Diamond Magnetic Microscopy of Malarial Hemozoin Nanocrystals

Fescenko, Ilja; Laraoui, Abdelghani; Smits, Janis; Mosavian, Nazanin; Kehayias, Pauli; Seto, Jong; Bougas, Lykourgos; Jarmola, Andrey; Acosta, Victor M.

doi:10.1103/physrevapplied.11.034029

Diamond Magnetic Microscopy of Malarial Hemozoin Nanocrystals

Journal Article · Tue Mar 12 00:00:00 EDT 2019 · Physical Review Applied

DOI:https://doi.org/10.1103/physrevapplied.11.034029· OSTI ID:1625641

Fescenko, Ilja ^[1]; Laraoui, Abdelghani ^[2]; Smits, Janis ^[3]; Mosavian, Nazanin ^[2]; Kehayias, Pauli ^[4]; Seto, Jong ^[5]; Bougas, Lykourgos ^[6]; Jarmola, Andrey ^[7]; Acosta, Victor M. ^[2]

Univ. of New Mexico, Albuquerque, NM (United States). Center for High Technology Materials (CHTM); DOE/OSTI
Univ. of New Mexico, Albuquerque, NM (United States). Center for High Technology Materials (CHTM)
Univ. of New Mexico, Albuquerque, NM (United States). Center for High Technology Materials (CHTM); Univ. of Latvia, Riga (Latvia)
Univ. of New Mexico, Albuquerque, NM (United States). Center for High Technology Materials (CHTM); Harvard Univ., Cambridge, MA (United States)
Univ. of California, San Francisco, CA (United States)
Johannes Gutenberg Univ., Mainz (Germany)
Univ. of California, Berkeley, CA (United States); ODMR Technologies, Inc., El Cerrito, CA (United States)

Magnetic microscopy of malarial hemozoin nanocrystals is performed by optically detected magnetic resonance imaging of near-surface diamond nitrogen-vacancy centers. Hemozoin crystals are extracted from Plasmodium falciparum–infected human blood cells and studied alongside synthetic hemozoin crystals. The stray magnetic fields produced by individual crystals are imaged at room temperature as a function of the applied field up to 350 mT. More than 100 nanocrystals are analyzed, revealing the distribution of their magnetic properties. Most crystals (96%) exhibit a linear dependence of the stray-field magnitude on the applied field, confirming hemozoin’s paramagnetic nature. A volume magnetic susceptibility of 3.4 × 10^–4 is inferred with use of a magnetostatic model informed by correlated scanning-electron-microscopy measurements of crystal dimensions. A small fraction of nanoparticles (4/82 for Plasmodium falciparum–produced nanoparticles and 1/41 for synthetic nanoparticles) exhibit a saturation behavior consistent with superparamagnetism. Translation of this platform to the study of living Plasmodium-infected cells may shed new light on hemozoin formation dynamics and their interaction with antimalarial drugs.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratory (SNL-NM), Albuquerque, NM (United States). Center for Integrated Nanotechnologies

Sponsoring Organization:: USDOE; National Institute of General Medical Sciences (NIGMS); National Institute of Mental Health (NIMH); National Institute of Biomedical Imaging and Bioengineering (NIBIB)

OSTI ID:: 1625641

Journal Information:: Physical Review Applied, Journal Name: Physical Review Applied Journal Issue: 3 Vol. 11; ISSN 2331-7019

Publisher:: American Physical Society (APS)Copyright Statement

Country of Publication:: United States

Language:: English

References (71)

Hemozoin Biocrystallization in Plasmodium falciparum and the antimalarial activity of crystallization inhibitors Hempelmann, Ernst Parasitology Research, Vol. 100, Issue 4 https://doi.org/10.1007/s00436-006-0313-x	journal	November 2006
Polarisation microscopy increases the sensitivity of hemozoin and Plasmodium detection in the histological assessment of placental malaria Romagosa, Cleofé; Menendez, Clara; Ismail, Mamudo R. Acta Tropica, Vol. 90, Issue 3 https://doi.org/10.1016/j.actatropica.2004.02.003	journal	May 2004
Magnetic susceptibility of iron in malaria-infected red blood cells Hackett, S.; Hamzah, J.; Davis, T. M. E. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1792, Issue 2 https://doi.org/10.1016/j.bbadis.2008.11.001	journal	February 2009
Microfluidic method for measuring viscosity using images from smartphone Kim, Sooyeong; Kim, Kyung Chun; Yeom, Eunseop Optics and Lasers in Engineering, Vol. 104 https://doi.org/10.1016/j.optlaseng.2017.05.016	journal	May 2018
Optical imaging techniques for the study of malaria Cho, Sangyeon; Kim, Soomin; Kim, Youngchan Trends in Biotechnology, Vol. 30, Issue 2 https://doi.org/10.1016/j.tibtech.2011.08.004	journal	February 2012
Theories on malarial pigment formation and quinoline action Sullivan, David J. International Journal for Parasitology, Vol. 32, Issue 13 https://doi.org/10.1016/s0020-7519(02)00193-5	journal	December 2002
Rapid Diagnostic for Point-of-Care Malaria Screening McBirney, Samantha E.; Chen, Dongyu; Scholtz, Alexis ACS Sensors, Vol. 3, Issue 7 https://doi.org/10.1021/acssensors.8b00269	journal	May 2018
Multi-Frequency High-Field EPR Study of Iron Centers in Malarial Pigments Sienkiewicz, Andrzej; Krzystek, J.; Vileno, Bertrand Journal of the American Chemical Society, Vol. 128, Issue 14 https://doi.org/10.1021/ja058420h	journal	March 2006
Nanometre-scale thermometry in a living cell Kucsko, G.; Maurer, P. C.; Yao, N. Y. Nature, Vol. 500, Issue 7460 https://doi.org/10.1038/nature12373	journal	July 2013
Single-cell magnetic imaging using a quantum diamond microscope Glenn, David R.; Lee, Kyungheon; Park, Hongkun Nature Methods, Vol. 12, Issue 8 https://doi.org/10.1038/nmeth.3449	journal	June 2015
Quantum measurement and orientation tracking of fluorescent nanodiamonds inside living cells McGuinness, L. P.; Yan, Y.; Stacey, A. Nature Nanotechnology, Vol. 6, Issue 6 https://doi.org/10.1038/nnano.2011.64	journal	May 2011
Mapping the microscale origins of magnetic resonance image contrast with subcellular diamond magnetometry Davis, Hunter C.; Ramesh, Pradeep; Bhatnagar, Aadyot Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02471-7	journal	January 2018
Malaria pigment crystals as magnetic micro-rotors: key for high-sensitivity diagnosis Butykai, A.; Orbán, A.; Kocsis, V. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01431	journal	March 2013
Superparamagnetic Properties of Hemozoin Inyushin, M.; Kucheryavih, Yu.; Kucheryavih, L. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep26212	journal	May 2016
Resonance Raman microscopy in combination with partial dark-field microscopy lights up a new path in malaria diagnostics Wood, Bayden R.; Hermelink, Antje; Lasch, Peter The Analyst, Vol. 134, Issue 6 https://doi.org/10.1039/b822603b	journal	January 2009
Single spin optically detected magnetic resonance with 60–90 GHz (E-band) microwave resonators Aslam, Nabeel; Pfender, Matthias; Stöhr, Rainer Review of Scientific Instruments, Vol. 86, Issue 6 https://doi.org/10.1063/1.4922664	journal	June 2015
A magnetic source imaging camera Dolgovskiy, V.; Fescenko, I.; Sekiguchi, N. Applied Physics Letters, Vol. 109, Issue 2 https://doi.org/10.1063/1.4958700	journal	July 2016
Red blood cell adhesion on a solid/liquid interface Lavalle, Ph.; Stoltz, J. -F.; Senger, B. Proceedings of the National Academy of Sciences, Vol. 93, Issue 26 https://doi.org/10.1073/pnas.93.26.15136	journal	December 1996
Magnetometry with nitrogen-vacancy defects in diamond Rondin, L.; Tetienne, J-P; Hingant, T. Reports on Progress in Physics, Vol. 77, Issue 5 https://doi.org/10.1088/0034-4885/77/5/056503	journal	May 2014
Birefringent Hemozoin Identifies Malaria Lawrence, Christine; Olson, Julie A. American Journal of Clinical Pathology, Vol. 86, Issue 3 https://doi.org/10.1093/ajcp/86.3.360	journal	September 1986
High-Sensitivity Magnetometry Based on Quantum Beats in Diamond Nitrogen-Vacancy Centers Fang, Kejie; Acosta, Victor M.; Santori, Charles Physical Review Letters, Vol. 110, Issue 13 https://doi.org/10.1103/physrevlett.110.130802	journal	March 2013
Dark-field microscopy for detection of malaria in unstained blood films Jamjoom, G. A. Journal of Clinical Microbiology, Vol. 17, Issue 5 https://doi.org/10.1128/jcm.17.5.717-721.1983	journal	May 1983
Nitrogen-Vacancy Centers in Diamond: Nanoscale Sensors for Physics and Biology Schirhagl, Romana; Chang, Kevin; Loretz, Michael Annual Review of Physical Chemistry, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-physchem-040513-103659	journal	April 2014
A novel mechanism for egress of malarial parasites from red blood cells Abkarian, Manouk; Massiera, Gladys; Berry, Laurence Blood, Vol. 117, Issue 15 https://doi.org/10.1182/blood-2010-08-299883	journal	April 2011
In vivo microscopy of hemozoin: towards a needle free diagnostic for malaria Burnett, Jennifer L.; Carns, Jennifer L.; Richards-Kortum, Rebecca Biomedical Optics Express, Vol. 6, Issue 9 https://doi.org/10.1364/boe.6.003462	journal	August 2015
Synthetic Plasmodium-Like Hemozoin Activates the Immune Response: A Morphology - Function Study Jaramillo, Maritza; Bellemare, Marie-Josée; Martel, Caroline PLoS ONE, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pone.0006957	journal	September 2009
A Novel Flow Cytometric Hemozoin Detection Assay for Real-Time Sensitivity Testing of Plasmodium falciparum Rebelo, Maria; Sousa, Claudia; Shapiro, Howard M. PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061606	journal	April 2013
Evaluation of a Novel Magneto-Optical Method for the Detection of Malaria Parasites Orbán, Ágnes; Butykai, Ádám; Molnár, András PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0096981	journal	May 2014
Interdependent Dynamics of LAI-Albedo across the Roofing Landscapes: Mongolian and Tibetan Plateaus Tian, Li; Chen, Jiquan; Shao, Changliang Remote Sensing, Vol. 10, Issue 7 https://doi.org/10.3390/rs10071159	journal	July 2018
Broadband magnetometry by infrared-absorption detection of nitrogen-vacancy ensembles in diamond Acosta, V. M.; Bauch, E.; Jarmola, A. arXiv https://doi.org/10.48550/arxiv.1009.4747	text	January 2010
Scanning nano-spin ensemble microscope for nanoscale magnetic and thermal imaging Tetienne, Jean-Philippe; Lombard, Alain; Simpson, David A. arXiv https://doi.org/10.48550/arxiv.1509.00586	text	January 2015
Solution nuclear magnetic resonance spectroscopy on a nanostructured diamond chip Kehayias, P.; Jarmola, A.; Mosavian, N. arXiv https://doi.org/10.48550/arxiv.1701.01401	text	January 2017
Two-dimensional nuclear magnetic resonance spectroscopy with a microfluidic diamond quantum sensor Smits, Janis; Damron, Joshua; Kehayias, Pauli arXiv https://doi.org/10.48550/arxiv.1901.02952	text	January 2019
Iron (III) porphyrin aggregates grafted on agarose gel as models of hemoglobin degradation products Brémard, C.; Girerd, J. J.; Merlin, J. C. Journal of Molecular Structure, Vol. 267 https://doi.org/10.1016/0022-2860(92)87019-R	journal	March 1992
Theories on malarial pigment formation and quinoline action Sullivan, David J. International Journal for Parasitology, Vol. 32, Issue 13 https://doi.org/10.1016/S0020-7519(02)00193-5	journal	December 2002
Physico-chemical aspects of hemozoin (malaria pigment) structure and formation Egan, Timothy J. Journal of Inorganic Biochemistry, Vol. 91, Issue 1 https://doi.org/10.1016/S0162-0134(02)00372-0	journal	July 2002
Malarial hemozoin: From target to tool Coronado, Lorena M.; Nadovich, Christopher T.; Spadafora, Carmenza Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1840, Issue 6 https://doi.org/10.1016/j.bbagen.2014.02.009	journal	June 2014
Temperature dependence of the spin relaxation time of Fe 3 O 4 and hemozoin superparamagnetic nanocrystals Khmelinskii, I.; Makarov, V. Chemical Physics, Vol. 493 https://doi.org/10.1016/j.chemphys.2017.06.015	journal	August 2017
Structural and morphological characterization of hemozoin produced bySchistosoma mansoniandRhodnius prolixus Oliveira, Marcus F.; Kycia, Stefan W.; Gomez, Ariel FEBS Letters, Vol. 579, Issue 27 https://doi.org/10.1016/j.febslet.2005.09.035	journal	October 2005
Scanning Nanospin Ensemble Microscope for Nanoscale Magnetic and Thermal Imaging Tetienne, Jean-Philippe; Lombard, Alain; Simpson, David A. Nano Letters, Vol. 16, Issue 1 https://doi.org/10.1021/acs.nanolett.5b03877	journal	December 2015
Aggregated Heme Detoxification Byproducts in Malarial Trophozoites: β-Hematin and Malaria Pigment Have a Single S = ⁵/₂ Iron Environment in the Bulk Phase as Determined by EPR and Magnetic Mössbauer Spectroscopy Bohle, D. Scott; Debrunner, Peter; Jordan, Peter A. Journal of the American Chemical Society, Vol. 120, Issue 32 https://doi.org/10.1021/ja980962u	journal	July 1998
Highly Sensitive Detection of Physiological Spins in a Microfluidic Device Ziem, Florestan C.; Götz, Nicolas S.; Zappe, Andrea Nano Letters, Vol. 13, Issue 9 https://doi.org/10.1021/nl401522a	journal	August 2013
Optical magnetic imaging of living cells Le Sage, D.; Arai, K.; Glenn, D. R. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12072	journal	April 2013
Micromagnetic resonance relaxometry for rapid label-free malaria diagnosis Peng, Weng Kung; Kong, Tian Fook; Ng, Chee Sheng Nature Medicine, Vol. 20, Issue 9 https://doi.org/10.1038/nm.3622	journal	August 2014
Solution nuclear magnetic resonance spectroscopy on a nanostructured diamond chip Kehayias, P.; Jarmola, A.; Mosavian, N. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00266-4	journal	August 2017
NMR relaxation properties of the synthetic malaria pigment β-hematin Gossuin, Yves; Okusa Ndjolo, Philippe; Vuong, Quoc Lam Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-15238-3	journal	November 2017
A reference document on Permissible Limits for solvents and buffers during in vitro antimalarial screening Naidu, Renugah; Subramanian, Gowtham; Lim, Ying Bena Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33226-z	journal	October 2018
Efficient monitoring of the blood-stage infection in a malaria rodent model by the rotating-crystal magneto-optical method Orbán, Ágnes; Rebelo, Maria; Molnár, Petra Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23218	journal	March 2016
Broadband magnetometry by infrared-absorption detection of nitrogen-vacancy ensembles in diamond Acosta, V. M.; Bauch, E.; Jarmola, A. Applied Physics Letters, Vol. 97, Issue 17 https://doi.org/10.1063/1.3507884	journal	October 2010
Room-temperature detection of a single 19 nm super-paramagnetic nanoparticle with an imaging magnetometer Gould, Michael; Barbour, Russell J.; Thomas, Nicole Applied Physics Letters, Vol. 105, Issue 7 https://doi.org/10.1063/1.4893602	journal	August 2014
High-frequency and high-field optically detected magnetic resonance of nitrogen-vacancy centers in diamond Stepanov, Viktor; Cho, Franklin H.; Abeywardana, Chathuranga Applied Physics Letters, Vol. 106, Issue 6 https://doi.org/10.1063/1.4908528	journal	February 2015
High density nitrogen-vacancy sensing surface created via He ⁺ ion implantation of ¹² C diamond Kleinsasser, Ed E.; Stanfield, Matthew M.; Banks, Jannel K. Q. Applied Physics Letters, Vol. 108, Issue 20 https://doi.org/10.1063/1.4949357	journal	May 2016
Optical magnetic detection of single-neuron action potentials using quantum defects in diamond Barry, John F.; Turner, Matthew J.; Schloss, Jennifer M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 49 https://doi.org/10.1073/pnas.1601513113	journal	November 2016
Magnetic field imaging with nitrogen-vacancy ensembles Pham, L. M.; Le Sage, D.; Stanwix, P. L. New Journal of Physics, Vol. 13, Issue 4 https://doi.org/10.1088/1367-2630/13/4/045021	journal	April 2011
Vertical distribution of nitrogen-vacancy centers in diamond formed by ion implantation and annealing Santori, Charles; Barclay, Paul E.; Fu, Kai-Mei C. Physical Review B, Vol. 79, Issue 12 https://doi.org/10.1103/PhysRevB.79.125313	journal	March 2009
Diamonds with a high density of nitrogen-vacancy centers for magnetometry applications Acosta, V. M.; Bauch, E.; Ledbetter, M. P. Physical Review B, Vol. 80, Issue 11 https://doi.org/10.1103/PhysRevB.80.115202	journal	September 2009
Temperature Dependence of the Nitrogen-Vacancy Magnetic Resonance in Diamond Acosta, V. M.; Bauch, E.; Ledbetter, M. P. Physical Review Letters, Vol. 104, Issue 7 https://doi.org/10.1103/PhysRevLett.104.070801	journal	February 2010
High-Sensitivity Magnetometry Based on Quantum Beats in Diamond Nitrogen-Vacancy Centers Fang, Kejie; Acosta, Victor M.; Santori, Charles Physical Review Letters, Vol. 110, Issue 13 https://doi.org/10.1103/PhysRevLett.110.130802	journal	March 2013
Efficient Readout of a Single Spin State in Diamond via Spin-to-Charge Conversion Shields, B. J.; Unterreithmeier, Q. P.; de Leon, N. P. Physical Review Letters, Vol. 114, Issue 13 https://doi.org/10.1103/PhysRevLett.114.136402	journal	March 2015
Ultralong Dephasing Times in Solid-State Spin Ensembles via Quantum Control Bauch, Erik; Hart, Connor A.; Schloss, Jennifer M. Physical Review X, Vol. 8, Issue 3 https://doi.org/10.1103/PhysRevX.8.031025	journal	July 2018
Automated three-dimensional tracking of living cells by digital holographic microscopy Langehanenberg, Patrik; Ivanova, Lyubomira; Bernhardt, Ingolf Journal of Biomedical Optics, Vol. 14, Issue 1 https://doi.org/10.1117/1.3080133	journal	January 2009
Quantum imaging of current flow in graphene Tetienne, Jean-Philippe; Dontschuk, Nikolai; Broadway, David A. Science Advances, Vol. 3, Issue 4 https://doi.org/10.1126/sciadv.1602429	journal	April 2017
Dark-field microscopy for detection of malaria in unstained blood films Jamjoom, G. A. Journal of Clinical Microbiology, Vol. 17, Issue 5 https://doi.org/10.1128/JCM.17.5.717-721.1983	journal	May 1983
The Langevin Equation: With Applications to Stochastic Problems in Physics, Chemistry and Electrical Engineering Coffey, William T.; Kalmykov, Yuri P. World Scientific Series in Contemporary Chemical Physics, Vol. 28 https://doi.org/10.1142/10490	book	May 2017
Effects of hemin and hemodialysis in a patient with acute intermittent porphyria and renal failure Attarian, Shirin; Yu, Chunli; Anderson, Karl E. Blood Advances, Vol. 1, Issue 14 https://doi.org/10.1182/bloodadvances.2017005660	journal	June 2017
Simple flow cytometric detection of haemozoin containing leukocytes and erythrocytes for research on diagnosis, immunology and drug sensitivity testing Frita, Rosangela; Rebelo, Maria; Pamplona, Ana Malaria Journal, Vol. 10, Issue 1 https://doi.org/10.1186/1475-2875-10-74	journal	January 2011
Improved methods for magnetic purification of malaria parasites and haemozoin Kim, Charles C.; Wilson, Emily B.; DeRisi, Joseph L. Malaria Journal, Vol. 9, Issue 1 https://doi.org/10.1186/1475-2875-9-17	journal	January 2010
In vivo microscopy of hemozoin: towards a needle free diagnostic for malaria Burnett, Jennifer L.; Carns, Jennifer L.; Richards-Kortum, Rebecca Biomedical Optics Express, Vol. 6, Issue 9 https://doi.org/10.1364/BOE.6.003462	journal	August 2015
Sensitive Detection of Malaria Infection by Third Harmonic Generation Imaging Bélisle, Jonathan M.; Costantino, Santiago; Leimanis, Mara L. Biophysical Journal, Vol. 94, Issue 4 https://doi.org/10.1529/biophysj.107.125443	journal	February 2008
Tuning the Magnetic Properties of Nanoparticles Kolhatkar, Arati; Jamison, Andrew; Litvinov, Dmitri International Journal of Molecular Sciences, Vol. 14, Issue 8 https://doi.org/10.3390/ijms140815977	journal	July 2013
In vivo microscopy of hemozoin: towards a needle free diagnostic for malaria Burnett, Jennifer L.; Carns, Jennifer L.; Richards-Kortum, Rebecca Figshare https://doi.org/10.6084/m9.figshare.c.3753008.v1	collection	January 2015

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59 BASIC BIOLOGICAL SCIENCES
Nitrogen vacancy centers in diamond
magnetic susceptibility
medical imaging
nanocrystals
optically detected magnetic resonance
paramagnets
parasitic diseases
quantum sensing

Diamond Magnetic Microscopy of Malarial Hemozoin Nanocrystals

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