Abstract

Clinical diagnosis of malaria suffers from poor specificity leading to overtreatment with antimalarial medications. Alternatives, like blood smear microscopy or antigen-based tests, require a blood sample. We investigate in vivo microscopy as a needle-free malaria diagnostic. Two optical signatures, birefringence and absorbance, of the endogenous malaria by-product hemozoin were evaluated as in vivo optical biomarkers. Hemozoin birefringence was difficult to detect in highly scattering tissue; however, hemozoin absorbance was observed in increasingly complex biological environments and detectable over a clinically-relevant range of parasitemia in vivo in a P. yoelii-infected mouse model of malaria.

© 2015 Optical Society of America

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2014 (2)

E. Y. Lukianova-Hleb, K. M. Campbell, P. E. Constantinou, J. Braam, J. S. Olson, R. E. Ware, D. J. Sullivan, and D. O. Lapotko, “Hemozoin-generated vapor nanobubbles for transdermal reagent- and needle-free detection of malaria,” Proc. Natl. Acad. Sci. U.S.A. 111(3), 900–905 (2014).
[Crossref] [PubMed]

B. Yu, A. Shah, V. K. Nagarajan, and D. G. Ferris, “Diffuse reflectance spectroscopy of epithelial tissue with a smart fiber-optic probe,” Biomed. Opt. Express 5(3), 675–689 (2014).
[Crossref] [PubMed]

2013 (3)

A. García-Hernández, R. Roldán-Marín, P. Iglesias-Garcia, and J. Malvehy, “In vivo noninvasive imaging of healthy lower lip mucosa: a correlation study between high-definition optical coherence tomography, reflectance confocal microscopy, and histology,” Dermatol. Res. Pract. 2013, 205256 (2013).
[Crossref] [PubMed]

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
[Crossref] [PubMed]

A. Butykai, A. Orbán, V. Kocsis, D. Szaller, S. Bordács, E. Tátrai-Szekeres, L. F. Kiss, A. Bóta, B. G. Vértessy, T. Zelles, and I. Kézsmárki, “Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis,” Sci. Rep. 3, 1431 (2013).
[Crossref] [PubMed]

2012 (3)

F. Paize, R. Sarginson, N. Makwana, P. B. Baines, A. P. J. Thomson, I. Sinha, C. A. Hart, A. Riordan, K. C. Hawkins, E. D. Carrol, and C. M. Parry, “Changes in the sublingual microcirculation and endothelial adhesion molecules during the course of severe meningococcal disease treated in the paediatric intensive care unit,” Intensive Care Med. 38(5), 863–871 (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]

T. P. Santisakultarm, N. R. Cornelius, N. Nishimura, A. I. Schafer, R. T. Silver, P. C. Doerschuk, W. L. Olbricht, and C. B. Schaffer, “In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice,” Am. J. Physiol. Heart Circ. Physiol. 302(7), H1367–H1377 (2012).
[Crossref] [PubMed]

2011 (1)

2010 (1)

D. M. Newman, R. J. Matelon, M. L. Wears, and L. B. Savage, “The in vivo diagnosis of malaria: Feasibility study into a magneto-optic fingertip probe,” IEEE J. Sel. Top. Quantum Electron. 16(3), 573–580 (2010).
[Crossref]

2009 (2)

T. Frosch, S. Koncarevic, K. Becker, and J. Popp, “Morphology-sensitive Raman modes of the malaria pigment hemozoin,” Analyst (Lond.) 134(6), 1126–1132 (2009).
[Crossref] [PubMed]

J. A. Rowe, A. Claessens, R. A. Corrigan, and M. Arman, “Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications,” Expert Rev. Mol. Med. 11, e16 (2009).
[Crossref] [PubMed]

2008 (4)

T. J. Egan, “Recent advances in understanding the mechanism of hemozoin (malaria pigment) formation,” J. Inorg. Biochem. 102(5-6), 1288–1299 (2008).
[Crossref] [PubMed]

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
[Crossref] [PubMed]

I. Pavlova, C. R. Weber, R. A. Schwarz, M. Williams, A. El-Naggar, A. Gillenwater, and R. Richards-Kortum, “Monte Carlo model to describe depth selective fluorescence spectra of epithelial tissue: applications for diagnosis of oral precancer,” J. Biomed. Opt. 13(6), 064012 (2008).
[Crossref] [PubMed]

S. McGee, J. Mirkovic, V. Mardirossian, A. Elackattu, C.-C. Yu, S. Kabani, G. Gallagher, R. Pistey, L. Galindo, K. Badizadegan, Z. Wang, R. Dasari, M. S. Feld, and G. Grillone, “Model-based spectroscopic analysis of the oral cavity: impact of anatomy,” J. Biomed. Opt. 13(6), 064034 (2008).
[Crossref] [PubMed]

2007 (2)

H. Rodulfo, M. De Donato, R. Mora, L. González, and C. E. Contreras, “Comparison of the diagnosis of malaria by microscopy, immunochromatography and PCR in endemic areas of Venezuela,” Braz. J. Med. Biol. Res. 40(4), 535–543 (2007).
[Crossref] [PubMed]

T. Hänscheid, T. J. Egan, and M. P. Grobusch, “Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator,” Lancet Infect. Dis. 7(10), 675–685 (2007).
[Crossref] [PubMed]

2006 (1)

M. E. Rafael, T. Taylor, A. Magill, Y. W. Lim, F. Girosi, and R. Allan, “Reducing the burden of childhood malaria in Africa: the role of improved,” Nature 444(Suppl 1), 39–48 (2006).
[Crossref] [PubMed]

2005 (1)

2004 (3)

A. L. L. Clark, A. Gillenwater, R. Alizadeh-Naderi, A. K. El-Naggar, and R. Richards-Kortum, “Detection and diagnosis of oral neoplasia with an optical coherence microscope,” J. Biomed. Opt. 9(6), 1271–1280 (2004).
[Crossref] [PubMed]

P. F. Scholl, D. Kongkasuriyachai, P. A. Demirev, A. B. Feldman, J. S. Lin, D. J. Sullivan, and N. Kumar, “Rapid detection of malaria infection in vivo by laser desorption mass spectrometry,” Am. J. Trop. Med. Hyg. 71(5), 546–551 (2004).
[PubMed]

M. M. Stevenson and E. M. Riley, “Innate immunity to malaria,” Nat. Rev. Immunol. 4(3), 169–180 (2004).
[Crossref] [PubMed]

2003 (1)

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
[Crossref] [PubMed]

2002 (2)

T. C. Minh, S. Ichioka, K. Harii, M. Shibata, J. Ando, and T. Nakatsuka, “Dorsal bipedicled island skin flap: a new flap model in mice,” Scand. J. Plast. Reconstr. Surg. Hand Surg. 36(5), 262–267 (2002).
[Crossref] [PubMed]

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

2001 (1)

T. Planche, S. Krishna, M. Kombila, K. Engel, J. F. Faucher, E. Ngou-Milama, and P. G. Kremsner, “Comparison of methods for the rapid laboratory assessment of children with malaria,” Am. J. Trop. Med. Hyg. 65(5), 599–602 (2001).
[PubMed]

2000 (1)

M. Ho, M. J. Hickey, A. G. Murray, G. Andonegui, and P. Kubes, “Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment,” J. Exp. Med. 192(8), 1205–1212 (2000).
[Crossref] [PubMed]

1999 (2)

J. Kopacz and N. Kumar, “Murine γ δ T Lymphocytes Elicited during Plasmodium yoelii Infection Respond to Plasmodium Heat Shock Proteins,” Infect. Immun. 67(1), 57–63 (1999).
[PubMed]

W. M. White, M. Rajadhyaksha, S. González, R. L. Fabian, and R. R. Anderson, “Noninvasive imaging of human oral mucosa in vivo by confocal reflectance microscopy,” Laryngoscope 109(10), 1709–1717 (1999).
[Crossref] [PubMed]

1991 (1)

1967 (1)

H. Wayland and P. C. Johnson, “Erythrocyte velocity measurement in microvessels by a two-slit photometric method,” J. Appl. Physiol. 22(2), 333–337 (1967).
[PubMed]

Ali, A. S.

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
[Crossref] [PubMed]

Alizadeh-Naderi, R.

A. L. L. Clark, A. Gillenwater, R. Alizadeh-Naderi, A. K. El-Naggar, and R. Richards-Kortum, “Detection and diagnosis of oral neoplasia with an optical coherence microscope,” J. Biomed. Opt. 9(6), 1271–1280 (2004).
[Crossref] [PubMed]

Allan, R.

M. E. Rafael, T. Taylor, A. Magill, Y. W. Lim, F. Girosi, and R. Allan, “Reducing the burden of childhood malaria in Africa: the role of improved,” Nature 444(Suppl 1), 39–48 (2006).
[Crossref] [PubMed]

Allen, J. E.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Anderson, R. R.

W. M. White, M. Rajadhyaksha, S. González, R. L. Fabian, and R. R. Anderson, “Noninvasive imaging of human oral mucosa in vivo by confocal reflectance microscopy,” Laryngoscope 109(10), 1709–1717 (1999).
[Crossref] [PubMed]

Ando, J.

T. C. Minh, S. Ichioka, K. Harii, M. Shibata, J. Ando, and T. Nakatsuka, “Dorsal bipedicled island skin flap: a new flap model in mice,” Scand. J. Plast. Reconstr. Surg. Hand Surg. 36(5), 262–267 (2002).
[Crossref] [PubMed]

Andonegui, G.

M. Ho, M. J. Hickey, A. G. Murray, G. Andonegui, and P. Kubes, “Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment,” J. Exp. Med. 192(8), 1205–1212 (2000).
[Crossref] [PubMed]

Angiuoli, S. V.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Arifler, D.

Arman, M.

J. A. Rowe, A. Claessens, R. A. Corrigan, and M. Arman, “Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications,” Expert Rev. Mol. Med. 11, e16 (2009).
[Crossref] [PubMed]

Aydin-Schmidt, B.

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
[Crossref] [PubMed]

Backman, V.

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
[Crossref] [PubMed]

Badizadegan, K.

S. McGee, J. Mirkovic, V. Mardirossian, A. Elackattu, C.-C. Yu, S. Kabani, G. Gallagher, R. Pistey, L. Galindo, K. Badizadegan, Z. Wang, R. Dasari, M. S. Feld, and G. Grillone, “Model-based spectroscopic analysis of the oral cavity: impact of anatomy,” J. Biomed. Opt. 13(6), 064034 (2008).
[Crossref] [PubMed]

Baines, P. B.

F. Paize, R. Sarginson, N. Makwana, P. B. Baines, A. P. J. Thomson, I. Sinha, C. A. Hart, A. Riordan, K. C. Hawkins, E. D. Carrol, and C. M. Parry, “Changes in the sublingual microcirculation and endothelial adhesion molecules during the course of severe meningococcal disease treated in the paediatric intensive care unit,” Intensive Care Med. 38(5), 863–871 (2012).
[Crossref] [PubMed]

Baltzell, K. A.

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
[Crossref] [PubMed]

Becker, K.

T. Frosch, S. Koncarevic, K. Becker, and J. Popp, “Morphology-sensitive Raman modes of the malaria pigment hemozoin,” Analyst (Lond.) 134(6), 1126–1132 (2009).
[Crossref] [PubMed]

Behrend, M. R.

Bergman, L. W.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Bidwell, S. L.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Bin Yunus, E.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
[Crossref] [PubMed]

Björkman, A.

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
[Crossref] [PubMed]

Boone, C. W.

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
[Crossref] [PubMed]

Bordács, S.

A. Butykai, A. Orbán, V. Kocsis, D. Szaller, S. Bordács, E. Tátrai-Szekeres, L. F. Kiss, A. Bóta, B. G. Vértessy, T. Zelles, and I. Kézsmárki, “Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis,” Sci. Rep. 3, 1431 (2013).
[Crossref] [PubMed]

Bóta, A.

A. Butykai, A. Orbán, V. Kocsis, D. Szaller, S. Bordács, E. Tátrai-Szekeres, L. F. Kiss, A. Bóta, B. G. Vértessy, T. Zelles, and I. Kézsmárki, “Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis,” Sci. Rep. 3, 1431 (2013).
[Crossref] [PubMed]

Braam, J.

E. Y. Lukianova-Hleb, K. M. Campbell, P. E. Constantinou, J. Braam, J. S. Olson, R. E. Ware, D. J. Sullivan, and D. O. Lapotko, “Hemozoin-generated vapor nanobubbles for transdermal reagent- and needle-free detection of malaria,” Proc. Natl. Acad. Sci. U.S.A. 111(3), 900–905 (2014).
[Crossref] [PubMed]

Butykai, A.

A. Butykai, A. Orbán, V. Kocsis, D. Szaller, S. Bordács, E. Tátrai-Szekeres, L. F. Kiss, A. Bóta, B. G. Vértessy, T. Zelles, and I. Kézsmárki, “Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis,” Sci. Rep. 3, 1431 (2013).
[Crossref] [PubMed]

Campbell, K. M.

E. Y. Lukianova-Hleb, K. M. Campbell, P. E. Constantinou, J. Braam, J. S. Olson, R. E. Ware, D. J. Sullivan, and D. O. Lapotko, “Hemozoin-generated vapor nanobubbles for transdermal reagent- and needle-free detection of malaria,” Proc. Natl. Acad. Sci. U.S.A. 111(3), 900–905 (2014).
[Crossref] [PubMed]

Carlton, J. M.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Carrol, E. D.

F. Paize, R. Sarginson, N. Makwana, P. B. Baines, A. P. J. Thomson, I. Sinha, C. A. Hart, A. Riordan, K. C. Hawkins, E. D. Carrol, and C. M. Parry, “Changes in the sublingual microcirculation and endothelial adhesion molecules during the course of severe meningococcal disease treated in the paediatric intensive care unit,” Intensive Care Med. 38(5), 863–871 (2012).
[Crossref] [PubMed]

Carucci, D. J.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Chang, S. K.

Charunwatthana, P.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
[Crossref] [PubMed]

Cho, J. K.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Claessens, A.

J. A. Rowe, A. Claessens, R. A. Corrigan, and M. Arman, “Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications,” Expert Rev. Mol. Med. 11, e16 (2009).
[Crossref] [PubMed]

Clark, A. L. L.

A. L. L. Clark, A. Gillenwater, R. Alizadeh-Naderi, A. K. El-Naggar, and R. Richards-Kortum, “Detection and diagnosis of oral neoplasia with an optical coherence microscope,” J. Biomed. Opt. 9(6), 1271–1280 (2004).
[Crossref] [PubMed]

Constantinou, P. E.

E. Y. Lukianova-Hleb, K. M. Campbell, P. E. Constantinou, J. Braam, J. S. Olson, R. E. Ware, D. J. Sullivan, and D. O. Lapotko, “Hemozoin-generated vapor nanobubbles for transdermal reagent- and needle-free detection of malaria,” Proc. Natl. Acad. Sci. U.S.A. 111(3), 900–905 (2014).
[Crossref] [PubMed]

Contreras, C. E.

H. Rodulfo, M. De Donato, R. Mora, L. González, and C. E. Contreras, “Comparison of the diagnosis of malaria by microscopy, immunochromatography and PCR in endemic areas of Venezuela,” Braz. J. Med. Biol. Res. 40(4), 535–543 (2007).
[Crossref] [PubMed]

Cornelius, N. R.

T. P. Santisakultarm, N. R. Cornelius, N. Nishimura, A. I. Schafer, R. T. Silver, P. C. Doerschuk, W. L. Olbricht, and C. B. Schaffer, “In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice,” Am. J. Physiol. Heart Circ. Physiol. 302(7), H1367–H1377 (2012).
[Crossref] [PubMed]

Corrigan, R. A.

J. A. Rowe, A. Claessens, R. A. Corrigan, and M. Arman, “Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications,” Expert Rev. Mol. Med. 11, e16 (2009).
[Crossref] [PubMed]

Cummings, L. M.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Cunningham, D. A.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Dann, E. J.

Dasari, R.

S. McGee, J. Mirkovic, V. Mardirossian, A. Elackattu, C.-C. Yu, S. Kabani, G. Gallagher, R. Pistey, L. Galindo, K. Badizadegan, Z. Wang, R. Dasari, M. S. Feld, and G. Grillone, “Model-based spectroscopic analysis of the oral cavity: impact of anatomy,” J. Biomed. Opt. 13(6), 064034 (2008).
[Crossref] [PubMed]

Dasari, R. R.

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
[Crossref] [PubMed]

Day, N. P.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
[Crossref] [PubMed]

De Donato, M.

H. Rodulfo, M. De Donato, R. Mora, L. González, and C. E. Contreras, “Comparison of the diagnosis of malaria by microscopy, immunochromatography and PCR in endemic areas of Venezuela,” Braz. J. Med. Biol. Res. 40(4), 535–543 (2007).
[Crossref] [PubMed]

Demirev, P. A.

P. F. Scholl, D. Kongkasuriyachai, P. A. Demirev, A. B. Feldman, J. S. Lin, D. J. Sullivan, and N. Kumar, “Rapid detection of malaria infection in vivo by laser desorption mass spectrometry,” Am. J. Trop. Med. Hyg. 71(5), 546–551 (2004).
[PubMed]

Doerschuk, P. C.

T. P. Santisakultarm, N. R. Cornelius, N. Nishimura, A. I. Schafer, R. T. Silver, P. C. Doerschuk, W. L. Olbricht, and C. B. Schaffer, “In vivo two-photon excited fluorescence microscopy reveals cardiac- and respiration-dependent pulsatile blood flow in cortical blood vessels in mice,” Am. J. Physiol. Heart Circ. Physiol. 302(7), H1367–H1377 (2012).
[Crossref] [PubMed]

Dondorp, A. M.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
[Crossref] [PubMed]

Egan, T. J.

T. J. Egan, “Recent advances in understanding the mechanism of hemozoin (malaria pigment) formation,” J. Inorg. Biochem. 102(5-6), 1288–1299 (2008).
[Crossref] [PubMed]

T. Hänscheid, T. J. Egan, and M. P. Grobusch, “Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator,” Lancet Infect. Dis. 7(10), 675–685 (2007).
[Crossref] [PubMed]

Elackattu, A.

S. McGee, J. Mirkovic, V. Mardirossian, A. Elackattu, C.-C. Yu, S. Kabani, G. Gallagher, R. Pistey, L. Galindo, K. Badizadegan, Z. Wang, R. Dasari, M. S. Feld, and G. Grillone, “Model-based spectroscopic analysis of the oral cavity: impact of anatomy,” J. Biomed. Opt. 13(6), 064034 (2008).
[Crossref] [PubMed]

Elfving, K.

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
[Crossref] [PubMed]

El-Naggar, A.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. Williams, A. El-Naggar, A. Gillenwater, and R. Richards-Kortum, “Monte Carlo model to describe depth selective fluorescence spectra of epithelial tissue: applications for diagnosis of oral precancer,” J. Biomed. Opt. 13(6), 064012 (2008).
[Crossref] [PubMed]

El-Naggar, A. K.

A. L. L. Clark, A. Gillenwater, R. Alizadeh-Naderi, A. K. El-Naggar, and R. Richards-Kortum, “Detection and diagnosis of oral neoplasia with an optical coherence microscope,” J. Biomed. Opt. 9(6), 1271–1280 (2004).
[Crossref] [PubMed]

Engel, K.

T. Planche, S. Krishna, M. Kombila, K. Engel, J. F. Faucher, E. Ngou-Milama, and P. G. Kremsner, “Comparison of methods for the rapid laboratory assessment of children with malaria,” Am. J. Trop. Med. Hyg. 65(5), 599–602 (2001).
[PubMed]

Ermolaeva, M. D.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Fabian, R. L.

W. M. White, M. Rajadhyaksha, S. González, R. L. Fabian, and R. R. Anderson, “Noninvasive imaging of human oral mucosa in vivo by confocal reflectance microscopy,” Laryngoscope 109(10), 1709–1717 (1999).
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Faiz, M. A.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
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J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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T. Planche, S. Krishna, M. Kombila, K. Engel, J. F. Faucher, E. Ngou-Milama, and P. G. Kremsner, “Comparison of methods for the rapid laboratory assessment of children with malaria,” Am. J. Trop. Med. Hyg. 65(5), 599–602 (2001).
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T. Planche, S. Krishna, M. Kombila, K. Engel, J. F. Faucher, E. Ngou-Milama, and P. G. Kremsner, “Comparison of methods for the rapid laboratory assessment of children with malaria,” Am. J. Trop. Med. Hyg. 65(5), 599–602 (2001).
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Kubes, P.

M. Ho, M. J. Hickey, A. G. Murray, G. Andonegui, and P. Kubes, “Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment,” J. Exp. Med. 192(8), 1205–1212 (2000).
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P. F. Scholl, D. Kongkasuriyachai, P. A. Demirev, A. B. Feldman, J. S. Lin, D. J. Sullivan, and N. Kumar, “Rapid detection of malaria infection in vivo by laser desorption mass spectrometry,” Am. J. Trop. Med. Hyg. 71(5), 546–551 (2004).
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J. Kopacz and N. Kumar, “Murine γ δ T Lymphocytes Elicited during Plasmodium yoelii Infection Respond to Plasmodium Heat Shock Proteins,” Infect. Immun. 67(1), 57–63 (1999).
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E. Y. Lukianova-Hleb, K. M. Campbell, P. E. Constantinou, J. Braam, J. S. Olson, R. E. Ware, D. J. Sullivan, and D. O. Lapotko, “Hemozoin-generated vapor nanobubbles for transdermal reagent- and needle-free detection of malaria,” Proc. Natl. Acad. Sci. U.S.A. 111(3), 900–905 (2014).
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Laver, N.

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
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Lim, Y. W.

M. E. Rafael, T. Taylor, A. Magill, Y. W. Lim, F. Girosi, and R. Allan, “Reducing the burden of childhood malaria in Africa: the role of improved,” Nature 444(Suppl 1), 39–48 (2006).
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Limmathurotsakul, D.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
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Lin, J. S.

P. F. Scholl, D. Kongkasuriyachai, P. A. Demirev, A. B. Feldman, J. S. Lin, D. J. Sullivan, and N. Kumar, “Rapid detection of malaria infection in vivo by laser desorption mass spectrometry,” Am. J. Trop. Med. Hyg. 71(5), 546–551 (2004).
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Lukianova-Hleb, E. Y.

E. Y. Lukianova-Hleb, K. M. Campbell, P. E. Constantinou, J. Braam, J. S. Olson, R. E. Ware, D. J. Sullivan, and D. O. Lapotko, “Hemozoin-generated vapor nanobubbles for transdermal reagent- and needle-free detection of malaria,” Proc. Natl. Acad. Sci. U.S.A. 111(3), 900–905 (2014).
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Magill, A.

M. E. Rafael, T. Taylor, A. Magill, Y. W. Lim, F. Girosi, and R. Allan, “Reducing the burden of childhood malaria in Africa: the role of improved,” Nature 444(Suppl 1), 39–48 (2006).
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F. Paize, R. Sarginson, N. Makwana, P. B. Baines, A. P. J. Thomson, I. Sinha, C. A. Hart, A. Riordan, K. C. Hawkins, E. D. Carrol, and C. M. Parry, “Changes in the sublingual microcirculation and endothelial adhesion molecules during the course of severe meningococcal disease treated in the paediatric intensive care unit,” Intensive Care Med. 38(5), 863–871 (2012).
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A. García-Hernández, R. Roldán-Marín, P. Iglesias-Garcia, and J. Malvehy, “In vivo noninvasive imaging of healthy lower lip mucosa: a correlation study between high-definition optical coherence tomography, reflectance confocal microscopy, and histology,” Dermatol. Res. Pract. 2013, 205256 (2013).
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K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
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D. M. Newman, R. J. Matelon, M. L. Wears, and L. B. Savage, “The in vivo diagnosis of malaria: Feasibility study into a magneto-optic fingertip probe,” IEEE J. Sel. Top. Quantum Electron. 16(3), 573–580 (2010).
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A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
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Minh, T. C.

T. C. Minh, S. Ichioka, K. Harii, M. Shibata, J. Ando, and T. Nakatsuka, “Dorsal bipedicled island skin flap: a new flap model in mice,” Scand. J. Plast. Reconstr. Surg. Hand Surg. 36(5), 262–267 (2002).
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Mora, R.

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K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
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Müller, M. G.

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
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M. Ho, M. J. Hickey, A. G. Murray, G. Andonegui, and P. Kubes, “Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment,” J. Exp. Med. 192(8), 1205–1212 (2000).
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Nakatsuka, T.

T. C. Minh, S. Ichioka, K. Harii, M. Shibata, J. Ando, and T. Nakatsuka, “Dorsal bipedicled island skin flap: a new flap model in mice,” Scand. J. Plast. Reconstr. Surg. Hand Surg. 36(5), 262–267 (2002).
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D. M. Newman, R. J. Matelon, M. L. Wears, and L. B. Savage, “The in vivo diagnosis of malaria: Feasibility study into a magneto-optic fingertip probe,” IEEE J. Sel. Top. Quantum Electron. 16(3), 573–580 (2010).
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T. Planche, S. Krishna, M. Kombila, K. Engel, J. F. Faucher, E. Ngou-Milama, and P. G. Kremsner, “Comparison of methods for the rapid laboratory assessment of children with malaria,” Am. J. Trop. Med. Hyg. 65(5), 599–602 (2001).
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Omar, R.

K. A. Baltzell, D. Shakely, M. Hsiang, J. Kemere, A. S. Ali, A. Björkman, A. Mårtensson, R. Omar, K. Elfving, M. Msellem, B. Aydin-Schmidt, P. J. Rosenthal, and B. Greenhouse, “Prevalence of PCR Detectable Malaria Infection among Febrile Patients with a Negative Plasmodium falciparum Specific Rapid Diagnostic Test in Zanzibar,” Am. J. Trop. Med. Hyg. 88(2), 289–291 (2013).
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F. Paize, R. Sarginson, N. Makwana, P. B. Baines, A. P. J. Thomson, I. Sinha, C. A. Hart, A. Riordan, K. C. Hawkins, E. D. Carrol, and C. M. Parry, “Changes in the sublingual microcirculation and endothelial adhesion molecules during the course of severe meningococcal disease treated in the paediatric intensive care unit,” Intensive Care Med. 38(5), 863–871 (2012).
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Parry, C. M.

F. Paize, R. Sarginson, N. Makwana, P. B. Baines, A. P. J. Thomson, I. Sinha, C. A. Hart, A. Riordan, K. C. Hawkins, E. D. Carrol, and C. M. Parry, “Changes in the sublingual microcirculation and endothelial adhesion molecules during the course of severe meningococcal disease treated in the paediatric intensive care unit,” Intensive Care Med. 38(5), 863–871 (2012).
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I. Pavlova, C. R. Weber, R. A. Schwarz, M. Williams, A. El-Naggar, A. Gillenwater, and R. Richards-Kortum, “Monte Carlo model to describe depth selective fluorescence spectra of epithelial tissue: applications for diagnosis of oral precancer,” J. Biomed. Opt. 13(6), 064012 (2008).
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J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Peterson, J. D.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Pistey, R.

S. McGee, J. Mirkovic, V. Mardirossian, A. Elackattu, C.-C. Yu, S. Kabani, G. Gallagher, R. Pistey, L. Galindo, K. Badizadegan, Z. Wang, R. Dasari, M. S. Feld, and G. Grillone, “Model-based spectroscopic analysis of the oral cavity: impact of anatomy,” J. Biomed. Opt. 13(6), 064034 (2008).
[Crossref] [PubMed]

Planche, T.

T. Planche, S. Krishna, M. Kombila, K. Engel, J. F. Faucher, E. Ngou-Milama, and P. G. Kremsner, “Comparison of methods for the rapid laboratory assessment of children with malaria,” Am. J. Trop. Med. Hyg. 65(5), 599–602 (2001).
[PubMed]

Pop, M.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Popp, J.

T. Frosch, S. Koncarevic, K. Becker, and J. Popp, “Morphology-sensitive Raman modes of the malaria pigment hemozoin,” Analyst (Lond.) 134(6), 1126–1132 (2009).
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Prahl, S. A.

Preiser, P. R.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Quackenbush, J.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
[Crossref] [PubMed]

Rafael, M. E.

M. E. Rafael, T. Taylor, A. Magill, Y. W. Lim, F. Girosi, and R. Allan, “Reducing the burden of childhood malaria in Africa: the role of improved,” Nature 444(Suppl 1), 39–48 (2006).
[Crossref] [PubMed]

Rahman, M. R.

A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
[Crossref] [PubMed]

Raine, J. D.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Rajadhyaksha, M.

W. M. White, M. Rajadhyaksha, S. González, R. L. Fabian, and R. R. Anderson, “Noninvasive imaging of human oral mucosa in vivo by confocal reflectance microscopy,” Laryngoscope 109(10), 1709–1717 (1999).
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Richards-Kortum, R.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. Williams, A. El-Naggar, A. Gillenwater, and R. Richards-Kortum, “Monte Carlo model to describe depth selective fluorescence spectra of epithelial tissue: applications for diagnosis of oral precancer,” J. Biomed. Opt. 13(6), 064012 (2008).
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D. Arifler, R. A. Schwarz, S. K. Chang, and R. Richards-Kortum, “Reflectance spectroscopy for diagnosis of epithelial precancer: model-based analysis of fiber-optic probe designs to resolve spectral information from epithelium and stroma,” Appl. Opt. 44(20), 4291–4305 (2005).
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A. L. L. Clark, A. Gillenwater, R. Alizadeh-Naderi, A. K. El-Naggar, and R. Richards-Kortum, “Detection and diagnosis of oral neoplasia with an optical coherence microscope,” J. Biomed. Opt. 9(6), 1271–1280 (2004).
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Riedmuller, S. B.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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van Marie, J.

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J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Vértessy, B. G.

A. Butykai, A. Orbán, V. Kocsis, D. Szaller, S. Bordács, E. Tátrai-Szekeres, L. F. Kiss, A. Bóta, B. G. Vértessy, T. Zelles, and I. Kézsmárki, “Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis,” Sci. Rep. 3, 1431 (2013).
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Waters, A. P.

J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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I. Pavlova, C. R. Weber, R. A. Schwarz, M. Williams, A. El-Naggar, A. Gillenwater, and R. Richards-Kortum, “Monte Carlo model to describe depth selective fluorescence spectra of epithelial tissue: applications for diagnosis of oral precancer,” J. Biomed. Opt. 13(6), 064012 (2008).
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A. M. Dondorp, C. Ince, P. Charunwatthana, J. Hanson, A. van Kuijen, M. A. Faiz, M. R. Rahman, M. Hasan, E. Bin Yunus, A. Ghose, R. Ruangveerayut, D. Limmathurotsakul, K. Mathura, N. J. White, and N. P. Day, “Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria,” J. Infect. Dis. 197(1), 79–84 (2008).
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J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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W. M. White, M. Rajadhyaksha, S. González, R. L. Fabian, and R. R. Anderson, “Noninvasive imaging of human oral mucosa in vivo by confocal reflectance microscopy,” Laryngoscope 109(10), 1709–1717 (1999).
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J. M. Carlton, S. V. Angiuoli, B. B. Suh, T. W. Kooij, M. Pertea, J. C. Silva, M. D. Ermolaeva, J. E. Allen, J. D. Selengut, H. L. Koo, J. D. Peterson, M. Pop, D. S. Kosack, M. F. Shumway, S. L. Bidwell, S. J. Shallom, S. E. van Aken, S. B. Riedmuller, T. V. Feldblyum, J. K. Cho, J. Quackenbush, M. Sedegah, A. Shoaibi, L. M. Cummings, L. Florens, J. R. Yates, J. D. Raine, R. E. Sinden, M. A. Harris, D. A. Cunningham, P. R. Preiser, L. W. Bergman, A. B. Vaidya, L. H. van Lin, C. J. Janse, A. P. Waters, H. O. Smith, O. R. White, S. L. Salzberg, J. C. Venter, C. M. Fraser, S. L. Hoffman, M. J. Gardner, and D. J. Carucci, “Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii,” Nature 419(6906), 512–519 (2002).
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Yelin, D.

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A. Butykai, A. Orbán, V. Kocsis, D. Szaller, S. Bordács, E. Tátrai-Szekeres, L. F. Kiss, A. Bóta, B. G. Vértessy, T. Zelles, and I. Kézsmárki, “Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis,” Sci. Rep. 3, 1431 (2013).
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T. Frosch, S. Koncarevic, K. Becker, and J. Popp, “Morphology-sensitive Raman modes of the malaria pigment hemozoin,” Analyst (Lond.) 134(6), 1126–1132 (2009).
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Cancer (1)

M. G. Müller, T. A. Valdez, I. Georgakoudi, V. Backman, C. Fuentes, S. Kabani, N. Laver, Z. Wang, C. W. Boone, R. R. Dasari, S. M. Shapshay, and M. S. Feld, “Spectroscopic detection and evaluation of morphologic and biochemical changes in early human oral carcinoma,” Cancer 97(7), 1681–1692 (2003).
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IEEE J. Sel. Top. Quantum Electron. (1)

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Supplementary Material (2)

NameDescription
» Visualization 1: AVI (4027 KB)      Hemozoin detected in the microvasculature of a P. yoelii-infected mouse. under TR mode
» Visualization 2: AVI (578 KB)      Frame rate reduced video of circulating hemozoin particle detected under TR in mouse model.

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Figures (6)

Fig. 1
Fig. 1 (a) Diagnostic concept: malaria-infected cells are detected circulating through the superficial microvasculature using in vivo microscopy. (b) The malaria parasite by-product, hemozoin, visualized under bright-field and (c) cross-polarized illumination.
Fig. 2
Fig. 2 (a) Schematic diagram of the MVM with three illumination modes: TR, transmission red, TG, transmission green, and XP, cross polarized reflectance. (b) USAF 1951 resolution target imaged under TR and XP (inset). (c) The measured and calculated magnification of the MVM as a function of working distance.
Fig. 3
Fig. 3 MVM imaging of multilayer phantom. (a) Negative control blood sample imaged under TR and (b) XP. (c) P. yoelii-infected blood sample imaged under TR and (d) XP. Arrows indicate hemozoin particles. Scale bars = 20 µm. (e) Temporal variations in SBR quantified for 10 colocalized ROIs. (f) The SBR as a function of increasing epithelial scattering by increasing Intralipid concentration.
Fig. 4
Fig. 4 Ex vivo imaging of microvasculature in excised mouse tissue from (a-c) a negative control animal and (d-i) a P. yoelii-infected animal. Arrows indicate hemozoin particles. Scale bars = 20 µm.
Fig. 5
Fig. 5 In vivo imaging of circulating blood in superficial microvasculature of mouse model. (a,b) Axial translation of focal plane in TG mode in P. yoelii-infected animal. (c,d) Selected frames from TR mode video (Visualization 1) collected at imaging site outlined in (b). (e) Imaging of non-infected animal in TG mode and (f) TR mode. Scale bars = 20 µm.
Fig. 6
Fig. 6 In vivo imaging of circulating hemozoin over a range of parasitemia in mouse model. (a) Vessel located using TG mode. (b) Overlaid frames from correlating TR mode Visualization 2 show single hemozoin tracked over 0.25 s. Scale bars = 20 µm. (c) Hemozoin flux plotted as a function of parasitemia according to subject (A-H). (d) Estimation of time to detect one hemozoin structure as a function of parasitemia.

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