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The Use of Texture Analysis in the Morpho-Functional Characterization of Mast Cell Degranulation in Rainbow Trout (Onchorhynchus mykiss)

Published online by Cambridge University Press:  04 September 2013

Maurizio Manera
Maurizio Manera*
Affiliation:
Faculty of Biosciences, Agro-Alimentary and Environmental Technologies, University of Teramo, St Crispi 212, I-64100 Teramo, Italy Centre of Environmental Education, Protection, Research and Documentation, Municipality of Notaresco, St Pontecavalcavia, I-64024 Notaresco (TE), Italy
*
*Corresponding author. E-mail: [email protected]
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Abstract

Degranulation of intestinal mast cells in rainbow trout was studied ex vivo by means of texture analysis and related to the maximal intestinal contraction elicited by degranulation itself. Two strips from the same intestinal segment from ten trout were sampled, processed for light microscopy and stained with Giemsa solution. One of the two strips was exposed to an incremental dose of compound 48/80 in an isolated organ bath before processing. Gray-level RGB channel equivalent and 8-bit gray-level images of five granular cytoplasm areas of mast cells for each section were analyzed for texture features and to evaluate discrimination possibility between treatment groups by means of linear discriminant analysis according to feature selection methods and RGB stacks. Differential mean values (after–before compound 48/80) of the green (r2 = 0.84, p < 0.01) and blue (r2 = 0.83, p < 0.01) RGB channels and 8-bit grayscale (r2 = 0.76, p < 0.05) image correlated significantly with the respective value of maximal intestinal contraction. A possible acidic (anionic) nature for the putative pro-contractile basophil agonist can be inferred.

Keywords

image analysisgray-level analysisisolated organ bathpro-contractile agonistintestinehistochemistryGiemsa's stain
Type
Biomedical and Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 6 , December 2013 , pp. 1436 - 1444
Copyright
Copyright © Microscopy Society of America 2013 

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References

Benattar, L. & Flandrin, G. (1999). Morphometry and quality control for a May-Grunwald Giemsa stained preparation. A 40 centers cooperative study. Leuk Lymph 33, 587–591.Google Scholar
Burka, J.F., Briand, H.A., Blair, R.M.J., Purcell, L.M. & Calder, G.F. (1990). The effects of temperature on contractile mechanisms of rainbow trout (Salmo gairdneri) intestine. Can J Physiol Pharm 68, 700–704.Google Scholar
Castellano, G., Bonilha, L., Li, L.M. & Cendes, F. (2004). Texture analysis of medical images. Clin Radiol 59, 1061–1069.CrossRefGoogle ScholarPubMed
Dezfuli, B.S. & Giari, L. (2008). Mast cells in the gills and intestines of naturally infected fish: Evidence of migration and degranulation. J Fish Dis 31, 845–852.CrossRefGoogle ScholarPubMed
Diamond, J., Anderson, N.H., Bartels, P.H., Montironi, R. & Hamilton, P.W. (2004). The use of morphological characteristics and texture analysis in the identification of tissue composition in prostatic neoplasia. Human Pathol 35, 1121–1131.CrossRefGoogle ScholarPubMed
Ekman-Ordeberg, G., Akerud, A., Dubicke, A., Malmström, A. & Hellgren, M. (2010). Does low molecular weight heparin shorten term labor? Acta Obstet Gynecol Scand 89, 147–150.Google Scholar
Ekman-Ordeberg, G., Hellgren, M., Akerud, A., Andersson, E., Dubicke, A., Sennstrom, M., Byström, B., Tzortzatos, G., Gomez, M.F., Edlund, M., Lindahl, U. & Malmström, A. (2009). Low molecular weight heparin stimulates myometrial contractility and cervical remodeling in vitro. Acta Obstet Gynecol Scand 88, 984–989.Google Scholar
Ekman-Ordeberg, G. & Malmström, A. (2008). Use of sulfated glycosaminoglycans for establishing effective labor in women. U.S. Patent Application Publication. US 2008/0269165 A1. Google Scholar
Ellis, A.E. (1977). The leucocytes of fish. A review. J Fish Biol 11, 453–491.CrossRefGoogle Scholar
Ezeasor, D.N. & Stokoe, W.M. (1980). A cytochemical, light and electron microscopic study of the eosinophilic granule cells in the gut of the rainbow trout, Salmo gairdneri Richardson. J Fish Biol 17, 619–634.Google Scholar
Flaño, E., López-Fierr, P., Razquin, B. & Villena, A. (1996). In vitro differentiation of eosinophilic granular cells in Renibacterium salmoninarum-infected gill cultures from rainbow trout. Fish Shellfish Immunol 6, 173–184.CrossRefGoogle Scholar
Gonzales, R.C. & Woods, R.E. (2008). Digital Image Processing. Upper Saddle River, NJ: Prentice Hall.Google Scholar
Hammel, I., Shoichetman, T., Amihai, D., Galli, S.J. & Skutelsky, E. (2010). Localization of anionic constituents in mast cell granules of brachymorphic (bm/bm) mice by using avidin-conjugated colloidal gold. Cell Tissue Res 339, 561–570.CrossRefGoogle ScholarPubMed
Haralick, R.M. (1979). Statistical and structural approaches to texture. Proc IEEE 67, 786–804.CrossRefGoogle Scholar
Haralick, R.M., Shanmugam, K. & Dinstien, I. (1973). Textural features for image classification. IEEE Trans Syst Man Cyber 6, 610–621.Google Scholar
He, S.H. (2004). Key role of mast cells and their major secretory products in inflammatory bowel disease. World J Gastroenterol 10(3), 309–318.CrossRefGoogle ScholarPubMed
Herlidou-Même, S., Constans, J.M., Carsin, B., Olivie, D., Eliat, P.A., Nadal-Desbarats, L., Gondry, C., Le Rumeur, E., Idy-Peretti, I. & de Certaines, J.D. (2003). MRI texture analysis on texture test objects, normal brain and intracranial tumors. Magn Reson Imaging 21, 989–993.CrossRefGoogle ScholarPubMed
Horobin, R.W. & Walter, K.J. (1987). Understanding Romanowsky staining. I. The Romanowsky-Giemsa effect in blood smears. Histoch 86, 331–336.Google Scholar
Kiernan, J.A. (2010). On chemical reactions and staining mechanisms. In Education Guide—Special Stains and H & E, Kumar, G.L. & Kiernan, J.A. (Eds.), pp. 167–176. Carpinteria, CA: Dako North America.Google Scholar
Leknes, I.L. (2007). Eosinophilic granule cells and endocytic cells in intestinal wall of pearl gouramy (Anabantidae: Teleostei). Fish Shellfish Immun 23, 897–900.Google Scholar
Li, E., Zhao, A., Shea-Donohue, T. & Singer, S.M. (2007). Mast cell-mediated changes in smooth muscle contractility during mouse giardiasis. Infect Immun 75, 4514–4518.Google Scholar
Loukas, C.G. & Linney, A. (2004). A survey on histological image analysis-based assessment of three major biological factors influencing radiotherapy: Proliferation, hypoxia and vasculature. Comput Meth Progr Bio 74, 183–199.CrossRefGoogle ScholarPubMed
Mahmoud-Ghoneima, D., Cherelb, Y., Lemairec, L., de Certainesa, J.D. & Manière, A. (2006). Texture analysis of magnetic resonance images of rat muscles during atrophy and regeneration. Magn Reson Imaging 24, 167–171.Google Scholar
Manera, M. & Borreca, C. (2012). Assessment of mast cells degranulation in rainbow trout (Oncorhynchus mykiss Walbaum) by means of gray-level and texture analysis (gray level correlation matrices). Res Vet Sci 93, 886–891.Google Scholar
Manera, M. & Britti, D. (2006). Assessment of blood chemistry normal ranges in rainbow trout. J Fish Biol 69, 1427–1434.CrossRefGoogle Scholar
Manera, M. & Britti, D. (2008). Assessment of serum protein fractions in rainbow trout using automated electrophoresis and densitometry. Vet Clin Pathol 37, 452–456.CrossRefGoogle ScholarPubMed
Manera, M., Giammarino, A., Borreca, C., Giari, L. & Dezfuli, B.S. (2011). Degranulation of mast cells due to compound 48/80 induces concentration-dependent intestinal contraction in rainbow trout (Oncorhynchus mykiss Walbaum) ex vivo. J Exp Zool Part A: Ecol Gen Physiol 315, 447–457.CrossRefGoogle ScholarPubMed
Manera, M., Giammarino, A., Perugini, M. & Amorena, M. (2008). In vitro evaluation of gut contractile response to histamine in rainbow trout (Oncorhynchus mykiss Walbaum, 1792). Res Vet Sci 84, 126–131.Google Scholar
Materka, A. (1998–2005). MaZda user's manual . Available at http://www.eletel.p.lodz.pl/programy/mazda/download/mazda_manual.pdf. Accessed May 19, 2013.Google Scholar
Materka, A. & Strzelecki, M. (1998). Texture analysis methods—A review. COST B11 Report, Brussels. Available at http://www.eletel.p.lodz.pl/programy/cost/pdf_1.pdf. Accessed May 19, 2013.Google Scholar
Matsuyama, T. & Iida, T. (1999). Degranulation of eosinophilic granular cells with possible involvement in neutrophil migration to site of inflammation in tilapia. Develop Comp Immunol 23, 451–457.Google Scholar
Mulero, I., Pilar Sepulcre, M., Meseguer, J., García-Ayala, A. & Mulero, V. (2007). Histamine is stored in mast cells of most evolutionarily advanced fish and regulates the fish inflammatory response. P Natl Acad Sci USA 104, 19434–19439.Google Scholar
Murata, S.I., Herman, P. & Lakowicz, J.R. (2001). Texture analysis of fluorescence lifetime images of nuclear DNA with effect of fluorescence resonance energy transfer. Cytometry 43, 94–100.Google Scholar
Paton, W.D.N. (1951). Compound 48/80: A potent histamine liberator. Br J Pharmacol Chemoter 6, 499–508.Google Scholar
Reite, O.B. (1997). Mast cells/eosinophilic granule cells of salmonids: Staining properties and responses to noxious agents. Fish Shellfish Immunol 7, 567–584.Google Scholar
Reite, O.B. (1998). Mast cells/eosinophilic granule cells of teleostean fish: A review focusing on staining properties and functional responses. Fish Shellfish Immunol 8, 489–513.Google Scholar
Reite, O.B. & Evensen, Ø. (2006). Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunol 20, 192–208.Google Scholar
Rijnierse, A., Nijkamp, F.P. & Kraneveld, A.D. (2007). Mast cells and nerves tickle in the tummy implications for inflammatory bowel disease and irritable bowel syndrome. Pharmacol Therapeut 116, 207–235.Google Scholar
Rocha, J.S. & Chiarini-Garcia, H. (2007). Mast cell heterogeneity between two different species of Hoplias sp. (Characiformes: Erythrinidae): Response to fixatives, anatomical distribution, histochemical contents and ultrastructural features. Fish Shellfish Immunol 22, 218–229.Google Scholar
Rothschild, A.M. (1970). Mechanisms of histamine release by compound 48/80. Brit J Pharmacol 38, 253–262.CrossRefGoogle ScholarPubMed
Sanderson, J.B. (1994). Biological Microtechnique. Oxford, UK: BIOS Scientific Publications & Royal Microscopical Society.Google Scholar
Schmale, M.C., Vicha, D. & Cacal, S.M. (2004). Degranulation of eosinophilic granule cells in neurofibromas and gastrointestinal tract in the bicolor damselfish. Fish Shellfish Immunol 17, 53–63.Google Scholar
Sertel, O., Kong, J., Catalyurek, U.V., Lozanski, G., Saltz, J.H. & Gurcan, M.N. (2009). Histopathological image analysis using model-based intermediate representations and color texture: Follicular lymphoma grading. J Sign Proc Syst 55, 169–183.CrossRefGoogle Scholar
Sharipo, E., Hartanto, V. & Lepor, H. (1992). Quantifying the smooth muscle content of the prostate using double-immunoenzymatic staining and color assisted image analysis. J Urol 147, 1167–1170.Google Scholar
Silphaduang, U., Colorni, A. & Noga, E.J. (2006). Evidence for widespread distribution of piscidin antimicrobial peptides in teleost fish. Dis Aquat Org 72, 241–252.CrossRefGoogle ScholarPubMed
Sire, M. & Vernier, J.M. (1995). Partial characterisation of eosinophilic granule cells (EGCs) and identification of mast cell of the intestinal lamina propria in rainbow trout (Oncorhynchus mykiss). Biochemical and cytochemical study. Biol Cell 85, 35–41.Google Scholar
Skutelsky, E., Shoichetman, T. & Hammel, H. (1995). An histochemical approach to characterization of anionic constituents in mast cell secretory granules. Histoch Cell Biol 104, 453–458.Google Scholar
Stenton, G.R., Vliagoftis, H. & Befus, A.D. (1998). Role of intestinal mast cells in modulating gastrointestinal pathophysiology. Ann All Asthma Immunol 81, 1–15.Google Scholar
Strzelecki, M., Szczypinski, P., Materka, A. & Klepaczko, A. (2013). A software tool for automatic classification and segmentation of 2D/3D medical images. Nucl Instr Meth Phys Res A 702, 137–140.Google Scholar
Szczypinski, P., Klepaczko, A., Pazurek, M. & Piotr, D. (2012). Texture and color based image segmentation and pathology detection in capsule endoscopy videos. Comput Meth Programs Biomed (ahead of print). doi:10.1016/j.cmpb.2012.09.004. Available at www.ncbi.nlm.hih.gov/pubmed/23164524; www.sciencedirect.com/science/article/pii/S0169260712002192.Google Scholar
Szczypinski, P., Strzelecki, M. & Materka, A. (2007). MaZda—A software for texture analysis. In Proceedings of ISITC, Kim, H., Song, S.S., Strzelecki, M., Choi, J., An, D.U. & Kim, S. (Eds.), pp. 245–249. Jeonju, Korea: Institute of Electrical and Electronics Engineers.Google Scholar
Szczypinski, P., Strzelecki, M., Materka, A. & Klepaczko, A. (2009). MaZda—A software package for image texture analysis. Comput Meth Programs Biomed 94, 66–76.Google Scholar
Van Nassauw, L., Adriaensen, D. & Timmermans, J.P. (2007). The bidirectional communication between neurons and mast cells within the gastrointestinal tract. Auton Neurosci 133, 91–103.Google Scholar
Weller, P.F., Ackerman, S.J. & Smith, J.A. (1988). Eosinophil granule cationic proteins: Major basic protein is distinct from the smaller subunit of eosinophil peroxidase. J Leukocyte Biol 43, 1–4.Google Scholar
Wittekind, D.H. (1983). On the nature of Romanowsky-Giemsa staining and its significance for cytochemistry and histochemistry: An overall review. Histoch J 15, 1029–1047.Google Scholar
Yu, O., Mauss, Y., Zollner, G., Nmaer, I.J. & Chambron, J. (1999). Distinct patterns of active and non-active plaques using texture analysis on brain NMR images in multiple sclerosis patients: Preliminary results. Magn Reson Imaging 17, 1261–1267.Google Scholar