Susceptibility Testing by Volatile Organic Compound Detection Direct from Positive Blood Cultures: A Proof-of-Principle Laboratory Study

Overview

Journal Antibiotics (Basel)

Specialty Pharmacology

Date 2022 Jun 24

PMID 35740111

Authors

Sacha Danielle Kuil

Soemeja Hidad

Caroline Schneeberger

Pragya Singh

Paul Rhodes

Menno Douwe de Jong

Caroline Elisabeth Visser

Affiliations

Soon will be listed here.

Abstract

Background: Bacteria produce volatile organic compounds (VOCs) during growth, which can be detected by colorimetric sensor arrays (CSAs). The SpecifAST system (Specific Diagnostics) employs this technique to enable antibiotic susceptibility testing (AST) directly from blood cultures without prior subculture of isolates. The aim of this study was to compare the SpecifAST AST results and analysis time to the VITEK2 (bioMérieux) system.

Methods: In a 12-month single site prospective study, remnants of clinical positive monomicrobial blood cultures were combined with a series of antibiotic concentrations. Volatile emission was monitored at 37 °C via CSAs. Minimal Inhibitory Concentrations (MICs) of seven antimicrobial agents for , and spp. were compared to VITEK2 AST results. MICs were interpreted according to EUCAST clinical breakpoints. Performance was assessed by calculating agreement and discrepancy rates.

Results: In total, 96 positive blood cultures containing , and spp. were tested (269 bug-drug combinations). The categorical agreement of the SpecifAST system compared to the VITEK2 system was 100% and 91% for Gram-negatives and Gram-positives, respectively. Errors among Gram-positives were from coagulase-negative staphylococci. Overall results were available in 3.1 h (±0.9 h) after growth detection without the need for subculture steps.

Conclusion: The AST results based on VOC detection are promising and warrant further evaluation in studies with a larger sample of bacterial species and antimicrobials.

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References

Ratiu I, Ligor T, Bocos-Bintintan V, Buszewski B . Mass spectrometric techniques for the analysis of volatile organic compounds emitted from bacteria. Bioanalysis. 2017; 9(14):1069-1092. DOI: 10.4155/bio-2017-0051. View

Weisskopf L, Schulz S, Garbeva P . Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions. Nat Rev Microbiol. 2021; 19(6):391-404. DOI: 10.1038/s41579-020-00508-1. View

Romero-Gomez M, Gomez-Gil R, Pano-Pardo J, Mingorance J . Identification and susceptibility testing of microorganism by direct inoculation from positive blood culture bottles by combining MALDI-TOF and Vitek-2 Compact is rapid and effective. J Infect. 2012; 65(6):513-20. DOI: 10.1016/j.jinf.2012.08.013. View

Carey J, Suslick K, Hulkower K, Imlay J, Imlay K, Ingison C . Rapid identification of bacteria with a disposable colorimetric sensing array. J Am Chem Soc. 2011; 133(19):7571-6. PMC: 3097425. DOI: 10.1021/ja201634d. View

Bard J, Lee F . Why Can't We Just Use PCR? The Role of Genotypic versus Phenotypic Testing for Antimicrobial Resistance Testing. Clin Microbiol Newsl. 2020; 40(11):87-95. PMC: 7132721. DOI: 10.1016/j.clinmicnews.2018.05.003. View

Kangas M, Burks R, Atwater J, Lukowicz R, Williams P, Holmes A . Colorimetric Sensor Arrays for the Detection and Identification of Chemical Weapons and Explosives. Crit Rev Anal Chem. 2016; 47(2):138-153. PMC: 5351797. DOI: 10.1080/10408347.2016.1233805. View

Dubourg G, Lamy B, Ruimy R . Rapid phenotypic methods to improve the diagnosis of bacterial bloodstream infections: meeting the challenge to reduce the time to result. Clin Microbiol Infect. 2018; 24(9):935-943. DOI: 10.1016/j.cmi.2018.03.031. View

van Belkum A, Burnham C, Rossen J, Mallard F, Rochas O, Dunne Jr W . Innovative and rapid antimicrobial susceptibility testing systems. Nat Rev Microbiol. 2020; 18(5):299-311. DOI: 10.1038/s41579-020-0327-x. View

Maugeri G, Lychko I, Sobral R, Roque A . Identification and Antibiotic-Susceptibility Profiling of Infectious Bacterial Agents: A Review of Current and Future Trends. Biotechnol J. 2018; 14(1):e1700750. PMC: 6330097. DOI: 10.1002/biot.201700750. View

10.

Machen A, Drake T, Wang Y . Same day identification and full panel antimicrobial susceptibility testing of bacteria from positive blood culture bottles made possible by a combined lysis-filtration method with MALDI-TOF VITEK mass spectrometry and the VITEK2 system. PLoS One. 2014; 9(2):e87870. PMC: 3925102. DOI: 10.1371/journal.pone.0087870. View

11.

Schulz-Bohm K, Martin-Sanchez L, Garbeva P . Microbial Volatiles: Small Molecules with an Important Role in Intra- and Inter-Kingdom Interactions. Front Microbiol. 2018; 8:2484. PMC: 5733050. DOI: 10.3389/fmicb.2017.02484. View

12.

Archer G, Scott J . Conjugative transfer genes in staphylococcal isolates from the United States. Antimicrob Agents Chemother. 1991; 35(12):2500-4. PMC: 245420. DOI: 10.1128/AAC.35.12.2500. View

13.

Kunze-Szikszay N, Euler M, Kuhns M, Thiess M, Gross U, Quintel M . Headspace analyses using multi-capillary column-ion mobility spectrometry allow rapid pathogen differentiation in hospital-acquired pneumonia relevant bacteria. BMC Microbiol. 2021; 21(1):69. PMC: 7916313. DOI: 10.1186/s12866-021-02102-8. View

14.

Jorgensen J, Ferraro M . Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin Infect Dis. 2009; 49(11):1749-55. DOI: 10.1086/647952. View

15.

Robinson E, Stilwell A, Attai A, Donohue L, Shah M, Hill B . Implementation of a Rapid Phenotypic Susceptibility Platform for Gram-Negative Bloodstream Infections With Paired Antimicrobial Stewardship Intervention: Is the Juice Worth the Squeeze?. Clin Infect Dis. 2021; 73(5):783-792. PMC: 8423462. DOI: 10.1093/cid/ciab126. View

16.

Morris C, Simner P . Tailoring Antimicrobial Susceptibility Testing to Individual Species of Coagulase-Negative Staphylococci: Next Up, Staphylococcus epidermidis. J Clin Microbiol. 2019; 57(12). PMC: 6879275. DOI: 10.1128/JCM.01391-19. View

17.

Smart A, de Lacy Costello B, White P, Avison M, Batty C, Turner C . Sniffing out resistance - Rapid identification of urinary tract infection-causing bacteria and their antibiotic susceptibility using volatile metabolite profiles. J Pharm Biomed Anal. 2019; 167:59-65. DOI: 10.1016/j.jpba.2019.01.044. View

18.

Charnot-Katsikas A, Tesic V, Love N, Hill B, Bethel C, Boonlayangoor S . 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; 56(1). PMC: 5744213. DOI: 10.1128/JCM.01166-17. View

19.

Boots A, Smolinska A, van Berkel J, Fijten R, Stobberingh E, Boumans M . Identification of microorganisms based on headspace analysis of volatile organic compounds by gas chromatography-mass spectrometry. J Breath Res. 2014; 8(2):027106. DOI: 10.1088/1752-7155/8/2/027106. View

20.

Steppert I, Schonfelder J, Schultz C, Kuhlmeier D . Rapid in vitro differentiation of bacteria by ion mobility spectrometry. Appl Microbiol Biotechnol. 2021; 105(10):4297-4307. PMC: 8140968. DOI: 10.1007/s00253-021-11315-w. View