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Prediction of methicillin-resistant Staphylococcus aureusin patients with non-nosocomial pneumonia

  • Won Jai Jung1,
  • Young Ae Kang1,
  • Moo Suk Park1,
  • Seon Cheol Park1,
  • Ah Young Leem1,
  • Eun Young Kim1,
  • Kyung Soo Chung1,
  • Young Sam Kim1,
  • Se Kyu Kim1,
  • Joon Chang1 and
  • Ji Ye Jung1Email author
BMC Infectious Diseases201313:370

https://doi.org/10.1186/1471-2334-13-370

Received: 15 April 2013

Accepted: 29 July 2013

Published: 9 August 2013

Abstract

Background

Methicillin-resistant Staphylococcus aureus (MRSA) is recognized as an important cause of not only hospital acquired pneumonia, but also non-nosocomial pneumonia. However, the risk factors for non-nosocomial MRSA pneumonia are not clearly defined. Our objective was to identify risk factors at admission that were associated with non-nosocomial MRSA pneumonia.

Methods

We evaluated 943 patients admitted to a university-affiliated hospital with culture-positive bacterial pneumonia developed outside the hospital from January 2008 to December 2011. We compared the clinical characteristics between MRSA and non-MRSA pneumonia, and identified risk factors associated with MRSA pneumonia.

Results

Of 943 patients, MRSA was identified in 78 (8.2%). Higher mortality was observed in MRSA than in non-MRSA patients (33.3% vs. 21.5%; P = 0.017). In a logistic regression analysis, MRSA pneumonia was observed more frequently in patients with a previous history of MRSA infection (OR = 6.05; P < 0.001), a PSI score ≥120 (OR = 2.40; P = 0.015), intravenous antibiotic treatment within 30 days of pneumonia (OR = 2.23; P = 0.018). By contrast, non-MRSA pneumonia was observed more often in patients with a single infiltrate on chest radiography (OR = 0.55; P = 0.029).

Conclusions

Anti-MRSA antibiotics could be considered in hospitalized non-nosocomial patients with several risk factors identified herein. The presence or absence of these factors would provide useful guidance in selecting initial empirical antibiotics.

Keywords

Pneumonia Methicillin-resistant Staphylococcus aureus Non-nosocomial Risk factors Community-acquired pneumonia Healthcare-associated pneumonia

Background

Methicillin-resistant Staphylococcus aureus (MRSA) is the major bacterial pathogen of hospital-acquired pneumonia and ventilator-associated pneumonia, with an incidence ranging from 20% to 40% [1, 2]. However, increased out-of-hospital services have led to the spread of MRSA beyond the hospital, and 2.2% to 22.3% of healthcare-associated pneumonia (HCAP) cases are caused by MRSA [36]. In community-acquired pneumonia (CAP), MRSA was thought to be an uncommon pathogen, comprising only 1–5% of cases [710]. Recently, the incidence of community-associated MRSA pneumonia has increased and it is regarded as an emerging problem [1114].

Previous studies have reported that non-nosocomial MRSA pneumonia, including CAP and HCAP, was likely to be severe and life-threatening with a high mortality [1115]. Therefore, recent guidelines regarding the treatment of non-nosocomial MRSA pneumonia have recommended empirical therapy for MRSA in selected patients [1618]. However, optimal selection of such patients was not clearly described. The lack of rapid, sensitive, and specific diagnostic methods for MRSA detection in pneumonia patients makes clinicians to initiate the antibiotics treatments empirically without any degree of certainty. Some guidelines recommend that patients with particular risk factors should be started with anti-MRSA therapy; however, these recommendations are usually based on evidence from case studies or opinions of experts, resulting in inconsistencies [1119]. Moreover, among non-nosocomial pneumonia patients, risk factors were primarily identified for CAP [20]; thus, there are limited data regarding overall characteristics and risk factors of MRSA pneumonia developed outside a hospital.

The aims of our study were to examine the proportion of pneumonia caused by MRSA among patients admitted to the hospital and to identify risk factors for MRSA at admission. This study may provide more clarified approaches for clinicians to predict MRSA pneumonia and guide initial antibiotic treatment decisions.

Methods

Study design and subjects

The present retrospective observational study included patients admitted with pneumonia to Severance Hospital in Seoul, South Korea between January 1, 2008 and December 31, 2011.

All patients were hospitalized with pneumonia, aged ≥ 20 years, and had culture-positive bacterial infections. Patients were classified into either non-MRSA or MRSA groups according to culture results.

The electronic medical records and imaging studies were reviewed. Data on baseline demographics, clinical manifestation, radiographic findings, and treatment outcomes were compared between MRSA and non-MRSA groups. Risk factors associated with MRSA pneumonia were identified for the prediction of MRSA pneumonia. The study protocol was approved by the Severance Institutional Review Board.

Definitions

Pneumonia was defined as the presence of a new infiltrate on chest radiography and signs or symptoms of lower respiratory tract infection (e.g., cough, expectoration, and chest pain) that were not attributable to other causes [12]. MRSA pneumonia was defined as pneumonia coinciding with isolation of MRSA as the only potential pathogen.

HCAP was defined by at least one of the following criteria according to American Thoracic Society (ATS) and Infectious Disease Society of America (IDSA) guidelines: hospitalization within 90 days before pneumonia diagnosis; admission from a nursing home or a long-term care facility; infusion therapy such as intravenous antibiotics, chemotherapy, or wound care within 30 days before pneumonia diagnosis; and/or chronic hemodialysis or peritoneal dialysis [17].

Immunosuppressed patients were defined as those in at least one of the following categories: (1) daily use of an oral corticosteroid (≥ 15 mg prednisone/day for more than 1 month or combination therapy with low-dose steroids and other immunosuppressants, including azathioprine, mycophenolate, cyclosporine, and methotrexate); (2) radiation therapy or chemotherapy for malignancy within 6 months prior to admission; (3) infection with human immunodeficiency virus; (4) recipient of either an organ or a bone marrow transplant; or (5) underlying acquired immune deficiency disorder [20, 21].

Microbiological studies

Pathogens from respiratory specimens (bronchoalveolar lavage fluid, pleural effusion, lung abscess, or sputum) and blood were investigated using standard microbiological procedures. Sputum samples were cultured using semi-quantitative methods, and an etiological diagnosis was confirmed when a predominant microorganism was isolated from group 5 sputum, according to Murray and Washington’s grading system [22]. Positive blood cultures were considered an etiological diagnosis if no other infection source was evident. Positive urine antigen for Streptococcus pneumoniae or Legionella were considered evidence of infection. Antibodies against Mycoplasma pneumoniae were detected by microparticle agglutination assay (MAG). High elevated titer (> 1:160) or four-fold increase of the titer between 2–4 weeks interval is regarded as Mycoplasma infection [23]. Organisms such as coagulase-negative staphylococci and diphtheroids were considered contaminants.

Statistical analysis

Categorical variables were analyzed using the χ2 test or Fisher’s exact test. Continuous variables were analyzed using t-test or the Mann–Whitney U test. To identify independent risk factors for MRSA pneumonia, multivariate analysis using logistic regression was conducted. Multi-collinearity of these variables was checked, and the goodness of fit of the model was verified by the Hosmer–Lemeshow test. The predictive value of the risk-scoring model was evaluated using receiver operating characteristic (ROC) curve analysis. A P value less than 0.05 was deemed to be statistically significant.

Results

Patient characteristics

Among 943 total patients, 78 (8.3%) were diagnosed with MRSA pneumonia; the remaining 865 (91.7%) comprised the non-MRSA group. Table 1 shows the baseline and clinical characteristics of the MRSA and non-MRSA groups. More patients in the MRSA group were categorized as HCAP than in the non-MRSA group (73.1% vs. 45.1%; P < 0.001). Diabetes, cerebral vascular accident, cardiovascular disease, and malignancy as underlying disease were more common in the MRSA group. Tube feeding, hypoxia at admission, and a previous history of MRSA infection within 1 year were more frequently observed in the MRSA group. Disease severity was more prominent in the MRSA group based on the CURB-65 and pneumonia severity index (PSI). The distribution of pathogens in non-MRSA group is presented in Table 2. Common organisms included Pseudomonas aeruginosa (18.5%), Streptococcus pneumoniae (17.7%), Klebsiella pneumoniae (16.5%), and Mycoplasma pneumoniae (15.5%).
Table 1

Characteristics of patients with MRSA and non-MRSA pneumonia a

Characteristics

MRSA

Non-MRSA

P-value

(n=78)

(n=865)

Age

71.4 ± 9.3

66.0 ± 14.8

< 0.001

Male

58 (74.4)

565 (65.3)

0.106

Female

20 (25.6)

300 (34.7)

Type of pneumonia

   

   Community acquired

21 (26.9)

475 (54.9)

< 0.001

   Health care associated

57 (73.1)

390 (45.1)

Underlying diseases

   

   Diabetes mellitus

30 (38.5)

237 (27.4)

0.038

   Chronic lung diseaseb

20 (25.6)

239 (27.6)

0.706

   Cerebral vascular accident

22 (28.2)

162 (18.7)

0.043

   Renal disease

14 (17.9)

104 (12.0)

0.13

   Hypertension

44 (9.7)

408 (47.2)

0.118

   Cardiovascular disease

21 (26.9)

148 (17.1)

0.03

   Liver disease

6 (7.7)

50 (5.8)

0.454

   Rheumatologic disease

3 (3.8)

31 (3.6)

0.756

   Malignancy

36 (46.2)

303 (35.0)

0.05

Clinical manifestation and parameters

   

   Bloody sputum

1 (1.3)

42 (4.9)

0.147

   Confusion (decreased consciousness)

17 (21.8)

134 (15.5)

0.146

   Shock at onset

20 (25.6)

267 (30.9)

0.337

   Hypoxemiac

49 (62.8)

437 (50.5)

0.037

   Acute renal failure at onset

13 (16.7)

162 (18.7)

0.654

   Leukocytes /uL

12700 ± 7700

11800 ± 7300

0.341

   Blood urea nitrogen > 30 mg/dL

25 (32.1)

255 (29.5)

0.634

   Sodium < 130 mmol/L

15 (19.2)

132 (15.3)

0.355

   pH < 7.35

7 (9)

72 (8.3)

0.843

Immunosuppressedd

24 (30.8)

215 (24.9)

0.25

MRSA history in previous 1 year

20 (25.6)

33 (3.8)

< 0.001

Tube feeding

12 (15.4)

64 (7.4)

0.013

CURB65

1.94 ± 1.07

1.6 ± 1.15

0.015

Pneumonia Severity Index

144.7 ± 26.1

127.6 ± 38.4

< 0.001

Admission via ER

64 (82.1)

700 (80.9)

0.808

aData are presented as numbers (percentages) and plus-minus values are means ± standard deviation unless otherwise indicated.

bChronic lung disease includes asthma, COPD, and structural lung diseases, such as bronchiectasis and interstitial lung disease.

cPaO2 < 60 mmHg, SpO2 < 90% or need for oxygen therapy.

dImmunosuppression includes the following: (1) daily administration of systemic corticosteroids (at least 15 mg of prednisone per day for more than one month or combination therapy with low dose corticosteroids and other immunosuppressants including azathioprine, mycophenolate, methotrexate, cyclosporine, or cyclophosphamide); (2) seropositivity for human immunodeficiency virus; (3) received either a solid organ transplant or bone marrow transplant; (4) treated with radiation therapy or chemotherapy for an underlying malignancy during the 6 months prior to hospital admission; (5) an underlying acquired immune deficiency disorder.

Abbreviations: MRSA methicillin-resistant Staphylococcus aureus, ER emergency room.

Table 2

Distribution of isolated pathogens in patients with non-nosocomial pnseumonia a

Microbes

No. of isolates

(%)

Gram-positive pathogens

 

   MRSA

78 (8.3)

   MSSA

51 (5.4)

   Streptococcus pneumoniae

167 (17.7)

Gram-negative pathogens

 

   Pseudomonas aeruginosa

175 (18.5)

   Escherichia Coli

49 (5.2)

   Klebsiella pneumoniae

156 (16.5)

   Enterobacter species

31 (3.3)

   Acinetobacter baumannii

24 (2.5)

   Stenotrophomonas maltophilia

18 (1.9)

   Haemophilus influenza

10 (1.1)

   Moraxella catarrhalis

24 (2.5)

Othersb

25 (2.6)

Atypical pathogens

 

   Mycoplasma pneumoniae

146 (15.5)

   Legionella pneumophila

2 (0.2)

aData are presented as numbers (percentages). Multiple pathogens were isolated in 91 patients.

b Serratia marcescens (n=12), Proteus mirabilis (n=5), Citrobacter species (n=3), Morganella morganii (n=2), Burkholderia cepacia (n=1), Bacteroides fragilis (n=1), Enterococcus faecalis (n=1).

Abbreviations: MRSA methicillin-resistant Staphylococcus aureus, MSSA methicillin-sensitive Staphylococcus aureus.

HCAP risk factors

Among the HCAP risk factors, recent hospitalization was the most common risk factor in both groups (Table 3). Patients in the MRSA group were significantly more likely to be recently hospitalized, reside in a nursing home, or receive recent intravenous antibiotics.
Table 3

Comparison of HCAP risk factors between MRSA and non-MRSA pneumonia a

Risk factors

MRSA

Non-MRSA

P-value

Hospitalization for ≥ 2 d in the preceding 90d

50 (64.1)

313 (36.2)

< 0.001

Residence in a nursing home or extended care facility

16 (20.5)

74 (8.6)

0.001

Intravenous antibiotic treatment within 30 days

22 (28.2)

80 (9.2)

<0.001

Chemotherapy within 30 days of pneumonia

6 (7.7)

115 (13.3)

0.156

Wound care within 30 days of pneumonia

1 (1.3)

4 (0.5)

0.351

Hemodialysis clinic

2 (2.6)

30 (3.5)

1

aData are presented as numbers (percentages) unless otherwise indicated.

Abbreviations: HCAP healthcare-associated pneumonia, MRSA methicillin-resistant Staphylococcus aureus.

Chest radiography

On the chest radiographs, multiple infiltrates were the most common finding in the MRSA group (39.7%), and the single infiltrate was in the non-MRSA group (52%)(Table 4). The presence of a single infiltrate was significantly more frequent in non-MRSA than MRSA groups (52% vs. 35.9%; P = 0.006).
Table 4

Chest radiograph findings of pneumonia patients with MRSA and non-MRSA a

Chest radiograph findings

MRSA

Non-MRSA

P-value

(n=78)

(n=865)

Single infiltrate

28 (35.9)

450 (52.0)

0.006

Multiple infiltrates

31 (39.7)

263 (30.4)

0.088

Diffuse bilateral infiltrates

19 (24.4)

152 (17.6)

0.136

Cavitation

1 (1.3)

11 (1.3)

1

Pleural effusion

16 (20.5)

126 (14.6)

0.16

aData are presented as numbers (percentages) unless otherwise indicated.

Abbreviation: MRSA methicillin resistant Staphylococcus aureus.

Treatment and clinical outcomes

From the first day of admission, glycopeptide antibiotics were administered to 14 (17.9%) patients in the MRSA group and 95 (11.0%) patients in the non-MRSA group without a significant difference (P = 0.065). The proportion of patients who were intubated was not different between the groups as well as the percentage of patients admitted to the intensive care unit (Table 5). However, in-hospital mortality was significantly higher in the MRSA group than in the non-MRSA group (33.3% vs. 21.5%; P = 0.017), and the MRSA group had a longer length of hospitalization compared with the non-MRSA group (16.5 days vs. 11 days; P = 0.001).
Table 5

Treatment and clinical outcomes of pneumonia patients with MRSA and non-MRSA a

Treatment and clinical outcomes

MRSA

Non-MRSA

P-value

(n=78)

(n=865)

Treatment

   

   Intubation in ER

11 (14.1)

94 (10.9)

0.384

   Intubation in overall

18 (23.1)

185 (21.4)

0.728

   ICU admission via ER

11 (14.1)

152 (17.6)

0.438

   ICU admission in overall

22 (28.2)

212 (24.5)

0.469

Clinical outcomes

   

   In-hospital mortality

26 (33.3)

186 (21.5)

0.017

   Days of ICU stay, median(IQR)

15.5 (11–30)b

10 (3–20)c

0.057

   Days of hospital stay, median(IQR)

16.5 (10–30)

11 (6–20)

0.001

aData are presented as numbers (percentages) unless otherwise indicated.

bn = 22.

cn = 212.

Abbreviations: MRSA methicillin resistant Staphylococcus aureus, ER emergency room, IQR interquartile range, ICU intensive care unit.

Factors associated with MRSA pneumonia at admission

A multivariate analysis identified three risk factors independently associated with MRSA pneumonia (Table 6). A previous history of MRSA infection within 1 year had the highest odds ratio (OR) of 6.05 (95% confidence interval [CI], 2.99–12.22; P < 0.001). A high PSI score (≥ 120) (OR = 2.40; 95% CI, 1.18–4.86; P = 0.015) and recent administration of intravenous antibiotics (OR = 2.23; 95% CI, 1.15–4.32; P = 0.018) were also identified as significant indicator of MRSA pneumonia. By contrast, a single infiltrate on chest radiography suggested a significantly lower risk of MRSA pneumonia (OR = 0.55; 95% CI, 0.33–0.94; P = 0.029).
Table 6

Multivariate analysis of risk factors for MRSA pneumonia

Risk factors

Odds ratio

95% CI

P-value

Age

1.02

0.99-1.04

0.135

Hospitalization for ≥ 2 days in the preceding 90 days

1.77

0.99-3.15

0.053

Residence in a nursing home or extended care facility

1.50

0.71-3.17

0.287

Intravenous antibiotic treatment within 30 days

2.23

1.15-4.32

0.018

Tube feeding

0.85

0.39-2.15

0.853

Hypoxemiaa

1.12

0.66-1.91

0.671

Single infiltrate

0.55

0.33-0.94

0.029

MRSA history in the previous 1 year

6.05

2.99-12.22

<0.001

PSI score ≥ 120

2.40

1.18-4.86

0.015

aPaO2 < 60 mmHg, SpO2 < 90%, or need for oxygen therapy.

Abbreviations: MRSA methicillin-resistant Staphylococcus aureus, PSI pneumonia severity index, CI confidence interval.

Discussion

This is the first study performing multivariate analysis to identify risk factors for prediction of non-nosocomial MRSA pneumonia. We found that patients presenting with previous history of MRSA infection, PSI score ≥ 120, or previous intravenous antibiotics treatment within 30 days were at high risk of MRSA pneumonia and those with single infiltrate on chest radiography were at low risk.

In our study, the prevalence of MRSA as the identified etiology of non-nosocomial pneumonia was 8.3% (12.8% for HCAP and 4.2% for CAP), which was consistent with that in previous reports ranging from 3% to 30% for HCAP and 0% to 15% for CAP [24]. Because our hospital, as a large tertiary referral hospital, has many patients with prior local hospital contact, the MRSA prevalence of pneumonia is likely higher than what would be found in typical community practice. Nevertheless, our results show that MRSA is not a rare cause of CAP. The boundaries among hospital-acquired, healthcare-associated, and community-acquired MRSA pneumonia are becoming blurred because of the continuous movement of patients, and thus infections, between the hospital and community.

The current HCAP criteria include a heterogeneous group of patients with various backgrounds, particularly diverse microbial etiologies [17]. Recently, the concept of HCAP has become controversial, and several studies suggested that the definition of HCAP should be refined to improve the prediction of resistant pathogens [25, 26]. In the same context, risk factors for pneumonia due to MRSA are subtly different from those for other potentially resistant pathogens and treatment for MRSA pneumonia is distinct from that for other drug-resistant pathogens. Recent IDSA guidelines recommend empirically starting antimicrobials both in cases of CAP and HCAP if certain risk factors accompany MRSA pneumonia [27]. However, the level of evidence supporting this recommendation is low with varying risk factors reported [7, 11, 1315, 19, 27]. Therefore, a specific predicting method for MRSA pneumonia is necessary and we investigated risk factors for MRSA in all non-nosocomial pneumonia including risk factors for HCAP.

Of HCAP criteria, recent hospitalization, residence in a nursing home, chemotherapy, and dialysis were not independent risk factors for MRSA in the present study. As a tertiary university-affiliated hospital, underlying disease of malignancy was observed in more than one-third of both MRSA and non-MRSA groups, resulting in no significant difference of chemotherapy. The total number of patients on dialysis in the present study was relatively small compared with that in previous studies, so it might be an important risk factor for MRSA pneumonia in other community settings.

Besides HCAP criteria, a history of MRSA infection within 1 year and severe illness were most significant predictor of MRSA pneumonia. Known colonization or infection with MRSA is one of the most essential risk factors in MRSA pneumonia [7, 27, 28]. Previous studies have reported that patients with MRSA pneumonia tended to be severely ill [19, 27]. Although single variables related to disease severity such as intubation, shock, and intensive care unit admission were not significantly different between the MRSA and non-MRSA groups in this study, the higher values for PSI score that represent severe disease was associated with MRSA pneumonia. Several studies reported multiple infiltrates on chest radiograph as a high risk factor for MRSA pneumonia [28], but other drug-resistant pathogens also tended to show multiple infiltrates. Thus, multiple infiltrates are not a distinct indicator for prediction of MRSA. Instead, if the patient presented with a single infiltrate on chest radiography, there was a low probability for MRSA pneumonia. Although an association between influenza and MRSA pneumonia has been established in several studies [27], we could not evaluate the relationship between them because of the low frequency of testing for influenza infection and a lack of data regarding a previous history of influenza.

Currently, there is no specific microbiological or serological diagnostic method to confirm MRSA infection immediately on presentation of non-nosocomial pneumonia. Thus, there is a need for a distinct protocol for an appropriate initial treatment for MRSA pneumonia. The identified four variables are all clinical findings available at admission and objective indices with little potential for various interpretations. Those factors could provide a clue for physicians regarding whether to start anti-MRSA treatment empirically. For years, vancomycin was the only antibiotic available for the treatment of MRSA pneumonia [1], and linezolid is an alternative choice achieving greater levels in lung epithelial lining fluid than in plasma [29]. Further study is underway to clarify which agent is more superior for the treatment of MRSA pneumonia [1].

Rapid institution of appropriate antibiotic therapy in patients with highly suspected MRSA pneumonia is strongly recommended according to several guidelines [1, 18, 27]. Delay of effective antibiotic therapy was associated with increased mortality in patients with ventilator associated pneumonia or septic shock [30, 31]. Among the patients with MRSA bacteremia, inappropriate empirical antibiotic therapy and non-eradicable foci including pneumonia were independent risk factors for mortality [32]. However, unnecessary broad-spectrum antibiotic therapy may promote the emergence of resistant organisms in the patients and the environment. Therefore, antibiotics de-escalation should be considered according to patient’s clinical response and the final results of cultures.

Our study has several limitations. First, this was a retrospective study of patients admitted to a single center. This center is a major, university-affiliated, tertiary referral hospital in South Korea, implying that the study population was relatively severely ill and had several comorbidities. Therefore, patients in this study may not reflect those at other institutions. Physicians should consider the characteristics of their local patient population when applying our approach at their institution. Second, we analyzed only patients with culture-positive pneumonia. Culture-negative pneumonia comprised a significant proportion of all pneumonia cases. However, we included only culture-positive cases because our goal was specifically to identify MRSA risk factors. Third, a positive culture of MRSA may reflect colonization rather than true infection for some cases although we considered MRSA as the only potential pathogen. Finally, our sample size was limited to only 78 MRSA pneumonia patients; however, ours is still one of the largest sample sizes on this topic to date [7, 1115]. The prospective study with a greater number of subjects is necessary to improve prediction for MRSA pneumonia.

Conclusion

MRSA is distinct from other drug-resistant pathogens in terms of disease severity and different antibiotic treatment. This study identified clinical risk factors that predict MRSA in hospitalized, non-nosocomial pneumonia. Anti-MRSA antibiotics could be considered in patients with several risk factors identified herein until MRSA has been excluded. The presence or absence of these factors would provide useful guidance for initial selection of empirical antibiotics.

Abbreviations

MRSA: 

Methicillin-resistant Staphylococcus aureus

CAP: 

Community acquired pneumonia

HCAP: 

Healthcare-associated pneumonia

IDSA: 

Infectious Disease Society of America

ATS: 

American Thoracic Society

ROC: 

receiver operating characteristic

PSI: 

pneumonia severity index

CURB-65: 

Confusion, urea, respiration, blood pressure and age ≥65 years.

Declarations

Acknowledgments

The authors are indebted to all who participated in this study. Thank you to all the health care professionals of Severance Hospital, specifically those from the pulmonology units and the emergency department.

Authors’ Affiliations

(1)
Division of Pulmonology, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine

References

  1. Rubinstein E, Kollef MH, Nathwani D: Pneumonia caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2008, 46 (Suppl 5): S378-385.View ArticlePubMedGoogle Scholar
  2. Hidron AI, Low CE, Honig EG, Blumberg HM: Emergence of community-acquired meticillin-resistant Staphylococcus aureus strain USA300 as a cause of necrotising community-onset pneumonia. The Lancet infectious diseases. 2009, 9 (6): 384-392. 10.1016/S1473-3099(09)70133-1.View ArticlePubMedGoogle Scholar
  3. Schreiber MP, Chan CM, Shorr AF: Resistant pathogens in nonnosocomial pneumonia and respiratory failure: is it time to refine the definition of health-care-associated pneumonia?. Chest. 2010, 137 (6): 1283-1288. 10.1378/chest.09-2434.View ArticlePubMedGoogle Scholar
  4. Chalmers JD, Taylor JK, Singanayagam A, Fleming GB, Akram AR, Mandal P, Choudhury G, Hill AT: Epidemiology, antibiotic therapy, and clinical outcomes in health care-associated pneumonia: a UK cohort study. Clin Infect Dis. 2011, 53 (2): 107-113. 10.1093/cid/cir274.View ArticlePubMedGoogle Scholar
  5. Park SC, Kang YA, Park BH, Kim EY, Park MS, Kim YS, Kim SK, Chang J, Jung JY: Poor prediction of potentially drug-resistant pathogens using current criteria of health care-associated pneumonia. Respir Med. 2012, 106 (9): 1311-1319. 10.1016/j.rmed.2012.04.003.View ArticlePubMedGoogle Scholar
  6. Shindo Y, Sato S, Maruyama E, Ohashi T, Ogawa M, Hashimoto N, Imaizumi K, Sato T, Hasegawa Y: Health-care-associated pneumonia among hospitalized patients in a Japanese community hospital. Chest. 2009, 135 (3): 633-640. 10.1378/chest.08-1357.View ArticlePubMedGoogle Scholar
  7. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, Albrecht V, Limbago B, Talan DA: Prevalence of methicillin-resistant staphylococcus aureus as an etiology of community-acquired pneumonia. Clin Infect Dis. 2012, 54 (8): 1126-1133. 10.1093/cid/cis022.View ArticlePubMedGoogle Scholar
  8. Fang GD, Fine M, Orloff J, Arisumi D, Yu VL, Kapoor W, Grayston JT, Wang SP, Kohler R, Muder RR, et al: New and emerging etiologies for community-acquired pneumonia with implications for therapy. A prospective multicenter study of 359 cases. Medicine (Baltimore). 1990, 69 (5): 307-316.View ArticleGoogle Scholar
  9. Rello J, Bodi M, Mariscal D, Navarro M, Diaz E, Gallego M, Valles J: Microbiological testing and outcome of patients with severe community-acquired pneumonia. Chest. 2003, 123 (1): 174-180. 10.1378/chest.123.1.174.View ArticlePubMedGoogle Scholar
  10. Marston BJ, Plouffe JF, File TM, Hackman BA, Salstrom SJ, Lipman HB, Kolczak MS, Breiman RF: Incidence of community-acquired pneumonia requiring hospitalization. Results of a population-based active surveillance Study in Ohio. The Community-Based Pneumonia Incidence Study Group. Arch Intern Med. 1997, 157 (15): 1709-1718. 10.1001/archinte.1997.00440360129015.View ArticlePubMedGoogle Scholar
  11. Kallen AJ, Brunkard J, Moore Z, Budge P, Arnold KE, Fosheim G, Finelli L, Beekmann SE, Polgreen PM, Gorwitz R, et al: Staphylococcus aureus community-acquired pneumonia during the 2006 to 2007 influenza season. Ann Emerg Med. 2009, 53 (3): 358-365. 10.1016/j.annemergmed.2008.04.027.View ArticlePubMedGoogle Scholar
  12. Gillet Y, Vanhems P, Lina G, Bes M, Vandenesch F, Floret D, Etienne J: Factors predicting mortality in necrotizing community-acquired pneumonia caused by Staphylococcus aureus containing Panton-Valentine leukocidin. Clin Infect Dis. 2007, 45 (3): 315-321. 10.1086/519263.View ArticlePubMedGoogle Scholar
  13. Francis JS, Doherty MC, Lopatin U, Johnston CP, Sinha G, Ross T, Cai M, Hansel NN, Perl T, Ticehurst JR, et al: Severe community-onset pneumonia in healthy adults caused by methicillin-resistant Staphylococcus aureus carrying the Panton-Valentine leukocidin genes. Clin Infect Dis. 2005, 40 (1): 100-107. 10.1086/427148.View ArticlePubMedGoogle Scholar
  14. Centers for Disease C: Prevention: Severe methicillin-resistant Staphylococcus aureus community-acquired pneumonia associated with influenza--Louisiana and Georgia, December 2006-January 2007. MMWR Morb Mortal Wkly Rep. 2007, 56 (14): 325-325.Google Scholar
  15. Lobo LJ, Reed KD, Wunderink RG: Expanded clinical presentation of community-acquired methicillin-resistant Staphylococcus aureus pneumonia. Chest. 2010, 138 (1): 130-136.View ArticlePubMedGoogle Scholar
  16. Mandell LA, Wunderink RG, Anzueto A, Bartlett JG, Campbell GD, Dean NC, Dowell SF, File TM, Musher DM, Niederman MS, 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.View ArticlePubMedGoogle Scholar
  17. American Thoracic S: Infectious Diseases Society of A: 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.View ArticleGoogle Scholar
  18. Nathwani D, Morgan M, Masterton RG, Dryden M, Cookson BD, French G, Lewis D: Guidelines for UK practice for the diagnosis and management of methicillin-resistant Staphylococcus aureus (MRSA) infections presenting in the community. J Antimicrob Chemother. 2008, 61 (5): 976-994. 10.1093/jac/dkn096.View ArticlePubMedGoogle Scholar
  19. Defres S, Marwick C, Nathwani D: MRSA as a cause of lung infection including airway infection, community-acquired pneumonia and hospital-acquired pneumonia. Eur Respir J. 2009, 34 (6): 1470-1476. 10.1183/09031936.00122309.View ArticlePubMedGoogle Scholar
  20. Shorr AF, Zilberberg MD, Micek ST, Kollef MH: Prediction of infection due to antibiotic-resistant bacteria by select risk factors for health care-associated pneumonia. Arch Intern Med. 2008, 168 (20): 2205-2210. 10.1001/archinte.168.20.2205.View ArticlePubMedGoogle Scholar
  21. Micek ST, Kollef KE, Reichley RM, Roubinian N, Kollef MH: Health care-associated pneumonia and community-acquired pneumonia: a single-center experience. Antimicrob Agents Chemother. 2007, 51 (10): 3568-3573. 10.1128/AAC.00851-07.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Murray PR, Washington JA: Microscopic and baceriologic analysis of expectorated sputum. Mayo Clin Proc. 1975, 50 (6): 339-344.PubMedGoogle Scholar
  23. Daxboeck F, Krause R, Wenisch C: Laboratory diagnosis of Mycoplasma pneumoniae infection. Clin Microbiol Infect. 2003, 9 (4): 263-273. 10.1046/j.1469-0691.2003.00590.x.View ArticlePubMedGoogle Scholar
  24. Zilberberg MD, Shorr AF: Healthcare-associated pneumonia: the state of evidence to date. Curr Opin Pulm Med. 2011, 17 (3): 142-147. 10.1097/MCP.0b013e328343eb33.View ArticlePubMedGoogle Scholar
  25. Brito V, Niederman MS: Healthcare-associated pneumonia is a heterogeneous disease, and all patients do not need the same broad-spectrum antibiotic therapy as complex nosocomial pneumonia. Curr Opin Infect Dis. 2009, 22 (3): 316-325. 10.1097/QCO.0b013e328329fa4e.View ArticlePubMedGoogle Scholar
  26. Ewig S, Welte T, Chastre J, Torres A: Rethinking the concepts of community-acquired and health-care-associated pneumonia. Lancet Infect Dis. 2010, 10 (4): 279-287. 10.1016/S1473-3099(10)70032-3.View ArticlePubMedGoogle Scholar
  27. Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, Gorwitz RJ, Kaplan SL, Karchmer AW, Levine DP, Murray BE, et al: Clinical practice guidelines by the infectious diseases society of america for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children. Clin Infect Dis. 2011, 52 (3): e18-55. 10.1093/cid/ciq146.View ArticlePubMedGoogle Scholar
  28. Kwong JC, Chua K, Charles PG: Managing Severe Community-Acquired Pneumonia Due to Community Methicillin-Resistant Staphylococcus aureus (MRSA). Curr Infect Dis Rep. 2012, 14 (3): 330-338. 10.1007/s11908-012-0254-8.View ArticlePubMedGoogle Scholar
  29. Conte JE, Golden JA, Kipps J, Zurlinden E: Intrapulmonary pharmacokinetics of linezolid. Antimicrob Agents Chemother. 2002, 46 (5): 1475-1480. 10.1128/AAC.46.5.1475-1480.2002.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Kollef MH, Ward S: The influence of mini-BAL cultures on patient outcomes: implications for the antibiotic management of ventilator-associated pneumonia. Chest. 1998, 113 (2): 412-420. 10.1378/chest.113.2.412.View ArticlePubMedGoogle Scholar
  31. Kumar A, Roberts D, Wood KE, Light B, Parrillo JE, Sharma S, Suppes R, Feinstein D, Zanotti S, Taiberg L, 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): 1589-1596. 10.1097/01.CCM.0000217961.75225.E9.View ArticlePubMedGoogle Scholar
  32. Kim S, Park W, Lee K, Kang C, Kim H, Oh M, Kim E, Choe K: Outcome of Staphylococcus aureus bacteremia in patients with eradicable foci versus noneradicable foci. Clin Infect Dis. 2003, 37 (6): 794-799. 10.1086/377540.View ArticlePubMedGoogle Scholar
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    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/13/370/prepub

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