Automated imaging, identification, and counting of similar cells from digital
                hologram reconstructions

Mona Mihailescu; Mihaela Scarlat; Alexandru Gheorghiu; Julia Costescu; Mihai Kusko; Irina Alexandra Paun; Eugen Scarlat

doi:10.1364/AO.50.003589

Automated imaging, identification, and counting of similar cells from digital hologram reconstructions

Mona Mihailescu, Mihaela Scarlat, Alexandru Gheorghiu, Julia Costescu, Mihai Kusko, Irina Alexandra Paun, and Eugen Scarlat

Applied Optics
Vol. 50,
Issue 20,
pp. 3589-3597
(2011)
•https://doi.org/10.1364/AO.50.003589

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Mona Mihailescu, Mihaela Scarlat, Alexandru Gheorghiu, Julia Costescu, Mihai Kusko, Irina Alexandra Paun, and Eugen Scarlat, "Automated imaging, identification, and counting of similar cells from digital hologram reconstructions," Appl. Opt. 50, 3589-3597 (2011)

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Abstract

This paper presents our method, which simultaneously combines automatic imaging, identification, and counting with the acquisition of morphological information for at least 1000 blood cells from several three-dimensional images of the same sample. We started with seeking parameters to differentiate between red blood cells that are similar but different with respect to their development stage, i.e., mature or immature. We highlight that these cells have different diffractive patterns with complementary central intensity distribution in a given plane along the propagation axis. We use the Fresnel approximation to simulate propagation through cells modeled as spheroid-shaped phase objects and to find the cell property that has the dominant influence on this behavior. Starting with images obtained in the reconstruction step of the digital holographic microscopy technique, we developed a code for automated simultaneous individual cell image separation, identification, and counting, even when the cells are partially overlapped on a slide, and accurate measuring of their morphological features. To find the centroids of each cell, we propose a method based on analytical functions applied at threshold intervals. Our procedure separates the mature from the immature red blood cells and from the white blood cells through a decision based on gradient and radius values.

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E. B. Krumbhaar, “Reticulosis-increased percentage in the peripheral blood,” in Hematology: Landmark Papers of the Twentieth Century, M.A.Lichtman, L.A.Boxer, E.Henderson, and J.L.Spivak, eds. (Academic, 2000), p. 805.
L. M. Lowenstein, “The Mammalian reticulocyte,” in International Review of Cytology, G.H.Bourne and J.F.Danielli, eds. (Academic, 1959), Vol. 8.
[Crossref] [PubMed]
L. Blanc, A. De Gassart, C. Géminard, P. Bette-Bobillo, and M. Vidal, “Exosome release by reticulocytes—an integral part of the red blood cell differentiation system,” Blood Cells Mol. Dis. 35, 21–26 (2005).
[Crossref] [PubMed]
J. G. Stephens, “Surface and fragility differences between mature and immature red cells,” J. Physiol. 99, 30–48 (1940).
[PubMed]
A. K. Percy, E. Schmell, B. J. Earles, and W. J. Lennarz, “Phospholipid biosynthesis in the membranes of immature and mature red blood cells,” Biochemistry 12, 2456–2461 (1973).
[Crossref] [PubMed]
T. Lecklin, A. Tuominen, and M. Nikinmaa, “The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes,” J. Exp. Biol. 203, 3025–3031(2000).
[PubMed]
Y. M. Serebrennikova, J. Patel, W. K. Milhous, and L. H. Garc?a-Rubio, “Quantitative analysis of morphological alterations in Plasmodium falciparum infected red blood cells through theoretical interpretation of spectral measurements,” J. Therm. Biol. 265, 493–500 (2010).
[Crossref]
J. C. Thompson and B. W. Manktelow, “Pathogenesis and red blood cell destruction in hemoglobinemic leptospirosis,” J. Comp. Pathol. 96, 529–540 (1986).
[Crossref] [PubMed]
S. Christel and C. Little, “Morphological changes during heating of erythrocytes from stored human blood,” J. Therm. Biol. 9, 221–228 (1984).
[Crossref]
I. A. Kabat, W. Leyko, B. Kwiatkowski, and I. Zakrzewska, “Osmotic properties and morphological changes of submicroscopic surface structures of mammalian red blood cells subjected to UV-irradiation in vitro,” Zentralbl. Bakteriol. Orig. B 159, 88–94 (1974).
[PubMed]
A. J. McGoron, C. H. Joiner, M. B. Palascak, W. J. Claussen, and R. S. Franco, “Dehydration of mature and immature sickle red blood cells during fast oxygenation/deoxygenation cycles: role of KCl cotransport and extracellular calcium,” Blood 95, 2164–2168 (2000).
[PubMed]
N. Mochandas, M. R. Clark, M. S. Jacobs, and S. B. Shohet, “Analysis of factors regulating erythrocyte deformability,” J. Clin. Invest. 66, 563–573 (1980).
[Crossref]
M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]
S. Rancourt-Grenier, M.-T. Wei, J.-J. Bai, A. Chiou, P. P. Bareil, P.-L. Duval, and Y. Sheng, “Dynamic deformation of red blood cell in dual-trap optical tweezers,” Opt. Express 18, 10462–10472 (2010).
[Crossref] [PubMed]
C. Fang-Yen, S. Oh, Y. Park, W. Choi, S. Song, H. S. Seung, R. R. Dasari, and M. S. Feld, “Imaging voltage-dependent cell motions with heterodyne Mach–Zehnder phase microscopy,” Opt. Lett. 32, 1572–1574 (2007).
[Crossref] [PubMed]
B.-W. Yang and Z. Li, “Measuring microinteractions between coagulating red blood cells using optical tweezers,” Biomed. Opt. Express 1, 1217–1224 (2010).
[Crossref]
Y. K. Park, C. A. Best, K. Badizadegan, R. R. Dasari, M. S. Feld, T. Kuriabova, M. L. Henle, A. J. Levine, and G. Popescu, “Measurement of red blood cell mechanics during morphological changes,” Proc. Natl. Acad. Sci. USA 107, 6731–6736 (2010).
[Crossref] [PubMed]
Y.-S. Choi and S. Lee, “Three-dimensional volumetric measurement of red blood cell motion using digital holographic microscopy,” Appl. Opt. 48, 2983–2990 (2009).
[Crossref] [PubMed]
B. Rappaz, A. Barbul, A. Hoffmann, D. Boss, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Spatial analysis of erythrocyte membrane fluctuations by digital holographic microscopy,” Blood Cells Mol. Dis. 42, 228–232 (2009).
[Crossref] [PubMed]
M. Paturzo, F. Merola, S. Grilli, S. De Nicola, A. Finizio, and P. Ferraro, “Super-resolution in digital holography by a two-dimensional dynamic phase grating,” Opt. Express 16, 17107–17118 (2008).
[Crossref] [PubMed]
V. Mico, Z. Zalevsky, C. Ferreira, and J. García, “Super-resolution digital holographic microscopy for three-dimensional samples,” Opt. Express 16, 19260–19270 (2008).
[Crossref]
G. J. Streekstra1, J. G. G. Dobbe, and A. G. Hoekstra, “Quantification of the fraction poorly deformable red blood cells using ektacytometry,” Opt. Express 18, 14173–14182 (2010).
[Crossref]
J. W. Goodman, Introduction to Fourier Optics (McGraw-Hill, 1968).
M. Mihailescu, “Natural quasi-periodic binary structure with focusing property in near-field diffraction pattern,” Opt. Express 18, 12526–12536 (2010).
[Crossref] [PubMed]
B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry Part A 73A, 895–903 (2008).
[Crossref]
W. Groner, N. Mohandas, and M. Bessis, “New optical technique for measuring erythrocyte deformability with the ektacytometer,” Clin. Chem. 26, 1435–1442 (1980).
[PubMed]
F. M. Gaffney, “Experimental hemolytic anemia with particular reference to the corpuscular hemoglobin concentrations of the erythrocytes,” Br. J. Haematol. 3, 311–319 (1957).
[Crossref] [PubMed]
G. d’Onofrio, R. Chirillo, G. Zini, G. Caenaro, M. Tommasi, and G. Micciulli, “Simultaneous measurement of reticulocyte and red blood cell indices in healthy subjects and patients with microcytic and macrocytic anemia,” Blood 85, 818–823 (1995).
[PubMed]
F. Montfort, F. Charrière, T. Colomb, E. Cuche, P. Marquet, and C. Depeursinge, “Purely numerical compensation for microscope objective phase curvature in digital holographic microscopy: influence of digital phase masks position,” J. Opt. Soc. Am. A 23, 2944–2953 (2006).
[Crossref]
M. Mir, Z. Wang, K. Tangella, and G. Popescu, “Phase cytometry: blood on a CD-ROM,” Opt. Express 17, 2579–2585 (2009).
[Crossref] [PubMed]

2010 (7)

Y. M. Serebrennikova, J. Patel, W. K. Milhous, and L. H. Garc?a-Rubio, “Quantitative analysis of morphological alterations in Plasmodium falciparum infected red blood cells through theoretical interpretation of spectral measurements,” J. Therm. Biol. 265, 493–500 (2010).
[Crossref]

B.-W. Yang and Z. Li, “Measuring microinteractions between coagulating red blood cells using optical tweezers,” Biomed. Opt. Express 1, 1217–1224 (2010).
[Crossref]

Y. K. Park, C. A. Best, K. Badizadegan, R. R. Dasari, M. S. Feld, T. Kuriabova, M. L. Henle, A. J. Levine, and G. Popescu, “Measurement of red blood cell mechanics during morphological changes,” Proc. Natl. Acad. Sci. USA 107, 6731–6736 (2010).
[Crossref] [PubMed]

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

S. Rancourt-Grenier, M.-T. Wei, J.-J. Bai, A. Chiou, P. P. Bareil, P.-L. Duval, and Y. Sheng, “Dynamic deformation of red blood cell in dual-trap optical tweezers,” Opt. Express 18, 10462–10472 (2010).
[Crossref] [PubMed]

G. J. Streekstra1, J. G. G. Dobbe, and A. G. Hoekstra, “Quantification of the fraction poorly deformable red blood cells using ektacytometry,” Opt. Express 18, 14173–14182 (2010).
[Crossref]

M. Mihailescu, “Natural quasi-periodic binary structure with focusing property in near-field diffraction pattern,” Opt. Express 18, 12526–12536 (2010).
[Crossref] [PubMed]

2009 (3)

M. Mir, Z. Wang, K. Tangella, and G. Popescu, “Phase cytometry: blood on a CD-ROM,” Opt. Express 17, 2579–2585 (2009).
[Crossref] [PubMed]

Y.-S. Choi and S. Lee, “Three-dimensional volumetric measurement of red blood cell motion using digital holographic microscopy,” Appl. Opt. 48, 2983–2990 (2009).
[Crossref] [PubMed]

B. Rappaz, A. Barbul, A. Hoffmann, D. Boss, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Spatial analysis of erythrocyte membrane fluctuations by digital holographic microscopy,” Blood Cells Mol. Dis. 42, 228–232 (2009).
[Crossref] [PubMed]

2008 (3)

M. Paturzo, F. Merola, S. Grilli, S. De Nicola, A. Finizio, and P. Ferraro, “Super-resolution in digital holography by a two-dimensional dynamic phase grating,” Opt. Express 16, 17107–17118 (2008).
[Crossref] [PubMed]

V. Mico, Z. Zalevsky, C. Ferreira, and J. García, “Super-resolution digital holographic microscopy for three-dimensional samples,” Opt. Express 16, 19260–19270 (2008).
[Crossref]

B. Rappaz, A. Barbul, Y. Emery, R. Korenstein, C. Depeursinge, P. J. Magistretti, and P. Marquet, “Comparative study of human erythrocytes by digital holographic microscopy, confocal microscopy, and impedance volume analyzer,” Cytometry Part A 73A, 895–903 (2008).
[Crossref]

2007 (1)

C. Fang-Yen, S. Oh, Y. Park, W. Choi, S. Song, H. S. Seung, R. R. Dasari, and M. S. Feld, “Imaging voltage-dependent cell motions with heterodyne Mach–Zehnder phase microscopy,” Opt. Lett. 32, 1572–1574 (2007).
[Crossref] [PubMed]

2006 (1)

F. Montfort, F. Charrière, T. Colomb, E. Cuche, P. Marquet, and C. Depeursinge, “Purely numerical compensation for microscope objective phase curvature in digital holographic microscopy: influence of digital phase masks position,” J. Opt. Soc. Am. A 23, 2944–2953 (2006).
[Crossref]

2005 (1)

L. Blanc, A. De Gassart, C. Géminard, P. Bette-Bobillo, and M. Vidal, “Exosome release by reticulocytes—an integral part of the red blood cell differentiation system,” Blood Cells Mol. Dis. 35, 21–26 (2005).
[Crossref] [PubMed]

2000 (3)

E. B. Krumbhaar, “Reticulosis-increased percentage in the peripheral blood,” in Hematology: Landmark Papers of the Twentieth Century, M.A.Lichtman, L.A.Boxer, E.Henderson, and J.L.Spivak, eds. (Academic, 2000), p. 805.

T. Lecklin, A. Tuominen, and M. Nikinmaa, “The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes,” J. Exp. Biol. 203, 3025–3031(2000).
[PubMed]

A. J. McGoron, C. H. Joiner, M. B. Palascak, W. J. Claussen, and R. S. Franco, “Dehydration of mature and immature sickle red blood cells during fast oxygenation/deoxygenation cycles: role of KCl cotransport and extracellular calcium,” Blood 95, 2164–2168 (2000).
[PubMed]

1995 (1)

G. d’Onofrio, R. Chirillo, G. Zini, G. Caenaro, M. Tommasi, and G. Micciulli, “Simultaneous measurement of reticulocyte and red blood cell indices in healthy subjects and patients with microcytic and macrocytic anemia,” Blood 85, 818–823 (1995).
[PubMed]

1986 (1)

J. C. Thompson and B. W. Manktelow, “Pathogenesis and red blood cell destruction in hemoglobinemic leptospirosis,” J. Comp. Pathol. 96, 529–540 (1986).
[Crossref] [PubMed]

1984 (1)

S. Christel and C. Little, “Morphological changes during heating of erythrocytes from stored human blood,” J. Therm. Biol. 9, 221–228 (1984).
[Crossref]

1980 (2)

N. Mochandas, M. R. Clark, M. S. Jacobs, and S. B. Shohet, “Analysis of factors regulating erythrocyte deformability,” J. Clin. Invest. 66, 563–573 (1980).
[Crossref]

W. Groner, N. Mohandas, and M. Bessis, “New optical technique for measuring erythrocyte deformability with the ektacytometer,” Clin. Chem. 26, 1435–1442 (1980).
[PubMed]

1974 (1)

I. A. Kabat, W. Leyko, B. Kwiatkowski, and I. Zakrzewska, “Osmotic properties and morphological changes of submicroscopic surface structures of mammalian red blood cells subjected to UV-irradiation in vitro,” Zentralbl. Bakteriol. Orig. B 159, 88–94 (1974).
[PubMed]

1973 (1)

A. K. Percy, E. Schmell, B. J. Earles, and W. J. Lennarz, “Phospholipid biosynthesis in the membranes of immature and mature red blood cells,” Biochemistry 12, 2456–2461 (1973).
[Crossref] [PubMed]

1968 (1)

J. W. Goodman, Introduction to Fourier Optics (McGraw-Hill, 1968).

1959 (1)

L. M. Lowenstein, “The Mammalian reticulocyte,” in International Review of Cytology, G.H.Bourne and J.F.Danielli, eds. (Academic, 1959), Vol. 8.
[Crossref] [PubMed]

1957 (1)

F. M. Gaffney, “Experimental hemolytic anemia with particular reference to the corpuscular hemoglobin concentrations of the erythrocytes,” Br. J. Haematol. 3, 311–319 (1957).
[Crossref] [PubMed]

1940 (1)

J. G. Stephens, “Surface and fragility differences between mature and immature red cells,” J. Physiol. 99, 30–48 (1940).
[PubMed]

Badizadegan, K.

Bai, J.-J.

Barbul, A.

Bareil, P. P.

Bessis, M.

W. Groner, N. Mohandas, and M. Bessis, “New optical technique for measuring erythrocyte deformability with the ektacytometer,” Clin. Chem. 26, 1435–1442 (1980).
[PubMed]

Best, C. A.

Bette-Bobillo, P.

Blanc, L.

Boss, D.

Caenaro, G.

Charrière, F.

Chiou, A.

Chirillo, R.

Choi, W.

Choi, Y.-S.

Y.-S. Choi and S. Lee, “Three-dimensional volumetric measurement of red blood cell motion using digital holographic microscopy,” Appl. Opt. 48, 2983–2990 (2009).
[Crossref] [PubMed]

Christel, S.

S. Christel and C. Little, “Morphological changes during heating of erythrocytes from stored human blood,” J. Therm. Biol. 9, 221–228 (1984).
[Crossref]

Clark, M. R.

N. Mochandas, M. R. Clark, M. S. Jacobs, and S. B. Shohet, “Analysis of factors regulating erythrocyte deformability,” J. Clin. Invest. 66, 563–573 (1980).
[Crossref]

Claussen, W. J.

Colomb, T.

Cuche, E.

d’Onofrio, G.

Dasari, R. R.

De Gassart, A.

De Nicola, S.

Depeursinge, C.

Ding, H.

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

Dobbe, J. G. G.

G. J. Streekstra1, J. G. G. Dobbe, and A. G. Hoekstra, “Quantification of the fraction poorly deformable red blood cells using ektacytometry,” Opt. Express 18, 14173–14182 (2010).
[Crossref]

Duval, P.-L.

Earles, B. J.

Emery, Y.

Fang-Yen, C.

Feld, M. S.

Ferraro, P.

Ferreira, C.

V. Mico, Z. Zalevsky, C. Ferreira, and J. García, “Super-resolution digital holographic microscopy for three-dimensional samples,” Opt. Express 16, 19260–19270 (2008).
[Crossref]

Finizio, A.

Franco, R. S.

Gaffney, F. M.

García, J.

V. Mico, Z. Zalevsky, C. Ferreira, and J. García, “Super-resolution digital holographic microscopy for three-dimensional samples,” Opt. Express 16, 19260–19270 (2008).
[Crossref]

Garcia-Rubio, L. H.

Géminard, C.

Goodman, J. W.

J. W. Goodman, Introduction to Fourier Optics (McGraw-Hill, 1968).

Grilli, S.

Groner, W.

W. Groner, N. Mohandas, and M. Bessis, “New optical technique for measuring erythrocyte deformability with the ektacytometer,” Clin. Chem. 26, 1435–1442 (1980).
[PubMed]

Henle, M. L.

Hoekstra, A. G.

G. J. Streekstra1, J. G. G. Dobbe, and A. G. Hoekstra, “Quantification of the fraction poorly deformable red blood cells using ektacytometry,” Opt. Express 18, 14173–14182 (2010).
[Crossref]

Hoffmann, A.

Jacobs, M. S.

N. Mochandas, M. R. Clark, M. S. Jacobs, and S. B. Shohet, “Analysis of factors regulating erythrocyte deformability,” J. Clin. Invest. 66, 563–573 (1980).
[Crossref]

Joiner, C. H.

Kabat, I. A.

Korenstein, R.

Krumbhaar, E. B.

Kuriabova, T.

Kwiatkowski, B.

Lecklin, T.

T. Lecklin, A. Tuominen, and M. Nikinmaa, “The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes,” J. Exp. Biol. 203, 3025–3031(2000).
[PubMed]

Lee, S.

Y.-S. Choi and S. Lee, “Three-dimensional volumetric measurement of red blood cell motion using digital holographic microscopy,” Appl. Opt. 48, 2983–2990 (2009).
[Crossref] [PubMed]

Lennarz, W. J.

Levine, A. J.

Leyko, W.

Li, Z.

B.-W. Yang and Z. Li, “Measuring microinteractions between coagulating red blood cells using optical tweezers,” Biomed. Opt. Express 1, 1217–1224 (2010).
[Crossref]

Little, C.

S. Christel and C. Little, “Morphological changes during heating of erythrocytes from stored human blood,” J. Therm. Biol. 9, 221–228 (1984).
[Crossref]

Lowenstein, L. M.

L. M. Lowenstein, “The Mammalian reticulocyte,” in International Review of Cytology, G.H.Bourne and J.F.Danielli, eds. (Academic, 1959), Vol. 8.
[Crossref] [PubMed]

Magistretti, P. J.

Manktelow, B. W.

J. C. Thompson and B. W. Manktelow, “Pathogenesis and red blood cell destruction in hemoglobinemic leptospirosis,” J. Comp. Pathol. 96, 529–540 (1986).
[Crossref] [PubMed]

Marquet, P.

McGoron, A. J.

Merola, F.

Micciulli, G.

Mico, V.

V. Mico, Z. Zalevsky, C. Ferreira, and J. García, “Super-resolution digital holographic microscopy for three-dimensional samples,” Opt. Express 16, 19260–19270 (2008).
[Crossref]

Mihailescu, M.

M. Mihailescu, “Natural quasi-periodic binary structure with focusing property in near-field diffraction pattern,” Opt. Express 18, 12526–12536 (2010).
[Crossref] [PubMed]

Milhous, W. K.

Mir, M.

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

M. Mir, Z. Wang, K. Tangella, and G. Popescu, “Phase cytometry: blood on a CD-ROM,” Opt. Express 17, 2579–2585 (2009).
[Crossref] [PubMed]

Mochandas, N.

N. Mochandas, M. R. Clark, M. S. Jacobs, and S. B. Shohet, “Analysis of factors regulating erythrocyte deformability,” J. Clin. Invest. 66, 563–573 (1980).
[Crossref]

Mohandas, N.

W. Groner, N. Mohandas, and M. Bessis, “New optical technique for measuring erythrocyte deformability with the ektacytometer,” Clin. Chem. 26, 1435–1442 (1980).
[PubMed]

Montfort, F.

Nikinmaa, M.

T. Lecklin, A. Tuominen, and M. Nikinmaa, “The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes,” J. Exp. Biol. 203, 3025–3031(2000).
[PubMed]

Oh, S.

Palascak, M. B.

Park, Y.

Park, Y. K.

Patel, J.

Paturzo, M.

Percy, A. K.

Popescu, G.

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

M. Mir, Z. Wang, K. Tangella, and G. Popescu, “Phase cytometry: blood on a CD-ROM,” Opt. Express 17, 2579–2585 (2009).
[Crossref] [PubMed]

Rancourt-Grenier, S.

Rappaz, B.

Reedy, J.

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

Schmell, E.

Serebrennikova, Y. M.

Seung, H. S.

Sheng, Y.

Shohet, S. B.

N. Mochandas, M. R. Clark, M. S. Jacobs, and S. B. Shohet, “Analysis of factors regulating erythrocyte deformability,” J. Clin. Invest. 66, 563–573 (1980).
[Crossref]

Song, S.

Stephens, J. G.

J. G. Stephens, “Surface and fragility differences between mature and immature red cells,” J. Physiol. 99, 30–48 (1940).
[PubMed]

Streekstra1, G. J.

G. J. Streekstra1, J. G. G. Dobbe, and A. G. Hoekstra, “Quantification of the fraction poorly deformable red blood cells using ektacytometry,” Opt. Express 18, 14173–14182 (2010).
[Crossref]

Tangella, K.

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

M. Mir, Z. Wang, K. Tangella, and G. Popescu, “Phase cytometry: blood on a CD-ROM,” Opt. Express 17, 2579–2585 (2009).
[Crossref] [PubMed]

Thompson, J. C.

J. C. Thompson and B. W. Manktelow, “Pathogenesis and red blood cell destruction in hemoglobinemic leptospirosis,” J. Comp. Pathol. 96, 529–540 (1986).
[Crossref] [PubMed]

Tommasi, M.

Tuominen, A.

T. Lecklin, A. Tuominen, and M. Nikinmaa, “The adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes,” J. Exp. Biol. 203, 3025–3031(2000).
[PubMed]

Vidal, M.

Wang, Z.

M. Mir, H. Ding, Z. Wang, J. Reedy, K. Tangella, and G. Popescu, “Blood screening using diffraction phase cytometry,” J. Biomed. Opt. 15, 027016 (2010).
[Crossref] [PubMed]

M. Mir, Z. Wang, K. Tangella, and G. Popescu, “Phase cytometry: blood on a CD-ROM,” Opt. Express 17, 2579–2585 (2009).
[Crossref] [PubMed]

Wei, M.-T.

Yang, B.-W.

B.-W. Yang and Z. Li, “Measuring microinteractions between coagulating red blood cells using optical tweezers,” Biomed. Opt. Express 1, 1217–1224 (2010).
[Crossref]

Zakrzewska, I.

Zalevsky, Z.

V. Mico, Z. Zalevsky, C. Ferreira, and J. García, “Super-resolution digital holographic microscopy for three-dimensional samples,” Opt. Express 16, 19260–19270 (2008).
[Crossref]

Zini, G.

Appl. Opt. (1)

Y.-S. Choi and S. Lee, “Three-dimensional volumetric measurement of red blood cell motion using digital holographic microscopy,” Appl. Opt. 48, 2983–2990 (2009).
[Crossref] [PubMed]

Biochemistry (1)

Biomed. Opt. Express (1)

B.-W. Yang and Z. Li, “Measuring microinteractions between coagulating red blood cells using optical tweezers,” Biomed. Opt. Express 1, 1217–1224 (2010).
[Crossref]

Blood (2)

Blood Cells Mol. Dis. (2)

Br. J. Haematol. (1)

Clin. Chem. (1)

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Fig. 1

(a) Classical bright-field microscopy on a slide using chromatographic substances to differentiate the cells; (b) hologram of the same slide in the region of interest recorded using off-axis DHM setup; (c) 3D image in false colors of the reconstructed cells from the previous hologram. The IRBCs are highlighted in all images.

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Fig. 2

IRBCs and MRBCs observed in classical DIC microscopy without chromatographic substances. (a) Sample 3, (c) Sample 13; and in DHM (b) Sample 3, (d) Sample 13. The IRBCs are highlighted in all images.

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Fig. 3

Holograms from regions with at least one IRBC recorded at different distances between the microscope objective and sample: (a) Sample 27 at $z_{1}$ , (b) Sample 27 at $z_{2}$ , (c) Sample 19 at $z_{3}$ , (d) Sample 19 at $z_{4}$ . The IRBCs are highlighted in all images.

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Fig. 4

Diffraction pattern (with reference beam obstructed in DHM setup) from an MRBC (top) and an IRBC (bottom) recorded at different distances between the microscope objective and Sample 27 in the same region as in Fig. 3 at (a) $z = 9 μm$ , (b) $z = 6 μm$ , (c) $z = 3 μm$ , (d) $z = 0 μm$ , (e) $z = - 6 μm$ .

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Fig. 5

Simulated diffraction pattern from MRBC (top) and IRBC (bottom) at the same distances between sample and objective as in Fig. 4.

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Fig. 6

Central intensity dependence on (a) equatorial radius at $z_{i}$ , (b) equatorial radius at $z_{i + 1}$ , (c) polar radius at $z_{i}$ , (d) polar radius at $z_{i + 1}$ .