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Epidemiology treatment and_outcomes_of_sa_nosocomial_pneumonia_chest_2005-1
1.
Epidemiology, Treatment, and
Outcomes of Nosocomial Bacteremic Staphylococcus aureus Pneumonia* C. Andrew DeRyke, Thomas P. Lodise, Jr., Michael J. Rybak and Peggy S. McKinnon Chest 2005;128;1414-1422 DOI 10.1378/chest.128.3.1414 The online version of this article, along with updated information and services can be found online on the World Wide Web at: http://chestjournal.chestpubs.org/content/128/3/1414.full.html Chest is the official journal of the American College of Chest Physicians. It has been published monthly since 1935. Copyright2005by the American College of Chest Physicians, 3300 Dundee Road, Northbrook, IL 60062. All rights reserved. No part of this article or PDF may be reproduced or distributed without the prior written permission of the copyright holder. (http://chestjournal.chestpubs.org/site/misc/reprints.xhtml) ISSN:0012-3692 Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
2.
Epidemiology, Treatment, and Outcomes
of Nosocomial Bacteremic Staphylococcus aureus Pneumonia* C. Andrew DeRyke, PharmD; Thomas P. Lodise, Jr., PharmD; Michael J. Rybak, PharmD, MS; and Peggy S. McKinnon, PharmD Objective: To describe outcomes associated with nosocomial bacteremic Staphylococcus aureus pneumonia (NBSAP) and to determine whether delay in adequate antimicrobial treatment is a risk factor for negative clinical and microbiological outcomes. Design: Retrospective cohort analysis. Setting: This study was conducted at Detroit Receiving Hospital and University Health Center, which is a 279-bed, level 1 trauma center in Detroit, MI. Patients: All episodes of NBSAP identified from January 1, 1999, to April 30, 2004. Results: Of 206 patients identified over a 5-year period with positive blood and respiratory cultures for S aureus, 60 patients met strict clinical, radiographic, and microbiological criteria for NBSAP. The overall mean ( SD) characteristics include the following: age, 55.5 15.0 years; acute physiology and chronic health evaluation II score, 20 (range, 3 to 41); ICU at onset, 93.3%; mechanical ventilation, 83.3%; length of stay (LOS) prior to NBSAP, 9 days (range, 2 to 81 days); methicillin-resistant S aureus (MRSA) rate, 70%; and all-cause hospital and infection-related mortality (IRM), 55.5% and 40.0%, respectively. Overall, S aureus pneumonia developed late in the patient’s hospital stay in ICU patients previously receiving mechanical ventilation and was associated with high crude mortality and IRM rates. No significant difference existed with respect to mortality or infection-related LOS between patients who had received early appropriate antibiotic therapy vs those who had received delayed appropriate antibiotic therapy at the onset of pneumonia or in patients with methicillin-sensitive S aureus pneumonia vs those with MRSA pneumonia. Conclusion: IRM from NBSAP is high, and standard therapies evaluated at the time of this study resulted in poor clinical outcomes. Delayed therapy was not found to be a predictor of adverse outcomes; however, this lack of ability to detect a difference may be a product of small sample size. These findings suggest that newer agents with enhanced clinical activity in NBSAP are needed and that these should be evaluated in a real-world setting, where outcomes of the most ill patients can be assessed. (CHEST 2005; 128:1414 –1422) Key words: bacteremia; clinical outcomes; critical care; cross-infection; hospital mortality; ICU; infection; staphylo- coccal infections; staphylococcal pneumonia; ventilator-associated pneumonia Abbreviations: APACHE acute physiology and chronic health evaluation; CART classification and regression tree analysis; IR-LOS infection-related length of stay; IRM infection-related mortality; NBSAP nosocomial bactere- mic Staphylococcus aureus pneumonia; MRSA methicillin-resistant Staphylococcus aureus; MSSA methicillin- sensitive Staphylococcus aureus; VAP ventilator-associated pneumonia N osocomial pneumonia is infection and second most common hospital currently the is the monia ranges from 7.8 to 68.0%, and is influenced by the duration of hospital and ICU stay, the specific leading cause of death from hospital-acquired infec- diagnostic method used for pathogen detection, and tions.1 The incidence of acquiring nosocomial pneu- the patient population studied.1 The rate of nosoco- mial pneumonia secondary to Staphylococcus aureus *From the Anti-Infective Research Laboratory, Wayne State has increased steadily over the past 2 decades.2 In University, Detroit, MI (Drs. Rybak and McKinnon); the De- partment of Pharmacy, Barnes Jewish Hospital, St. Louis, MO Reproduction of this article is prohibited without written permission (Dr. McKinnon); the Center for Anti-Infective Research and from the American College of Chest Physicians (www.chestjournal. Development, Hartford Hospital, Hartford, CT (Dr. DeRyke); org/misc/reprints.shtml). and Albany College of Pharmacy, Albany, NY (Dr. Lodise). Correspondence to: Peggy S. McKinnon, PharmD, Barnes-Jewish Manuscript received December 23, 2004; revision accepted Hospital, Mailstop 90 –52-411, 216 South Kings Hwy, St. Louis, January 26, 2005. MO 63110; e-mail: psm9154@bjc.org 1414 Clinical Investigations Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
3.
one review3 of
three major studies examining the University Human Investigation Committee. This investigation etiology of ventilator-associated pneumonia (VAP), S included all of the episodes of NBSAP identified from January 1, 1999, to April 30, 2004. Nosocomial pneumonia, or hospital- aureus was the most frequently isolated Gram-posi- acquired pneumonia, was defined as pneumonia occurring 48 tive organism and the second-most isolated organism h after hospital admission and excluding any infection that was only behind Pseudomonas aeruginosa. Most studies incubating at the time of hospital admission.17 estimate that S aureus accounts for 15 to 35% of all For the purposes of this investigation, the diagnosis of NBSAP nosocomial pneumonia cases; however, the true in- was defined based on clinical, radiographic, and microbiological cidence depends on many factors, such as patient criteria.18 –21 Within 72 h of the first positive culture, a chest demographics, local susceptibility patterns, and radiograph must also have been abnormal, and the patient must have had signs and symptoms consistent with nosocomial pneu- methods of diagnosis.3 monia. In order to fulfill the requirement for bacteremic pneu- monia, at least one S aureus-positive blood culture not related to For editorial comment see page 1093 another source of infection and one S aureus-positive respiratory culture must have been obtained within 72 h of each other as Although there is increased recognition of S au- well. Possible respiratory cultures included positive growth in the reus as a major pathogen causing nosocomial pneu- culture of pleural fluid, positive sputum culture/tracheal aspirate monia, there are few studies4 –7 with descriptive data (defined as secretions from the lungs, bronchi, or trachea that specifically evaluating patient outcomes of S aureus contain numerous or a moderate number of neutrophils and rare pneumonia. In addition, in the last decade, evidence or few squamous epithelial cells) findings, and a positive quanti- tative culture result from minimally contaminated lower respira- has accumulated demonstrating that initial inappro- tory tract specimens (eg, BAL fluid with 10,000 cfu/mL). priate antibiotic treatment is an important indepen- Radiographic criteria for pneumonia were met if the chest dent predictor of excess mortality in patients with radiograph yielded a new or progressive and persistent infiltrate, nosocomial pneumonia.8 –11 To our knowledge, no consolidation, or cavitation. Persistence of an infiltrate was data exist examining the impact of delayed appropri- defined as having the infiltrate present radiographically for at ate antibiotic treatment specifically for bacteremic S least 72 h. Patients were defined as symptomatic if one of the aureus pneumonia. In a retrospective study12 evalu- following were present: fever (ie, temperature 38°C or 100.4°F) or hypothermia (ie, temperature 35°C or 95°F) with ating S aureus bacteremia, a delay in treatment with no other recognized cause; leukopenia (ie, WBC count, 4,000 antibiotics for 44.75 h was found to be an inde- cells/ L) or leukocytosis (ie, WBC count, 10,000 cells/ L); or, pendent predictor of infection-related mortality for adults 70 years old, altered mental status with no other (IRM) [adjusted odds ratio, 3.8; 95% confidence recognized cause. Patients also had to exhibit one of the following interval, 1.3 to 11.0; p 0.01]. It is unknown if this signs: new onset of purulent sputum, change in the character of 44.75-h breakpoint is applicable to patients with the sputum, increased respiratory secretions, or increased suc- bacteremic S aureus pneumonia. Although the im- tioning requirements; new onset or worsening of cough, dyspnea, or tachypnea (respiratory rate, 25 breaths/min); or worsening pact of methicillin resistance on the outcomes of gas exchange (eg, O2 desaturation [Pao2/fraction of inspired patients with S aureus bacteremia has been exten- oxygen ratio of 240], increased oxygen requirements, or in- sively evaluated, little information exists on the im- creased ventilation demand). pact of the methicillin resistance of patients with Medical charts were screened to exclude the following possible nosocomial bacteremic S aureus pneumonia (NBSAP). alternative causes for fever and radiographic chest densities. The Furthermore, less information exists on the impact of presence of atelectasis was defined by the complete disappear- empirical antibiotic selection on NBSAP. Over the past ance of radiographic densities within 48 h of evaluation. Conges- tive heart failure with pulmonary edema was defined as a few years, studies13–16 have suggested that vancomycin resolution of pulmonary infiltrates following diuresis. A pulmo- may not be optimal for the treatment of S aureus nary embolism was defined by the presence of at least two pneumonia, especially in the subset of patients who segmental or larger mismatched perfusion abnormalities on a have been infected with methicillin-resistant S aureus ventilation-perfusion scan or suggestive radiographic findings on (MRSA). To evaluate the epidemiology, treatment, and pulmonary angiography and spiral CT scan. outcomes of NBSAP, a retrospective cohort analysis Patients with endovascular infections, including endocarditis, was performed. Specifically, we examined the impact of were excluded because of the potential for hematogenous spread of S aureus to the lungs, thus complicating our retrospective methicillin resistance, empirical therapy, and delayed diagnosis of S aureus pneumonia. Patients with endocarditis were treatment on the outcomes of patients with NBSAP. identified by transthoracic or transesophageal echocardiography and/or documentation of the diagnosis in the medical record. Materials and Methods Study Design Study Population To evaluate the epidemiology, treatment, and outcomes of NBSAP, a retrospective cohort analysis was performed. Specifi- This study was conducted at Detroit Receiving Hospital and cally, we examined the impact of methicillin resistance, empirical University Health Center, which is a 279-bed, level 1 trauma therapy, and delayed treatment on the outcomes of patients with center in Detroit, MI, and was approved by the Wayne State NBSAP. www.chestjournal.org CHEST / 128 / 3 / SEPTEMBER, 2005 1415 Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
4.
Data Collection
antimicrobial therapy. To prevent bias, investigators involved in the outcome assessments were blinded to both susceptibility data Clinical Data: Data extracted from the patient medical records and treatment data, including the time to receipt of treatment. and pharmacy database included the following: age; sex; comor- bidities present; prior antibiotic use (within 30 days prior to NBSAP); length of hospitalization before the onset of nosocomial Definitions pneumonia (total hospitalization and hospitalization in the ICU); mechanical ventilation at the onset of nosocomial pneumonia; Clinical outcomes were evaluated as successes or failures. Charlson comorbidity index score22; and severity of illness based Clinical success included clinical resolution, which was defined as on APACHE (acute physiology and chronic health evaluation) II the complete resolution of all signs and symptoms of pneumonia scores at the time of admission to the ICU.23 If the patients were (return to preinfection baseline) along with improvement, or lack not admitted to the ICU, the APACHE II score was determined of progression, of all abnormalities on the chest radiograph, and at hospital admission. clinical improvement, which was defined in patients if a partial The following comorbid conditions were documented: diabe- resolution of clinical signs and symptoms occurred such that no tes mellitus; heart failure; COPD; asthma; hepatic dysfunction; additional antimicrobial therapy was required, along with the renal failure (as indicated by the necessity for dialysis); malig- improvement or stabilization of chest radiographic findings. nancy; HIV infection; alcoholism; presence of decubitus ulcers Patients who died or whose conditions did not improve were (stage II to IV); administration of immunosuppressive drugs (ie, deemed as having clinical failure. Clinical failure was defined as receipt of 20 mg prednisone or an equivalent corticosteroid the persistence of clinical signs and symptoms, the persistence of per day for 14 days before the onset of nosocomial pneumonia positive culture findings, and/or a lack of resolution of infiltrates or the receipt of any neoplastic chemotherapy in the 3 months on the chest radiograph. before the onset of nosocomial pneumonia); surgery requiring Microbiological outcomes were categorized as eradication or 48 h of hospitalization in the 30 days before the onset of persistence. Microbiological eradication included documented nosocomial pneumonia; and the presence of burns on 30% of eradication, defined as the elimination of baseline pathogens the body surface area. based on subsequent negative blood and respiratory culture Microbiological Data: Collected microbiological data included findings, and presumed eradication, which was denoted in pa- all of the positive blood or respiratory culture findings, irrespec- tients in whom presumed eradication occurred based on clinical tive of the pathogen identified. Susceptibility testing was per- resolution, but no subsequent cultures were obtained. Microbi- formed using the microtiter-well method, and the results were ological persistence included documented persistence, which was interpreted according to National Committee for Clinical Labo- defined as the persistence of bacteria despite the appropriate use ratory Standards guidelines24 by the clinical microbiological of antibiotic therapy based on in vitro susceptibility results, and laboratory. presumed persistence, which was denoted in patients in whom Treatment Data: All of the antimicrobial agents administered presumed microbiological failure occurred based on clinical to provide activity against S aureus isolates were noted. Empiric failure, but no subsequent cultures were obtained. treatment was the first antibiotic regimen provided following the Death was considered to be related to NBSAP (ie, IRM) if one onset of infection. Treatment was considered to be appropriate or more of the following criteria were present: (1) blood and/or on the basis of the following two factors: the timing of treatment respiratory cultures were positive for S aureus at the time of relative to the first positive blood or respiratory culture finding; death; (2) death occurred before the resolution of signs and and the in vitro susceptibility of the blood or respiratory isolate. symptoms of the nosocomial pneumonia; (3) death occurred Timing was evaluated based on a previously described breakpoint 14 days after the onset of nosocomial pneumonia without of 44.75 h, which was determined by classification and regression another explanation; (4) autopsy findings indicated pneumonia as tree analysis (CART) as an independent predictor of mortality in a cause of death; and (5) pneumonia was indicated as a cause of S aureus bactermia.12 If a patient had received at least one IV death on the death certificate. antibiotic to which the S aureus blood or respiratory isolate was The calculation of IR-LOS was measured from the time when susceptible and the antibiotic had been administered within the first positive blood or respiratory culture finding was col- 44.75 h, it was considered to be appropriate early treatment. For lected until the end of antimicrobial treatment, death, or hospital example, an individual with MRSA bacteremia receiving vanco- discharge. The calculation of IR-LOS excluded patients who died mycin within 44.75 h would be classified as having received early secondary to nosocomial pneumonia. appropriate treatment. A patient with MRSA initially treated with An infection-related cost of hospitalization was determined for a -lactam but not receiving vancomycin within 44.75 h would be each patient. The Detroit Receiving Hospital accounting depart- considered as having received delayed treatment. In addition, we ment supplied the cost figures. For patients who lived or did not utilized CART analysis to determine whether there was a differ- die secondary to NBSAP, the cost was calculated from the onset ent breakpoint to better describe the critical time to appropriate of infection until the last day that antimicrobial therapy active antibiotic treatment for this cohort of NBSAP patients. against S aureus was administered (ie, the IR-LOS). For those patients who died because of NBSAP, the cost was calculated from the onset of infection until the day of the patient’s death. Outcome Assessment The following primary end points were assessed: (1) IRM; (2) Statistical Analysis hospital (crude) mortality; and (3) infection-related length of stay length (IR-LOS) after the onset of NBSAP. Secondary outcomes Categoric variables were compared by the Pearson 2 test or included the following: (1) clinical response; (2) microbiological Fisher exact test, and continuous variables were compared by the response; and (3) cost of hospitalization after the onset of Student t test or Mann-Whitney U test. Multivariate analyses NBSAP. were performed to determine the independent association of For the early treatment vs delayed treatment analyses, patients antibiotic resistance and delayed treatment with the clinical who died within 72 h of the onset of infection were excluded. outcome of interest while adjusting for confounding variables. Clinical and microbiological outcomes were assessed at the Clinical features significantly associated with the outcome by following four time points: day 3; day 7; day 10; and at the end of univariate analysis were included in the explanatory multivariate 1416 Clinical Investigations Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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model. The univariate
predictors had to represent 10% of the tive Staphylococcus sp. The most common concom- cohort to prevent overfitting of the multivariate model. Dichot- itant respiratory organisms were P aeruginosa (nine omous outcomes (eg, IRM and clinical status) were analyzed with standard logistic regression. A p value of 0.05 was considered cases); A baumannii (eight cases); Klebsiella spp to be significant for two-tailed tests. A statistical software package (seven cases); Escherichia coli (six cases); Candida (SPSS, version 10.0; SPSS; Chicago, IL) was used for all of the albicans (four cases); Enterobacter spp (three cases); calculations. and nine others. The clinical and microbiological success rates at the end of treatment were 56.7% and 53.3%, respec- Results tively. Thirty-three patients (55.5%) died during hospitalization, and 24 (40.0%) died secondary to Baseline Data NBSAP (ie, IRM). Nine patients died for reasons not Of the 206 patients identified either by Interna- attributable to the pneumonia. In seven cases, treat- tional Classification of Diseases, ninth revision, codes ment for NBSAP had stopped at least 2 weeks before for S aureus pneumonia and/or by concomitant the patient died. Withdrawal from support occurred blood and respiratory cultures positive for S aureus, in two patients irrespective of the concomitant pneu- 60 met the strict inclusion criteria as assessed for monia. NBSAP. The primary reasons for exclusion from the The relationship between APACHE II score and study included a lack of clinical or radiologic findings death is shown in Figure 1. A linear relationship supporting a pneumonia diagnosis (n 46), alter- existed demonstrating that patients who were more nate clinical diagnoses (n 43), infection that was acutely ill at the time of admission to the ICU had a not nosocomial (n 26), time correlation between greater mortality rate (R2 0.74). microbiological findings (n 25), and chart not available (n 6). Alternative clinical diagnoses po- Outcomes of Bacteremic MRSA vs Methicillin- tentially causing the infection isolated more than Sensitive S aureus Pneumonia MSSAP once included the following: endocarditis (n 12); IV line-related sepsis (n 16); alternative pathogen Of the 60 patients, 42 patients (70%) were in- most likely caused infection (n 5); and pelvic fected with MRSA. A comparison of clinical features abscess (n 2). Overall, the mean ( SD) age was between MRSA and methicillin-sensitive S aureus 55.5 15.0 years, and the median APACHE II score (MSSA) patients is presented in Table 1. By univar- was 20 (range, 3 to 41). Most patients were men iate analysis, MRSA patients were more likely than (66.7%), and were predominantly African American MSSA patients to have received prior antibiotic (56.7%) and white (38.3%). An equal number of treatment and had a longer median length of stay patients were admitted to surgery (41.7%) and med- prior to the onset of NBSAP. In addition, a signifi- icine services (41.7%), and 16.7% of the patients cant difference existed between the two groups with were admitted to the burn unit. Twenty-three pa- respect to appropriate treatment. In the MSSA tients (38.3%) underwent surgery 1 month prior group, 72.2% of patients received appropriate ther- to the development of NBSAP. Bilateral infiltrates apy within 44.75 h of the onset of infection com- were evident on chest radiography in 75% of the pared with only 50% of patients in the MRSA patients identified. Most patients were in the ICU at time of onset of NBSAP (93.3%), and 83.3% of patients were receiving mechanical ventilation. The median length of stay prior to the onset of NBSAP was 9 days (range, 2 to 81 days). The origin of the respiratory cultures used for the microbiological determination of pneumonia came from aspirated sputum in 90% of the cases, and from BAL fluid in 10% of cases. Of the 60 patients, 42 patients (70%) were infected with MRSA. Forty-four patients (73.3%) had concomitant organisms (6 in blood only, 7 in blood and respiratory cultures, and 31 in respiratory cultures only). The most common concomitant organisms in the blood were as follows: Enterococcus spp (five cases); Acinetobacter bau- mannii (three cases); Streptococcus viridans (two Figure 1. IRM grouped by APACHE II score. APACHE II cases); Klebsiella pneumoniae (one case); Streptococ- scores grouped in values of 10. Dotted line represented linear cus pneumoniae (one case); and one cogulase-nega- regression line. www.chestjournal.org CHEST / 128 / 3 / SEPTEMBER, 2005 1417 Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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Table 1—Characteristics of
MSSA vs MRSA median length of time needed to switch to optimal Pneumonia therapy for the eight patients who had been empir- MSSA MRSA ically treated with vancomycin was 71.5 h (range, 16 Characteristics (n 18) (n 42) p Value to 123 h). Of the 42 MRSA patients, 24 (57.1%) Age, yr 55.2 17.6 58.4 13.9 0.45 received empiric vancomycin treatment, 8 (19.0%) APACHE II score 20.5 (5–41) 20.0 (3–36) 0.72 received -lactam agents, 6 (14.3%) received clinda- Charlson index score 2 (0–6) 2 (0–7) 0.53 mycin, 3 (7.1%) received trimethoprim/sulfamethox- Diabetes 3 (16.7) 15 (35.7) 0.14 azole, 1 was started on therapy with levofloxacin; and Decubitus ulcers 0 7 (16.7) 0.09 1 patient died before receiving appropriate antibiotic Prior antibiotics 3 (16.7) 30 (71.4) 0.01 Vent at NBSAP onset 13 (72.2) 37 (88.1) 0.13 treatment. Once susceptibility data were available, LOS prior to NBSAP onset, d 4 (2–31) 11.5 (4–81) 0.03 40 patients (95.2%) received vancomycin for primary ICU LOS prior to NBSAP 3 (0–31) 9 (0–58) 0.059 antimicrobial treatment of pneumonia. Two patients onset, d were never appropriately treated with antibiotics. Time to adequate therapy, h 24 (8–51) 44 (1–149) 0.013 Nine patients (50.0%) in the MSSA subgroup were *Values given as mean SD, No. of patients (%), or median (range), treated with combination therapy compared with unless otherwise indicated. LOS length of stay; Vent receiving seven patients (16.7%) in the MRSA subgroup. The mechanical ventilation. median duration of combination therapy was 3 days in both groups (MSSA group range, 1 to 10 days; MRSA group range, 1 to 8 days). Eleven vancomycin subgroup (p 0.01) [Fig 2]. Furthermore, MSSA trough levels were collected in a total of nine patients pneumonia patients received appropriate treatment with a median value of 17.4 g/mL (range, 9.2 to in significantly less time than did MRSA pneumonia 26.7 g/mL). patients (24 h [range, 8 to 51 h] vs 44 h [range, 1 to The comparison values of hospital mortality, IRM, 149 h], respectively; p 0.013). No difference was and IR-LOS between MSSA and MRSA patients are detected in the duration of therapy between the two displayed in Figure 3. No significant differences in groups (MSSA group, 10 days [range, 2.5 to 25.0 these primary end points were observed between the days]; MRSA group, 11 days [range, 1.0 to 21.5 groups. Similarly, no significant differences in hos- days]). pital mortality, IRM, and IR-LOS were noted for the Of the 18 MSSA patients, 8 patients (44.4%) were different empiric antibiotic regimens, stratified by empirically treated with vancomycin, 7 patients methicillin susceptibility. Multivariate analyses were (38.9%) were empirically treated with a -lactam, 1 performed, and the associations between methicillin patient was empirically treated with clindamycin, 1 susceptibility and outcomes were identical to those patient was empirically treated with levofloxacin, and from the univariate analyses. 1 patient died prior to identification of the causative IRM was higher in the empiric vancomycin group organism and subsequent appropriate antibiotic than in the empiric -lactam group; however, this therapy. Once sensitivity reports were obtained, was not statistically significant. For the 18 patients 77.8% of the MSSA patients received a -lactam infected with MSSA, the hospital mortality and IRM agent as the primary antimicrobial treatment. The rates in the patients receiving empiric -lactams were 57.1% and 28.6%, respectively, compared with 62.5% and 50.0%, respectively, in the empiric van- comycin group. For the 42 patients infected with MRSA, the hospital mortality and IRM rates in patients receiving empiric vancomycin were 50.0% and 45.8%, respectively, compared with 62.5% and 25.0%, respectively, in the empiric -lactam group. These findings, however, were not statistically signif- icant, and an additional evaluation of this subset revealed that patients who had been empirically treated with -lactams tended to be younger (me- dian age, 52 vs 56 years, respectively) and to have lower APACHE II scores (median, 17 vs 21, respec- tively). Overall clinical success was achieved in 59.5% of MRSA patients compared with 50.0% of MSSA Figure 2. Receipt of adequate treatment within the 44.75-h patients. No differences in clinical or microbiological breakpoint established for S aureus bacteremia. success were determined at days 3, 7, or 10, or at the 1418 Clinical Investigations Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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Figure 3. Outcomes
of NBSAP based on MSSA vs MRSA pneumonia. end of antimicrobial therapy for any treatment reg- no significant difference in the rate of response was imen, stratified by methicillin susceptibility. Simi- seen at days 3, 7, and 10, and at the end of larly, because 83.3% of patients were receiving me- antimicrobial therapy or the first day to clinical chanical ventilation at the time of onset, no improvement (5 days [range, 2 to 14 days] vs 5 days difference in clinical response was observed in this [range, 2 to 11 days], respectively). In the CART VAP subset of patients compared with the whole analysis that was performed to identify a specific cohort. Of note, the overall clinical cure rate in “time to therapy” for the bacteremic S aureus pneu- patients receiving vancomycin was 56.3%; 58.3% in monia cohort, no additional time breakpoint in ap- the subset of MRSA patients. propriate antibiotic treatment was found that pro- duced an increased probability of IRM. Outcomes in Delayed vs Early Appropriate The evaluation of the appropriateness of therapy Therapy for concomitant pathogens was also assessed. Alter- native pathogens were appropriately treated 85% of Five patients were excluded in the appropriate the time based on the susceptibility profile. The therapy analyses secondary to death within 72 h of clinical success was 59.5% for patients treated ap- the onset of infection. Of the remaining 55 patients, propriately for both NBSAP and the alternative 24 patients (43.6%) did not receive appropriate pathogen. This result was similar to the clinical antibiotic treatment within 44.75 h of the onset of success rate observed for the entire cohort (56.7%). infection, and 31 patients (56.4%) received appro- Complete, infection-related cost data were avail- priate antibiotic treatment within 44.75 h of the able for 22 of the 60 patients. The greatest reason for onset of infection. There were no significant differ- increased cost was length of hospitalization. In the ences between the two groups (delayed vs early) with patients who lived, the median total cost was $35,072 respect to the APACHE II score at time of admission (range, $19,764 to $312,511) compared with $22,098 to the ICU (20.5 [range, 5 to 41] vs 18 [range, 4 to (range, $1,218 to $66,351) in the patients who died. 40], respectively; p 0.6) and Charlson comorbidity No differences in cost were evident in patients based index score (2 [range, 0 to 6] vs 2 [range, 0 to 6], on methicillin susceptibility or early empiric treat- respectively; p 0.9). The median time to the start ment. of appropriate treatment was 68.5 h (range, 45 to 149 h) in the delayed-treatment group and 25 h (range, 4 to 44 h) in the early-treatment group. Only Discussion 16 patients received appropriate antibiotic treatment within 24 h of the onset of infection The previous literature specifically focusing on S No differences existed with respect to the primary aureus nosocomial pneumonia is limited. Our review outcomes based on the receipt of delayed vs early of 60 patients is one of the largest reports of a appropriate antibiotic therapy (Fig 4). In addition, real-world experience describing the outcomes of www.chestjournal.org CHEST / 128 / 3 / SEPTEMBER, 2005 1419 Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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Figure 4. Outcomes
of NBSAP based on early vs delayed treatment. bacteremic staphylococcal pneumonia. The distribu- pneumonia patients. In the 55 patients with bacteri- tion of pathogens responsible for nosocomial pneu- ologically evaluable S aureus pneumonia, the overall monia differs depending on factors such as the clinical success rate in vancomycin-treated patients length of hospital admission before onset of the was 50.9% compared with 44.4% in the 18 patients disease, admission to the ICU, and duration of infected with MRSA. Stevens et al14 specifically mechanical ventilation.25 S aureus pneumonia typi- evaluated therapy with linezolid vs therapy with cally develops in patients who have had a longer vancomycin for the treatment of MRSA infections. length of hospital stay before onset of disease, have Data from 29 patients with MRSA pneumonia re- received mechanical ventilation for 5 days (ie, vealed that a clinical cure was achieved in 75.0% of late-onset VAP), and have been exposed to previous patients treated with either agent. In a study analyz- antimicrobial therapy. A prediction model26 has ing data from two previous double-blind studies of been developed to determine which characteristics patients with S aureus nosocomial pneumonia, Wun- predict for the development of MRSA in patients derink et al15 found that there was no difference in with S aureus bacteremia. The greatest risk factor clinical cure between the use of linezolid and van- was previous antibiotic exposure with an odds ratio comycin among all of the S aureus nosocomial of 9.2 (95% confidence interval, 4.8 to 17.9). Rello pneumonia patients (51.5% vs 43.4%, respectively; and Diaz3 also found previous antimicrobial therapy p 0.182). However, in the subset of 133 MRSA to be a risk factor for MRSA pneumonia as well. Our nosocomial pneumonia patients, a significant differ- findings for this cohort of 60 patients concur with ence was found (59% vs 35.5%, respectively; this description. The median length of hospital stay p 0.009). Kollef et al16 examined clinical cures in before the first positive culture finding was 9 days. patients who specifically had VAP and found signif- Most of our patients (93.3%) were in the ICU icant differences in favor of the empiric use of receiving mechanical ventilation (83.3%) at the onset linezolid over vancomycin in both the S aureus VAP of disease, and 55% of patients received antibiotic group (48.9% vs 35.2%, respectively; p 0.06) and therapy prior to the onset of pneumonia. Further- the MRSA VAP group (62.2% vs 21.2%, respectively; more, 71.4% of patients who developed MRSA p 0.001). Our findings were similar to these re- pneumonia had received previous antibiotic therapy ported values. Overall clinical success was achieved within 30 days prior to the onset of nosocomial in 56.7% of all patients and in 59.5% of the subset of pneumonia. This was significantly different from the MRSA patients compared with 50.0% of the subset 16.7% of MSSA pneumonia patients (p 0.01). of MSSA patients. Highlighting the empiric use of Clinical success has been reported in S aureus vancomycin, the overall clinical success rate was nosocomial pneumonia in a number of trials, mostly 56.3%, with 58.3% cure rates in the MRSA patient comparing vancomycin with the newer agents quinu- population. Among patients with MRSA, the IRM pristin/dalfopristin and linezolid. Fagon et al27 com- rate was higher in patients receiving empiric vanco- pared the efficacy of therapy with quinupristin/ mycin (45.8%) compared with that in patients receiv- dalfopristin and vancomycin in Gram-positive ing empiric -lactam agents (25.0%). These findings 1420 Clinical Investigations Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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were not statistically
significant, and an additional not predict clinical success or decreased mortality. evaluation of this subset of patients revealed that Another reason may be in part attributable to the patients empirically treated with -lactam agents slow activity or lack of efficacy of vancomycin, such tended to be younger and to have lower APACHE II that even the early administration of this agent is scores, partially explaining this finding. Because associated with poor clinical outcomes.31,32 80% of patients were already receiving mechani- The greatest limitation of our study was the small cal ventilation at the onset of NBSAP, these percent- number of patients (n 60) who met our strict ages did not change after analyzing this subset of inclusion criteria. The main reason that so few patients. patients were available for inclusion over the 5 years Patients included in this analysis were critically ill was the requirement for patients to have concomi- and had numerous underlying chronic comorbidities, tant S aureus bacteremia, as well as pneumonia. This as evidenced by a median APACHE II score of 20 requirement was essential because of the retrospec- (range, 3 to 41). Consequently, the mortality rate was tive design of our investigation and the high rate of high in our study, with an associated crude mortality tracheal aspirates used as the respiratory source of rate of 55.5% and an IRM rate of 40.0%. These values also correlate well with those from previous this pathogen. We wanted to be confident that the literature6,7,28 –30 in which the mortality rate attribut- patients who were involved in this analysis developed able to S aureus has ranged between 28% and 50%. bacteremia secondary to nosocomial pneumonia and The mortality rate among nosocomial acquired bac- not by hematogenous spread of S aureus, as can teremic pneumonia patients was found to be 52.5% occur in other conditions, such as endocarditis, in a previous study.5 which was one of the exclusion criteria. The most surprising outcomes from our results Additional limitations were inherent to the retro- were a lack of difference with respect to overall spective design of the study. Characterizing NBSAP hospital mortality rate, IRM rate, and IR-LOS based was difficult, although stringent inclusion criteria on the receipt of early vs delayed antibiotic therapy. were used. Many patients who likely had nosocomial Numerous reports8 –11 have been published stating S aureus pneumonia were excluded from the analysis that mortality significantly increases in patients who because of the lack of a concomitant positive blood develop pneumonia if empiric antibiotic therapies culture finding. Also, numerous comorbidities con- are not started at the time of clinical suspicion, founded the accurate assessment of IRM. To ac- before cultures have been collected and sensitivity count for this, an independent reviewer with no has been reported. Our lack of ability to detect a knowledge of the culture and sensitivity data or of difference may be a product of a small sample size the choice and timing of antibiotic therapy was leading to a potential type II error. In a previous designated to determine the primary outcome based study12 examining S aureus bacteremia, a delay in on clinical data recorded throughout the course of therapy of 44.75 h was found to be associated with the patient’s hospital stay. a 3.8 times higher rate of IRM. The 44.75-h break- In conclusion, this investigation includes one of point for appropriate therapy, however, was not the largest collections of patients to have bacteremic predictive in this series of pneumonia patients. In nosocomial pneumonia that was specifically attribut- addition, an additional breakpoint of time to appro- able to S aureus. S aureus pneumonia developed late priate therapy was not identified using CART. Some in the patient’s hospital stay and in ICU patients who potential reasons for no differences being detected had previously received mechanical ventilation, and are the low number of patients (n 60) and the high was associated with a high crude mortality and IRM mortality rate (55%) associated with this series. In rates. No significant differences were detected with addition, only 16 patients received appropriate anti- respect to crude mortality, IRM, or IR-LOS between biotic therapy within 24 h of the onset of infection. It patients who developed MSSA vs those who devel- may be difficult to ascertain the impact of delayed oped MRSA pneumonia or depending on whether therapy given the high rate of delayed treatment. the patient had received early vs delayed appropriate Of interest, as demonstrated in Figure 1, a linear antibiotic therapy. The small sample size may have relationship existed with respect to IRM and increas- precluded our ability to detect a difference in these ing APACHE II score. Because of the requirement groups. Patients who were empirically treated with of concomitant bacteremia, this subset of pneumonia vancomycin for MSSA and MRSA pneumonia expe- patients likely represents those patients who are rienced a high mortality rate. These findings suggest most severely ill with rapid disease progression. The that newer agents with enhanced clinical activity in severe illness exhibited in these patients may be the NBSAP are needed and that these should be evalu- main factor determining mortality and may serve as ated in a real-world setting, where outcomes of the the reason why appropriate antibiotic treatment did sickest patients can be assessed. The group of pa- www.chestjournal.org CHEST / 128 / 3 / SEPTEMBER, 2005 1421 Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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tients who will
experience the greatest benefit from linezolid with vancomycin. Intensive Care Med 2004; 30: these newer agents remains to be determined. 388 –394 17 American Thoracic Society. Hospital-acquired pneumonia in adults: diagnosis, assessment of severity, initial antimicrobial therapy, and preventive strategies: a consensus statement; References American Thoracic Society, November 1995. Am J Respir 1 Hoffken G, Niederman MS. Nosocomial pneumonia: the Crit Care Med 1996; 153:1711–1725 importance of a de-escalating strategy for antibiotic treatment 18 Micek ST, Ward S, Fraser VJ, et al. A randomized controlled of pneumonia in the ICU. Chest 2002; 122:2183–2196 trial of an antibiotic discontinuation policy for clinically 2 Lynch JP III. Hospital-acquired pneumonia: risk factors, suspected ventilator-associated pneumonia. Chest 2004; 125: microbiology, and treatment. Chest 2001; 119:373S–384S 1791–1799 3 Rello J, Diaz E. Pneumonia in the intensive care unit. 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Epidemiology, Treatment, and
Outcomes of Nosocomial Bacteremic Staphylococcus aureus Pneumonia* C. Andrew DeRyke, Thomas P. Lodise, Jr., Michael J. Rybak and Peggy S. McKinnon Chest 2005;128; 1414-1422 DOI 10.1378/chest.128.3.1414 This information is current as of April 17, 2011 Updated Information & Services Updated Information and services can be found at: http://chestjournal.chestpubs.org/content/128/3/1414.full.html References This article cites 31 articles, 17 of which can be accessed free at: http://chestjournal.chestpubs.org/content/128/3/1414.full.html#ref-list-1 Cited Bys This article has been cited by 4 HighWire-hosted articles: http://chestjournal.chestpubs.org/content/128/3/1414.full.html#related-urls Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.chestpubs.org/site/misc/reprints.xhtml Reprints Information about ordering reprints can be found online: http://www.chestpubs.org/site/misc/reprints.xhtml Citation Alerts Receive free e-mail alerts when new articles cite this article. To sign up, select the "Services" link to the right of the online article. Images in PowerPoint format Figures that appear in CHEST articles can be downloaded for teaching purposes in PowerPoint slide format. See any online figure for directions. Downloaded from chestjournal.chestpubs.org at 97185 Health Organization on April 17, 2011 © 2005 American College of Chest Physicians
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