Infections caused by non-Typhi serovars of Salmonella at the
Infectious Diseases Clinic of the University Hospital Brno in 2011–2013

Authors: P. Polák 1,2;  M. Vrba 3;  Z. Bortlíček 4;  J. Juránková 3,5;  M. Freibergerová 1;  P. Husa 1,2;  J. Kamelander 6;  M. Dastych 1
Authors‘ workplace: Lékařská fakulta Masarykovy univerzity Brno 1;  Klinika infekčních chorob, Fakultní nemocnice Brno 2;  Oddělení klinické mikrobiologie, Fakultní nemocnie Brno 3;  Ústav biostatistiky a analýz, Masarykova univerzita Brno 4;  Katedra laboratorních metod, Lékařská fakulta Masarykovy univerzity Brno 5;  Oddělení klinické hematologie, Fakultní nemocnice Brno 6;  Oddělení klinické biochemie, Fakultní nemocnice Brno 7
Published in: Epidemiol. Mikrobiol. Imunol. 63, 2014, č. 4, s. 289-296
Category: Review articles, original papers, case report


The aim of the study is to describe the basic clinical, laboratory, and microbiological characteristics in adult patients with salmonellosis hospitalized at the Infectious Diseases Clinic of the University Hospital Brno in 2011–2013.

Materials and methods:
A retrospective analysis of clinical and laboratory parameters of 161 patients hospitalized at the Infectious Diseases Clinic of the University Hospital Brno from 1 January 2011 to 31 December 2013.

Invasive salmonellosis was seen in 22.4 % of the study group. The overall lethality rate reached 3.1 %. Treatment with antibiotics was used in 93.8% of patients. Transient mild to moderate leukocytopenia was reported in 4.3 % of patients and thrombocytopenia in 9.3% of patients. Transient changes in white blood cells as well as in the thrombocyte count were not clinically important. Long-term treatment with proton pump inhibitors is a risk factor for salmonellosis (p = 0.128), but not for invasive salmonellosis. Long-term use of opioids (p = 0.003) and/or acetylsalicylic acid (p = 0.015) is a risk factor for invasive salmonellosis. Other risk factors for invasive disease are: age over 70 years (p = 0.011), arterial hypertension (p = 0.004), disease duration of less than three days (p = 0.006), serum creatinine level above 250 μmol/l (p = 0.01), peripheral leucocyte count above 12 x 109/l (p=0.001), and body temperature above 38 °C (p = 0.001). Hypokalemia does not represent a risk factor for invasive salmonellosis.

Aged patients on long-term opioids or acetylsalicylic acid, with disease duration of less than three days, and meeting the criteria for systemic inflammatory response syndrome are at the highest risk for invasive salmonellosis. Empirical antibiotics are prescribed too often and the treatment is not properly de-escalated.

almonellosis – antibiotic resistance – sepsis – carriage


1. Ahmer BM, Gunn JS. Interaction of Salmonella spp. with the intestinal microbiota. Front Microbiol, 2011;2:1–9.

2. Akwar HT, Poppe C, Wilson J, et al. Associations of antimicrobial uses with antimicrobial resistance of fecal Escherichia coli from pigs on 47 farrow-to-finish farms in Ontario and British Columbia. Can J Vet Res, 2008;72(2):202–210.

3. Bertelsen LS, Paesold G, Eckmann L, et al. Salmonella infection induces a hypersecretory phenotype in human intestinal xenografts by inducing cyclooxygenase 2. Infect Immun, 2003;71(4):2102–2109.

4. Botti V, Navillod FV, Domenis L, et al. Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet Ital, 2013;49(2):195–202.

5. Bowman CC, Bost KL. Cyclooxygenase-2-mediated prostaglandin E2 production in mesenteric lymph nodes and in cultured macrophages and dendritic cells after infection with Salmonella. J Immunol, 2004;172(4):2469–2475.

6. Crawford JM, Clardy J. Bacterial symbionts and natural products. Chem Commun (Camb), 2011;47(27):7559–7566.

7. Černý Z, Nezval J, Latová Z, et al. Salmoneloza u dospělých. Výskyt a klinické projevy na Klinice infekčních chorob v Brně v letech 1970 až 1975. Čas Lek Čes, 1977;116(12):373-7.

8. Elhadi N, Aljindan R, Aljeldah M. Prevalence of nontyphoidal Salmonella serogroups and their antimicrobial resistance patterns in a university teaching hospital in Eastern Province of Saudi Arabia. Infect Drug Resist, 2013;6:199–205.

9. Farhadi A, Gundlapalli S, Shaikh M, et al. Susceptibility to gut leakiness: a possible mechanism for endotoxaemia in non-alcoholic steatohepatitis. Liver Int, 2008;28(7):1026–1033.

10. Feasey NA, Dougan G, Kingsley RA, et al. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet, 2012;379(9835):2489–2499.

11. Feng P, Rahim RT, Cowan A, et al. Effects of mu, kappa or delta opioids administered by pellet or pump on oral Salmonella infection and gastrointestinal transit. Eur J Pharmacol, 2006;534(1-3):250–257.

12. Gordon MA. Invasive nontyphoidal Salmonella disease: epidemiology, pathogenesis and diagnosis. Curr Opin Infect Dis, 2011;24(5):484–489.

13. Haiko J, Suomalainen M, Ojala T, et al. Invited review: Breaking barriers-attack on innate immune defences by omptin surface proteases of enterobacterial pathogens. Innate Immun, 2009;15(2):67–80.

14. Hernández SB, Cota I, Ducret A, et al. Adaptation and preadaptation of Salmonella enterica to bile. PLoS Genet, 2012;8(1):e1002459.

15. Hsu RB, Tsay YG, Chen RJ, et al. Risk factors for primary bacteremia and endovascular infection in patients without acquired immunodeficiency syndrome who have nontyphoid salmonellosis. Clin Infect Dis, 2003;36(7):829–834.

16. Hugunin KM, Fry C, Shuster K, et al. Effects of tramadol and buprenorphine on select immunologic factors in a cecal ligation and puncture model. Shock, 2010;34(3):250–260.

17. Chen PL, Chang CM, Wu CJ, et al. Extraintestinal focal infections in adults with nontyphoid Salmonella bacteraemia: predisposing factors and clinical outcome. J Intern Med, 2007;261(1):91–100.

18. Chen PL, Lee CC, Li CY, et al. A simple scoring algorithm predicting vascular infections in adults with nontyphoid Salmonella bacteremia. Clin Infect Dis, 2012;55(2):194–200.

19. Kim M, Kim S, Park B, et al. Core Lipopolysaccharide-specific phage SSU5 as an auxiliary component of a phage cocktail for Salmonella biocontrol. Appl Environ Microbiol, 2014;80(3):1026–34.

20. Kocianová H, Litvová S, Štefkovičová M, et al. Exotickí domáci miláčikovia jako potenciálny zdroj salmonel. Epidemiol Mikrobiol Imunol, 2010;59(1):9–12.

21. Kotalová R. Léčba akutních gastroenteritid. Postgrad Med, 2010;12(suppl. 2):6–15.

22. Laupland KB, Schønheyder HC, Kennedy KJ, et al. Salmonella enterica bacteraemia: a multi-national population-based cohort study. BMC Infect Dis, 2010;10(95):1–6.

23. Magiorakos AP, Srinivasan A, Carey RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Inf, 2011;18(3):268–281.

24. Martins A, Hunyadi A, Amaral L. Mechanisms of resistance in bacteria: an evolutionary approach. Open Microbiol J, 2013;7:53–58.

25. Mather AE, Reid SW, Maskell DJ, et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science, 2013;341(6153):1514–1517.

26. Myšková P, Karpíšková R, Dědičová D. Epidemické případy salmonelóz v České republice v roce 2012. Epidemiol Mikrobiol Imunol, 2013;62(2):59–63.

27. Okoro CK, Kingsley RA, Connor TR et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet, 2012;44(11):1215–21.

28. Onwuezobe IA, Oshun PO, Odigwe CC. Antimicrobials for treating symptomatic non-typhoidal Salmonella infection. Cochrane Database Syst Rev, 2012;11:CD001167.

29. O’Regan E, Quinn T, Pagès JM, et al. Multiple regulatory pathways associated with high-level ciprofloxacin and multidrug resistance in Salmonella enterica serovar enteritidis: involvement of RamA and other global regulators. Antimicrob Agents Chemother, 2009;53(3):1080–1087.

30. Osterberg J, Ljungdahl M, Haglund U. Influence of cyclooxygenase inhibitors on gut immune cell distribution and apoptosis rate in experimental sepsis. Shock, 2006;25(2):147–154.

31. Parry CM, Thomas S, Aspinall EJ, et al. A retrospective study of secondary bacteraemia in hospitalised adults with community acquired non-typhoidal Salmonella gastroenteritis. BMC Infect Dis, 2013;13(107):1–10.

32. Poracká L´, Kmeťová M, Schréter I, et al. Niektoré klinické hľadiská pri vybraných bakteriálnych črevných nákazách. Časť 3. Retrospektívny pohľad na salmonelózu. Slov Lek, 2000;10(24):202–205.

33. Romero D, Traxler MF, López D, et al. Antibiotics as signal molecules. Chem Rev, 2011;111(9):5492–5505.

34. Roy S, Ninkovic J, Banerjee S, et al. Opioid drug abuse and modulation of immune function: consequences in the susceptibility to opportunistic infections. J Neuroimmune Pharmacol, 2011;4:442–465.

35. Sánchez-Vargas FM, Abu-El-Haija MA, Gómez-Duarte OG. Salmonella infections: an update on epidemiology, management, and prevention. Travel Med Infect Dis, 2011;9(6):263–77.

36. Sharma M. Lytic bacteriophages: Potential interventions against enteric bacterial pathogens on produce. Bacteriophage, 2013;1(3):2: e25518.

37. Šrámová H, Karpíšková R, Beneš Č. Salmonelózy v České re-publice v letech 1989-1998. Epidemiol, mikrobiol, imunol. 2000;49(1):34–38.

38. van der Veen EL, Schilder AG, Timmers TK, et al. Effect of long-term trimethoprim/sulfamethoxazole treatment on resistance and integron prevalence in the intestinal flora: a randomized, double-blind, placebo-controlled trial in children. J Antimicrob Chemother, 2009;63(5):1011–1016.

39. Vega NM, Allison KR, Samuels AN, et al. Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance. Proc Natl Acad Sci USA, 2013;110(35):14420–14425.

40. Weinberger M, Andorn N, Agmon V, et al. Blood invasiveness of Salmonella enterica as a function of age and serotype. Epidemiol Infect, 2004;132(6):1023–1028.

41. Woodford N, Wareham DW, Guerra B, et al. Carbapenemase-producing Enterobacteriaceae and non-Enterobacteriaceae from animals and the environment: an emerging public health risk of our own making? J Antimicrob Chemother, 2014;69(2):287–291.

42. Žemličková H, Dědičová D, Jakubů V, et al. Antibiotická rezistence u netyfových sérovarů Salmonella spp. v České republice. Epidemiol Mikrobiol Imunol, 2013;62(2):43–49.

43. The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2012[online]. Dostupný na

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