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Drug-Resistant Staphylococcus aureus Strains Reveal Distinct Biochemical Features with Raman Microspectroscopy
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    Drug-Resistant Staphylococcus aureus Strains Reveal Distinct Biochemical Features with Raman Microspectroscopy
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    • Oscar D. Ayala
      Oscar D. Ayala
      Biophotonics Center, Vanderbilt University, 410 24th Avenue South, Nashville, Tennessee 37235, United States
      Department of Biomedical Engineering, Vanderbilt University, 5824 Stevenson Center, Nashville, Tennessee 37232, United States
    • Catherine A. Wakeman
      Catherine A. Wakeman
      Department of Biological Sciences, Texas Tech University, 2901 Main Street, Lubbock, Texas 79409, United States
    • Isaac J. Pence
      Isaac J. Pence
      Biophotonics Center, Vanderbilt University, 410 24th Avenue South, Nashville, Tennessee 37235, United States
      Department of Biomedical Engineering, Vanderbilt University, 5824 Stevenson Center, Nashville, Tennessee 37232, United States
    • Jennifer A. Gaddy
      Jennifer A. Gaddy
      Department of Medicine, Division of Infectious Diseases, Vanderbilt University Medical Center, 1161 21st Avenue South, Medical Center North, Nashville, Tennessee 37232, United States
      Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, 1161 21st Avenue South, Medical Center North, Nashville, Tennessee 37232, United States
      Tennessee Valley Healthcare Systems, Department of Veterans Affairs, 1310 24th Avenue South, Nashville, Tennessee 37212, United States
    • James C. Slaughter
      James C. Slaughter
      Department of Biostatistics, Vanderbilt University School of Medicine, 2525 West End Avenue, Suite 11000, Nashville, Tennessee 37203, United States
    • Eric P. Skaar
      Eric P. Skaar
      Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, 1161 21st Avenue South, Medical Center North, Nashville, Tennessee 37232, United States
    • Anita Mahadevan-Jansen*
      Anita Mahadevan-Jansen
      Biophotonics Center, Vanderbilt University, 410 24th Avenue South, Nashville, Tennessee 37235, United States
      Department of Biomedical Engineering, Vanderbilt University, 5824 Stevenson Center, Nashville, Tennessee 37232, United States
      *E-mail: [email protected]
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    ACS Infectious Diseases

    Cite this: ACS Infect. Dis. 2018, 4, 8, 1197–1210
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    https://doi.org/10.1021/acsinfecdis.8b00029
    Published May 30, 2018
    Copyright © 2018 American Chemical Society

    Abstract

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    Staphylococcus aureus (S. aureus) is a leading cause of hospital-acquired infections, such as bacteremia, pneumonia, and endocarditis. Treatment of these infections can be challenging since strains of S. aureus, such as methicillin-resistant S. aureus (MRSA), have evolved resistance to antimicrobials. Current methods to identify infectious agents in hospital environments often rely on time-consuming, multistep culturing techniques to distinguish problematic strains (i.e., antimicrobial resistant variants) of a particular bacterial species. Therefore, a need exists for a rapid, label-free technique to identify drug-resistant bacterial strains to guide proper antibiotic treatment. Here, our findings demonstrate the ability to characterize and identify microbes at the subspecies level using Raman microspectroscopy, which probes the vibrational modes of molecules to provide a biochemical “fingerprint”. This technique can distinguish between different isolates of species such as Streptococcus agalactiae and S. aureus. To determine the ability of this analytical approach to detect drug-resistant bacteria, isogenic variants of S. aureus including the comparison of strains lacking or expressing antibiotic resistance determinants were evaluated. Spectral variations observed may be associated with biochemical components such as amino acids, carotenoids, and lipids. Mutants lacking carotenoid production were distinguished from wild-type S. aureus and other strain variants. Furthermore, spectral biomarkers of S. aureus isogenic bacterial strains were identified. These results demonstrate the feasibility of Raman microspectroscopy for distinguishing between various genetically distinct forms of a single bacterial species in situ. This is important for detecting antibiotic-resistant strains of bacteria and indicates the potential for future identification of other multidrug resistant pathogens with this technique.

    Copyright © 2018 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsinfecdis.8b00029.

    • A summary of S. aureus strains evaluated using Raman microspectroscopy; the differences in S. aureus pigmentation for the strains studied (PDF)

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    38. Chi-Sing Ho, Neal Jean, Catherine A. Hogan, Lena Blackmon, Stefanie S. Jeffrey, Mark Holodniy, Niaz Banaei, Amr A. E. Saleh, Stefano Ermon, Jennifer Dionne. Rapid identification of pathogenic bacteria using Raman spectroscopy and deep learning. Nature Communications 2019, 10 (1) https://doi.org/10.1038/s41467-019-12898-9
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    ACS Infectious Diseases

    Cite this: ACS Infect. Dis. 2018, 4, 8, 1197–1210
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsinfecdis.8b00029
    Published May 30, 2018
    Copyright © 2018 American Chemical Society

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