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X-ray micro-computed tomography (μCT): an emerging opportunity in parasite imaging

  • James D. B. O'Sullivan (a1), Julia Behnsen (a1), Tobias Starborg (a2), Andrew S. MacDonald (a2), Alexander T. Phythian-Adams (a2), Kathryn J. Else (a2), Sheena M. Cruickshank (a2) and Philip J. Withers (a1)...

Abstract

X-ray micro-computed tomography (μCT) is a technique which can obtain three-dimensional images of a sample, including its internal structure, without the need for destructive sectioning. Here, we review the capability of the technique and examine its potential to provide novel insights into the lifestyles of parasites embedded within host tissue. The current capabilities and limitations of the technology in producing contrast in soft tissues are discussed, as well as the potential solutions for parasitologists looking to apply this technique. We present example images of the mouse whipworm Trichuris muris and discuss the application of μCT to provide unique insights into parasite behaviour and pathology, which are inaccessible to other imaging modalities.

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Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: James D. B. O'Sullivan, E-mail: james.osullivan-4@postgrad.manchester.ac.uk

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Arganda-Carreras, I, Fernández-González, R, Muñoz-Barrutia, A and Ortiz-De-Solorzano, C (2010) 3D reconstruction of histological sections: application to mammary gland tissue. Microscopy Research and Technique 73, 10191029.
Aslanidi, OV, Nikolaidou, T, Zhao, J, Smaill, BH, Gilbert, SH, Holden, AV, Lowe, T, Withers, PJ, Stephenson, RS, Jarvis, JC, Hancox, JC, Boyett, MR and Zhang, H (2013) Application of micro-computed tomography with iodine staining to cardiac imaging, segmentation, and computational model development. IEEE Transactions on Medical Imaging 32, 817.
Bagi, CM, Zakur, DE, Berryman, E, Andresen, CJ and Wilkie, D (2015) Correlation between μCT imaging, histology and functional capacity of the osteoarthritic knee in the rat model of osteoarthritis. Journal of Translational Medicine 13, 276.
Bech, M, Jensen, TH, Feidenhans, R, Bunk, O, David, C and Pfeiffer, F (2009) Soft-tissue phase-contrast tomography with an X-ray tube source. Physics in Medicine and Biology 54, 27472753.
Bradley, RS and Withers, PJ (2016) Correlative multiscale tomography of biological materials. MRS Bulletin 41, 549556.
Bradley, RS, McNeil, A and Withers, PJ (2010) An examination of phase retrieval algorithms as applied to phase contrast tomography using laboratory sources. Proc. SPIE 7804, Developments in X-Ray Tomography VII, 780404 (2 September 2010). doi:10.1117/12.860536.
Bulantová, J, Macháček, T, Panská, L, Krejčí, F, Karch, J, Jährling, N, Saghafi, S, Dodt, H-U and Horák, P (2016) Trichobilharzia regenti (Schistosomatidae): 3D imaging techniques in characterization of larval migration through the CNS of vertebrates. Micron 83, 6271.
Burnett, TL, McDonald, SA, Gholinia, A, Geurts, R, Janus, M, Slater, T, Haigh, SJ, Ornek, C, Almuaili, F, Engelberg, DL, Thompson, GE and Withers, PJ (2014) Correlative tomography. Scientific Reports 4, 4711.
Burstein, P, Bjorkholm, PJ, Chase, RC and Seguin, FH (2002) The largest and smallest X-ray computed tomography systems. Nuclear Instruments and Methods in Physics Research 221, 207212.
Bushong, EA, Johnson, DD, Kim, K-Y, Terada, M, Hatori, M, Peltier, ST, Panda, S, Merkle, A and Ellisman, MH (2015) X-ray microscopy as an approach to increasing accuracy and efficiency of serial block-face imaging for correlated light and electron microscopy of biological specimens. Microscopy and Microanalysis 21, 231238.
Cnudde, V and Boone, MN (2013) High-resolution X-ray computed tomography in geosciences: a review of the current technology and applications. Earth-Science Reviews 123, 117.
Crowther, RA, DeRosier, DJ and Klug, A (1970) The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences 317, 319340.
Cunha, L, Horvath, I, Ferreira, S, Lemos, J, Costa, P, Vieira, D, Veres, DS, Szigeti, K, Summavielle, T, Máthé, D and Metello, LF (2014) Preclinical imaging: an essential ally in modern biosciences. Molecular Diagnosis & Therapy 18, 153173.
de Kemp, RA, Epstein, FH, Catana, C, Tsui, BMW and Ritman, EL (2010) Small-animal molecular imaging methods. Journal of Nuclear Medicine 51, 1832.
de Souza e Silva, JM, Zanette, I, Noël, PB, Cardoso, MB, Kimm, MA and Pfeiffer, F (2015) Three-dimensional non-destructive soft-tissue visualization with X-ray staining micro-tomography. Scientific Reports 5, 14088.
Descamps, E, Sochacka, A, De Kegel, B, Van Loo, D, Hoorebeke, V and Adriaens, D (2014) Soft tissue discrimination with contrast agents using micro-CT scanning. Belgium Journal of Zoology 144, 2040.
Dillon, AR, Tillson, DM, Hathcock, J, Brawner, B, Wooldridge, A, Cattley, R, Welles, B, Barney, S, Lee-Fowler, T, Botzman, L, Sermersheim, M and Garbarino, R (2013) Lung histopathology, radiography, high-resolution computed tomography, and bronchio-alveolar lavage cytology are altered by Toxocara cati infection in cats and is independent of development of adult intestinal parasites. Veterinary Parasitology 193, 413426.
Dover, SD, Elliott, A and Kernaghan, AK (1981) Three-dimensional reconstruction from images of tilted specimens: the paramyosin filament. Journal of Microscopy 122, 2333.
Duke, PJ, Doan, L, Luong, H, Kelley, C, Leboeuf, W, Diep, Q, Johnson, E and Cody, DD (2009) Correlation between micro-CT sections and histological sections of mouse skull defects implanted with engineered cartilage. Gravitational and Space Biology Bulletin 22, 4550.
Egerton, RF (2005a) The scanning electron microscope. In Physical Principles of Electron Microscopy. New York: Springer US, pp. 129151.
Egerton, RF (2005b) TEM specimens and images. In Physical Principles of Electron Microscopy. New York: Springer US, pp. 93124.
Elliott, JC and Dover, SD (1982) X-ray microtomography. Journal of Microscopy 126, 211213.
Elliott, JC, Dowker, SEP and Knight, RD (1981) Scanning X-ray microradiography of a section of a carious lesion in dental enamel. Journal of Microscopy 123, 8992.
Ford, NL, Thornton, MM and Holdsworth, DW (2003) Fundamental image quality limits for microcomputed tomography in small animals. Medical Physics 30, 28692877.
Geffre, CP, Pond, E, Pond, GD, Sroka, IC, Gard, JM, Skovan, BA, Meek, WE, Landowski, TH, Nagle, RB and Cress, AE (2015) Combined micro CT and histopathology for evaluation of skeletal metastasis in live animals. American Journal of Translational Research 7, 348355.
Gignac, PM, Kley, NJ, Clarke, JA, Colbert, MW, Morhardt, AC, Cerio, D, Cost, IN, Cox, PG, Daza, JD, Early, CM, Echols, MS, Henkelman, RM, Herdina, AN, Holliday, CM, Li, Z, Mahlow, K, Merchant, S, Müller, J, Orsbon, CP, Paluh, DJ, Thies, ML, Tsai, HP and Witmer, LM (2016) Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. Journal of Anatomy 228, 889909.
Ha, YR, Kang, S-A, Ryu, J, Yeom, E, Kim, MK and Lee, SJ (2016) SPECT/CT analysis of splenic function in genistein-treated malaria-infected mice. Experimental Parasitology 170, 1015.
Hale, VL, Watermeyer, JM, Hackett, F, Vizcay-Barrena, G, van Ooij, C, Thomas, JA, Spink, MC, Harkiolaki, M, Duke, E, Fleck, RA, Blackman, MJ and Saibil, HR (2017) Parasitophorous vacuole poration precedes its rupture and rapid host erythrocyte cytoskeleton collapse in Plasmodium falciparum egress. Proceedings of the National Academy of Sciences 114, 34393444.
Handschuh, S, Baeumler, N, Schwaha, T and Ruthensteiner, B (2013) A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario. Frontiers in Zoology 10, 44.
Hanssen, E, Knoechel, C, Dearnley, M, Dixon, MWA, Le Gros, M, Larabell, C and Tilley, L (2012) Soft X-ray microscopy analysis of cell volume and hemoglobin content in erythrocytes infected with asexual and sexual stages of Plasmodium falciparum. Journal of Structural Biology 177, 224232.
Henriques, C, Henriques-Pons, A, Meuser-Batista, M, Ribeiro, A and de Souza, W (2014) In vivo imaging of mice infected with bioluminescent Trypanosoma cruzi unveils novel sites of infection. Parasites & Vectors 7, 89.
Holme, MN, Schulz, G, Deyhle, H, Weitkamp, T, Beckmann, F, Lobrinus, JA, Rikhtegar, F, Kurtcuoglu, V, Zanette, I, Saxer, T and Müller, B (2014) Complementary X-ray tomography techniques for histology-validated 3D imaging of soft and hard tissues using plaque-containing blood vessels as examples. Nature Protocols 9, 14011415.
Jia, T, Melville, S, Rg Utzinger, J, King, CH and Zhou, X (2012) Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 6, e1621.
Lee, TC, Kashyap, RL and Chu, CN (1994) Building skeleton models via 3-D medial surface axis thinning algorithms. CVGIP: Graphical Models and Image Processing 56, 462478.
Lee, CH, Im, J-G, Goo, JM, Lee, HJ, Hong, S-T, Shen, CH, Chung, DH, Son, KR, Chang, JM and Eo, H (2007) Serial CT findings of paragonimus infested dogs and the micro-CT findings of the worm cysts. Korean Journal of Radiology 8, 372.
Loussert, C, Forestier, C and Humbel, BM (2012) Correlative light and electron microscopy in parasite research. In Müller-Reichert, T and Verkade, P (eds). Correlative Light and Electron Microscopy, Elsevier, pp. 6273. doi:10.1016/B978-0-12-416026-2.00004-2.
Lowe, T, Garwood, RJ, Simonsen, TJ, Bradley, RS and Withers, PJ (2013) Metamorphosis revealed: time-lapse three-dimensional imaging inside a living chrysalis. Journal of the Royal Society Interface 10, 20130304.
Maire, E and Withers, PJ (2014) Quantitative X-ray tomography. International Materials Reviews 59, 143.
Masi, B, Perles-Barbacaru, T-A, Laprie, C, Dessein, H, Bernard, M, Dessein, A and Viola, A (2015) In vivo MRI assessment of hepatic and splenic disease in a murine model of schistosomiasis. PLoS Neglected Tropical Diseases 9, e0004036.
Metscher, BD (2009a) MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiology 9, 11.
Metscher, BD (2009b) MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Developmental Dynamics 238, 632640.
Mokso, R, Schwyn, DA, Walker, SM, Doube, M, Wicklein, M, Müller, T, Stampanoni, M, Taylor, GK and Krapp, HG (2015) Four-dimensional in vivo X-ray microscopy with projection-guided gating. Scientific Reports 5, 8727.
Momose, A, Kawamoto, S, Koyama, I, Hamaishi, Y, Takai, K and Suzuki, Y (2003) Demonstration of X-ray Talbot interferometry. Japanese Journal of Applied Physics 42, 866868.
Nierenberger, M, Rémond, Y, Ahzi, S and Choquet, P (2015) Assessing the three-dimensional collagen network in soft tissues using contrast agents and high resolution micro-CT: application to porcine iliac veins. Comptes Rendus Biologies 338, 425433.
Olivo, A and Speller, R (2007) A coded-aperture technique allowing X-ray phase contrast imaging with conventional sources. Applied Physics Letters 91, 074106.
Particelli, F, Mecozzi, L, Beraudi, A, Montesi, M, Baruffaldi, F and Viceconti, M (2012) A comparison between micro-CT and histology for the evaluation of cortical bone: effect of polymethylmethacrylate embedding on structural parameters. Journal of Microscopy 245, 302310.
Paulus, MJ, Gleason, SS, Kennel, SJ, Hunsicker, PR and Johnson, DK (2000) High resolution X-ray computed tomography: an emerging tool for small animal cancer research. Neoplasia 2, 6270.
Pauwels, E, Van Loo, D, Cornillie, P, Brabant, L and Van Hoorebeke, L (2013) An exploratory study of contrast agents for soft tissue visualization by means of high resolution X-ray computed tomography imaging. Journal of Microscopy 250, 2131.
Pullan, RL, Smith, JL, Jasrasaria, R and Brooker, SJ (2014) Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites & Vectors 7, 37.
Qin, C, Feng, J, Zhu, S, Ma, X, Zhong, J, Wu, P, Jin, Z and Tian, J (2014) Recent advances in bioluminescence tomography: methodology and system as well as application. Laser & Photonics Reviews 8, 94114.
Ritman, EL (2011) Current status of developments and applications of micro-CT. Annual Review of Biomedical Engineering 13, 531552.
Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T, Preibisch, S, Rueden, C, Saalfeld, S, Schmid, B, Tinevez, J-Y, White, DJ, Hartenstein, V, Eliceiri, K, Tomancak, P and Cardona, A (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676682.
Sena, G, Almeida, AP, Braz, D, Nogueira, LP, Colaço, MV, Soares, J, Cardoso, SC, Garcia, ES, Azambuja, P, Gonzalez, MS, Mohammadi, S, Tromba, G and Barroso, RC (2014) Phase contrast X-ray synchrotron microtomography for virtual dissection of the head of Rhodnius prolixus. Journal of Physics: Conference Series 499, 012018.
Shapiro, EM, Skrtic, S, Sharer, K, Hill, JM, Dunbar, CE and Koretsky, AP (2004) MRI detection of single particles for cellular imaging. Proceedings of the National Academy of Sciences of the United States of America 101, 1090110906.
Sharpe, J, Ahlgren, U, Perry, P, Hill, B, Ross, A, Hecksher-Sørensen, J, Baldock, R and Davidson, D (2002) Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296, 541545.
Siciliano, G and Alano, P (2015) Enlightening the malaria parasite life cycle: bioluminescent Plasmodium in fundamental and applied research. Frontiers in Microbiology 6, 391.
Speich, B, Ali, SM, Ame, SM, Bogoch, II, Alles, R, Huwyler, J, Albonico, M, Hattendorf, J, Utzinger, J and Keiser, J (2015) Efficacy and safety of albendazole plus ivermectin, albendazole plus mebendazole, albendazole plus oxantel pamoate, and mebendazole alone against Trichuris trichiura and concomitant soil-transmitted helminth infections: a four-arm, randomised controlled trial. The Lancet Infectious Diseases 15, 277284.
Stock, SR (2008) Recent advances in X-ray microtomography applied to materials. International Materials Reviews 53, 129181.
Sutherland, IA and Leathwick, DM (2011) Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends in Parasitology 27, 176181.
Tafforeau, P, Boistel, R, Boller, E, Bravin, A, Brunet, M, Chaimanee, Y, Cloetens, P, Feist, M, Hoszowska, J, Jaeger, J-J, Kay, RF, Lazzari, V, Marivaux, L, Nel, A, Nemoz, C, Thibault, X, Vignaud, P and Zabler, S (2006) Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Applied Physics A 83, 195202.
Ter-Pogossian, MM, Phelps, ME, Hoffman, EJ and Mullani, NA (1975) A positron-emission transaxial tomograph for nuclear imaging (PETT). Radiology 114, 8998.
Vercruysse, J, Albonico, M, Behnke, JM, Kotze, AC, Prichard, RK, McCarthy, JS, Montresor, A and Levecke, B (2011) Is anthelmintic resistance a concern for the control of human soil-transmitted helminths? International Journal for Parasitology 1, 1427.
Vickerton, P, Jarvis, J and Jeffery, N (2013) Concentration-dependent specimen shrinkage in iodine-enhanced microCT. Journal of Anatomy 223, 185193.
Voieta, I, de Queiroz, LC, Andrade, LM, Silva, LCS, Fontes, VF, Barbosa, A Jr, Resende, V, Petroianu, A, Andrade, Z, Antunes, CM and Lambertucci, JR (2010) Imaging techniques and histology in the evaluation of liver fibrosis in hepatosplenic schistosomiasis mansoni in Brazil: a comparative study. Memórias do Instituto Oswaldo Cruz 105, 414421.
Winkler, B (2006) Applications of neutron radiography and neutron tomography. Reviews in Mineralogy and Geochemistry 63, 459471.
Withers, PJ (2007) X-ray nanotomography. Materials Today 10, 2634.
Wolstenholme, AJ, Fairweather, I, Prichard, R, von Samson-Himmelstjerna, G and Sangster, NC (2004) Drug resistance in veterinary helminths. Trends in Parasitology 20, 469476.
Wu, J (2014) Propagation based X-ray phase-contrast imaging technique for the microstructure analysis of biological soft tissues. Optik – International Journal for Light and Electron Optics 125, 10621064.
Zamir, A, Endrizzi, M, Hagen, CK, Vittoria, FA, Urbani, L, De Coppi, P and Olivo, A (2016) Robust phase retrieval for high resolution edge illumination X-ray phase-contrast computed tomography in non-ideal environments. Scientific Reports 6, 31197.
Zanette, I, Weitkamp, T, Le Duc, G and Pfeiffer, F (2013) X-ray grating-based phase tomography for 3D histology. RSC Advances 3, 19816.

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