Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 9/2010

01-09-2010 | Article

The epidemiology of extraintestinal non-typhoid Salmonella in Israel: the effects of patients’ age and sex

Authors: R. Zaidenstein, C. Peretz, I. Nissan, A. Reisfeld, S. Yaron, V. Agmon, M. Weinberger

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 9/2010

Login to get access

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.
Literature
1.
go back to reference 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 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
2.
go back to reference 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–S134CrossRefPubMed 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–S134CrossRefPubMed
3.
go back to reference 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–S148CrossRefPubMed 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–S148CrossRefPubMed
4.
go back to reference 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 132:1023–1028CrossRefPubMed 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 132:1023–1028CrossRefPubMed
5.
go back to reference 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):822–827CrossRefPubMed 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):822–827CrossRefPubMed
6.
go back to reference 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):81–87PubMed 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):81–87PubMed
7.
go back to reference Cohen JI, Bartlett JA, Corey GR (1987) Extra-intestinal manifestations of Salmonella infections. Medicine (Baltimore) 66:349–388 Cohen JI, Bartlett JA, Corey GR (1987) Extra-intestinal manifestations of Salmonella infections. Medicine (Baltimore) 66:349–388
8.
go back to reference Mandal BK, Brennand J (1988) Bacteraemia in salmonellosis: a 15 year retrospective study from a regional infectious diseases unit. Br Med J 297:1242–1243CrossRef Mandal BK, Brennand J (1988) Bacteraemia in salmonellosis: a 15 year retrospective study from a regional infectious diseases unit. Br Med J 297:1242–1243CrossRef
9.
go back to reference 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):151–158CrossRefPubMed 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):151–158CrossRefPubMed
10.
go back to reference 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):147–153CrossRefPubMed 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):147–153CrossRefPubMed
11.
go back to reference Zaidi E, Bachur R, Harper M (1999) Non-typhi Salmonella bacteremia in children. Pediatr Infect Dis J 18(12):1073–1077CrossRefPubMed Zaidi E, Bachur R, Harper M (1999) Non-typhi Salmonella bacteremia in children. Pediatr Infect Dis J 18(12):1073–1077CrossRefPubMed
12.
go back to reference 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):408–413CrossRefPubMed 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):408–413CrossRefPubMed
13.
go back to reference 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 19:693–696PubMed 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 19:693–696PubMed
14.
15.
go back to reference 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):804–808CrossRefPubMed 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):804–808CrossRefPubMed
16.
go back to reference Schutze GE, Schutze SE, Kirby RS (1997) Extraintestinal salmonellosis in a children’s hospital. Pediatr Infect Dis J 16(5):482–485CrossRefPubMed Schutze GE, Schutze SE, Kirby RS (1997) Extraintestinal salmonellosis in a children’s hospital. Pediatr Infect Dis J 16(5):482–485CrossRefPubMed
17.
go back to reference 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):686–688CrossRefPubMed 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):686–688CrossRefPubMed
18.
go back to reference 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):3291–3296PubMed 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):3291–3296PubMed
19.
go back to reference 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):161–164PubMed 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):161–164PubMed
20.
go back to reference 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):91–100CrossRefPubMed 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):91–100CrossRefPubMed
21.
go back to reference 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):60–63CrossRefPubMed 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):60–63CrossRefPubMed
22.
go back to reference 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):109–114CrossRefPubMed 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):109–114CrossRefPubMed
23.
go back to reference 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] 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]
24.
go back to reference Tauxe RV (1999) Salmonella enteritidis and Salmonella typhimurium DT104: successful subtypes in the modern world. ASM Press, Washington DC, pp 37–52 Tauxe RV (1999) Salmonella enteritidis and Salmonella typhimurium DT104: successful subtypes in the modern world. ASM Press, Washington DC, pp 37–52
25.
go back to reference Langridge GC, Nair S, Wain J (2009) Nontyphoidal Salmonella serovars cause different degrees of invasive disease globally. J Infect Dis 199(4):602–603CrossRefPubMed Langridge GC, Nair S, Wain J (2009) Nontyphoidal Salmonella serovars cause different degrees of invasive disease globally. J Infect Dis 199(4):602–603CrossRefPubMed
26.
go back to reference 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):513–521CrossRefPubMed 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):513–521CrossRefPubMed
27.
go back to reference 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 12:999–1005CrossRefPubMed 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 12:999–1005CrossRefPubMed
28.
go back to reference 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):2575–2579CrossRefPubMed 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):2575–2579CrossRefPubMed
29.
go back to reference Kauffmann F (1975) Classification of bacteria. A realistic scheme with special reference to the classification of Salmonella and Escherichia species. Munksgaard, Copenhagen Kauffmann F (1975) Classification of bacteria. A realistic scheme with special reference to the classification of Salmonella and Escherichia species. Munksgaard, Copenhagen
31.
go back to reference 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 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
32.
go back to reference 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–S156CrossRefPubMed 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–S156CrossRefPubMed
33.
go back to reference Lan R, Reeves PR, Octavia S (2009) Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol 9(5):996–1005CrossRefPubMed Lan R, Reeves PR, Octavia S (2009) Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol 9(5):996–1005CrossRefPubMed
34.
go back to reference 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):897–902CrossRefPubMed 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):897–902CrossRefPubMed
36.
go back to reference Schutze GE, Sikes JD, Stefanova R, Cave MD (1999) The home environment and salmonellosis in children. Pediatrics 103(1):E1CrossRefPubMed Schutze GE, Sikes JD, Stefanova R, Cave MD (1999) The home environment and salmonellosis in children. Pediatrics 103(1):E1CrossRefPubMed
37.
go back to reference Wilson R, Feldman RA, Davis J, LaVenture M (1982) Salmonellosis in infants: the importance of intrafamilial transmission. Pediatrics 69(4):436–438PubMed Wilson R, Feldman RA, Davis J, LaVenture M (1982) Salmonellosis in infants: the importance of intrafamilial transmission. Pediatrics 69(4):436–438PubMed
38.
go back to reference Khanna KV, Markham RB (1999) A perspective on cellular immunity in the elderly. Clin Infect Dis 28(4):710–713CrossRefPubMed Khanna KV, Markham RB (1999) A perspective on cellular immunity in the elderly. Clin Infect Dis 28(4):710–713CrossRefPubMed
39.
go back to reference Smith JL (1998) Foodborne illness in the elderly. J Food Prot 61(9):1229–1239PubMed Smith JL (1998) Foodborne illness in the elderly. J Food Prot 61(9):1229–1239PubMed
40.
go back to reference Morris JG Jr, Potter M (1997) Emergence of new pathogens as a function of changes in host susceptibility. Emerg Infect Dis 3:435–441CrossRefPubMed Morris JG Jr, Potter M (1997) Emergence of new pathogens as a function of changes in host susceptibility. Emerg Infect Dis 3:435–441CrossRefPubMed
41.
go back to reference Laupland KB, Ross T, Pitout JD, Church DL, Gregson DB (2007) Community-onset urinary tract infections: a population-based assessment. Infection 35(3):150–153CrossRefPubMed Laupland KB, Ross T, Pitout JD, Church DL, Gregson DB (2007) Community-onset urinary tract infections: a population-based assessment. Infection 35(3):150–153CrossRefPubMed
42.
go back to reference 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):284–289CrossRefPubMed 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):284–289CrossRefPubMed
43.
go back to reference Stamm WE, Raz R (1999) Factors contributing to susceptibility of postmenopausal women to recurrent urinary tract infections. Clin Infect Dis 28(4):723–725CrossRefPubMed Stamm WE, Raz R (1999) Factors contributing to susceptibility of postmenopausal women to recurrent urinary tract infections. Clin Infect Dis 28(4):723–725CrossRefPubMed
44.
go back to reference 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):989–993CrossRefPubMed 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):989–993CrossRefPubMed
45.
go back to reference Blaser MJ, Feldman RA (1981) Salmonella bacteremia: reports to the Centers for Disease Control, 1968–1979. J Infect Dis 143:743–746PubMed Blaser MJ, Feldman RA (1981) Salmonella bacteremia: reports to the Centers for Disease Control, 1968–1979. J Infect Dis 143:743–746PubMed
46.
go back to reference Cherubin CE, Neu HC, Imperato PJ, Harvey RP, Bellen N (1974) Septicemia with non-typhoid Salmonella. Medicine (Baltimore) 53:365–376CrossRef Cherubin CE, Neu HC, Imperato PJ, Harvey RP, Bellen N (1974) Septicemia with non-typhoid Salmonella. Medicine (Baltimore) 53:365–376CrossRef
47.
go back to reference 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):216–221CrossRefPubMed 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):216–221CrossRefPubMed
48.
go back to reference 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):94–97CrossRefPubMed 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):94–97CrossRefPubMed
49.
go back to reference 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):679–687CrossRefPubMed 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):679–687CrossRefPubMed
50.
go back to reference Messer RD, Warnock TH, Heazlewood RJ, Hanna JN (1997) Salmonella meningitis in children in far north Queensland. J Paediatr Child Health 33(6):535–538CrossRefPubMed Messer RD, Warnock TH, Heazlewood RJ, Hanna JN (1997) Salmonella meningitis in children in far north Queensland. J Paediatr Child Health 33(6):535–538CrossRefPubMed
51.
go back to reference 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 12:377–381CrossRefPubMed 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 12:377–381CrossRefPubMed
52.
go back to reference 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):454–456CrossRefPubMed 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):454–456CrossRefPubMed
53.
go back to reference 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):862–865CrossRefPubMed 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):862–865CrossRefPubMed
54.
go back to reference 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):36–39CrossRefPubMed 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):36–39CrossRefPubMed
55.
go back to reference 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):551–555PubMed 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):551–555PubMed
56.
go back to reference 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):485–488CrossRefPubMed 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):485–488CrossRefPubMed
Metadata
Title
The epidemiology of extraintestinal non-typhoid Salmonella in Israel: the effects of patients’ age and sex
Authors
R. Zaidenstein
C. Peretz
I. Nissan
A. Reisfeld
S. Yaron
V. Agmon
M. Weinberger
Publication date
01-09-2010
Publisher
Springer-Verlag
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 9/2010
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-010-0968-1

Other articles of this Issue 9/2010

European Journal of Clinical Microbiology & Infectious Diseases 9/2010 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine