  35. 35.
    Diniz PP, Billeter SA, Otranto D, De Caprariis D, Petanides T, Mylonakis ME, Koutinas AF, Breitschwerdt EB (2009) Molecular documentation of Bartonella infection in dogs in Greece and Italy. J Clin Microbiol 47:1565–1567PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Chomel BB, McMillan-Cole AC, Kasten RW, Stuckey MJ, Sato S, Maruyama S, Diniz PP, Breitschwerdt EB (2012) Candidatus Bartonella merieuxii, a potential new zoonotic Bartonella species for canids from Iraq. PLOS Neglect Trop Dis 6:e1843CrossRefGoogle Scholar
  37. 37.
    Sun J, Fu G, Lin J, Song X, Lu L, Liu Q (2010) Seroprevalence of Bartonella in Eastern China and analysis of risk factors. BMC Infect Dis 10:121PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Rolain JM, Boureau-Voultoury A, Raoult D (2009) Serological evidence of Bartonella vinsonii lymphadenopathies in a child bitten by a dog. Clin Microbiol Infect 15(Suppl 2):122–123PubMedCrossRefGoogle Scholar
  39. 39.
    Pérez C, Maggi RG, Diniz PP, Breitschwerdt EB (2011) Molecular and serological diagnosis of Bartonella infection in 61 dogs from the United States. J Vet Intern Med 25:805–810PubMedCrossRefGoogle Scholar
  40. 40.
    Maggi RG, Mascarelli PE, Pultorak EL, Hegarty BC, Bradley JM, Mozayeni BR, Breitschwerdt EB (2011) Bartonella spp. bacteremia in high-risk immunocompetent patients. Diag Microbiol Infect Dis 71:430–437CrossRefGoogle Scholar
  41. 41.
    Oliveira AM, Maggi RG, Woods CW, Breitschwerdt EB (2010) Suspected needle stick transmission of Bartonella vinsonii subspecies berkhoffi to a veterinarian. J Vet Intern Med 24:1229–1232PubMedCrossRefGoogle Scholar
  42. 42.
    Lin JW, Chen CM, Chang CC (2011) Unknown fever and back pain caused by Bartonella henselae in a veterinarian after a needle puncture: a case report and literature review. Vector Borne Zoonotic Dis 11:589–591PubMedCrossRefGoogle Scholar
  43. 43.
    O’Reilly KL, Bauer RW, Freeland RL, Foil LD, Hughes KJ, Rohde KR, Roy AF, Stout RW, Triche PC (1999) Acute clinical disease in cats following infection with a pathogenic strain of Bartonella henselae (LSU16). Infect Immun 67:3066–3072PubMedCentralPubMedGoogle Scholar
  44. 44.
    Boulouis HJ, Chang CC, Henn JB, Kasten RW, Chomel BB (2005) Factors associated with the rapid emergence of zoonotic Bartonella infections. Vet Res 36:383–410PubMedCrossRefGoogle Scholar
  45. 45.
    Bouchouicha R, Durand B, Monteil M, Chomel BB, Berrich M, Arvand M, Birtles RJ, Breitschwerdt EB, Koehler JE, Maggi RG, Maruyama S, Kasten R, Petit E, Boulouis HJ, Haddad N (2009) Molecular epidemiology of feline and human Bartonella henselae isolates. Emerg Infect Dis 15:813–816PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Amandine Drut
    • 1
  • Isabelle Bublot
    • 1
  • Edward B. Breitschwerdt
    • 2
  • Luc Chabanne
    • 3
  • Muriel Vayssier-Taussat
    • 4
  • Jean-Luc Cadoré
    • 1
  1. 1.Service de Pathologie Médicale des Carnivores Domestiques, VetAgro Sup Lyon Campus VétérinaireUniversité de LyonMarcy l’EtoileFrance
  2. 2.Intracellular Pathogens Research Laboratory, Center for Comparative Medicine and Translational Research, College of Veterinary MedicineNorth Carolina State UniversityRaleighUSA
  3. 3.Département des Animaux de Compagnie and Jeune Equipe Hémopathogènes Vectorisés, VetAgro Sup Lyon Campus VétérinaireUniversité de LyonMarcy l’EtoileFrance
  4. 4.USC BiparINRAMaisons-AlfortFrance

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