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February 26, 1997, Vol 277, No. 8 >
ARTICLE | February 26, 1997

Relationship of Microbiologic Diagnostic Criteria to Morbidity and Mortality in Patients With Ventilator-Associated Pneumonia FREE

Fabienne Bregeon, MD; Laurent Papazian, MD; Alexandre Visconti, MD; Régine Gregoire, MD; Xavier Thirion, MD; François Gouin, MD
[+] Author Affiliations

Reprints: Fabienne Bregeon, MD, Département d'Anesthésiology-Réanimation, Hôpital Sainte-Marguerite, 13274 Marseille Cedex 9, France.

Concepts in Emergency and Critical Care section editor: Roger C. Bone, MD, Consulting Editor, JAMA.

Advisory Panel: Bart Chernow, MD, Baltimore, Md; David Dantzker, MD, New Hyde Park, NY; Jerrold Leiken, MD, Chicago, III; Joseph E. Parrillo, MD, Chicago, III; William J. Sibbald, MD, London, Ontario; and Jean-Louis Vincent, MD, PhD, Brussels, Belgium.


JAMA. 1997;277(8):655-662. doi:10.1001/jama.1997.03540320057036
Text Size: A A A
Published online
Article
References

Objective.  —To evaluate whether the mortality and the morbidity of ventilatorassociated pneumonia, defined by positive result of protected specimen brush culture, was different from that defined by other methods.

Design.  —Matched-cohort study. All patients with clinical suspicion of pneumonia were investigated with protected specimen brush, bronchoalveolar lavage, and blind bronchial samplings. Two groups were defined: brush-positive patients (positive culture of the protected specimen brush) and brush-negative patients (negative culture of the protected specimen brush, but positive culture with another method).

Setting.  —A 14-bed medicosurgical intensive care unit (ICU) in an 850-bed teaching hospital.

Patients.  —All patients with documented ventilator-associated pneumonia over 4 years 9 months. A total of 102 cases documented by protected specimen brush culture and 223 documented by another sampling procedure. Patients were matched according to diagnosis on admission, age, sex, date of admission, Acute Physiology and Chronic Health Evaluation II (APACHE II) score, and date of onset of pneumonia.

Main Outcome Measures.  —Mortality rate, duration of mechanical ventilation, duration of ICU stay, duration of hospital stay, sampling methods, and microbiologic cultures.

Results.  —A total of 76 pairs were submitted for analysis. The effectiveness of matching was 81.85%. There was no difference in mortality between brush-positive patients and brush-negative patients. The ICU fatality rate was 38% in the brushpositive group and 39.4% in the brush-negative group (odds ratio [OR], 0.95; 95% confidence interval [CI], 0.46-1.93). The hospital fatality rate was 41% (OR, 1; 95% CI, 0.5-2.01). The mean (SD) duration of ventilation was 26(23) days in the 2 groups (range, 3-132 days). The duration of ICU stay was 33 (27.4) days in the 2 groups (range, 3-152 days).

Conclusions.  —When confounding factors are controlled, patient outcome is the same if ventilator-associated pneumonia has been diagnosed by protected specimen brush or by another sampling method.

REFERENCES

1 +
Knaus WA.  Prognosis with mechanical ventilation: the influence of disease, severity of disease, age and chronic health status on survival from an acute illness . Am Rev Respir Dis . 1989;;140:S8-S13.
2 +
Langer M, Mosconi P, Cigada M, Mandelli M, Tognoni G, ICUGIC.  Long-term respiratory support and risk of pneumonia in critically ill patients . Am Rev Respir Dis . 1989;;140:302-305.
3 +
Gross PA, Van Antwerpen C.  Nosocomial infections and hospital deaths: a case-control study . Am J Med . 1983;;75:658-661.
4 +
Craig CP, Connelly S.  Effect of intensive care unit nosocomial pneumonia on duration of stay and mortality . Am J Infect Control . 1984;;12:233-238.
5 +
Craven DE, Kunches LM, Kilinsky V, Lichtenberg DA, Make BJ, McCabe WR.  Risk factors for pneumonia and fatality in patients receiving continuous mechanical ventilation . Am Rev Respir Dis . 1986;;133:792-796.
6 +
Leu HS, Kaiser DL, Mori M, Woolson RF, Wenzel RP.  Hospital-acquired pneumonia attributable mortality and morbidity . Am J Epidemiol . 1989;; 129:1258-1267.
7 +
Torres A, Aznar R, Mariagatell J, et al.  Incidence, risk and prognosis factors of nosocomial pneumonia in mechanically ventilated patients . Am Rev Respir Dis . 1990;;142:523-528.
8 +
Rello J, Quitana E, Ausina V, Castella J, Luquin M, Prats G.  Incidence, etiology and outcome of nosocomial pneumonia in mechanically ventilated patients . Chest . 1991;;100:439-444.
9 +
Kollef MH.  Ventilator-associated pneumonia: a multivariate analysis . JAMA . 1993;;270:1965-1970.
10 +
Fagon JY, Chastre J, Hance AJ, Montravers P, Novara A, Gibert C.  Nosocomial pneumonia in ventilated patients: a cohort study evaluating attributable mortality and hospital stay . Am J Med . 1993;; 94:281-288.
11 +
Papazian L, Brégeon F, Thirion X, et al.  Effect of ventilator-associated pneumonia on mortality and morbidity . Am J Respir Crit Care Med . 1996;;154:91-97.
12 +
Papazian L, Thomas P, Garbe L, et al.  Bronchoscopic or blind bronchial sampling techniques for the diagnosis of ventilator-associated pneumonia . Am J Respir Crit Care Med . 1995;;152:1982-1891.
13 +
Torres A, El-Ebiary M, Padro L, et al.  Validation of different techniques for the diagnosis of ventilator-associated pneumonia: comparison with immediate postmortem pulmonary biopsy . Am J Respir Crit Care Med . 1994;;149:324-331.
14 +
Marquette CH, Copin M-C, Wallet F, et al.  Diagnostic tests for pneumonia in ventilated patients: prospective evaluation of diagnostic accuracy using histology as a diagnostic gold standard . Am Rev Respir Dis . 1995;;151:1878-1888.
15 +
Pingleton SK, Fagon J-Y, Leeper KV.  Patient selection for clinical investigation of ventilator-associated pneumonia: criteria for evaluating diagnostic technique . Chest . 1992;;102( (suppl) ):553S-556S.
16 +
Van Saene HKF, Stoutenbeeck CP, Zandstra DF.  Eleven important definitions . Réan Urg . 1992;; 1:385-387.
17 +
Rouby JJ, Rossignon MD, Nicolas MH, et al.  A prospective study of protected bronchoalveolar lavage in the diagnosis of nosocomial pneumonia . Anesthesiology . 1989;;71:79-85.
18 +
Pham LH, Brun-Buisson C, Legrand P, et al.  Diagnosis of nosocomial bronchopneumonia in mechanically ventilated patients: comparison of a plugged telescoping catheter with the protected specimen brush . Am Rev Respir Dis . 1991;;143:1055-1061.
19 +
Wimberley N, Faling LJ, Bartlett JG.  A fiberoptic bronchoscopy technique to obtain uncontaminated lower airway secretions for bacterial culture . Am Rev Respir Dis . 1979;;119:337-343.
20 +
Chastre J, Viau F, Brun P, et al.  Prospective evaluation of the protected specimen brush for the diagnosis of pulmonary infections in ventilated patients . Am Rev Respir Dis . 1984;;130:924-929.
21 +
Knaus WA, Draper EA, Wagner DP, Zimmerman JE.  APACHE II: a severity of disease classification system . Crit Care Med . 1985;;13:818-829.
22 +
McCabe WR, Jackson GG.  Gram negative bacteremia: etiology and ecology . Arch Intern Med . 1962;;110:847-864.
23 +
Knaus WA, Draper EA, Wagner DP, Zimmerman JE.  Prognosis in acute organ-system failure . Ann Surg . 1985;;202:685-693.
24 +
SAS User's Guide: Statistics, Version 5. Cary, NC: SAS Institute Inc; 1988:126-154.
25 +
Wayne WD.  Paired comparison test . In: Daniel WW. Biostatistics: A Foundation for Analysis in the Health Sciences . 6th ed. New York, NY: John Wiley & Sons Inc; 1995;:235-241.
26 +
Kleinbaum DG, Kapper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods . New York, NY: Van Nostrand Reinhold Co; 1982;.
27 +
Kappstein FG, Schulgen T, Beyer U, Geiger F, Schumacher M, Daschner FD.  Prolongation of hospital stay and extracost due to ventilator-associated pneumonia in an intensive care unit . Eur J Clin Microbiol Infect Dis . 1992;;11:504-508.
28 +
Fagon J-Y, Chastre J, Hance AJ, et al.  Detection of nosocomial lung infection in ventilated patients: use of protected specimen brush and quantitative culture techniques in 147 patients . Am Rev Respir Dis . 1988;;138:110-116.
29 +
Baker AM, Bowton DL, Haponik EF.  Decision making in nosocomial pneumonia: an analytic approach to the interpretation of quantitative bronchoscopic cultures . Chest . 1995;;107:85-95.
30 +
Kollef MH, Silver P, Murphy DM, Trovillion E.  The effect of late-onset ventilator associated pneumonia in determining patient mortality . Chest . 1995;; 108:1655-1662.
31 +
Rello J, Torres A, Ricart M, et al.  Ventilator-associated pneumonia by Staphylococcus aureus . Am J Respir Crit Care Med . 1994;;150:1545-1549.
32 +
Prod'hom G, Leuenberger P, Koerfer J, Blum A, Chiolero R, Schaller M-D.  Nosocomial pneumonia in mechanically ventilated patients receiving antacid, ranitidine or sucralfate as prophylaxis for stress ulcer . Ann Intern Med . 1994;;120:653-662.
33 +
Kollef MH, Shapiro SD, Fraser VJ, et al.  Mechanical ventilation with or without 7-day circuit changes . Ann Intern Med . 1995;;123:168-174.
34 +
Baker AM, Meredith J, Haponik EF.  Pneumonia in intubated trauma patients: microbiology and outcome . Am J Respir Crit Care Med . 1996;;153:343-349.
35 +
Andrews CP, Coalson JJ, Smith JD, Johanson WG.  Diagnosis of nosocomial bacterial pneumonia in acute, diffuse lung injury . Chest . 1981;;80:254-258.
36 +
Fagon J-Y, Chastre J, Domart Y, et al.  Nosocomial pneumonia in patients receiving continuous mechanical ventilation: prospective analysis of 52 episodes with use of a protected specimen brush and quantitative culture techniques . Am Rev Respir Dis . 1989;;139:877-884.
37 +
Chevret S, Hemmer M, Carlet J, Langer M.  European Cooperative Group on Nosocomial Pneumonia: incidence and risk factors of pneumonia acquired in intensive care units . Intensive Care Med . 1993;;19:256-264.
38 +
Gastinne H, Wolff M, Delatour F, Faurisson F, Chevret S.  A controlled trial in intensive care units of selective decontamination of the digestive tract with nonabsorbable antibiotics . N Engl J Med . 1992;; 326:594-599.
39 +
Vincent J-L, Bihari DJ, Suter PM, et al, for the EPIC International Advisory Committee.  The prevalence of nosocomial infection in intensive care units in Europe: results of the European Prevalence of Infection in Intensive Care (EPIC) study . JAMA . 1995;;274:639-644.
40 +
Jimenez P, Torres A, Rodriguez-Roisin R, et al.  Incidence and etiology of pneumonia acquired during mechanical ventilation . Crit Care Med . 1989;; 17:882-885.
41 +
Torres A, Gatell JM, Aznar E, et al.  Re-intubation increases the risk of nosocomial pneumonia in patients needing mechanical ventilation . Am J Respir Crit Care Med . 1995;;152:137-141.
42 +
Djedaini K, Billiard M, Mier L, et al.  Changing heat and moisture exchangers every 48 hours rather than 24 hours does not affect their efficacy and the incidence of nosocomial pneumonia . Am J Respir Crit Care Med . 1995;;152:1562-1569.
43 +
Rouby JJ, Poète P, Martin De La Salle E, et al.  Prevention of gram-negative nosocomial bronchopneumonia by intratracheal colistin in critically ill patients . Intensive Care Med . 1994;;20:187-192.
44 +
Aubas S, Aubas P, Capdevila X, Darbas H, Roustan JP, Du Cailar J.  Bronchoalveolar lavage for diagnosing bacterial pneumonia in mechanically ventilated patients . Am J Respir Crit Care Med . 1994;;149:860-866.
45 +
Cohen IL, Lambrinos J.  Investigating the impact of age on outcome of mechanical ventilation using a population of 41,848 patients from a statewide database . Chest . 1995;;107:1673-1680.
46 +
Langer M, Cigada M, Mandelli M, Mosconi P, Tognoni G, ICUGIC.  Early onset pneumonia: a multicenter study in intensive care units . Intensive Care Med . 1987;;13:342-346.
47 +
Fagon J-Y, Chastre J, Hance AJ, Domart Y, Trouillet J-L, Gibert C.  Evaluation of clinical judgment in the identification and treatment of nosocomial pneumonia . Chest . 1993;;103:547-553.
48 +
Niederman MS, Torres A, Summer W.  Invasive diagnostic testing is not needed routinely to manage suspected ventilator-associated pneumonia . Am J Respir Crit Care Med . 1994;;150:565-569.
49 +
Kollef MH.  Ventilator-associated pneumonia: a multivariate analysis . JAMA . 1993;;270:1965-1970.
50 +
Salata RA, Lederman MM, Shlaes DM, et al.  Diagnosis of nosocomial pneumonia in intubated, intensive care unit patients . Am Rev Respir Dis . 1987;;135:326-332.
51 +
Moore RD, Smith CR, Lietman PS.  Association of aminoglycoside plasma levels with therapeutic outcome in gram-negative pneumonia . Am J Med . 1984;;77:657-662.
52 +
Rello J, Ausina V, Ricart M, Castella J, Prats G.  Impact of previous antimicrobial therapy on the etiology and outcome of ventilator-associated pneumonia . Chest . 1993;;104:1230-1235.

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

1 +
Knaus WA.  Prognosis with mechanical ventilation: the influence of disease, severity of disease, age and chronic health status on survival from an acute illness . Am Rev Respir Dis . 1989;;140:S8-S13.
2 +
Langer M, Mosconi P, Cigada M, Mandelli M, Tognoni G, ICUGIC.  Long-term respiratory support and risk of pneumonia in critically ill patients . Am Rev Respir Dis . 1989;;140:302-305.
3 +
Gross PA, Van Antwerpen C.  Nosocomial infections and hospital deaths: a case-control study . Am J Med . 1983;;75:658-661.
4 +
Craig CP, Connelly S.  Effect of intensive care unit nosocomial pneumonia on duration of stay and mortality . Am J Infect Control . 1984;;12:233-238.
5 +
Craven DE, Kunches LM, Kilinsky V, Lichtenberg DA, Make BJ, McCabe WR.  Risk factors for pneumonia and fatality in patients receiving continuous mechanical ventilation . Am Rev Respir Dis . 1986;;133:792-796.
6 +
Leu HS, Kaiser DL, Mori M, Woolson RF, Wenzel RP.  Hospital-acquired pneumonia attributable mortality and morbidity . Am J Epidemiol . 1989;; 129:1258-1267.
7 +
Torres A, Aznar R, Mariagatell J, et al.  Incidence, risk and prognosis factors of nosocomial pneumonia in mechanically ventilated patients . Am Rev Respir Dis . 1990;;142:523-528.
8 +
Rello J, Quitana E, Ausina V, Castella J, Luquin M, Prats G.  Incidence, etiology and outcome of nosocomial pneumonia in mechanically ventilated patients . Chest . 1991;;100:439-444.
9 +
Kollef MH.  Ventilator-associated pneumonia: a multivariate analysis . JAMA . 1993;;270:1965-1970.
10 +
Fagon JY, Chastre J, Hance AJ, Montravers P, Novara A, Gibert C.  Nosocomial pneumonia in ventilated patients: a cohort study evaluating attributable mortality and hospital stay . Am J Med . 1993;; 94:281-288.
11 +
Papazian L, Brégeon F, Thirion X, et al.  Effect of ventilator-associated pneumonia on mortality and morbidity . Am J Respir Crit Care Med . 1996;;154:91-97.
12 +
Papazian L, Thomas P, Garbe L, et al.  Bronchoscopic or blind bronchial sampling techniques for the diagnosis of ventilator-associated pneumonia . Am J Respir Crit Care Med . 1995;;152:1982-1891.
13 +
Torres A, El-Ebiary M, Padro L, et al.  Validation of different techniques for the diagnosis of ventilator-associated pneumonia: comparison with immediate postmortem pulmonary biopsy . Am J Respir Crit Care Med . 1994;;149:324-331.
14 +
Marquette CH, Copin M-C, Wallet F, et al.  Diagnostic tests for pneumonia in ventilated patients: prospective evaluation of diagnostic accuracy using histology as a diagnostic gold standard . Am Rev Respir Dis . 1995;;151:1878-1888.
15 +
Pingleton SK, Fagon J-Y, Leeper KV.  Patient selection for clinical investigation of ventilator-associated pneumonia: criteria for evaluating diagnostic technique . Chest . 1992;;102( (suppl) ):553S-556S.
16 +
Van Saene HKF, Stoutenbeeck CP, Zandstra DF.  Eleven important definitions . Réan Urg . 1992;; 1:385-387.
17 +
Rouby JJ, Rossignon MD, Nicolas MH, et al.  A prospective study of protected bronchoalveolar lavage in the diagnosis of nosocomial pneumonia . Anesthesiology . 1989;;71:79-85.
18 +
Pham LH, Brun-Buisson C, Legrand P, et al.  Diagnosis of nosocomial bronchopneumonia in mechanically ventilated patients: comparison of a plugged telescoping catheter with the protected specimen brush . Am Rev Respir Dis . 1991;;143:1055-1061.
19 +
Wimberley N, Faling LJ, Bartlett JG.  A fiberoptic bronchoscopy technique to obtain uncontaminated lower airway secretions for bacterial culture . Am Rev Respir Dis . 1979;;119:337-343.
20 +
Chastre J, Viau F, Brun P, et al.  Prospective evaluation of the protected specimen brush for the diagnosis of pulmonary infections in ventilated patients . Am Rev Respir Dis . 1984;;130:924-929.
21 +
Knaus WA, Draper EA, Wagner DP, Zimmerman JE.  APACHE II: a severity of disease classification system . Crit Care Med . 1985;;13:818-829.
22 +
McCabe WR, Jackson GG.  Gram negative bacteremia: etiology and ecology . Arch Intern Med . 1962;;110:847-864.
23 +
Knaus WA, Draper EA, Wagner DP, Zimmerman JE.  Prognosis in acute organ-system failure . Ann Surg . 1985;;202:685-693.
24 +
SAS User's Guide: Statistics, Version 5. Cary, NC: SAS Institute Inc; 1988:126-154.
25 +
Wayne WD.  Paired comparison test . In: Daniel WW. Biostatistics: A Foundation for Analysis in the Health Sciences . 6th ed. New York, NY: John Wiley & Sons Inc; 1995;:235-241.
26 +
Kleinbaum DG, Kapper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods . New York, NY: Van Nostrand Reinhold Co; 1982;.
27 +
Kappstein FG, Schulgen T, Beyer U, Geiger F, Schumacher M, Daschner FD.  Prolongation of hospital stay and extracost due to ventilator-associated pneumonia in an intensive care unit . Eur J Clin Microbiol Infect Dis . 1992;;11:504-508.
28 +
Fagon J-Y, Chastre J, Hance AJ, et al.  Detection of nosocomial lung infection in ventilated patients: use of protected specimen brush and quantitative culture techniques in 147 patients . Am Rev Respir Dis . 1988;;138:110-116.
29 +
Baker AM, Bowton DL, Haponik EF.  Decision making in nosocomial pneumonia: an analytic approach to the interpretation of quantitative bronchoscopic cultures . Chest . 1995;;107:85-95.
30 +
Kollef MH, Silver P, Murphy DM, Trovillion E.  The effect of late-onset ventilator associated pneumonia in determining patient mortality . Chest . 1995;; 108:1655-1662.
31 +
Rello J, Torres A, Ricart M, et al.  Ventilator-associated pneumonia by Staphylococcus aureus . Am J Respir Crit Care Med . 1994;;150:1545-1549.
32 +
Prod'hom G, Leuenberger P, Koerfer J, Blum A, Chiolero R, Schaller M-D.  Nosocomial pneumonia in mechanically ventilated patients receiving antacid, ranitidine or sucralfate as prophylaxis for stress ulcer . Ann Intern Med . 1994;;120:653-662.
33 +
Kollef MH, Shapiro SD, Fraser VJ, et al.  Mechanical ventilation with or without 7-day circuit changes . Ann Intern Med . 1995;;123:168-174.
34 +
Baker AM, Meredith J, Haponik EF.  Pneumonia in intubated trauma patients: microbiology and outcome . Am J Respir Crit Care Med . 1996;;153:343-349.
35 +
Andrews CP, Coalson JJ, Smith JD, Johanson WG.  Diagnosis of nosocomial bacterial pneumonia in acute, diffuse lung injury . Chest . 1981;;80:254-258.
36 +
Fagon J-Y, Chastre J, Domart Y, et al.  Nosocomial pneumonia in patients receiving continuous mechanical ventilation: prospective analysis of 52 episodes with use of a protected specimen brush and quantitative culture techniques . Am Rev Respir Dis . 1989;;139:877-884.
37 +
Chevret S, Hemmer M, Carlet J, Langer M.  European Cooperative Group on Nosocomial Pneumonia: incidence and risk factors of pneumonia acquired in intensive care units . Intensive Care Med . 1993;;19:256-264.
38 +
Gastinne H, Wolff M, Delatour F, Faurisson F, Chevret S.  A controlled trial in intensive care units of selective decontamination of the digestive tract with nonabsorbable antibiotics . N Engl J Med . 1992;; 326:594-599.
39 +
Vincent J-L, Bihari DJ, Suter PM, et al, for the EPIC International Advisory Committee.  The prevalence of nosocomial infection in intensive care units in Europe: results of the European Prevalence of Infection in Intensive Care (EPIC) study . JAMA . 1995;;274:639-644.
40 +
Jimenez P, Torres A, Rodriguez-Roisin R, et al.  Incidence and etiology of pneumonia acquired during mechanical ventilation . Crit Care Med . 1989;; 17:882-885.
41 +
Torres A, Gatell JM, Aznar E, et al.  Re-intubation increases the risk of nosocomial pneumonia in patients needing mechanical ventilation . Am J Respir Crit Care Med . 1995;;152:137-141.
42 +
Djedaini K, Billiard M, Mier L, et al.  Changing heat and moisture exchangers every 48 hours rather than 24 hours does not affect their efficacy and the incidence of nosocomial pneumonia . Am J Respir Crit Care Med . 1995;;152:1562-1569.
43 +
Rouby JJ, Poète P, Martin De La Salle E, et al.  Prevention of gram-negative nosocomial bronchopneumonia by intratracheal colistin in critically ill patients . Intensive Care Med . 1994;;20:187-192.
44 +
Aubas S, Aubas P, Capdevila X, Darbas H, Roustan JP, Du Cailar J.  Bronchoalveolar lavage for diagnosing bacterial pneumonia in mechanically ventilated patients . Am J Respir Crit Care Med . 1994;;149:860-866.
45 +
Cohen IL, Lambrinos J.  Investigating the impact of age on outcome of mechanical ventilation using a population of 41,848 patients from a statewide database . Chest . 1995;;107:1673-1680.
46 +
Langer M, Cigada M, Mandelli M, Mosconi P, Tognoni G, ICUGIC.  Early onset pneumonia: a multicenter study in intensive care units . Intensive Care Med . 1987;;13:342-346.
47 +
Fagon J-Y, Chastre J, Hance AJ, Domart Y, Trouillet J-L, Gibert C.  Evaluation of clinical judgment in the identification and treatment of nosocomial pneumonia . Chest . 1993;;103:547-553.
48 +
Niederman MS, Torres A, Summer W.  Invasive diagnostic testing is not needed routinely to manage suspected ventilator-associated pneumonia . Am J Respir Crit Care Med . 1994;;150:565-569.
49 +
Kollef MH.  Ventilator-associated pneumonia: a multivariate analysis . JAMA . 1993;;270:1965-1970.
50 +
Salata RA, Lederman MM, Shlaes DM, et al.  Diagnosis of nosocomial pneumonia in intubated, intensive care unit patients . Am Rev Respir Dis . 1987;;135:326-332.
51 +
Moore RD, Smith CR, Lietman PS.  Association of aminoglycoside plasma levels with therapeutic outcome in gram-negative pneumonia . Am J Med . 1984;;77:657-662.
52 +
Rello J, Ausina V, Ricart M, Castella J, Prats G.  Impact of previous antimicrobial therapy on the etiology and outcome of ventilator-associated pneumonia . Chest . 1993;;104:1230-1235.

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