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Expert Opinion on Pharmacotherapy Volume 9, 2008 - Issue 16
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Review

Antibiotic management of sepsis: current concepts

Diogo Diniz Gomes Bugano Medical Student, 5th year University of São Paulo, Medical School, Rua Antônio Carlos Salles Filho 57, 05745-250 São Paulo, São Paulo, Brasil
, MS,
Luis Fernando Aranha Camargo Infectious Disease Specialist Hospital Israelita Albert Einstein, Avenida Albert Einstein 627, 5th Floor, Morumbi, 05652-900 São Paulo, São Paulo, Brasil
, MD PhD,
Jaime Freitas Bastos Hospital Israelita Albert Einstein, Intensive Care Unit, Avenida Albert Einstein 627, 5th Floor, Morumbi, 05652-900 São Paulo, Brasil +55 11 37471520; +55 11 37469411; [email protected]
, MD PhD &
Eliezer Silva Hospital Israelita Albert Einstein, Intensive Care Unit, Avenida Albert Einstein 627, 5th Floor, Morumbi, 05652-900 São Paulo, Brasil +55 11 37471520; +55 11 37469411; [email protected]
, MD PhD
Pages 2817-2828 | Published online: 20 Oct 2008

Bibliography

  • Angus DC, Linde-Zwirble WT, Lidicker J, et al. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001;29(7):1303-10
  • Martin GS, Mannino DM, Eaton S, et al. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003;348(16):1546-54
  • Dombrovskiy VY, Martin AA, Sunderram J, et al. Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003. Crit Care Med 2007;35(5):1244-50
  • Sands KE, Bates DW, Lanken PN, et al. Epidemiology of sepsis syndrome in 8 academic medical centers. JAMA 1997;278(3):234-40
  • Vincent JL, Sakr Y, Sprung CL, et al. Sepsis in European intensive care units: results of the SOAP study. Crit Care Med 2006;34(2):344-53
  • Burchardi H, Schneider H. Economic aspects of severe sepsis: a review of intensive care unit costs, cost of illness and cost effectiveness of therapy. Pharmacoeconomics 2004;22(12):793-813
  • Price J, Ekleberry A, Grover A, et al. Evaluation of clinical practice guidelines on outcome of infection in patients in the surgical intensive care unit. Crit Care Med 1999;27(10):2118-24
  • Ferrer R, Artigas A, Levy MM, et al. Improvement in process of care and outcome after a multicenter severe sepsis educational program in Spain. JAMA 2008;299(19):2294-303
  • Dellinger RP, Levy MM, Carlet JM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Intensive Care Med 2008;34(1):17-60
  • American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992;20(6):864-74
  • Esteban A, Frutos-Vivar F, Ferguson ND, et al. Sepsis incidence and outcome: contrasting the intensive care unit with the hospital ward. Crit Care Med 2007;35(5):1284-9
  • Wang HE, Shapiro NI, Angus DC, et al. National estimates of severe sepsis in United States emergency departments. Crit Care Med 2007;35(8):1928-36
  • Valles J, Rello J, Ochagavia A, et al. Community-acquired bloodstream infection in critically ill adult patients: impact of shock and inappropriate antibiotic therapy on survival. Chest 2003;123(5):1615-24
  • Kumar A, Roberts D, Wood KE, et al. Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 2006;34(6):1589-96
  • Bates DW, Sands K, Miller E, et al. Predicting bacteremia in patients with sepsis syndrome. Academic Medical Center Consortium Sepsis Project Working Group. J Infect Dis 1997;176(6):1538-51
  • Smith-Elekes S, Weinstein MP. Blood cultures. Infect Dis Clin North Am 1993;7(2):221-34
  • Safdar N, Handelsman J, Maki DG. Does combination antimicrobial therapy reduce mortality in Gram-negative bacteraemia? A meta-analysis. Lancet Infect Dis 2004;4(8):519-27
  • Paul M, Benuri-Silbiger I, Soares-Weiser K, et al. Beta lactam monotherapy versus beta lactam-aminoglycoside combination therapy for sepsis in immunocompetent patients: systematic review and meta-analysis of randomised trials. BMJ 2004;328(7441):668-72
  • Norrby SR, Geddes AM. Efficacy of cefpirome in the treatment of septicaemia. Scand J Infect Dis Suppl 1993;9151-9
  • Colardyn F, Faulkner KL. Intravenous meropenem versus imipenem/cilastatin in the treatment of serious bacterial infections in hospitalized patients. Meropenem Serious Infection Study Group. J Antimicrob Chemother 1996;38(3):523-37
  • Mehtar S, Dewar EP, Leaper DJ, et al. A multi-centre study to compare meropenem and cefotaxime and metronidazole in the treatment of hospitalized patients with serious infections. J Antimicrob Chemother 1997;39(5):631-8
  • Garau J, Blanquer J, Cobo L, et al. Prospective, randomised, multicentre study of meropenem versus imipenem/cilastatin as empiric monotherapy in severe nosocomial infections. Eur J Clin Microbiol Infect Dis 1997;16(11):789-96
  • Verwaest C. Meropenem versus imipenem/cilastatin as empirical monotherapy for serious bacterial infections in the intensive care unit. Clin Microbiol Infect 2000;6(6):294-302
  • Jaccard C, Troillet N, Harbarth S, et al. Prospective randomized comparison of imipenem-cilastatin and piperacillin-tazobactam in nosocomial pneumonia or peritonitis. Antimicrob Agents Chemother 1998;42(11):2966-72
  • Pascual A, Perea E, Alvarez M, et al. The Meropenem Yearly Susceptibility Test Information Collection antimicrobial susceptibility program in Spain: a 5-year analysis. Diagn Microbiol Infect Dis 2007;57(2):195-200
  • Gea-Banacloche JC, Opal SM, Jorgensen J, et al. Sepsis associated with immunosuppressive medications: an evidence-based review. Crit Care Med 2004;32(11 Suppl):S578-90
  • Wunderink RG, Rello J, Cammarata SK, et al. Linezolid vs vancomycin: analysis of two double-blind studies of patients with methicillin-resistant Staphylococcus aureus nosocomial pneumonia. Chest 2003;124(5):1789-97
  • Nichols RL, Graham DR, Barriere SL, et al. Treatment of hospitalized patients with complicated gram-positive skin and skin structure infections: two randomized, multicentre studies of quinupristin/dalfopristin versus cefazolin, oxacillin or vancomycin. Synercid Skin and Skin Structure Infection Group. J Antimicrob Chemother 1999;44(2):263-73
  • Swoboda S, Ober M, Hainer C, et al. Tigecycline for the treatment of patients with severe sepsis or septic shock: a drug use evaluation in a surgical intensive care unit. J Antimicrob Chemother 2008;61(3):729-33
  • Blumberg HM, Jarvis WR, Soucie JM, et al. Risk factors for candidal bloodstream infections in surgical intensive care unit patients: the NEMIS prospective multicenter study. The National Epidemiology of Mycosis Survey. Clin Infect Dis 2001;33(2):177-86
  • Mora-Duarte J, Betts R, Rotstein C, et al. Comparison of caspofungin and amphotericin B for invasive candidiasis. N Engl J Med 2002;347(25):2020-9
  • Walsh TJ, Teppler H, Donowitz GR, et al. Caspofungin versus liposomal amphotericin B for empirical antifungal therapy in patients with persistent fever and neutropenia. N Engl J Med 2004;351(14):1391-402
  • Kullberg BJ, Sobel JD, Ruhnke M, et al. Voriconazole versus a regimen of amphotericin B followed by fluconazole for candidaemia in non-neutropenic patients: a randomised non-inferiority trial. Lancet 2005;366(9495):1435-42
  • Walsh TJ, Pappas P, Winston DJ, et al. Voriconazole compared with liposomal amphotericin B for empirical antifungal therapy in patients with neutropenia and persistent fever. N Engl J Med 2002;346(4):225-34
  • Joffe AR, Muscedere J, Marshall JC, et al. The safety of targeted antibiotic therapy for ventilator-associated pneumonia: a multicenter observational study. J Crit Care 2008;23(1):82-90
  • Uzzan B, Cohen R, Nicolas P, et al. Procalcitonin as a diagnostic test for sepsis in critically ill adults and after surgery or trauma: a systematic review and meta-analysis. Crit Care Med 2006;34(7):1996-2003
  • Jensen JU, Heslet L, Jensen TH, et al. Procalcitonin increase in early identification of critically ill patients at high risk of mortality. Crit Care Med 2006;34(10):2596-602
  • Christ-Crain M, Jaccard-Stolz D, Bingisser R, et al. Effect of procalcitonin-guided treatment on antibiotic use and outcome in lower respiratory tract infections: cluster-randomised, single-blinded intervention trial. Lancet 2004;363(9409):600-7
  • Christ-Crain M, Stolz D, Bingisser R, et al. Procalcitonin guidance of antibiotic therapy in community-acquired pneumonia: a randomized trial. Am J Respir Crit Care Med 2006;174(1):84-93
  • Combes A, Luyt CE, Fagon JY, et al. Early predictors for infection recurrence and death in patients with ventilator-associated pneumonia. Crit Care Med 2007;35(1):146-54
  • Nobre V, Harbarth S, Graf JD, et al. Use of procalcitonin to shorten antibiotic treatment duration in septic patients: a randomized trial. Am J Respir Crit Care Med 2008;177(5):498-505
  • Mandell LA, Wunderink RG, Anzueto A, et al. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis 2007;44(Suppl 2):S27-72
  • van der Eerden MM, Vlaspolder F, de Graaff CS, et al. Comparison between pathogen directed antibiotic treatment and empirical broad spectrum antibiotic treatment in patients with community acquired pneumonia: a prospective randomised study. Thorax 2005;60(8):672-8
  • Metersky ML, Ma A, Bratzler DW, et al. Predicting bacteremia in patients with community-acquired pneumonia. Am J Respir Crit Care Med 2004;169(3):342-7
  • Mufson MA, Stanek RJ. Bacteremic pneumococcal pneumonia in one American City: a 20-year longitudinal study, 1978–1997. Am J Med 1999;107(1A):S34-43
  • Baddour LM, Yu VL, Klugman KP, et al. Combination antibiotic therapy lowers mortality among severely ill patients with pneumococcal bacteremia. Am J Respir Crit Care Med 2004;170(4):440-4
  • Waterer GW, Somes GW, Wunderink RG. Monotherapy may be suboptimal for severe bacteremic pneumococcal pneumonia. Arch Intern Med 2001;161(15):1837-42
  • Martinez JA, Horcajada JP, Almela M, et al. Addition of a macrolide to a beta-lactam-based empirical antibiotic regimen is associated with lower in-hospital mortality for patients with bacteremic pneumococcal pneumonia. Clin Infect Dis 2003;36(4):389-95
  • Weiss K, Low DE, Cortes L, et al. Clinical characteristics at initial presentation and impact of dual therapy on the outcome of bacteremic Streptococcus pneumoniae pneumonia in adults. Can Respir J 2004;11(8):589-93
  • Krumpe PE, Cohn S, Garreltes J, et al. Intravenous and oral mono- or combination-therapy in the treatment of severe infections: ciprofloxacin versus standard antibiotic therapy. Ciprofloxacin Study Group. J Antimicrob Chemother 1999;43(Suppl A):117-28
  • Fink MP, Snydman DR, Niederman MS, et al. Treatment of severe pneumonia in hospitalized patients: results of a multicenter, randomized, double-blind trial comparing intravenous ciprofloxacin with imipenem-cilastatin. The Severe Pneumonia Study Group. Antimicrob Agents Chemother 1994;38(3):547-57
  • Siami GA, Wilkins WT, Bess DT, et al. Comparison of ciprofloxacin with imipenem in the treatment of severe pneumonia in hospitalised geriatric patients. Drugs 1995;49(Suppl 2):436-8
  • Torres A, Bauer TT, Leon-Gil C, et al. Treatment of severe nosocomial pneumonia: a prospective randomised comparison of intravenous ciprofloxacin with imipenem/cilastatin. Thorax 2000;55(12):1033-9
  • West M, Boulanger BR, Fogarty C, et al. Levofloxacin compared with imipenem/cilastatin followed by ciprofloxacin in adult patients with nosocomial pneumonia: a multicenter, prospective, randomized, open-label study. Clin Ther 2003;25(2):485-506
  • Arancibia F, Bauer TT, Ewig S, et al. Community-acquired pneumonia due to gram-negative bacteria and pseudomonas aeruginosa: incidence, risk, and prognosis. Arch Intern Med 2002;162(16):1849-58
  • Chastre J, Wolff M, Fagon JY, et al. Comparison of 8 vs 15 days of antibiotic therapy for ventilator-associated pneumonia in adults: a randomized trial. JAMA 2003;290(19):2588-98
  • Arancibia F, Ewig S, Martinez JA, et al. Antimicrobial treatment failures in patients with community-acquired pneumonia: causes and prognostic implications. Am J Respir Crit Care Med 2000;162(1):154-60
  • Roson B, Carratala J, Fernandez-Sabe N, et al. Causes and factors associated with early failure in hospitalized patients with community-acquired pneumonia. Arch Intern Med 2004;164(5):502-8
  • Menendez R, Torres A, Zalacain R, et al. Risk factors of treatment failure in community acquired pneumonia: implications for disease outcome. Thorax 2004;59(11):960-5
  • Richards MJ, Edwards JR, Culver DH, et al. Nosocomial infections in medical intensive care units in the United States. National Nosocomial Infections Surveillance System. Crit Care Med 1999;27(5):887-92
  • Fagon JY, Chastre J, Wolff M, et al. Invasive and noninvasive strategies for management of suspected ventilator-associated pneumonia. A randomized trial. Ann Intern Med 2000;132(8):621-30
  • American Thoracic Society; Infectious Diseases Society of America. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med 2005;171(4):388-416
  • Sanchez-Nieto JM, Torres A, Garcia-Cordoba F, et al. Impact of invasive and noninvasive quantitative culture sampling on outcome of ventilator-associated pneumonia: a pilot study. Am J Respir Crit Care Med 1998;157(2):371-6
  • Iregui M, Ward S, Sherman G, et al. Clinical importance of delays in the initiation of appropriate antibiotic treatment for ventilator-associated pneumonia. Chest 2002;122(1):262-8
  • Wood GC, Hanes SD, Croce MA, et al. Comparison of ampicillin-sulbactam and imipenem-cilastatin for the treatment of acinetobacter ventilator-associated pneumonia. Clin Infect Dis 2002;34(11):1425-30
  • Paterson DL, Ko WC, Von GA, et al. Antibiotic therapy for Klebsiella pneumoniae bacteremia: implications of production of extended-spectrum beta-lactamases. Clin Infect Dis 2004;39(1):31-7
  • Varez-Lerma F. Modification of empiric antibiotic treatment in patients with pneumonia acquired in the intensive care unit. ICU-Acquired Pneumonia Study Group. Intensive Care Med 1996;22(5):387-94
  • Rello J, Ollendorf DA, Oster G, et al. Epidemiology and outcomes of ventilator-associated pneumonia in a large US database. Chest 2002;122(6):2115-21
  • Fabregas N, Ewig S, Torres A, et al. Clinical diagnosis of ventilator associated pneumonia revisited: comparative validation using immediate post-mortem lung biopsies. Thorax 1999; 54(10):867-73.
  • Veinstein A, Brun-Buisson C, Derrode N, et al. Validation of an algorithm based on direct examination of specimens in suspected ventilator-associated pneumonia. Intensive Care Med 2006;32(5):676-83
  • Shorr AF, Sherner JH, Jackson WL, et al. Invasive approaches to the diagnosis of ventilator-associated pneumonia: a meta-analysis. Crit Care Med 2005;33(1):46-53
  • Ruiz M, Torres A, Ewig S, et al. Noninvasive versus invasive microbial investigation in ventilator-associated pneumonia: evaluation of outcome. Am J Respir Crit Care Med 2000;162(1):119-25
  • The Canadian Critical Care Trials Group. A randomized trial of diagnostic techniques for ventilator-associated pneumonia. N Engl J Med 2006;355(25):2619-30
  • Muscedere J, Dodek P, Keenan S, et al. Comprehensive evidence-based clinical practice guidelines for ventilator-associated pneumonia: diagnosis and treatment. J Crit Care 2008;23(1):138-47
  • Heyland DK, Dodek P, Muscedere J, et al. Randomized trial of combination versus monotherapy for the empiric treatment of suspected ventilator-associated pneumonia. Crit Care Med 2008;36(3):737-44
  • Kljucar S, Heimesaat M, von Pritzbuer E, Olms K. [Ceftazidime with and without tobramycin versus azlocillin plus tobramycin in the therapy of bronchopulmonary infections in intensive care patients]. Infection 1987;15(Suppl 4):S185-91
  • Garnacho-Montero J, Sa-Borges M, Sole-Violan J, et al. Optimal management therapy for Pseudomonas aeruginosa ventilator-associated pneumonia: an observational, multicenter study comparing monotherapy with combination antibiotic therapy. Crit Care Med 2007;35(8):1888-95
  • Hedrick TL, McElearney ST, Smith RL, et al. Duration of antibiotic therapy for ventilator-associated pneumonia caused by non-fermentative gram-negative bacilli. Surg Infect (Larchmt ) 2007;8(6):589-97
  • Wagenlehner FM, Weidner W, Naber KG. Optimal management of urosepsis from the urological perspective. Int J Antimicrob Agents 2007;30(5):390-7
  • Tenke P, Kovacs B, Johansen TE, et al. European and Asian guidelines on management and prevention of catheter-associated urinary tract infections. Int J Antimicrob Agents 2008;31(Suppl 1):S68-78
  • Johansen TE, Cek M, Naber KG, et al. Hospital acquired urinary tract infections in urology departments: pathogens, susceptibility and use of antibiotics. Data from the PEP and PEAP-studies. Int J Antimicrob Agents 2006;28(Suppl 1):S91-107
  • Wagenlehner FM, Loibl E, Vogel H, et al. Incidence of nosocomial urinary tract infections on a surgical intensive care unit and implications for management. Int J Antimicrob Agents 2006;28(Suppl 1):S86-90
  • Harding GK, Nicolle LE, Ronald AR, et al. How long should catheter-acquired urinary tract infection in women be treated? A randomized controlled study. Ann Intern Med 1991;114(9):713-9
  • Mermel LA, Farr BM, Sherertz RJ, et al. Guidelines for the management of intravascular catheter-related infections. Infect Control Hosp Epidemiol 2001;22(4):222-42
  • Safdar N, Fine JP, Maki DG. Meta-analysis: methods for diagnosing intravascular device-related bloodstream infection. Ann Intern Med 2005;142(6):451-66
  • Raad I, Darouiche R, Vazquez J, et al. Efficacy and safety of weekly dalbavancin therapy for catheter-related bloodstream infection caused by gram-positive pathogens. Clin Infect Dis 2005;40(3):374-80
  • Raad I, Hanna H, Dvorak T, et al. Optimal antimicrobial catheter lock solution, using different combinations of minocycline, EDTA, and 25-percent ethanol, rapidly eradicates organisms embedded in biofilm. Antimicrob Agents Chemother 2007;51(1):78-83
  • Fowler VG Jr, Sanders LL, Sexton DJ, et al. Outcome of Staphylococcus aureus bacteremia according to compliance with recommendations of infectious diseases specialists: experience with 244 patients. Clin Infect Dis 1998;27(3):478-86
  • Nguyen MH, Peacock JE Jr, Tanner DC, et al. Therapeutic approaches in patients with candidemia. Evaluation in a multicenter, prospective, observational study. Arch Intern Med 1995;155(22):2429-35
  • Nucci M, Colombo AL, Silveira F, et al. Risk factors for death in patients with candidemia. Infect Control Hosp Epidemiol 1998;19(11):846-50
  • Elting LS, Bodey GP. Septicemia due to Xanthomonas species and non-aeruginosa Pseudomonas species: increasing incidence of catheter-related infections. Medicine 1990;69(5):296-306
  • Pieracci FM, Barie PS. Intra-abdominal infections. Curr Opin Crit Care 2007;13(4):440-9
  • Brook I, Frazier EH. Aerobic and anaerobic microbiology in intra-abdominal infections associated with diverticulitis. J Med Microbiol 2000;49(9):827-30
  • Roehrborn A, Thomas L, Potreck O, et al. The microbiology of postoperative peritonitis. Clin Infect Dis 2001;33(9):1513-9
  • Rossi F, Baquero F, Hsueh PR, et al. In vitro susceptibilities of aerobic and facultatively anaerobic Gram-negative bacilli isolated from patients with intra-abdominal infections worldwide: 2004 results from SMART (Study for Monitoring Antimicrobial Resistance Trends). J Antimicrob Chemother 2006;58(1):205-10
  • Mazuski JE, Sawyer RG, Nathens AB, et al. The Surgical Infection Society guidelines on antimicrobial therapy for intra-abdominal infections: an executive summary. Surg Infect (Larchmt)2002;3(3):161-73
  • Solomkin JS, Mazuski JE, Baron EJ, et al. Guidelines for the selection of anti-infective agents for complicated intra-abdominal infections. Clin Infect Dis 2003;37(8):997-1005
  • Burnett RJ, Haverstock DC, Dellinger EP, et al. Definition of the role of enterococcus in intraabdominal infection: analysis of a prospective randomized trial. Surgery 1995;118(4):716-21
  • Wong PF, Gilliam AD, Kumar S, et al. Antibiotic regimens for secondary peritonitis of gastrointestinal origin in adults. Cochrane Database Syst Rev 2005;2:CD004539
  • Eagye Kuti JL, Nicolau DP. Evaluating empiric treatment options for secondary peritonitis using pharmacodynamic profiling. Surg Infect Larchmt 2007;8(2):215-26
  • Weigelt J, Kaafarani HM, Itani KM, et al. Linezolid eradicates MRSA better than vancomycin from surgical-site infections. Am J Surg 2004;188(6):760-6
  • Falagas ME, Kasiakou SK. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis 2005;40(9):1333-41
  • Ostrosky-Zeichner L, Oude Lashof AM, Kullberg BJ, et al. Voriconazole salvage treatment of invasive candidiasis. Eur J Clin Microbiol Infect Dis 2003;22(11):651-5
  • Lennard ES, Dellinger EP, Wertz MJ, et al. Implications of leukocytosis and fever at conclusion of antibiotic therapy for intra-abdominal sepsis. Ann Surg 1982;195(1):19-24
  • Rivers E, Nguyen B, Havstad S, et al. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 2001;345(19):1368-77
  • Gao F, Melody T, Daniels DF, et al. The impact of compliance with 6-hour and 24-hour sepsis bundles on hospital mortality in patients with severe sepsis: a prospective observational study. Crit Care 2005;9(6):R764-70
  • Micek ST, Roubinian N, Heuring T, et al. Before-after study of a standardized hospital order set for the management of septic shock. Crit Care Med 2006;34(11):2707-13
  • Kortgen A, Niederprum P, Bauer M. Implementation of an evidence-based ‘standard operating procedure’ and outcome in septic shock. Crit Care Med 2006;34(4):943-9
  • Shorr AF, Micek ST, Jackson WL Jr, et al. Economic implications of an evidence-based sepsis protocol: can we improve outcomes and lower costs? Crit Care Med 2007;35(5):1257-62
  • Talmor D, Greenberg D, Howell MD, et al. The costs and cost-effectiveness of an integrated sepsis treatment protocol. Crit Care Med 2008;36(4):1168-74

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