Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 22, Number 5—May 2016

Differences in Genotype, Clinical Features, and Inflammatory Potential of Borrelia burgdorferi sensu stricto Strains from Europe and the United States

Tjasa Cerar1, Franc Strle1, Dasa Stupica, Eva Ruzic-Sabljic, Gail McHugh, Allen C. Steere, and Klemen StrleComments to Author 
Author affiliations: University of Ljubljana, Ljubljana, Slovenia (T. Cerar, E. Ruzic-Sabljic); University Medical Center, Ljubljana (F. Strle, D. Stupica); Massachusetts General Hospital, Boston, Massachusetts, USA (G. McHugh, A.S. Steere, K. Strle)

Main Article

Table 1

Characterization of Borrelia burgdorferi sensu stricto strains, by RST and OspC, from patients in Slovenia and the United States*

Genotype Slovenia, n = 29, no. (%) United States, n = 90†, no. (%)
RST1 21 (72) 38 (42)
OspC type A 0 27 (30)
OspC type B‡ 17 (58) 11 (12)
OspC type Q 2 (7) 0
OspC type R 1 (3) 0
OspC type M1 1 (3) 0
RST2 0 39 (43)
OspC type F 0 1 (1)
OspC type H 0 4 (4)
OspC type K 0 25 (28)
OspC type N 0 9 (10)
RST3 8 (28) 13 (14)
OspC type D 0 1 (1)
OspC type E 0 3 (3)
OspC type G 0 2 (2)
OspC type I 0 7 (8)
OspC type L 7 (24) 0
OspC type S 1 (3) 0

*RST, ribosomal RNA intergenic sequence type; OspC, outer surface protein C.
†Based on previously published data (10).
‡Found in central Europe and the United States.

Main Article

  1. Stanek  G, Wormser  GP, Gray  J, Strle  F. Lyme borreliosis. Lancet. 2012;379:46173. DOIPubMedGoogle Scholar
  2. Steere  AC. Lyme disease. N Engl J Med. 2001;345:11525. DOIPubMedGoogle Scholar
  3. Wang  G, van Dam  AP, Schwartz  I, Dankert  J. Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin Microbiol Rev. 1999;12:63353 .PubMedGoogle Scholar
  4. Jones  KL, Muellegger  RR, Means  TK, Lee  M, Glickstein  LJ, Damle  N, Higher mRNA levels of chemokines and cytokines associated with macrophage activation in erythema migrans skin lesions in patients from the United States than in patients from Austria with Lyme borreliosis. Clin Infect Dis. 2008;46:8592 . DOIPubMedGoogle Scholar
  5. Strle  F, Nadelman  RB, Cimperman  J, Nowakowski  J, Picken  RN, Schwartz  I, Comparison of culture-confirmed erythema migrans caused by Borrelia burgdorferi sensu stricto in New York State and by Borrelia afzelii in Slovenia. Ann Intern Med. 1999;130:326 . DOIPubMedGoogle Scholar
  6. Wormser  GP, McKenna  D, Carlin  J, Nadelman  RB, Cavaliere  LF, Holmgren  D, Brief communication: hematogenous dissemination in early Lyme disease. Ann Intern Med. 2005;142:7515. DOIPubMedGoogle Scholar
  7. Strle  F, Ruzic-Sabljic  E, Logar  M, Maraspin  V, Lotric-Furlan  S, Cimperman  J, Comparison of erythema migrans caused by Borrelia burgdorferi and Borrelia garinii. Vector Borne Zoonotic Dis. 2011;11:12538. DOIPubMedGoogle Scholar
  8. Strle  K, Drouin  EE, Shen  S, El Khoury  J, McHugh  G, Ruzic-Sabljic  E, Borrelia burgdorferi stimulates macrophages to secrete higher levels of cytokines and chemokines than Borrelia afzelii or Borrelia garinii. J Infect Dis. 2009;200:193643. DOIPubMedGoogle Scholar
  9. Belfaiza  J, Postic  D, Bellenger  E, Baranton  G, Girons  IS. Genomic fingerprinting of Borrelia burgdorferi sensu lato by pulsed-field gel electrophoresis. J Clin Microbiol. 1993;31:28737 .PubMedGoogle Scholar
  10. Jones  KL, Glickstein  LJ, Damle  N, Sikand  VK, McHugh  G, Steere  AC. Borrelia burgdorferi genetic markers and disseminated disease in patients with early Lyme disease. J Clin Microbiol. 2006;44:440713. DOIPubMedGoogle Scholar
  11. Liveris  D, Varde  S, Iyer  R, Koenig  S, Bittker  S, Cooper  D, Genetic diversity of Borrelia burgdorferi in Lyme disease patients as determined by culture versus direct PCR with clinical specimens. J Clin Microbiol. 1999;37:5659 .PubMedGoogle Scholar
  12. Wang  IN, Dykhuizen  DE, Qiu  W, Dunn  JJ, Bosler  EM, Luft  BJ. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics. 1999;151:1530 .PubMedGoogle Scholar
  13. Margos  G, Gatewood  AG, Aanensen  DM, Hanincova  K, Terekhova  D, Vollmer  SA, MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc Natl Acad Sci U S A. 2008;105:87305. DOIPubMedGoogle Scholar
  14. Ronquist  F, Teslenko  M, van der Mark  P, Ayres  DL, Darling  A, Hohna  S, MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:53942. DOIPubMedGoogle Scholar
  15. Barbour  AG. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984;57:5215 .PubMedGoogle Scholar
  16. Strle  K, Jones  KL, Drouin  EE, Li  X, Steere  AC. Borrelia burgdorferi RST1 (OspC type A) genotype is associated with greater inflammation and more severe Lyme disease. Am J Pathol. 2011;178:272639. DOIPubMedGoogle Scholar
  17. Wormser  GP, Brisson  D, Liveris  D, Hanincova  K, Sandigursky  S, Nowakowski  J, Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. J Infect Dis. 2008;198:135864. DOIPubMedGoogle Scholar
  18. Wormser  GP, Liveris  D, Nowakowski  J, Nadelman  RB, Cavaliere  LF, McKenna  D, Association of specific subtypes of Borrelia burgdorferi with hematogenous dissemination in early Lyme disease. J Infect Dis. 1999;180:7205. DOIPubMedGoogle Scholar
  19. Seifert  SN, Khatchikian  CE, Zhou  W, Brisson  D. Evolution and population genomics of the Lyme borreliosis pathogen, Borrelia burgdorferi. Trends Genet. 2015;31:2017. DOIPubMedGoogle Scholar
  20. Bennet  L, Fraenkel  CJ, Garpmo  U, Halling  A, Ingman  M, Ornstein  K, Clinical appearance of erythema migrans caused by Borrelia afzelii and Borrelia garinii: effect of the patient’s sex. Wien Klin Wochenschr. 2006;118:5317. DOIPubMedGoogle Scholar
  21. Barbour  AG, Travinsky  B. Evolution and distribution of the ospC gene, a transferable serotype determinant of Borrelia burgdorferi. MBio. 2010;1:e0015310. DOIPubMedGoogle Scholar
  22. Rudenko  N, Golovchenko  M, Honig  V, Mallatova  N, Krbkova  L, Mikulasek  P, Detection of Borrelia burgdorferi sensu stricto ospC alleles associated with human Lyme borreliosis worldwide in non-human-biting tick Ixodes affinis and rodent hosts in southeastern United States. Appl Environ Microbiol. 2013;79:144453. DOIPubMedGoogle Scholar
  23. Qiu  WG, Bruno  JF, McCaig  WD, Xu  Y, Livey  I, Schriefer  ME, Wide distribution of a high-virulence Borrelia burgdorferi clone in Europe and North America. Emerg Infect Dis. 2008;14:1097104. DOIPubMedGoogle Scholar
  24. Hanincova  K, Mukherjee  P, Ogden  NH, Margos  G, Wormser  GP, Reed  KD, Multilocus sequence typing of Borrelia burgdorferi suggests existence of lineages with differential pathogenic properties in humans. PLoS ONE. 2013;8:e73066 . DOIPubMedGoogle Scholar
  25. Jungnick  S, Margos  G, Rieger  M, Dzaferovic  E, Bent  SJ, Overzier  E, Borrelia burgdorferi sensu stricto and Borrelia afzelii: population structure and differential pathogenicity. Int J Med Microbiol. 2015;305:67381. DOIPubMedGoogle Scholar
  26. Sadziene  A, Wilske  B, Ferdows  MS, Barbour  AG. The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect Immun. 1993;61:21925 .PubMedGoogle Scholar
  27. Carlsson  SA, Granlund  H, Jansson  C, Nyman  D, Wahlberg  P. Characteristics of erythema migrans in Borrelia afzelii and Borrelia garinii infections. Scand J Infect Dis. 2003;35:313. DOIPubMedGoogle Scholar
  28. Logar  M, Ruzic-Sabljic  E, Maraspin  V, Lotric-Furlan  S, Cimperman  J, Jurca  T, Comparison of erythema migrans caused by Borrelia afzelii and Borrelia garinii. Infection. 2004;32:159. DOIPubMedGoogle Scholar
  29. Strle  F, Ruzic-Sabljic  E, Logar  M, Maraspin  V, Lotric-Furlan  S, Cimperman  J, Comparison of erythema migrans caused by Borrelia burgdorferi and Borrelia garinii. Vector Borne Zoonotic Dis. 2011;11:12538. DOIPubMedGoogle Scholar
  30. Strle  F, Ruzic-Sabljic  E, Cimperman  J, Lotric-Furlan  S, Maraspin  V. Comparison of findings for patients with Borrelia garinii and Borrelia afzelii isolated from cerebrospinal fluid. Clin Infect Dis. 2006;43:70410. DOIPubMedGoogle Scholar
  31. Mason  LM, Herkes  EA, Krupna-Gaylord  MA, Oei  A, Van der Poll  T, Wormser  GP, Borrelia burgdorferi clinical isolates induce human innate immune responses that are not dependent on genotype. Immunobiology. 2015;220:114150. DOIPubMedGoogle Scholar
  32. Strle  K, Stupica  D, Drouin  EE, Steere  AC, Strle  F. Elevated levels of IL-23 in a subset of patients with post-Lyme disease symptoms following erythema migrans. Clin Infect Dis. 2014;58:37280. DOIPubMedGoogle Scholar

Main Article

1These authors contributed equally to this article.

Page created: April 13, 2016
Page updated: April 13, 2016
Page reviewed: April 13, 2016
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.