Abstract
The purpose of this study was to examine the rate and clinical consequences of nalidixic acid-resistant (NAR) isolates in travellers with enteric fever presenting to a hospital in a developed country. We retrospectively examined microbiologically confirmed cases of enteric fever in adult returned travellers over an 18-year period presenting to two tertiary referral hospitals in Melbourne, Australia. There were 59 cases of Salmonella typhi infection, 43 cases of S. paratyphi A infection and two cases of S. paratyphi B infection. Most patients reported recent travel to India (36%) or Indonesia (29%). NAR isolates were commonly encountered (41% of all isolates), particularly from India (75%), Pakistan (80%) and Bangladesh (60%). The number of NAR isolates increased progressively after 2003. Patients with NAR isolates had prolonged mean fever clearance time (5.6 vs. 3.3 days, P = 0.03) and prolonged hospital stay (7.9 vs. 5.7 days, P = 0.02) compared to non-resistant isolates. This represents the largest report of NAR enteric fever in returned travellers. NAR isolates predominate in cases of enteric fever from South Asia and result in prolonged fever clearance time and hospital stay. Empiric therapy with alternative antibiotics such as ceftriaxone or azithromycin should be considered in patients with suspected enteric fever from this region.
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References
Bhutta ZA (1996) Impact of age and drug resistance on mortality in typhoid fever. Arch Dis Child 75(3):214–217
Wain J, Hoa NT, Chinh NT, Vinh H, Everett MJ, Diep TS et al (1997) Quinolone-resistant Salmonella typhi in Viet Nam: molecular basis of resistance and clinical response to treatment. Clin Infect Dis 25(6):1404–1410
Renuka K, Kapil A, Kabra SK, Wig N, Das BK, Prasad VV et al (2004) Reduced susceptibility to ciprofloxacin and gyra gene mutation in North Indian strains of Salmonella enterica serotype Typhi and serotype Paratyphi A. Microb Drug Resist 10(2):146–153.
Kadhiravan T, Wig N, Kapil A, Kabra SK, Renuka K, Misra A (2005) Clinical outcomes in typhoid fever: adverse impact of infection with nalidixic acid-resistant Salmonella typhi. BMC Infect Dis 5(1):37
Crump JA, Kretsinger K, Gay K, Hoekstra RM, Vugia DJ, Hurd S et al (2008) Clinical response and outcome of infection with Salmonella enteric serotype Typhi with decreased susceptibility to fluoroquinolones: a United States FoodNet multicenter retrospective cohort study. Antimicrob Agents Chemother 52(4):1278–1284
Slinger R, Desjardins M, McCarthy AE, Ramotar K, Jessamine P, Guibord C et al (2004) Suboptimal clinical response to ciprofloxacin in patients with enteric fever due to Salmonella spp. with reduced fluoroquinolone susceptibility: a case series. BMC Infect Dis 4:36
Sood S, Kapil A, Dash N, Das BK, Goel V, Seth P (1999) Paratyphoid fever in India: an emerging problem. Emerg Infect Dis 5(3):483–484
Tankhiwale SS, Agrawal G, Jalgaonkar SV (2003) An unusually high occurrence of Salmonella enterica serotype Paratyphi A in patients with enteric fever. Indian J Med Res 117:10–12
Ochiai RL, Wang X, von Seidlein L, Yang J, Bhutta ZA, Bhattacharya SK et al (2005) Salmonella Paratyphi A rates, Asia. Emerg Infect Dis 11(11):1764–1766
Gupta SK, Medalla F, Omondi MW, Whichard JM, Fields PI, Gerner-Smidt P et al (2008) Laboratory-based surveillance of paratyphoid fever in the United States: travel and antimicrobial resistance. Clin Infect Dis 46(11):1656–1663
Maskey AP, Day JN, Phung QT, Thwaites GE, Campbell JI, Zimmerman M et al (2006) Salmonella enterica serovar Paratyphi A and S. enterica serovar Typhi cause indistinguishable clinical syndromes in Kathmandu, Nepal. Clin Infect Dis 42(9):1247–1253
Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F et al (2006) Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 43(9):1185–1193
Clinical and Laboratory Standards Institute (CLSI) Performance standards for antimicrobial susceptibility testing; fifteenth informational supplement. CLSI, Wayne, Pennsylvania, 2005:M100-S15
O’Brien DP, Leder K, Matchett E, Brown GV, Torresi J (2006) Illness in returned travelers and immigrants/refugees: the 6-year experience of two Australian infectious diseases units. J Travel Med 13(3):145–152
Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bull World Health Organ 82(5):346–353
Bhan MK, Bahl R, Bhatnagar S (2005) Typhoid and paratyphoid fever. Lancet 366(9487):749–762
Caumes E, Ehya N, Nguyen J, Bricaire F (2001) Typhoid and paratyphoid fever: a 10-year retrospective study of 41 cases in a Parisian hospital. J Travel Med 8(6):293–297
Brown L, Fielding J, Gregory J, Guy R, Higgins N, Klug G et al. Surveillance of notifiable infectious diseases in Victoria, 2005. In: Services DoH, ed.: Communicable Disease Control Unit, Rural & Regional Health and Aged Care Services 2007.
Basnyat B, Maskey AP, Zimmerman MD, Murdoch DR (2005) Enteric (typhoid) fever in travelers. Clin Infect Dis 41(10):1467–1472
Bhutta ZA (2006) Current concepts in the diagnosis and treatment of typhoid fever. BMJ 333(7558):78–82
Sen B, Dutta S, Sur D, Manna B, Deb AK, Bhattacharya SK et al (2007) Phage typing, biotyping & antimicrobial resistance profile of Salmonella enterica serotype Typhi from Kolkata. Indian J Med Res 125(5):685–688
Cooke FJ, Day M, Wain J, Ward LR, Threlfall EJ (2007) Cases of typhoid fever imported into England, Scotland and Wales (2000–2003). Trans R Soc Trop Med Hyg 101(4):398–404
Cooke FJ, Wain J (2004) The emergence of antibiotic resistance in typhoid fever. Travel Med Infect Dis 2(2):67–74
Centers for Disease Control and Prevention (CDC) (2004) National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Human Isolates Final Report. CDC, Atlanta, GA
Threlfall EJ, Day M, de Pinna E, Lewis H, Lawrence J (2006) Drug-resistant enteric fever in the UK. Lancet 367(9522):1576
Therapeutic Guidelines (2006) Therapeutic Guidelines: antibiotic, 13th edn. Therapeutic Guidelines Limited, Melbourne, Australia
Parry CM, Ho VA, Phuong le T, Bay PV, Lanh MN, Tung le T et al (2007) Randomized controlled comparison of ofloxacin, azithromycin, and an ofloxacin-azithromycin combination for treatment of multidrug-resistant and nalidixic acid-resistant typhoid fever. Antimicrob Agents Chemother 51(3):819–825
Frenck RW Jr, Mansour A, Nakhla I, Sultan Y, Putnam S, Wierzba T et al (2004) Short-course azithromycin for the treatment of uncomplicated typhoid fever in children and adolescents. Clin Infect Dis 38(7):951–957
Saha SK, Talukder SY, Islam M, Saha S (1999) A highly ceftriaxone-resistant Salmonella typhi in Bangladesh. Pediatr Infect Dis J 18(4):387
Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ (2002) Typhoid fever. N Engl J Med 347(22):1770–1782
Manchanda V, Bhalla P, Sethi M, Sharma VK (2006) Treatment of enteric fever in children on the basis of current trends of antimicrobial susceptibility of Salmonella enterica serovar typhi and paratyphi A. Indian J Med Microbiol 24(2):101–106
Kumar R, Gupta N; Shalini (2007) Multidrug-resistant typhoid fever. Indian J Pediatr 74(1):39–42
Ekdahl K, de Jong B, Andersson Y (2005) Risk of travel-associated typhoid and paratyphoid fevers in various regions. J Travel Med 12:197–204
Wilde H (2007) Enteric fever due to Salmonella typhi and paratyphi A: a neglected and emerging problem. Vaccine 25:5246–5247
Bodhidatta L, Taylor DN, Thisyakorn U, Echeverria P (1987) Control of typhoid fever in Bangkok, Thailand, by annual immunization of schoolchildren with parenteral typhoid vaccine. Rev Infect Dis 9(4):841–845
Australian Bureau of Statistics. Overseas Arrivals and Departures, 2006
Kapil A, Sood S, Reddaiah VP, Das B, Seth P (1997) Paratyphoid fever due to Salmonella enterica serotype Paratyphi A. Emerg Infect Dis 3(3):407
Provost S, Gagnon S, Lonergan G, Bui YG, Labbé AC (2006) Hepatitis A, typhoid and malaria among travelers—surveillance data from Québec (Canada). J Travel Med 13(4):219–226
Leder K, Black J, O’Brien D, Greenwood Z, Kain KC, Schwartz E et al (2004) Malaria in travelers: a review of the GeoSentinel surveillance network. Clin Infect Dis 39(8):1104–1112
Wilson ME, Weld LH, Boggild A, Keystone JS, Kain KC, von Sonnenburg F et al (2007) Fever in returned travelers: results from the GeoSentinel Surveillance Network. Clin Infect Dis 44(12):1560–1568
Basnyat B (2005) Typhoid and paratyphoid fever. Lancet 366(9497):1603
Walia M, Gaind R, Mehta R, Paul P, Aggarwal P, Kalaivani M (2005) Current perspectives of enteric fever: a hospital-based study from India. Ann Trop Paediatr 25(3):161–174
Kadhiravan T, Wig N, Renuka K, Kapil A, Kabra SK, Misra A (2008) Is nalidixic acid resistance linked to clinical virulence in Salmonella enterica serovar Typhi infections? J Med Microbiol 57(Pt 8):1046–1048
Acknowledgements
We acknowledge Elizabeth Matchett, Royal Microbiologic Hospital, Joan Pauling, Melbourne Diagnostic Unit, and Despina Kotsanas, Southern Health, for their contribution to the data collection.
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Hume, S., Schulz, T., Vinton, P. et al. Increasing rates and clinical consequences of nalidixic acid-resistant isolates causing enteric fever in returned travellers: an 18-year experience. Eur J Clin Microbiol Infect Dis 28, 963–970 (2009). https://doi.org/10.1007/s10096-009-0732-6
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DOI: https://doi.org/10.1007/s10096-009-0732-6