Macrolide resistance in Treponema pallidum subsp. pallidum in the Czech Republic and in other countries
Authors:
L. Grillová 1; L. Mikalová 1; H. Zákoucká 2; J. Židlická 3; D. Šmajs 1*
Authors‘ workplace:
Biologický ústav, Lékařská fakulta, Masarykova univerzita, Brno
1; Národní referenční laboratoř pro diagnostiku syfilis, Státní zdravotní ústav, Praha
2; Státní ústav pro kontrolu léčiv, Praha
3
Published in:
Epidemiol. Mikrobiol. Imunol. 64, 2015, č. 1, s. 4-10
Category:
Review articles, original papers, case report
Overview
Treponema pallidum subsp. pallidum (TPA) is the causative agent of the sexually transmitted disease syphilis. In the Czech Republic, several hundred cases of syphilis are reported annually; e.g. in 2012, 696 syphilis cases were documented. In the last decades, an increasing prevalence of macrolide resistant TPA strains harboring A2058G or A2059G mutations in the 23S rRNA gene has been reported. Macrolides were used (and rarely are still being used) in the Czech Republic for the treatment of syphilis in patients allergic to penicillin. While 37% of TPA strains were resistant to macrolides between 2004 and 2010, this rate increased to 67% between 2011–2013. High prevalence of A2058G or A2059G mutations and increasing rates of macrolide resistant TPA strains have also been documented in other developed countries. Therefore, macrolides should not be used in the treatment of syphilis.
Key words:
syphilis – Treponema pallidum – resistence – macrolides
Sources
1. Procházka K. Venerologie. Lékařské knihkupectví a nakladatelstvíMladé generace lékařů v Praze, 1948.
2. Hübschmann K. Venerologie. Státní zdravotnické nakladatelství Praha, 1959.
3. Pohlavní nemoci [online]. Ústav zdravotnických informací a statistiky ČR. 2003-2012. 1x ročně. Dostupný z http://www.uzis.cz/category/tematicke-rady/zdravotnicka-statistika/pohlavni-nemoci. SSN:1210-8634.
4. Urbášková P, Marešová V, Jindrák V et al. Konsenses používání antibiotik II. Makrolidová antibiotika. Dostupné z http://www.szu.cz/konsensy-pouzivani-antibiotik.
5. Adriaenssens N, Coenen S, Versporten A et al. European Surveillance of Antimicrobial Consumption (ESAC): Outpatient macrolide, lincosamide and streptogramin (MLS) use in Europe (1997-2009). J Antimicrob Chemother, 2011;66(6):37–45.
6. Vanicek J, Stastnik M, Kianicka B et al. Rare neurological presentation of human granulocytic anaplasmosis. Eur J Neurol, 2013;20(5):70–72.
7. Hashisaki P, Wertzberger GG, Conrad GL. Erythromycin failure in the treatment of syphilis in a pregnant woman. Sex Transm Dis, 1983;10(1):36–38.
8. Stapleton JT, Stamm LV, Bassford PJ. Potential for development of antibiotic resistance in pathogenic treponemes. Rev Infect Dis, 1985;7(2):314–317.
9. Stamm LV, Stapleton JT, Bassford PJ. In vitro assay to demonstrate high-level erythromycin resistance of a clinical isolate of Treponema pallidum. Antimicrob Agents Chemother, 1988;32(2):164–169.
10. Duncan WC. Failure of erythromycin to cure secondary syphilis in a patient infected with the human immunodeficiency virus. Arch Dermatol, 1989;125(1):82–84.
11. Sands M, Markus A. Lues maligna, or ulceronodular syphilis, in a man infected with human immunodeficiency virus: Case report and review. Clin Infect Dis, 1995;20(2):387–390.
12. Klausner JD, Kohn RP, Kent CK. Azithromycin versus penicillin for early syphilis. N Engl J Med, 2006;354(2):203–205.
13. Lukehart SA, Godornes C, Molini BJ et al. Macrolide resistance in Treponema pallidum in the United States and Ireland. N Engl J Med, 2004;351(2):154–158.
14. Mitchell SJ, Engelman J, Kent CK et al. Azithromycin-resistant syphilis infection: San Francisco, California, 2000-2004. Clin Infect Dis, 2006;42(3):337–345.
15. Matějková P, Flasarová M, Zákoucká H et al. Macrolide treatment failure in a case of secondary syphilis: A novel A2059G mutation in the 23S rRNA gene of Treponema pallidum subsp. pallidum. J Med Microbiol, 2009;58(6):832–836.
16. Woznicová V, Matějková P, Flasarová M et al. Clarithromycin treatment failure due to macrolide resistance in Treponema pallidum in a patient with primary syphilis. Acta Derm Venereol, 2010;90(2):206–207.
17. Zhou P, Li K, Lu H et al. Azithromycin treatment failure among primary and secondary syphilis patients in Shanghai. Sex Transm Dis, 2010;37(11):726–729.
18. Vester B, Douthwaite S. Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob Agents Chemother, 2001;45(1):1–12.
19. Vester B, Douthwaite S. Domain V of 23S rRNA contains all the structural elements necessary for recognition by the ErmE methyltransferase. J Bacteriol, 1994;176(22):6999–7004.
20. Xiong L, Shah S, Mauvais P et al. A ketolide resistance mutation in domain II of 23S rRNA reveals the proximity of hairpin 35 to the peptidyl transferase centre. Mol Microbiol, 1999;31(2):633–639.
21. Pfister P, Jenni S, Poehlsgaard J et al. The structural basis of macrolide-ribosome binding assessed using mutagenesis of 23S rRNA positions 2058 and 2059. J Mol Biol, 2004;342(5):1569–1581.
22. Gibreel A, Kos VN, Keelan M et al. Macrolide resistance in Campylobacter jejuni and Campylobacter coli: Molecular mechanism and stability of the resistance phenotype. Antimicrob Agents Chemother, 2005;49(7):2753–2759.
23. Versalovic J, Shortridge D, Kibler K et al. Mutations in 23S rRNA are associated with clarithromycin resistance in Helicobacter pylori. Antimicrob Agents Chemother, 1996;40(2):477–480.
24. Misyurina OY, Chipitsyna EV, Finashutina YP et al. Mutations in a 23S rRNA gene of Chlamydia trachomatis associated with resistance to macrolides. Antimicrob Agents Chemother, 2004;48(4):1347–1349.
25. Zhu H, Wang HP, Jiang Y et al. Mutations in 23S rRNA and ribosomal protein L4 account for resistance in Chlamydia trachomatis strains selected in vitro by macrolide passage. Andrologia, 2010;42(4):274–280.
26. Begovic J, Huys G, Mayo B et al. Human vaginal Lactobacillus rhamnosus harbor mutation in 23S rRNA associated with erythromycin resistance. Res Microbiol, 2009;160(6):421–426.
27. Wallace RJ, Meier A, Brown BA et al. Genetic basis for clarithromycin resistance among isolates of Mycobacterium chelonae and Mycobacterium abscessus. Antimicrob Agents Chemother, 1996;40(7):1676–1681.
28. Hantz S, Garnier F, Peuchant O et al. Multilocus variable-number tandem-repeat analysis-confirmed emergence of a macrolide resistance-associated mutation in Mycoplasma pneumoniae during macrolide therapy for interstitial pneumonia in an immunocompromised child. J Clin Microbiol, 2012;50:3402–3405.
29. Lucier TS, Heitzman K, Liu SK, Hu PC. Transition mutations in the 23S rRNA of erythromycin-resistant isolates of Mycoplasma pneumoniae. Antimicrob Agents Chemother, 1995;39(12):2770–2773.
30. Chisholm SA, Dave J, Ison CA. High-level azithromycin resistance occurs in Neisseria gonorrhoeae as a result of a single point mutation in the 23S rRNA genes. Antimicrob Agents Chemother, 2010;54(9):3812–3816.
31. Ross JI, Eady EA, Cove JH et al. Clinical resistance to erythromycin and clindamycin in cutaneous propionibacteria isolated from acne patients is associated with mutations in 23S rRNA. Antimicrob Agents Chemother, 1997;41(5):1162–1165.
32. Marvig RL, Sondergaard MSR, Damkiær S et al. Mutations in 23S rRNA confer resistance against azithromycin in Pseudomonas aeruginosa. Antimicrob Agents Chemother, 2012;56(8):4519–4521.
33. Prunier AL, Malbruny B, Tandé D. Clinical isolates of Staphylococcus aureus with ribosomal mutations conferring resistance to macrolides. Antimicrob Agents Chemother, 2002;46(9):3054–3056.
34. Boumghar-Bourtchai L, Chardon H, Malbruny B et al. Resistance to macrolides by ribosomal mutation in clinical isolates of Turicella otitidis. Int J Antimicrob Agents, 2009;34(3):274–277.
35. Meier A, Kirschner P, Springer B et al. Identification of mutations in 23S rRNA gene of clarithromycin-resistant Mycobacterium intracellulare. Antimicrob Agents Chemother, 1994;38(2):381–384.
36. Vacher S, Menard A, Bernard E et al. Detection of mutations associated with macrolide resistance in thermophilic Campylobacter spp. by real-time PCR. Microb Drug Resist, 2005;11(1):40–47.
37. Matsuoka M, Narita M, Okazaki N et al. Characterization and molecular analysis of macrolide-resistant Mycoplasma pneumoniae clinical isolates obtained in Japan. Antimicrob Agents Chemother, 2004;48(12):4624–4630.
38. Wang G, Taylor DE. Site-specific mutations in the 23S rRNA gene of Helicobacter pylori confer two types of resistance to macrolide-lincosamide-streptogramin B antibiotics. Antimicrob Agents Chemother, 1998;42(8):1952–1958.
39. Sigmund CD, Ettayebi M, Morgan EA. Antibiotic resistance mutations in 16S and 23S ribosomal RNA genes of Escherichia coli. Nucleic Acids Res, 1984;12(11):4653–4663.
40. Chrisment D, Charron A, Cazanave C et al. Detection of macrolide resistance in Mycoplasma genitalium in France. J Antimicrob Chemother, 2012;67(11):2598–2601.
41. Zhen-Hua Z, De-Qiang H, Yong X et al. Characterization of 23S rRNA gene mutation in primary and secondary clarithromycin-resistant Helicobacter pylori strains from East China. Turk J Gastroenterol, 2013;24(1):5–9.
42. Stamm LV, Bergen HL. A point mutation associated with bacterial macrolide resistance is present in both 23S rRNA genes of an erythromycin-resistant Treponema pallidum clinical isolate. Antimicrob Agents Chemother, 2000;44(3):806–807.
43. Stamm LV, Parrish EA. In vitro activity of azithromycin and CP-63,956 against Treponema pallidum. J Antimicrob Chemother, 1990;25(A)11–14.
44. Pandori MW, Gordones C, Castro L et al. Detection of azithromycin resistance in Treponema pallidum by real-time PCR. Antimicrob Agents Chemother, 2007;51(9):3425–3430.
45. Chen CY, Chi KH, Pillay A et al. Detection of the A2058G and A2059G 23S rRNA gene point mutations associated with azithromycin resistance in Treponema pallidum by use of a TaqMan real-time multiplex PCR assay. J Clin Microbiol, 2013;51(3):908–913.
46. Flasarová M, Šmajs D, Matějková P et al. Molecular detection and subtyping of Treponema pallidum subsp. pallidum in clinical specimens. Epidemiol Mikrobiol Imunol, 2006;55(3):105–111.
47. Flasarová M, Pospíšilová P, Mikalová L et al. Sequencing-based molecular typing of Treponema pallidum strains in the Czech Republic: All identified genotypes are related to the sequence of the SS14 strain. Acta Derm Venereol, 2012;92(6):669–674.
48. Grillová L, Pětrošová H, Mikalová L et al. Molecular Typing of Treponema pallidum in the Czech Republic during 2011-2013: Increased Prevalence of Identified Genotypes and of Isolates Encoding Macrolide Resistance. J Clin Microbiol, 2014;52(10):3693–3700.
49. Marra CM, Colina AP, Godornes C et al. Antibiotic selection may contribute to increases in macrolide-resistant Treponema pallidum. J Infect Dis, 2006;194(12):1771–1773.
50. Grimes M, Sahi SK, Godornes BC et al. Two mutations associated with macrolide resistance in Treponema pallidum: Increasing prevalence and correlation with molecular strain type in Seattle, Washington. Sex Transm Dis, 2012;39(12):954–958.
51. Chen XS, Yin YP, Wei WH et al. High prevalence of azithromycin resistance to Treponema pallidum in geographically different areas in China. Clin Microbiol Infect, 2013;19(10):975–979.
52. Xia HX, Buckley M, Keane CT et al. Clarithromycin resistance in Helicobacter pylori: prevalence in untreated dyspeptic patients and stability in vitro. J Antimicrob Chemother, 1996;37(2):473–481.
53. Alarcón T, Domingo D, Prieto N et al. Clarithromycin resistance stability in Helicobacter pylori: Influence of the MIC and type of mutation in the 23S rRNA. J Antimicrob Chemother, 2000;46(4):613–616.
54. Wolter N, Smith AM, Farrell DJ et al. Heterogeneous macrolide resistance and gene conversion in the pneumococcus. Antimicrob Agents Chemother, 2006;50(1):359–361.
55. Binet R, Bowlin AK, Maurelli AT et al. Impact of azithromycin resistance mutations on the virulence and fitness of Chlamydia caviae in guinea pigs. Antimicrob Agents Chemother, 2010;54(3):1094–1101.
56. Read P, Jeoffreys N, Tagg K et al. Azithromycin resistant syphilis-causing strains in Sydney: Prevalence and risk factors. J Clin Microbiol, 2014;52(8):2776–2781.
57. Li Z, Hou J, Zheng R et al. Two mutations associated with macrolide resistance in Treponema pallidum in Shandong, China. J Clin Microbiol, 2013;51(12):4270–4271.
58. Su JR, Pillay A, Hook EW et al. Prevalence of the 23S rRNA A2058G point mutation and molecular subtypes in Treponema pallidum in the United States, 2007 to 2009. Sex Transm Dis, 2012;39(10):794–798.
59. Muldoon EG, Walsh A, Crowley B et al. Treponema pallidum azithromycin resistance in Dublin, Ireland. Sex Transm Dis, 2012;39(10):784–786.
60. Tipple C, McClure MO, Taylor GP. High prevalence of macrolide resistant Treponema pallidum strains in a London centre. Sex Transm Infect, 2011;87(6):486–488.
61. Martin IE, Tsang RSW, Sutherland K et al. Molecular typing of Treponema pallidum strains in western Canada: Predominance of 14d subtypes. Sex Transm Dis, 2010;37(9):544–548.
62. Müller EE, Paz-Bailey G, Lewis DA. Macrolide resistance testing and molecular subtyping of Treponema pallidum strains from southern Africa. Sex Transm Infect, 2012;88(6):470–474.
63. Wu BR, Yang CJ, Tsai MS et al. Multicentre surveillance of prevalence of the 23S rRNA A2058G and A2059G point mutations and molecular subtypes of Treponema pallidum in Taiwan, 2009–2013. Clin Microbiol Infect, 2014;20(8):802–807.
64. Van Damme K, Behets F, Ravelomanana N et al. Evaluation of azithromycin resistance in Treponema pallidum specimens from Madagascar. Sex Transm Dis, 2009;36(12):775–776.
65. Morshed MG, Jones HD. Treponema pallidum macrolide resistance in BC. CMAJ, 2004; 174(3):349.
66. Martin IE, Gu W, Yang Y et al. Macrolide resistance and molecular types of Treponema pallidum causing primary syphilis in Shanghai, China. Clin Infect Dis, 2009;49(4):515–521.
67. Wu H, Chang SY, Lee NY et al. Evaluation of macrolide resistance and enhanced molecular typing of Treponema pallidum in patients with syphilis in Taiwan: A prospective multicenter study. J Clin Microbiol, 2012;50(7):2299–2304.
68. Katz KA, Pillay A, Ahrens K et al. Molecular epidemiology of syphilis, San Francisco, 2004-2007. Sex Transm Dis, 2010;37(10):660–663.
69. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines. MMWR, 1982;31(2):33–60.
70. Centers for Disease Control and Prevention. Sexually Transmitted Diseases Treatment Guidelines. MMWR, 1989;38(8):1–43.
71. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines. MMWR, 1993;42(14):1–102.
72. Centers for Disease Control and Prevention. Guidelines for treatment of sexually transmitted diseases. MMWR, 1998;47(1):1–111.
73. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines. MMWR, 2002;51(6):1–78.
74. Centers for disease control and Prevention. Sexually transmitted diseases treatment guidelines. MMWR, 2006;55(11):1–94.
75. Workowski KA, Berman S. Sexually transmitted diseases treatment guidelines. MMWR, 2010;59(12):1–110.
76. Wu BR, Liu WC, Wu PY et al. Surveillance study of Treponema pallidum harbouring tetracycline resistance mutations in patients with syphilis. Int J Antimicrob Agents, 2014;44(4):370–372.
Labels
Hygiene and epidemiology Medical virology Clinical microbiologyArticle was published in
Epidemiology, Microbiology, Immunology
2015 Issue 1
Most read in this issue
- Macrolide resistance in Treponema pallidum subsp. pallidum in the Czech Republic and in other countries
- Contribution of the detection of IgA antibodies to the laboratory diagnosis of mumps in the population with a high vaccination coverage
- A case of tuberculous meningitis associated with persistently reduced CD4+ T lymphocyte counts
- Minimum inhibitory concentrations of erythromycin and other antibiotics for Czech strains of Bordetella pertussis