Automated quantitative characterization of alginate/hydroxyapatite bone tissue engineering scaffolds by means of micro-CT image analysis

Journal of Materials Science: Materials in Medicine

Volumn 22, Issue 12, 2011, Pages 2617-2629

  Brun, Francesco ^a,b   Turco, Gianluca ^a   Accardo, Agostino ^a   Paoletti, Sergio ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b SINCROTRONE TRIESTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYSIS PROCESS; AUTOMATED SEGMENTATION; BONE TISSUE ENGINEERING; CRITICAL ISSUES; DATA SETS; DESCRIPTORS; MANUAL SEGMENTATION; MICRO ARCHITECTURES; MICRO CT; QUALITATIVE OBSERVATIONS; QUANTITATIVE CHARACTERIZATION; QUANTITATIVE INFORMATION; TISSUE ENGINEERING SCAFFOLD; VOLUME OF INTEREST; X-RAY COMPUTED MICROTOMOGRAPHY;

BONE; HYDROXYAPATITE; IMAGE ANALYSIS; IMAGING TECHNIQUES; NETWORK ARCHITECTURE; QUALITY CONTROL; SCAFFOLDS (BIOLOGY); TISSUE;

COMPUTERIZED TOMOGRAPHY;

ALGINIC ACID; HYDROXYAPATITE; TISSUE SCAFFOLD; GLUCURONIC ACID; HEXURONIC ACID;

ARTICLE; AUTOMATION; BONE TISSUE; IMAGE ANALYSIS; MICRO-COMPUTED TOMOGRAPHY; PRIORITY JOURNAL; TISSUE ENGINEERING; ANISOTROPY; BONE; CHEMISTRY; COMPUTER PROGRAM; IMAGE PROCESSING; MATERIALS TESTING; POROSITY; PROCEDURES; THREE DIMENSIONAL IMAGING; TISSUE SCAFFOLD; X RAY;

ALGINATES; ANISOTROPY; AUTOMATION; BONE AND BONES; DURAPATITE; GLUCURONIC ACID; HEXURONIC ACIDS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MATERIALS TESTING; POROSITY; SOFTWARE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; X-RAY MICROTOMOGRAPHY; X-RAYS;

EID: 84355162198     PISSN: 09574530     EISSN: 15734838     Source Type: Journal    
DOI: 10.1007/s10856-011-4447-8     Document Type: Article

References (46)

1. JD Bobyn RM Pilliar HU Cameron GC Weatherly 1980 The optimum pore size for the fixation of porous surfaced metal implants by the ingrowth of bone Clin Orthop Relat Res 150 263 270 (Pubitemid 10039063)
2. F Brun D Dreossi 2010 Efficient curve-skeleton computation for the analysis of biomedical 3D images Biomed Sci Instrum 46 475 480
3. F Brun L Mancini P Kasae S Favretto D Dreossi G Tromba 2010 Pore3D: a software library for quantitative analysis of porous media Nucl Instrum Methods Phys Res A 615 326 332 10.1016/j.nima.2010.02.063 1:CAS:528:DC%2BC3cXjvFSrsro%3D
4. S Cartmell K Huynh A Lin S Nagaraja R Guldberg 2010 Quantitative microcomputed tomography analysis of mineralization within threedimensional scaffolds in vitro J Biomed Mater Res A 69 97 104
5. A Darling W Sun 2004 3D microtomographic characterization of precision extruded poly-ε-caprolactone tissue scaffolds J Biomed Mater Res A 70 311 317 10.1002/jbm.b.30050 1:STN:280:DC%2BD2czlvFSnuw%3D%3D (Pubitemid 39006910)
6. A Elmoutaouakkil G Fuchs P Bergounhon R Peres F Peyrin 2003 Three-dimensional quantitative analysis of polymer foams from synchrotron radiation X-ray microtomography J Phys D 2003 37 43 10.1088/0022-3727/36/10A/308
7. R Filmon RN Gaborit F Grizon M Galloyer C Cincu MF Basle D Chappard 2002 Non-connected versus interconnected macroporosity in poly(2-hydroxyethyl methacrylate) polymers. An X-ray microtomographic and histomorphometric study J Biomater Sci Polym Ed 13 1105 1117 10.1163/156856202320813828 1:CAS:528:DC%2BD38XpsFCktro%3D (Pubitemid 35402147)
8. T Hildebrand P Rüegsegger 1997 A new method for the model-independent assessment of thickness in three-dimensional images J Microsc 185 67 75 10.1046/j.1365-2818.1997.1340694.x (Pubitemid 27060526)
9. A Hilldore A Wojtowicz AW Johnson 2006 Micro-CT based quantification of non-mineralized tissue on cultured hydroxyapatite scaffolds J Biomed Mater Res A 82 1012 1021
10. A Hilldore AW Morgan JR Woodard AJ Wagoner Johnson 2009 The curve integration method is comparable to manual segmentation for the analysis of bone/scaffold composites using micro-CT J Biomed Mater Res B 88 271 279
11. ST Ho DW Hutmacher 2006 A comparison of micro CT with other techniques used in the characterization of scaffolds Biomaterials 27 1362 1376 10.1016/j.biomaterials.2005.08.035 1:CAS:528:DC%2BD2MXht1Klu7bF (Pubitemid 41739562)
12. SJ Hollister 2005 Porous scaffold design for tissue engineering Nat Mater 4 518 524 10.1038/nmat1421 1:CAS:528:DC%2BD2MXlvFOis7Y%3D (Pubitemid 40952745)
13. SF Hulbert FA Young RS Mathews JJ Klawitter CD Talbert FH Stelling 1970 Potential of ceramic materials as permanently implantable skeletal prostheses J Biomed Mater Res 4 433 456 10.1002/jbm.820040309 1:STN:280: DyaE3M%2FgsVaqtg%3D%3D
14. 3Ap-collagen sponges using X-ray high-resolution microtomography Biomaterials 25 2577 2583 10.1016/j. biomaterials.2003.09.071 1:CAS:528:DC%2BD2cXmtFChsw%3D%3D (Pubitemid 38147448)
15. AC Jones B Milthorpe H Averdunk A Limaye TJ Senden A Sakellariou AP Sheppard RM Sok MA Knackstedt A Brandwood D Rohner DW Hutmacher 2004 Analysis of 3D bone ingrowth into polymer scaffolds via micro-computed tomography imaging Biomaterials 25 4947 4954 10.1016/j.biomaterials.2004.01.047 1:CAS:528:DC%2BD2cXjtlymsb0%3D (Pubitemid 38520825)
16. JN Kapur PK Sahoo AKC Wong 1985 A new method for gray-level picture thresholding using the entropy of the histogram Graph Models Image Process 29 273 285 10.1016/0734-189X(85)90125-2 (Pubitemid 15510905)
17. V Karageorgiou D Kaplan 2005 Porosity of 3D biomaterial scaffolds and osteogenesis Biomaterials 26 5474 5491 10.1016/j.biomaterials.2005.02.002 1:CAS:528:DC%2BD2MXjs1Wnsrc%3D (Pubitemid 40592136)
18. Karande TS, Agrawal CM. Functions and requirements of synthetic scaffolds in tissue engineering. In: Laurencin C, Nair L, editors. Nanotechnology and tissue engineering: the scaffold. Broken Sound Parkway, NW: CRC Press; 2008. p. 53-86.
19. RA Ketcham TM Ryan 2004 Quantification and visualization of anisotropy in trabecular bon J Microsc 213 158 171 10.1111/j.1365-2818.2004.01277.x 1:STN:280:DC%2BD2c%2Fjt1SgsA%3D%3D (Pubitemid 38221866)
20. J Kittler J Illingworth 1986 Minimum error thresholding Pattern Recogn 19 41 47 10.1016/0031-3203(86)90030-0 (Pubitemid 16504603)
21. ASP Lin TH Barrows S Cartmell R Guldberg 2003 Microarchitectural and mechanical characterization of oriented porous polymer scaffolds Biomaterials 24 481 489 10.1016/S0142-9612(02)00361-7 1:CAS:528:DC%2BD38XotlKgsbY%3D (Pubitemid 35287519)
22. WB Lindquist 2002 Quantitative analysis of three dimensional X-ray tomographic images Proc SPIE 4503 103 115 10.1117/12.452833
23. WB Lindquist SM Lee 1996 Medial axis analysis of void structure in three-dimensional tomographic images of porous media J Geophys Res 101 8297 8310 10.1029/95JB03039 (Pubitemid 26476143)
24. B Lindquist A Venkatarangan 1999 Investigating 3D geometry of porous media from high resolution images Phys Chem Earth A 25 593 599 10.1016/S1464-1895(99)00085-X (Pubitemid 30024545)
25. PB Malafaya TC Santos M van Griensven RL Reis 2008 Morphology, mechanical characterization and in vivo neo-vascularization of chitosan particle aggregated scaffolds architectures Biomaterials 29 3914 3926 10.1016/j.biomaterials.2008.06.023 1:CAS:528:DC%2BD1cXps1Srtr0%3D
26. I Martin M Mastrogiacomo G De Leo A Muraglia F Beltrame R Cancedda R Quarto 2002 Fluorescence microscopy imaging of bone for automated histomorphometry Tissue Eng 8 847 852 10.1089/10763270260424204 (Pubitemid 35239762)
27. M Mastrogiacomo V Komlev M Hausard F Peyrin F Turquier S Casari A Cedola F Rustichelli R Cancedda 2004 Synchrotron radiation microtomography of bone engineered from bone marrow stromal cells Tissue Eng 10 1767 1774 10.1089/ten.2004.10.1767 1:STN:280:DC%2BD2M%2Fls12hsQ%3D%3D (Pubitemid 40054218)
28. M Mastrogiacomo S Scaglione R Martinetti L Dolcini F Beltrame R Cancedda 2006 Role of scaffold internal structure on in vivo bone formation in macro-porous calcium phospate bioceramics Biomaterials 27 3230 3237 10.1016/j.biomaterials.2006.01.031 1:CAS:528:DC%2BD28Xit1aisbc%3D (Pubitemid 43348525)
29. MJ Moore E Jabbari EL Ritman L Lu BL Currier AJ Windebank MJ Yaszemski 2004 Quantitative analysis of interconnectivity of porous biodegradable scaffolds with micro-computed tomography J Biomed Mater Res A 71 258 267 10.1002/jbm.a.30138 (Pubitemid 39362906)
30. R Murugan S Ramakrishna 2004 Bioresorbable composite bone paste using polysaccharide based nano hydroxyapatite Biomaterials 25 3829 3835 10.1016/j.biomaterials.2003.10.016 1:CAS:528:DC%2BD2cXitVKisbY%3D (Pubitemid 38327071)
31. A Odgaard HJ Gundersen 1993 Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions Bone 14 173 182 10.1016/8756-3282(93)90245-6 1:STN:280:DyaK3szis1Cltw%3D%3D (Pubitemid 23098966)
32. W Oh B Lindquist 1999 Image thresholding by indicator kriging IEEE Trans Pattern Anal Mach Intell 21 590 602 10.1109/34.777370
33. Ohser J, Schladitz K. 3D images of materials structures: processing and analysis. Weinheim: Wiley-VCH; 2009.
34. N Otsu 1979 A threshold selection method from gray-level histograms IEEE Trans Syst Man Cybern 9 62 66 10.1109/TSMC.1979.4310076 (Pubitemid 9413341)
35. B Otsuki M Takemoto S Fujibayashi M Neo T Kokubo T Nakamura 2006 Pore throat size and connectivity determine bone and tissue ingrowth into porous implants: three-dimensional micro-CT based structural analyses of porous bioactive titanium implants Biomaterials 27 5892 5900 10.1016/j.biomaterials. 2006.08.013 1:CAS:528:DC%2BD28Xpt1yjsbc%3D (Pubitemid 44332516)
36. F Peyrin M Mastrogiacomo R Cancedda R Martinetti 2007 SEM and 3D synchrotron radiation micro-tomography in the study of bioceramic scaffolds for tissue-engineering applications Biotechnol Bioeng 97 638 648 10.1002/bit.21249 1:CAS:528:DC%2BD2sXlslSgtrk%3D (Pubitemid 46848077)
37. T Pun 1981 Entropic thresholding: a new approach Comp Graph Image Process 16 210 239 10.1016/0146-664X(81)90038-1
38. S Rajagopalan L Lu MJ Yaszemski RA Robb 2005 Optimal segmentation of microcomputed tomographic images of porous tissue-engineering scaffolds J Biomed Mater Res A 75 877 887 (Pubitemid 41772705)
39. TW Ridler S Calvard 1978 Picture thresholding using an iterative selection method IEEE Trans Syst Man Cybern 8 630 632 10.1109/TSMC.1978.4310039 (Pubitemid 8623043)
40. Rosenfeld A, Kak AC. Digital picture processing. New York: Academic Press, Inc; 1982.
41. M Sezgin B Sankur 2004 Survey over image thresholding techniques and quantitative performance evaluation J Electron Imag 13 146 165 10.1117/1.1631315
42. WH Tsai 1985 Moment-preserving thresholding: a new approach Graph Models Image Process 19 377 393
43. G Turco E Marsich F Bellomo S Semeraro I Donati F Brun M Grandolfo A Accardo S Paoletti 2009 Alginate/hydroxyapatite biocomposite for bone ingrowth: a trabecular structure with high and isotropic connectivity Biomacromolecules 10 1575 1583 10.1021/bm900154b 1:CAS:528:DC%2BD1MXktVOksL4%3D
44. WJ Whitehouse 1974 The quantitative morphology of anisotropic trabecular bone J Microsc 101 153 168 10.1111/j.1365-2818.1974.tb03878.x 1:STN:280:DyaE2M%2FktlWisQ%3D%3D
45. WA Yasnoff JK Mui JW Bacus 1977 Error measures for scene segmentation Pattern Recogn 9 217 231 10.1016/0031-3203(77)90006-1 (Pubitemid 8592958)
46. YJ Zhang 1996 A survey on evaluation methods for image segmentation Pattern Recogn 29 1335 1346 10.1016/0031-3203(95)00169-7 (Pubitemid 126405520)