Clinical Rheumatology

, Volume 36, Issue 7, pp 1669–1675 | Cite as

Culture, PCR, DNA sequencing, and second harmonic generation (SHG) visualization of Bartonella henselae from a surgically excised human femoral head

  • M. Ericson
  • N. Balakrishnan
  • B.R. Mozayeni
  • C.W. Woods
  • J. Dencklau
  • S. Kelly
  • E. B. BreitschwerdtEmail author
Brief Report


Bartonella henselae is an emerging, zoonotic pathogen that appears to represent an occupational risk for individuals with arthropod exposures and animal contact [1, 2]. Rheumatic and musculoskeletal abnormalities have been previously reported in patients with or following historical cat scratch disease (CSD), caused predominantly or solely by B. henselae [3, 4, 5] In contrast to the classical self-limiting clinical presentation of fever and lymphadenopathy and a history of cat scratch in patients with CSD, recent evidence supports the possibility of persistent intravascular infections in previously immunocompetent patients with accompanying rheumatic symptoms [1, 6]. Historically, systemic bartonellosis has been reported in immunocompromised patients, such as HIV/AIDS or transplant recipients [7]. Recently, Bartonellaspp. bacteremia has been reported in healthy Brazilian blood donors and in previously healthy, immunocompetent patients who developed chronic and often...


Femoral Head Second Harmonic Generation Spongy Tissue Second Harmonic Generation Signal Bartonella Henselae 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Keith T. Brickman for facilitating rapid transport of the femoral head from the surgery site to the NCSU-CVM IPRL for microbiological culture. This research was supported in part by unrestricted donations to the NCSU-CVM Foundation for Vector Borne Diseases Research.

Compliance with ethical standards

Conflict of interest

In conjunction with Dr. Sushama Sontakke and North Carolina State University, Edward B. Breitschwerdt, DVM, holds US Patent No. 7,115,385; Media and methods for cultivation of microorganisms, which was issued on October 3, 2006. He is a co-founder, stock holder, and chief scientific officer for Galaxy Diagnostics, a company that provides advanced diagnostic testing for the detection of Bartonella species infections. Robert B. Mozayeni, MD, is chief medical officer for Galaxy Diagnostics. The remaining authors have no competing interests.


  1. 1.
    Lantos PM, Maggi RG, Ferguson B, VarkeyJ PLP, Breitschwerdt EB et al (2015) Detection of Bartonella species in the blood of veterinarians and veterinary technicians: a newly recognized occupational hazard. Vector Borne Zoonotic Dis Dis 14:563–570CrossRefGoogle Scholar
  2. 2.
    Maggi RG, Mascarelli PE, Pultorak EL, Hegarty BC, Bradley JM, Mozayeni BR et al (2011) Bartonella spp. bacteremia in high-risk immunocompetent patients. Diagn Microbiol Infect Dis 71:43–37CrossRefGoogle Scholar
  3. 3.
    Giladi M, Maman E, Paran D, Bickels J, Comaneshter D, Avidor B et al (2005) Cat-scratch disease-associated arthropathy. Arthritis Rheum 52:3611–3617CrossRefPubMedGoogle Scholar
  4. 4.
    Graveleau J, Grossi O, Lefebvre M, Redon H, Caignon JM, Pallardy A et al (2011) Vertebral osteomyelitis: an unusual presentation of Bartonella henselae infection. Semin Arthritis Rheum 41:511–516CrossRefPubMedGoogle Scholar
  5. 5.
    Maman E, Bickels J, Ephros M, Paran D, Comaneshter D, Metzkor-Cotter E et al (2007) Musculoskeletal manifestations of cat scratch disease. Clin Infect Dis 45:1535–1540CrossRefPubMedGoogle Scholar
  6. 6.
    Maggi RG, Mozayeni BR, Pultorak EL, Hegarty BC, Bradley JM, Correa M et al (2012) Bartonella spp. bacteremia and rheumatic symptoms in patients from Lyme disease-endemic region. Emerg Infect Dis 18:783–791CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Rostad CA, McElroy AK, Hilinski JA, Thompson MP, Drew CP, Denison AM et al (2012) Bartonella henselae-mediated disease in solid organ transplant recipients: two pediatric cases and a literature review. Transpl Infect Dis 14:71–81CrossRefGoogle Scholar
  8. 8.
    Vayssier-Taussat M, Moutailler S, Féménia F, Raymond P, Croce O, La Scola B et al (2016) Identification of novel zoonotic activity of Bartonella spp., France. Emerg Infect Dis 22:457–462CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Pitassi LH, de Paiva Diniz PP, Scorpio DG, Drummond MR, Lania BG, Barjas-Castro ML et al (2015) Bartonella spp. bacteremia in blood donors from Campinas, Brazil. PLoS Negl Trop Dis 9:1–12Google Scholar
  10. 10.
    Duncan AW, Maggi RG, Breitschwerdt EB (2007) A combined approach for the enhanced detection and isolation of Bartonella species in dog blood samples: pre-enrichment culture followed by PCR and subculture onto agar plates. J Microbiol Meth 69:273–281CrossRefGoogle Scholar
  11. 11.
    Kehoe SP, Chomel BB, Stuckey MJ, Kasten RW, Balakrishnan N, Sacks BN et al (2014) Zoonotic Bartonella species in cardiac valves of healthy coyotes, California, USA. Emerg Infect Dis 20:2133–2136CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Varanat M, Maggi RG, Linder KE, Breitschwerdt EB (2011) Molecular prevalence of Bartonella, Babesia, and hemotropic Mycoplasma sp. in dogs with splenic disease. J Vet Intern Med 25:1284–1291CrossRefPubMedGoogle Scholar
  13. 13.
    Balakrishnan N, Ericson M, Maggi R, Breitschwerdt EB (2016) Vasculitis, cerebral infarction and persistent Bartonella henselae infection in a child. Parasit Vectors 9:254CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bestvater F, Spiess E, Stobrawa G, Hacker M, Feurer T, Porwol T et al (2002) Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging. J Microsc 208:108–115CrossRefPubMedGoogle Scholar
  15. 15.
    Keret D, Giladi M, Kletter Y, Wientroub S (1998) Cat-scratch disease osteomyelitis from a dog scratch. J Bone Join Surg Br 80:766–767CrossRefGoogle Scholar
  16. 16.
    Puri K, Kerppel AJ, Schlaudecker EP (2015) Bartonella osteomyelitis of the acetabulum: case report and review of the literature. Vector Borne Zoonotic Dis 15:463–467CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Krause R, Wenisch C, Fladerer P, Daxböck F, Krejs GJ et al (2000) Osteomyelitis of the hip joint associated with systemic cat-scratch disease in an adult. Eur J Clin Microbiol Infect Dis 10:781–783CrossRefGoogle Scholar
  18. 18.
    Dillon B, Cagney M, Manolios N, Iredell JR (2000) Failure to detect Bartonella henselae infection in synovial fluid from sufferers of chronic arthritis. Rheumatol Int 19:219–222CrossRefPubMedGoogle Scholar
  19. 19.
    Breitschwerdt EB (2014) Bartonellosis: one health perspectives for an emerging infectious disease. ILAR J 55:46–58CrossRefPubMedGoogle Scholar
  20. 20.
    Popa C, Abdollahi-Roodsaz S, Joosten LA, Takahashi N, Sprong T, Matera G et al (2007) Bartonella quintana lipopolysaccharide is a natural antagonist of Toll-like receptor 4. Infect Immun 75:4831–4837CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Abdollahi-Roodsaz S, Joosten LA, Roelofs MF, Radstake TR, Matera G et al (2007) Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis Rheum 56:2957–2967CrossRefPubMedGoogle Scholar
  22. 22.
    Campagnola PJ, Clark HA, Mohler WA, Lewis A, Loew LM (2001) Second-harmonic imaging microscopy of living cells. J Biomed Opt 6:277–286CrossRefPubMedGoogle Scholar
  23. 23.
    Williams RM, Zipfel WR, Webb WW (2005) Interpreting second-harmonic generation images of collagen I fibrils. Biophys J 88:1377–1386Google Scholar
  24. 24.
    Merrell DS, Falkow S (2004) Frontal and stealth attack strategies in microbial pathogenesis. Nature 430:250–256Google Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2016

Authors and Affiliations

  • M. Ericson
    • 1
  • N. Balakrishnan
    • 2
  • B.R. Mozayeni
    • 3
  • C.W. Woods
    • 4
    • 5
  • J. Dencklau
    • 1
  • S. Kelly
    • 6
  • E. B. Breitschwerdt
    • 2
    Email author
  1. 1.Tissue Imaging Research Laboratory, Department of DermatologyUniversity of Minnesota Medical SchoolMinneapolisUSA
  2. 2.Department of Clinical Sciences, Intracellular Pathogens Research Laboratory, College of Veterinary MedicineNorth Carolina State UniversityRaleighUSA
  3. 3.Translational Medicine Group PCNorth BethesdaUSA
  4. 4.Duke University Medical CenterDurhamUSA
  5. 5.Department of MedicineDurham Veterans Administration Medical CenterDurhamUSA
  6. 6.North Carolina Orthopedic Clinic, Duke MedicineDurhamUSA

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