Abstract

Rapid identification of bacterial species is crucial in medicine and food hygiene. In order to achieve rapid and label-free identification of bacterial species at the single bacterium level, we propose and experimentally demonstrate an optical method based on Fourier transform light scattering (FTLS) measurements and statistical classification. For individual rod-shaped bacteria belonging to four bacterial species (Listeria monocytogenes, Escherichia coli, Lactobacillus casei, and Bacillus subtilis), two-dimensional angle-resolved light scattering maps are precisely measured using FTLS technique. The scattering maps are then systematically analyzed, employing statistical classification in order to extract the unique fingerprint patterns for each species, so that a new unidentified bacterium can be identified by a single light scattering measurement. The single-bacterial and label-free nature of our method suggests wide applicability for rapid point-of-care bacterial diagnosis.

© 2015 Optical Society of America

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2015 (1)

2014 (10)

J. Park, H. Yu, J.-H. Park, and Y. Park, “LCD panel characterization by measuring full Jones matrix of individual pixels using polarization-sensitive digital holographic microscopy,” Opt. Express 22(20), 24304–24311 (2014).
[Crossref] [PubMed]

J. Jung and Y. Park, “Spectro-angular light scattering measurements of individual microscopic objects,” Opt. Express 22(4), 4108–4114 (2014).
[Crossref] [PubMed]

J. H. Kang, M. Super, C. W. Yung, R. M. Cooper, K. Domansky, A. R. Graveline, T. Mammoto, J. B. Berthet, H. Tobin, M. J. Cartwright, A. L. Watters, M. Rottman, A. Waterhouse, A. Mammoto, N. Gamini, M. J. Rodas, A. Kole, A. Jiang, T. M. Valentin, A. Diaz, K. Takahashi, and D. E. Ingber, “An extracorporeal blood-cleansing device for sepsis therapy,” Nat. Med. 20(10), 1211–1216 (2014).
[Crossref] [PubMed]

D. K. Kang, M. M. Ali, K. Zhang, S. S. Huang, E. Peterson, M. A. Digman, E. Gratton, and W. Zhao, “Rapid detection of single bacteria in unprocessed blood using Integrated Comprehensive Droplet Digital Detection,” Nat. Commun. 5, 5427 (2014).
[Crossref] [PubMed]

Y. Jo, J. Jung, J. W. Lee, D. Shin, H. Park, K. T. Nam, J. H. Park, and Y. Park, “Angle-resolved light scattering of individual rod-shaped bacteria based on Fourier transform light scattering,” Sci. Rep. 4, 5090 (2014).
[Crossref] [PubMed]

K. Lee and Y. Park, “Quantitative phase imaging unit,” Opt. Lett. 39(12), 3630–3633 (2014).
[Crossref] [PubMed]

K. Kim, Z. Yaqoob, K. Lee, J. W. Kang, Y. Choi, P. Hosseini, P. T. So, and Y. Park, “Diffraction optical tomography using a quantitative phase imaging unit,” Opt. Lett. 39(24), 6935–6938 (2014).
[Crossref] [PubMed]

K. Kim, H. Yoon, M. Diez-Silva, M. Dao, R. R. Dasari, and Y. Park, “High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography,” J. Biomed. Opt. 19(1), 011005 (2014).
[Crossref] [PubMed]

Y. Kim, H. Shim, K. Kim, H. Park, J. H. Heo, J. Yoon, C. Choi, S. Jang, and Y. Park, “Common-path diffraction optical tomography for investigation of three-dimensional structures and dynamics of biological cells,” Opt. Express 22(9), 10398–10407 (2014).
[Crossref] [PubMed]

M. Mir, T. Kim, A. Majumder, M. Xiang, R. Wang, S. C. Liu, M. U. Gillette, S. Stice, and G. Popescu, “Label-free characterization of emerging human neuronal networks,” Sci. Rep. 4, 4434 (2014).
[Crossref] [PubMed]

2013 (7)

I. Moon, A. Anand, M. Cruz, and B. Javidi, “Identification of Malaria-infected red blood cells via digital shearing interferometry and statistical inference,” IEEE Photon. J. 5(5), 6900207 (2013).
[Crossref]

K. Lee, K. Kim, J. Jung, J. Heo, S. Cho, S. Lee, G. Chang, Y. Jo, H. Park, and Y. Park, “Quantitative phase imaging techniques for the study of cell pathophysiology: from principles to applications,” Sensors (Basel) 13(4), 4170–4191 (2013).
[Crossref] [PubMed]

G. F. Crosta, Y. L. Pan, K. B. Aptowicz, C. Casati, R. G. Pinnick, R. K. Chang, and G. W. Videen, “Automated classification of single airborne particles from two-dimensional angle-resolved optical scattering (TAOS) patterns by non-linear filtering,” J. Quant. Spectrosc. Ra. 131, 215–233 (2013).
[Crossref]

B. K. Wilson and G. D. Vigil, “Automated bacterial identification by angle resolved dark-field imaging,” Biomed. Opt. Express 4(9), 1692–1701 (2013).
[PubMed]

A. Suchwalko, I. Buzalewicz, A. Wieliczko, and H. Podbielska, “Bacteria species identification by the statistical analysis of bacterial colonies Fresnel patterns,” Opt. Express 21(9), 11322–11337 (2013).
[Crossref] [PubMed]

H. J. Chung, C. M. Castro, H. Im, H. Lee, and R. Weissleder, “A magneto-DNA nanoparticle system for rapid detection and phenotyping of bacteria,” Nat. Nanotechnol. 8(5), 369–375 (2013).
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K. Lee, H. D. Kim, K. Kim, Y. Kim, T. R. Hillman, B. Min, and Y. Park, “Synthetic Fourier transform light scattering,” Opt. Express 21(19), 22453–22463 (2013).
[Crossref] [PubMed]

2012 (6)

Y. Kim, J. Jeong, J. Jang, M. W. Kim, and Y. Park, “Polarization holographic microscopy for extracting spatio-temporally resolved Jones matrix,” Opt. Express 20(9), 9948–9955 (2012).
[Crossref] [PubMed]

N. J. Loman, C. Constantinidou, J. Z. Chan, M. Halachev, M. Sergeant, C. W. Penn, E. R. Robinson, and M. J. Pallen, “High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity,” Nat. Rev. Microbiol. 10(9), 599–606 (2012).
[Crossref] [PubMed]

K. Kim and Y. Park, “Fourier transform light scattering angular spectroscopy using digital inline holography,” Opt. Lett. 37(19), 4161–4163 (2012).
[Crossref] [PubMed]

Y. Kim, J. M. Higgins, R. R. Dasari, S. Suresh, and Y. Park, “Anisotropic light scattering of individual sickle red blood cells,” J. Biomed. Opt. 17(4), 040501 (2012).
[Crossref] [PubMed]

D. Boss, A. Hoffmann, B. Rappaz, C. Depeursinge, P. J. Magistretti, D. Van de Ville, and P. Marquet, “Spatially-resolved eigenmode decomposition of red blood cells membrane fluctuations questions the role of ATP in flickering,” PLoS ONE 7(8), e40667 (2012).
[Crossref] [PubMed]

A. Anand, V. K. Chhaniwal, N. R. Patel, and B. Javidi, “Automatic identification of Malaria-infected RBC with digital holographic microscopy using correlation algorithms,” IEEE Photon. J. 4(5), 1456–1464 (2012).
[Crossref]

2011 (8)

I. Moon, M. Daneshpanah, A. Anand, and B. Javidi, “Cell identification computational 3-D holographic microscopy,” Opt. Photonics News 22(6), 18–23 (2011).
[Crossref]

R. Liu, D. K. Dey, D. Boss, P. Marquet, and B. Javidi, “Recognition and classification of red blood cells using digital holographic microscopy and data clustering with discriminant analysis,” J. Opt. Soc. Am. A 28(6), 1204–1210 (2011).
[Crossref] [PubMed]

Y. Park, C. A. Best-Popescu, R. R. Dasari, and G. Popescu, “Light scattering of human red blood cells during metabolic remodeling of the membrane,” J. Biomed. Opt. 16(1), 011013 (2011).
[Crossref] [PubMed]

Y. L. Pan, M. J. Berg, S. S. Zhang, H. Noh, H. Cao, R. K. Chang, and G. Videen, “Measurement and autocorrelation analysis of two-dimensional light-scattering patterns from living cells for label-free classification,” Cytometry A 79(4), 284–292 (2011).
[Crossref] [PubMed]

S. K. Debnath and Y. Park, “Real-time quantitative phase imaging with a spatial phase-shifting algorithm,” Opt. Lett. 36(23), 4677–4679 (2011).
[Crossref] [PubMed]

A. Niemz, T. M. Ferguson, and D. S. Boyle, “Point-of-care nucleic acid testing for infectious diseases,” Trends Biotechnol. 29(5), 240–250 (2011).
[Crossref] [PubMed]

A. Kumar, “Optimizing Antimicrobial Therapy in Sepsis and Septic Shock,” Crit. Care Nurs. Clin. North Am. 23(1), 79–97 (2011).
[Crossref] [PubMed]

I. Buzalewicz, A. Wieliczko, and H. Podbielska, “Influence of various growth conditions on Fresnel diffraction patterns of bacteria colonies examined in the optical system with converging spherical wave illumination,” Opt. Express 19(22), 21768–21785 (2011).
[Crossref] [PubMed]

2010 (6)

E. Bae, N. Bai, A. Aroonnual, J. P. Robinson, A. K. Bhunia, and E. D. Hirleman, “Modeling light propagation through bacterial colonies and its correlation with forward scattering patterns,” J. Biomed. Opt. 15(4), 045001 (2010).
[Crossref] [PubMed]

N. N. Boustany, S. A. Boppart, and V. Backman, “Microscopic imaging and spectroscopy with scattered light,” Annu. Rev. Biomed. Eng. 12(1), 285–314 (2010).
[Crossref] [PubMed]

H. F. Ding, E. Berl, Z. Wang, L. J. Millet, M. U. Gillette, J. M. Liu, M. Boppart, and G. Popescu, “Fourier Transform Light Scattering of Biological Structure and Dynamics,” IEEE J. Sel. Top. Quantum Electron. 16(4), 909–918 (2010).
[Crossref]

Y. Park, M. Diez-Silva, D. Fu, G. Popescu, W. Choi, I. Barman, S. Suresh, and M. S. Feld, “Static and dynamic light scattering of healthy and malaria-parasite invaded red blood cells,” J. Biomed. Opt. 15(2), 020506 (2010).
[Crossref] [PubMed]

B. Javidi, M. Daneshpanah, and I. Moon, “Three-Dimensional Holographic Imaging for Identification of Biological Micro/Nanoorganisms,” IEEE Photon. J. 2(2), 256–259 (2010).
[Crossref]

D. Shin, M. Daneshpanah, A. Anand, and B. Javidi, “Optofluidic system for three-dimensional sensing and identification of micro-organisms with digital holographic microscopy,” Opt. Lett. 35(23), 4066–4068 (2010).
[Crossref] [PubMed]

2009 (4)

I. Moon, M. Daneshpanah, B. Javidi, and A. Stern, “Automated three-dimensional identification and tracking of micro/nanobiological organisms by computational holographic microscopy,” Proc. IEEE 97(6), 990–1010 (2009).
[Crossref]

S. Seo, T. W. Su, D. K. Tseng, A. Erlinger, and A. Ozcan, “Lensfree holographic imaging for on-chip cytometry and diagnostics,” Lab Chip 9(6), 777–787 (2009).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

P. M. Dark, P. Dean, and G. Warhurst, “Bench-to-bedside review: the promise of rapid infection diagnosis during sepsis using polymerase chain reaction-based pathogen detection,” Crit. Care 13(4), 217 (2009).
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2008 (5)

R. M. Jarvis and R. Goodacre, “Characterisation and identification of bacteria using SERS,” Chem. Soc. Rev. 37(5), 931–936 (2008).
[Crossref] [PubMed]

B. Rajwa, M. Venkatapathi, K. Ragheb, P. P. Banada, E. D. Hirleman, T. Lary, and J. P. Robinson, “Automated classification of bacterial particles in flow by multiangle scatter measurement and support vector machine classifier,” Cytometry A 73(4), 369–379 (2008).
[Crossref] [PubMed]

M. Venkatapathi, B. Rajwa, K. Ragheb, P. P. Banada, T. Lary, J. P. Robinson, and E. D. Hirleman, “High speed classification of individual bacterial cells using a model-based light scatter system and multivariate statistics,” Appl. Opt. 47(5), 678–686 (2008).
[Crossref] [PubMed]

I. Moon and B. Javidi, “3-D visualization and identification of biological microorganisms using partially temporal incoherent light in-line computational holographic imaging,” IEEE Trans. Med. Imaging 27(12), 1782–1790 (2008).
[Crossref] [PubMed]

H. Ding, Z. Wang, F. Nguyen, S. A. Boppart, and G. Popescu, “Fourier transform light scattering of inhomogeneous and dynamic structures,” Phys. Rev. Lett. 101(23), 238102 (2008).
[Crossref] [PubMed]

2007 (5)

I. Moon and B. Javidi, “Three-dimensional identification of stem cells by computational holographic imaging,” J. R. Soc. Interface 4(13), 305–313 (2007).
[Crossref] [PubMed]

A. Stern and B. Javidi, “Theoretical analysis of three-dimensional imaging and recognition of micro-organisms with a single-exposure on-line holographic microscope,” J. Opt. Soc. Am. A 24(1), 163–168 (2007).
[Crossref] [PubMed]

A. E. Cohen and W. E. Moerner, “Principal-components analysis of shape fluctuations of single DNA molecules,” Proc. Natl. Acad. Sci. U.S.A. 104(31), 12622–12627 (2007).
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P. P. Banada, S. Guo, B. Bayraktar, E. Bae, B. Rajwa, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Optical forward-scattering for detection of Listeria monocytogenes and other Listeria species,” Biosens. Bioelectron. 22(8), 1664–1671 (2007).
[Crossref] [PubMed]

D. G. Remick, “Pathophysiology of sepsis,” Am. J. Pathol. 170(5), 1435–1444 (2007).
[Crossref] [PubMed]

2006 (6)

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

C. A. Rebuffo, J. Schmitt, M. Wenning, F. von Stetten, and S. Scherer, “Reliable and rapid identification of Listeria monocytogenes and Listeria species by artificial neural network-based Fourier transform infrared spectroscopy,” Appl. Environ. Microbiol. 72(2), 994–1000 (2006).
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J. Garnacho-Montero, T. Aldabo-Pallas, C. Garnacho-Montero, A. Cayuela, R. Jiménez, S. Barroso, and C. Ortiz-Leyba, “Timing of adequate antibiotic therapy is a greater determinant of outcome than are TNF and IL-10 polymorphisms in patients with sepsis,” Crit. Care 10(4), R111 (2006).
[Crossref] [PubMed]

I. Moon and B. Javidi, “Volumetric three-dimensional recognition of biological microorganisms using multivariate statistical method and digital holography,” J. Biomed. Opt. 11(6), 064004 (2006).
[Crossref] [PubMed]

G. Popescu, T. Ikeda, R. R. Dasari, and M. S. Feld, “Diffraction phase microscopy for quantifying cell structure and dynamics,” Opt. Lett. 31(6), 775–777 (2006).
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Y. Park, G. Popescu, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express 14(18), 8263–8268 (2006).
[Crossref] [PubMed]

2005 (5)

B. Javidi, I. Moon, S. Yeom, and E. Carapezza, “Three-dimensional imaging and recognition of microorganism using single-exposure on-line (SEOL) digital holography,” Opt. Express 13(12), 4492–4506 (2005).
[Crossref] [PubMed]

I. Moon and B. Javidi, “Shape tolerant three-dimensional recognition of biological microorganisms using digital holography,” Opt. Express 13(23), 9612–9622 (2005).
[Crossref] [PubMed]

S. A. Alexandrov, T. R. Hillman, and D. D. Sampson, “Spatially resolved Fourier holographic light scattering angular spectroscopy,” Opt. Lett. 30(24), 3305–3307 (2005).
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C. Xie, J. Mace, M. A. Dinno, Y. Q. Li, W. Tang, R. J. Newton, and P. J. Gemperline, “Identification of single bacterial cells in aqueous solution using confocal laser tweezers Raman spectroscopy,” Anal. Chem. 77(14), 4390–4397 (2005).
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2003 (1)

R. S. Hotchkiss and I. E. Karl, “The pathophysiology and treatment of sepsis,” N. Engl. J. Med. 348(2), 138–150 (2003).
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2001 (2)

L. Mariey, J. P. Signolle, C. Amiel, and J. Travert, “Discrimination, classification, identification of microorganisms using FTIR spectroscopy and chemometrics,” Vib. Spectrosc. 26(2), 151–159 (2001).
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2000 (1)

K. C. Schuster, I. Reese, E. Urlaub, J. R. Gapes, and B. Lendl, “Multidimensional information on the chemical composition of single bacterial cells by confocal Raman microspectroscopy,” Anal. Chem. 72(22), 5529–5534 (2000).
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1998 (1)

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1994 (1)

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1993 (1)

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1992 (1)

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1991 (1)

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1985 (1)

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1984 (1)

S. S. Rao, D. Paolini, and G. G. Leppard, “Effects of low-Ph stress on the morphology and activity of bacteria from lakes receiving acid precipitation,” Hydrobiologia 114(2), 115–121 (1984).
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1972 (1)

P. J. Wyatt and D. T. Phillips, “Structure of single bacteria from light scattering,” J. Theor. Biol. 37(3), 493–501 (1972).
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1970 (1)

P. J. Wyatt, “Cell wall thickness, size distribution, refractive index ratio and dry weight content of living bacteria (Staphylococcus aureus),” Nature 226(5242), 277–279 (1970).
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1969 (1)

P. J. Wyatt, “Identification of bacteria by differential light scattering,” Nature 221(5187), 1257–1258 (1969).
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1968 (2)

P. J. Wyatt, “Differential light scattering: a physical method for identifying living bacterial cells,” Appl. Opt. 7(10), 1879–1896 (1968).
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1949 (1)

1936 (1)

R. A. Fisher, “The use of multiple measurements in taxonomic problems,” Ann. Eugen. 7(2), 179–188 (1936).
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Adil, A.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

Aldabo-Pallas, T.

J. Garnacho-Montero, T. Aldabo-Pallas, C. Garnacho-Montero, A. Cayuela, R. Jiménez, S. Barroso, and C. Ortiz-Leyba, “Timing of adequate antibiotic therapy is a greater determinant of outcome than are TNF and IL-10 polymorphisms in patients with sepsis,” Crit. Care 10(4), R111 (2006).
[Crossref] [PubMed]

Alexandrov, S. A.

Ali, M. M.

D. K. Kang, M. M. Ali, K. Zhang, S. S. Huang, E. Peterson, M. A. Digman, E. Gratton, and W. Zhao, “Rapid detection of single bacteria in unprocessed blood using Integrated Comprehensive Droplet Digital Detection,” Nat. Commun. 5, 5427 (2014).
[Crossref] [PubMed]

Amiel, C.

L. Mariey, J. P. Signolle, C. Amiel, and J. Travert, “Discrimination, classification, identification of microorganisms using FTIR spectroscopy and chemometrics,” Vib. Spectrosc. 26(2), 151–159 (2001).
[Crossref]

Anand, A.

I. Moon, A. Anand, M. Cruz, and B. Javidi, “Identification of Malaria-infected red blood cells via digital shearing interferometry and statistical inference,” IEEE Photon. J. 5(5), 6900207 (2013).
[Crossref]

A. Anand, V. K. Chhaniwal, N. R. Patel, and B. Javidi, “Automatic identification of Malaria-infected RBC with digital holographic microscopy using correlation algorithms,” IEEE Photon. J. 4(5), 1456–1464 (2012).
[Crossref]

I. Moon, M. Daneshpanah, A. Anand, and B. Javidi, “Cell identification computational 3-D holographic microscopy,” Opt. Photonics News 22(6), 18–23 (2011).
[Crossref]

D. Shin, M. Daneshpanah, A. Anand, and B. Javidi, “Optofluidic system for three-dimensional sensing and identification of micro-organisms with digital holographic microscopy,” Opt. Lett. 35(23), 4066–4068 (2010).
[Crossref] [PubMed]

Aptowicz, K. B.

G. F. Crosta, Y. L. Pan, K. B. Aptowicz, C. Casati, R. G. Pinnick, R. K. Chang, and G. W. Videen, “Automated classification of single airborne particles from two-dimensional angle-resolved optical scattering (TAOS) patterns by non-linear filtering,” J. Quant. Spectrosc. Ra. 131, 215–233 (2013).
[Crossref]

Aroonnual, A.

E. Bae, N. Bai, A. Aroonnual, J. P. Robinson, A. K. Bhunia, and E. D. Hirleman, “Modeling light propagation through bacterial colonies and its correlation with forward scattering patterns,” J. Biomed. Opt. 15(4), 045001 (2010).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

Backman, V.

N. N. Boustany, S. A. Boppart, and V. Backman, “Microscopic imaging and spectroscopy with scattered light,” Annu. Rev. Biomed. Eng. 12(1), 285–314 (2010).
[Crossref] [PubMed]

Badizadegan, K.

Bae, E.

E. Bae, N. Bai, A. Aroonnual, J. P. Robinson, A. K. Bhunia, and E. D. Hirleman, “Modeling light propagation through bacterial colonies and its correlation with forward scattering patterns,” J. Biomed. Opt. 15(4), 045001 (2010).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

P. P. Banada, S. Guo, B. Bayraktar, E. Bae, B. Rajwa, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Optical forward-scattering for detection of Listeria monocytogenes and other Listeria species,” Biosens. Bioelectron. 22(8), 1664–1671 (2007).
[Crossref] [PubMed]

Bai, N.

E. Bae, N. Bai, A. Aroonnual, J. P. Robinson, A. K. Bhunia, and E. D. Hirleman, “Modeling light propagation through bacterial colonies and its correlation with forward scattering patterns,” J. Biomed. Opt. 15(4), 045001 (2010).
[Crossref] [PubMed]

Banada, P. P.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

B. Rajwa, M. Venkatapathi, K. Ragheb, P. P. Banada, E. D. Hirleman, T. Lary, and J. P. Robinson, “Automated classification of bacterial particles in flow by multiangle scatter measurement and support vector machine classifier,” Cytometry A 73(4), 369–379 (2008).
[Crossref] [PubMed]

M. Venkatapathi, B. Rajwa, K. Ragheb, P. P. Banada, T. Lary, J. P. Robinson, and E. D. Hirleman, “High speed classification of individual bacterial cells using a model-based light scatter system and multivariate statistics,” Appl. Opt. 47(5), 678–686 (2008).
[Crossref] [PubMed]

P. P. Banada, S. Guo, B. Bayraktar, E. Bae, B. Rajwa, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Optical forward-scattering for detection of Listeria monocytogenes and other Listeria species,” Biosens. Bioelectron. 22(8), 1664–1671 (2007).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Barman, I.

Y. Park, M. Diez-Silva, D. Fu, G. Popescu, W. Choi, I. Barman, S. Suresh, and M. S. Feld, “Static and dynamic light scattering of healthy and malaria-parasite invaded red blood cells,” J. Biomed. Opt. 15(2), 020506 (2010).
[Crossref] [PubMed]

Barroso, S.

J. Garnacho-Montero, T. Aldabo-Pallas, C. Garnacho-Montero, A. Cayuela, R. Jiménez, S. Barroso, and C. Ortiz-Leyba, “Timing of adequate antibiotic therapy is a greater determinant of outcome than are TNF and IL-10 polymorphisms in patients with sepsis,” Crit. Care 10(4), R111 (2006).
[Crossref] [PubMed]

Bayraktar, B.

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

P. P. Banada, S. Guo, B. Bayraktar, E. Bae, B. Rajwa, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Optical forward-scattering for detection of Listeria monocytogenes and other Listeria species,” Biosens. Bioelectron. 22(8), 1664–1671 (2007).
[Crossref] [PubMed]

B. Bayraktar, P. P. Banada, E. D. Hirleman, A. K. Bhunia, J. P. Robinson, and B. Rajwa, “Feature extraction from light-scatter patterns of Listeria colonies for identification and classification,” J. Biomed. Opt. 11(3), 034006 (2006).
[Crossref] [PubMed]

Berg, M. J.

Y. L. Pan, M. J. Berg, S. S. Zhang, H. Noh, H. Cao, R. K. Chang, and G. Videen, “Measurement and autocorrelation analysis of two-dimensional light-scattering patterns from living cells for label-free classification,” Cytometry A 79(4), 284–292 (2011).
[Crossref] [PubMed]

Berl, E.

H. F. Ding, E. Berl, Z. Wang, L. J. Millet, M. U. Gillette, J. M. Liu, M. Boppart, and G. Popescu, “Fourier Transform Light Scattering of Biological Structure and Dynamics,” IEEE J. Sel. Top. Quantum Electron. 16(4), 909–918 (2010).
[Crossref]

Berthet, J. B.

J. H. Kang, M. Super, C. W. Yung, R. M. Cooper, K. Domansky, A. R. Graveline, T. Mammoto, J. B. Berthet, H. Tobin, M. J. Cartwright, A. L. Watters, M. Rottman, A. Waterhouse, A. Mammoto, N. Gamini, M. J. Rodas, A. Kole, A. Jiang, T. M. Valentin, A. Diaz, K. Takahashi, and D. E. Ingber, “An extracorporeal blood-cleansing device for sepsis therapy,” Nat. Med. 20(10), 1211–1216 (2014).
[Crossref] [PubMed]

Best-Popescu, C. A.

Y. Park, C. A. Best-Popescu, R. R. Dasari, and G. Popescu, “Light scattering of human red blood cells during metabolic remodeling of the membrane,” J. Biomed. Opt. 16(1), 011013 (2011).
[Crossref] [PubMed]

Bhunia, A. K.

E. Bae, N. Bai, A. Aroonnual, J. P. Robinson, A. K. Bhunia, and E. D. Hirleman, “Modeling light propagation through bacterial colonies and its correlation with forward scattering patterns,” J. Biomed. Opt. 15(4), 045001 (2010).
[Crossref] [PubMed]

P. P. Banada, K. Huff, E. Bae, B. Rajwa, A. Aroonnual, B. Bayraktar, A. Adil, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Label-free detection of multiple bacterial pathogens using light-scattering sensor,” Biosens. Bioelectron. 24(6), 1685–1692 (2009).
[Crossref] [PubMed]

P. P. Banada, S. Guo, B. Bayraktar, E. Bae, B. Rajwa, J. P. Robinson, E. D. Hirleman, and A. K. Bhunia, “Optical forward-scattering for detection of Listeria monocytogenes and other Listeria species,” Biosens. Bioelectron. 22(8), 1664–1671 (2007).
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K. Lee, K. Kim, J. Jung, J. Heo, S. Cho, S. Lee, G. Chang, Y. Jo, H. Park, and Y. Park, “Quantitative phase imaging techniques for the study of cell pathophysiology: from principles to applications,” Sensors (Basel) 13(4), 4170–4191 (2013).
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Y. Jo, J. Jung, J. W. Lee, D. Shin, H. Park, K. T. Nam, J. H. Park, and Y. Park, “Angle-resolved light scattering of individual rod-shaped bacteria based on Fourier transform light scattering,” Sci. Rep. 4, 5090 (2014).
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Park, Y.

K. Kim, J. Yoon, and Y. Park, “Simultaneous 3D visualization and position tracking of optically trapped particles using optical diffraction tomography,” Optica 2, 343–346 (2015).

K. Kim, Z. Yaqoob, K. Lee, J. W. Kang, Y. Choi, P. Hosseini, P. T. So, and Y. Park, “Diffraction optical tomography using a quantitative phase imaging unit,” Opt. Lett. 39(24), 6935–6938 (2014).
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J. Park, H. Yu, J.-H. Park, and Y. Park, “LCD panel characterization by measuring full Jones matrix of individual pixels using polarization-sensitive digital holographic microscopy,” Opt. Express 22(20), 24304–24311 (2014).
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K. Lee and Y. Park, “Quantitative phase imaging unit,” Opt. Lett. 39(12), 3630–3633 (2014).
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J. Jung and Y. Park, “Spectro-angular light scattering measurements of individual microscopic objects,” Opt. Express 22(4), 4108–4114 (2014).
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K. Kim, H. Yoon, M. Diez-Silva, M. Dao, R. R. Dasari, and Y. Park, “High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography,” J. Biomed. Opt. 19(1), 011005 (2014).
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K. Kim and Y. Park, “Fourier transform light scattering angular spectroscopy using digital inline holography,” Opt. Lett. 37(19), 4161–4163 (2012).
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Y. Kim, J. Jeong, J. Jang, M. W. Kim, and Y. Park, “Polarization holographic microscopy for extracting spatio-temporally resolved Jones matrix,” Opt. Express 20(9), 9948–9955 (2012).
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Y. Kim, J. M. Higgins, R. R. Dasari, S. Suresh, and Y. Park, “Anisotropic light scattering of individual sickle red blood cells,” J. Biomed. Opt. 17(4), 040501 (2012).
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S. K. Debnath and Y. Park, “Real-time quantitative phase imaging with a spatial phase-shifting algorithm,” Opt. Lett. 36(23), 4677–4679 (2011).
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N. J. Loman, C. Constantinidou, J. Z. Chan, M. Halachev, M. Sergeant, C. W. Penn, E. R. Robinson, and M. J. Pallen, “High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity,” Nat. Rev. Microbiol. 10(9), 599–606 (2012).
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B. Rajwa, M. Venkatapathi, K. Ragheb, P. P. Banada, E. D. Hirleman, T. Lary, and J. P. Robinson, “Automated classification of bacterial particles in flow by multiangle scatter measurement and support vector machine classifier,” Cytometry A 73(4), 369–379 (2008).
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C. A. Rebuffo, J. Schmitt, M. Wenning, F. von Stetten, and S. Scherer, “Reliable and rapid identification of Listeria monocytogenes and Listeria species by artificial neural network-based Fourier transform infrared spectroscopy,” Appl. Environ. Microbiol. 72(2), 994–1000 (2006).
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Opt. Lett. (7)

Opt. Photonics News (1)

I. Moon, M. Daneshpanah, A. Anand, and B. Javidi, “Cell identification computational 3-D holographic microscopy,” Opt. Photonics News 22(6), 18–23 (2011).
[Crossref]

Optica (1)

Phys. Rev. Lett. (1)

H. Ding, Z. Wang, F. Nguyen, S. A. Boppart, and G. Popescu, “Fourier transform light scattering of inhomogeneous and dynamic structures,” Phys. Rev. Lett. 101(23), 238102 (2008).
[Crossref] [PubMed]

PLoS ONE (1)

D. Boss, A. Hoffmann, B. Rappaz, C. Depeursinge, P. J. Magistretti, D. Van de Ville, and P. Marquet, “Spatially-resolved eigenmode decomposition of red blood cells membrane fluctuations questions the role of ATP in flickering,” PLoS ONE 7(8), e40667 (2012).
[Crossref] [PubMed]

Proc. IEEE (1)

I. Moon, M. Daneshpanah, B. Javidi, and A. Stern, “Automated three-dimensional identification and tracking of micro/nanobiological organisms by computational holographic microscopy,” Proc. IEEE 97(6), 990–1010 (2009).
[Crossref]

Proc. Natl. Acad. Sci. U.S.A. (1)

A. E. Cohen and W. E. Moerner, “Principal-components analysis of shape fluctuations of single DNA molecules,” Proc. Natl. Acad. Sci. U.S.A. 104(31), 12622–12627 (2007).
[Crossref] [PubMed]

Sci. Rep. (2)

M. Mir, T. Kim, A. Majumder, M. Xiang, R. Wang, S. C. Liu, M. U. Gillette, S. Stice, and G. Popescu, “Label-free characterization of emerging human neuronal networks,” Sci. Rep. 4, 4434 (2014).
[Crossref] [PubMed]

Y. Jo, J. Jung, J. W. Lee, D. Shin, H. Park, K. T. Nam, J. H. Park, and Y. Park, “Angle-resolved light scattering of individual rod-shaped bacteria based on Fourier transform light scattering,” Sci. Rep. 4, 5090 (2014).
[Crossref] [PubMed]

Sensors (Basel) (1)

K. Lee, K. Kim, J. Jung, J. Heo, S. Cho, S. Lee, G. Chang, Y. Jo, H. Park, and Y. Park, “Quantitative phase imaging techniques for the study of cell pathophysiology: from principles to applications,” Sensors (Basel) 13(4), 4170–4191 (2013).
[Crossref] [PubMed]

Trends Biotechnol. (1)

A. Niemz, T. M. Ferguson, and D. S. Boyle, “Point-of-care nucleic acid testing for infectious diseases,” Trends Biotechnol. 29(5), 240–250 (2011).
[Crossref] [PubMed]

Vib. Spectrosc. (1)

L. Mariey, J. P. Signolle, C. Amiel, and J. Travert, “Discrimination, classification, identification of microorganisms using FTIR spectroscopy and chemometrics,” Vib. Spectrosc. 26(2), 151–159 (2001).
[Crossref]

Other (9)

G. Popescu, Quantitative Phase Imaging of Cells and Tissues (McGraw-Hill Professional, 2011).

M. K. Kim, Digital Holographic Microscopy (Springer, 2011).

C. M. Bishop, Pattern Recognition and Machine Learning (Springer, 2006), Vol. 1.

I. Jolliffe, Principal Component Analysis (Wiley Online Library, 2005).

W. Zhao, A. Krishnaswamy, R. Chellappa, D. L. Swets, and J. Weng, “Discriminant analysis of principal components for face recognition,” in Face Recognition (Springer, 1998), pp. 73–85.

G. McLachlan, Discriminant Analysis and Statistical Pattern Recognition (John Wiley & Sons, 2004), Vol. 544.

R. Kohavi, “A study of cross-validation and bootstrap for accuracy estimation and model selection,” in IJCAI, 1995), 1137–1145.

R. Walpole, R. Myers, S. Myers, and K. Ye, Probability and Statistics for Engineers and Scientists (Prentice Hall, 2004).

B. Yegnanarayana, Artificial Neural Networks (PHI Learning Pvt. Ltd., 2009).

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Figures (7)

Fig. 1
Fig. 1

The size distribution of the four bacterial species, L. monocytogenes, E.coli, L. casei, and B. subtilis (67, 69, 78, and 55 bacterial cells, respectively). The lengths of the major and minor axes of each rod-shaped bacterium [indicated in Fig. 3(a)] in unsynchronized growth states are observed and plotted (see the following sections for the imaging method). It is impractical to identify the species from only cellular shapes, which are observable using conventional optical microscopy.

Fig. 2
Fig. 2

Experimental setup of DPM. The DPM setup is a laser-interferometric microscope in a common-path geometry. A sample is positioned between the condenser and objective lenses. OL: objective lens; CL: condenser lens; M1-2: mirrors; L1-6: lenses.

Fig. 3
Fig. 3

QPI and FTLS of individual bacterium. (a) Amplitude and (b) phase images of an isolated L. monocytogenes bacterium observed using QPI. (c) The corresponding 2D light scattering map generated by FTLS using the full optical field information from (a) and (b). The pseudo-FTLS maps by numerical propagation (d) without amplitude information, and (e) without phase information. The results indicate that phase information, a unique feature of QPI, is central to single-bacterial characterization rather than easily accessible amplitude information.

Fig. 4
Fig. 4

Overall procedure for single-bacterial identification. 2D ALS maps of isolated individual bacteria are measured using FTLS. The measured FTLS maps are then systematically analyzed in order to extract the unique fingerprint patterns for each species (classifiers) so that a new unidentified bacterium can be identified by a single light scattering measurement.

Fig. 5
Fig. 5

PCA of the FTLS patterns to extract the features for training the classifiers. (a) The first 16 principal patterns generated by PCA of all measured FTLS patterns. Each principal pattern is scaled into [–1, 1] for visualization purposes. (b) The full spectra of the principal pattern coefficients up to the 250th coefficient. Each row represents an individual bacterium, whereas each column represents a principal pattern. The principal patterns included here contain 99.9% of the original variance or information.

Fig. 6
Fig. 6

Feature selection and optimization for training the classifiers. (a) The p-value of each principal pattern coefficient as a measure of species-distinguishing capability is calculated using ANOVA and then the principal patterns are sorted in the order of ascending p-values. The principal pattern coefficients are presented in box plots for (b) the most distinguishable (index = 1) and (c) the most indistinguishable (index = 255) principal patterns. The first principal patterns with p-values close to zero are informative for classification, while the last principal patterns with p-values close to one are noisy. Thus, we select the principal patterns in a consecutive or accumulative manner, from left to right, as the features for statistical classification. The cross-validation accuracy for the classifiers trained in this manner is plotted in (d), where the optimal classification is achieved in the middle as expected.

Fig. 7
Fig. 7

Single-bacterial identification with the optimized classifier. The proportion of each output species for a certain input species, where leave-one-out cross-validation is utilized to precisely mimic the independently measured data, is plotted. The overall accuracy was 94.05%, with sensitivities of 95.52%, 95.65%, 88.46%, and 98.18% and specificities of 99.51%, 96.50%, 97.91%, and 98.13% for L. monocytogenes, E. coli, L. casei, and B. subtilis, respectively.

Tables (1)

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Table 1 Identification performance of the optimized classifier

Equations (2)

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E( r )=A( r )exp[ iΔϕ( r ) ],
I( u )= 1 2π | E( r )exp( 2πi u r ) d 2 r | 2 ,

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