Staphylococcus aureus (SA) is a leading cause of bacteremia. High mortality rates from 20% to 50%, frequent recurrences from 5% to 10%, and lasting impairment in more than one-third of the survivors characterize S. aureus bloodstream infections (BSI) (Asgeirsson et al. 2018; Kern and Rieg 2020). S. aureus infections are particularly problematic due to the frequent antibiotic resistance, among which methicillin resistance is the most clinically relevant (Turner et al. 2019). Patients with methicillin-resistant S. aureus (MRSA) bacteremia stay longer in hospitals and generate higher costs than those with bacteremia caused by methicillin-susceptible S. aureus (MSSA) (Tsuzuki et al. 2021).
MRSA often requires vancomycin therapy. Vancomycin use is associated with increased antimicrobial and monitoring costs and may bring about drug-induced acute kidney injury in up to 15% of patients (Pritchard et al. 2010). Furthermore, empirical anti-MRSA treatment for MSSA bacteremia can lead to poor outcomes compared with standard therapy (Jones et al. 2020). Therefore, rapid and accurate discrimination of MRSA from MSSA is essential for clinical diagnosis to facilitate a specific antimicrobial therapy (Srisrattakarn et al. 2022).
When the positive blood culture starts, conventional S. aureus identification takes about 48 to 72 h to complete. Recent advances in molecular and nonmolecular testing methods significantly reduced the turnaround
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License (https://creativecommons.org/licenses/by-nc-nd/4.0/).
Rapid and simple techniques are required to address the challenges raised by S. aureus BSI, employing rapid pathogen identification and susceptibility testing to enable specific targeted antibiotic therapy on time.
This review updates recent advances in rapid and simple assays to identify S. aureus in bloodstream infections and discusses the advantages and limitations of these methods.
Methods
The authors searched PubMed and Google Scholar with the following terms: bloodstream infections, S. aureus, rapid diagnostics, bacteremia, and blood cultures. English and Japanese literature for randomized clinical trials (RCTs), meta-analyses, systematic reviews, and observational studies were evaluated (1999–2022). The author agreed with the quality of included studies.
Direct detection of S. aureus from blood samples
Hybrisep – an in situ hybridization method. Hybrisep is an in situ hybridization-based assay which detects specific bacterial DNA in smears enriched in polymorphonuclear neutrophils (PMN) from the blood of suspected BSI individuals. At an early stage of sepsis, neutrophils ingest bacteria, and bacterial DNA can be detected in the blood smears by an in situ hybridization (ISH) method. In 1999, an ISH assay targeted phagocyted bacteria from blood was developed by collecting the blood and preparing neutrophil-enriched smears. The neutrophils were then permeabilized and incubated with specific probes (Shimada et al. 1999). Digoxygenin-labelled probes and anti-digoxygenin-alkaline phosphatase conjugates were utilized. BCIP (5-bromo-4-chloro-3-indolyl-phosphate) with NBT (nitro blue tetrazolium) was used as a substrate for ALP and allowed the signal visualization. These signals were observed in the cell cytoplasm under a microscope. Blue-colored dots represented the phagocytized bacteria in neutrophils, and it was assumed a positive result. The first available kit Hybrisep (Fuso Pharmaceuticals, Japan), provided five probes, including those specific to S. aureus. In 2014, Enomoto et al. (2014) introduced a new ISH assay that contained a universal probe targeting 59 species of 35 genera. The hybridization and washing procedures were performed automatically by Hybristat. The whole process takes about eight hours.
The ISH assay was used to investigate blood smears from 60 patients with suspected sepsis (Kudo et al. 2009). Nine S. aureus strains were detected with ISH assay, while only one blood was found to be positive for S. aureus by conventional culture. Discrepancies were found to be due to the effect of antibiotic treatment. Three of the nine patients with positive S. aureus blood cultures underwent antibiotic therapy before blood sampling. Therefore, the ISH method appeared less affected by antibiotic treatment than blood culture.
Over 40% of patients can take antibiotics before blood collection (Roh et al. 2012). Although new blood culture bottles contain neutralization of antimicrobial substances, the elimination effect for antibiotics is limited by the concentration of antibiotics in the blood (Mitteregger et al. 2013). ISH depends on the hybridization performed in neutrophils; thus, a reduced number of neutrophils resulting from immunosuppressive therapy may decrease the sensitivity of the ISH assay. As an independent-culture method, ISH is beneficial for managing patients with BSI, despite the absence of S. aureus in blood culture. So far, the Hybrisep kit and Hybristat are available only in Japan. Only limited studies on ISH for S. aureus detection in blood have been reported (Kudo et al. 2009). Further studies of ISH for S. aureus detection in blood should be conducted through multicenter cooperation.
T2Dx magnetic resonance assay. The T2Dx system (T2 Biosystems, USA), an automated instrument, uses a method based on magnetic resonance changes in the water proton T2 relaxation signal in the presence of a magnetic field (Neely et al. 2013). The protocol includes a pathogen-specific amplification step, and the amplicons are hybridized into specific probe-enriched nanoparticles (Paolucci et al. 2010). The T2Bacteria Panel enables multiplex detection of the ESKAPE pathogens (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species). De Angelis et al. (2018), upon evaluation of 140 suspected BSI samples, detected two of two S. aureus strains with the T2Bacteria Panel and confirmed this finding by blood culture. The remaining 138 samples were negative when using the T2Bacteria Panel and a paired blood culture. The sensitivity and specificity of T2Dx for S. aureus identification was 100% compared to the blood culture. Another study by Drevinek et al. (2021) found a good sensitivity of the T2Dx system. In 55 samples, two of two S. aureus strains were detected by the T2Bacteria Panel, but the corresponding blood culture detected only one strain. Nguyen et al. (2019) conducted a prospective multi-center study involving 1,427 samples. The T2Dx system and blood culture identified 41 and 16 S. aureus strains, respectively. The turnaround time of the T2Dx system was shorter than that of the blood culture (3.6–7.7 h vs. 38.5–71.7 h, respectively). It demonstrates that the T2Dx system has value over blood culture in patients receiving antimicrobial therapy.
Rapid detection of S. aureus from positive blood cultures
BinaxNOW Staphylococcus aureus test with BinaxNow PBP2a assay. The principle of BinaxNow Staphylococcus aureus (Alere, USA) and BinaxNowPBP2a (Alere SAS, France) assays is an immunochromatographic test for the identification of S. aureus and the determination of methicillin resistance, respectively. BinaxNow Staphylococcus aureus test was FDA approved for direct identification of S. aureus. It uses polyclonal antibodies to qualitatively detect an S. aureus-specific protein in a positive blood culture (Dhiman et al. 2013). Qian et al. (2014) collected 104 blood cultures from 2012 to 2013 that were tested with this method. The blood cultures included 41 S. aureus (14 MRSA, 27 MSSA), 60 CoNS (coagulase-negative Staphylococci), three other Gram-positive cocci in pairs and clusters (one of Micrococcus species, one anerobic Gram-positive coccus, and one of Gemella species). The BinaxNow Staphylococcus aureus test showed 97.6% sensitivity, 100% specificity, and positive and negative predictive values of 100% and 98.4%, respectively, upon S. aureus identification in positive blood culture. The performance was equally efficient in both aerobic and anaerobic bottles. Only one false-negative result was found due to antibiotic treatment of the patient and the resulting reduction in the antigen’s level. Dhiman et al. (2013) evaluated 319 positive blood cultures containing clusters of Gram-positive cocci using the BinaxNow Staphylococcus aureus test. The study achieved 95.8% of sensitivity and 99.6% of specificity. One false-positive result occurred in the blood culture containing a presumptive Staphylococcus lugdunensis isolate not later confirmed. One false-negative result was confirmed by repeated testing. It might have resulted from a decrease in the bacterial concentration below the detection limit (5.42 × 108 cells/ ml). One study combined BinaxNow Staphylococcus aureus for species identification and BinaxNow PBP2a assay to detect methicillin resistance (Heraud et al. 2015). Seventy-nine positive blood cultures with Gram-positive cocci in clusters were tested. A sensitivity of 94% and specificity of 98% in identifying S. aureus and 100% sensitivity and specificity of methicillin resistance detection were reported. These tests are valuable alternatives for the diagnosis of MRSA bacteremia.
Gram staining. Gram staining is an essential technique in microbiology. It was invented by Danish bacteriologist Hans Christian Gram in 1882 (Wu and Yang 2020). Gram staining distinguishes Gram-positive from Gram-negative organisms based on differences in their cell walls. The thick cell walls of Gram-positive bacteria retain the purple crystal violet-iodine complex after treatment with ethanol (O’Toole 2016). Once a blood culture is detected as positive by an automated, continuously monitoring blood culture system, a smear is Gram stained, providing a quick presumptive identification of pathogens. It might be helpful in directing the bread antibiotic therapy (Boyanova 2018). Gram staining is a crucial but easy, rapid, and inexpensive method for pathogen detection in a positive blood culture. A series of evaluating criteria were developed based on the type of blood culture bottle, bacterial species, and cluster characteristics (Murdoch and Greenlees 2004). These criteria may help an experienced microbiological technician to distinguish S. aureus from CoNS in positive blood cultures. It allowed for achieving the overall sensitivity and specificity of 89% and 98%, respectively. A prospective observational study with 118 blood samples showed that a pink-colored “oozing sign” could also be used to distinguish S. aureus from CoNS (Hadano et al. 2018). The study demonstrated a sensitivity and specificity of 78.7% and 95.0%, respectively. Compared to the previous study by Murdoch and Greenlees (2004), this method focused on the “oozing sign” regardless of blood culture bottle type, organism species, and cluster characteristics. Therefore, it is simpler and more suitable than the previous method for application in routine work. A significant advantage of Gram staining is to be a good alternative for a community hospital without a diagnostic microbiology laboratory. The quality of Gram staining depends on the skills and can vary over time and between technicians. With the development of automated Gram staining systems, the comparability and consistency of results can be improved in laboratories (Baron et al. 2010). It also holds for new automated image acquisition systems as a convolutional neural network-based classification of Gram staining results (Smith et al. 2018). Integrating these techniques with previous evaluation criteria in S. aureus identification may make the Gram staining method more uncomplicated and accurate. Early identification of S. aureus in blood cultures is vital because the clinical signs of S. aureus bacteremia may be unspecific and therefore, the patients may be no symptomatic early in the course of the infection (Mitchell and Howden 2005).
PNA FISH and QuickFISH assays. Fluorescent in situ hybridization (FISH) is a diagnostic technique using a probe (e.g., peptide nucleic (PNA) probe) to target the 16S rRNA gene of S. aureus directly in the blood culture smears. Fluorescence in situ hybridization using the PNA probes is a useful diagnostic tool for pathogen-directed therapy (Weaver et al. 2019). PNA probes have unique performance characteristics that render PNA FISH to be applied widely to positive blood cultures. The first commercially available kit was PNA FISH (OpGen®, USA, previously AdvanDx). González et al. (2004) evaluated 285 blood cultures containing Gram-positive cocci similar to staphylococci using PNA FISH. The results showed 100% sensitivity, and 99.4% specificity, and their positive and negative predictive values were 99.2% and 100%, respectively. The PNA probe recognizes both MRSA and MSSA. In ten positive blood cultures mixed with other bacteria, S. aureus was correctly identified. Only one weak positive hybridization was obtained with a positive blood culture of Staphylococcus schleiferi. Oliveira et al. (2003) performed a blinded comparison of S. aureus PNA FISH in eight centres with three types of blood culture bottles produced by different manufacturers (ESP, BACTEC, and BacT/Alert). The sensitivity ranged from 98.5% to 100%, the specificity was between 98.5% and 99.1%.
Even a potentially interfering substance as charcoal did not affect the performance of S. aureus PNA FISH. The total analysis time is up to 2.5 h, and hands-on time is below 30 min. QuickFISH was launched in 2013 (Carretto et al. 2013), a modified PNA FISH version with several timesaving innovations. It takes less than 30 min. because procedure does not include washing or mounting of slides, and the hands-on time is about 5 min. Deck et al. (2012) tested 722 positive blood cultures containing Gram-positive cocci in cluster using the Staphylococcus QuickFISH method. The sensitivity was 99.5%, and the combined specificity was 89.5%. Two false positive and seven false negative results were found. The discrepancies between the Staphylococcus QuickFISH method and the standard method were due to human errors or to the limited sequence alignment of the probes designed. The Staphylococcus QuickFISH method can speed up the S. aureus identification in blood cultures. It would help in the patient’s management when catheter-related BSI is suspected. Early catheter removal is recommended when S. aureus is detected to decrease the risks of persistent bacteremia and hematogenous complications.
Accelerate PhenoTM system. The fully automated Accelerate PhenoTM system provides rapid identification and susceptibility of microorganisms in positive blood samples (Cenci et al. 2020). The system combines FISH for bacterial identification and an automated microscope for assessing bacterial growth rates and calculating the MIC value (Marschal et al. 2017). Molecular methods and MALDI-TOF MS can also identify microorganisms in positive blood cultures and their susceptibility phenotype in a few hours. However, these methods must provide the susceptibility phenotype that clinicians request to make a therapeutic decision. This need drove Accelerate DiagnosticTM (USA) to develop an Accelerate PhenoTM system (APS). The multiplex fluorescence in situ hybridization using target-specific probes is a diagnostic strategy APS uses to identify on-panel microbes. The minimum inhibitory concentration (MIC) is evaluated after analyzing the bacterial morphokinetic growth pattern in the presence of a given antimicrobial agent (Marschal et al. 2017). Charnot-Katsikas et al. (2017) investigated 232 blood cultures using APS and compared the results with the standard method. After considering the discrepant results, the sensitivity and specificity for S. aureus were 94.7% and 99.0%, respectively.
The categorical agreement between APS and standard antimicrobial susceptibility tests (AST) was 98.5%. Only two minor errors were found upon conventional testing of 68 S. aureus strains. When using APS for blood culture, the turnaround time was shortened to about 23.47 h, 41.86 h, and 25.5 min. for identification, susceptibility, and hands-on time, respectively. Lutgring et al. (2018) demonstrated that the sensitivity and specificity of S. aureus detection using APS in positive blood cultures were 96.9%, and 95.2%, respectively. The categorical agreement between APS and culture-based AST was 100% upon S. aureus testing. Since the identification and AST were performed in 1.5 h and 7 h, respectively, as opposed to a few days with conventional testing, it would decrease morbidity and mortality of patients with BSI. It is due to the switch from broad-spectrum empiric therapy to targeted specific antibiotic therapy since it decreases adverse effects and the emergence of multi-drug resistance organisms. However, APS has low performance for correct identification, and AST results in polymicrobial blood cultures. It is also of a high cost compared to standard methods. All these APS characteristics should be considered for a diagnostic and treatment decision.
MALDI-TOF MS. One of the soft ionization techniques, a matrix-assisted laser desorption ionizationtime of flight mass spectrometry (MALDI-TOF MS), generates a protein-based spectral profile or “fingerprint” unique to a given species of pathogen. The microorganism identification relies on the characteristic spectrum of each species.
MALDI-TOF MS has revolutionized microorganism identification and is now widely used in routine laboratory testing. Two main commercial systems are used worldwide, the Vitek MS (bioMerieux, France) and Microflex LT Biotyper (Bruker Daltonics, USA). The detection limit is 108 CFU/ ml of positive blood culture broth (Christner et al. 2010).
S. aureus identification from positive blood culture with MALDI-TOF MS can be conducted according to two protocols: (a) after short-term incubation on a solid medium or (b) directly from the positive blood culture pellet. Curtoni et al. (2017) reported reliable species identification in less than 5 h. The identification of S. aureus was successful at 85.7% and 100% after 3 h and 5 h of incubation, respectively. It means that MALDI-TOF MS can be a reliable, easy, and rapid method for the S. aureus identification from positive blood culture when performed after a short-term culture of bacteria on a solid medium. Direct identification from blood culture involves the protein extraction after bacterial lysis and filtration (Foster 2013; Lin et al. 2018), use of a Sepsityper® kit (Bruker) or serum separator tube (Zengin and Bayraktar 2021), and in-house saponin-based bacterial extraction (Hu et al. 2020; Ponderand et al. 2020). Tsuchida et al. (2018) compared an in-house lysis filtration protocol with a Sepsityper® kit for S. aureus identification. Out of a total of 19 S. aureus strains, 17 were identified to species level by a lysis filtration protocol, two to genus level, whereas 11 of these strains were identified to species level and four to genus level. Four strains could not be identified by the Sepsityper® kit. The results showed that Sepsityper® kit failed to identify completely Gram-positive cocci in positive blood cultures.
Another study employed a serum separator tube followed by MALDI-TOF MS for S. aureus identification (Zengin and Bayraktar 2021). A total of 36 S. aureus strains were confirmed by a short-term incubation routine identification (SIRID) method and 32 strains from 36 monomicrobial cultures were correctly identified by direct rapid identification (RID) method using a serum separator tube followed by MALDI-TOF MS. The mean turnaround time of RID method was significantly lower compared to SIRID method (2.86 h vs. 19.49 h, p < 0.001). This study indicated that the serum separator tube method was suitable for the rapid identification of S. aureus in a blood culture.
MALDI-TOF MS has been proposed to detect strains susceptible or resistant to several antibiotics. Some studies reported accurate discrimination of S. aureus isolates susceptible to vancomycin (Mather et al. 2016). Recently, Liu et al. (2021) presented the machine learning algorithms for rapid MALDI-TOF MS-based MRSA screening. By selecting 38 m/z features for the classifying model and coupling it with machine-learning algorithms, a rapid and simple method to distinguish MRSA from MSSA was established. This method makes resistance detection more convenient and effective in routine microbiology laboratories.
FilmArray system. The FilmArray is a multiplex-PCR-based system that combines samples the preparation, PCR amplification, detection, and analysis (Peker et al. 2018). The BioFire FilmArray BCID2 panel can simultaneously identify 43 pathogens and ten antimicrobial resistance genes (Cortazzo et al. 2021). It takes about 2 min. of hands-on time and 1 h turnaround time. Sze et al. (2021) compared BioFire FilmArray BCID2 with MALDI-TOF MS for the S. aureus identification in blood cultures and reported both sensitivity and specificity of 100%. Furthermore, two out of two MRSA were detected by the BCID2 panel. Holma et al. (2022) presented similar results. These findings showed that the BioFire FilmArray BCID2 proves to be a good tool for the early detection of MRSA and the administration of effective antimicrobial therapy.
Xpert MRSA/SA BC assay. The Xpert MRSA/SA BC assay is based on a multiplex PCR. It targets the junction between S. aureus conserved open reading frame (orfx) and the SCC containing the mecA gene (SCC mecA). It enables Xpert MRSA/SA BC to detect and identify MRSA and MSSA in 1 h (Belmekki et al. 2013). A prospective study at two clinical centers investigated the impact of rapid detection of S. aureus in positive blood cultures on patient management (McHugh et al. 2020). In 264 blood cultures, 39 were positive for S. aureus, and one strain was identified as MRSA. Compared with the culture method, Xpert MRSA/SA BC has 100% sensitivity and 100% specificity for identifying S. aureus and 100% specificity for MRSA detection. For the Xpert MRSA/SA BC assay, the median turnaround time from blood culture processing to the final result was 1.7 h, compared to the 25.7 h turnaround time of the culture method. Xpert MRSA/SA BC results allowed early specific therapy for S. aureus and de-escalation of antimicrobial therapy for MSSA. Reddy and Whitelaw (2021) explored whether Xpert MRSA/SA BC assay can be utilized as an antimicrobial stewardship tool. Of 231 samples tested, concordance was 100% between the Xpert MRSA/SA BC assay and culture method. It can discriminate MRSA from MSSA and significantly reduce the laboratory turnaround time. This study showed the potential benefit of time reduction for the appropriate therapy introduction in most patients with S. aureus BSI.
Conclusions
Timely and targeted specific antibiotic therapy of S. aureus BSI improves survival and decreases the length of hospital stay and adverse effects of antibiotics. Although new approaches are utilized for rapid identification and AST, conventional methods are still indispensable.
Several rapid and simple methods, such as PNA FISH, MALDI-TOF MS, and the Accelerate PhenoTM system, are being used to diagnose positive blood cultures. PNA FISH and QuickFISH are well-validated methods. Utilization of MALDI-TOF MS directly from blood culture pellets is still in progress. The pre-treatment of the sample is being recognized as a standard approach. The Accelerate PhenoTM system provides not only rapid identification but also susceptibility reports (as the MIC values), while the low throughput of one sample per machine hinder this method from wide utilization. Gram staining integrated with machine-learning-based image analysis may lead to the rapid identification of S. aureus from blood culture. The BinaxNow Staphylococcus aureus and BinaxNow PBP2a appear to be a golden pair for the rapid identification and determination of methicillin resistance of S. aureus. The Hybrisep in situ hybridization and T2Dx assays have a high detection positive rate compared to blood cultures. Limited studies have been here reported and validated. Further validation and studies should be performed to determine its performance for the rapid identification of S. aureus from blood cultures. FilmArray BCID2 and Xpert MRSA/SA BC are very useful tools in routine microbiology laboratories for rapid discrimination of MRSA from MSSA.
Every approach has its characteristics (summarized in Table I and II). Each laboratory should consider some important factors such as turnaround time, panels of antibiotics offered, and hands-on time when searching for an appropriate method (Sze et al. 2021). Polymicrobial infections in BSI are not infrequent. It is essential to select an accurate method for such samples (Abat et al. 2015). Direct identification of S. aureus from blood rather than blood culture should be a direction of future development to maximize the benefits of rapid identification of S. aureus from blood cultures. Rapid identification methods combined with rapid AST determination are also necessary (Pliakos et al. 2018). Simple and rapid identification of S. aureus from blood culture plus phenotype AST will significantly impact the optimizing BSI management.
Characteristics and performance of different methods for the identification of S. aureus in the blood or blood cultures.
FISH – fluorescent in situ hybridization, PNA – peptide nucleic acid, MALDI-TOF MS – matrix-assisted laser desorption/ionisation-time of flight mass spectrometry, NA – not available
Comments on rapid and simple methods for the identification of S. aureus from the blood or blood cultures.
Assays
Automated
Personnel experience
Equipment requirement
Throughput
Cost
Comments
Hybrisep
yes
yes
proprietary equipment
low
moderate
+: rapid, sensitive and specific–: limited number of publications
T2Dx
yes
no
proprietary equipment
low
high
+: rapid, sensitive, and specific–: no resistance markers
BinaX Now S. aureus
no
no
no
low
low
+: rapid, sensitive and specific–: cross-reaction with S. lugdunensis
BinaX Now PBP2a
no
no
no
low
low
+: rapid, sensitive, and specific–: no identification
Gram staining
yes
yes
generic equipment
low
low
+: rapid, simple–: variable sensitivity and specificity
PNA FISH
no
yes
generic equipment
low
high
+: rapid, sensitive, and specific–: no resistance markers
QuickFISH
no
yes
generic equipment
low
high
+: rapid, sensitive, and specific–: no resistance markers
Accelerate PhenoTM system
yes
no
proprietary equipment
low
high
+: rapid, sensitive, and specific, with AST results–: low throughout
MALDI-TOF MS
no
yes
proprietary equipment
high
low
+: rapid, sensitive, and specific, cost-effective–: enrichment, not standardization
FilmArray BCID2
yes
no
proprietary equipment
low
high
+: rapid, sensitive, and specific, with resistance results–: low throughout
Xpert MRSA/SA BC
yes
no
proprietary equipment
low
high
+: rapid, sensitive, and specific, with resistance results–: expensive
FISH – fluorescent in situ hybridization, PNA – peptide nucleic acid, MALDI-TOF MS – matrix-assisted laser desorption/ionisation-time of flight mass spectrometry
Abat C, Chaudet H, Colson P, Rolain JM, Raoult D. Real-time microbiology laboratory surveillance system to detect abnormal events and emerging infections, Marseille, France. Emerg Infect Dis. 2015 Aug;21(8):1302–1310. https://doi.org/10.3201/eid2108.141419AbatCChaudetHColsonPRolainJMRaoultDReal-time microbiology laboratory surveillance system to detect abnormal events and emerging infections, Marseille, FranceEmerg Infect Dis2015Aug21813021310https://doi.org/10.3201/eid2108.14141910.3201/eid2108.141419451772726196165Search in Google Scholar
Asgeirsson H, Thalme A, Weiland O. Staphylococcus aureus bacteraemia and endocarditis – epidemiology and outcome: a review. Infect Dis (Lond). 2018 Mar;50(3):175–192. https://doi.org/10.1080/23744235.2017.1392039AsgeirssonHThalmeAWeilandOStaphylococcus aureus bacteraemia and endocarditis – epidemiology and outcome: a reviewInfect Dis (Lond)2018Mar503175192https://doi.org/10.1080/23744235.2017.139203910.1080/23744235.2017.139203929105519Search in Google Scholar
Baron EJ, Mix S, Moradi W. Clinical utility of an automated instrument for gram staining single slides. J Clin Microbiol. 2010 Jun; 48(6):2014–2015. https://doi.org/10.1128/jcm.02503-09BaronEJMixSMoradiWClinical utility of an automated instrument for gram staining single slidesJ Clin Microbiol2010Jun48620142015https://doi.org/10.1128/jcm.02503-0910.1128/JCM.02503-09288453120410348Search in Google Scholar
Belmekki M, Mammeri H, Hamdad F, Rousseau F, Canarelli B, Biendo M. Comparison of Xpert MRSA/SA nasal and MRSA/SA ELITe MGB assays for detection of the mecA gene with susceptibility testing methods for determination of methicillin resistance in Staphylococcus aureus isolates. J Clin Microbiol. 2013 Oct;51(10):3183–3191. https://doi.org/10.1128/jcm.00860-13BelmekkiMMammeriHHamdadFRousseauFCanarelliBBiendoMComparison of Xpert MRSA/SA nasal and MRSA/SA ELITe MGB assays for detection of the mecA gene with susceptibility testing methods for determination of methicillin resistance in Staphylococcus aureus isolatesJ Clin Microbiol2013Oct511031833191https://doi.org/10.1128/jcm.00860-1310.1128/JCM.00860-13381163023863569Search in Google Scholar
Boyanova L. Direct Gram staining and its various benefits in the diagnosis of bacterial infections. Postgrad Med. 2018 Jan;130(1):105–110. https://doi.org/10.1080/00325481.2018.1398049BoyanovaLDirect Gram staining and its various benefits in the diagnosis of bacterial infectionsPostgrad Med2018Jan1301105110https://doi.org/10.1080/00325481.2018.139804910.1080/00325481.2018.139804929091518Search in Google Scholar
Carretto E, Bardaro M, Russello G, Mirra M, Zuelli C, Barbarini D. Comparison of the Staphylococcus QuickFISH BC test with the tube coagulase test performed on positive blood cultures for evaluation and application in a clinical routine setting. J Clin Microbiol. 2013 Jan;51(1):131–135. https://doi.org/10.1128/jcm.02103-12CarrettoEBardaroMRusselloGMirraMZuelliCBarbariniDComparison of the Staphylococcus QuickFISH BC test with the tube coagulase test performed on positive blood cultures for evaluation and application in a clinical routine settingJ Clin Microbiol2013Jan511131135https://doi.org/10.1128/jcm.02103-1210.1128/JCM.02103-12353624523100336Search in Google Scholar
Cenci E, Paggi R, Socio GV, Bozza S, Camilloni B, Pietrella D, Mencacci A. Accelerate Pheno™ blood culture detection system: a literature review. Future Microbiol. 2020 Oct; 15:1595–1605. https://doi.org/10.2217/fmb-2020-0177CenciEPaggiRSocioGVBozzaSCamilloniBPietrellaDMencacciAAccelerate Pheno™ blood culture detection system: a literature reviewFuture Microbiol2020Oct1515951605https://doi.org/10.2217/fmb-2020-017710.2217/fmb-2020-017733215528Search in Google Scholar
Charnot-Katsikas A, Tesic V, Love N, Hill B, Bethel C, Boonlayangoor S, Beavis KG. Use of the Accelerate Pheno system for identification and antimicrobial susceptibility testing of pathogens in positive blood cultures and impact on time to results and workflow. J Clin Microbiol. 2017 Dec 26;56(1):e01166-17. https://doi.org/10.1128/jcm.01166-17Charnot-KatsikasATesicVLoveNHillBBethelCBoonlayangoorSBeavisKGUse of the Accelerate Pheno system for identification and antimicrobial susceptibility testing of pathogens in positive blood cultures and impact on time to results and workflowJ Clin Microbiol2017Dec 26561e0116617https://doi.org/10.1128/jcm.01166-1710.1128/JCM.01166-17574421329118168Search in Google Scholar
Christner M, Rohde H, Wolters M, Sobottka I, Wegscheider K, Aepfelbacher M. Rapid identification of bacteria from positive blood culture bottles by use of matrix-assisted laser desorption-ionization time of flight mass spectrometry fingerprinting. J Clin Microbiol. 2010 May;48(5):1584–1591. https://doi.org/10.1128/jcm.01831-09ChristnerMRohdeHWoltersMSobottkaIWegscheiderKAepfelbacherMRapid identification of bacteria from positive blood culture bottles by use of matrix-assisted laser desorption-ionization time of flight mass spectrometry fingerprintingJ Clin Microbiol2010May48515841591https://doi.org/10.1128/jcm.01831-0910.1128/JCM.01831-09286388820237093Search in Google Scholar
Cortazzo V, D’Inzeo T, Giordano L, Menchinelli G, Liotti FM, Fiori B, De Maio F, Luzzaro F, Sanguinetti M, Posteraro B, et al. Comparing BioFire FilmArray BCID2 and BCID panels for direct detection of bacterial pathogens and antimicrobial resistance genes from positive blood cultures. J Clin Microbiol. 2021 Mar 19;59(4): e03163-20. https://doi.org/10.1128/jcm.03163-20CortazzoVD’InzeoTGiordanoLMenchinelliGLiottiFMFioriBDe MaioFLuzzaroFSanguinettiMPosteraroBet alComparing BioFire FilmArray BCID2 and BCID panels for direct detection of bacterial pathogens and antimicrobial resistance genes from positive blood culturesJ Clin Microbiol2021Mar 19594e0316320https://doi.org/10.1128/jcm.03163-2010.1128/JCM.03163-20809273433472903Search in Google Scholar
Curtoni A, Cipriani R, Marra ES, Barbui AM, Cavallo R, Costa C. Rapid identification of microorganisms from positive blood culture by MALDI-TOF MS after short-term incubation on solid medium. Curr Microbiol. 2017 Jan;74(1):97–102. https://doi.org/10.1007/s00284-016-1161-2CurtoniACiprianiRMarraESBarbuiAMCavalloRCostaCRapid identification of microorganisms from positive blood culture by MALDI-TOF MS after short-term incubation on solid mediumCurr Microbiol2017Jan74197102https://doi.org/10.1007/s00284-016-1161-210.1007/s00284-016-1161-227858149Search in Google Scholar
De Angelis G, Posteraro B, De Carolis E, Menchinelli G, Franceschi F, Tumbarello M, De Pascale G, Spanu T, Sanguinetti M. T2Bacteria magnetic resonance assay for the rapid detection of ESKAPEc pathogens directly in whole blood. J Antimicrob Chem-other. 2018 Mar 1;73(suppl 4):iv20–iv26. https://doi.org/10.1093/jac/dky049DeAngelis GPosteraroBDeCarolis EMenchinelliGFranceschiFTumbarelloMDePascale GSpanuTSanguinettiMT2Bacteria magnetic resonance assay for the rapid detection of ESKAPEc pathogens directly in whole bloodJ Antimicrob Chem-other2018Mar 173suppl 4iv20–iv26https://doi.org/10.1093/jac/dky04910.1093/jac/dky04929608753Search in Google Scholar
Deck MK, Anderson ES, Buckner RJ, Colasante G, Coull JM, Crystal B, Della Latta P, Fuchs M, Fuller D, Harris W, et al. Multicenter evaluation of the Staphylococcus QuickFISH method for simultaneous identification of Staphylococcus aureus and coagulase-negative staphylococci directly from blood culture bottles in less than 30 minutes. J Clin Microbiol. 2012 Jun;50(6):1994–1998. https://doi.org/10.1128/jcm.00225-12DeckMKAndersonESBucknerRJColasanteGCoullJMCrystalBDellaLatta PFuchsMFullerDHarrisWet alMulticenter evaluation of the Staphylococcus QuickFISH method for simultaneous identification of Staphylococcus aureus and coagulase-negative staphylococci directly from blood culture bottles in less than 30 minutesJ Clin Microbiol2012Jun50619941998https://doi.org/10.1128/jcm.00225-1210.1128/JCM.00225-12337210222493336Search in Google Scholar
Dhiman N, Trienski TL, DiPersio LP, DiPersio JR. Evaluation of the BinaxNOW Staphylococcus aureus test for rapid identification of Gram-positive cocci from VersaTREK blood culture bottles. J Clin Microbiol. 2013 Sep;51(9):2939–2942. https://doi.org/10.1128/jcm.01087-13DhimanNTrienskiTLDiPersioLPDiPersioJREvaluation of the BinaxNOW Staphylococcus aureus test for rapid identification of Gram-positive cocci from VersaTREK blood culture bottlesJ Clin Microbiol2013Sep51929392942https://doi.org/10.1128/jcm.01087-1310.1128/JCM.01087-13375466423804393Search in Google Scholar
Drevinek P, Hurych J, Antuskova M, Tkadlec J, Berousek J, Prikrylova Z, Bures J, Vajter J, Soucek M, Masopust J, et al. Direct detection of ESKAPEc pathogens from whole blood using the T2Bacteria Panel allows early antimicrobial stewardship intervention in patients with sepsis. Microbiologyopen. 2021 Jun;10(3):e1210. https://doi.org/10.1002/mbo3.1210DrevinekPHurychJAntuskovaMTkadlecJBerousekJPrikrylovaZBuresJVajterJSoucekMMasopustJet alDirect detection of ESKAPEc pathogens from whole blood using the T2Bacteria Panel allows early antimicrobial stewardship intervention in patients with sepsisMicrobiologyopen2021Jun103e1210https://doi.org/10.1002/mbo3.121010.1002/mbo3.1210820928234180598Search in Google Scholar
Enomoto H, Inoue S, Matsuhisa A, Nishiguchi S. Diagnosis of spontaneous bacterial peritonitis and an in situ hybridization approach to detect an “unidentified” pathogen. Int J Hepatol. 2014; 2014:634617. https://doi.org/10.1155/2014/634617EnomotoHInoueSMatsuhisaANishiguchiSDiagnosis of spontaneous bacterial peritonitis and an in situ hybridization approach to detect an “unidentified” pathogenInt J Hepatol20142014634617https://doi.org/10.1155/2014/63461710.1155/2014/634617412357625132996Search in Google Scholar
Foster AG. Rapid Identification of microbes in positive blood cultures by use of the Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry system. J Clin Microbiol. 2013 Nov;51(11):3717–3719. https://doi.org/10.1128/jcm.01679-13FosterAGRapid Identification of microbes in positive blood cultures by use of the Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry systemJ Clin Microbiol2013Nov511137173719https://doi.org/10.1128/jcm.01679-1310.1128/JCM.01679-13388975623985920Search in Google Scholar
Gonzalez MD, Chao T, Pettengill MA. Modern blood culture: management decisions and method options. Clin Lab Med. 2020 Dec; 40(4):379–392. https://doi.org/10.1016/j.cll.2020.07.001GonzalezMDChaoTPettengillMAModern blood culture: management decisions and method optionsClin Lab Med2020Dec404379392https://doi.org/10.1016/j.cll.2020.07.00110.1016/j.cll.2020.07.001750151933121610Search in Google Scholar
González V, Padilla E, Giménez M, Vilaplana C, Pérez A, Fernández G, Quesada MD, Pallarés MA, Ausina V. Rapid diagnosis ofGonzálezVPadillaEGiménezMVilaplanaCPérezAFernándezGQuesadaMDPallarésMAAusinaVRapid diagnosis ofSearch in Google Scholar
Staphylococcus aureus bacteremia using S. aureus PNA FISH. Eur J Clin Microbiol Infect Dis. 2004 May;23(5):396–398. https://doi.org/10.1007/s10096-004-1112-xStaphylococcus aureus bacteremia using S aureus PNA FISHEur J Clin Microbiol Infect Dis2004May235396398https://doi.org/10.1007/s10096-004-1112-x10.1007/s10096-004-1112-x15112062Search in Google Scholar
Hadano Y, Isoda M, Ishibashi K, Kakuma T. Validation of blood culture gram staining for the detection of Staphylococcus aureus by the ‘oozing sign’ surrounding clustered gram-positive cocci: a prospective observational study. BMC Infect Dis. 2018 Sep 29;18(1):490. https://doi.org/10.1186/s12879-018-3412-2HadanoYIsodaMIshibashiKKakumaTValidation of blood culture gram staining for the detection of Staphylococcus aureus by the ‘oozing sign’ surrounding clustered gram-positive cocci: a prospective observational studyBMC Infect Dis2018Sep 29181490https://doi.org/10.1186/s12879-018-3412-210.1186/s12879-018-3412-2616287430268097Search in Google Scholar
Heraud S, Freydiere AM, Doleans-Jordheim A, Bes M, Tristan A, Vandenesch F, Laurent F, Dauwalder O. Direct identification of Staphylococcus aureus and determination of methicillin susceptibility from positive blood-culture bottles in a Bact/ALERT system using Binax Now S. aureus and PBP2a tests. Ann Lab Med. 2015 Jul; 35(4):454–457. https://doi.org/10.3343/alm.2015.35.4.454HeraudSFreydiereAMDoleans-JordheimABesMTristanAVandeneschFLaurentFDauwalderODirect identification of Staphylococcus aureus and determination of methicillin susceptibility from positive blood-culture bottles in a Bact/ALERT system using Binax Now Saureus and PBP2a tests. Ann Lab Med2015Jul354454457https://doi.org/10.3343/alm.2015.35.4.45410.3343/alm.2015.35.4.454444658626131419Search in Google Scholar
Holma T, Torvikoski J, Friberg N, Nevalainen A, Tarkka E, Antikainen J, Martelin JJ. Rapid molecular detection of pathogenic microorganisms and antimicrobial resistance markers in blood cultures: evaluation and utility of the next-generation FilmArray Blood Culture Identification 2 panel. Eur J Clin Microbiol Infect Dis. 2022 Mar;41(3):363–371. https://doi.org/10.1007/s10096-021-04314-2HolmaTTorvikoskiJFribergNNevalainenATarkkaEAntikainenJMartelinJJRapid molecular detection of pathogenic microorganisms and antimicrobial resistance markers in blood cultures: evaluation and utility of the next-generation FilmArray Blood Culture Identification 2 panelEur J Clin Microbiol Infect Dis2022Mar413363371https://doi.org/10.1007/s10096-021-04314-210.1007/s10096-021-04314-2883127434350523Search in Google Scholar
Hu YL, Hsueh SC, Ding GS, Chuang PC, Chen JM, Lu CY, Chang LY, Huang LM, Lee PI, Hsueh PR. Applicability of an in-house saponin-based extraction method in Bruker Biotyper matrix-assisted laser desorption/ionization time-of-flight mass spectrometry system for identifying bacterial and fungal species in positively flagged pediatric VersaTREK blood cultures. J Microbiol Immunol Infect. 2020 Dec;53(6):916–924. https://doi.org/10.1016/j.jmii.2020.01.004HuYLHsuehSCDingGSChuangPCChenJMLuCYChangLYHuangLMLeePIHsuehPRApplicability of an in-house saponin-based extraction method in Bruker Biotyper matrix-assisted laser desorption/ionization time-of-flight mass spectrometry system for identifying bacterial and fungal species in positively flagged pediatric VersaTREK blood culturesJ Microbiol Immunol Infect2020Dec536916924https://doi.org/10.1016/j.jmii.2020.01.00410.1016/j.jmii.2020.01.00432094073Search in Google Scholar
Jones BE, Ying J, Stevens V, Haroldsen C, He T, Nevers M, Christensen MA, Nelson RE, Stoddard GJ, Sauer BC, et al. Empirical anti-MRSA vs standard antibiotic therapy and risk of 30-day mortality in patients hospitalized for pneumonia. JAMA Intern Med. 2020 Apr 1;180(4):552–560. https://doi.org/10.1001/jamainternmed.2019.7495JonesBEYingJStevensVHaroldsenCHeTNeversMChristensenMANelsonREStoddardGJSauerBCet alEmpirical anti-MRSA vs standard antibiotic therapy and risk of 30-day mortality in patients hospitalized for pneumoniaJAMA Intern Med2020Apr 11804552560https://doi.org/10.1001/jamainternmed.2019.749510.1001/jamainternmed.2019.7495704281832065604Search in Google Scholar
Kern WV, Rieg S. Burden of bacterial bloodstream infection – a brief update on epidemiology and significance of multidrug-resistant pathogens. Clin Microbiol Infect. 2020 Feb; 26 (2):151–157. https://doi.org/10.1016/j.cmi.2019.10.031KernWVRiegSBurden of bacterial bloodstream infection – a brief update on epidemiology and significance of multidrug-resistant pathogensClin Microbiol Infect2020Feb262151157https://doi.org/10.1016/j.cmi.2019.10.03110.1016/j.cmi.2019.10.03131712069Search in Google Scholar
Kudo M, Matsuo Y, Nakasendo A, Inoue S, Goto H, Tsukiji J, Watanuki Y, Ueda A, Kaneko T, Ishigatsubo Y. Potential clinical benefit of the in situ hybridization method for the diagnosis of sepsis. J Infect Chemother. 2009 Feb;15(1):23–26. https://doi.org/10.1007/s10156-008-0655-7KudoMMatsuoYNakasendoAInoueSGotoHTsukijiJWatanukiYUedaAKanekoTIshigatsuboYPotential clinical benefit of the in situ hybridization method for the diagnosis of sepsisJ Infect Chemother2009Feb1512326https://doi.org/10.1007/s10156-008-0655-710.1007/s10156-008-0655-719280296Search in Google Scholar
Lin JF, Ge MC, Liu TP, Chang SC, Lu JJ. A simple method for rapid microbial identification from positive monomicrobial blood culture bottles through matrix-assisted laser desorption ionization time-of-flight mass spectrometry. J Microbiol Immunol Infect. 2018 Oct;51(5):659–665. https://doi.org/10.1016/j.jmii.2017.03.005LinJFGeMCLiuTPChangSCLuJJA simple method for rapid microbial identification from positive monomicrobial blood culture bottles through matrix-assisted laser desorption ionization time-of-flight mass spectrometryJ Microbiol Immunol Infect2018Oct515659665https://doi.org/10.1016/j.jmii.2017.03.00510.1016/j.jmii.2017.03.00528711436Search in Google Scholar
Liu X, Su T, Hsu YS, Yu H, Yang HS, Jiang L, Zhao Z. Rapid identification and discrimination of methicillin-resistant Staphylococcus aureus strains via matrix-assisted laser desorption/ ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 2021 Jan 30;35(2):e8972. https://doi.org/10.1002/rcm.8972LiuXSuTHsuYSYuHYangHSJiangLZhaoZRapid identification and discrimination of methicillin-resistant Staphylococcus aureus strains via matrix-assisted laser desorption/ ionization time-of-flight mass spectrometryRapid Commun Mass Spectrom2021Jan 30352e8972https://doi.org/10.1002/rcm.897210.1002/rcm.897233053243Search in Google Scholar
Lutgring JD, Bittencourt C, McElvania TeKippe E, Cavuoti D, Hollaway R, Burd EM. Evaluation of the Accelerate Pheno system: results from two academic medical centers. J Clin Microbiol. 2018 Mar 26;56(4):e01672-17. https://doi.org/10.1128/jcm.01672-17LutgringJDBittencourtCMcElvaniaTeKippe ECavuotiDHollawayRBurdEMEvaluation of the Accelerate Pheno system: results from two academic medical centersJ Clin Microbiol2018Mar 26564e0167217https://doi.org/10.1128/jcm.01672-1710.1128/JCM.01672-17586984929386262Search in Google Scholar
Marschal M, Bachmaier J, Autenrieth I, Oberhettinger P, Willmann M, Peter S. Evaluation of the Accelerate Pheno system for fast identification and antimicrobial susceptibility testing from positive blood cultures in bloodstream infections caused by Gram-negative pathogens. J Clin Microbiol. 2017 Jul;55(7):2116–2126. https://doi.org/10.1128/jcm.00181-17MarschalMBachmaierJAutenriethIOberhettingerPWillmannMPeterSEvaluation of the Accelerate Pheno system for fast identification and antimicrobial susceptibility testing from positive blood cultures in bloodstream infections caused by Gram-negative pathogensJ Clin Microbiol2017Jul55721162126https://doi.org/10.1128/jcm.00181-1710.1128/JCM.00181-17548391328446572Search in Google Scholar
Mather CA, Werth BJ, Sivagnanam S, SenGupta DJ, Butler-Wu SM. Rapid detection of vancomycin-intermediate Staphylococcus aureus by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol. 2016 Apr;54(4):883–890. https://doi.org/10.1128/jcm.02428-15MatherCAWerthBJSivagnanamSSenGuptaDJButler-WuSMRapid detection of vancomycin-intermediate Staphylococcus aureus by matrix-assisted laser desorption ionization-time of flight mass spectrometryJ Clin Microbiol2016Apr544883890https://doi.org/10.1128/jcm.02428-1510.1128/JCM.02428-15480991626763961Search in Google Scholar
McHugh MP, Parcell BJ, MacKenzie FM, Templeton KE; Scottish Microbiology and Virology Network Smvn Molecular Diagnostics Evaluation Group. Rapid molecular testing for Staphylococcus aureus bacteraemia improves clinical management. J Med Microbiol. 2020 Apr;69(4):552–557. https://doi.org/10.1099/jmm.0.001171McHughMPParcellBJMacKenzieFMTempletonKEScottish Microbiology and Virology Network Smvn Molecular Diagnostics Evaluation Group. Rapid molecular testing for Staphylococcus aureus bacteraemia improves clinical managementJ Med Microbiol2020Apr694552557https://doi.org/10.1099/jmm.0.00117110.1099/jmm.0.00117132141812Search in Google Scholar
Mitchell DH, Howden BP. Diagnosis and management of Staphylococcus aureus bacteraemia. Intern Med J. 2005 Dec;35 Suppl 2:S17–S24. https://doi.org/10.1111/j.1444-0903.2005.00977.xMitchellDHHowdenBPDiagnosis and management of Staphylococcus aureus bacteraemiaIntern Med J2005Dec;35 Suppl2S17S24https://doi.org/10.1111/j.1444-0903.2005.00977.x10.1111/j.1444-0903.2005.00977.x16271058Search in Google Scholar
Mitteregger D, Barousch W, Nehr M, Kundi M, Zeitlinger M, Makristathis A, Hirschl AM. Neutralization of antimicrobial substances in new BacT/Alert FA and FN Plus blood culture bottles. J Clin Microbiol. 2013 May;51(5):1534–1540. https://doi.org/10.1128/jcm.00103-13MittereggerDBarouschWNehrMKundiMZeitlingerMMakristathisAHirschlAMNeutralization of antimicrobial substances in new BacT/Alert FA and FN Plus blood culture bottlesJ Clin Microbiol2013May51515341540https://doi.org/10.1128/jcm.00103-1310.1128/JCM.00103-13364790023486710Search in Google Scholar
Murdoch DR, Greenlees RL. Rapid identification of Staphylococcus aureus from BacT/ ALERT blood culture bottles by direct Gram stain characteristics. J Clin Pathol. 2004 Feb;57(2):199–201. https://doi.org/10.1136/jcp.2003.10538MurdochDRGreenleesRLRapid identification of Staphylococcus aureus from BacT/ ALERT blood culture bottles by direct Gram stain characteristicsJ Clin Pathol2004Feb572199201https://doi.org/10.1136/jcp.2003.1053810.1136/jcp.2003.10538177020214747451Search in Google Scholar
Neely LA, Audeh M, Phung NA, Min M, Suchocki A, Plourde D, Blanco M, Demas V, Skewis LR, Anagnostou T, et al. T2 magnetic resonance enables nanoparticle-mediated rapid detection of candidemia in whole blood. Sci Transl Med. 2013 Apr 24;5(182):182ra54. https://doi.org/10.1126/scitranslmed.3005377NeelyLAAudehMPhungNAMinMSuchockiAPlourdeDBlancoMDemasVSkewisLRAnagnostouTet alT2 magnetic resonance enables nanoparticle-mediated rapid detection of candidemia in whole bloodSci Transl Med2013Apr 245182182ra54https://doi.org/10.1126/scitranslmed.300537710.1126/scitranslmed.300537723616121Search in Google Scholar
Nguyen MH, Clancy CJ, Pasculle AW, Pappas PG, Alangaden G, Pankey GA, Schmitt BH, Rasool A, Weinstein MP, Widen R, et al. Performance of the T2Bacteria panel for diagnosing bloodstream infections: a diagnostic accuracy study. Ann Intern Med. 2019 Jun 18;170(12):845–852. https://doi.org/10.7326/m18-2772NguyenMHClancyCJPasculleAWPappasPGAlangadenGPankeyGASchmittBHRasoolAWeinsteinMPWidenRet alPerformance of the T2Bacteria panel for diagnosing bloodstream infections: a diagnostic accuracy studyAnn Intern Med2019Jun 1817012845852https://doi.org/10.7326/m18-277210.7326/M18-277231083728Search in Google Scholar
Oliveira K, Brecher SM, Durbin A, Shapiro DS, Schwartz DR, De Girolami PC, Dakos J, Procop GW, Wilson D, Hanna CS, et al. Direct identification of Staphylococcus aureus from positive blood culture bottles. J Clin Microbiol. 2003 Feb;41(2):889–891. https://doi.org/10.1128/jcm.41.2.889-891.2003OliveiraKBrecherSMDurbinAShapiroDSSchwartzDRDe GirolamiPCDakosJProcopGWWilsonDHannaCSet alDirect identification of Staphylococcus aureus from positive blood culture bottlesJ Clin Microbiol2003Feb412889891https://doi.org/10.1128/jcm.41.2.889-891.200310.1128/JCM.41.2.889-891.200314967012574309Search in Google Scholar
O’Toole GA. Classic spotlight: how the Gram stain works. J Bacteriol. 2016 Nov 4;198(23):3128. https://doi.org/10.1128/jb.00726-16O’TooleGAClassic spotlight: how the Gram stain worksJ Bacteriol2016Nov 4198233128https://doi.org/10.1128/jb.00726-1610.1128/JB.00726-16510589227815540Search in Google Scholar
Paolucci M, Landini MP, Sambri V. Conventional and molecular techniques for the early diagnosis of bacteraemia. Int J Antimicrob Agents. 2010 Dec;36(Suppl2):S6–S16. https://doi.org/10.1016/j.ijantimicag.2010.11.010PaolucciMLandiniMPSambriVConventional and molecular techniques for the early diagnosis of bacteraemiaInt J Antimicrob Agents2010Dec36Suppl2S6S16https://doi.org/10.1016/j.ijantimicag.2010.11.01010.1016/j.ijantimicag.2010.11.01021129933Search in Google Scholar
Parkes-Smith J, Bergh H, Harris PNA. Assessing the performance of the Cepheid Xpert in identifying and differentiating methicillin-susceptible Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from blood culture bottles. Pathology. 2022 Sep 5:S0031-3025(22)00232-X. https://doi.org/10.1016/j.pathol.2022.07.006Parkes-SmithJBerghHHarrisPNAAssessing the performance of the Cepheid Xpert in identifying and differentiating methicillin-susceptible Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from blood culture bottlesPathology2022Sep5S00313025(22)00232-Xhttps://doi.org/10.1016/j.pathol.2022.07.00610.1016/j.pathol.2022.07.00636130845Search in Google Scholar
Peker N, Couto N, Sinha B, Rossen JW. Diagnosis of bloodstream infections from positive blood cultures and directly from blood samples: recent developments in molecular approaches. Clin Microbiol Infect. 2018 Sep;24(9):944–955. https://doi.org/10.1016/j.cmi.2018.05.007PekerNCoutoNSinhaBRossenJWDiagnosis of bloodstream infections from positive blood cultures and directly from blood samples: recent developments in molecular approachesClin Microbiol Infect2018Sep249944955https://doi.org/10.1016/j.cmi.2018.05.00710.1016/j.cmi.2018.05.00729787889Search in Google Scholar
Pliakos EE, Andreatos N, Shehadeh F, Ziakas PD, Mylonakis E. The cost-effectiveness of rapid diagnostic testing for the diagnosis of bloodstream infections with or without antimicrobial stewardship. Clin Microbiol Rev. 2018 May 30;31(3):e00095-17. https://doi.org/10.1128/cmr.00095-17PliakosEEAndreatosNShehadehFZiakasPDMylonakisEThe cost-effectiveness of rapid diagnostic testing for the diagnosis of bloodstream infections with or without antimicrobial stewardshipClin Microbiol Rev2018May 30313e0009517https://doi.org/10.1128/cmr.00095-1710.1128/CMR.00095-17605684429848775Search in Google Scholar
Ponderand L, Pavese P, Maubon D, Giraudon E, Girard T, Landelle C, Maurin M, Caspar Y. Evaluation of Rapid Sepsityper® protocol and specific MBT-Sepsityper module (Bruker Daltonics) for the rapid diagnosis of bacteremia and fungemia by MALDI-TOF-MS. Ann Clin Microbiol Antimicrob. 2020 Dec 9;19(1):60. https://doi.org/10.1186/s12941-020-00403-wPonderandLPavesePMaubonDGiraudonEGirardTLandelleCMaurinMCasparYEvaluation of Rapid Sepsityper® protocol and specific MBT-Sepsityper module (Bruker Daltonics) for the rapid diagnosis of bacteremia and fungemia by MALDI-TOF-MSAnn Clin Microbiol Antimicrob2020Dec 919160https://doi.org/10.1186/s12941-020-00403-w10.1186/s12941-020-00403-w772719633298064Search in Google Scholar
Pritchard L, Baker C, Leggett J, Sehdev P, Brown A, Bayley KB. Increasing vancomycin serum trough concentrations and incidence of nephrotoxicity. Am J Med. 2010 Dec; 123(12):1143–1149. https://doi.org/10.1016/j.amjmed.2010.07.025PritchardLBakerCLeggettJSehdevPBrownABayleyKBIncreasing vancomycin serum trough concentrations and incidence of nephrotoxicityAm J Med2010Dec1231211431149https://doi.org/10.1016/j.amjmed.2010.07.02510.1016/j.amjmed.2010.07.02521183005Search in Google Scholar
Qian Q, Eichelberger K, Kirby JE. Rapid identification of Staphylococcus aureus directly from Bactec blood culture broth by the BinaxNOW S. aureus test. J Clin Microbiol. 2014 Jan; 52(1):319–320. https://doi.org/10.1128/jcm.02291-13QianQEichelbergerKKirbyJERapid identification of Staphylococcus aureus directly from Bactec blood culture broth by the BinaxNOW Saureus test. J Clin Microbiol2014Jan521319320https://doi.org/10.1128/jcm.02291-1310.1128/JCM.02291-13391147124153135Search in Google Scholar
Reddy K, Whitelaw A. Can the Xpert MRSA/SA BC assay be used as an antimicrobial stewardship tool? A prospective assay validation and descriptive impact assessment study in a South African setting. BMC Infect Dis. 2021 Feb 15;21(1):177. https://doi.org/10.1186/s12879-021-05857-7ReddyKWhitelawACan the Xpert MRSA/SA BC assay be used as an antimicrobial stewardship tool? A prospective assay validation and descriptive impact assessment study in a South African settingBMC Infect Dis2021Feb 15211177https://doi.org/10.1186/s12879-021-05857-710.1186/s12879-021-05857-7788537333588782Search in Google Scholar
Roh KH, Kim JY, Kim HN, Lee HJ, Sohn JW, Kim MJ, Cho Y, Kim YK, Lee CK. Evaluation of BACTEC Plus aerobic and anaerobic blood culture bottles and BacT/Alert FAN aerobic and anaerobic blood culture bottles for the detection of bacteremia in ICU patients. Diagn Microbiol Infect Dis. 2012 Jul;73(3):239–242. https://doi.org/10.1016/j.diagmicrobio.2012.03.022RohKHKimJYKimHNLeeHJSohnJWKimMJChoYKimYKLeeCKEvaluation of BACTEC Plus aerobic and anaerobic blood culture bottles and BacT/Alert FAN aerobic and anaerobic blood culture bottles for the detection of bacteremia in ICU patientsDiagn Microbiol Infect Dis2012Jul733239242https://doi.org/10.1016/j.diagmicrobio.2012.03.02210.1016/j.diagmicrobio.2012.03.02222541787Search in Google Scholar
Shimada J, Hayashi I, Inamatsu T, Ishida M, Iwai S, Kamidono S, Kurosawa H, Masaoka T, Matsumoto F, Monden M, et al. Clinical trial of in-situ hybridization method for the rapid diagnosis of sepsis. J Infect Chemother. 1999 Mar;5(1):21–31. https://doi.org/10.1007/s101560050004ShimadaJHayashiIInamatsuTIshidaMIwaiSKamidonoSKurosawaHMasaokaTMatsumotoFMondenMet alClinical trial of in-situ hybridization method for the rapid diagnosis of sepsisJ Infect Chemother1999Mar512131https://doi.org/10.1007/s10156005000410.1007/s10156005000411810486Search in Google Scholar
Smith KP, Kang AD, Kirby JE. Automated interpretation of blood culture Gram stains by use of a deep convolutional neural network. J Clin Microbiol. 2018 Feb 22;56(3):e01521-17. https://doi.org/10.1128/jcm.01521-17SmithKPKangADKirbyJEAutomated interpretation of blood culture Gram stains by use of a deep convolutional neural networkJ Clin Microbiol2018Feb 22563e0152117https://doi.org/10.1128/jcm.01521-1710.1128/JCM.01521-17582403029187563Search in Google Scholar
Srisrattakarn A, Panpru P, Tippayawat P, Chanawong A, Tavichakorntrakool R, Daduang J, Wonglakorn L, Lulitanond A. Rapid detection of methicillin-resistant Staphylococcus aureus in positive blood-cultures by recombinase polymerase amplification combined with lateral flow strip. PLoS One. 2022 Jun 30;17(6):e0270686. https://doi.org/10.1371/journal.pone.0270686SrisrattakarnAPanpruPTippayawatPChanawongATavichakorntrakoolRDaduangJWonglakornLLulitanondARapid detection of methicillin-resistant Staphylococcus aureus in positive blood-cultures by recombinase polymerase amplification combined with lateral flow stripPLoS One2022Jun 30176e0270686https://doi.org/10.1371/journal.pone.027068610.1371/journal.pone.0270686924619135771885Search in Google Scholar
Sze DTT, Lau CCY, Chan TM, Ma ESK, Tang BSF. Comparison of novel rapid diagnostic of blood culture identification and antimicrobial susceptibility testing by Accelerate Pheno system and Bio-Fire FilmArray Blood Culture Identification and BioFire FilmArray Blood Culture Identification 2 panels. BMC Microbiol. 2021 Dec 18; 21(1):350. https://doi.org/10.1186/s12866-021-02403-ySzeDTTLauCCYChanTMMaESKTangBSFComparison of novel rapid diagnostic of blood culture identification and antimicrobial susceptibility testing by Accelerate Pheno system and Bio-Fire FilmArray Blood Culture Identification and BioFire FilmArray Blood Culture Identification 2 panelsBMC Microbiol2021Dec 18211350https://doi.org/10.1186/s12866-021-02403-y10.1186/s12866-021-02403-y868425634922463Search in Google Scholar
Tsuchida S, Murata S, Miyabe A, Satoh M, Takiwaki M, Matsushita K, Nomura F. An improved in-house lysis-filtration protocol for bacterial identification from positive blood culture bottles with high identification rates by MALDI-TOF MS. J Microbiol Methods. 2018 May; 148:40–45. https://doi.org/10.1016/j.mimet.2018.03.014TsuchidaSMurataSMiyabeASatohMTakiwakiMMatsushitaKNomuraFAn improved in-house lysis-filtration protocol for bacterial identification from positive blood culture bottles with high identification rates by MALDI-TOF MSJ Microbiol Methods2018May1484045https://doi.org/10.1016/j.mimet.2018.03.01410.1016/j.mimet.2018.03.01429608928Search in Google Scholar
Tsuzuki S, Yu J, Matsunaga N, Ohmagari N. Length of stay, hospitalisation costs and in-hospital mortality of methicillin-susceptible and methicillin-resistant Staphylococcus aureus bacteremia in Japan. Public Health. 2021 Sep;198:292–296. https://doi.org/10.1016/j.puhe.2021.07.046TsuzukiSYuJMatsunagaNOhmagariNLength of stay, hospitalisation costs and in-hospital mortality of methicillin-susceptible and methicillin-resistant Staphylococcus aureus bacteremia in JapanPublic Health2021Sep198292296https://doi.org/10.1016/j.puhe.2021.07.04610.1016/j.puhe.2021.07.04634507134Search in Google Scholar
Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichen-berger EM, Shah PP, Carugati M, Holland TL, Fowler VG Jr. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol. 2019 Apr; 17(4):203–218. https://doi.org/10.1038/s41579-018-0147-4TurnerNASharma-KuinkelBKMaskarinecSAEichen-bergerEMShahPPCarugatiMHollandTLFowlerVGJrMethicillin-resistant Staphylococcus aureus: an overview of basic and clinical researchNat Rev Microbiol2019Apr174203218https://doi.org/10.1038/s41579-018-0147-410.1038/s41579-018-0147-4693988930737488Search in Google Scholar
Weaver AJ, Brandenburg KS, Sanjar F, Wells AR, Peacock TJ, Leung KP. Clinical utility of PNA-FISH for burn wound diagnostics: a noninvasive, culture-independent technique for rapid identification of pathogenic organisms in burn wounds. J Burn Care Res. 2019 Jun 21;40 (4):464–470. https://doi.org/10.1093/jbcr/irz047WeaverAJBrandenburgKSSanjarFWellsARPeacockTJLeungKPClinical utility of PNA-FISH for burn wound diagnostics: a noninvasive, culture-independent technique for rapid identification of pathogenic organisms in burn woundsJ Burn Care Res2019Jun 21404464470https://doi.org/10.1093/jbcr/irz04710.1093/jbcr/irz047658740630893424Search in Google Scholar
Wu KY, Yang TX. A novel improved Gram staining method based on the capillary tube. Pol J Microbiol. 2020 Dec;69(4):503–508. https://doi.org/10.33073/pjm-2020-043WuKYYangTXA novel improved Gram staining method based on the capillary tubePol J Microbiol2020Dec694503508https://doi.org/10.33073/pjm-2020-04310.33073/pjm-2020-043781236033574878Search in Google Scholar
Zengin Canalp H, Bayraktar B. Direct rapid identification from positive blood cultures by MALDI-TOF MS: specific focus on turnaround times. Microbiol Spectr. 2021 Dec 22;9(3):e0110321. https://doi.org/10.1128/spectrum.01103-21ZenginCanalp HBayraktarBDirect rapid identification from positive blood cultures by MALDI-TOF MS: specific focus on turnaround timesMicrobiol Spectr2021Dec 2293e0110321https://doi.org/10.1128/spectrum.01103-2110.1128/spectrum.01103-21867291134908465Search in Google Scholar
