Abstract
Non-typhoidal Salmonellae (NTS) are an important cause of infectious diarrhoea world-wide. In the absence of immune deficiency, gastroenteritis caused by NTS is usually mild, self limiting and rarely requires intervention. NTS are also an important cause of invasive disease, particularly in developing countries, likely secondary to the high prevalence of co-existing malnutrition, malaria and HIV infection. This review provides an overview of the microbiology, epidemiology and pathogenesis of NTS, and compares recommendations for the treatment of NTS gastroenteritis in children.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Grimont PAD, Weill F (2007) Antigenic Formulae of the Salmonella Serovars. 9th edn. Institut Pasteur, Paris
Tindall BJ, Grimont PAD, Garrity GM, Euzeby JP (2005) Nomenclature and taxonomy of the genus Salmonella. Int J Syst Evol Microbiol 55:521–524
Nataro JP, Bopp CA, Fields PI, Kaper JB, Strockbine NA (2011) Escherichia, Shigella, and Salmonella. In: Versalovic J, Carroll KC, Funke G, Jorgensen JH, Landry ML, Warnock DW (eds). Manual of Clinical Microbiology, 10th edn. ASM, Washington, DC, p 603–626
Pegues DA, Miller SI (2010) Salmonella Species, including Salmonella Typhi. In: Mandell GL, Bennett JE, Dolin R (eds). Mandell, Douglas and Bennett’s Principles and Practices of Infectious Diseases, 7th edn. Elsevier, Philadelphia, p 2887–2903
Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B (2000) Salmonella nomenclature. J Clin Microbiol 38:2465–2467
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ et al (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889
Vieira A, Jensen AR, Pires SM, Karlsmose S, Wegener HC, Wong DLF (2009) WHO Global Foodborne Infections Network Country Databank—a resource to link human and non-human sources of Salmonella. Int Soc Vet Epidemiol Econ 643:512–517
Braden CR (2006) Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 43:512–517
Hohmann EL (2001) Nontyphoidal salmonellosis. Clin Infect Dis 32:263–269
Mermin J, Hutwagner L, Vugia D, Shallow S, Daily P, Bender J et al (2004) Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. Clin Infect Dis 38(Suppl 3):S253–261
Weikel CS, Guerrant RL (1985) Nosocomial salmonellosis. Infection Control: IC 6:218–220
AAP (2006) Salmonella Infections. In: Pickering LK, Baker CJ, Kimberlin DW, Long SS (eds). Red Book: 2009 Report of the Commitee on Infectious Diseases, 28th edn. American Academy of Pediatrics, Elk Grove Village, p 584–588
Blaser MJ, Newman LS (1982) A review of human salmonellosis: I. Infective dose. Rev Infect Dis 4:1096–1106
Seals JE, Parrott PL, McGowan JE, Jr., Feldman RA (1983) Nursery salmonellosis: delayed recognition due to unusually long incubation period. Infection Control: IC 4:205–208
Garcia-del Portillo F (2001) Salmonella intracellular proliferation: where, when and how? Microbes Infect 3:1305–311
Dougan G, John V, Palmer S, Mastroeni P (2011) Immunity to salmonellosis. Immunol Rev 240:196–210
Gondwea EN, Molyneuxa ME, Goodallc M, Graham SM, Mastroenig P, Draysonc MT et al (2010) Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. PNAS 107:3070–3075
MacLennan CA, Gondwe EN, Msefula CL, Kingsley RA, Thomson NR, White SA et al (2008) The neglected role of antibody in protection against nontyphoidal salmonella bacteremia in African children. J Clin Invest 118:1553–1562
Tennant SM, Hartland EL, Phumoonna T, Lyras D, Rood JI, Robins-Browne RM et al (2008) Influence of gastric acid on susceptibility to infection with ingested bacterial pathogens. Infect Immun 76:639–645
Buchin PJ, Andriole VT, Spiro HM (1980) Salmonella infections and hypochlorhydria. J Clin Gastroenterol 2:133–138
O’Ryan ML, Nataro JP, Cleary TG (2011) Microorganisms Responsible for Neonatal Diarrhea. In: Remington JS, Klein JO, Wilson CB, Nizet V, Maldonado Y (eds). Remington: Infectious Diseases of the Fetus and Newborn, 7th edn. Elsevier, Philadelphia, p. 359–418
Moir S, Fauci AS (2010) Immunology. Salmonella susceptibility. Science 328:439–440 (New York, NY)
Celum CL, Chaisson RE, Rutherford GW, Barnhart JL, Echenberg DF (1987) Incidence of salmonellosis in patients with AIDS. J Infect Dis 156:998–1002
Ramos JM, Garcia-Corbeira P, Aguado JM, Arjona R, Ales JM, Soriano F (1994) Clinical significance of primary vs. secondary bacteremia due to nontyphoid Salmonella in patients without AIDS. Clin Infect Dis 19:777–780
Abruzzi A, Fried B (2011) Coinfection of Schistosoma (Trematoda) with bacteria, protozoa and helminths. Adv Parasitol 77:1–85
Jertborn M, Haglind P, Iwarson S, Svennerholm AM (1990) Estimation of symptomatic and asymptomatic Salmonella infections. Scand J Infect Dis 22:451–455
Mandal BK, Brennand J (1988) Bacteraemia in salmonellosis: a 15 year retrospective study from a regional infectious diseases unit. BMJ 297:1242–1243 (Clinical research ed)
Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D’Angelo M, Hurd S et al (2008) Salmonellosis outcomes differ substantially by serotype. J Infect Dis 198:109–114
Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S et al (2004) Invasive Salmonella infections in the United States, FoodNet, 1996–1999: incidence, serotype distribution, and outcome. Clin Infect Dis 38(Suppl 3):S149–156
Gordon MA (2011) Invasive nontyphoidal Salmonella disease: epidemiology, pathogenesis and diagnosis. Curr Opin Infect Dis 24:484–489
Graham SM (2010) Nontyphoidal salmonellosis in Africa. Curr Opin Infect Dis 23:409–414
Scott AJ, Berkley JA, Mwangi I, Ochola L, Uyoga S, Macharia A et al (2011) Relation between falciparum malaria and bacteraemia in Kenyan children: a population–based, case-control study and a longitudinal study. Lancet 378:1316–1323
Schutze GE, Schutze SE, Kirby RS (1997) Extraintestinal salmonellosis in a children’s hospital. Pediatr Infect Dis J 16:482–485
Owusu-Ofori A, Scheld WM (2003) Treatment of Salmonella meningitis: two case reports and a review of the literature. Int J Infect Dis 7:53–60
Sirinavin S, Jayanetra P, Lolekha S, Layangkul T (1988) Predictors for extraintestinal infection in Salmonella enteritis in Thailand. Pediatr Infect Dis J 7:44–48
Galanakis E, Bitsori M, Maraki S, Giannakopoulou C, Samonis G, Tselentis Y (2007) Invasive non-typhoidal salmonellosis in immunocompetent infants and children. Int J Infect Dis 11:36–39
Zaidi E, Bachur R, Harper M (1999) Non-typhi Salmonella bacteremia in children. Pediatr Infect Dis J 18:1073–1077
Katz BZ, Shapiro ED (1986) Predictors of persistently positive blood cultures in children with "occult" Salmonella bacteremia. Pediatr Infect Dis 5:713–714
Ramos JM, Aguado JM, Garcia-Corbeira P, Ales JM, Soriano F (1996) Clinical spectrum of urinary tract infections due on nontyphoidal Salmonella species. Clin Infect Dis 23:388–390
Gasem MH, Keuter M, Dolmans WMV, Van Der Ven-Jongekrijg J, Djokomoeljanto R, Van Der Meer JWM (2003) Persistence of Salmonellae in blood and bone marrow: randomized controlled trial comparing ciprofloxacin and chloramphenicol treatments against enteric fever. Antimicrob Agents Chemother 47:1727–1731
Ternhag A, Torner A, Svensson A, Ekdahl K, Giesecke J (2008) Short–and long-term effects of bacterial gastrointestinal infections. Emerg Infect Dis 14:143–148
Arnedo-Pena A, Beltran-Fabregat J, Vila-Pastor B, Tirado-Balaguer MD, Herrero–Carot C, Bellido-Blasco JB et al (2010) Reactive arthritis and other musculoskeletal sequelae following an outbreak of Salmonella hadar in Castellon, Spain. J Rheumatol 37:1735–1742
Buchwald DS, Blaser MJ (1984) A review of human salmonellosis: II. Duration of excretion following infection with nontyphi Salmonella. Rev Infect Dis 6:345–356
Corrado ML, DuPont HL, Cooperstock M, Fekety R, Murray DM (1992) Evaluation of new anti-infective drugs for the treatment of chronic carriage of Salmonella. Infectious Diseases Society of America and the Food and Drug Administration. Clin Infect Dis 15(Suppl 1):S259–262
Gilbert DN, Moellering RC, Eliopoulis GM, Saag MS (2011) The Sanford Guide to Antimicrobial Therapy, 41st edn
Ingham B, Brentnall DW, Dale EA, McFadzean JA (1977) Arthropathy induced by antibacterial fused N-alkyl-4-pyridone-3-carboxylic acids. Toxicol Lett 1:21–26
Adefurin A, Sammons H, Jacqz-Aigrain E, Choonara I (2011) Ciprofloxacin safety in paediatrics: a systematic review. Arch Dis Child 96:874–880
Pickering LK (2009) Approach to Patients with Gastrointestinal Tract Infections and Food Poisoning. In: Feigin RD, Cherry J, Demmler-Harrison G, Kaplan S (eds). Textbook of Pediatric Infectious Diseases. Elsevier, Philadelphia, p 621–653
Graham SM (2008) Salmonellosis. In: McIntosh N, Helms P, Smyth R, Logan S (eds). Forfar and Arneil’s Textbook of Pediatrics, 7th edn. Elsevier, Philadelphia, p 1246–1249
Isaacs D (2007) Gastrointestinal infections. In: Elliot E, Gilbert R, Moyer V, Pichichero M (eds). Evidence-based Pediatric Infectious Diseases. Blackwell Publishing, United Kingdom, p 74–101
Reller ME (2009) Salmonella Species. In: Long SS, Pickering LK, Prober C (eds). Principles and Practice of Pediatric Infectious Diseases, 3rd edn. Elsevier, Philadelphia, p 812–817
Bhutta ZA (2011) Salmonella. In: Kliegman RM, Stanton BMD, St Geme J, Schor N, Behrman RE (eds). Nelson Textbook of Pediatrics, 19th edn. Elsevier, Philadelphia, p 948–958
Pickering LK (2006) Salmonella Infections. In: McMillan JA, Feigin RD, DeAngelis D, Jones MD (eds). Oski’s Pediatrics: Principles and Practice, 4th edn. Lippincott Williams and Wilkins, Philadelphia, p 1112–1116
Pavia AT (2011) Salmonella, Shigella, and Escherichia coli. In: Rudolph C, Rudolph A, Lister G, First L, Gershon A (eds). Rudolph’s Pediatrics, 22nd edn. McGraw Hill, New York
Guerrant RL, Van Gilder T, Steiner TS, Thielman NM, Slutsker L, Tauxe RV et al (2001) Practice guidelines for the management of infectious diarrhea. Clin Infect Dis 32:331–351
(2009) Diarrhoea and vomiting caused by gastroenteritis: diagnosis, assessment and management in children younger than 5 years. RCOG, London
Hohmann EL (2012) Approach to the patient with nontyphoidal Salmonella in a stool culture. In: Baron EL (ed). UpToDate, Waltham
Sirinavin S, Garner P (2000) Antibiotics for treating salmonella gut infections. Cochrane Database Syst Rev (Online):CD001167
Garcia de Olarte D, Hugo TS, Nancy AO, Nelson JD, Haltalin KC (1974) Treatment of Diarrhea in Malnourished Infants and Children: A Double-Blind Study Comparing Ampicillin and Placebo. Am J Dis Child 127:379–388
Nelson JD, Kusmiesz H, Jackson LH, Woodman E (1980) Treatment of Salmonella gastroenteritis with ampicillin, amoxicillin, or placebo. Pediatrics 65:1125–1130
Haltalin KC, Kusmiesz HT, Hinton LV, Nelson JD (1972) Treatment of Acute Diarrhea in Outpatients: Double-Blind Study Comparing Ampicillin and Placebo. Am J Dis Child 124:554–561
Kazemi M, Gumpert TG, Marks MI (1973) A controlled trial comparing sulfametboxazole–trimethoprim, ampicillin, and no therapy in the treatment of salmonella gastroenteritis in children. J Pediatr 83:646–650
Macdonald WB, Friday F, McEacharn M (1954) The Effect of Chloramphenicol in Salmonella Enteritis of Infancy. Arch Dis Child 29:238–241
Geme JW, 3rd, Hodes HL, Marcy SM, Pickering LK, Rodriguez WJ, McCracken GH, Jr. et al (1988) Consensus: management of Salmonella infection in the first year of life. Pediatr Infect Dis J 7:615–621
Voltersvik P, Halstensen A, Langeland N, Digranes A, Peterson LE, Rolstad T et al (2000) Eradication of non-typhoid salmonellae in acute enteritis after therapy with ofloxacin for 5 or 10 days. J Antimicrob Chemother 46:457–459
Stoycheva MV, Murdjeva MA (2006) Antimicrobial therapy of salmonelloses–current state and perspectives. Folia Med (Plovdiv) 48:5–10
Tsai MH, Huang YC, Lin TY, Huang YL, Kuo CC, Chiu CH (2011) Reappraisal of parenteral antimicrobial therapy for nontyphoidal Salmonella enteric infection in children. Clin Microbiol Infect 17:300–305
Onwuezobe IA, Oshun PO (2008) Antbiotics for treating nontyphoidal Salmonella diarrhoea. Cochrane Database Syst. Rev
Sirinavin S, Thavornnunth J, Sakchainanont B, Bangtrakulnonth A, Chongthawonsatid S, Junumporn S (2003) Norfloxacin and azithromycin for treatment of nontyphoidal salmonella carriers. Clin Infect Dis 37:685–691
Zavala Trujillo I, Quiroz C, Gutierrez MA, Arias J, Renteria M (1991) Fluoroquinolones in the treatment of typhoid fever and the carrier state. Eur J Clin Microbiol Infect Dis 10:334–341
Nelson MR, Shanson DC, Hawkins DA, Gazzard BG (1992) Salmonella, Campylobacter and Shigella in HIV-seropositive patients. AIDS (London, England) 6:1495–1498
Kaplan JE, Benson C, Holmes KH, Brooks JT, Pau A, Masur H et al (2009) Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 58:1–207, (quiz CE1–4)
Roberts C, Wilkins EG (1987) Salmonella screening of pregnant women. J Hosp Infect 10:67–72
Schloesser RL, Schaefer V, Groll AH (2004) Fatal transplacental infection with non–typhoidal Salmonella. Scand J Infect Dis 36:773–774
Cooke FJ, Ginwalla S, Hampton MD, Wain J, Ross-Russell R, Lever A et al (2009) Report of neonatal meningitis due to Salmonella enterica serotype Agona and review of breast milk-associated neonatal Salmonella infections. J Clin Microbiol 47:3045–3049
Cahill SM, Wachsmuth K, Costarrica M, Embarek P (2008) Powdered Infant Formula as a Source of Salmonella Infection in Infants. Clin Infect Dis 46:268–273
Van Der Klooster JM, Roelofs HJ (1997) Management of Salmonella infections during pregnancy and puerperium. Neth J Med 51:83–86
Varma JK, Molbak K, Barrett TJ, Beebe JL, Jones TF, Rabatsky-Ehr T et al (2005) Antimicrobial–resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. J Infect Dis 191:554–561
Su L-H, Chiu C-H, Chu C, Ou JT (2004) Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clin Infect Dis 39:546–551
Parry CM, Threlfall EJ (2008) Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis 21:531–538
Angulo FJ, Johnson KR, Tauxe RV, Cohen ML (2000) Origins and consequences of antimicrobial-resistant nontyphoidal Salmonella: implications for the use of fluoroquinolones in food animals. Microb Drug Resist (Larchmont, NY) 6:77–83
Crump JA, Medalla FM, Joyce KW, Krueger AL, Hoekstra RM, Whichard JM et al (2011) Antimicrobial resistance among invasive nontyphoidal Salmonella enterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996–2007. Antimicrob Agents Chemother 55:1148–1154
Meakins S, Fisher IST, Berghold C, Gerner-Smidt P, Tschape H, Cormican M et al (2008) Antimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000–2004: a report from the Enter-net International Surveillance Network. Microb Drug Resist (Larchmont, NY) 14:31–35
Reddy EA, Shaw AV, Crump JA (2010) Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 10:417–432
Nordmann P, Poirel L, Mak JK, White PA, McIver CJ, Taylor P (2008) Multidrug-resistant Salmonella strains expressing emerging antibiotic resistance determinants. Clin Infect Dis 46:324–325
Miriagou V, Tzouvelekis LS, Rossiter S, Tzelepi E, Angulo FJ, Whichard JM (2003) Imipenem resistance in a Salmonella clinical strain due to plasmid-mediated class A carbapenemase KPC-2. Antimicrob Agents Chemother 47:1297–1300
Hakanen A, Kotilainen P, Jalava J, Siitonen A, Huovinen P (1999) Detection of decreased fluoroquinolone susceptibility in Salmonellas and validation of nalidixic acid screening test. J Clin Microbiol 37:3572–3577
Hakanen AJ, Lindgren M, Huovinen P, Jalava J, Siitonen A, Kotilainen P (2005) New quinolone resistance phenomenon in Salmonella enterica: nalidixic acid-susceptible isolates with reduced fluoroquinolone susceptibility. J Clin Microbiol 43:5775–5778
Chorba TL, Meriwether RA, Jenkins BR, Gunn RA, MacCormack JN (1987) Control of a non-foodborne outbreak of salmonellosis: day care in isolation. Am J Public Health 77:979–981
Tauxe RV, Hassan LF, Findeisen KO, Sharrar RG, Blake PA (1988) Salmonellosis in nurses: lack of transmission to patients. J Infect Dis 157:370–373
(1987) Food handlers and salmonella food poisoning Lancet 2:606–607
Kassis I, Dagan R, Chipman M, Alkan M, Simo A, Gorodischer R (1990) The use of prophylactic furazolidone to control a nosocomial epidemic of multiply resistant Salmonella typhimurium in pediatric wards. Pediatr Infect Dis J 9:551–555
Dyson C, Ribeiro CD, Westmoreland D (1995) Large scale use of ciprofloxacin in the control of a Salmonella outbreak in a hospital for the mentally handicapped. J Hosp Infect 29:287–296
Linnemann CC, Jr., Cannon CG, Staneck JL, McNeely BL (1985) Prolonged hospital epidemic of salmonellosis: use of trimethoprim-sulfamethoxazole for control. Infection control: IC 6:221–225
Siegel JD, Rhinehart E, Jackson M, Chiarello L (2007) Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Healthcare Settings. Healthcare Infection Control Practices Advisory Committee (HICPAC)
NHMRC (2010) Australian Guidelines for the Prevention and Control of Infection in Healthcare. Commonwealth of Australia 1–262
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Haeusler, G., Curtis, N. (2013). Non-typhoidal Salmonella in Children: Microbiology, Epidemiology and Treatment. In: Curtis, N., Finn, A., Pollard, A. (eds) Hot Topics in Infection and Immunity in Children IX. Advances in Experimental Medicine and Biology, vol 764. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4726-9_2
Download citation
DOI: https://doi.org/10.1007/978-1-4614-4726-9_2
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-4725-2
Online ISBN: 978-1-4614-4726-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)