Abstract

Diagnosis of malaria must be rapid, accurate, simple to use, portable and low cost, as suggested by the World Health Organization (WHO). Despite recent efforts, the gold standard remains the light microscopy of a stained blood film. This method can detect low parasitemia and identify different species of Plasmodium. However, it is time consuming, it requires well trained microscopist and good instrumentation to minimize misinterpretation, thus the costs are considerable. Moreover, the equipment cannot be easily transported and installed. In this paper we propose a new technique named “secondary speckle sensing microscopy” (S3M) based upon extraction of correlation based statistics of speckle patterns generated while illuminating red blood cells with a laser and inspecting them under a microscope. Then, using fuzzy logic ruling and principle component analysis, good quality of separation between healthy and infected red blood cells was demonstrated in preliminary experiments. The proposed technique can be used for automated high rate detection of malaria infected red blood cells.

© 2012 OSA

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2012 (1)

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

2011 (6)

C. A. Moxon, G. E. Grau, and A. G. Craig, “Malaria: modification of the red blood cell and consequences in the human host,” Br. J. Haematol.154(6), 670–679 (2011).
[CrossRef] [PubMed]

M. G. Millholland, R. Chandramohanadas, A. Pizzarro, A. Wehr, H. Shi, C. Darling, C. T. Lim, and D. C. Greenbaum, “The malaria parasite progressively dismantles the host erythrocyte cytoskeleton for efficient egress,” Mol. Cell. Proteomics10(12), M111.010678 (2011).
[CrossRef] [PubMed]

L. Gervais, N. de Rooij, and E. Delamarche, “Microfluidic chips for point-of-care immunodiagnostics,” Adv. Mater. (Deerfield Beach Fla.)23(24), H151–H176 (2011).
[CrossRef] [PubMed]

H. Bow, I. V. Pivkin, M. Diez-Silva, S. J. Goldfless, M. Dao, J. C. Niles, S. Suresh, and J. Han, “A microfabricated deformability-based flow cytometer with application to malaria,” Lab Chip11(6), 1065–1073 (2011).
[CrossRef] [PubMed]

Y. Beiderman, A. D. Amsel, Y. Tzadka, D. Fixler, V. Mico, J. Garcia, M. Teicher, and Z. Zalevsky, “A microscope configuration for nanometer 3-D movement monitoring accuracy,” Micron42(4), 366–375 (2011).
[CrossRef] [PubMed]

Y. Beiderman, R. Blumenberg, N. Rabani, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Demonstration of remote optical measurement configuration that correlates to glucose concentration in blood,” Biomed. Opt. Express2(4), 858–870 (2011).
[CrossRef] [PubMed]

2010 (4)

Y. Beiderman, I. Horovitz, N. Burshtein, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Remote estimation of blood pulse pressure via temporal tracking of reflected secondary speckles pattern,” J. Biomed. Opt.15(6), 061707 (2010).
[CrossRef] [PubMed]

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

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]

H. W. Hou, A. A. S. Bhagat, A. G. L. Chong, P. Mao, K. S. W. Tan, J. Han, and C. T. Lim, “Deformability based cell margination--a simple microfluidic design for malaria-infected erythrocyte separation,” Lab Chip10(19), 2605–2613 (2010).
[CrossRef] [PubMed]

2009 (3)

A. G. Maier, B. M. Cooke, A. F. Cowman, and L. Tilley, “Malaria parasite proteins that remodel the host erythrocyte,” Nat. Rev. Microbiol.7(5), 341–354 (2009).
[CrossRef] [PubMed]

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A113(47), 13327–13330 (2009).
[CrossRef] [PubMed]

C. S. Yelleswarapu, M. Tipping, S. R. Kothapalli, A. Veraksa, and D. V. Rao, “Common-path multimodal optical microscopy,” Opt. Lett.34(8), 1243–1245 (2009).
[CrossRef] [PubMed]

2008 (5)

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis.41(1), 10–16 (2008).
[CrossRef] [PubMed]

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.105(37), 13730–13735 (2008).
[CrossRef] [PubMed]

C. K. Murray, R. A. Gasser, A. J. Magill, and R. S. Miller, “Update on rapid diagnostic testing for malaria,” Clin. Microbiol. Rev.21(1), 97–110 (2008).
[CrossRef] [PubMed]

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

R. Lima, T. Ishikawa, Y. Imai, M. Takeda, S. Wada, and T. Yamaguchi, “Radial dispersion of red blood cells in blood flowing through glass capillaries: the role of hematocrit and geometry,” J. Biomech.41(10), 2188–2196 (2008).
[CrossRef] [PubMed]

2007 (2)

C. Wongsrichanalai, M. J. Barcus, S. Muth, A. Sutamihardja, and W. H. Wernsdorfer, “A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT),” Am. J. Trop. Med. Hyg.77(6Suppl), 119–127 (2007).
[PubMed]

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

2006 (2)

2005 (2)

F. Omodeo-Salè, A. Motti, A. Dondorp, N. J. White, and D. Taramelli, “Destabilisation and subsequent lysis of human erythrocytes induced by Plasmodium falciparum haem products,” Eur. J. Haematol.74(4), 324–332 (2005).
[CrossRef] [PubMed]

S. Suresh, J. Spatz, J. P. Mills, A. Micoulet, M. Dao, C. T. Lim, M. Beil, and T. Seufferlein, “Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria,” Acta Biomater.1(1), 15–30 (2005).
[CrossRef] [PubMed]

2003 (2)

F. Omodeo-Salè, A. Motti, N. Basilico, S. Parapini, P. Olliaro, and D. Taramelli, “Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum,” Blood102(2), 705–711 (2003).
[CrossRef] [PubMed]

J. P. Shelby, J. White, K. Ganesan, P. K. Rathod, and D. T. Chiu, “A microfluidic model for single-cell capillary obstruction by Plasmodium falciparum-infected erythrocytes,” Proc. Natl. Acad. Sci. U.S.A.100(25), 14618–14622 (2003).
[CrossRef] [PubMed]

2000 (1)

A. M. Dondorp, P. A. Kager, J. Vreeken, and N. J. White, “Abnormal blood flow and red blood cell deformability in severe malaria,” Parasitol. Today (Regul. Ed.)16(6), 228–232 (2000).
[CrossRef] [PubMed]

1999 (1)

A. M. Dondorp, K. T. Chotivanich, S. Fucharoen, K. Silamut, J. Vreeken, P. A. Kager, and N. J. White, “Red cell deformability, splenic function and anaemia in thalassaemia,” Br. J. Haematol.105(2), 505–508 (1999).
[CrossRef] [PubMed]

1998 (1)

1987 (1)

S. Wold, K. Esbensen, and P. Geladi, “Principal component analysis,” Chemom. Intell. Lab. Syst.2(1-3), 37–52 (1987).
[CrossRef]

1976 (1)

W. Trager and J. B. Jensen, “Human malaria parasites in continuous culture,” Science193(4254), 673–675 (1976).
[CrossRef] [PubMed]

1965 (1)

L. A. Zadeh, “Fuzzy sets,” Inf. Control8(3), 338–353 (1965).
[CrossRef]

1901 (1)

K. Pearson, “On lines and planes of closest fit to systems of points in space,” Philos. Mag.2, 559–572 (1901).

Ahmad, H.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Almeras, L.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Amsel, A. D.

Y. Beiderman, A. D. Amsel, Y. Tzadka, D. Fixler, V. Mico, J. Garcia, M. Teicher, and Z. Zalevsky, “A microscope configuration for nanometer 3-D movement monitoring accuracy,” Micron42(4), 366–375 (2011).
[CrossRef] [PubMed]

Badizadegan, K.

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A113(47), 13327–13330 (2009).
[CrossRef] [PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis.41(1), 10–16 (2008).
[CrossRef] [PubMed]

G. Popescu, Y. K. Park, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express14(18), 8263–8268 (2006).
[CrossRef] [PubMed]

Barcus, M. J.

C. Wongsrichanalai, M. J. Barcus, S. Muth, A. Sutamihardja, and W. H. Wernsdorfer, “A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT),” Am. J. Trop. Med. Hyg.77(6Suppl), 119–127 (2007).
[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]

Basilico, N.

F. Omodeo-Salè, A. Motti, N. Basilico, S. Parapini, P. Olliaro, and D. Taramelli, “Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum,” Blood102(2), 705–711 (2003).
[CrossRef] [PubMed]

Beiderman, Y.

Y. Beiderman, A. D. Amsel, Y. Tzadka, D. Fixler, V. Mico, J. Garcia, M. Teicher, and Z. Zalevsky, “A microscope configuration for nanometer 3-D movement monitoring accuracy,” Micron42(4), 366–375 (2011).
[CrossRef] [PubMed]

Y. Beiderman, R. Blumenberg, N. Rabani, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Demonstration of remote optical measurement configuration that correlates to glucose concentration in blood,” Biomed. Opt. Express2(4), 858–870 (2011).
[CrossRef] [PubMed]

Y. Beiderman, I. Horovitz, N. Burshtein, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Remote estimation of blood pulse pressure via temporal tracking of reflected secondary speckles pattern,” J. Biomed. Opt.15(6), 061707 (2010).
[CrossRef] [PubMed]

Beil, M.

S. Suresh, J. Spatz, J. P. Mills, A. Micoulet, M. Dao, C. T. Lim, M. Beil, and T. Seufferlein, “Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria,” Acta Biomater.1(1), 15–30 (2005).
[CrossRef] [PubMed]

Belghazi, M.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Benke, A.

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

Bhagat, A. A. S.

H. W. Hou, A. A. S. Bhagat, A. G. L. Chong, P. Mao, K. S. W. Tan, J. Han, and C. T. Lim, “Deformability based cell margination--a simple microfluidic design for malaria-infected erythrocyte separation,” Lab Chip10(19), 2605–2613 (2010).
[CrossRef] [PubMed]

Blumenberg, R.

Bonnefoy, S.

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

Boss, D.

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

Bourdon, S.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Bow, H.

H. Bow, I. V. Pivkin, M. Diez-Silva, S. J. Goldfless, M. Dao, J. C. Niles, S. Suresh, and J. Han, “A microfabricated deformability-based flow cytometer with application to malaria,” Lab Chip11(6), 1065–1073 (2011).
[CrossRef] [PubMed]

Burshtein, N.

Y. Beiderman, I. Horovitz, N. Burshtein, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Remote estimation of blood pulse pressure via temporal tracking of reflected secondary speckles pattern,” J. Biomed. Opt.15(6), 061707 (2010).
[CrossRef] [PubMed]

Chandramohanadas, R.

M. G. Millholland, R. Chandramohanadas, A. Pizzarro, A. Wehr, H. Shi, C. Darling, C. T. Lim, and D. C. Greenbaum, “The malaria parasite progressively dismantles the host erythrocyte cytoskeleton for efficient egress,” Mol. Cell. Proteomics10(12), M111.010678 (2011).
[CrossRef] [PubMed]

Chiu, D. T.

J. P. Shelby, J. White, K. Ganesan, P. K. Rathod, and D. T. Chiu, “A microfluidic model for single-cell capillary obstruction by Plasmodium falciparum-infected erythrocytes,” Proc. Natl. Acad. Sci. U.S.A.100(25), 14618–14622 (2003).
[CrossRef] [PubMed]

Choi, W.

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]

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A113(47), 13327–13330 (2009).
[CrossRef] [PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis.41(1), 10–16 (2008).
[CrossRef] [PubMed]

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.105(37), 13730–13735 (2008).
[CrossRef] [PubMed]

Chong, A. G. L.

H. W. Hou, A. A. S. Bhagat, A. G. L. Chong, P. Mao, K. S. W. Tan, J. Han, and C. T. Lim, “Deformability based cell margination--a simple microfluidic design for malaria-infected erythrocyte separation,” Lab Chip10(19), 2605–2613 (2010).
[CrossRef] [PubMed]

Chotivanich, K. T.

A. M. Dondorp, K. T. Chotivanich, S. Fucharoen, K. Silamut, J. Vreeken, P. A. Kager, and N. J. White, “Red cell deformability, splenic function and anaemia in thalassaemia,” Br. J. Haematol.105(2), 505–508 (1999).
[CrossRef] [PubMed]

Cooke, B. M.

A. G. Maier, B. M. Cooke, A. F. Cowman, and L. Tilley, “Malaria parasite proteins that remodel the host erythrocyte,” Nat. Rev. Microbiol.7(5), 341–354 (2009).
[CrossRef] [PubMed]

Cowman, A. F.

A. G. Maier, B. M. Cooke, A. F. Cowman, and L. Tilley, “Malaria parasite proteins that remodel the host erythrocyte,” Nat. Rev. Microbiol.7(5), 341–354 (2009).
[CrossRef] [PubMed]

Craig, A. G.

C. A. Moxon, G. E. Grau, and A. G. Craig, “Malaria: modification of the red blood cell and consequences in the human host,” Br. J. Haematol.154(6), 670–679 (2011).
[CrossRef] [PubMed]

Dao, M.

H. Bow, I. V. Pivkin, M. Diez-Silva, S. J. Goldfless, M. Dao, J. C. Niles, S. Suresh, and J. Han, “A microfabricated deformability-based flow cytometer with application to malaria,” Lab Chip11(6), 1065–1073 (2011).
[CrossRef] [PubMed]

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

S. Suresh, J. Spatz, J. P. Mills, A. Micoulet, M. Dao, C. T. Lim, M. Beil, and T. Seufferlein, “Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria,” Acta Biomater.1(1), 15–30 (2005).
[CrossRef] [PubMed]

Darling, C.

M. G. Millholland, R. Chandramohanadas, A. Pizzarro, A. Wehr, H. Shi, C. Darling, C. T. Lim, and D. C. Greenbaum, “The malaria parasite progressively dismantles the host erythrocyte cytoskeleton for efficient egress,” Mol. Cell. Proteomics10(12), M111.010678 (2011).
[CrossRef] [PubMed]

Dasari, R. R.

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A113(47), 13327–13330 (2009).
[CrossRef] [PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis.41(1), 10–16 (2008).
[CrossRef] [PubMed]

G. Popescu, Y. K. Park, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express14(18), 8263–8268 (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).
[CrossRef] [PubMed]

David, P. H.

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

de Rooij, N.

L. Gervais, N. de Rooij, and E. Delamarche, “Microfluidic chips for point-of-care immunodiagnostics,” Adv. Mater. (Deerfield Beach Fla.)23(24), H151–H176 (2011).
[CrossRef] [PubMed]

Delamarche, E.

L. Gervais, N. de Rooij, and E. Delamarche, “Microfluidic chips for point-of-care immunodiagnostics,” Adv. Mater. (Deerfield Beach Fla.)23(24), H151–H176 (2011).
[CrossRef] [PubMed]

Depeursinge, C.

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

Diez-Silva, M.

H. Bow, I. V. Pivkin, M. Diez-Silva, S. J. Goldfless, M. Dao, J. C. Niles, S. Suresh, and J. Han, “A microfabricated deformability-based flow cytometer with application to malaria,” Lab Chip11(6), 1065–1073 (2011).
[CrossRef] [PubMed]

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]

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.105(37), 13730–13735 (2008).
[CrossRef] [PubMed]

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

Dondorp, A.

F. Omodeo-Salè, A. Motti, A. Dondorp, N. J. White, and D. Taramelli, “Destabilisation and subsequent lysis of human erythrocytes induced by Plasmodium falciparum haem products,” Eur. J. Haematol.74(4), 324–332 (2005).
[CrossRef] [PubMed]

Dondorp, A. M.

A. M. Dondorp, P. A. Kager, J. Vreeken, and N. J. White, “Abnormal blood flow and red blood cell deformability in severe malaria,” Parasitol. Today (Regul. Ed.)16(6), 228–232 (2000).
[CrossRef] [PubMed]

A. M. Dondorp, K. T. Chotivanich, S. Fucharoen, K. Silamut, J. Vreeken, P. A. Kager, and N. J. White, “Red cell deformability, splenic function and anaemia in thalassaemia,” Br. J. Haematol.105(2), 505–508 (1999).
[CrossRef] [PubMed]

Esbensen, K.

S. Wold, K. Esbensen, and P. Geladi, “Principal component analysis,” Chemom. Intell. Lab. Syst.2(1-3), 37–52 (1987).
[CrossRef]

Fan, R.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Feld, M. S.

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]

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A113(47), 13327–13330 (2009).
[CrossRef] [PubMed]

G. Popescu, Y. Park, W. Choi, R. R. Dasari, M. S. Feld, and K. Badizadegan, “Imaging red blood cell dynamics by quantitative phase microscopy,” Blood Cells Mol. Dis.41(1), 10–16 (2008).
[CrossRef] [PubMed]

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.105(37), 13730–13735 (2008).
[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).
[CrossRef] [PubMed]

G. Popescu, Y. K. Park, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Diffraction phase and fluorescence microscopy,” Opt. Express14(18), 8263–8268 (2006).
[CrossRef] [PubMed]

Fixler, D.

Y. Beiderman, A. D. Amsel, Y. Tzadka, D. Fixler, V. Mico, J. Garcia, M. Teicher, and Z. Zalevsky, “A microscope configuration for nanometer 3-D movement monitoring accuracy,” Micron42(4), 366–375 (2011).
[CrossRef] [PubMed]

Fontaine, A.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Fourquet, P.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Fu, D.

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]

Fucharoen, S.

A. M. Dondorp, K. T. Chotivanich, S. Fucharoen, K. Silamut, J. Vreeken, P. A. Kager, and N. J. White, “Red cell deformability, splenic function and anaemia in thalassaemia,” Br. J. Haematol.105(2), 505–508 (1999).
[CrossRef] [PubMed]

Fusai, T.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Ganesan, K.

J. P. Shelby, J. White, K. Ganesan, P. K. Rathod, and D. T. Chiu, “A microfluidic model for single-cell capillary obstruction by Plasmodium falciparum-infected erythrocytes,” Proc. Natl. Acad. Sci. U.S.A.100(25), 14618–14622 (2003).
[CrossRef] [PubMed]

Garcia, J.

Y. Beiderman, A. D. Amsel, Y. Tzadka, D. Fixler, V. Mico, J. Garcia, M. Teicher, and Z. Zalevsky, “A microscope configuration for nanometer 3-D movement monitoring accuracy,” Micron42(4), 366–375 (2011).
[CrossRef] [PubMed]

Y. Beiderman, R. Blumenberg, N. Rabani, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Demonstration of remote optical measurement configuration that correlates to glucose concentration in blood,” Biomed. Opt. Express2(4), 858–870 (2011).
[CrossRef] [PubMed]

Y. Beiderman, I. Horovitz, N. Burshtein, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Remote estimation of blood pulse pressure via temporal tracking of reflected secondary speckles pattern,” J. Biomed. Opt.15(6), 061707 (2010).
[CrossRef] [PubMed]

Gasser, R. A.

C. K. Murray, R. A. Gasser, A. J. Magill, and R. S. Miller, “Update on rapid diagnostic testing for malaria,” Clin. Microbiol. Rev.21(1), 97–110 (2008).
[CrossRef] [PubMed]

Geladi, P.

S. Wold, K. Esbensen, and P. Geladi, “Principal component analysis,” Chemom. Intell. Lab. Syst.2(1-3), 37–52 (1987).
[CrossRef]

Gervais, L.

L. Gervais, N. de Rooij, and E. Delamarche, “Microfluidic chips for point-of-care immunodiagnostics,” Adv. Mater. (Deerfield Beach Fla.)23(24), H151–H176 (2011).
[CrossRef] [PubMed]

Goldfless, S. J.

H. Bow, I. V. Pivkin, M. Diez-Silva, S. J. Goldfless, M. Dao, J. C. Niles, S. Suresh, and J. Han, “A microfabricated deformability-based flow cytometer with application to malaria,” Lab Chip11(6), 1065–1073 (2011).
[CrossRef] [PubMed]

Gould, J.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Granjeaud, S.

A. Fontaine, S. Bourdon, M. Belghazi, M. Pophillat, P. Fourquet, S. Granjeaud, M. Torrentino-Madamet, C. Rogier, T. Fusai, and L. Almeras, “Plasmodium falciparum infection-induced changes in erythrocyte membrane proteins,” Parasitol. Res.110(2), 545–556 (2012).
[CrossRef] [PubMed]

Grau, G. E.

C. A. Moxon, G. E. Grau, and A. G. Craig, “Malaria: modification of the red blood cell and consequences in the human host,” Br. J. Haematol.154(6), 670–679 (2011).
[CrossRef] [PubMed]

Greenbaum, D. C.

M. G. Millholland, R. Chandramohanadas, A. Pizzarro, A. Wehr, H. Shi, C. Darling, C. T. Lim, and D. C. Greenbaum, “The malaria parasite progressively dismantles the host erythrocyte cytoskeleton for efficient egress,” Mol. Cell. Proteomics10(12), M111.010678 (2011).
[CrossRef] [PubMed]

Gur, E.

Han, J.

H. Bow, I. V. Pivkin, M. Diez-Silva, S. J. Goldfless, M. Dao, J. C. Niles, S. Suresh, and J. Han, “A microfabricated deformability-based flow cytometer with application to malaria,” Lab Chip11(6), 1065–1073 (2011).
[CrossRef] [PubMed]

H. W. Hou, A. A. S. Bhagat, A. G. L. Chong, P. Mao, K. S. W. Tan, J. Han, and C. T. Lim, “Deformability based cell margination--a simple microfluidic design for malaria-infected erythrocyte separation,” Lab Chip10(19), 2605–2613 (2010).
[CrossRef] [PubMed]

Heath, J. R.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Hood, L.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Horovitz, I.

Y. Beiderman, I. Horovitz, N. Burshtein, M. Teicher, J. Garcia, V. Mico, and Z. Zalevsky, “Remote estimation of blood pulse pressure via temporal tracking of reflected secondary speckles pattern,” J. Biomed. Opt.15(6), 061707 (2010).
[CrossRef] [PubMed]

Hou, H. W.

H. W. Hou, A. A. S. Bhagat, A. G. L. Chong, P. Mao, K. S. W. Tan, J. Han, and C. T. Lim, “Deformability based cell margination--a simple microfluidic design for malaria-infected erythrocyte separation,” Lab Chip10(19), 2605–2613 (2010).
[CrossRef] [PubMed]

Ikeda, T.

Imai, Y.

R. Lima, T. Ishikawa, Y. Imai, M. Takeda, S. Wada, and T. Yamaguchi, “Radial dispersion of red blood cells in blood flowing through glass capillaries: the role of hematocrit and geometry,” J. Biomech.41(10), 2188–2196 (2008).
[CrossRef] [PubMed]

Ishikawa, T.

R. Lima, T. Ishikawa, Y. Imai, M. Takeda, S. Wada, and T. Yamaguchi, “Radial dispersion of red blood cells in blood flowing through glass capillaries: the role of hematocrit and geometry,” J. Biomech.41(10), 2188–2196 (2008).
[CrossRef] [PubMed]

Jensen, J. B.

W. Trager and J. B. Jensen, “Human malaria parasites in continuous culture,” Science193(4254), 673–675 (1976).
[CrossRef] [PubMed]

Jourdain, P.

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

Kager, P. A.

A. M. Dondorp, P. A. Kager, J. Vreeken, and N. J. White, “Abnormal blood flow and red blood cell deformability in severe malaria,” Parasitol. Today (Regul. Ed.)16(6), 228–232 (2000).
[CrossRef] [PubMed]

A. M. Dondorp, K. T. Chotivanich, S. Fucharoen, K. Silamut, J. Vreeken, P. A. Kager, and N. J. White, “Red cell deformability, splenic function and anaemia in thalassaemia,” Br. J. Haematol.105(2), 505–508 (1999).
[CrossRef] [PubMed]

Kothapalli, S. R.

Kühn, J.

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

Kwong, G. A.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Lang, M. J.

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

Lim, C. T.

M. G. Millholland, R. Chandramohanadas, A. Pizzarro, A. Wehr, H. Shi, C. Darling, C. T. Lim, and D. C. Greenbaum, “The malaria parasite progressively dismantles the host erythrocyte cytoskeleton for efficient egress,” Mol. Cell. Proteomics10(12), M111.010678 (2011).
[CrossRef] [PubMed]

H. W. Hou, A. A. S. Bhagat, A. G. L. Chong, P. Mao, K. S. W. Tan, J. Han, and C. T. Lim, “Deformability based cell margination--a simple microfluidic design for malaria-infected erythrocyte separation,” Lab Chip10(19), 2605–2613 (2010).
[CrossRef] [PubMed]

J. P. Mills, M. Diez-Silva, D. J. Quinn, M. Dao, M. J. Lang, K. S. W. Tan, C. T. Lim, G. Milon, P. H. David, O. Mercereau-Puijalon, S. Bonnefoy, and S. Suresh, “Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.104(22), 9213–9217 (2007).
[CrossRef] [PubMed]

S. Suresh, J. Spatz, J. P. Mills, A. Micoulet, M. Dao, C. T. Lim, M. Beil, and T. Seufferlein, “Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria,” Acta Biomater.1(1), 15–30 (2005).
[CrossRef] [PubMed]

Lima, R.

R. Lima, T. Ishikawa, Y. Imai, M. Takeda, S. Wada, and T. Yamaguchi, “Radial dispersion of red blood cells in blood flowing through glass capillaries: the role of hematocrit and geometry,” J. Biomech.41(10), 2188–2196 (2008).
[CrossRef] [PubMed]

Liu, C.-C.

R. Fan, O. Vermesh, A. Srivastava, B. K. H. Yen, L. Qin, H. Ahmad, G. A. Kwong, C.-C. Liu, J. Gould, L. Hood, and J. R. Heath, “Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood,” Nat. Biotechnol.26(12), 1373–1378 (2008).
[CrossRef] [PubMed]

Lue, N.

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A113(47), 13327–13330 (2009).
[CrossRef] [PubMed]

Lykotrafitis, G.

Y. Park, M. Diez-Silva, G. Popescu, G. Lykotrafitis, W. Choi, M. S. Feld, and S. Suresh, “Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum,” Proc. Natl. Acad. Sci. U.S.A.105(37), 13730–13735 (2008).
[CrossRef] [PubMed]

Magill, A. J.

C. K. Murray, R. A. Gasser, A. J. Magill, and R. S. Miller, “Update on rapid diagnostic testing for malaria,” Clin. Microbiol. Rev.21(1), 97–110 (2008).
[CrossRef] [PubMed]

Magistretti, P. J.

N. Pavillon, A. Benke, D. Boss, C. Moratal, J. Kühn, P. Jourdain, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Cell morphology and intracellular ionic homeostasis explored with a multimodal approach combining epifluorescence and digital holographic microscopy,” J Biophotonics3(7), 432–436 (2010).
[CrossRef] [PubMed]

Maier, A. G.

A. G. Maier, B. M. Cooke, A. F. Cowman, and L. Tilley, “Malaria parasite proteins that remodel the host erythrocyte,” Nat. Rev. Microbiol.7(5), 341–354 (2009).
[CrossRef] [PubMed]

Mao, P.

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Figures (15)

Fig. 1
Fig. 1

Secondary speckle sensing microscopy (S3M) optical setup.

Fig. 2
Fig. 2

Some examples of the 20 relevant parameters corresponding to an inspected healthy RBC.

Fig. 3
Fig. 3

(a). Microscope image of an infected RBC. (b). Speckle pattern

Fig. 4
Fig. 4

Some examples of the relevant 20 parameters for one of the infected RBC.

Fig. 5
Fig. 5

An example of 4 parameters measured for the 12 hRBC (healthy cell samples).

Fig. 6
Fig. 6

An example of 4 parameters measured for the 13 iRBC (infected cells samples)

Fig. 7
Fig. 7

Three pairs of parameters for the healthy cell samples. The first 5 samples are used to determine the rules. Notice that some cells do not fit the reordering rule derived by averaging.

Fig. 8
Fig. 8

Three pairs of parameters for the infected cell samples. The first 5 samples are used to determine the rules. Notice that some cells do not fit the reordering rule derived by averaging.

Fig. 9
Fig. 9

Fuzzy logic ruling.

Fig. 10
Fig. 10

An example of applied Gaussian weighting.

Fig. 11
Fig. 11

Results for the fuzzy logic processing: (a) 8 of 12 samples are correctly diagnosed for being healthy (above at list one threshold line) and (b) 9 of 13 samples are correctly diagnosed for being infected (below at least one threshold line).

Fig. 12
Fig. 12

Values of parameter 1 of healthy and infected cells for data taken at a distance of 50 μm.

Fig. 13
Fig. 13

(a). Parameter 15 compared to others for distance of 50 μm. (b). All parameters and values for distance of 50 μm.

Fig. 14
Fig. 14

Normalized data.

Fig. 15
Fig. 15

Separation between infected and healthy cells. The figure presents the plot of the length of the vectors versus the index.

Tables (4)

Tables Icon

Table 1 Set of the 20 Inspected Parameters and their Assigned Serial Number

Tables Icon

Table 2 Parameter ordering for hRBCs from the highest to the smallest

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Table 3 Parameter ordering for iRBCs from the highest (left) to the smallest (right)

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Table 4 Unified parameters ordering for hRBC (first row) and iRBC (second row) and selection of three pairs of parameters for processing (bold)

Equations (3)

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x n = pos max { s n s n1 } ,     x n cum = pos max { s n s n1 } ,
i=1 n D ii tr(D)
ρ i = ( SS' ) ii

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