Abstract
Extraintestinal disease occurs in 5–8% of non-typhoid Salmonella enterica (NTS) infections and is more likely to be associated with hospitalization and death. The study examined the epidemiology of extraintestinal NTS infections in Israel and the possible effects of patients’ age and sex. NTS isolates passively submitted to the National Salmonella Reference Center during 1996–2006 were the source for the study cohort. Poisson regression models were used to assess incidence trends over the study years and to evaluate the effects of patients’ age and sex on the incidence of extraintestinal NTS manifestations. A total of 36,822 stool and 1,415 (3.7%) patient-unique NTS isolates from blood (74.1%), urine (18.3%), and other sources (3.7%) were studied. Serotypes Enteritidis, Virchow, and Typhimurium accounted for 66.3% of the isolates. Analysis showed a highly significant quadratic (U-shaped) relationship between patients’ age and the incidence of extraintestinal isolation (p < 0.001), with increasing risk in the two extremes of age. Differences between the incidence of blood and urine sources were significant in patients <10 and ≥60 years old (relative risk [RR] = 5.88, 95% confidence interval [CI] 3.36–10.30, p < 0.001 and RR = 1.66, 95% CI 1.09–2.53, p = 0.017, respectively). Males ≥60 years of age were more likely than females of the same age to have bacteremia (RR = 1.90, 95% CI 1.39–2.61, p > 0.001) and less likely to have urinary NTS isolation (RR = 0.50, 95% CI 0.28–0.89, p = 0.018). Serotype Virchow had the highest incidence in patients <10 years of age, while serotype Enteritidis had the highest incidence in patients ≥60 years old. The study revealed a complex effect of patients’ age and sex on the epidemiology of extraintestinal NTS manifestations.
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References
Pegues DA, Miller SI (2009) Salmonella species, including Salmonella typhi. In: Mandell GL, Bennett JE, Dolin R (eds) Mandell, Douglas, and Bennett’s principles and practice of infectious diseases, 6th edn. Churchill Livingstone, Elsevier, Philadelphia, pp 2887–2903
Voetsch AC, Van Gilder TJ, Angulo FJ, Farley MM, Shallow S, Marcus R, Cieslak PR, Deneen VC, Tauxe RV (2004) FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 38(Suppl 3):S127–S134
Kennedy M, Villar R, Vugia DJ, Rabatsky-Ehr T, Farley MM, Pass M, Smith K, Smith P, Cieslak PR, Imhoff B, Griffin PM (2004) Hospitalizations and deaths due to Salmonella infections, FoodNet, 1996–1999. Clin Infect Dis 38(Suppl 3):S142–S148
Weinberger M, Andorn N, Agmon V, Cohen D, Shohat T, Pitlik SD (2004) Blood invasiveness of Salmonella enterica as a function of age and serotype. Epidemiol Infect 132:1023–1028
Shimoni Z, Pitlik S, Leibovici L, Samra Z, Konigsberger H, Drucker M, Agmon V, Ashkenazi S, Weinberger M (1999) Nontyphoid Salmonella bacteremia: age-related differences in clinical presentation, bacteriology, and outcome. Clin Infect Dis 28(4):822–827
Levine WC, Buehler JW, Bean NH, Tauxe RV (1991) Epidemiology of nontyphoidal Salmonella bacteremia during the human immunodeficiency virus epidemic. J Infect Dis 164(1):81–87
Cohen JI, Bartlett JA, Corey GR (1987) Extra-intestinal manifestations of Salmonella infections. Medicine (Baltimore) 66:349–388
Mandal BK, Brennand J (1988) Bacteraemia in salmonellosis: a 15 year retrospective study from a regional infectious diseases unit. Br Med J 297:1242–1243
Gradel KO, Schønheyder HC, Pedersen L, Thomsen RW, Nørgaard M, Nielsen H (2006) Incidence and prognosis of non-typhoid Salmonella bacteraemia in Denmark: a 10-year county-based follow-up study. Eur J Clin Microbiol Infect Dis 25(3):151–158
Gradel KO, Dethlefsen C, Schønheyder HC, Nielsen H (2008) Magnitude of bacteraemia is associated with increased mortality in non-typhoid salmonellosis: a one-year follow-up study. APMIS 116(2):147–153
Zaidi E, Bachur R, Harper M (1999) Non-typhi Salmonella bacteremia in children. Pediatr Infect Dis J 18(12):1073–1077
Yen YF, Wang FD, Chiou CS, Chen YY, Lin ML, Chen TL, Liu CY (2009) Prognostic factors and clinical features of non-typhoid Salmonella bacteremia in adults. J Chin Med Assoc 72(8):408–413
Lee S-C, Yang P-H, Shieh W-B, Lasserre R (1994) Bacteremia due to non-typhi Salmonella: analysis of 64 cases and review. Clin Infect Dis 19:693–696
Wilkins EG, Roberts C (1988) Extraintestinal salmonellosis. Epidemiol Infect 100(3):361–368
Vazquez-Torres A, Jones-Carson J, Bäumler AJ, Falkow S, Valdivia R, Brown W, Le M, Berggren R, Parks WT, Fang FC (1999) Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401(6755):804–808
Schutze GE, Schutze SE, Kirby RS (1997) Extraintestinal salmonellosis in a children’s hospital. Pediatr Infect Dis J 16(5):482–485
Schønheyder HC, Ejlertsen T (1995) Survey of extraintestinal nontyphoid Salmonella infections in a Danish region. Inverse relation of invasiveness to frequency of isolation APMIS 103(9):686–688
Rodríguez M, de Diego I, Mendoza MC (1998) Extraintestinal salmonellosis in a general hospital (1991 to 1996): relationships between Salmonella genomic groups and clinical presentations. J Clin Microbiol 36(11):3291–3296
Chiu CH, Lin TY, Ou JT (1999) Predictors for extraintestinal infection of non-typhoidal Salmonella in patients without AIDS. Int J Clin Pract 53(3):161–164
Chen PL, Chang CM, Wu CJ, Ko NY, Lee NY, Lee HC, Shih HI, Lee CC, Wang RR, Ko WC (2007) Extraintestinal focal infections in adults with nontyphoid Salmonella bacteraemia: predisposing factors and clinical outcome. J Intern Med 261(1):91–100
Benenson S, Raveh D, Schlesinger Y, Alberton J, Rudensky B, Hadas-Halpern I, Yinnon AM (2001) The risk of vascular infection in adult patients with nontyphi Salmonella bacteremia. Am J Med 110(1):60–63
Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D’Angelo M, Hurd S, Medus C, Cronquist A, Angulo FJ (2008) Salmonellosis outcomes differ substantially by serotype. J Infect Dis 198(1):109–114
Weinberger M, Yaron S, Agmon V, Yishai R, Rosenberg A, Peretz C (2010) Excess short- and long-term mortality following infection with non-typhoid Salmonella in Israel. Clin Microbiol Infect [Epub ahead of print]
Tauxe RV (1999) Salmonella enteritidis and Salmonella typhimurium DT104: successful subtypes in the modern world. ASM Press, Washington DC, pp 37–52
Langridge GC, Nair S, Wain J (2009) Nontyphoidal Salmonella serovars cause different degrees of invasive disease globally. J Infect Dis 199(4):602–603
Weinberger M, Keller N (2005) Recent trends in the epidemiology of non-typhoid Salmonella and antimicrobial resistance: the Israeli experience and worldwide review. Curr Opin Infect Dis 18(6):513–521
Weinberger M, Solnik-Isaac H, Shachar D, Reisfeld A, Valinsky L, Andorn N, Agmon V, Yishai R, Bassal R, Fraser A, Yaron S, Cohen D (2006) Salmonella enterica serotype Virchow: epidemiology, resistance patterns and molecular characterisation of an invasive Salmonella serotype in Israel. Clin Microbiol Infect 12:999–1005
Solnik-Isaac H, Weinberger M, Tabak M, Ben-David A, Shachar D, Yaron S (2007) Quinolone resistance of Salmonella enterica serovar Virchow isolates from humans and poultry in Israel: evidence for clonal expansion. J Clin Microbiol 45(8):2575–2579
Kauffmann F (1975) Classification of bacteria. A realistic scheme with special reference to the classification of Salmonella and Escherichia species. Munksgaard, Copenhagen
Statistical Abstracts of the Israel Central Bureau of Statistics, the State of Israel. Available online at: http://www1.cbs.gov.il/reader/shnatonenew_site.htm. last accessed: February 20, 2010)
The European Food Safety Authority (EFSA) European Centre for Disease Prevention and Control (2009) The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. The EFSA Journal 223:1–312
Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S, Smith K, Angulo FJ (2004) Invasive Salmonella infections in the United States, FoodNet, 1996–1999: incidence, serotype distribution, and outcome. Clin Infect Dis 38(Suppl 3):S149–S156
Lan R, Reeves PR, Octavia S (2009) Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol 9(5):996–1005
Sivapalasingam S, Hoekstra RM, McQuiston JR, Fields PI, Tauxe RV (2004) Salmonella bacteriuria: an increasing entity in elderly women in the United States. Epidemiol Infect 132(5):897–902
Hohmann EL (2001) Nontyphoidal salmonellosis. Clin Infect Dis 32(2):263–269
Schutze GE, Sikes JD, Stefanova R, Cave MD (1999) The home environment and salmonellosis in children. Pediatrics 103(1):E1
Wilson R, Feldman RA, Davis J, LaVenture M (1982) Salmonellosis in infants: the importance of intrafamilial transmission. Pediatrics 69(4):436–438
Khanna KV, Markham RB (1999) A perspective on cellular immunity in the elderly. Clin Infect Dis 28(4):710–713
Smith JL (1998) Foodborne illness in the elderly. J Food Prot 61(9):1229–1239
Morris JG Jr, Potter M (1997) Emergence of new pathogens as a function of changes in host susceptibility. Emerg Infect Dis 3:435–441
Laupland KB, Ross T, Pitout JD, Church DL, Gregson DB (2007) Community-onset urinary tract infections: a population-based assessment. Infection 35(3):150–153
Bengtsson C, Bengtsson U, Björkelund C, Lincoln K, Sigurdsson JA (1998) Bacteriuria in a population sample of women: 24-year follow-up study. Results from the prospective population-based study of women in Gothenburg, Sweden. Scand J Urol Nephrol 32(4):284–289
Stamm WE, Raz R (1999) Factors contributing to susceptibility of postmenopausal women to recurrent urinary tract infections. Clin Infect Dis 28(4):723–725
Hu KK, Boyko EJ, Scholes D, Normand E, Chen CL, Grafton J, Fihn SD (2004) Risk factors for urinary tract infections in postmenopausal women. Arch Intern Med 164(9):989–993
Blaser MJ, Feldman RA (1981) Salmonella bacteremia: reports to the Centers for Disease Control, 1968–1979. J Infect Dis 143:743–746
Cherubin CE, Neu HC, Imperato PJ, Harvey RP, Bellen N (1974) Septicemia with non-typhoid Salmonella. Medicine (Baltimore) 53:365–376
Altekruse SF, Yang S, Timbo BB, Angulo FJ (1999) A multi-state survey of consumer food-handling and food-consumption practices. Am J Prev Med 16(3):216–221
Yagupsky P, Maimon N, Dagan R (2002) Increasing incidence of nontyphi Salmonella bacteremia among children living in southern Israel. Int J Infect Dis 6(2):94–97
Ispahani P, Slack RC (2000) Enteric fever and other extraintestinal salmonellosis in University Hospital, Nottingham, UK, between 1980 and 1997. Eur J Clin Microbiol Infect Dis 19(9):679–687
Messer RD, Warnock TH, Heazlewood RJ, Hanna JN (1997) Salmonella meningitis in children in far north Queensland. J Paediatr Child Health 33(6):535–538
Usera MA, Echeita A, Aladueña A, Blanco MC, Reymundo R, Prieto MI, Tello O, Cano R, Herrera D, Martinez-Navarro F (1996) Interregional foodborne salmonellosis outbreak due to powdered infant formula contaminated with lactose-fermenting Salmonella virchow. Eur J Epidemiol 12:377–381
Ruiz J, Núñez ML, Sempere MA, Díaz J, Gómez J (1995) Systemic infections in three infants due to a lactose-fermenting strain of Salmonella virchow. Eur J Clin Microbiol Infect Dis 14(5):454–456
Bitsori M, Galanakis E, Maraki S, Raissaki M, Velivassakis E, Sbyrakis S (2001) Invasive Salmonella virchow infection in childhood. Scand J Infect Dis 33(11):862–865
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(1):36–39
Usera MA, Rodríguez A, Echeita A, Cano R (1998) Multiple analysis of a foodborne outbreak caused by infant formula contaminated by an atypical Salmonella virchow strain. Eur J Clin Microbiol Infect Dis 17(8):551–555
Sechter I, Katzenelson E, Reisfeld A (1991) Salmonella serovars (others than Typhi and Paratyphi) from extra-intestinal sources. Israel, 1984–9. Epidemiol Infect 106(3):485–488
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This research was supported by grant no. 1275/04 of the Israel Science Foundation.
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Zaidenstein, R., Peretz, C., Nissan, I. et al. The epidemiology of extraintestinal non-typhoid Salmonella in Israel: the effects of patients’ age and sex. Eur J Clin Microbiol Infect Dis 29, 1103–1109 (2010). https://doi.org/10.1007/s10096-010-0968-1
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DOI: https://doi.org/10.1007/s10096-010-0968-1