Resistance monitoring working group: Resistance to erythromycin, ciprofloxacin, and tetracycline in human isolates of Campylobacter spp. in the Czech Republic tested by the EUCAST standard method

Czech version

Authors: H. Žemličková ¹; V. Jakubů ¹; M. Marejková ²; P. Urbášková ¹
Authors‘ workplace: Národní referenční laboratoř pro antibiotika, Státní zdravotní ústav, Praha ¹; Národní referenční laboratoř pro E. coli a shigely, Státní zdravotní ústav, Praha ²
Published in: Epidemiol. Mikrobiol. Imunol. 63, 2014, č. 3, s. 184-190
Category: Review articles, original papers, case report

*Pracovní skupina pro monitorování rezistence

Overview

Study aim:
To determine the frequency of Campylobacter spp. isolated from humans in the Czech Republic and to test their susceptibility to antimicrobials commonly used to treat campylobacteriosis by the standard EUCAST method.

Material and methods:
Consecutive Campylobacter isolates recovered from clinical specimens in 49 microbiological laboratories within one month in 2013 were identified using matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry (MALDI-TOF MS). Susceptibility to erythromycin, ciprofloxacin, and tetracycline was tested by the microdilution method and the results were interpreted based on the EUCAST clinical breakpoints to differentiate between susceptible and resistant strains.

Results:
Of the study set of 769 Campylobacter spp. strains, 90.1 % were assigned to C. jejuni, 9.8 % to C. coli, and a single strain to C. fetus (0.1 %). Except one blood isolate of C. jejuni, all other isolates were recovered from the stool. Ciprofloxacin resistance (MIC > 0.5 mg/l) was detected in 61.9 % strains of C. jejuni and in 72.0 % strains of C. coli, tetracycline resistance (MIC > 2 mg/l) was detected in 32.0 % of strains of both species, and erythromycin resistance was found in 0.3 % of strains of C. jejuni (MIC > 8 mg/l) and in 2.7 % of strains of C. coli (MIC > 4 mg/l). A C. coli strain was multidrug resistant (i.e. resistant to all three antimicrobials tested).

Conclusions:
Despite the fact that most Campylobacter infections in humans cure on their own, the resistance of the causative strains to the antimicrobials of choice and alternative agents needs to be studied because of its relevance to the treatment of severe cases that require antibiotics. Resistance to macrolides was found rather infrequently in this study in both C. jejuni (0.1 %) and C. coli (2.7 %) strains. Nevertheless, alarming is ciprofloxacin resistance confirmed in 61.9 % of C. jejuni strains and 72.0 % C. coli strains. As the species C. coli is more often resistant to antimicrobials than C. jejuni and ciprofloxacin along with other fluoroquinolones is commonly used to treat severe food-borne and generalized infections, it is crucial to identify the Campylobacter strains to the species level and to test their susceptibility to relevant antibiotics by a valid and reproducible method to be able to provide an effective therapy.

Keywords:
Campylobacter spp. – antimicrobial resistence – microdilution method – EUCAST breakpoints

Sources

1. Vybrané infekční nemoci v ČR v letech 2004-2013. Zprávy Centra epidemiologie a mikrobiologie 2013;22:392–393. (dostupné také na http://www.szu.cz/publikace/data/vybrane-infekcni-nemoci-v-cr-v-letech-2003-2012-absolutne).

2. Blaser MJ, Taylor DN, Feldman RA. Epidemiology of Campylobacter jejuni infections. Epidemiol Rev, 1983;5:157–176.

3. Pigrau C, Bartolome R, Almirante B, et al. Bacteremia due to Campylobacter species: clinical findings and antimicrobial susceptibility patterns. Clin Infect Dis, 1997;25:1414–1420.

4. Taylor DN, Echeverria P, Pitarangsi C, et al. The influence of immunity and strain characteristics on the epidemiology of campylobacteriosis. J Clin Microbiol, 1988;26:863–868.

5. Allos BM, Blaser MJ. Campylobacter jejuni and related species. In: GL Mandell, JE Bennett, R Dolin (eds.). Mandell, Douglas and Bennett´s principles and practice of infectious diseases, Elsevier, 2010.

6. Ternhag A, Asikainen T, Giesecke J, et al. A meta-analysis on the effects of antibiotic treatment on duration of symptoms caused by infection with Campylobacter species. Clin Infect Dis, 2007;44:696–700.

7. Centers for Disease Control and Prevention. Campylobacter. General Information. Dostupné na: http://www.cdc.gov/nczved/divisions/dfbmd/diseases/campylobacter/

8. Bessède E, Solecki O, Sifré E, et al. Identification of Campylobacter species and related organisms by matrix assisted laser desorption ionization–time of flight (MALDI-TOF) mass spectrometry. Clin Microbiol Infect, 2011;17:1735–1739.

9. Urbášková, P. Rezistence bakterií k antibiotikům. Vybrané metody. Trios 1998.

10. European Committee on Antimicrobial Susceptibility Testing. Preparation of MH plates and broth (v.3,0, 2013). Dostupné na: http://www.eucast.org/antimicrobial_susceptibility_testing/media_preparation/

11. European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Dostupné na: http://www.eucast.org/clinical_breakpoints/

12. Lastovica AJ, Skirrow MB. Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. coli. In: I. Nachmkin and M. J. Blaser (ed.). Campylobacter, 2nd ed. American Society for Microbiology, Washington, DC; 2000: 89–120.

13. McNulty CA. The treatment of Campylobacter infections in man. J Antimicrob Chemother, 1987;19:281–284.

14. Vanhoof R, Gordts B, Dierickx R, et al. Bacteriostatic and bactericidal activities of 24 antimicrobial agents against Campylobacter fetus subsp. jejuni. Antimicrob Agents Chemother, 1980;18:118–121.

15. Fliegelman RM, Petrak RM, Goodman LJ, Segreti J, Trenholme GM, Kaplan RL. Comparative in vitro activities of twelve antimicrobial agents against Campylobacter species. Antimicrob Agents Chemother, 1985;27:429–30.

16. Lariviere LA, Gaudreau CL, Turgeon FF. Susceptibility of clinical isolates Campylobacter jejuni to twenty-five antimicrobial agents. J Antimicrob Chemother, 1986;18:681–685.

17. Clinical and Laboratory Standards Institute. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria; approved guideline. CLSI Document M45-A. Clinical and Laboratory Standards Institute, USA, Pa, 2006.

18. Bardon J, Kolar M, Cekanova L, et al. Prevalence of Campylobacter jejuni and its resistance to antibiotics in poultry in the Czech Republic. Zoonoses Public Health, 2009;56:111–116.

19. Rautelin H, Renkonen OV, Kosunen TU. Emergence of fluorochinolone resistance in Campylobacter jejuni and Campylobacter coli in subjects in Finland. Antimicrob Agents Chemother, 1991;35:2065–2069.

20. Sjögren E, Kaijser B, Werner M. Antimicrobial susceptibilities of Campylobacter jejuni and Campylobacter coli isolated in Sweden: a 10-year follow-up report. Antimicrob Agents Chemother, 1992;36:2847–2849.

21. Engberg J, Aarestrup FM, Taylor DE, et al. Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerg Infect Dis, 2001;7:24–34.

22. Endtz HP, Ruijs GJ, van Klingeren B, et al. Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J Antimicrob Chemother, 1991;27:199–208.

23. Sáenz Y, Zarazaga M, Lantero M, et al. Antibiotic resistance in Campylobacter strains isolated from animals, foods, and humans in Spain in 1997-1998. Antimicrob Agents Chemother, 2000;44:267–271.

24. de Jong A, Thomas V, Simjee S, et al. Pan-European monitoring of susceptibility to human-use antimicrobial agents in enteric bacteria isolated from healthy food-producing animals. J Antimicrob Chemother, 2012;67:638–651.

25. Iovine NM, Blaser MJ. Antimicrobial resistance in Campylobacter [letter]. Emerg Infect Dis, 2004. Dostupné na: http://wwwnc.cdc.gov/eid/article/10/7/04-0580.htm

26. Piddock LJ, Ricci V, Pumbwe L, Everett MJ, Griggs DJ. Fluoroquinolone resistance in Campylobacter species from man and animals: detection of mutations in topoisomerase genes. J Antimicrob Chemother, 2003;51:19–26.

27. Charvalos E, Tselentis Y, Hamzehpour MM, Kohler T, Pechere JC. Evidence for an efflux pump in multidrug-resistant Campylobacter jejuni. Antimicrob Agents Chemother, 1995;39:2019–2022.

28. Lin J, Michel LO, Zhang Q. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob Agents Chemother, 2002;46:2124–2131.

29. Beilei G, McDermott PF, White DG, Meng J. Role of efflux pumps and topoisomerase mutations in fluoroquinolone resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother, 2005;49:3347–3354.

30. Price LB, Lackey LG, Vailes R, Silbergeld E. The persistence of fluoroquinolone-resistant Campylobacter in poultry production. Environ Health Perspect, 2007;115:1035–1039.

31. Adler-Mosca H, Lüthy-Hottenstein J, Martinetti Lucchini G, Burnens A, Altwegg M. Development of resistance to quinolones in five patients with campylobacteriosis treated with norfloxacin or ciprofloxacin. Eur J Clin Microbiol Infect Dis, 1991;10:953–957.

32. Caldwell DB, Wang Y, Lin J. Development, stability, and molecular mechanisms of macrolide resistance in Campylobacter jejuni. Antimicrob Agents Chemother, 2008;52:3947–3954.

33. Lethopolku M, Kotilainen P, Haanper-Heikkinen M, et al. Ribosomal mutations as the main cause of macrolide resistance in Campylobacter jejuni and Campylobacter coli. Antimicrob Agents Chemother, 2011;55:5939–5941.

34. Gibreel N, Wetsch M, Taylor DE. Contribution of the CmeABC efflux pump to macrolide and tetracycline resistance in Campylobacter jejuni. Antimicrob Agents Chemother, 2007;51:3212–3216.

35. Luangtongkum T, Shen Z, Seng VW, et al. Impaired fitness and transmission of macrolide-resistant Campylobacter jejuni in its natural host. Antimicrob Agents Chemother, 2012;56:1300–1308.

36. Lindow JC, Poly F, Tribble DR, et al. Caught in the act: in vivo development of macrolide resistance to Campylobacter jejuni infection. J Clin Microbiol, 2010;48:3012–3015.