Abstract

Monitoring the early onset of bacterial film formation is critical in many clinical, environmental, and food quality control applications. We built a small inexpensive optical surface cytometer, in contrast with bulk spectroscopic methods, around a light-emitting diode (LED) and a complementary metal-oxide-semiconductor (CMOS) image sensor. It is designed to offer a large field-of-view of 200 mm2 and a large depth-of-field of 2-3 mm to overcome the limitations of routine methods like spectrophotometry and fluorescence microscopy. It provides a direct measurement without the need for complex image post-processing with a limit-of-detection around 104 cells/mm2, which is competitive with other similar yet more complex devices already available.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article

Corrections

Rafaël Sibilo, Juan Miguel Pérez, Felix Tebbenjohanns, Cedric Hurth, and Valerio Pruneri, "Surface cytometer for fluorescent detection and growth monitoring of bacteria over a large field-of-view: publisher’s note," Biomed. Opt. Express 10, 3698-3698 (2019)
https://www.osapublishing.org/boe/abstract.cfm?uri=boe-10-7-3698

20 June 2019: A correction was made to the author listing.


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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]
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  21. P. Stiefel, S. Schmidt-Emrich, K. Maniura-Weber, and Q. Ren, “Critical aspects of using bacterial cell viability assays with the fluorophores SYTO9 and propidium iodide,” BMC Microbiol. 15, 36 (2015).
  22. M. H. Zwietering, I. Jongenburger, F. M. Rombouts, and K. van’t Riet, “Modeling of the Bacterial Growth Curve,” Appl. Environ. Microbiol. 56(6), 1875–1881 (1990).
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  23. K. M. C. Tjørve and E. Tjørve, “The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family,” PLoS One 12(6), e0178691 (2017).
    [Crossref] [PubMed]
  24. H. Fujikawa and S. Morozumi, “Modeling Surface Growth of Escherichia coli on Agar Plates,” Appl. Environ. Microbiol. 71(12), 7920–7926 (2005).
    [Crossref] [PubMed]
  25. H. Zipper, H. Brunner, J. Bernhagen, and F. Vitzthum, “Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications,” Nucleic Acids Res. 32(12), e103 (2004).
    [Crossref] [PubMed]
  26. P. Soille and L. M. Vincent, “Watersheds in Digital Spaces: An Efficient Algorithm Based on Immersion Simulations,” Proc. SPIE 1360, 240–250 (1990).
  27. A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
    [Crossref] [PubMed]
  28. H. E. Kubitschek, “Cell Volume Increase in Escherichia coli after Shifts to Richer Media,” J. Bacteriol. 172(1), 94–101 (1990).
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    [Crossref] [PubMed]
  30. H. H. Tuson and D. B. Weibel, “Bacteria-surface interactions,” Soft Matter 9(17), 4368–4380 (2013).
    [Crossref] [PubMed]
  31. Y. Chao and T. Zhang, “Optimization of fixation methods for observation of bacterial cell morphology and surface ultrastructures by atomic force microscopy,” Appl. Microbiol. Biotechnol. 92(2), 381–392 (2011).
    [Crossref] [PubMed]
  32. A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
    [Crossref] [PubMed]
  33. A. K. Kniggendorf, T. W. Gaul, and M. Meinhardt-Wollweber, “Effects of Ethanol, Formaldehyde, and Gentle Heat Fixation in Confocal Resonance Raman Microscopy of Purple Nonsulfur Bacteria,” Microsc. Res. Tech. 74(2), 177–183 (2011).
    [Crossref] [PubMed]

2018 (1)

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

2017 (5)

Z. A. Islamy Mazrad, I. In, K. D. Lee, and S. Y. Park, “Rapid fluorometric bacteria detection assay and photothermal effect by fluorescent polymer of coated surfaces and aqueous state,” Biosens. Bioelectron. 89(Pt 2), 1026–1033 (2017).
[Crossref] [PubMed]

X. W. Hua, Y. W. Bao, H. Y. Wang, Z. Chen, and F. G. Wu, “Bacteria-derived fluorescent carbon dots for microbial live/dead differentiation,” Nanoscale 9(6), 2150–2161 (2017).
[Crossref] [PubMed]

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Y. Lu, S. Horikawa, I. H. Chen, S. Du, H. C. Wikle, S. J. Suh, and B. A. Chin, “Highly sensitive surface-scanning detector for the direct bacterial detection using magnetoelastic (ME) biosensors,” Proc. SPIE 10217, 1021703 (2017).
[Crossref]

K. M. C. Tjørve and E. Tjørve, “The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family,” PLoS One 12(6), e0178691 (2017).
[Crossref] [PubMed]

2016 (5)

S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
[Crossref]

X. Liu, M. Marrakchi, D. Xu, H. Dong, and S. Andreescu, “Biosensors based on modularly designed synthetic peptides for recognition, detection and live/dead differentiation of pathogenic bacteria,” Biosens. Bioelectron. 80, 9–16 (2016).
[Crossref] [PubMed]

H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
[Crossref] [PubMed]

H. L. Røder, S. J. Sørensen, and M. Burmølle, “Studying Bacterial Multispecies Biofilms: Where to Start?” Trends Microbiol. 24(6), 503–513 (2016).
[Crossref] [PubMed]

S. M. Yoo and S. Y. Lee, “Optical Biosensors for the Detection of Pathogenic Microorganisms,” Trends Biotechnol. 34(1), 7–25 (2016).
[Crossref] [PubMed]

2015 (3)

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

P. Stiefel, S. Schmidt-Emrich, K. Maniura-Weber, and Q. Ren, “Critical aspects of using bacterial cell viability assays with the fluorophores SYTO9 and propidium iodide,” BMC Microbiol. 15, 36 (2015).

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

2014 (4)

A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
[Crossref] [PubMed]

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
[Crossref] [PubMed]

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

H. Schmidt and T. Eickhorst, “Detection and quantification of native microbial populations on soil-grown rice roots by catalyzed reporter deposition-fluorescence in situ hybridization,” FEMS Microbiol. Ecol. 87(2), 390–402 (2014).
[Crossref] [PubMed]

2013 (3)

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J. P. Muller, “Fluorescence Characterization of Clinically-Important Bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Y. Chai, S. Horikawa, S. Li, H. C. Wikle, and B. A. Chin, “A surface-scanning coil detector for real-time, in-situ detection of bacteria on fresh food surfaces,” Biosens. Bioelectron. 50, 311–317 (2013).
[Crossref] [PubMed]

H. H. Tuson and D. B. Weibel, “Bacteria-surface interactions,” Soft Matter 9(17), 4368–4380 (2013).
[Crossref] [PubMed]

2012 (2)

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

2011 (2)

A. K. Kniggendorf, T. W. Gaul, and M. Meinhardt-Wollweber, “Effects of Ethanol, Formaldehyde, and Gentle Heat Fixation in Confocal Resonance Raman Microscopy of Purple Nonsulfur Bacteria,” Microsc. Res. Tech. 74(2), 177–183 (2011).
[Crossref] [PubMed]

Y. Chao and T. Zhang, “Optimization of fixation methods for observation of bacterial cell morphology and surface ultrastructures by atomic force microscopy,” Appl. Microbiol. Biotechnol. 92(2), 381–392 (2011).
[Crossref] [PubMed]

2007 (1)

M. Berney, F. Hammes, F. Bosshard, H. U. Weilenmann, and T. Egli, “Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry,” Appl. Environ. Microbiol. 73, 3283–3290 (2007).

2005 (1)

H. Fujikawa and S. Morozumi, “Modeling Surface Growth of Escherichia coli on Agar Plates,” Appl. Environ. Microbiol. 71(12), 7920–7926 (2005).
[Crossref] [PubMed]

2004 (1)

H. Zipper, H. Brunner, J. Bernhagen, and F. Vitzthum, “Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications,” Nucleic Acids Res. 32(12), e103 (2004).
[Crossref] [PubMed]

2001 (1)

M. P. Buttner, P. Cruz-Perez, and L. D. Stetzenbach, “Enhanced Detection of Surface-Associated Bacteria in Indoor Environments by Quantitative PCR,” Appl. Environ. Microbiol. 67(6), 2564–2570 (2001).
[Crossref] [PubMed]

1990 (3)

P. Soille and L. M. Vincent, “Watersheds in Digital Spaces: An Efficient Algorithm Based on Immersion Simulations,” Proc. SPIE 1360, 240–250 (1990).

H. E. Kubitschek, “Cell Volume Increase in Escherichia coli after Shifts to Richer Media,” J. Bacteriol. 172(1), 94–101 (1990).
[Crossref] [PubMed]

M. H. Zwietering, I. Jongenburger, F. M. Rombouts, and K. van’t Riet, “Modeling of the Bacterial Growth Curve,” Appl. Environ. Microbiol. 56(6), 1875–1881 (1990).
[PubMed]

Ahmed, M. U.

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

Andreescu, S.

X. Liu, M. Marrakchi, D. Xu, H. Dong, and S. Andreescu, “Biosensors based on modularly designed synthetic peptides for recognition, detection and live/dead differentiation of pathogenic bacteria,” Biosens. Bioelectron. 80, 9–16 (2016).
[Crossref] [PubMed]

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Azeredo, J.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Azevedo, N. F.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Bao, Y. W.

X. W. Hua, Y. W. Bao, H. Y. Wang, Z. Chen, and F. G. Wu, “Bacteria-derived fluorescent carbon dots for microbial live/dead differentiation,” Nanoscale 9(6), 2150–2161 (2017).
[Crossref] [PubMed]

Barbaree, J. M.

S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
[Crossref]

Berney, M.

M. Berney, F. Hammes, F. Bosshard, H. U. Weilenmann, and T. Egli, “Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry,” Appl. Environ. Microbiol. 73, 3283–3290 (2007).

Bernhagen, J.

H. Zipper, H. Brunner, J. Bernhagen, and F. Vitzthum, “Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications,” Nucleic Acids Res. 32(12), e103 (2004).
[Crossref] [PubMed]

Bishop, E. S.

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

Bosshard, F.

M. Berney, F. Hammes, F. Bosshard, H. U. Weilenmann, and T. Egli, “Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry,” Appl. Environ. Microbiol. 73, 3283–3290 (2007).

Braescu, L.

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

Briandet, R.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Brunner, H.

H. Zipper, H. Brunner, J. Bernhagen, and F. Vitzthum, “Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications,” Nucleic Acids Res. 32(12), e103 (2004).
[Crossref] [PubMed]

Burmølle, M.

H. L. Røder, S. J. Sørensen, and M. Burmølle, “Studying Bacterial Multispecies Biofilms: Where to Start?” Trends Microbiol. 24(6), 503–513 (2016).
[Crossref] [PubMed]

Buttner, M. P.

M. P. Buttner, P. Cruz-Perez, and L. D. Stetzenbach, “Enhanced Detection of Surface-Associated Bacteria in Indoor Environments by Quantitative PCR,” Appl. Environ. Microbiol. 67(6), 2564–2570 (2001).
[Crossref] [PubMed]

Cardona, A.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Casas-Finet, J. R.

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

Catalan, V.

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A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
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S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
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X. W. Hua, Y. W. Bao, H. Y. Wang, Z. Chen, and F. G. Wu, “Bacteria-derived fluorescent carbon dots for microbial live/dead differentiation,” Nanoscale 9(6), 2150–2161 (2017).
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Y. Lu, S. Horikawa, I. H. Chen, S. Du, H. C. Wikle, S. J. Suh, and B. A. Chin, “Highly sensitive surface-scanning detector for the direct bacterial detection using magnetoelastic (ME) biosensors,” Proc. SPIE 10217, 1021703 (2017).
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S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
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Y. Chai, S. Horikawa, S. Li, H. C. Wikle, and B. A. Chin, “A surface-scanning coil detector for real-time, in-situ detection of bacteria on fresh food surfaces,” Biosens. Bioelectron. 50, 311–317 (2013).
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J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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X. Liu, M. Marrakchi, D. Xu, H. Dong, and S. Andreescu, “Biosensors based on modularly designed synthetic peptides for recognition, detection and live/dead differentiation of pathogenic bacteria,” Biosens. Bioelectron. 80, 9–16 (2016).
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Y. Lu, S. Horikawa, I. H. Chen, S. Du, H. C. Wikle, S. J. Suh, and B. A. Chin, “Highly sensitive surface-scanning detector for the direct bacterial detection using magnetoelastic (ME) biosensors,” Proc. SPIE 10217, 1021703 (2017).
[Crossref]

S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
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H. Schmidt and T. Eickhorst, “Detection and quantification of native microbial populations on soil-grown rice roots by catalyzed reporter deposition-fluorescence in situ hybridization,” FEMS Microbiol. Ecol. 87(2), 390–402 (2014).
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H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
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H. Fujikawa and S. Morozumi, “Modeling Surface Growth of Escherichia coli on Agar Plates,” Appl. Environ. Microbiol. 71(12), 7920–7926 (2005).
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Gaul, T. W.

A. K. Kniggendorf, T. W. Gaul, and M. Meinhardt-Wollweber, “Effects of Ethanol, Formaldehyde, and Gentle Heat Fixation in Confocal Resonance Raman Microscopy of Purple Nonsulfur Bacteria,” Microsc. Res. Tech. 74(2), 177–183 (2011).
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A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
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Haisch, C.

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
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Hammes, F.

M. Berney, F. Hammes, F. Bosshard, H. U. Weilenmann, and T. Egli, “Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry,” Appl. Environ. Microbiol. 73, 3283–3290 (2007).

Hartenstein, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
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J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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Y. Lu, S. Horikawa, I. H. Chen, S. Du, H. C. Wikle, S. J. Suh, and B. A. Chin, “Highly sensitive surface-scanning detector for the direct bacterial detection using magnetoelastic (ME) biosensors,” Proc. SPIE 10217, 1021703 (2017).
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S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
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Y. Chai, S. Horikawa, S. Li, H. C. Wikle, and B. A. Chin, “A surface-scanning coil detector for real-time, in-situ detection of bacteria on fresh food surfaces,” Biosens. Bioelectron. 50, 311–317 (2013).
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X. W. Hua, Y. W. Bao, H. Y. Wang, Z. Chen, and F. G. Wu, “Bacteria-derived fluorescent carbon dots for microbial live/dead differentiation,” Nanoscale 9(6), 2150–2161 (2017).
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Z. A. Islamy Mazrad, I. In, K. D. Lee, and S. Y. Park, “Rapid fluorometric bacteria detection assay and photothermal effect by fluorescent polymer of coated surfaces and aqueous state,” Biosens. Bioelectron. 89(Pt 2), 1026–1033 (2017).
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Z. A. Islamy Mazrad, I. In, K. D. Lee, and S. Y. Park, “Rapid fluorometric bacteria detection assay and photothermal effect by fluorescent polymer of coated surfaces and aqueous state,” Biosens. Bioelectron. 89(Pt 2), 1026–1033 (2017).
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H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
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H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
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J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
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H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
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A. K. Kniggendorf, T. W. Gaul, and M. Meinhardt-Wollweber, “Effects of Ethanol, Formaldehyde, and Gentle Heat Fixation in Confocal Resonance Raman Microscopy of Purple Nonsulfur Bacteria,” Microsc. Res. Tech. 74(2), 177–183 (2011).
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J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
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V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
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S. M. Yoo and S. Y. Lee, “Optical Biosensors for the Detection of Pathogenic Microorganisms,” Trends Biotechnol. 34(1), 7–25 (2016).
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Y. Chai, S. Horikawa, S. Li, H. C. Wikle, and B. A. Chin, “A surface-scanning coil detector for real-time, in-situ detection of bacteria on fresh food surfaces,” Biosens. Bioelectron. 50, 311–317 (2013).
[Crossref] [PubMed]

Liu, X.

X. Liu, M. Marrakchi, D. Xu, H. Dong, and S. Andreescu, “Biosensors based on modularly designed synthetic peptides for recognition, detection and live/dead differentiation of pathogenic bacteria,” Biosens. Bioelectron. 80, 9–16 (2016).
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Liu, Y.

S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
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A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
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J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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X. Liu, M. Marrakchi, D. Xu, H. Dong, and S. Andreescu, “Biosensors based on modularly designed synthetic peptides for recognition, detection and live/dead differentiation of pathogenic bacteria,” Biosens. Bioelectron. 80, 9–16 (2016).
[Crossref] [PubMed]

Martínez, P.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

McGivney, J. B.

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

Meinhardt-Wollweber, M.

A. K. Kniggendorf, T. W. Gaul, and M. Meinhardt-Wollweber, “Effects of Ethanol, Formaldehyde, and Gentle Heat Fixation in Confocal Resonance Raman Microscopy of Purple Nonsulfur Bacteria,” Microsc. Res. Tech. 74(2), 177–183 (2011).
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Mergulhão, F.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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Meyer, R. L.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
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Mircescu, N. E.

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
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Moore, G.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J. P. Muller, “Fluorescence Characterization of Clinically-Important Bacteria,” PLoS One 8(9), e75270 (2013).
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Morozumi, S.

H. Fujikawa and S. Morozumi, “Modeling Surface Growth of Escherichia coli on Agar Plates,” Appl. Environ. Microbiol. 71(12), 7920–7926 (2005).
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Muller, J. P.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J. P. Muller, “Fluorescence Characterization of Clinically-Important Bacteria,” PLoS One 8(9), e75270 (2013).
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Müller, V.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
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M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
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Niessner, R.

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
[Crossref] [PubMed]

Nychas, G.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Ozcan, A.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

Park, S. Y.

Z. A. Islamy Mazrad, I. In, K. D. Lee, and S. Y. Park, “Rapid fluorometric bacteria detection assay and photothermal effect by fluorescent polymer of coated surfaces and aqueous state,” Biosens. Bioelectron. 89(Pt 2), 1026–1033 (2017).
[Crossref] [PubMed]

Pavlovic, R.

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

Pérez, J. M.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Pietzsch, T.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Preibisch, S.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Pruneri, V.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Ren, Q.

P. Stiefel, S. Schmidt-Emrich, K. Maniura-Weber, and Q. Ren, “Critical aspects of using bacterial cell viability assays with the fluorophores SYTO9 and propidium iodide,” BMC Microbiol. 15, 36 (2015).

Rice, S. A.

H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
[Crossref] [PubMed]

Roberts, T. A.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J. P. Muller, “Fluorescence Characterization of Clinically-Important Bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Røder, H. L.

H. L. Røder, S. J. Sørensen, and M. Burmølle, “Studying Bacterial Multispecies Biofilms: Where to Start?” Trends Microbiol. 24(6), 503–513 (2016).
[Crossref] [PubMed]

Rombouts, F. M.

M. H. Zwietering, I. Jongenburger, F. M. Rombouts, and K. van’t Riet, “Modeling of the Bacterial Growth Curve,” Appl. Environ. Microbiol. 56(6), 1875–1881 (1990).
[PubMed]

Rueden, C.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Saalfeld, S.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Safavieh, M.

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

Schenerman, M. A.

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

Schindelin, J.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Schmid, B.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Schmidt, H.

H. Schmidt and T. Eickhorst, “Detection and quantification of native microbial populations on soil-grown rice roots by catalyzed reporter deposition-fluorescence in situ hybridization,” FEMS Microbiol. Ecol. 87(2), 390–402 (2014).
[Crossref] [PubMed]

Schmidt-Emrich, S.

P. Stiefel, S. Schmidt-Emrich, K. Maniura-Weber, and Q. Ren, “Critical aspects of using bacterial cell viability assays with the fluorophores SYTO9 and propidium iodide,” BMC Microbiol. 15, 36 (2015).

Simões, M.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Soille, P.

P. Soille and L. M. Vincent, “Watersheds in Digital Spaces: An Efficient Algorithm Based on Immersion Simulations,” Proc. SPIE 1360, 240–250 (1990).

Sokullu, E.

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

Sørensen, S. J.

H. L. Røder, S. J. Sørensen, and M. Burmølle, “Studying Bacterial Multispecies Biofilms: Where to Start?” Trends Microbiol. 24(6), 503–513 (2016).
[Crossref] [PubMed]

Sousa, J. M.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

Steinberg, P.

H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
[Crossref] [PubMed]

Sternberg, C.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Stetzenbach, L. D.

M. P. Buttner, P. Cruz-Perez, and L. D. Stetzenbach, “Enhanced Detection of Surface-Associated Bacteria in Indoor Environments by Quantitative PCR,” Appl. Environ. Microbiol. 67(6), 2564–2570 (2001).
[Crossref] [PubMed]

Stiefel, P.

P. Stiefel, S. Schmidt-Emrich, K. Maniura-Weber, and Q. Ren, “Critical aspects of using bacterial cell viability assays with the fluorophores SYTO9 and propidium iodide,” BMC Microbiol. 15, 36 (2015).

Strouse, R. J.

A. I. Dragan, R. Pavlovic, J. B. McGivney, J. R. Casas-Finet, E. S. Bishop, R. J. Strouse, M. A. Schenerman, and C. D. Geddes, “SYBR Green I: fluorescence properties and interaction with DNA,” J. Fluoresc. 22(4), 1189–1199 (2012).
[Crossref] [PubMed]

Su, Y.

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

Suh, S. J.

Y. Lu, S. Horikawa, I. H. Chen, S. Du, H. C. Wikle, S. J. Suh, and B. A. Chin, “Highly sensitive surface-scanning detector for the direct bacterial detection using magnetoelastic (ME) biosensors,” Proc. SPIE 10217, 1021703 (2017).
[Crossref]

S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
[Crossref]

Sun, B.

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

Szewzyk, U.

H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
[Crossref] [PubMed]

Tinevez, J. Y.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Tjørve, E.

K. M. C. Tjørve and E. Tjørve, “The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family,” PLoS One 12(6), e0178691 (2017).
[Crossref] [PubMed]

Tjørve, K. M. C.

K. M. C. Tjørve and E. Tjørve, “The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family,” PLoS One 12(6), e0178691 (2017).
[Crossref] [PubMed]

Tomancak, P.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Tresse, O.

J. Azeredo, N. F. Azevedo, R. Briandet, N. Cerca, T. Coenye, A. R. Costa, M. Desvaux, G. Di Bonaventura, M. Hébraud, Z. Jaglic, M. Kačániová, S. Knøchel, A. Lourenço, F. Mergulhão, R. L. Meyer, G. Nychas, M. Simões, O. Tresse, and C. Sternberg, “Critical review on biofilm methods,” Crit. Rev. Microbiol. 43(3), 313–351 (2017).
[Crossref] [PubMed]

Tseng, D.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

Tuson, H. H.

H. H. Tuson and D. B. Weibel, “Bacteria-surface interactions,” Soft Matter 9(17), 4368–4380 (2013).
[Crossref] [PubMed]

van’t Riet, K.

M. H. Zwietering, I. Jongenburger, F. M. Rombouts, and K. van’t Riet, “Modeling of the Bacterial Growth Curve,” Appl. Environ. Microbiol. 56(6), 1875–1881 (1990).
[PubMed]

Veli, M.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

Vincent, L. M.

P. Soille and L. M. Vincent, “Watersheds in Digital Spaces: An Efficient Algorithm Based on Immersion Simulations,” Proc. SPIE 1360, 240–250 (1990).

Vitzthum, F.

H. Zipper, H. Brunner, J. Bernhagen, and F. Vitzthum, “Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications,” Nucleic Acids Res. 32(12), e103 (2004).
[Crossref] [PubMed]

Wang, H.

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

Wang, H. Y.

X. W. Hua, Y. W. Bao, H. Y. Wang, Z. Chen, and F. G. Wu, “Bacteria-derived fluorescent carbon dots for microbial live/dead differentiation,” Nanoscale 9(6), 2150–2161 (2017).
[Crossref] [PubMed]

Ward, J. M.

L. R. Dartnell, T. A. Roberts, G. Moore, J. M. Ward, and J. P. Muller, “Fluorescence Characterization of Clinically-Important Bacteria,” PLoS One 8(9), e75270 (2013).
[Crossref] [PubMed]

Weibel, D. B.

H. H. Tuson and D. B. Weibel, “Bacteria-surface interactions,” Soft Matter 9(17), 4368–4380 (2013).
[Crossref] [PubMed]

Weilenmann, H. U.

M. Berney, F. Hammes, F. Bosshard, H. U. Weilenmann, and T. Egli, “Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry,” Appl. Environ. Microbiol. 73, 3283–3290 (2007).

Westerlund, F.

V. Müller, J. M. Sousa, H. C. Koydemir, M. Veli, D. Tseng, L. Cerqueira, A. Ozcan, N. F. Azevedo, and F. Westerlund, “Identification of a pathogenic bacteria in complex samples using a smartphone based fluorescence microscope,” RSC Advances 8(64), 36493–36502 (2018).
[Crossref]

White, D. J.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Wikle, H. C.

Y. Lu, S. Horikawa, I. H. Chen, S. Du, H. C. Wikle, S. J. Suh, and B. A. Chin, “Highly sensitive surface-scanning detector for the direct bacterial detection using magnetoelastic (ME) biosensors,” Proc. SPIE 10217, 1021703 (2017).
[Crossref]

S. Horikawa, I. H. Chen, S. Du, Y. Liu, H. C. Wikle, S. J. Suh, J. M. Barbaree, and B. A. Chin, “Method for Detection of a Few Pathogenic Bacteria and Determination of Live versus Dead Cells,” Proc. SPIE 9864, 98640H (2016).
[Crossref]

Y. Chai, S. Horikawa, S. Li, H. C. Wikle, and B. A. Chin, “A surface-scanning coil detector for real-time, in-situ detection of bacteria on fresh food surfaces,” Biosens. Bioelectron. 50, 311–317 (2013).
[Crossref] [PubMed]

Wingender, J.

H. C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S. A. Rice, and S. Kjelleberg, “Biofilms: an emergent form of bacterial life,” Nat. Rev. Microbiol. 14(9), 563–575 (2016).
[Crossref] [PubMed]

Wu, F. G.

X. W. Hua, Y. W. Bao, H. Y. Wang, Z. Chen, and F. G. Wu, “Bacteria-derived fluorescent carbon dots for microbial live/dead differentiation,” Nanoscale 9(6), 2150–2161 (2017).
[Crossref] [PubMed]

Xu, D.

X. Liu, M. Marrakchi, D. Xu, H. Dong, and S. Andreescu, “Biosensors based on modularly designed synthetic peptides for recognition, detection and live/dead differentiation of pathogenic bacteria,” Biosens. Bioelectron. 80, 9–16 (2016).
[Crossref] [PubMed]

Yáñez, M. A.

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Yang, D.

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
[Crossref] [PubMed]

Yoo, S. M.

S. M. Yoo and S. Y. Lee, “Optical Biosensors for the Detection of Pathogenic Microorganisms,” Trends Biotechnol. 34(1), 7–25 (2016).
[Crossref] [PubMed]

Yu, A. C.

A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
[Crossref] [PubMed]

Yu, S.

A. C. Yu, J. F. Loo, S. Yu, S. K. Kong, and T. F. Chan, “Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique,” Appl. Microbiol. Biotechnol. 98(2), 855–862 (2014).
[Crossref] [PubMed]

Zhang, T.

Y. Chao and T. Zhang, “Optimization of fixation methods for observation of bacterial cell morphology and surface ultrastructures by atomic force microscopy,” Appl. Microbiol. Biotechnol. 92(2), 381–392 (2011).
[Crossref] [PubMed]

Zhou, H.

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
[Crossref] [PubMed]

Zhou, Y.

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

Zhu, Y.

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

Zipper, H.

H. Zipper, H. Brunner, J. Bernhagen, and F. Vitzthum, “Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications,” Nucleic Acids Res. 32(12), e103 (2004).
[Crossref] [PubMed]

Zourob, M.

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

Zwietering, M. H.

M. H. Zwietering, I. Jongenburger, F. M. Rombouts, and K. van’t Riet, “Modeling of the Bacterial Growth Curve,” Appl. Environ. Microbiol. 56(6), 1875–1881 (1990).
[PubMed]

Anal. Chem. (1)

H. Zhou, D. Yang, N. P. Ivleva, N. E. Mircescu, R. Niessner, and C. Haisch, “SERS Detection of Bacteria in Water by in Situ Coating with Ag Nanoparticles,” Anal. Chem. 86(3), 1525–1533 (2014).
[Crossref] [PubMed]

Analyst (Lond.) (2)

M. Safavieh, M. U. Ahmed, E. Sokullu, A. Ng, L. Braescu, and M. Zourob, “A Simple Cassette as Point-of-Care Diagnostic Device for Naked-eye Colorimetric Bacteria Detection,” Analyst (Lond.) 139(2), 482–487 (2014).
[Crossref] [PubMed]

J. M. Pérez, M. Jofre, P. Martínez, M. A. Yáñez, V. Catalan, and V. Pruneri, “An image cytometer based on angular spatial frequency processing and its validation for rapid detection and quantification of waterborne microorganisms,” Analyst (Lond.) 140(22), 7734–7741 (2015).
[Crossref] [PubMed]

Angew. Chem. Int. Ed. Engl. (1)

H. Wang, Y. Zhou, X. Jiang, B. Sun, Y. Zhu, H. Wang, Y. Su, and Y. He, “Simultaneous Capture, Detection, and Inactivation of Bacteria As Enabled by a Surface-Enhanced Raman Scattering Multifunctional Chip,” Angew. Chem. Int. Ed. Engl. 54(17), 5132–5136 (2015).
[Crossref] [PubMed]

Appl. Environ. Microbiol. (4)

M. P. Buttner, P. Cruz-Perez, and L. D. Stetzenbach, “Enhanced Detection of Surface-Associated Bacteria in Indoor Environments by Quantitative PCR,” Appl. Environ. Microbiol. 67(6), 2564–2570 (2001).
[Crossref] [PubMed]

M. Berney, F. Hammes, F. Bosshard, H. U. Weilenmann, and T. Egli, “Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight kit in combination with flow cytometry,” Appl. Environ. Microbiol. 73, 3283–3290 (2007).

M. H. Zwietering, I. Jongenburger, F. M. Rombouts, and K. van’t Riet, “Modeling of the Bacterial Growth Curve,” Appl. Environ. Microbiol. 56(6), 1875–1881 (1990).
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Figures (9)

Fig. 1
Fig. 1 (A) Details of the optical elements interfacing with the sample. The critical distances were: D1 = 10 mm between the LED and the achromatic lens, D2 = 50 mm between the lens and the object, and D3 = 11 mm between the imaging lens backplane and the CMOS image sensor array (CMOS-ISA). The blue and green arrows represent the limit (bold) and central rays (light) of the excitation and emission paths, respectively. (B) Surface cytometer optical setup including the light-emitting diode (LED) light source, imaging lens, color and interference filters, and the CMOS-ISA. The scaler bar of 20 mm was added for scaling.
Fig. 2
Fig. 2 Determination of the filed-of-view (FOV) and lateral resolution of the device using the positive 1951 USAF target. Entire restricted 200 mm2 imaging FOV on the CMOS-ISA (A). The dashed yellow square represents Groups 4 and 5 on the calibration grid while the black dashed square delimits the FOV used (16.5 x 12.4 mm). Magnification of Groups 4 and 5 (B) showing the highest resolved elements in Group 4 used to determine the lateral resolution of 25.4 lines/mm (39 µm). Cross-section (C) indicated by the black arrow after conversion in a 16-bit grayscale image.
Fig. 3
Fig. 3 Average growth curve in liquid phase obtained using optical density measurement, or turbidity, at 600 nm (A). The error bars obtained originate from experiments performed on different days with cells in different dormant states prior to seeding the LB culture medium. The red line is a fit to a logistic population growth model yielding a seed ratio of the inoculum size to the carrying capacity x0 = 0.0077 ± 0.001 and a maximum growth rate r = 0.0140 ± 0.0004 s−1. The growth curve generated by the surface cytometer (B) is in close agreement with the reference optical density curve and yields x0 = 0.017 ± 0.005 and r = 0.0120 ± 0.0009 s−1.
Fig. 4
Fig. 4 (A) Time evolution from microscopy images acquired on a Nikon Ti-U microscope to benchmark our device using SYBR Green stained aliquots of E. coli growing at 37 °C. The intensity scale is identical for all images and the images have been background subtracted using a rolling ball method with a radius of 10 pixels. (B) Growth curve obtained by particle analysis using a watershed algorithm to better separate adjacent cells, then restricting to a size and circularity according to the expected dimensions of E. coli organisms. The red line is a sigmoid fit that represents the expected curve.
Fig. 5
Fig. 5 Evolution with the distance from the surface (focus) of (A) the mean fluorescence in the green channel of the surface cytometer device compared to (B) the fluorescent particles counted for confocal images in the Z-stack for an E. coli culture sample in the exponential phase (OD = 2.0). The sample was stained with SYBR Green directly in the LB culture medium (black circles, ●), after fixation with glutaraldehyde at 2.5% (v/v) final (red squares, ■), or absolute ethanol to 40% (v/v) final (blue diamonds, ♦). The higher depth-of-focus results in a much higher measurement volume in the surface cytometer compared to traditional microscopy.
Fig. 6
Fig. 6 Evolution of the fluorescence signal detected by the CMOS-ISA sensor for a serial dilution of Alexa Fluor 488 (AF488) dye in deionized water. The red curve represents the average baseline value for deionized water when the LED is ON. The first data point above the baseline occurs for 1-2 nM of AF488, which determines the practical limit of detection (LOD) of the system for a diluted molecular fluorescent dye.
Fig. 7
Fig. 7 Stability of the LED used in the surface cytometer setup (color and interference excitation filters removed). (A) Evolution of the signal acquired by the CMOS-ISA in the same experimental conditions as the ones used to monitor bacterial growth (3 100-ms captures separated by 5 s over a total time of 17 minutes. (B) Evolution of the signal acquired by the CMOS-ISA for 100 consecutive captures (exposition: 100 ms) separated by 5 s. In both cases, the drift of the LED (50% duty cycle and 20 MHz) was only 0.26% over more than 17 minutes. This is negligible compared to the changes in the signal from bacterial growth. The red line is a linear fit to appreciate the drift.
Fig. 8
Fig. 8 Transmission microscope image (A) of a fresh culture aliquot stained first with SYBR Green I for 20 min, then with Propidium Iodide for 5 min. All bacteria present on the surface appeared green from the SYBR nucleic acid stain in the green (FITC) channel (B) of the Nikon Ti-U epifluorescence microscope, but no red signal appeared in the red (excitation CWL = 488 nm/emission CWL = 600 nm) channel (C). This indicates the validity of our assumption that a vast majority of the samples obtained immediately from a fresh culture are alive.
Fig. 9
Fig. 9 Images form the CMOS-ISA of the surface cytometer for a control made of only PBS buffer (A), a bacterial culture sample stained with SYBR Green I at an OD value of 0.1 (B), 0.25 (C), 0.5 (D), and 1.0 (E). The red, green, and blue channels were split and the shown green channel was subtracted with the average of the blue and red channel to take the camera response into account. (F) is the evolution of the histogram count for the control and the samples at OD = 0.1 and OD = 1.0 and illustrates the evolution of the green signal.

Tables (1)

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Table 1 Comparison of our method to other available ones for bacterial biofilm monitoring.

Equations (3)

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O D ( t ) = B G + A G   e x p ( e x p ( e k z A ( T l a g t ) + 1 ) )
O D ( t ) = B R + A R ( 1 + ( 1 x 0 1 ) e x p ( r t ) )
c = 4 π A P 2

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