REVIEW URRENT C OPINION
Surveillance cultures in healthcare-associated pneumonia: sense or nonsense? Johannes B.J. Scholte a, Walther N.K.A. van Mook a, and Catharina F.M. Linssen b
Purpose of review This review explores the usefulness of surveillance cultures in healthcare-associated pneumonia (HCAP). Recent findings The definition of HCAP is controversial. Causative micro-organisms of HCAP resemble those found in hospital-acquired pneumonia (HAP) and ventilator-associated pneumonia (VAP). Some types of surveillance cultures have proven useful in hospitalized patients. Whereas numerous studies have investigated the role of surveillance cultures in VAP, one may wonder whether surveillance culture implementation should belong in HCAP management guidelines. Summary Studies exploring the usefulness of obtaining surveillance cultures in VAP are numerous, but are mostly retrospective, observational and/or quasi-experimental in nature. Surveillance cultures may be useful for antibiotic guidance, but positive predictive value and specificity of surveillance cultures are low, obviously negatively impacting on cost effectiveness, especially in the large population at risk for HCAP. On the other hand, multidrug-resistance is increasing and surveillance cultures for methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci in ICU-admitted patients appeared useful and cost-effective. Furthermore, surveillance cultures for the presence of multidrug-resistant Gram-negative bacilli might be useful for antibiotic guidance. Currently, neither community-acquired pneumonia, HCAP, HAP nor VAP guidelines incorporate surveillance cultures. In the future, surveillance cultures in populations at risk for HCAP may be able to differentiate HCAP from other kinds of pneumonia and authorize its reason for existence. Keywords guidelines, healthcare-associated pneumonia, ICUs, multidrug-resistant, surveillance cultures, ventilator-associated pneumonia
INTRODUCTION Healthcare-associated pneumonia (HCAP) is a relatively new phenomenon that develops outside the hospital, although in patients somehow related to the healthcare system. The population at risk for HCAP is inconsistently defined in literature, and consequently HCAP seems to occur in a rather heterogeneous population accounting for approximately one third of all pneumonia cases developing outside the hospital [1]. Yet, patients with HCAP are significantly older and suffer from more comorbidities [2,3 ,4 ]. According to the most widely used international guideline for HCAP by the American Thoracic Society (ATS) and Infectious Diseases Society of America [5], HCAP resembles hospital-acquired pneumonia (HAP) and ventilator-associated pneumonia (VAP), and consequently HCAP should be &
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included in the spectrum of HAP and VAP and treated accordingly. Indeed, large studies demonstrated that HCAP is frequently caused by similar pathogens as seen in HAP and VAP, especially methicillin-resistant Staphylococcus aureus (MRSA) and Pseudomonas aeruginosa [2,3 ,6,7,8 ], although other studies demonstrated more resemblance to community-acquired &
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a Department of Intensive Care Medicine, Maastricht University Medical Center and bDepartment of Medical Microbiology, Atrium Medical Center, Heerlen, The Netherlands
Correspondence to Catharina F.M. Linssen, Department of Medical Microbiology, Atrium Medical Center, Heerlen, Postbox 4446, 6401 CX Heerlen, The Netherlands. Tel: +31 0 455767803; fax: +31 0 455767098; e-mail:
[email protected] Curr Opin Pulm Med 2014, 20:259–271 DOI:10.1097/MCP.0000000000000044
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KEY POINTS The benefit of surveillance cultures will be higher in populations with a high prevalence of highly pathogenic MDR micro-organisms, in combination with a high risk for pneumonia development, such as ICU patients.
of suspicion of infection. Frequently, surveillance cultures are part of a broader framework of surveillance. Indeed, surveillance programs are acknowledged to reduce mortality [13–15,16 ]. For VAP, there appeared to be a microbiological continuity between airway colonization, biofilm formation (on endotracheal tubes) and the subsequent development of VAP [17 ]. Colonization is thus known to precede infection [18], and this finding is in support of surveillance culture use in VAP from a pathophysiological point of view. No prospective randomized trials comparing the implementation of surveillance cultures versus no surveillance cultures in the management of any type of pneumonia were available when preparing this review. Furthermore, no studies were powered for hard end points such as mortality or were prospective randomized clinical trials. Additionally, it is unknown how often surveillance cultures should be obtained; the frequency will depend on the aim of the surveillance cultures. Daily cultures may be profitable for the individual patient, since inadequate antibiotic use may be diminished [19]; however, monthly cultures may be sufficient when monitoring MDR is the goal. As concentrations of pathogenic micro-organisms may be high and stable before the onset of VAP, performing surveillance culture three times weekly appears to be too frequent [20], and consequently twice a week seems best practice [21 ]. The next sections provide an overview of the studies conducted on the use of surveillance cultures respectively in relation to VAP, MRSA, vancomycinresistant enterococci (VRE) and MDR Gram-negative bacilli, as well as several miscellaneous studies. Results are presented in Tables 1–3 [19,20,21 , 22–41,42 ,43–57]. &
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The usefulness of surveillance cultures is frequently assessed in patients with (suspected) VAP and may be useful for antibiotic guidance. With increasing prevalence of MDR and increasing size of the HCAP population, surveillance cultures may have a future role in HCAP management. Contemporary HCAP guidelines so far do not recommend routine use of surveillance cultures. Further research on the usefulness of surveillance cultures in specific subpopulations of patients will improve the understanding and management of HCAP patients.
pneumonia (CAP) regarding causative microorganisms [4 ,9]. A recent review of 24 studies confirms that HCAP patients, when compared with CAP patients, are more at risk for infections with MRSA, multidrug-resistant (MDR) Enterobacteriaceae or P. aeruginosa [10 ]. Furthermore, some studies demonstrate that HCAP increases the length of hospital stay and mortality rates, possibly related to comorbidities and age [6,11]. Undoubtedly, MDR is an increasing problem worldwide [12] and the population at risk of HCAP is extending. Notwithstanding the abovementioned commonalities and differences between CAP, HCAP, HAP and VAP, one might hypothesize that surveillance cultures can play a role in the diagnosis of HCAP. Indeed, surveillance cultures of endotracheal aspirate (ETA) are already frequently used to guide antibiotic therapy for VAP by selecting patients with MDR micro-organisms. After providing a concise background regarding the use of surveillance cultures, this review aims to explore the potential usefulness of surveillance cultures in specific types of pneumonia and the extent to which surveillance cultures are included in current pneumonia guidelines, thereby attempting to provide recommendations regarding the role of surveillance cultures in future HCAP management. &
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SURVEILLANCE CULTURES FOR MANAGEMENT OF VENTILATORASSOCIATED PNEUMONIA Methods and results of studies concerning the use of surveillance cultures in VAP management are summarized in Table 1. One systematic review and 24 studies were included. The systematic review concerning the value of surveillance cultures of ETA included 791 episodes of clinically suspected or confirmed VAP derived from 14 studies [21 ]. The review calculated a pooled sensitivity between 72 and 84%, and a pooled specificity between 90 and 98% for surveillance cultures of ETA in predicting the bacterial pathogen in VAP. However, in many studies incorporated in the review &&
BACKGROUND OF SURVEILLANCE CULTURES Unlike cultures obtained for diagnostic purposes, surveillance cultures are obtained in the absence 260
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Year
1993
1995
1997
1999
2000
2002
2003
2005
2006
Study
A’Court et al. [22]
de Latorre et al. [23]
Delclaux et al. [24]
Cardenosa et al. [19]
Flanagan et al. [25]
Hayon et al. [26]
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Bouza et al. [27]
Michel et al. [28]
Depuydt et al. [29]
Belgium
France
Spain
France
United Kingdom
Spain
France
Spain
United Kingdom
Country
MO indentified by SC of ETA
MO indentified by SC of ETA
MO identified by all SC
MO identified by all SC
MO identified by SC of NBL
MO identified by all SC
MO identified by SC of NBL
MO identified by all SC
MO identified by SC of NBL
Bacteria
ETA thrice weekly
Quantitative culture of ETA twice a week
PBS or ETA after surgery, before extubation, 3 days after surgery and weekly thereafter
ETA, nasal, rectal and urine on admission and weekly. Catheters when removed
After 72 h on MV: NBL twice weekly and when VAP suspected
ETA, pharynx and gastric samples every 24 h
NBL every 48–72 h
Quantitative culture of ETA, pharyngeal and stomach samples thrice weekly.
NBL alternate-day
Site of SC
Single center retrospective observational study of 128 patients with HAP and bacteremia while on MV
Single center, observational, 299 patients on MV
356 patients in single center prospective after major heart surgery
Single center, observational 91 patients with 125 VAP episodes
3 ICUs, 145 patients > 72 h on MV
Single ICU, prospective. 123 patients on MV
Single center, 8 ICUs. Prospectively evaluation of 30 ARDS patients. 24 VAP episodes
Single ICU, prospective, 80 patients > 48 h on MV
Single center 150 patients on MV
Patients
Table 1. Methodology and results of studies concerning surveillance cultures for management of ventilator-associated pneumonia
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(Continued )
67of 128 (SN 52%) HAP with bacteremia previously detected by tracheal SC. When SC detected correctly: more appropriate antibiotic use and better survival
34 of 41 (SN 84%) VAP-causative pathogens previously detected by ETA. More appropriate (95%) antibiotic use compared to guidelines based (83%)
1626 SC obtained. 28 VAP: SN 3.7%. PPV: 1.7%. mortality of colonized patients 11.5% versus 1.6% in noncolonized patients
58 of the732 SC were positive. 17 of 220 VAP causing pathogens previously detected (SN 7%). 453 false positive results
PPV 17% and SN 74% for development of VAP diagnosed with PSB or BAL
2316 SC samples, 255 positive. 25 VAP pathogens found. ETA SN 88%, pharynx SN 68%, stomach SN 28%. Low PPV and specificity
PPV 89% and SN 67% for development of VAP when NBL revealed colonization
SC pos 72/80, only 12 VAP cases, diagnosed with ETA (¼incorporation bias). 10 of 21 VAP (SN 48%) causing MO previously detected by SC of phagyneal or stomach samples
Concordance with BAL results 16/20 (SN 80%). CFU in NBL were increasing prior to VAP development and decreasing when clinical improvement
Outcome
Surveillance cultures in pneumonia Scholte et al.
261
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262
2006
2007
2007
2008
2008
2008
2009
2009
2009
Bagnulo et al. [31]
Malacarne et al. [32]
Depuydt et al. [33]
Boots et al. [20]
Nair et al. [34]
Jung et al. [35]
Pirracchio et al. [36]
Lampati et al. [37]
Year
Depuydt et al. [30]
Study
Table 1 (Continued)
www.co-pulmonarymedicine.com Italy
France
France
India
Australia
Belgium
Italy
Uruguay
Belgium
Country
MO indentified by SC of ETA
All MO, arranged by individual species
MO indentified by SC of ETA
MO indentified by SC of ETA
MO identified by SC of NBL
MDR MO
A.baumannii in late onset VAP
All MO, especially MDR
MO identified by all SC
Bacteria
ETA once weekly in one ICU and twice weekly in the other ICU
Nose and throat at admission
ETA at admission and weekly thereafter
ETA after 48h of MV
NBL < 12 h after admission, 48h after admission and afterwards thrice weekly
Urinary samples and ETA thrice weekly. Oral, nasal, and rectal samples ad admission and weekly
ETA twice weekly in patients >72 h on MV
Semi-quantitative ETA twice weekly
Urine, ETA and oral thrice weekly and anal swab weekly 48–96 hrs before bacteremia
Site of SC
Two centers. Partly prospective. 56 VAP episodes
136 VAP (diagnosed using PSB) cases proven by PSB 85%, SN 20–85%
SN 72%. In 77 SC and BAL concordant: 85% received adequate antibiotic therapy. In 23 pts not concordant: 65% adequate antibiotic treatment. 71% adequate when ATS guidelines were followed equal mortality
6 of 11 (SN 55%) VAP (proven by BAL) causing MO previously detected by SC
49 of 58 VAP-causative MO previously detected by NBL. SN 84%, SP 50%, PPV 31%, NPV 93%
SN 69% (ETA), 82% (all SC) for MDR VAP. PPV 90% (ETA), 87% (all SC). Appropriate antibiotic use in 77% and 89% of MDR VAP compared to 76– 88% based on hypothetic antibiotic use. Limited use of broad spectrum antibiotics
SN 90%; 18 of 20 VAP episodes due to A.baumanii were previously positive in ETA SC. PPV 45% when VAP present
60% concordance between BAL and SC by ETA. 80% concordance when MDR
86 of 112 (SN 76%) previously detected by SC of ETA MDR HAP: 31/44 (SN 71%) ETA was concordant. 39/44 (SN 89%) any SC was concordant. 47 false positive SC. In a subgroup of patients with 2 risk factors for MDR: more appropriate antibiotic use when SC results were used
Outcome
Infectious diseases
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USA
Argentina
2012
2012
2012
2013
Brusselaers et al. [40]
Brusselaers && et al. [21 ]
Chan et al. [41]
Luna et al. & [42 ]
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MRSA
All MO, especially MDR
MO, especially MDR identified by SC of ETA
MO identified by all SC
All MO, especially MDR
ETA
Nose, oral swabs or ETA and wounds on admission and weekly
ETA
ETA thrice weekly
ETA at ICU admission and every second day
ETA every three days
283 patients 48 h on MV, 65 BAL-proven VAP episodes in 55 pts. Prospective observational cohort. Single center
Prospective observational single center study. 924 suspected VAP, 388 proven VAP, 37 MRSA VAP
Systematic review and diagnostic test accuracy meta-analysis. 14 articles. 791 (suspected) VAP episodes
53 burn patients. 70 VAP episodes. Single center. Retrospective observational cohort
Single pulmonary ICU, prospective, observational. 92 patients 4 days on MV
Single center. Prospective observational cohort of 200 patients 48 h on MV. VAP based on CPIS and ETA 105 cfu/ml
146 ETA/BAL pairs. Complete concordance 36%. Partial concordance 19%. ETA Two-fold contact precautions. Suggested reduction in VRE transmission
A: 17.1 VRE/100 000 patient days. More monoclonal B: 8.2 VRE/100 000 patient days. More polyclonal
Results
CI, confidence interval; ETA, endotracheal aspirate; MO, micro-organisms; MRSA, methicillin-resistant Staphylococcus aureus; MV, mechanical ventilation; PCR, polymerase chain reaction; SC, surveillance cultures; VRE, vancomycin-resistant enterococci.
Year
Study
Table 2. Methodology and results of larger studies concerning surveillance cultures for methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci
Infectious diseases
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Surveillance cultures in pneumonia Scholte et al. Table 3. Methodology and results of studies concerning surveillance cultures for multidrug-resistant Gram-negative bacilli and overage studies Study
Year
Country
Bacteria
SC
Method and patients
Outcome
Bertrand et al. [50]
2001
France
Pseudomonas aeruginosa
Rectal swab, nose swab and ETA at admission and weekly thereafter
3009 patients admitted to 4 ICUs
Rectal swab: SN 34%, SP 93%, PPV 29% and NPV 95% K 0.25 for development of P. aeruginosapositive clinical cultures ETA and oral swab: SN 22%, SP 96%, PPV 27% and NPV 95%. K 0.20
Blot et al. [51]
2005
Belgium
MDR GNB
Oral, urine, ETA thrice weekly. Rectal weekly
Single center, retrospective analysis of 157 episodes of MDR GNB bacteremia while on MV
SN 117/157 (75%). More appropriate initial antibiotic therapy when SC concordant. Equal mortality
Reddy et al. [52]
2007
USA
ESBL-producing Enterobacteriaceae
Rectal weekly
Single center observational, 17 872 high care patients
SCþ in 413/17 872 (2.3%). 50% also positive for VRE Bacteremia due to ESBL-producing Enterobacteriaceae: 102. SN 76%, SP 98%, PPV 8%, NPV 99%
Papadomichelakis et al. [53]
2008
Greece
MDR GNB in VAP or bacteremia
ETA twice weekly and rectal weekly in all ICU patients
Single ICU, retrospective 31 episodes of VAP and 55 episodes of bacteremia
SN 74% (23/31) for VAP and 67% (37/55) for bacteremia More appropriate antibiotic treatment when SC concordant. Equal mortality
Baba et al. [54]
2011
Australia
Nosocomial GNB bacteremia
Twice weekly rectal and ETA
Single center, retrospective 228 episodes of GNB bacteremia
All: SN 28%. Predictive value for MDR: SN 51–57%, SP 88–94%, PPV: 51–73%, NPV: 79–94%
2006
France
MRSA and ESBLproducing Enterobacteriaceae
Nasal and rectal swab at admission and weekly thereafter
Single center, prospective observational cohort 412 ICU patients
More nosocomial infections when MRSA or ESBL pos (RR 2.08)
Miscellaneous Galoisy-Guibal et al. [55]
SN 17%, SP 92%, PPV 38%, and NPV 79% for development of nosocomial infection Vandewoude et al. [56]
2006
Belgium
Aspergillus spp.
ETA thrice weekly
Single center, retrospective. analysis of 25 216 ICU patients
172 of 25 216 ICU patients SC of ETA positive for Aspergillus spp., 66 had probable and 17 had definitive invasive aspergillosis: PPV 48.3%
Sreeramoju et al. [57]
2008
USA
GNB
ETA 1 h after cardiac surgery, after surgery and weekly thereafter
Single center, prospective observational cohort of 286 post cardiac surgery patients
Colonization associated with (early) development of infection when >1 week on MV (RR 2.3) SN 73%, SP 75%, PPV 48%, NPV 90%
ESBL, extended-spectrum b-lactamase; ETA, endotracheal aspiration; GNB, Gram-negative bacilli; MDR, multidrug-resistant; MV, mechanical ventilation; NPV, negative predictive value; PPV, positive predictive value; RR, relative risk; SC, surveillance cultures; SN, sensitivity; SP, specificity; VAP, ventilator-associated pneumonia; VRE, vancomycin-resistant enterococci.
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as well as in many of the 24 studies presented in Table 2, some methodological concerns arise. First, most studies concerned retrospective analysis of VAP episodes, and randomized controlled trials were lacking. The former may reveal higher predictive values for surveillance cultures compared with the value of surveillance cultures by taking all obtained surveillance cultures into account (the latter being a more correct method). Second, no worldwide accepted gold standard was available for diagnosing VAP [58 ] and studies used different diagnostic approaches, while not always distinguishing colonization from infection [50]. When ETA is used for VAP diagnosis, it is not correct to compare micro-organisms identified by ETA with VAP-causing micro-organisms, the latter also being based on ETA results. This so-called incorporation bias, which overestimates diagnostic accuracy [59], was most likely present in a significant number of studies [23,33,39,40,60,61]. In some studies, incorporation bias may be present, because diagnostic methods were not clearly described [24,50]. Third, studies were difficult to compare because of the heterogeneity in study population (postcardiac surgery, medical ICU), MDR prevalence, surveillance culture sampling sites and frequency, as well as the previously discussed method for VAP diagnosis. Furthermore, cutoff for positive ETA surveillance cultures varied. Some included surveillance cultures of ETA samples with at least 104 cfu/ml [35], whereas others included surveillance cultures of ETA samples with less than 105 cfu/ml [38]. Other studies compared individual micro-organisms identified in surveillance cultures, thereby artificially increasing the specificity by increasing the numbers of ‘true negatives’ [36]. Finally, some studies presented data from cases in the same hospital and same period, suggesting publication bias [29,30,33]. After taking into account these concerns, some studies suggest that more appropriate antibiotic treatment is given when guided by available surveillance cultures compared with ATS guidelines [5] or a hypothetical antibiotic treatment model [28–30,33,35,38]. However, the methodology used herein was perhaps less suited to demonstrate such correlation, and MDR presence may have been caused by other risk factors such as previous antibiotic treatment and prolonged mechanical ventilation (potential confounders). Whereas improved survival is suggested by one study [29], others demonstrate equal mortality [35] and no study was found to be sufficiently powered to demonstrate any mortality differences. Surveillance cultures of gastric samples appeared not useful for antibiotic guidance in &&
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VAP management [19]. In one study, 33% of all VAP causative pathogens were previously detected by nasal swab, rectal swab or urine culture [26]. Sensitivity increased by 13–18% in two studies when the results of all performed surveillance cultures were taken into account [30,33]. However, the expected negative effect on positive predictive value and specificity of this strategy (taking into account all surveillance cultures) was not provided. Overall, sensitivity of previously available surveillance cultures for VAP seems moderate to even high, and therefore could more appropriately guide antibiotic treatment, especially in the case of P. aeruginosa and MDR. However, a decrease in infection attributable mortality when surveillance cultures were performed was so far not demonstrated. The positive predictive value of surveillance cultures seems low and, in our opinion, surveillance culture results should therefore always be used together with clinical criteria before the initiation of antibiotics.
SURVEILLANCE CULTURES FOR MANAGEMENT OF METHICILLINRESISTANT STAPHYLOCOCCUS AUREUS AND VANCOMYCIN-RESISTANT ENTEROCOCCI MRSA and VRE are resistant Gram-positive microorganisms that are frequently found in hospitaladmitted patients, and probably in the healthcare-associated population. MRSA infection is associated with increased mortality, morbidity and costs compared with methicillin-susceptible S. aureus [62,63]. MRSA is a more potent causative micro-organism for pneumonia than VRE, which is sometimes considered relatively harmless. As surveillance culture may early identify patients colonized with MRSA and/or VRE, subsequently implemented contact precautions and/or eradication protocols could prevent transmission and infection [64–66]. Studies concerning the usefulness of surveillance cultures in the light of MRSA and VRE are summarized in Table 2. Most studies originated from United States, where VRE and MRSA are relatively endemic, obviously limiting generalization to the European context because of marked differences in VRE and MRSA prevalence. Many studies demonstrated potential usefulness of surveillance cultures on high-risk units at admission and weekly thereafter in controlling the spread of both MRSA and VRE [43–47,67], and the prevention of hospital-acquired VRE or MRSA infections [43–45,47,68]. Currently, there is no evidence that the implementation of surveillance cultures for Volume 20 Number 3 May 2014
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the management of MRSA/VRE reduces infections or mortality.
SURVEILLANCE CULTURES FOR MANAGEMENT OF MULTIDRUGRESISTANT GRAM-NEGATIVE BACILLI MDR Gram-negative bacilli are notorious causes of nosocomial infections and are increasingly jeopardizing patients. Surveillance cultures may lead to the identification of MDR and subsequent appropriate treatment in case of an infection. An overview of studies focusing on the usefulness of surveillance cultures in MDR Gram-negative bacilli infections is provided in Table 3. Overall, only quasi-experimental observational studies were available, studies were difficult to compare and results were frequently inconsistent. Nevertheless, specificity and negative predictive values appeared high, sensitivity moderate and positive predictive value low. Two studies demonstrated that appropriate antibiotic therapy was given more frequently to patients when surveillance cultures correctly predicted the micro-organism causing bacteremia [51,53]. Acknowledging that they were neither designed nor powered for mortality, two studies failed to demonstrate impact on mortality [51,53]. Additional studies are needed to establish the role of surveillance cultures for these micro-organisms, as it may have some beneficial aspects, especially in antibiotic guidance.
MISCELLANEOUS STUDIES, INCLUDING SURVEILLANCE CULTURES IN SELECTIVE DIGESTIVE TRACT DECONTAMINATION Summarized results of miscellaneous studies are incorporated in Table 3. Surveillance cultures of ETA positive for Gram-negative bacilli are predictive of subsequent nosocomial infections [57]. Moreover, surveillance culture of ETA positive for Aspergillus spp. in critically ill patients should prompt further analysis, given its positive predictive value of almost 50% for the subsequent presence of probable or definitive invasive aspergillosis [56]. Guidelines for selective digestive tract decontamination (SDD) suggest to obtain surveillance cultures of throat and rectal swabs twice a week [69,70]. SDD-resistant micro-organisms were detected earlier and more frequently on admission surveillance cultures [71]. Yet, no study currently available has demonstrated any evidence of usefulness of surveillance cultures in SDD. Nevertheless, surveillance cultures of throat and faeces samples may assess the SDD compliance and effectiveness, distinguish exogenous from endogenous infections and detect antimicrobial resistance [70].
COST-EFFECTIVENESS OF SURVEILLANCE CULTURES The presumed benefit of surveillance cultures lies in the early detection of MDR colonization and the subsequent contact precautions for individual patients, aiming to achieve lower MDR colonization and infection rates in the population, which in turn leads to less contact precautions, including declined long-term expensive antibiotic use. Furthermore, more appropriate antibiotic administration leads to lower rates of infection and, presumably, mortality. On the other hand, the costs of surveillance cultures consist of the labor associated with sample collection by the nurse, laboratory-processing costs and the possible attributable short-term costs for more contact precautions. Furthermore, a theoretical consequence of obtaining surveillance cultures may be the risk of infection due to frequent manipulations of endotracheal tubes and catheters. Although surveillance cultures may diminish antibiotic use in general [28,33], costs of the antibiotics eventually used may nevertheless be higher [28]. In nonepidemic situations, obtaining surveillance cultures for the presence of specific MDR micro-organisms appeared not cost-effective [72]. Surveillance culture implementation for VRE presence was cost-effective in one study [73]. Screening all ICU patients for MRSA colonization combined with the subsequent isolation and/or decolonization proved to be cost-effective for all ICU patients [46,74] during an MRSA outbreak [75], as well as in a theoretical model [76,77]. Overall, the potential financial benefit will be higher in the context of a high prevalence, more pathogenic MDR (MRSA > VRE) and a high risk for pneumonia, such as patients admitted to the ICU. With worldwide increasing numbers of MDR and of patients (becoming) at risk for HCAP, combined with possible lower laboratory costs, surveillance cultures may become more cost-effective in future.
GUIDELINES Guidelines concerning the management of CAP, HCAP, HAP and/or VAP are numerous [78]. A list of frequently used guidelines is provided in Table 4, including their statements on the use of surveillance cultures [5,79–91]. None of these guidelines provides clear recommendations concerning surveillance culture use.
SURVEILLANCE CULTURES FOR HEALTHCARE-ASSOCIATED PNEUMONIA Unfortunately, guidelines dealing with HCAP are numerous and contradictory. Furthermore, to our knowledge, no studies have dealt with the value of
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268
www.co-pulmonarymedicine.com 2007 2008
2008
2009
2009 2009
2010
2011
Feldman et al. [81]
Muscedere et al. [82,83]
Masterton et al. [84]
Mosier et al. [85]
Correa et al. [86]
Lim et al. [87]
Menendez et al. [88]
Woodhead et al. [89]
Swedish Society of Infectious Disease
Dutch Working Party on Antibiotic Policy and Dutch Association of Chest Physicians
European Society of Clinical Microbiology and Infectious Disease and European Respiratory Society
Spanish Society of Pulmonology and Thoracic Surgery
British Thoracic Society
Brazilian Thoracic Society
American Burn Association
British Society of Antimicrobial Chemotherapy
VAP guidelines committee and Canadian Critical Care Trials Group
South African Thoracic Society
Gulf Cooperation Council
ATS and Infectious Diseases Society of America
ATS and Infectious Diseases Society of America
Organization
Swedish guidelines on the management of CAP in immunocompetent adults
Guidelines on the management of CAP in adults
Guidelines for the management of adult lower respiratory tract infections – full version
CAP. New guidelines of the Spanish Society of Chest Diseases and Thoracic Surgery
BTS guidelines for the management of CAP in adults: update 2009
Brazilian guidelines for CAP in immunocompetent adults
Guidelines for prevention, diagnosis, and treatment of VAP in burn patients
Guidelines for the management of HAP in the UK: Report of the Working Party on HAP
Comprehensive evidenced-based clinical practice guidelines for VAP
Management of CAP in adults
Practice guidelines for the management of CAP
Consensus guidelines on the management of CAP in adults
Treatment of HAP, VAP and HCAP
Name
Not mentioned
Not mentioned
Consider periodic surveillance of colonization in patients with exacerbations or bronchiectasis (level B3 evidence)
Not mentioned
Not mentioned
Not mentioned
Positive MRSA SC predicts MRSA VAP. No recommendation.
No studies for SC for HAP and consequently no recommendations
Not mentioned
Not mentioned
Not mentioned
Not mentioned
Not mentioned
Statement concerning SC
ATS, American Thoracic Society; BTS, British Thoracic Society; CAP, community-acquired pneumonia; HAP, hospital-acquired pneumonia; HCAP, healthcare-associated pneumonia; SC, surveillance cultures; VAP, ventilator-associated pneumonia.
2012
2007
Memish et al. [80]
Spindler et al. [91]
2007
Mandell et al. [79]
2012
2005
ATS [5]
Wiersinga et al. [90]
Year
Reference
Table 4. Current guidelines including their statement concerning surveillance cultures
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Surveillance cultures in pneumonia Scholte et al.
surveillance cultures in HCAP. However, as mentioned earlier, micro-organisms involved in HCAP are comparable with those found in HAP and VAP [5]. As MDR is increasing [12] in both Gram-negative (e.g. Klebsiella pneumoniae, P. aeruginosa) and Grampositive (MRSA, VRE) micro-organisms involved in causing HAP, we thus hypothesize that surveillance cultures can also be of value in HCAP. In patients that have been previously identified as carriers of MDR micro-organisms, for example, one could argue that follow-up surveillance cultures to monitor the persistence of these MDR micro-organisms is indicated. This strategy could prevent patients from receiving inappropriate therapy when confronted with HCAP. Previously known surveillance cultures may also decrease the percentage of HCAP in which the causative micro-organism(s) remains unidentified, which is currently more than 30% [9]. As the Western population is increasingly becoming geriatric, with associated increases in healthcare services and costs, the population at risk for HCAP is also increasing annually. This will lead to additional costs, use of more antibiotics and/or potential increase of MDR micro-organisms. With this perspective, it seems paramount to optimize attempts to sequentially map the causative microorganisms involved.
CONCLUSION Although frequently quasi-experimental in nature and performed in heterogeneous populations, several studies have indicated that surveillance cultures could appropriately guide antibiotic treatment in VAP and MDR Gram-negative bacilli management. In a high-risk population, surveillance cultures for the presence of MRSA and VRE appeared useful, at least in countries with an already high prevalence of these micro-organisms. Surveillance cultures of ETA positive for Gram-negative bacilli and Aspergillus spp. are predictive for the development of nosocomial infections and invasive aspergillosis. Surveillance cultures could be cost-effective, especially in the context of a high prevalence of MDR in a population at high risk for pneumonia together with lower laboratory costs. So far, contemporary pneumonia management guidelines lack recommendations regarding the routine use of surveillance cultures. Despite these facts, surveillance cultures may have an important future role in HCAP management, especially owing to increasing MDR and population at risk. Further research on the usefulness of surveillance cultures is urgently needed to improve the understanding and management of HCAP patients, thereby proving its possible place in guidelines.
Acknowledgements We gratefully thank Helke A. van Dessel, medical microbiologist and Paul M.H.J. Roekaerts, professor of intensive care medicine, both associated with the Maastricht University Medical Center, Maastricht, The Netherlands for commenting on this manuscript. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Attridge RT. Healthcare-associated pneumonia: refining the HCAP criteria. In: Pharmacotherapy Conference; November 20, 2009. San Antonio, TX: University of Texas Health Sciences Center; 2009. pp. 1–25. 2. Carratala J, Mykietiuk A, Fernandez-Sabe N, et al. Healthcare-associated pneumonia requiring hospital admission: epidemiology, antibiotic therapy, and clinical outcomes. Arch Intern Med 2007; 167:1393–1399. 3. Quartin AA, Scerpella EG, Puttagunta S, Kett DH. A comparison of & microbiology and demographics among patients with healthcare-associated, hospital-acquired, and ventilator-associated pneumonia: a retrospective analysis of 1184 patients from a large, international study. BMC Infect Dis 2013; 13:561. Large analysis of HCAP, HAP and VAP patients, revealing that frequencies of causative MDR Gram-negative pathogens are similar in all groups. 4. Polverino E, Torres A, Menendez R, et al. Microbial aetiology of healthcare & associated pneumonia in Spain: a prospective, multicentre, case-control study. Thorax 2013; 68:1007–1014. Prospective multicenter case–control study, demonstrating more comorbidities and worse clinical outcome in HCAP patients compared with matched CAP patients. 5. American Thoracic Society. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med 2005; 171:388–416. 6. Micek ST, Kollef KE, Reichley RM, et al. Healthcare-associated pneumonia and community-acquired pneumonia: a single-center experience. Antimicrob Agents Chemother 2007; 51:3568–3573. 7. Kollef MH, Shorr A, Tabak YP, et al. Epidemiology and outcomes of healthcare-associated pneumonia: results from a large US database of culturepositive pneumonia. Chest 2005; 128:3854–3862. 8. Giannella M, Pinilla B, Capdevila JA, et al. Pneumonia treated in the & internal medicine department: focus on healthcare-associated pneumonia. Clin Microbiol Infect 2012; 18:786–794. Survey demonstrated HCAP to be more present in older patients with poor functional status and that etiology differs from CAP and HAP. 9. Garcia-Vidal C, Viasus D, Roset A, et al. Low incidence of multidrug-resistant organisms in patients with healthcare-associated pneumonia requiring hospitalization. Clin Microbiol Infect 2011; 17:1659–1665. 10. Chalmers JD, Rother C, Salih W, Ewig S. Healthcare associated && pneumonia does not accurately identify potentially resistant pathogens: a systematic review and meta-analysis. Clin Infect Dis 2013; 58:330– 339. Systematic recent review of 24 studies demonstrating that HCAP patients, compared to CAP patients, are more at risk for infections with MRSA, multidrug-resistant (MDR) Enterobacteriaceae or P. aeruginosa. 11. Venditti M, Falcone M, Corrao S, et al. Outcomes of patients hospitalized with community-acquired, healthcare-associated, and hospital-acquired pneumonia. Ann Intern Med 2009; 150:19–26. 12. van Duijn PJ, Dautzenberg MJ, Oostdijk EA. Recent trends in antibiotic resistance in European ICUs. Curr Opin Crit Care 2011; 17:658–665. 13. Gastmeier P, Geffers C, Brandt C, et al. Effectiveness of a nationwide nosocomial infection surveillance system for reducing nosocomial infections. J Hosp Infect 2006; 64:16–22. 14. Carlet J, Astagneau P, Brun-Buisson C, et al. French national program for prevention of healthcare-associated infections and antimicrobial resistance, 1992-2008: positive trends, but perseverance needed. Infect Control Hosp Epidemiol 2009; 30:737–745. 15. Gaynes R, Richards C, Edwards J, et al. Feeding back surveillance data to prevent hospital-acquired infections. Emerg Infect Dis 2001; 7: 295–298.
1070-5287 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-pulmonarymedicine.com
269
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Infectious diseases 16. Benet T, Allaouchiche B, Argaud L, Vanhems P. Impact of surveillance of hospital-acquired infections on the incidence of ventilator-associated pneumonia in intensive care units: a quasi-experimental study. Crit Care 2012; 16:R161. An increase in VAP rates and mortality was seen after the cessation of a surveillance program in one ICU compared to continuing the program in another ICU. 17. Gil-Perotin S, Ramirez P, Marti V, et al. Implications of endotracheal tube & biofilm in ventilator-associated pneumonia response: a state of concept. Crit Care 2012; 16:R93. Prospective study demonstrating the continuity of airway colonization, biofilm formation and VAP development. 18. Bonten MJ, Bergmans DC, Ambergen AW, et al. Risk factors for pneumonia, and colonization of respiratory tract and stomach in mechanically ventilated ICU patients. Am J Respir Crit Care Med 1996; 154:1339–1346. 19. Cardenosa Cendrero JA, Sole-Violan J, Bordes Benitez A, et al. Role of different routes of tracheal colonization in the development of pneumonia in patients receiving mechanical ventilation. Chest 1999; 116:462–470. 20. Boots RJ, Phillips GE, George N, Faoagali JL. Surveillance culture utility and safety using low-volume blind bronchoalveolar lavage in the diagnosis of ventilator-associated pneumonia. Respirology 2008; 13:87–96. 21. Brusselaers N, Labeau S, Vogelaers D, Blot S. Value of lower respiratory tract && surveillance cultures to predict bacterial pathogens in ventilator-associated pneumonia: systematic review and diagnostic test accuracy meta-analysis. Intensive Care Med 2013; 39:365–375. First systematic review on the value of surveillance cultures of ETA for VAP management. 22. A’Court CH, Garrard CS, Crook D, et al. Microbiological lung surveillance in mechanically ventilated patients, using nondirected bronchial lavage and quantitative culture. Q J Med 1993; 86:635–648. 23. de Latorre FJ, Pont T, Ferrer A, et al. Pattern of tracheal colonization during mechanical ventilation. Am J Respir Crit Care Med 1995; 152:1028–1033. 24. Delclaux C, Roupie E, Blot F, et al. Lower respiratory tract colonization and infection during severe acute respiratory distress syndrome: incidence and diagnosis. Am J Respir Crit Care Med 1997; 156:1092–1098. 25. Flanagan PG, Findlay GP, Magee JT, et al. The diagnosis of ventilatorassociated pneumonia using nonbronchoscopic, nondirected lung lavages. Intensive Care Med 2000; 26:20–30. 26. Hayon J, Figliolini C, Combes A, et al. Role of serial routine microbiologic culture results in the initial management of ventilator-associated pneumonia. Am J Respir Crit Care Med 2002; 165:41–46. 27. Bouza E, Perez A, Munoz P, et al. Ventilator-associated pneumonia after heart surgery: a prospective analysis and the value of surveillance. Crit Care Med 2003; 31:1964–1970. 28. Michel F, Franceschini B, Berger P, et al. Early antibiotic treatment for BALconfirmed ventilator-associated pneumonia: a role for routine endotracheal aspirate cultures. Chest 2005; 127:589–597. 29. Depuydt P, Benoit D, Vogelaers D, et al. Outcome in bacteremia associated with nosocomial pneumonia and the impact of pathogen prediction by tracheal surveillance cultures. Intensive Care Med 2006; 32:1773–1781. 30. Depuydt PO, Blot SI, Benoit DD, et al. Antimicrobial resistance in nosocomial bloodstream infection associated with pneumonia and the value of systematic surveillance cultures in an adult intensive care unit. Crit Care Med 2006; 34:653–659. 31. Bagnulo HGM, Galiana A, Bertulo M, Pedreira W. Are routine endotracheal aspirates predictive of etiology of ventilator-associated pneumonia? Crit Care 2007; 11 (Suppl 2):87. 32. Malacarne P, Corini M, Maremmani P, et al. Diagnostic characteristics of routine surveillance cultures of endotracheal aspirate samples in cases of lateonset ventilator-associated pneumonia due to Acinetobacter baumannii. Infect Control Hosp Epidemiol 2007; 28:867–869. 33. Depuydt P, Benoit D, Vogelaers D, et al. Systematic surveillance cultures as a tool to predict involvement of multidrug antibiotic resistant bacteria in ventilator-associated pneumonia. Intensive Care Med 2008; 34:675–682. 34. Nair S, Sen N, Peter JV, et al. Role of quantitative endotracheal aspirate and cultures as a surveillance and diagnostic tool for ventilator associated pneumonia: a pilot study. Indian J Med Sci 2008; 62:304–313. 35. Jung B, Sebbane M, Chanques G, et al. Previous endotracheal aspirate allows guiding the initial treatment of ventilator-associated pneumonia. Intensive Care Med 2009; 35:101–107. 36. Pirracchio R, Mateo J, Raskine L, et al. Can bacteriological upper airway samples obtained at intensive care unit admission guide empiric antibiotherapy for ventilator-associated pneumonia? Crit Care Med 2009; 37:2559– 2563. 37. Lampati L, Maggioni E, Langer M, et al. Can routine surveillance samples from tracheal aspirate predict bacterial flora in cases of ventilator-associated pneumonia? Minerva Anestesiol 2009; 75:555–562. 38. Joseph NM, Sistla S, Dutta TK, et al. Ventilator-associated pneumonia: role of colonizers and value of routine endotracheal aspirate cultures. Int J Infect Dis 2010; 14:e723–e729. 39. Gursel G, Aydogdu M, Nadir Ozis T, Tasyurek S. Comparison of the value of initial and serial endotracheal aspirate surveillance cultures in predicting the causative pathogen of ventilator-associated pneumonia. Scand J Infect Dis 2010; 42:341–346. &
270
www.co-pulmonarymedicine.com
40. Brusselaers N, Logie D, Vogelaers D, et al. Burns, inhalation injury and ventilator-associated pneumonia: value of routine surveillance cultures. Burns 2012; 38:364–370. 41. Chan JD, Dellit TH, Choudhuri JA, et al. Active surveillance cultures of methicillin-resistant Staphylococcus aureus as a tool to predict methicillin-resistant S. aureus ventilator-associated pneumonia. Crit Care Med 2012; 40:1437–1442. 42. Luna CM, Sarquis S, Niederman M, et al. Is an endotracheal routine cultures& based strategy the best way to prescribe antibiotics in ventilator-associated pneumonia? Chest 2013; 144:63–71. Prospective observational cohort study comparing ETA surveillance cultures (collected 7 days before VAP) guided strategy to ATS guideline guided strategy. ATS-guided stategy was more accurate (98%), but less antibiotics were used in the ETA group. 43. Price CS, Paule S, Noskin GA, Peterson LR. Active surveillance reduces the incidence of vancomycin-resistant enterococcal bacteremia. Clin Infect Dis 2003; 37:921–928. 44. Huang SS, Rifas-Shiman SL, Pottinger JM, et al. Improving the assessment of vancomycin-resistant enterococci by routine screening. J Infect Dis 2007; 195:339–346. 45. Huang SS, Rifas-Shiman SL, Warren DK, et al. Improving methicillinresistant Staphylococcus aureus surveillance and reporting in intensive care units. J Infect Dis 2007; 195:330–338. 46. McGinigle KL, Gourlay ML, Buchanan IB. The use of active surveillance cultures in adult intensive care units to reduce methicillin-resistant Staphylococcus aureus-related morbidity, mortality, and costs: a systematic review. Clin Infect Dis 2008; 46:1717–1725. 47. Robicsek A, Beaumont JL, Paule SM, et al. Universal surveillance for methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med 2008; 148:409–418. 48. Stano P, Avolio M, De Rosa R, et al. An antibiotic care bundle approach based on results of rapid molecular screening for nasal carriage of methicillinresistant Staphylococcus aureus in the intensive care unit. In Vivo 2012; 26:469–472. 49. Huskins WC, Huckabee CM, O’Grady NP, et al. Intervention to reduce transmission of resistant bacteria in intensive care. N Engl J Med 2011; 364:1407–1418. 50. Bertrand X, Thouverez M, Talon D, et al. Endemicity, molecular diversity and colonisation routes of Pseudomonas aeruginosa in intensive care units. Intensive Care Med 2001; 27:1263–1268. 51. Blot S, Depuydt P, Vogelaers D, et al. Colonization status and appropriate antibiotic therapy for nosocomial bacteremia caused by antibioticresistant Gram-negative bacteria in an intensive care unit. Infect Control Hosp Epidemiol 2005; 26:575–579. 52. Reddy P, Malczynski M, Obias A, et al. Screening for extended-spectrum betalactamase-producing Enterobacteriaceae among high-risk patients and rates of subsequent bacteremia. Clin Infect Dis 2007; 45:846–852. 53. Papadomichelakis E, Kontopidou F, Antoniadou A, et al. Screening for resistant Gram-negative microorganisms to guide empiric therapy of subsequent infection. Intensive Care Med 2008; 34:2169–2175. 54. Baba H, Nimmo GR, Allworth AM, et al. The role of surveillance cultures in the prediction of susceptibility patterns of Gram-negative bacilli in the intensive care unit. Eur J Clin Microbiol Infect Dis 2011; 30:739–744. 55. Galoisy-Guibal L, Soubirou JL, Desjeux G, et al. Screening for multidrugresistant bacteria as a predictive test for subsequent onset of nosocomial infection. Infect Control Hosp Epidemiol 2006; 27:1233–1241. 56. Vandewoude KH, Blot SI, Depuydt P, et al. Clinical relevance of Aspergillus isolation from respiratory tract samples in critically ill patients. Crit Care 2006; 10:R31. 57. Sreeramoju PV, Garcia-Houchins S, Bova J, et al. Correlation between respiratory colonization with Gram-negative bacteria and development of Gram-negative bacterial infection after cardiac surgery. Infect Control Hosp Epidemiol 2008; 29:546–548. 58. Novosel TJ, Hodge LA, Weireter LJ, et al. Ventilator-associated pneumonia: && depends on your definition. Am Surg 2012; 78:851–854. Analysis on different VAP definitions and their clinical consequences. VAP studies include a heterogenous population, which makes them hard to compare. 59. Worster A, Carpenter C. Incorporation bias in studies of diagnostic tests: how to avoid being biased about bias. CJEM 2008; 10:174–175. 60. Yang K, Zhuo H, Guglielmo BJ, Wiener-Kronish J. Multidrug-resistant Pseudomonas aeruginosa ventilator-associated pneumonia: the role of endotracheal aspirate surveillance cultures. Ann Pharmacother 2009; 43: 28–35. 61. Aydogdu M, Gursel G, Hizel K, Ozis TN. Comparison of the serial surveillance with quantitative and nonquantitative tracheal aspirate in predicting ventilatorassociated pneumonia etiology in patients receiving antibiotic therapy. Minerva Anestesiol 2010; 76:600–608. 62. Lodise TP, McKinnon PS. Clinical and economic impact of methicillin resistance in patients with Staphylococcus aureus bacteremia. Diagn Microbiol Infect Dis 2005; 52:113–122. 63. Cosgrove SE, Sakoulas G, Perencevich EN, et al. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003; 36:53–59.
Volume 20 Number 3 May 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Surveillance cultures in pneumonia Scholte et al. 64. Jernigan JA, Titus MG, Groschel DH, et al. Effectiveness of contact isolation during a hospital outbreak of methicillin-resistant Staphylococcus aureus. Am J Epidemiol 1996; 143:496–504. 65. Kluytmans-Vandenbergh MF, Kluytmans JA, Voss A. Dutch guideline for preventing nosocomial transmission of highly resistant microorganisms (HRMO). Infection 2005; 33:309–313. 66. Verhoef J, Beaujean D, Blok H, et al. A Dutch approach to methicillin-resistant Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 1999; 18:461–466. 67. Muto CA, Jernigan JA, Ostrowsky BE, et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 2003; 24:362– 386. 68. Wernitz MH, Swidsinski S, Weist K, et al. Effectiveness of a hospital-wide selective screening programme for methicillin-resistant Staphylococcus aureus (MRSA) carriers at hospital admission to prevent hospital-acquired MRSA infections. Clin Microbiol Infect 2005; 11:457–465. 69. de Smet AM, Hopmans TE, Minderhoud AL, et al. Decontamination of the digestive tract and oropharynx: hospital acquired infections after discharge from the intensive care unit. Intensive Care Med 2009; 35:1609–1613. 70. Van de Voort PHJ, van Saene HKF (editors). Selective digestive tract decontamination in intensive care medicine: a practical guide to controlling infection. 1 ed. Springer; 2008. 71. Viviani M, Van Saene HK, Pisa F, et al. The role of admission surveillance cultures in patients requiring prolonged mechanical ventilation in the intensive care unit. Anaesth Intensive Care 2010; 38:325–335. 72. Thouverez M, Talon D, Bertrand X. Control of Enterobacteriaceae producing extended-spectrum beta-lactamase in intensive care units: rectal screening may not be needed in nonepidemic situations. Infect Control Hosp Epidemiol 2004; 25:838–841. 73. Muto CA, Giannetta ET, Durbin LJ, et al. Cost-effectiveness of perirectal surveillance cultures for controlling vancomycin-resistant Enterococcus. Infect Control Hosp Epidemiol 2002; 23:429–435. 74. Nyman JA, Lees CH, Bockstedt LA, et al. Cost of screening intensive care unit patients for methicillin-resistant Staphylococcus aureus in hospitals. Am J Infect Control 2011; 39:27–34. 75. Karchmer TB, Durbin LJ, Simonton BM, Farr BM. Cost-effectiveness of active surveillance cultures and contact/droplet precautions for control of methicillin-resistant Staphylococcus aureus. J Hosp Infect 2002; 51:126– 132. 76. Robotham JV, Graves N, Cookson BD, et al. Screening, isolation, and decolonisation strategies in the control of meticillin resistant Staphylococcus aureus in intensive care units: cost effectiveness evaluation. BMJ 2011; 343:d5694. 77. Olchanski N, Mathews C, Fusfeld L, Jarvis W. Assessment of the influence of test characteristics on the clinical and cost impacts of methicillin-resistant Staphylococcus aureus screening programs in US hospitals. Infect Control Hosp Epidemiol 2011; 32:250–257.
78. Masterton R, Craven D, Rello J, et al. Hospital-acquired pneumonia guidelines in Europe: a review of their status and future development. J Antimicrob Chemother 2007; 60:206–213. 79. Mandell LA, Wunderink RG, Anzueto A, et al. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis 2007; 44 (Suppl 2):S27–72. 80. Memish ZA, Arabi YM, Ahmed QA, et al. Executive summary of the Gulf Cooperation Council practice guidelines for the management of community-acquired pneumonia. J Chemother 2007; 19 (Suppl 1): 7–11. 81. Feldman C, Brink AJ, Richards GA, et al. Management of community-acquired pneumonia in adults. S Afr Med J 2007; 97:1296–1306. 82. Muscedere J, Dodek P, Keenan S, et al. Comprehensive evidence-based clinical practice guidelines for ventilator-associated pneumonia: prevention. J Crit Care 2008; 23:126–137. 83. Muscedere J, Dodek P, Keenan S, et al. Comprehensive evidence-based clinical practice guidelines for ventilator-associated pneumonia: diagnosis and treatment. J Crit Care 2008; 23:138–147. 84. Masterton RG, Galloway A, French G, et al. Guidelines for the management of hospital-acquired pneumonia in the UK: report of the working party on hospital-acquired pneumonia of the British Society for Antimicrobial Chemotherapy. J Antimicrob Chemother 2008; 62:5–34. 85. Mosier MJ, Pham TN. American Burn Association Practice guidelines for prevention, diagnosis, and treatment of ventilator-associated pneumonia (VAP) in burn patients. J Burn Care Res 2009; 30:910– 928. 86. Correa Rde A, Lundgren FL, Pereira-Silva JL, et al. Brazilian guidelines for community-acquired pneumonia in immunocompetent adults: 2009. J Bras Pneumol 2009; 35:574–601. 87. Lim WS, Baudouin SV, George RC, et al. BTS guidelines for the management of community acquired pneumonia in adults: update 2009. Thorax 2009; 64 (Suppl 3):iii1–iii55. 88. Menendez R, Torres A, Aspa J, et al. Community acquired pneumonia. New guidelines of the Spanish Society of Chest Diseases and Thoracic Surgery (SEPAR). Arch Bronconeumol 2010; 46:543–558. 89. Woodhead M, Blasi F, Ewig S, et al. Guidelines for the management of adult lower respiratory tract infections: full version. Clin Microbiol Infect 2011; 17 (Suppl 6):E1–E59. 90. Wiersinga WJ, Bonten MJ, Boersma WG, et al. SWAB/NVALT (Dutch Working Party on Antibiotic Policy and Dutch Association of Chest Physicians) guidelines on the management of community-acquired pneumonia in adults. Neth J Med 2012; 70:90–101. 91. Spindler C, Stralin K, Eriksson L, et al. Swedish guidelines on the management of community-acquired pneumonia in immunocompetent adults: Swedish Society of Infectious Diseases 2012. Scand J Infect Dis 2012; 44:885–902.
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