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Three-dimensional pore space quantification of apple tissue using X-ray computed microtomography

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Abstract

The microstructure and the connectivity of the pore space are important variables for better understanding of the complex gas transport phenomena that occur in plant tissues. In this study, we present an experimental procedure for image acquisition and image processing to quantitatively characterize in 3D the pore space of apple tissues (Malus domestica Borkh.) for two cultivars (Jonagold and Braeburn) taken from the fleshy part of the cortex using X-ray computer microtomography. Preliminary sensitivity analyses were performed to determine the effect of the resolution and the volume size (REV, representative elementary volume analysis) on the computed porosity of apple samples. For comparison among cultivars, geometrical properties such as porosity, specific surface area, number of disconnected pore volumes and their distribution parameters were extracted and analyzed in triplicate based on the 3D skeletonization of the pore space (medial axis analysis). The results showed that microtomography provides a resolution at the micrometer level to quantitatively analyze and characterize the 3D topology of the pore space in apple tissue. The computed porosity was confirmed to be highly dependent of the resolution used, and the minimum REV of the cortical flesh of apple fruit was estimated to be 1.3 mm3. Comparisons among the two cultivars using a resolution of 8.5 μm with a minimum REV cube showed that in spite of the complexity and variability of the pore space network observed in Jonagold and Braeburn apples, the extracted parameters from the medial axis were significantly different (P-value < 0.05). Medial axis parameters showed potential to differentiate the microstructure between the two evaluated apple cultivars.

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Abbreviations

CCD:

Charge-coupled device

CT:

Computed tomography

REV:

Representative elementary volume

ROI:

Region of interest

SSA:

Specific surface area

STD:

Standard deviation

2D:

Two-dimensional

3D:

Three-dimensional

References

  • Aguilera JM (2005) Why food microstructure? J Food Eng 67:3–11

    Article  Google Scholar 

  • Babin P, Della Valle G, Dendievel R, Lassoued N, Salvo L (2005) Mechanical properties of bread crumbs from tomography based finite element simulations. J Mat Sci 40:5867–5873

    Article  CAS  Google Scholar 

  • Baoping J (1999) Nondestructive technology for fruits grading. In: Proceedings of 99th international conference on agricultural engineering Beijing, December, pp IV127–IV133

  • Barcelon EG, Tojo S, Watanabe K (1999) X-ray computed tomography for internal quality evaluation of peaches. J Agric Eng Res 73:323–330

    Article  Google Scholar 

  • Baumann H, Henze J (1983) Intercellular space volume of fruit. Acta Hortic 138:107–111

    Google Scholar 

  • Bear J (1972) Dynamics of fluids in porous media. Dover, New York

    Google Scholar 

  • Calbo AG, Sommer NF (1987) Intercellular volume and resistance to air flow of fruits and vegetables. J Am Soc Hortic Sci 112:131–134

    Google Scholar 

  • Celia M, Reeves P, Ferrand L (1995) Recent advances in pore scale models for multiphase flow in porous media. Rev Geophys Suppl 33:1049–1057

    Article  Google Scholar 

  • Cheng Q, Banks NH, Nicholson SE, Kingsley AM, Mackay BR (1998) Effects of temperature on gas exchange of ‘Braeburn’ apples. NZ J Crop Hortic Sci 26:299–306

    Google Scholar 

  • Dražeta L, Lang A, Alistair JH, Richard KV, Paula EJ (2004) Air volume measurement of ‘Braeburn’ apple fruit. J Exp Bot 55:1061–1069

    Article  PubMed  CAS  Google Scholar 

  • Esau K (1977) Anatomy of seed plants. Wiley, New York

    Google Scholar 

  • Fromm JH, Sautter I, Matthies D, Kremer J, Schumacher P, Ganter C (2001) Xylem water content and wood density in spruce and oak trees detected by high-resolution computed tomography. Plant Physiol 127:416–425

    Article  PubMed  CAS  Google Scholar 

  • Goffinet MC, Robinson TL, Lakso AN (1995) A comparison of ‘Empire’ apple fruit size and anatomy in unthinned and handthinned trees. J Hortic Sci 70:375–387

    Google Scholar 

  • Harker FR, Ferguson IB (1988) Calcium ion transport across discs of the cortical flesh of apple fruit in relation to fruit development. Physiol Plant 74:695–700

    Article  CAS  Google Scholar 

  • Harker FR, Hallet IC (1992) Physiological changes associated with development of mealiness of apple fruit during cool storage. HortScience 27:1291–1294

    Google Scholar 

  • Harker FR, Watkins CB, Brookfield PL, Miller MJ, Reid S, Jackson PJ, Bieleski RL, Bartley T (1999) Maturity and regional influences on watercore development and its postharvest disappearance in ‘Fuji’ apples. J Am Soc Hortic Sci 124:166–172

    Google Scholar 

  • Helmig R, Miller CT, Jakobs H, Class H, Hilpert M, Kees CE, Niessner J (2006) Multiphase flow and transport modeling in heterogeneous porous media. In: Di Bucchianico A, Mattheij RMM, Peletier MA (eds) Progress in industrial mathematics at ECMI 2004. Springer, Heidelberg, pp 449–485

  • Ho QT, Verlinden BE, Verboven P, Vandewalle S, Nicolaï BM (2006) A permeation–diffusion-reaction model of gas transport in cellular tissue of plant materials. J Exp Bot (in press)

  • Kader AA (1988) Respiration and gas exchange of vegetables. In: Weichmann J (ed) Postharvest physiology of vegetables. Marcel Dekker, New York, pp 25–43

    Google Scholar 

  • Khan AA, Vincent JFV (1990) Anisotropy of apple parenchyma. J Sci Food Agric 52:455–466

    Article  Google Scholar 

  • Khan AA, Vincent JFV (1993a) Compressive stiffness and fracture properties of apple and potato parenchyma. J Texture Stud 24:423–435

    Article  Google Scholar 

  • Khan AA, Vincent JFV (1993b) Anisotropy in the fracture properties of apple flesh as investigated by crack-opening tests. J Mat Sci 28:45–51

    Article  Google Scholar 

  • Kuroki S, Oshita S, Sotome I, Kawagoe Y, Seo Y (2004) Visualization of 3-D network of gas-filled intercellular spaces in cucumber fruit after harvest. Postharvest Biol Technol 33:255–262

    Article  Google Scholar 

  • Lammertyn J, Dresselaers T, Van Hecke P, Jancsók P, Wevers M, Nicolaï B (2003a) Analysis of the time course of core breakdown in ‘Conference’ pears by means of MRI and X-ray CT. Postharvest Biol Technol 29:19–28

    Article  CAS  Google Scholar 

  • Lammertyn J, Dresselaers T, Van Hecke P, Jancsók P, Wevers M, Nicolaï B (2003b) MRI and X-ray CT study of spatial distribution of core breakdown in ‘Conference’ pears. Magn Reson Imaging 21:805–815

    Article  CAS  Google Scholar 

  • Lee T-C, Kashyap R, Chu C-N (1994) Building skeleton models via 3-d medial surface/axis thinning algorithms. CVGIP Graph Models Image Process 56:462–478

    Article  Google Scholar 

  • Lim KS, Barigou M (2004) X-ray micro-computed tomography of aerated cellular food products. Food Res Int 37:1001–1012

    Article  Google Scholar 

  • Lindquist WD (1999) 3DMA general users manual. State of New York at Stony Brook, New York

    Google Scholar 

  • Lindquist WD, Lee S-M, Coker D, Jones K, Spanne P (1996) Medial axis analysis of three dimensional tomographic images of drill core samples. J Geophys Res 101B:8297–8310

    Article  Google Scholar 

  • Mardia KV, Hainsworth TJ (1988) A spatial thresholding method for image segmentation. IEEE Trans Pattern Anal Mach Intell 6:919–927

    Article  Google Scholar 

  • Maire E, Buffière J-Y, Salvo L, Blandin JJ, Ludwig W, Létang JM (2001) On the application of X-ray microtomography in the field of material science. Adv Eng Mater 3:539–546

    Article  CAS  Google Scholar 

  • Maire E, Fazekas A, Salvo L, Dendievel R, Youssef S, Cloetens P, Letang J.M (2003) X-ray tomography applied to the characterization of cellular materials. Related finite element modeling problems. Compos Sci Technol 63:2431–2443

    Article  Google Scholar 

  • Mebatsion HK, Verboven P, Verlinden BE, Ho QT, Nguyen TA, Nicolaï B (2006a) Microscale modeling of fruit tissue using Voronoi tessellations. Comput Electron Agric 52:36–48

    Article  Google Scholar 

  • Mebatsion HK, Verboven P, Ho QT, Mendoza F, Verlinden BE, Nguyen TA, Nicolaï B (2006b) Modeling fruit microstructure using novel ellipse tessellations algorithm. Comp Modeling Eng Sci 14:1–14

    Google Scholar 

  • Oh W, Lindquist W (1999) Image thresholding by indicator kriging. IEEE Trans Pattern Anal Mach Intell 21:590–602

    Article  Google Scholar 

  • Rajapakse NC, Banks NH, Hewett EW, Cleland DJ (1990) Development of oxygen concentration gradients in flesh tissues of bulky plant organs. J Am Soc Hortic Sci 115:793–797

    CAS  Google Scholar 

  • Raven JA (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Ann Bot 78:137–142

    Article  Google Scholar 

  • Ruess F, Stösser R (1993) Untersuchungen über das interzellularsystem bei apfelfrüchten mit methoden der digitalen bildverarbeitung. Gartenbauwissenschaft 58:197–205

    Google Scholar 

  • Russ JC (2005) Image analysis of food microstructure. Boca Raton, London

    Google Scholar 

  • Salvo L, Cloetens P, Maire E, Zabler S, Blandin JJ, Buffière JY, Ludwig W, Boller E, Bellet D, Josserond C (2003) X-ray micro-tomography an attractive characterisation technique in material science. Nucl Instrum Methods Phys Res B200:273–286

    Google Scholar 

  • Schotsmans W, Verlinden BE, Lammertyn J, Nicolaï BM (2004) The relationship between gas transport properties and the histology of apple. J Sci Food Agric 84:1131–1140

    Article  CAS  Google Scholar 

  • Soudain P, Phan Phuc A (1979) La diffusion des gaz dans les tissus vegetaux en rapport avec la structure des organes massifs. In: Perspectives nouvelles dans la conservation des fruits et legumes frais. Seminaire International, Centre de Recherches en Sciences Appliquées à l’Alimentation, L’Université du Québec à Montreal, Canada, pp 67–86

  • Thovert J, Salles J, Adler P (1993) Computerized characterization of the geometry of real porous media: their discretization, analysis and interpretation. J Microsc 170:65–79

    Google Scholar 

  • Tu K, De Baerdemaeker J, Deltour R, de Barsy T (1996) Monitoring post-harvest quality of Granny Smith apple under simulated shelf-life conditions: destructive, non-destructive and analytical measurements. Int J Food Sci Technol 31:267–276

    Article  CAS  Google Scholar 

  • van Dalen G, Blonk H, van Aalst H, Hendriks CL (2003) 3D imaging of foods using X-ray microthomography. GIT Imaging Microsc 3:18–21

    Google Scholar 

  • Vincent JFV (1989) Relationships between density and stiffness of apple flesh. J Sci Food Agric 31:267–276

    Google Scholar 

  • Volz RK, Harker FR, Hallet IC, Lang A (2004) Development of texture in apple fruit—a biophysical perspective. Acta Hort 636:473–479

    Google Scholar 

  • Westwood MN, Batjer LP, Billingsley HD (1967) Cell size, cell number and fruit density of apples as related to fruit size, position in the cluster and thinning method. Proc Am Soc Hortic Sci 91:51–62

    Google Scholar 

  • Yamaki S, Ino M (1992) Alteration of cellular compartmentation and membrane permeability to sugars in immature and mature apple fruit. J Am Soc Hortic Sci 117:951–954

    CAS  Google Scholar 

  • Yearsley CW, Banks NH, Ganesh S, Cleland DJ (1996) Determination of lower oxygen limits for apple fruit. Postharvest Biol Technol 8:95–109

    Article  CAS  Google Scholar 

  • Yearsley CW, Banks NH, Ganesh S (1997a) Temperature effects on the internal lower oxygen limits of apple fruit. Postharvest Biol Technol 11:73–83

    Article  Google Scholar 

  • Yearsley CW, Banks NH, Ganesh S (1997b) Effects of carbon dioxide on the internal lower oxygen limits of apple fruit. Postharvest Biol Technol 12:1–13

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank K.U. Leuven (Project OT 04/31) and the Fund for Scientific Research Flanders (FWO—Vlaanderen, Project G.0200.02) for financial support for this investigation.

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Authors and Affiliations

  1. BIOSYST, MeBioS, Faculty of Bioscience Engineering, Katholieke Universiteit Leuven, W. de Croylaan 42, 3001, Leuven, Belgium

    Fernando Mendoza, Pieter Verboven, Hibru K. Mebatsion & Bart Nicolaï

  2. Materials Performance and Non-Destructive Evaluation, Department of Metallurgy and Materials Engineering (MTM), Katholieke Universiteit Leuven, Kastelpark Arenberg 44, 3001, Leuven, Belgium

    Greet Kerckhofs & Martine Wevers

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  1. Fernando Mendoza
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  2. Pieter Verboven
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  3. Hibru K. Mebatsion
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  4. Greet Kerckhofs
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  5. Martine Wevers
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  6. Bart Nicolaï
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Correspondence to Fernando Mendoza.

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Mendoza, F., Verboven, P., Mebatsion, H.K. et al. Three-dimensional pore space quantification of apple tissue using X-ray computed microtomography. Planta 226, 559–570 (2007). https://doi.org/10.1007/s00425-007-0504-4

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