Abstract

During a sickle cell crisis in sickle cell anemia patients, deoxygenated red blood cells may change their mechanical properties and block small blood vessels, causing pain, local tissue damage, and possibly organ failure. Measuring the structural and morphological changes in sickle cells is important for understanding the factors contributing to vessel blockage and for developing an effective treatment. In this work, we image blood cells from sickle cell anemia patients using spectrally encoded flow cytometry, and analyze the interference patterns between reflections from the cell membranes. Using a numerical simulation for calculating the interference pattern obtained from a model of a red blood cell, we propose an analytical expression for the three-dimensional shape of characteristic sickle cells and compare our results to a previously suggested model. Our imaging approach offers new means for analyzing the morphology of sickle cells, and could be useful for studying their unique physiological and biomechanical properties.

© 2017 Optical Society of America

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References

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  4. G. W. Christoph, J. Hofrichter, and W. A. Eaton, “Understanding the shape of sickled red cells,” Biophys. J. 88(2), 1371–1376 (2005).
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  5. L. W. Diggs and J. Bibb, “The erythrocyte in sickle cell anemia: Morphology, size, hemoglobin content, fragility and sedimentation rate,” J. Am. Med. Assoc. 112(8), 695–701 (1939).
    [Crossref]
  6. R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
    [Crossref] [PubMed]
  7. R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
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    [Crossref] [PubMed]
  9. G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
    [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  24. X. Li, P. M. Vlahovska, and G. E. Karniadakis, “Continuum- and particle-based modeling of shapes and dynamics of red blood cells in health and disease,” Soft Matter 9(1), 28–37 (2013).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  26. M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
    [Crossref] [PubMed]
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    [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]

2017 (1)

X. Li, M. Dao, G. Lykotrafitis, and G. E. Karniadakis, “Biomechanics and biorheology of red blood cells in sickle cell anemia,” J. Biomech. 50, 34–41 (2017).
[Crossref] [PubMed]

2015 (1)

2014 (2)

G. Tomaiuolo, “Biomechanical properties of red blood cells in health and disease towards microfluidics,” Biomicrofluidics 8(5), 051501 (2014).
[Crossref] [PubMed]

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
[Crossref] [PubMed]

2013 (2)

K. Kim, K. S. Kim, H. Park, J. C. Ye, and Y. Park, “Real-time visualization of 3-D dynamic microscopic objects using optical diffraction tomography,” Opt. Express 21(26), 32269–32278 (2013).
[Crossref] [PubMed]

X. Li, P. M. Vlahovska, and G. E. Karniadakis, “Continuum- and particle-based modeling of shapes and dynamics of red blood cells in health and disease,” Soft Matter 9(1), 28–37 (2013).
[Crossref] [PubMed]

2012 (3)

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

L. Golan, D. Yeheskely-Hayon, L. Minai, E. J. Dann, and D. Yelin, “Noninvasive imaging of flowing blood cells using label-free spectrally encoded flow cytometry,” Biomed. Opt. Express 3(6), 1455–1464 (2012).
[Crossref] [PubMed]

H. Lei and G. E. Karniadakis, “Quantifying the rheological and hemodynamic characteristics of sickle cell anemia,” Biophys. J. 102(2), 185–194 (2012).
[Crossref] [PubMed]

2011 (2)

J. L. Maciaszek, B. Andemariam, and G. Lykotrafitis, “Microelasticity of red blood cells in sickle cell disease,” J. Strain Anal. Eng. Des. 46(5), 368–379 (2011).
[Crossref]

N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
[Crossref]

2010 (1)

2005 (1)

G. W. Christoph, J. Hofrichter, and W. A. Eaton, “Understanding the shape of sickled red cells,” Biophys. J. 88(2), 1371–1376 (2005).
[Crossref] [PubMed]

2003 (1)

Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
[Crossref] [PubMed]

1996 (1)

M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
[Crossref] [PubMed]

1994 (2)

T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
[Crossref] [PubMed]

1990 (1)

R. E. Samuel, E. D. Salmon, and R. W. Briehl, “Nucleation and growth of fibres and gel formation in sickle cell haemoglobin,” Nature 345(6278), 833–835 (1990).
[Crossref] [PubMed]

1989 (1)

V. Bennett, “The spectrin-actin junction of erythrocyte membrane skeletons,” Biochim. Biophys. Acta 988(1), 107–121 (1989).
[Crossref] [PubMed]

1987 (1)

G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
[PubMed]

1984 (1)

E. Evans, N. Mohandas, and A. Leung, “Static and dynamic rigidities of normal and sickle erythrocytes. Major influence of cell hemoglobin concentration,” J. Clin. Invest. 73(2), 477–488 (1984).
[Crossref] [PubMed]

1983 (1)

D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
[Crossref] [PubMed]

1980 (1)

R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
[Crossref] [PubMed]

1979 (2)

R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
[PubMed]

B. E. Glader, R. D. Propper, and G. R. Buchanan, “Microcytosis Associated with Sickle Cell Anemia,” Am. J. Clin. Pathol. 72(1), 63–64 (1979).
[Crossref] [PubMed]

1972 (2)

E. Evans and Y. C. Fung, “Improved Measurements of the Erythrocyte Geometry,” Microvasc. Res. 4(4), 335–347 (1972).
[Crossref] [PubMed]

B. Wranne, R. D. Woodson, and J. C. Detter, “Bohr Effect: interaction between H +, CO2, and 2,3-DPG in fresh and stored blood,” J. Appl. Physiol. 32(6), 749–754 (1972).
[PubMed]

1957 (1)

V. M. Ingram, “Gene mutations in human haemoglobin: the chemical difference between normal and sickle cell haemoglobin,” Nature 180(4581), 326–328 (1957).
[Crossref] [PubMed]

1949 (1)

L. Pauling, H. A. Itano, S. Singer, and I. Wells, “Sickle Cell Anemia a Molecular Disease,” Science 110(2865), 543–548 (1949).
[Crossref] [PubMed]

1939 (1)

L. W. Diggs and J. Bibb, “The erythrocyte in sickle cell anemia: Morphology, size, hemoglobin content, fragility and sedimentation rate,” J. Am. Med. Assoc. 112(8), 695–701 (1939).
[Crossref]

Altmeyer, P.

M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
[Crossref] [PubMed]

Andemariam, B.

J. L. Maciaszek, B. Andemariam, and G. Lykotrafitis, “Microelasticity of red blood cells in sickle cell disease,” J. Strain Anal. Eng. Des. 46(5), 368–379 (2011).
[Crossref]

Asakura, K.

T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

Asakura, T.

T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

Baez, S.

D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
[Crossref] [PubMed]

Baier, V.

M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
[Crossref] [PubMed]

Ballas, S. K.

Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
[Crossref] [PubMed]

Barabino, G. A.

G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
[PubMed]

Bennett, V.

V. Bennett, “The spectrin-actin junction of erythrocyte membrane skeletons,” Biochim. Biophys. Acta 988(1), 107–121 (1989).
[Crossref] [PubMed]

Bibb, J.

L. W. Diggs and J. Bibb, “The erythrocyte in sickle cell anemia: Morphology, size, hemoglobin content, fragility and sedimentation rate,” J. Am. Med. Assoc. 112(8), 695–701 (1939).
[Crossref]

Brambilla, D. J.

O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
[Crossref] [PubMed]

Briehl, R. W.

R. E. Samuel, E. D. Salmon, and R. W. Briehl, “Nucleation and growth of fibres and gel formation in sickle cell haemoglobin,” Nature 345(6278), 833–835 (1990).
[Crossref] [PubMed]

Buchanan, G. R.

B. E. Glader, R. D. Propper, and G. R. Buchanan, “Microcytosis Associated with Sickle Cell Anemia,” Am. J. Clin. Pathol. 72(1), 63–64 (1979).
[Crossref] [PubMed]

Byun, H.

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

Castro, O.

O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
[Crossref] [PubMed]

Choi, W.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
[Crossref] [PubMed]

Christoph, G. W.

G. W. Christoph, J. Hofrichter, and W. A. Eaton, “Understanding the shape of sickled red cells,” Biophys. J. 88(2), 1371–1376 (2005).
[Crossref] [PubMed]

Dann, E. J.

Dao, M.

X. Li, M. Dao, G. Lykotrafitis, and G. E. Karniadakis, “Biomechanics and biorheology of red blood cells in sickle cell anemia,” J. Biomech. 50, 34–41 (2017).
[Crossref] [PubMed]

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

Dasari, R. R.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
[Crossref] [PubMed]

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

Detter, J. C.

B. Wranne, R. D. Woodson, and J. C. Detter, “Bohr Effect: interaction between H +, CO2, and 2,3-DPG in fresh and stored blood,” J. Appl. Physiol. 32(6), 749–754 (1972).
[PubMed]

Diez-Silva, M.

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

Diggs, L. W.

L. W. Diggs and J. Bibb, “The erythrocyte in sickle cell anemia: Morphology, size, hemoglobin content, fragility and sedimentation rate,” J. Am. Med. Assoc. 112(8), 695–701 (1939).
[Crossref]

Eaton, J. W.

R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
[Crossref] [PubMed]

Eaton, W. A.

G. W. Christoph, J. Hofrichter, and W. A. Eaton, “Understanding the shape of sickled red cells,” Biophys. J. 88(2), 1371–1376 (2005).
[Crossref] [PubMed]

Eskin, S. G.

G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
[PubMed]

Evans, E.

E. Evans, N. Mohandas, and A. Leung, “Static and dynamic rigidities of normal and sickle erythrocytes. Major influence of cell hemoglobin concentration,” J. Clin. Invest. 73(2), 477–488 (1984).
[Crossref] [PubMed]

E. Evans and Y. C. Fung, “Improved Measurements of the Erythrocyte Geometry,” Microvasc. Res. 4(4), 335–347 (1972).
[Crossref] [PubMed]

Fabry, M. E.

D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
[Crossref] [PubMed]

Fung, Y. C.

E. Evans and Y. C. Fung, “Improved Measurements of the Erythrocyte Geometry,” Microvasc. Res. 4(4), 335–347 (1972).
[Crossref] [PubMed]

Glader, B. E.

B. E. Glader, R. D. Propper, and G. R. Buchanan, “Microcytosis Associated with Sickle Cell Anemia,” Am. J. Clin. Pathol. 72(1), 63–64 (1979).
[Crossref] [PubMed]

Golan, L.

Hamza, B.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
[Crossref] [PubMed]

Hearne, L.

Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
[Crossref] [PubMed]

Hebbel, R. P.

R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
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H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
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H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
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M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
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G. W. Christoph, J. Hofrichter, and W. A. Eaton, “Understanding the shape of sickled red cells,” Biophys. J. 88(2), 1371–1376 (2005).
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R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
[PubMed]

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Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
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V. M. Ingram, “Gene mutations in human haemoglobin: the chemical difference between normal and sickle cell haemoglobin,” Nature 180(4581), 326–328 (1957).
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Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
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Irimia, D.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
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L. Pauling, H. A. Itano, S. Singer, and I. Wells, “Sickle Cell Anemia a Molecular Disease,” Science 110(2865), 543–548 (1949).
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R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
[Crossref] [PubMed]

Karniadakis, G. E.

X. Li, M. Dao, G. Lykotrafitis, and G. E. Karniadakis, “Biomechanics and biorheology of red blood cells in sickle cell anemia,” J. Biomech. 50, 34–41 (2017).
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X. Li, P. M. Vlahovska, and G. E. Karniadakis, “Continuum- and particle-based modeling of shapes and dynamics of red blood cells in health and disease,” Soft Matter 9(1), 28–37 (2013).
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H. Lei and G. E. Karniadakis, “Quantifying the rheological and hemodynamic characteristics of sickle cell anemia,” Biophys. J. 102(2), 185–194 (2012).
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D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
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M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
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Kim, K. S.

Kim-Shapiro, D. B.

Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
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Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
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O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
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H. Lei and G. E. Karniadakis, “Quantifying the rheological and hemodynamic characteristics of sickle cell anemia,” Biophys. J. 102(2), 185–194 (2012).
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Leung, A.

E. Evans, N. Mohandas, and A. Leung, “Static and dynamic rigidities of normal and sickle erythrocytes. Major influence of cell hemoglobin concentration,” J. Clin. Invest. 73(2), 477–488 (1984).
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Li, X.

X. Li, M. Dao, G. Lykotrafitis, and G. E. Karniadakis, “Biomechanics and biorheology of red blood cells in sickle cell anemia,” J. Biomech. 50, 34–41 (2017).
[Crossref] [PubMed]

X. Li, P. M. Vlahovska, and G. E. Karniadakis, “Continuum- and particle-based modeling of shapes and dynamics of red blood cells in health and disease,” Soft Matter 9(1), 28–37 (2013).
[Crossref] [PubMed]

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Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
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Lykotrafitis, G.

X. Li, M. Dao, G. Lykotrafitis, and G. E. Karniadakis, “Biomechanics and biorheology of red blood cells in sickle cell anemia,” J. Biomech. 50, 34–41 (2017).
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J. L. Maciaszek, B. Andemariam, and G. Lykotrafitis, “Microelasticity of red blood cells in sickle cell disease,” J. Strain Anal. Eng. Des. 46(5), 368–379 (2011).
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Maciaszek, J. L.

J. L. Maciaszek, B. Andemariam, and G. Lykotrafitis, “Microelasticity of red blood cells in sickle cell disease,” J. Strain Anal. Eng. Des. 46(5), 368–379 (2011).
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Martel, J.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
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T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

McIntire, L. V.

G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
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O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
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Minai, L.

Mohandas, N.

E. Evans, N. Mohandas, and A. Leung, “Static and dynamic rigidities of normal and sickle erythrocytes. Major influence of cell hemoglobin concentration,” J. Clin. Invest. 73(2), 477–488 (1984).
[Crossref] [PubMed]

Moldow, C. F.

R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
[Crossref] [PubMed]

Nagel, R. L.

D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
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T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
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T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
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Park, Y.

K. Kim, K. S. Kim, H. Park, J. C. Ye, and Y. Park, “Real-time visualization of 3-D dynamic microscopic objects using optical diffraction tomography,” Opt. Express 21(26), 32269–32278 (2013).
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H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
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L. Pauling, H. A. Itano, S. Singer, and I. Wells, “Sickle Cell Anemia a Molecular Disease,” Science 110(2865), 543–548 (1949).
[Crossref] [PubMed]

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H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
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O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
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B. E. Glader, R. D. Propper, and G. R. Buchanan, “Microcytosis Associated with Sickle Cell Anemia,” Am. J. Clin. Pathol. 72(1), 63–64 (1979).
[Crossref] [PubMed]

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T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

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M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
[Crossref] [PubMed]

Rosse, W. F.

O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
[Crossref] [PubMed]

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R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
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R. E. Samuel, E. D. Salmon, and R. W. Briehl, “Nucleation and growth of fibres and gel formation in sickle cell haemoglobin,” Nature 345(6278), 833–835 (1990).
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R. E. Samuel, E. D. Salmon, and R. W. Briehl, “Nucleation and growth of fibres and gel formation in sickle cell haemoglobin,” Nature 345(6278), 833–835 (1990).
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Satterwhite, L. L.

N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
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Schwartz, E.

T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

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G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
[PubMed]

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N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
[Crossref]

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L. Pauling, H. A. Itano, S. Singer, and I. Wells, “Sickle Cell Anemia a Molecular Disease,” Science 110(2865), 543–548 (1949).
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Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
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O. S. Platt, D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug, “Mortality In Sickle Cell Disease. Life Expectancy and Risk Factors for Early Death,” N. Engl. J. Med. 330(23), 1639–1644 (1994).
[Crossref] [PubMed]

Stücker, M.

M. Stücker, V. Baier, T. Reuther, K. Hoffmann, K. Kellam, and P. Altmeyer, “Capillary blood cell velocity in human skin capillaries located perpendicularly to the skin surface: measured by a new laser Doppler anemometer,” Microvasc. Res. 52(2), 188–192 (1996).
[Crossref] [PubMed]

Sung, Y.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
[Crossref] [PubMed]

Suresh, S.

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

Telen, M. J.

N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
[Crossref]

Tomaiuolo, G.

G. Tomaiuolo, “Biomechanical properties of red blood cells in health and disease towards microfluidics,” Biomicrofluidics 8(5), 051501 (2014).
[Crossref] [PubMed]

Tomassini, N.

T. Asakura, J. A. Mattiello, K. Obata, K. Asakura, M. P. Reilly, N. Tomassini, E. Schwartz, and K. Ohene-Frempong, “Partially oxygenated sickled cells: Sickle-shaped red cells found in circulating blood of patients with sickle cell disease,” Proc. Natl. Acad. Sci. U.S.A. 91(26), 12589–12593 (1994).
[Crossref] [PubMed]

Truskey, G. A.

N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
[Crossref]

Udden, M.

G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
[PubMed]

Vlahovska, P. M.

X. Li, P. M. Vlahovska, and G. E. Karniadakis, “Continuum- and particle-based modeling of shapes and dynamics of red blood cells in health and disease,” Soft Matter 9(1), 28–37 (2013).
[Crossref] [PubMed]

Warren, R.

R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
[PubMed]

Wax, A.

N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
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L. Pauling, H. A. Itano, S. Singer, and I. Wells, “Sickle Cell Anemia a Molecular Disease,” Science 110(2865), 543–548 (1949).
[Crossref] [PubMed]

White, J. G.

R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
[Crossref] [PubMed]

Windisch, P.

D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
[Crossref] [PubMed]

Wise, G.

R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
[PubMed]

Woodson, R. D.

B. Wranne, R. D. Woodson, and J. C. Detter, “Bohr Effect: interaction between H +, CO2, and 2,3-DPG in fresh and stored blood,” J. Appl. Physiol. 32(6), 749–754 (1972).
[PubMed]

Wranne, B.

B. Wranne, R. D. Woodson, and J. C. Detter, “Bohr Effect: interaction between H +, CO2, and 2,3-DPG in fresh and stored blood,” J. Appl. Physiol. 32(6), 749–754 (1972).
[PubMed]

Yamada, O.

R. P. Hebbel, O. Yamada, C. F. Moldow, H. S. Jacob, J. G. White, and J. W. Eaton, “Abnormal adherence of sickle erythrocytes to cultured vascular endothelium: Possible mechanism for microvascular occlusion in sickle cell disease,” J. Clin. Invest. 65(1), 154–160 (1980).
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Yaqoob, Z.

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel,” Phys. Rev. Appl. 1(1), 014002 (2014).
[Crossref] [PubMed]

Ye, J. C.

Yeheskely-Hayon, D.

Yelin, D.

Zeidan, A.

Acta Biomater. (1)

H. Byun, T. R. Hillman, J. M. Higgins, M. Diez-Silva, Z. Peng, M. Dao, R. R. Dasari, S. Suresh, and Y. Park, “Optical measurement of biomechanical properties of individual erythrocytes from a sickle cell patient,” Acta Biomater. 8(11), 4130–4138 (2012).
[Crossref] [PubMed]

Am. J. Clin. Pathol. (1)

B. E. Glader, R. D. Propper, and G. R. Buchanan, “Microcytosis Associated with Sickle Cell Anemia,” Am. J. Clin. Pathol. 72(1), 63–64 (1979).
[Crossref] [PubMed]

Biochim. Biophys. Acta (1)

V. Bennett, “The spectrin-actin junction of erythrocyte membrane skeletons,” Biochim. Biophys. Acta 988(1), 107–121 (1989).
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Biomed. Opt. Express (2)

Biomicrofluidics (1)

G. Tomaiuolo, “Biomechanical properties of red blood cells in health and disease towards microfluidics,” Biomicrofluidics 8(5), 051501 (2014).
[Crossref] [PubMed]

Biophys. J. (3)

G. W. Christoph, J. Hofrichter, and W. A. Eaton, “Understanding the shape of sickled red cells,” Biophys. J. 88(2), 1371–1376 (2005).
[Crossref] [PubMed]

H. Lei and G. E. Karniadakis, “Quantifying the rheological and hemodynamic characteristics of sickle cell anemia,” Biophys. J. 102(2), 185–194 (2012).
[Crossref] [PubMed]

Z. Huang, L. Hearne, C. E. Irby, S. B. King, S. K. Ballas, and D. B. Kim-Shapiro, “Kinetics of increased deformability of deoxygenated sickle cells upon oxygenation,” Biophys. J. 85(4), 2374–2383 (2003).
[Crossref] [PubMed]

Blood (2)

R. Hoover, R. Rubin, G. Wise, and R. Warren, “Adhesion of normal and sickle erythrocytes to endothelial monolayer cultures,” Blood 54(4), 872–876 (1979).
[PubMed]

G. A. Barabino, L. V. McIntire, S. G. Eskin, D. A. Sears, and M. Udden, “Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow,” Blood 70(1), 152–157 (1987).
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J. Am. Med. Assoc. (1)

L. W. Diggs and J. Bibb, “The erythrocyte in sickle cell anemia: Morphology, size, hemoglobin content, fragility and sedimentation rate,” J. Am. Med. Assoc. 112(8), 695–701 (1939).
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J. Appl. Physiol. (1)

B. Wranne, R. D. Woodson, and J. C. Detter, “Bohr Effect: interaction between H +, CO2, and 2,3-DPG in fresh and stored blood,” J. Appl. Physiol. 32(6), 749–754 (1972).
[PubMed]

J. Biomech. (1)

X. Li, M. Dao, G. Lykotrafitis, and G. E. Karniadakis, “Biomechanics and biorheology of red blood cells in sickle cell anemia,” J. Biomech. 50, 34–41 (2017).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

N. T. Shaked, L. L. Satterwhite, M. J. Telen, G. A. Truskey, and A. Wax, “Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry,” J. Biomed. Opt. 16(3), 030506 (2011).
[Crossref]

J. Clin. Invest. (3)

D. K. Kaul, M. E. Fabry, P. Windisch, S. Baez, and R. L. Nagel, “Erythrocytes in Sickle Cell Anemia Are Heterogeneous in Their Rheological and Hemodynamic Characteristics,” J. Clin. Invest. 72(1), 22–31 (1983).
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Figures (5)

Fig. 1
Fig. 1 Schematic of SEFC system for confocal imaging of flowing blood cells. SLD: super-luminescence diode array. L1-L8: Achromatic lenses. BS: beam splitter. G: diffraction grating. DM: dichroic mirror.
Fig. 2
Fig. 2 Typical SEFC image of flowing blood cells. 5-times magnified views of selected cells are shown in the insets. w - white blood cell; n - normal red blood cell; s - sickle cell; g - granular cells; t - target-like cell.
Fig. 3
Fig. 3 Selected exemplary images of sickle cells obtained from (a) patient #1 and (b) patient #2. (c) Normal cells from patient #2. Left (right) hand panel of each pair of images corresponds to SEFC (brightfield) channel.
Fig. 4
Fig. 4 Shape modeling according to ref (23) and the resulting simulated interference patterns. (a) Elongated cell. (b) Sickle cell. (c) Granular cell.
Fig. 5
Fig. 5 Experimental images and simulated morphologies of (a) two elongated sickle cells and (b) a normal cell.

Equations (3)

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f(x,y)= a 0 + a 1 x 2 + a 2 y 2 + a 3 x 4 + a 4 y 4 + a 5 x 2 y 2 ,
( x/ b 1 ) p + ( y/ b 2 ) p =1.
g(x,y)=( a 0 + a 1 x 2 + a 2 y 2 + a 3 x 4 + a 4 y 4 + a 5 x 2 y 2 )( 1 c 1 e x 2 c 2 y 2 c 3 ).

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