Pefloxacin as a Surrogate Marker for Ciprofloxacin Resistance in Salmonella: Study from North India
Fluoroquinolones form the mainstay of therapy for the treatment of infections due to Salmonella enterica subsp. enterica. There is a complex interplay between several resistance mechanisms for quinolones and various fluoroquinolones discs, giving varying results, making detection and interpretation of fluoroquinolone resistance difficult. For detection of fluoroquinolone resistance in Salmonella ssp., we compared the use of pefloxacin and nalidixic acid discs as surrogate marker. Using MIC for ciprofloxacin as the gold standard, 43.5% of strains showed MIC as ≥1 μg/ml and were thus resistant to fluoroquinoloes. Based on the performance of nalidixic acid and pefloxacin discs as surrogate marker for ciprofloxacin resistance, both the discs could correctly detect all the resistant phenotypes; however, use of nalidixic acid disc showed false resistance in the majority of the sensitive phenotypes. We have also tested newer antimicrobial agents like cefixime, imipenem, tigecycline and azithromycin against Salmonella spp. Moreover, there was a comeback of susceptibility to older antimicrobials like ampicillin, chloramphenicol, and cotrimoxazole. We can also use cefixime, imipenem, tigecycline and azithromycin in the treatment of multidrug resistant S. typhi due to their high susceptibility.
[1] Asperilla MO, Smego RA, Scott LK. Quinolone antibiotics in the treatment of Salmonella infections. Rev Infect Dis 1990:12;73
[2] Harish BN, Menezes GA. Antimicrobial resistance in typhoidal salmonellae. Indian J Med Microbiol 2011; 29: 223-9.
[3] Rushdya AA, Mabroukb MI, Abu-Sefa FA, Kheiralla ZH, Adbel- All SM, Salehb NM. Contribution of different mechanisms to the resistance to fluoroquinolones in clinical isolates of Salmonella enterica. Braz J Infect Dis 2013; 17(4):431-7.
[4] Hopkins KL, Davies RH, Threlfall EJ. Mechanism of quinolone resistance in Escherichia coli and Salmonella: recent developments. Int J Antimicrobial Agents 2005:25 :358-73
[5] Ruiz J. Mechanisms of resistance to quinolone target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 2003; 51:1109-17.
[6] Soto SM, Ruiz J, Mendoa MC, Vila J. In-vitro fluoroquinolone- resistant mutants of Salmonella enterica serotype enteritis: analysis of mechanisms involved in resistance. Int J Antimicrob Agents 2003; 22:537-40
[7] Hopkins KL, Day M and Threlfall EJ. Plasmid mediated quinolone resistance in Salmonella enterica, United Kingdom. Emerg Infect Dis 2008:14(2); 340-2.
[8] Jacoby GA. Mechanisms of Resistance to Quinolones. Clinical Infectious Diseases 2005; 41: S120–6
[9] Parry CM, Thuy CT, Dongol S, Karkey A, Vinh, Ha. Suitable disc antimicrobial susceptibility breakpoints defining Salmonella enterica serovar typhi isolates with reduced susceptibility to fluroquinolones. Antimicrobial Agent Chemotherapy 2010 ;54 :5201-8.
[10] Komp Lindgren P, Karlsson A, Hughes D. Mutation rate and evolution of floroquinolones resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother 2003; 47:3222-22
[11] Crump JA, Barrett TJ, Nelson JT, Angulo FJ. Reevaluating floroquinolones breakpoints for Salmonella enterica serotype typhi and non typhoidal Salmonella. Clin Infect Dis 2003;37 :75-81.
[12] Skova R, Matuschekb E, Sjölund-Karlssonc M, Åhmanb J, Petersena A, Steggera M, Torpdahla M, Kahlmeterb G. Development of a Pefloxacin Disk Diffusion Method for Detection of Fluoroquinolone-resistant Salmonella enterica. J Clin Microbiol 2015 Aug 19. pii: JCM.01287-15.
[13] Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. CLSI document M100-S25 Clinical and laboratory standards institute, Wayne, Pennsylvania, USA.2015 35:3.
[14] World Health Organization. The diagnosis, treatment and prevention of typhoid fever. Geneva: World Health Organization. 2003 May:7.
[15] Perilla M, Ajello G, Bopp C, Elliott J, Facklam R. Manual for the laboratory identification and antimicrobial susceptibility testing of bacterial pathogens of public health importance in the developing world. Haemophilus influenzae Neisseria meningitidis Streptococcus pneumoniae Neisseria gonorrhoeae Salmonella serotype typhi Shigella and Vibrio cholerae. 2003.
[16] Testing ECoAS. Routine and extended internal quality control as recommended by EUCAST: Version; 2015.
[17] Choudhary A, Gopalakrishnan R, Senthur Nambi, Ramasubramanian V, Abdul Ghafur K & Thirunarayan M.A. Antimicrobial susceptibility of Salmonella enterica serovars in a tertiary care hospital in southern India. Ind J Med Res 2013; 137:800-802
[18] Bhattacharya SS, Das U, Choudhury BK. Occurrence & antibiogram of Salmonella typhi & S. paratyphi A isolated from Rourkela, Orissa. Indian J Med Res 2011:133; 431-3.
[19] Dutta S, Sur D, Manna B, Bhattacharya SK, Deen JL, Clemens JD. Rollback of Salmonella enterica serotype typhi resistance to chloramphenicol and other antimicrobials in Kolkata, India. Antimicrob Agents Chemother. 2005; 49:1662-3.
[20] Capoor MR, Nair D, Rawat D, Aggarwal P. Enteric fever perspective in India: Emergence of high level ciprofloxacin resistance and rising MICs to cephalosporins. J Med Microbiol 2007:56; 1131-2.
[21] Livermore DM. Tigecycline: what is it and where should it be used. J Antimicrob Agent 2005: 56; 611–14.
[22] Rai S, Jain S, Prasad KN, Ghoshal U, DholeTN. Rationale of azithromycin prescribing practices for enteric fever in India. Ind J Med Microbio 2012:30; 30-3.
[23] Gordillo ME, Singh KV, Murray BE. In vitro activity of azithromycin against bacterial enteric pathogens. Antimicrob Agents Chemother 1993; 37:1203-5.
[24] Metchock B. In-vitro activity of azithromycin compared with other macrolides and oral antibiotics against Salmonella typhi. J Antimicrob Chemother 1990; 25 Suppl A: 29-31.
[25] Chinh NT, Parry CM, ThilyN, Ha HD, Thong MX et al. A Randomized Controlled Comparison of Azithromycin and ofloxacin for Treatment of Multidrug-Resistant or Nalidixic Acid-Resistant Enteric Fever. Antimicrob Agent Chemother 2000; 44 (7):1855-9.
[26] Shah D. Role of azithromycin in enteric fever. Ind Pediatrics 2009; 46:51-2.
[1] Asperilla MO, Smego RA, Scott LK. Quinolone antibiotics in the treatment of Salmonella infections. Rev Infect Dis 1990:12;73
[2] Harish BN, Menezes GA. Antimicrobial resistance in typhoidal salmonellae. Indian J Med Microbiol 2011; 29: 223-9.
[3] Rushdya AA, Mabroukb MI, Abu-Sefa FA, Kheiralla ZH, Adbel- All SM, Salehb NM. Contribution of different mechanisms to the resistance to fluoroquinolones in clinical isolates of Salmonella enterica. Braz J Infect Dis 2013; 17(4):431-7.
[4] Hopkins KL, Davies RH, Threlfall EJ. Mechanism of quinolone resistance in Escherichia coli and Salmonella: recent developments. Int J Antimicrobial Agents 2005:25 :358-73
[5] Ruiz J. Mechanisms of resistance to quinolone target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 2003; 51:1109-17.
[6] Soto SM, Ruiz J, Mendoa MC, Vila J. In-vitro fluoroquinolone- resistant mutants of Salmonella enterica serotype enteritis: analysis of mechanisms involved in resistance. Int J Antimicrob Agents 2003; 22:537-40
[7] Hopkins KL, Day M and Threlfall EJ. Plasmid mediated quinolone resistance in Salmonella enterica, United Kingdom. Emerg Infect Dis 2008:14(2); 340-2.
[8] Jacoby GA. Mechanisms of Resistance to Quinolones. Clinical Infectious Diseases 2005; 41: S120–6
[9] Parry CM, Thuy CT, Dongol S, Karkey A, Vinh, Ha. Suitable disc antimicrobial susceptibility breakpoints defining Salmonella enterica serovar typhi isolates with reduced susceptibility to fluroquinolones. Antimicrobial Agent Chemotherapy 2010 ;54 :5201-8.
[10] Komp Lindgren P, Karlsson A, Hughes D. Mutation rate and evolution of floroquinolones resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother 2003; 47:3222-22
[11] Crump JA, Barrett TJ, Nelson JT, Angulo FJ. Reevaluating floroquinolones breakpoints for Salmonella enterica serotype typhi and non typhoidal Salmonella. Clin Infect Dis 2003;37 :75-81.
[12] Skova R, Matuschekb E, Sjölund-Karlssonc M, Åhmanb J, Petersena A, Steggera M, Torpdahla M, Kahlmeterb G. Development of a Pefloxacin Disk Diffusion Method for Detection of Fluoroquinolone-resistant Salmonella enterica. J Clin Microbiol 2015 Aug 19. pii: JCM.01287-15.
[13] Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. CLSI document M100-S25 Clinical and laboratory standards institute, Wayne, Pennsylvania, USA.2015 35:3.
[14] World Health Organization. The diagnosis, treatment and prevention of typhoid fever. Geneva: World Health Organization. 2003 May:7.
[15] Perilla M, Ajello G, Bopp C, Elliott J, Facklam R. Manual for the laboratory identification and antimicrobial susceptibility testing of bacterial pathogens of public health importance in the developing world. Haemophilus influenzae Neisseria meningitidis Streptococcus pneumoniae Neisseria gonorrhoeae Salmonella serotype typhi Shigella and Vibrio cholerae. 2003.
[16] Testing ECoAS. Routine and extended internal quality control as recommended by EUCAST: Version; 2015.
[17] Choudhary A, Gopalakrishnan R, Senthur Nambi, Ramasubramanian V, Abdul Ghafur K & Thirunarayan M.A. Antimicrobial susceptibility of Salmonella enterica serovars in a tertiary care hospital in southern India. Ind J Med Res 2013; 137:800-802
[18] Bhattacharya SS, Das U, Choudhury BK. Occurrence & antibiogram of Salmonella typhi & S. paratyphi A isolated from Rourkela, Orissa. Indian J Med Res 2011:133; 431-3.
[19] Dutta S, Sur D, Manna B, Bhattacharya SK, Deen JL, Clemens JD. Rollback of Salmonella enterica serotype typhi resistance to chloramphenicol and other antimicrobials in Kolkata, India. Antimicrob Agents Chemother. 2005; 49:1662-3.
[20] Capoor MR, Nair D, Rawat D, Aggarwal P. Enteric fever perspective in India: Emergence of high level ciprofloxacin resistance and rising MICs to cephalosporins. J Med Microbiol 2007:56; 1131-2.
[21] Livermore DM. Tigecycline: what is it and where should it be used. J Antimicrob Agent 2005: 56; 611–14.
[22] Rai S, Jain S, Prasad KN, Ghoshal U, DholeTN. Rationale of azithromycin prescribing practices for enteric fever in India. Ind J Med Microbio 2012:30; 30-3.
[23] Gordillo ME, Singh KV, Murray BE. In vitro activity of azithromycin against bacterial enteric pathogens. Antimicrob Agents Chemother 1993; 37:1203-5.
[24] Metchock B. In-vitro activity of azithromycin compared with other macrolides and oral antibiotics against Salmonella typhi. J Antimicrob Chemother 1990; 25 Suppl A: 29-31.
[25] Chinh NT, Parry CM, ThilyN, Ha HD, Thong MX et al. A Randomized Controlled Comparison of Azithromycin and ofloxacin for Treatment of Multidrug-Resistant or Nalidixic Acid-Resistant Enteric Fever. Antimicrob Agent Chemother 2000; 44 (7):1855-9.
[26] Shah D. Role of azithromycin in enteric fever. Ind Pediatrics 2009; 46:51-2.
@article{"International Journal of Medical, Medicine and Health Sciences:72978", author = "Varsha Gupta and Priya Datta and Gursimran Mohi and Jagdish Chander", title = "Pefloxacin as a Surrogate Marker for Ciprofloxacin Resistance in Salmonella: Study from North India", abstract = "Fluoroquinolones form the mainstay of therapy for the treatment of infections due to Salmonella enterica subsp. enterica. There is a complex interplay between several resistance mechanisms for quinolones and various fluoroquinolones discs, giving varying results, making detection and interpretation of fluoroquinolone resistance difficult. For detection of fluoroquinolone resistance in Salmonella ssp., we compared the use of pefloxacin and nalidixic acid discs as surrogate marker. Using MIC for ciprofloxacin as the gold standard, 43.5% of strains showed MIC as ≥1 μg/ml and were thus resistant to fluoroquinoloes. Based on the performance of nalidixic acid and pefloxacin discs as surrogate marker for ciprofloxacin resistance, both the discs could correctly detect all the resistant phenotypes; however, use of nalidixic acid disc showed false resistance in the majority of the sensitive phenotypes. We have also tested newer antimicrobial agents like cefixime, imipenem, tigecycline and azithromycin against Salmonella spp. Moreover, there was a comeback of susceptibility to older antimicrobials like ampicillin, chloramphenicol, and cotrimoxazole. We can also use cefixime, imipenem, tigecycline and azithromycin in the treatment of multidrug resistant S. typhi due to their high susceptibility.
", keywords = "Pefloxacin, salmonella, surrogate marker.", volume = "10", number = "5", pages = "272-4", }
