Skip to main content
Top
Published in: International Journal of Computer Assisted Radiology and Surgery 5/2013

01-09-2013 | Original Article

A computerized MRI biomarker quantification scheme for a canine model of Duchenne muscular dystrophy

Authors: Jiahui Wang, Zheng Fan, Krista Vandenborne, Glenn Walter, Yael Shiloh-Malawsky, Hongyu An, Joe N. Kornegay, Martin A. Styner

Published in: International Journal of Computer Assisted Radiology and Surgery | Issue 5/2013

Login to get access

Abstract

Purpose   Golden retriever muscular dystrophy (GRMD) is a widely used canine model of Duchenne muscular dystrophy (DMD). Recent studies have shown that magnetic resonance imaging (MRI) can be used to non-invasively detect consistent changes in both DMD and GRMD. In this paper, we propose a semiautomated system to quantify MRI biomarkers of GRMD.
Methods   Our system was applied to a database of 45 MRI scans from 8 normal and 10 GRMD dogs in a longitudinal natural history study. We first segmented six proximal pelvic limb muscles using a semiautomated full muscle segmentation method. We then performed preprocessing, including intensity inhomogeneity correction, spatial registration of different image sequences, intensity calibration of T2-weighted and T2-weighted fat-suppressed images, and calculation of MRI biomarker maps. Finally, for each of the segmented muscles, we automatically measured MRI biomarkers of muscle volume, intensity statistics over MRI biomarker maps, and statistical image texture features.
Results The muscle volume and the mean intensities in T2 value, fat, and water maps showed group differences between normal and GRMD dogs. For the statistical texture biomarkers, both the histogram and run-length matrix features showed obvious group differences between normal and GRMD dogs. The full muscle segmentation showed significantly less error and variability in the proposed biomarkers when compared to the standard, limited muscle range segmentation.
Conclusion   The experimental results demonstrated that this quantification tool could reliably quantify MRI biomarkers in GRMD dogs, suggesting that it would also be useful for quantifying disease progression and measuring therapeutic effect in DMD patients.
Literature
1.
go back to reference Moser H (1984) Duchenne muscular dystrophy: pathogenetic aspects and genetic prevention. Hum Genet 66:17–40PubMedCrossRef Moser H (1984) Duchenne muscular dystrophy: pathogenetic aspects and genetic prevention. Hum Genet 66:17–40PubMedCrossRef
2.
go back to reference Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928PubMedCrossRef Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928PubMedCrossRef
3.
go back to reference Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50:509–517 Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50:509–517
4.
go back to reference Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81:1189–1192PubMedCrossRef Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81:1189–1192PubMedCrossRef
5.
go back to reference Gaschen FP, Hoffman EP, Gorospe JR, Uhl EW, Senior DF, Cardinet GH 3rd, Pearce LK (1992) Dystrophin deficiency causes lethal muscle hypertrophy in cats. J Neurol Sci 110:149–159 Gaschen FP, Hoffman EP, Gorospe JR, Uhl EW, Senior DF, Cardinet GH 3rd, Pearce LK (1992) Dystrophin deficiency causes lethal muscle hypertrophy in cats. J Neurol Sci 110:149–159
6.
go back to reference Kornegay JN, Tuler SM, Miller DM, Levesque DC (1988) Muscular dystrophy in a litter of golden retriever dogs. Muscle Nerve 11:1056–1064 Kornegay JN, Tuler SM, Miller DM, Levesque DC (1988) Muscular dystrophy in a litter of golden retriever dogs. Muscle Nerve 11:1056–1064
7.
go back to reference Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, Kunkel LM, Scott MO, Fischbeck KH, Kornegay JN, Avery RJ, Williams JR, Schmickel RD, Sylvester JE (1988) The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 334:154–156 Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, Kunkel LM, Scott MO, Fischbeck KH, Kornegay JN, Avery RJ, Williams JR, Schmickel RD, Sylvester JE (1988) The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 334:154–156
8.
go back to reference Kornegay JN, Bogan JR, Bogan DJ, Childers MK, Li J, Nghiem P, Detwiler DA, Larsen CA, Grange RW, Bhavaraju-Sanka RK, Tou S, Keene BP, Howard JF Jr, Wang J, Fan Z, Schatzberg SJ, Styner MA, Flanigan KM, Xiao X, Hoffman EP (2012) Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome 23:85–108PubMedCrossRef Kornegay JN, Bogan JR, Bogan DJ, Childers MK, Li J, Nghiem P, Detwiler DA, Larsen CA, Grange RW, Bhavaraju-Sanka RK, Tou S, Keene BP, Howard JF Jr, Wang J, Fan Z, Schatzberg SJ, Styner MA, Flanigan KM, Xiao X, Hoffman EP (2012) Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome 23:85–108PubMedCrossRef
9.
go back to reference Kobayashi M, Nakamura A, Hasegawa D, Fujita M, Orima H, Takeda S (2009) Evaluation of dystrophic dog pathology by fat-suppressed T2-weighted imaging. Muscle Nerve 40:815–826PubMedCrossRef Kobayashi M, Nakamura A, Hasegawa D, Fujita M, Orima H, Takeda S (2009) Evaluation of dystrophic dog pathology by fat-suppressed T2-weighted imaging. Muscle Nerve 40:815–826PubMedCrossRef
10.
go back to reference Thibaud JL, Monnet A, Bertoldi D, Barthelemy I, Blot S, Carlier PG (2007) Characterization of dystrophic muscle in golden retriever muscular dystrophy dogs by nuclear magnetic resonance imaging. Neuromuscul Disord 17:575–584PubMedCrossRef Thibaud JL, Monnet A, Bertoldi D, Barthelemy I, Blot S, Carlier PG (2007) Characterization of dystrophic muscle in golden retriever muscular dystrophy dogs by nuclear magnetic resonance imaging. Neuromuscul Disord 17:575–584PubMedCrossRef
11.
go back to reference Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, Takeda S, Hoffman E (2009) Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 65:667–676 Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, Takeda S, Hoffman E (2009) Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 65:667–676
12.
go back to reference Lamminen AE (1990) Magnetic resonance imaging of primary skeletal muscle diseases: patterns of distribution and severity of involvement. Br J Radiol 63:946–950PubMedCrossRef Lamminen AE (1990) Magnetic resonance imaging of primary skeletal muscle diseases: patterns of distribution and severity of involvement. Br J Radiol 63:946–950PubMedCrossRef
13.
go back to reference Lovitt S, Moore SL, Marden FA (2006) The use of MRI in the evaluation of myopathy. Clin Neurophysiol 117:486–495PubMedCrossRef Lovitt S, Moore SL, Marden FA (2006) The use of MRI in the evaluation of myopathy. Clin Neurophysiol 117:486–495PubMedCrossRef
14.
go back to reference Marden FA, Connolly AM, Siegel MJ, Rubin DA (2005) Compositional analysis of muscle in boys with Duchenne muscular dystrophy using MR imaging. Skeletal Radiol 34:140–148PubMedCrossRef Marden FA, Connolly AM, Siegel MJ, Rubin DA (2005) Compositional analysis of muscle in boys with Duchenne muscular dystrophy using MR imaging. Skeletal Radiol 34:140–148PubMedCrossRef
15.
go back to reference Liu GC, Jong YJ, Chiang CH, Jaw TS (1993) Duchenne muscular dystrophy: MR grading system with functional correlation. Radiology 186:475–480 Liu GC, Jong YJ, Chiang CH, Jaw TS (1993) Duchenne muscular dystrophy: MR grading system with functional correlation. Radiology 186:475–480
16.
go back to reference Karpati G, Ajdukovic D, Arnold D, Gledhill RB, Guttmann R, Holland P, Koch PA, Shoubridge E, Spence D, Vanasse M, Watters GV, Abrahamowicz M, Duff C, Worton RG (1993) Myoblast transfer in Duchenne muscular dystrophy. Ann Neurol 34: 8–17 Karpati G, Ajdukovic D, Arnold D, Gledhill RB, Guttmann R, Holland P, Koch PA, Shoubridge E, Spence D, Vanasse M, Watters GV, Abrahamowicz M, Duff C, Worton RG (1993) Myoblast transfer in Duchenne muscular dystrophy. Ann Neurol 34: 8–17
17.
go back to reference Miller RG, Sharma KR, Pavlath GK, Gussoni E, Mynhier M, Lanctot AM, Greco CM, Steinman L, Blau HM (1997) Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve 20:469–478PubMedCrossRef Miller RG, Sharma KR, Pavlath GK, Gussoni E, Mynhier M, Lanctot AM, Greco CM, Steinman L, Blau HM (1997) Myoblast implantation in Duchenne muscular dystrophy: the San Francisco study. Muscle Nerve 20:469–478PubMedCrossRef
18.
go back to reference Mathur S, Lott DJ, Senesac C (2010) Age-related differences in lower-limb muscle cross-sectional area and torque production in boys with Duchenne muscular dystrophy. Arch Phys Med Rehabil 91:1051–1058PubMedCrossRef Mathur S, Lott DJ, Senesac C (2010) Age-related differences in lower-limb muscle cross-sectional area and torque production in boys with Duchenne muscular dystrophy. Arch Phys Med Rehabil 91:1051–1058PubMedCrossRef
19.
go back to reference Kornegay JN, Cundiff DD, Bogan DJ, Bogan JR, Okamura CS (2003) The cranial sartorius muscle undergoes true hypertrophy in dogs with golden retriever muscular dystrophy. Neuromuscul Disord 13:493–500PubMedCrossRef Kornegay JN, Cundiff DD, Bogan DJ, Bogan JR, Okamura CS (2003) The cranial sartorius muscle undergoes true hypertrophy in dogs with golden retriever muscular dystrophy. Neuromuscul Disord 13:493–500PubMedCrossRef
20.
go back to reference Childers MK, Okamura CS, Bogan DJ, Bogan JR, Sullivan MJ, Kornegay JN (2001) Myofiber injury and regeneration in a canine homologue of Duchenne muscular dystrophy. Am J Phys Med Rehabil 80:175–181 Childers MK, Okamura CS, Bogan DJ, Bogan JR, Sullivan MJ, Kornegay JN (2001) Myofiber injury and regeneration in a canine homologue of Duchenne muscular dystrophy. Am J Phys Med Rehabil 80:175–181
21.
go back to reference Wang J, Fan Z, Kornegay J, Styner M (2011) MRI-based quantification of Duchenne muscular dystrophy in a canine model. Proc SPIE Med Imaging 7965:79650G1–79650G9 Wang J, Fan Z, Kornegay J, Styner M (2011) MRI-based quantification of Duchenne muscular dystrophy in a canine model. Proc SPIE Med Imaging 7965:79650G1–79650G9
22.
go back to reference Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128PubMedCrossRef Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128PubMedCrossRef
23.
go back to reference Hou Z (2006) A review on MR image intensity inhomogeneity correction. Proc Int J Biomed Imaging 2006:49515-1–49515-11 Hou Z (2006) A review on MR image intensity inhomogeneity correction. Proc Int J Biomed Imaging 2006:49515-1–49515-11
24.
go back to reference Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29:1310–1320PubMedCrossRef Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29:1310–1320PubMedCrossRef
25.
go back to reference Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97PubMedCrossRef Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97PubMedCrossRef
26.
go back to reference Kim HK, Laor T, Horn PS, Racadio JM, Wong B, Dardzinski BJ (2010) T2 mapping in Duchenne muscular dystrophy: distribution of disease activity and correlation with clinical assessments. Radiology 255:899–908 Kim HK, Laor T, Horn PS, Racadio JM, Wong B, Dardzinski BJ (2010) T2 mapping in Duchenne muscular dystrophy: distribution of disease activity and correlation with clinical assessments. Radiology 255:899–908
27.
go back to reference Pluim JP, Maintz JB, Viergever MA (2003) Mutual-information-based registration of medical images: a survey. IEEE Trans Med Imaging 22:986–1004PubMedCrossRef Pluim JP, Maintz JB, Viergever MA (2003) Mutual-information-based registration of medical images: a survey. IEEE Trans Med Imaging 22:986–1004PubMedCrossRef
28.
go back to reference Perona P, Malik J (1990) Scale-space and edge detection using anisotropic diffusion. IEEE Trans Pattern Anal Mach Intell 12: 629–639 Perona P, Malik J (1990) Scale-space and edge detection using anisotropic diffusion. IEEE Trans Pattern Anal Mach Intell 12: 629–639
29.
go back to reference Chuah TK, Poh CL, Sheah K (2011) Quantitative texture analysis of MRI images for detection of cartilage-related bone marrow edema. Proc IEEE Eng Med Biol Soc 2011:5112–5115 Chuah TK, Poh CL, Sheah K (2011) Quantitative texture analysis of MRI images for detection of cartilage-related bone marrow edema. Proc IEEE Eng Med Biol Soc 2011:5112–5115
30.
go back to reference Mayerhoefer ME, Schima W, Trattnig S, Pinker K, Berger-Kulemann V, Ba-Ssalamah A (2010) Texture-based classification of focal liver lesions on MRI at 3.0 Tesla: a feasibility study in cysts and hemangiomas. J Magn Reson Imaging 32:352–359PubMedCrossRef Mayerhoefer ME, Schima W, Trattnig S, Pinker K, Berger-Kulemann V, Ba-Ssalamah A (2010) Texture-based classification of focal liver lesions on MRI at 3.0 Tesla: a feasibility study in cysts and hemangiomas. J Magn Reson Imaging 32:352–359PubMedCrossRef
31.
go back to reference Holli K, Laaperi AL, Harrison L, Luukkaala T, Toivonen T, Ryymin P, Dastidar P, Soimakallio S, Eskola H (2010) Characterization of breast cancer types by texture analysis of magnetic resonance images. Acad Radiol 17:135–141 Holli K, Laaperi AL, Harrison L, Luukkaala T, Toivonen T, Ryymin P, Dastidar P, Soimakallio S, Eskola H (2010) Characterization of breast cancer types by texture analysis of magnetic resonance images. Acad Radiol 17:135–141
32.
go back to reference Zhang J, Yu C, Jiang G, Liu W, Tong L (2012) 3D texture analysis on MRI images of Alzheimer’s disease. Brain Imaging Behav 6:61–69PubMedCrossRef Zhang J, Yu C, Jiang G, Liu W, Tong L (2012) 3D texture analysis on MRI images of Alzheimer’s disease. Brain Imaging Behav 6:61–69PubMedCrossRef
33.
go back to reference Herlidou S, Rolland Y, Bansard JY, Le Rumeur E, De Certaines JD (1999) Comparison of automated and visual texture analysis in MRI: characterization of normal and diseased skeletal muscle. Magn Reson Imaging 17:1393–1397 Herlidou S, Rolland Y, Bansard JY, Le Rumeur E, De Certaines JD (1999) Comparison of automated and visual texture analysis in MRI: characterization of normal and diseased skeletal muscle. Magn Reson Imaging 17:1393–1397
34.
go back to reference Mahmoud-Ghoneim D, Cherel Y, Lemaire L, De Certaines JD, Maniere A (2006) Texture analysis of magnetic resonance images of rat muscles during atrophy and regeneration. Magn Reson Imaging 24:167–171 Mahmoud-Ghoneim D, Cherel Y, Lemaire L, De Certaines JD, Maniere A (2006) Texture analysis of magnetic resonance images of rat muscles during atrophy and regeneration. Magn Reson Imaging 24:167–171
35.
go back to reference Galloway M (1975) Texture analysis using gray level run lengths. Comput Graph Imaging Proc 4:172–179 Galloway M (1975) Texture analysis using gray level run lengths. Comput Graph Imaging Proc 4:172–179
36.
go back to reference Bryk AS, Raudenbush SW (1992) Hierarchical linear models: applications and data analysis methods. Sage, Newbury Park Bryk AS, Raudenbush SW (1992) Hierarchical linear models: applications and data analysis methods. Sage, Newbury Park
37.
go back to reference Tegeler C, Grange R, Bogan D, Markert C, Case D, Kornegay J, Childers M (2010) Eccentric contractions induce rapid isometric torque drop in dystrophic-deficient dogs. Muscle Nerve 42:130–132 Tegeler C, Grange R, Bogan D, Markert C, Case D, Kornegay J, Childers M (2010) Eccentric contractions induce rapid isometric torque drop in dystrophic-deficient dogs. Muscle Nerve 42:130–132
38.
go back to reference Childers M, Bogan J, Bogan D, Greiner H, Holder M, Grange R, Kornegay J (2011) Chronic administration of a leupeptin-derived calpain inhibitor fails to ameliorate severe muscle pathology in a canine model of Duchenne muscular dystrophy. Front Pharmacol 2:89 Childers M, Bogan J, Bogan D, Greiner H, Holder M, Grange R, Kornegay J (2011) Chronic administration of a leupeptin-derived calpain inhibitor fails to ameliorate severe muscle pathology in a canine model of Duchenne muscular dystrophy. Front Pharmacol 2:89
39.
go back to reference Abramoff M, Magalhaes P, Ram S (2004) Image processing with image J. Biophoton Intern 11:36–42 Abramoff M, Magalhaes P, Ram S (2004) Image processing with image J. Biophoton Intern 11:36–42
Metadata
Title
A computerized MRI biomarker quantification scheme for a canine model of Duchenne muscular dystrophy
Authors
Jiahui Wang
Zheng Fan
Krista Vandenborne
Glenn Walter
Yael Shiloh-Malawsky
Hongyu An
Joe N. Kornegay
Martin A. Styner
Publication date
01-09-2013
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Computer Assisted Radiology and Surgery / Issue 5/2013
Print ISSN: 1861-6410
Electronic ISSN: 1861-6429
DOI
https://doi.org/10.1007/s11548-012-0810-6

Other articles of this Issue 5/2013

International Journal of Computer Assisted Radiology and Surgery 5/2013 Go to the issue