Travel Medicine and Infectious Disease
Volume 9, Issue 6 , Pages 263-277 , November 2011

Salmonella infections: An update on epidemiology, management, and prevention

  • Flor M. Sánchez-Vargas

      Affiliations

    • Department of Internal Medicine, Saint Francis Hospital, Evanston, IL, USA
  • ,
  • Maisam A. Abu-El-Haija

      Affiliations

    • Division of Pediatric Gastroenterology, University of Iowa Children’s Hospital, Iowa City, IA, USA
  • ,
  • Oscar G. Gómez-Duarte

      Affiliations

    • Division of Pediatric Infectious Diseases, University of Iowa Children’s Hospital, Iowa City, IA, USA
    • Corresponding Author InformationCorresponding author. Present address: Division of Pediatric Infectious Diseases, Vanderbilt University, D6201 MCN, 1161 21st Avenue South, Nashville, TN 37232-2581, USA. Tel.: +1 615 322 2250; fax: +1 615 343 9723.

Received 5 March 2011 ,Revised 30 September 2011 ,Accepted 3 November 2011.

References 

  1. Cunha BA. The death of Alexander the Great: malaria or typhoid fever?. Infect Dis Clin North Am. 2004;18(1):53–63
  2. Center for Disease Control (CDC) . Salmonella surveillance: annual summary. 2006;Available at: http://www.cdc.gov/ncidod/dbmd/phlisdata/salmtab/2006/SalmonellaIntroduction2006.pdf
  3. Kidgell C, Reichard U, Wain J, Linz B, Torpdahl M, Dougan G, et al. Salmonella typhi, the causative agent of typhoid fever, is approximately 50,000 years old. Infect Genet Evol. 2002;2(1):39–45
  4. August C, Konert J. Awarded the honorary chair for anatomy in Halle 100 years ago: Carl Joseph Eberth–discoverer of the typhus pathogen. Pathologe. 1993;14(4):234–236
  5. Papagrigorakis MJ, Yapijakis C, Synodinos PN, Baziotopoulou-Valavani E. DNA examination of ancient dental pulp incriminates typhoid fever as a probable cause of the Plague of Athens. Int J Infect Dis. 2006;10(3):206–214
  6. Wood M. We’ll say our goodbyes in Babylon. In: In the footsteps of Alexander the Great: a journey from Greece to Asia. Berkeley: University of California Press; 1997;p. 223–232
  7. Budd W. Typhoied fever: its nature, mode of spreading, and prevention. London: Longmans, Green, and Co; 1873;
  8. Sedgwick WT, Hazen A. Typhoid fever in Chicago. Eng News Am Rail J. 1892;1–21
  9. Woodward TE, Smadel JE, Ley HL, Green R, Mankikar DS. Preliminary report on the beneficial effect of chloromycetin in the treatment of typhoid fever. 1948. Wilderness Environ Med. 2004;15(3):218–220
  10. Hardy A. Salmonella: a continuing problem. Postgrad Med J. 2004;80(947):541–545
  11. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ. 2004;82(5):346–353
  12. Nguyen TQ, Reddy V, Sahl S, Kornstein L, Balter S. Importance of travel in domestically acquired typhoid fever infections: opportunities for prevention and early detection. J Immigr Minor Health. 2009;11(2):139–142
  13. Cooke FJ, Day M, Wain J, Ward LR, Threlfall EJ. Cases of typhoid fever imported into England, Scotland and Wales (2000–2003). Trans R Soc Trop Med Hyg. 2007;101(4):398–404
  14. Morris SK, Richardson SE, Sauve LJ, Ford-Jones EL, Jamieson F. Increasing fluoroquinolone resistance in Salmonella typhi in Ontario, 2002–2007. Am J Trop Med Hyg. 2009;80(6):1012–1013
  15. Gil Prieto R, Alejandre CG, Meca AA, Barrera VH, de Miguel AG. Epidemiology of hospital-treated Salmonella infection; data from a national cohort over a ten-year period. J Infect. 2009;58(3):175–181
  16. Meltzer E, Yossepowitch O, Sadik C, Dan M, Schwartz E. Epidemiology and clinical aspects of enteric fever in Israel. Am J Trop Med Hyg. 2006;74(4):540–545
  17. Ochiai RL, Acosta CJ, Danovaro-Holliday MC, Baiqing D, Bhattacharya SK, Agtini MD, et al. A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bull World Health Organ. 2008;86(4):260–268
  18. Crump JA, Mintz ED. Global trends in typhoid and paratyphoid fever. Clin Infect Dis. 2010;50(2):241–246
  19. Kothari A, Pruthi A, Chugh TD. The burden of enteric fever. J Infect Dev Ctries. 2008;2(4):253–259
  20. Mweu E, English M. Typhoid fever in children in Africa. Trop Med Int Health. 2008;13(4):532–540
  21. Linam WM, Gerber MA. Changing epidemiology and prevention of Salmonella infections. Pediatr Infect Dis J. 2007;26(8):747–748
  22. Fangtham M, Wilde H. Emergence of Salmonella paratyphi A as a major cause of enteric fever: need for early detection, preventive measures, and effective vaccines. J Travel Med. 2008;15(5):344–350
  23. Crump JA, Ram PK, Gupta SK, Miller MA, Mintz ED. Part I. Analysis of data gaps pertaining to Salmonella enterica serotype Typhi infections in low and medium human development index countries, 1984–2005. Epidemiol Infect. 2008;136(4):436–448
  24. Kariuki S. Typhoid fever in sub-Saharan Africa: challenges of diagnosis and management of infections. J Infect Dev Ctries. 2008;2(6):443–447
  25. Owais A, Sultana S, Zaman U, Rizvi A, Zaidi AKM. Incidence of typhoid bacteremia in infants and young children in southern coastal Pakistan. Pediatr Infect Dis J. 2010;29(11):1035–1039
  26. Kumar S, Rizvi M, Berry N. Rising prevalence of enteric fever due to multidrug-resistant Salmonella: an epidemiological study. J Med Microbiol. 2008;57(Pt 10):1247–1250
  27. Molloy A, Nair S, Cooke FJ, Wain J, Farrington M, Lehner PJ, et al. First report of Salmonella enterica serotype paratyphi A azithromycin resistance leading to treatment failure. J Clin Microbiol. 2010;48(12):4655–4657
  28. Zaki SA, Karande S. Multidrug-resistant typhoid fever: a review. J Infect Dev Ctries. 2011;5(5):324–337
  29. Chau TT, Campbell JI, Galindo CM, Van Minh Hoang N, Diep TS, Nga TTT, et al. Antimicrobial drug resistance of Salmonella enterica serovar typhi in asia and molecular mechanism of reduced susceptibility to the fluoroquinolones. Antimicrob Agents Chemother. 2007;51(12):4315–4323
  30. Chuang C-H, Su L-H, Perera J, Carlos C, Tan BH, Kumarasinghe G, et al. Surveillance of antimicrobial resistance of Salmonella enterica serotype Typhi in seven Asian countries. Epidemiol Infect. 2009;137(2):266–269
  31. Harish BN, Madhulika U, Parija SC. Isolated high-level ciprofloxacin resistance in Salmonella enterica subsp. enterica serotype Paratyphi A. J Med Microbiol. 2004;53(Pt 8):819
  32. Hasan R, Zafar A, Abbas Z, Mahraj V, Malik F, Zaidi A. Antibiotic resistance among Salmonella enterica serovars Typhi and Paratyphi A in Pakistan (2001–2006). J Infect Dev Ctries. 2008;2(4):289–294
  33. Lynch MF, Blanton EM, Bulens S, Polyak C, Vojdani J, Stevenson J, et al. Typhoid fever in the United States, 1999-2006. J Am Med Assoc. 2009;302(8):859–865
  34. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50(6):882–889
  35. Su L-H, Chiu C-H, Wu T-L, Chu C, Chia J-H, Kuo A-J, et al. Molecular epidemiology of Salmonella enterica serovar Enteritidis isolated in Taiwan. Microbiol Immunol. 2002;46(12):833–840
  36. Westrell T, Ciampa N, Boelaert F, Helwigh B, Korsgaard H, Chríel M, et al. Zoonotic infections in Europe in 2007: a summary of the EFSA-ECDC annual report. Euro Surveill. 2009;14(3):Available at: http://www.ncbi.nlm.nih.gov/pubmed/19161723[accessed 28.09.11]
  37. Galanis E, Lo Fo Wong DMA, Patrick ME, Binsztein N, Cieslik A, Chalermchikit T, et al. Web-based surveillance and global Salmonella distribution, 2000–2002. Emerging Infect Dis. 2006;12(3):381–388
  38. Crump JA, Ramadhani HO, Morrissey AB, Saganda W, Mwako MS, Yang L-Y, et al. Invasive bacterial and fungal infections among hospitalized HIV-infected and HIV-uninfected adults and adolescents in northern Tanzania. Clin Infect Dis. 2011;52(3):341–348
  39. Mandomando I, Macete E, Sigaúque B, Morais L, Quintó L, Sacarlal J, et al. Invasive non-typhoidal Salmonella in Mozambican children. Trop Med Int Health. 2009;14(12):1467–1474
  40. Morpeth SC, Ramadhani HO, Crump JA. Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis. 2009;49(4):606–611
  41. Dhanoa A, Fatt QK. Non-typhoidal Salmonella bacteraemia: epidemiology, clinical characteristics and its’ association with severe immunosuppression. Ann Clin Microbiol Antimicrob. 2009;8:15
  42. Khan MI, Ochiai RL, von Seidlein L, Dong B, Bhattacharya SK, Agtini MD, et al. Non-typhoidal Salmonella rates in febrile children at sites in five Asian countries. Trop Med Int Health. 2010;15(8):960–963
  43. Weinberger M, Keller N. Recent trends in the epidemiology of non-typhoid Salmonella and antimicrobial resistance: the Israeli experience and worldwide review. Curr Opin Infect Dis. 2005;18(6):513–521
  44. Laupland KB, Schønheyder HC, Kennedy KJ, Lyytikäinen O, Valiquette L, Galbraith J, et al. Salmonella enterica bacteraemia: a multi-national population-based cohort study. BMC Infect Dis. 2010;10:95
  45. Center for Disease Control (CDC) . Vital signs: incidence and trends of infection with pathogens transmitted commonly through food–foodborne diseases active surveillance network, 10 U.S. sites, 1996–2010. MMWR Morb Mortal Wkly Rep. 2011;60(22):749–755
  46. Barton Behravesh C, Jones TF, Vugia DJ, Long C, Marcus R, Smith K, et al. Deaths associated with bacterial pathogens transmitted commonly through food: foodborne diseases active surveillance network (FoodNet), 1996–2005. J Infect Dis. 2011;204(2):263–267
  47. Younus M, Hartwick E, Siddiqi AA, Wilkins M, Davies HD, Rahbar M, et al. The role of neighborhood level socioeconomic characteristics in Salmonella infections in Michigan (1997–2007): assessment using geographic information system. Int J Health Geogr. 2007;6(56):
  48. Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S, et al. Invasive Salmonella infections in the United States, FoodNet, 1996–1999: incidence, serotype distribution, and outcome. Clin Infect Dis. 2004;38(Suppl. 3):S149–156
  49. Lynch M, Painter J, Woodruff R, Braden C. Surveillance for foodborne-disease outbreaks–United States, 1998–2002. MMWR Surveill Summ. 2006;55(10):1–42
  50. Center for Disease Control (CDC). CDC – Outbreak of Enteritidis Infections – December 2, 2010-Salmonella. Available at: http://www.cdc.gov/salmonella/enteritidis/. [accessed 28.09.11].
  51. Center for Disease Control (CDC) . Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food–10 States, United States, 2005. MMWR Morb Mortal Wkly Rep. 2006;55(14):392–395
  52. Center for Disease Control (CDC) . Multistate outbreak of human Salmonella infections associated with exposure to turtles–United States, 2007–2008. MMWR Morb Mortal Wkly Rep. 2008;57(3):69–72
  53. Fisher IST. Dramatic shift in the epidemiology of Salmonella enterica serotype Enteritidis phage types in western Europe, 1998–2003 – results from the Enter-net international salmonella database. Euro Surveill. 2004;9(11):43–45
  54. Stevens MP, Humphrey TJ, Maskell DJ. Molecular insights into farm animal and zoonotic Salmonella infections. Philos Trans R Soc Lond, B, Biol Sci. 2009;364(1530):2709–2723
  55. Dione MM, Ikumapayi UN, Saha D, Mohammed NI, Geerts S, Ieven M, et al. Clonal differences between Non-Typhoidal Salmonella (NTS) recovered from children and animals living in close contact in the Gambia. PLoS Negl Trop Dis. 2011;5(5):e1148
  56. Kikuvi GM, Ombui JN, Mitema ES. Serotypes and antimicrobial resistance profiles of Salmonella isolates from pigs at slaughter in Kenya. J Infect Dev Ctries. 2010;4(4):243–248
  57. Jardine C, Reid-Smith RJ, Janecko N, Allan M, McEwen SA. Salmonella in raccoons (Procyon lotor) in southern Ontario, Canada. J Wildl Dis. 2011;47(2):344–351
  58. Siembieda JL, Miller WA, Byrne BA, Ziccardi MH, Anderson N, Chouicha N, et al. Zoonotic pathogens isolated from wild animals and environmental samples at two California wildlife hospitals. J Am Vet Med Assoc. 2011;238(6):773–783
  59. Swanson SJ, Snider C, Braden CR, Boxrud D, Wünschmann A, Rudroff JA, et al. Multidrug-resistant Salmonella enterica serotype Typhimurium associated with pet rodents. N Engl J Med. 2007;356(1):21–28
  60. Wacheck S, Fredriksson-Ahomaa M, König M, Stolle A, Stephan R. Wild boars as an important reservoir for foodborne pathogens. Foodborne Pathog Dis. 2010;7(3):307–312
  61. Aiken AM, Lane C, Adak GK. Risk of Salmonella infection with exposure to reptiles in England, 2004–2007. Euro Surveill. 2010;15(22):19581
  62. Mermin J, Hutwagner L, Vugia D, Shallow S, Daily P, Bender J, et al. Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. Clin Infect Dis. 2004;38(Suppl. 3):S253–261
  63. Helms M, Ethelberg S, Mølbak K. International Salmonella Typhimurium DT104 infections, 1992–2001. Emerging Infect Dis. 2005;11(6):859–867
  64. Sjölund-Karlsson M, Rickert R, Matar C, Pecic G, Howie RL, Joyce K, et al. Salmonella isolates with decreased susceptibility to extended-spectrum cephalosporins in the United States. Foodborne Pathog Dis. 2010;7(12):1503–1509
  65. Crump JA, Medalla FM, Joyce KW, Krueger AL, Hoekstra RM, Whichard JM, et al. Antimicrobial resistance among invasive nontyphoidal Salmonella enterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996 to 2007. Antimicrob Agents Chemother. 2011;55(3):1148–1154
  66. Meakins S, Fisher IST, Berghold C, Gerner-Smidt P, Tschäpe H, Cormican M, et al. Antimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000–2004: a report from the Enter-net International Surveillance Network. Microb Drug Resist. 2008;14(1):31–35
  67. Akinyemi KO, Bamiro BS, Coker AO. Salmonellosis in Lagos, Nigeria: incidence of Plasmodium falciparum-associated co-infection, patterns of antimicrobial resistance, and emergence of reduced susceptibility to fluoroquinolones. J Health Popul Nutr. 2007;25(3):351–358
  68. Jabeen K, Zafar A, Irfan S, Khan E, Mehraj V, Hasan R. Increase in isolation of extended spectrum beta lactamase producing multidrug resistant non typhoidal Salmonellae in Pakistan. BMC Infect Dis. 2010;10:101
  69. Kruger T, Szabo D, Keddy KH, Deeley K, Marsh JW, Hujer AM, et al. Infections with nontyphoidal Salmonella species producing TEM-63 or a novel TEM enzyme, TEM-131, in South Africa. Antimicrob Agents Chemother. 2004;48(11):4263–4270
  70. Ran L, Wu S, Gao Y, Zhang X, Feng Z, Wang Z, et al. Laboratory-based surveillance of nontyphoidal Salmonella infections in China. Foodborne Pathog Dis. 2011;8(8):921–927
  71. Hansen-Wester I, Stecher B, Hensel M. Type III secretion of Salmonella enterica serovar Typhimurium translocated effectors and SseFG. Infect Immun. 2002;70(3):1403–1409
  72. Takaya A, Suzuki M, Matsui H, Tomoyasu T, Sashinami H, Nakane A, et al. Lon, a stress-induced ATP-dependent protease, is critically important for systemic Salmonella enterica serovar typhimurium infection of mice. Infect Immun. 2003;71(2):690–696
  73. Gerlach RG, Jäckel D, Geymeier N, Hensel M. Salmonella pathogenicity island 4-mediated adhesion is coregulated with invasion genes in Salmonella enterica. Infect Immun. 2007;75(10):4697–4709
  74. Grassl GA, Finlay BB. Pathogenesis of enteric Salmonella infections. Curr Opin Gastroenterol. 2008;24(1):22–26
  75. Dieye Y, Dyszel JL, Kader R, Ahmer BMM. Systematic analysis of the regulation of type three secreted effectors in Salmonella enterica serovar Typhimurium. BMC Microbiol. 2007;7:3
  76. Galán JE, Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature. 2006;444(7119):567–573
  77. Winnen B, Schlumberger MC, Sturm A, Schüpbach K, Siebenmann S, Jenny P, et al. Hierarchical effector protein transport by the Salmonella Typhimurium SPI-1 type III secretion system. PLoS ONE. 2008;3(5):e2178
  78. Haraga A, Ohlson MB, Miller SI. Salmonellae interplay with host cells. Nat Rev Microbiol. 2008;6(1):53–66
  79. Kichi Uchiya, Groisman EA, Nikai T. Involvement of Salmonella pathogenicity island 2 in the up-regulation of interleukin-10 expression in macrophages: role of protein kinase A signal pathway. Infect Immun. 2004;72(4):1964–1973
  80. Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M. The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun. 1999;67(4):1560–1568
  81. Prost LR, Miller SI. The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Microbiol. 2008;10(3):576–582
  82. Prost LR, Sanowar S, Miller SI. Salmonella sensing of anti-microbial mechanisms to promote survival within macrophages. Immunol Rev. 2007;219:55–65
  83. Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol. 2007;85(2):112–118
  84. Coburn B, Li Y, Owen D, Vallance BA, Finlay BB. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun. 2005;73(6):3219–3227
  85. Raupach B, Kurth N, Pfeffer K, Kaufmann SHE. Salmonella typhimurium strains carrying independent mutations display similar virulence phenotypes yet are controlled by distinct host defense mechanisms. J Immunol. 2003;170(12):6133–6140
  86. Bakowski MA, Braun V, Brumell JH. Salmonella-containing vacuoles: directing traffic and nesting to grow. Traffic. 2008;9(12):2022–2031
  87. Fields PI, Swanson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U.S.A. 1986;83(14):5189–5193
  88. Ramsden AE, Holden DW, Mota LJ. Membrane dynamics and spatial distribution of Salmonella-containing vacuoles. Trends Microbiol. 2007;15(11):516–524
  89. Fink RC, Evans MR, Porwollik S, Vazquez-Torres A, Jones-Carson J, Troxell B, et al. FNR is a global regulator of virulence and anaerobic metabolism in Salmonella enterica serovar Typhimurium (ATCC 14028s). J Bacteriol. 2007;189(6):2262–2273
  90. Monack DM, Mueller A, Falkow S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol. 2004;2(9):747–765
  91. Wyant TL, Tanner MK, Sztein MB. Potent immunoregulatory effects of Salmonella typhi flagella on antigenic stimulation of human peripheral blood mononuclear cells. Infect Immun. 1999;67(3):1338–1346
  92. Osler W. Typhoid fever. In: The principles and practice of medicine. 1st ed.. New York: Appleton and Company; 1892;p. 2–39
  93. Connor BA, Schwartz E. Typhoid and paratyphoid fever in travellers. Lancet Infect Dis. 2005;5(10):623–628
  94. Bhan MK, Bahl R, Bhatnagar S. Typhoid and paratyphoid fever. Lancet. 2005;366(9487):749–762
  95. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ. Typhoid fever. N Engl J Med. 2002;347(22):1770–1782
  96. Patel TA, Armstrong M, Morris-Jones SD, Wright SG, Doherty T. Imported enteric fever: case series from the hospital for tropical diseases, London, United Kingdom. Am J Trop Med Hyg. 2010;82(6):1121–1126
  97. Pegues DA, Ohl ME, Miller SI. Salmonella species, including Salmonell Typhi. In: Mandell, Douglas and Bennett’s principles and practice of infectious diseases. 6th ed.. New York [u.a.]: Churchill Livingstone; 2005;
  98. Pohan HT. Clinical and laboratory manifestations of typhoid fever at Persahabatan Hospital, Jakarta. Acta Med Indones. 2004;36(2):78–83
  99. Thielman NM, Guerrant RL. Clinical practice. Acute infectious diarrhea. N Engl J Med. 2004;350(1):38–47
  100. Thisyakorn U, Mansuwan P, Taylor DN. Typhoid and paratyphoid fever in 192 hospitalized children in Thailand. Am J Dis Child. 1987;141(8):862–865
  101. Kuvandik C, Karaoglan I, Namiduru M, Baydar I. Predictive value of clinical and laboratory findings in the diagnosis of the enteric fever. New Microbiol. 2009;32(1):25–30
  102. Box CR. Typhoid fever: its chief complications. Br Med J. 1935;1(3871):538–540
  103. Feldman LS. Salmonella septic sacroiliitis: case report and review. Pediatr Infect Dis J. 2006;25(2):187–189
  104. Naithani R, Rai S, Choudhry VP. Septic arthritis of hip in a neutropenic child caused by Salmonella typhi. J Pediatr Hematol Oncol. 2008;30(2):182–184
  105. Saphra I, Winter JW. Clinical manifestations of salmonellosis in man; an evaluation of 7779 human infections identified at the New York Salmonella Center. N Engl J Med. 1957;256(24):1128–1134
  106. Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis. 2001;32(2):263–269
  107. Crump JA, Kretsinger K, Gay K, Hoekstra RM, Vugia DJ, Hurd S, et al. Clinical response and outcome of infection with Salmonella enterica serotype Typhi with decreased susceptibility to fluoroquinolones: a United States foodnet multicenter retrospective cohort study. Antimicrob Agents Chemother. 2008;52(4):1278–1284
  108. Gordon MA. Salmonella infections in immunocompromised adults. J Infect. 2008;56(6):413–422
  109. Fisker N, Vinding K, Mølbak K, Hornstrup MK. Clinical review of nontyphoid Salmonella infections from 1991 to 1999 in a Danish county. Clin Infect Dis. 2003;37(4):e47–52
  110. Huang DB, DuPont HL. Problem pathogens: extra-intestinal complications of Salmonella enterica serotype Typhi infection. Lancet Infect Dis. 2005;5(6):341–348
  111. Zaidenstein R, Peretz C, Nissan I, Reisfeld A, Yaron S, Agmon V, et al. The epidemiology of extraintestinal non-typhoid Salmonella in Israel: the effects of patients’ age and sex. Eur J Clin Microbiol Infect Dis. 2010;29(9):1103–1109
  112. Shimoni Z, Pitlik S, Leibovici L, Samra Z, Konigsberger H, Drucker M, et al. Nontyphoid Salmonella bacteremia: age-related differences in clinical presentation, bacteriology, and outcome. Clin Infect Dis. 1999;28(4):822–827
  113. Arii J, Tanabe Y, Miyake M, Mukai T, Matsuzaki M, Niinomi N, et al. Clinical and pathologic characteristics of nontyphoidal salmonella encephalopathy. Neurology. 2002;58(11):1641–1645
  114. Sirinavin S, Chiemchanya S, Vorachit M. Systemic nontyphoidal Salmonella infection in normal infants in Thailand. Pediatr Infect Dis J. 2001;20(6):581–587
  115. Nielsen H, Gradel KO, Schønheyder HC. High incidence of intravascular focus in nontyphoid Salmonella bacteremia in the age group above 50 years: a population-based study. Acta Pathol Microbiol Immunol. 2006;114(9):641–645
  116. Kankwatira AM, Mwafulirwa GAK, Gordon MA. Non-typhoidal salmonella bacteraemia–an under-recognized feature of AIDS in African adults. Trop Doct. 2004;34(4):198–200
  117. Larsen IK, Gradel KO, Helms M, Hornstrup MK, Jürgens G, Mens H, et al. Non-typhoidal Salmonella and Campylobacter infections among HIV-positive patients in Denmark. Scand J Infect Dis. 2011;43(1):3–7
  118. Gordon MA, Banda HT, Gondwe M, Gordon SB, Boeree MJ, Walsh AL, et al. Non-typhoidal salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS. 2002;16(12):1633–1641
  119. Feglo PK, Frimpong EH, Essel-Ahun M. Salmonellae carrier status of food vendors in Kumasi, Ghana. East Afr Med J. 2004;81(7):358–361
  120. Gonzalez-Escobedo G, Marshall JM, Gunn JS. Chronic and acute infection of the gall bladder by Salmonella Typhi: understanding the carrier state. Nat Rev Microbiol. 2011;9(1):9–14
  121. Levine MM, Black RE, Lanata C. Precise estimation of the numbers of chronic carriers of Salmonella typhi in Santiago, Chile, an endemic area. J Infect Dis. 1982;146(6):724–726
  122. Nath G, Singh H, Shukla VK. Chronic typhoid carriage and carcinoma of the gallbladder. Eur J Cancer Prev. 1997;6(6):557–559
  123. Nath G, Singh YK, Kumar K, Gulati AK, Shukla VK, Khanna AK, et al. Association of carcinoma of the gallbladder with typhoid carriage in a typhoid endemic area using nested PCR. J Infect Dev Ctries. 2008;2(4):302–307
  124. Nath G, Singh YK, Maurya P, Gulati AK, Srivastava RC, Tripathi SK. Does Salmonella Typhi primarily reside in the liver of chronic typhoid carriers?. J Infect Dev Ctries. 2010;4(4):259–261
  125. Vaishnavi C, Kochhar R, Singh G, Kumar S, Singh S, Singh K. Epidemiology of typhoid carriers among blood donors and patients with biliary, gastrointestinal and other related diseases. Microbiol Immunol. 2005;49(2):107–112
  126. Buchwald DS, Blaser MJ. A review of human salmonellosis: II. Duration of excretion following infection with nontyphi Salmonella. Rev Infect Dis. 1984;6(3):345–356
  127. World Health Organization (WHO) . Background document: the diagnosis, treatment and prevention of typhoid fever. Geneva: World Health Organization; 2003;1–38
  128. Baker S, Favorov M, Dougan G. Searching for the elusive typhoid diagnostic. BMC Infect Dis. 2010;10:45
  129. Guerra-Caceres JG, Gotuzzo-Herencia E, Crosby-Dagnino E, Miro-Quesada M, Carrillo-Parodi C. Diagnostic value of bone marrow culture in typhoid fever. Trans R Soc Trop Med Hyg. 1979;73(6):680–683
  130. Parry CM, Wijedoru L, Arjyal A, Baker S. The utility of diagnostic tests for enteric fever in endemic locations. Expert Rev Anti Infect Ther. 2011;9(6):711–725
  131. Vallenas C, Hernandez H, Kay B, Black R, Gotuzzo E. Efficacy of bone marrow, blood, stool and duodenal contents cultures for bacteriologic confirmation of typhoid fever in children. Pediatr Infect Dis. 1985;4(5):496–498
  132. Farooqui BJ, Khurshid M, Ashfaq MK, Khan MA. Comparative yield of Salmonella typhi from blood and bone marrow cultures in patients with fever of unknown origin. J Clin Pathol. 1991;44(3):258–259
  133. Nga TVT, Karkey A, Dongol S, Thuy HN, Dunstan S, Holt K, et al. The sensitivity of real-time PCR amplification targeting invasive Salmonella serovars in biological specimens. BMC Infect Dis. 2010;10:125
  134. Wain J, Hosoglu S. The laboratory diagnosis of enteric fever. J Infect Dev Ctries. 2008;2(6):421–425
  135. Gilman RH, Terminel M, Levine MM, Hernandez-Mendoza P, Hornick RB. Relative efficacy of blood, urine, rectal swab, bone-marrow, and rose-spot cultures for recovery of Salmonella typhi in typhoid fever. Lancet. 1975;1(7918):1211–1213
  136. Olopoenia LA, King AL. Widal agglutination test – 100 years later: still plagued by controversy. Postgrad Med J. 2000;76(892):80–84
  137. Gómez-Duarte OG, Bai J, Newell E. Detection of Escherichia coli, Salmonella spp., Shigella spp., Yersinia enterocolitica, Vibrio cholerae, and Campylobacter spp. enteropathogens by 3-reaction multiplex polymerase chain reaction. Diagn Microbiol Infect Dis. 2009;63(1):1–9
  138. Gordon MA. Invasive nontyphoidal Salmonella disease: epidemiology, pathogenesis and diagnosis. Curr Opin Infect Dis. 2011;24(5):484–489
  139. Hatta M, Ratnawati . Enteric fever in endemic areas of Indonesia: an increasing problem of resistance. J Infect Dev Ctries. 2008;2(4):279–282
  140. Hatta M, Smits HL. Detection of Salmonella typhi by nested polymerase chain reaction in blood, urine, and stool samples. Am J Trop Med Hyg. 2007;76(1):139–143
  141. Tennant SM, Diallo S, Levy H, Livio S, Sow SO, Tapia M, et al. Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Negl Trop Dis. 2010;4(3):e621
  142. Foley SL, White DG, McDermott PF, Walker RD, Rhodes B, Fedorka-Cray PJ, et al. Comparison of subtyping methods for differentiating Salmonella enterica serovar Typhimurium isolates obtained from food animal sources. J Clin Microbiol. 2006;44(10):3569–3577
  143. Kotetishvili M, Stine OC, Kreger A, Morris JG, Sulakvelidze A. Multilocus sequence typing for characterization of clinical and environmental salmonella strains. J Clin Microbiol. 2002;40(5):1626–1635
  144. Sangal V, Harbottle H, Mazzoni CJ, Helmuth R, Guerra B, Didelot X, et al. Evolution and population structure of Salmonella enterica serovar Newport. J Bacteriol. 2010;192(24):6465–6476
  145. Butler T, Islam A, Kabir I, Jones PK. Patterns of morbidity and mortality in typhoid fever dependent on age and gender: review of 552 hospitalized patients with diarrhea. Rev Infect Dis. 1991;13(1):85–90
  146. Capoor MR, Nair D. Quinolone and cephalosporin resistance in enteric fever. J Glob Infect Dis. 2010;2(3):258–262
  147. Thaver D, Zaidi AK, Critchley JA, Azmatullah A, Madni SA, Bhutta ZA. Fluoroquinolones for treating typhoid and paratyphoid fever (enteric fever). Cochrane Database Syst Rev. 2008;(4):CD004530
  148. Gendrel D, Chalumeau M, Moulin F, Raymond J. Fluoroquinolones in paediatrics: a risk for the patient or for the community?. Lancet Infect Dis. 2003;3(9):537–546
  149. Arjyal A, Basnyat B, Koirala S, Karkey A, Dongol S, Agrawaal KK, et al. Gatifloxacin versus chloramphenicol for uncomplicated enteric fever: an open-label, randomised, controlled trial. Lancet Infect Dis. 2011;11(6):445–454
  150. Arjyal A, Pandit A. Treatment of enteric fever. J Infect Dev Ctries. 2008;2(6):426–430
  151. Alam MN, Haq SA, Das KK, Baral PK, Mazid MN, Siddique RU, et al. Efficacy of ciprofloxacin in enteric fever: comparison of treatment duration in sensitive and multidrug-resistant Salmonella. Am J Trop Med Hyg. 1995;53(3):306–311
  152. Singh CP, Singh N, Brar GK, Lal G, Kumar H. Efficacy of ciprofloxacin and norfloxacin in multidrug resistant enteric fever in adults. J Indian Med Assoc. 1993;91(6):156–157
  153. Parry CM, Beeching NJ. Treatment of enteric fever. Br Med J. 2009;338:b1159
  154. Effa EE, Bukirwa H. Azithromycin for treating uncomplicated typhoid and paratyphoid fever (enteric fever). Cochrane Database Syst Rev. 2008;(4):CD006083
  155. Memon IA, Billoo AG, Memon HI. Cefixime: an oral option for the treatment of multidrug-resistant enteric fever in children. South Med J. 1997;90(12):1204–1207
  156. Parry CM, Threlfall EJ. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis. 2008;21(5):531–538
  157. Mølbak K. Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clin Infect Dis. 2005;41(11):1613–1620
  158. Sirinavin S, Jayanetra P, Thakkinstian A. Clinical and prognostic categorization of extraintestinal nontyphoidal Salmonella infections in infants and children. Clin Infect Dis. 1999;29(5):1151–1156
  159. Ruiz M, Rodríguez JC, Escribano I, Royo G. Available options in the management of non-typhi Salmonella. Expert Opin Pharmacother. 2004;5(8):1737–1743
  160. Graham SM, English M. Non-typhoidal salmonellae: a management challenge for children with community-acquired invasive disease in tropical African countries. Lancet. 2009;373(9659):267–269
  161. Dunne EF, Fey PD, Kludt P, Reporter R, Mostashari F, Shillam P, et al. Emergence of domestically acquired ceftriaxone-resistant Salmonella infections associated with AmpC beta-lactamase. J Am Med Assoc. 2000;284(24):3151–3156
  162. Gupta A, Fontana J, Crowe C, Bolstorff B, Stout A, Van Duyne S, et al. Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States. J Infect Dis. 2003;188(11):1707–1716
  163. Sow AG, Wane AA, Diallo MH, Boye CS-B, Aïdara-Kane A. Genotypic characterization of antibiotic-resistant Salmonella enteritidis isolates in Dakar, Senegal. J Infect Dev Ctries. 2007;1(3):284–288
  164. Mølbak K. Spread of resistant bacteria and resistance genes from animals to humans–the public health consequences. J Vet Med B Infect Dis Vet Public Health. 2004;51(8–9):364–369
  165. Adhikari B, Besser TE, Gay JM, Fox LK, Davis MA, Cobbold RN, et al. Introduction of new multidrug-resistant Salmonella enterica strains into commercial dairy herds. J Dairy Sci. 2009;92(9):4218–4228
  166. Emborg H-D, Baggesen DL, Aarestrup FM. Ten years of antimicrobial susceptibility testing of Salmonella from Danish pig farms. J Antimicrob Chemother. 2008;62(2):360–363
  167. Varma JK, Greene KD, Ovitt J, Barrett TJ, Medalla F, Angulo FJ. Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984–2002. Emerging Infect Dis. 2005;11(6):943–946
  168. Varma JK, Molbak K, Barrett TJ, Beebe JL, Jones TF, Rabatsky-Ehr T, et al. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. J Infect Dis. 2005;191(4):554–561
  169. Sirinavin S, Pokawattana L, Bangtrakulnondh A. Duration of nontyphoidal Salmonella carriage in asymptomatic adults. Clin Infect Dis. 2004;38(11):1644–1645
  170. Sirinavin S, Thavornnunth J, Sakchainanont B, Bangtrakulnonth A, Chongthawonsatid S, Junumporn S. Norfloxacin and azithromycin for treatment of nontyphoidal salmonella carriers. Clin Infect Dis. 2003;37(5):685–691
  171. Crum-Cianflone NF. Salmonellosis and the gastrointestinal tract: more than just peanut butter. Curr Gastroenterol Rep. 2008;10(4):424–431
  172. Heymann D. Control of communicable diseases manual: an official report of the American Public Health Association. Washington DC: American Public Health Assoc; 2004;
  173. National Association of State Public Health Veterinarians, Inc. (NASPHV) . Compendium of measures to prevent disease associated with animals in public settings, 2007: National Association of State Public Health Veterinarians, Inc. (NASPHV). MMWR Recomm Rep. 2007;56(RR-5):1–14
  174. Maki DG. Coming to grips with foodborne infection–peanut butter, peppers, and nationwide salmonella outbreaks. N Engl J Med. 2009;360(10):949–953
  175. Talbot EA, Gagnon ER, Greenblatt J. Common ground for the control of multidrug-resistant Salmonella in ground beef. Clin Infect Dis. 2006;42(10):1455–1462
  176. Guzman CA, Borsutzky S, Griot-Wenk M, Metcalfe IC, Pearman J, Collioud A, et al. Vaccines against typhoid fever. Vaccine. 2006;24(18):3804–3811
  177. Whitaker JA, Franco-Paredes C, del Rio C, Edupuganti S. Rethinking typhoid fever vaccines: implications for travelers and people living in highly endemic areas. J Travel Med. 2009;16(1):46–52
  178. Lin FY, Ho VA, Khiem HB, Trach DD, Bay PV, Thanh TC, et al. The efficacy of a Salmonella typhi Vi conjugate vaccine in two-to-five-year-old children. N Engl J Med. 2001;344(17):1263–1269
  179. Paterson GK, Maskell DJ. Recent advances in the field of Salmonella Typhi vaccines. Hum Vaccin. 2010;6(5):379–384
  180. Khan MI, Ochiai RL, Clemens JD. Population impact of Vi capsular polysaccharide vaccine. Expert Rev Vaccines. 2010;9(5):485–496
  181. Klugman KP, Gilbertson IT, Koornhof HJ, Robbins JB, Schneerson R, Schulz D, et al. Protective activity of Vi capsular polysaccharide vaccine against typhoid fever. Lancet. 1987;2(8569):1165–1169
  182. Yang HH, Kilgore PE, Yang LH, Park JK, Pan YF, Kim Y, et al. An outbreak of typhoid fever, Xing-An County, People’s Republic of China, 1999: estimation of the field effectiveness of Vi polysaccharide typhoid vaccine. J Infect Dis. 2001;183(12):1775–1780
  183. Yang HH, Wu CG, Xie GZ, Gu QW, Wang BR, Wang LY, et al. Efficacy trial of Vi polysaccharide vaccine against typhoid fever in south-western China. Bull World Health Organ. 2001;79(7):625–631
  184. Sur D, Ochiai RL, Bhattacharya SK, Ganguly NK, Ali M, Manna B, et al. A cluster-randomized effectiveness trial of Vi typhoid vaccine in India. N Engl J Med. 2009;361(4):335–344
  185. Szu SC, Taylor DN, Trofa AC, Clements JD, Shiloach J, Sadoff JC, et al. Laboratory and preliminary clinical characterization of Vi capsular polysaccharide-protein conjugate vaccines. Infect Immun. 1994;62(10):4440–4444
  186. Mai NL, Phan VB, Vo AH, Tran CT, Lin FYC, Bryla DA, et al. Persistent efficacy of Vi conjugate vaccine against typhoid fever in young children. N Engl J Med. 2003;349(14):1390–1391
  187. Thiem VD, Lin F-YC, Canh DG, Son NH, Anh DD, Mao ND, et al. The Vi conjugate typhoid vaccine is safe, elicits protective levels of IgG anti-Vi, and is compatible with routine infant vaccines. Clin Vaccine Immunol. 2011;18(5):730–735
  188. Germanier R, Füer E. Isolation and characterization of Gal E mutant Ty 21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine. J Infect Dis. 1975;131(5):553–558
  189. Levine MM, Ferreccio C, Black RE, Germanier R. Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet. 1987;1(8541):1049–1052
  190. Levine MM, Ferreccio C, Cryz S, Ortiz E. Comparison of enteric-coated capsules and liquid formulation of Ty21a typhoid vaccine in randomised controlled field trial. Lancet. 1990;336(8720):891–894
  191. American Academy of Pediatrics , Pickering L. Red book: 2009 report of the Committee on Infectious Diseases. 28th ed.. Elk Grove Village IL: American Academy of Pediatrics; 2009;
  192. Penha Filho RAC, de Paiva JB, da Silva MD, de Almeida AM, Berchieri A. Control of Salmonella Enteritidis and Salmonella Gallinarum in birds by using live vaccine candidate containing attenuated Salmonella Gallinarum mutant strain. Vaccine. 2010;28(16):2853–2859
  193. Pavic A, Groves PJ, Cox JM. Utilization of a novel autologous killed tri-vaccine (serogroups B [Typhimurium], C [Mbandaka] and E [Orion]) for Salmonella control in commercial poultry breeders. Avian Pathol. 2010;39(1):31–39
  194. Dórea FC, Cole DJ, Hofacre C, Zamperini K, Mathis D, Doyle MP, et al. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Appl Environ Microbiol. 2010;76(23):7820–7825
  195. Hur J, Lee JH. Immunization of pregnant sows with a novel virulence gene deleted live Salmonella vaccine and protection of their suckling piglets against salmonellosis. Vet Microbiol. 2010;143(2–4):270–276
  196. Denagamage TN, O’Connor AM, Sargeant JM, Rajić A, McKean JD. Efficacy of vaccination to reduce Salmonella prevalence in live and slaughtered swine: a systematic review of literature from 1979 to 2007. Foodborne Pathog Dis. 2007;4(4):539–549
  197. Selke M, Meens J, Springer S, Frank R, Gerlach G-F. Immunization of pigs to prevent disease in humans: construction and protective efficacy of a Salmonella enterica serovar Typhimurium live negative-marker vaccine. Infect Immun. 2007;75(5):2476–2483
  198. Collard JM, Bertrand S, Dierick K, Godard C, Wildemauwe C, Vermeersch K, et al. Drastic decrease of Salmonella enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol Infect. 2008;136(6):771–781

PII: S1477-8939(11)00120-7

doi: 10.1016/j.tmaid.2011.11.001

Travel Medicine and Infectious Disease
Volume 9, Issue 6 , Pages 263-277 , November 2011