Muscle percentage index as a marker of disease severity in golden retriever muscular dystrophy.


Journal

Muscle & nerve
ISSN: 1097-4598
Titre abrégé: Muscle Nerve
Pays: United States
ID NLM: 7803146

Informations de publication

Date de publication:
11 2019
Historique:
received: 30 08 2018
revised: 05 08 2019
accepted: 06 08 2019
pubmed: 10 8 2019
medline: 14 1 2020
entrez: 10 8 2019
Statut: ppublish

Résumé

Golden retriever muscular dystrophy (GRMD) is a spontaneous X-linked canine model of Duchenne muscular dystrophy that resembles the human condition. Muscle percentage index (MPI) is proposed as an imaging biomarker of disease severity in GRMD. To assess MPI, we used MRI data acquired from nine GRMD samples using a 4.7 T small-bore scanner. A machine learning approach was used with eight raw quantitative mapping of MRI data images (T1m, T2m, two Dixon maps, and four diffusion tensor imaging maps), three types of texture descriptors (local binary pattern, gray-level co-occurrence matrix, gray-level run-length matrix), and a gradient descriptor (histogram of oriented gradients). The confusion matrix, averaged over all samples, showed 93.5% of muscle pixels classified correctly. The classification, optimized in a leave-one-out cross-validation, provided an average accuracy of 80% with a discrepancy in overestimation for young (8%) and old (20%) dogs. MPI could be useful for quantifying GRMD severity, but careful interpretation is needed for severe cases.

Identifiants

pubmed: 31397906
doi: 10.1002/mus.26657
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

621-628

Informations de copyright

© 2019 Wiley Periodicals, Inc.

Références

Mendell JR, Shilling C, Leslie ND, et al. Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol. 2012;71:304-313.
Guiraud S, Aartsma-Rus A, Vieira NM, Davies KE, van Ommen G-JB, Kunkel LM. The pathogenesis and therapy of muscular dystrophies. Annu Rev Genom Hum Genet. 2015;16:281-308.
Brinkmeyer-Langford C, Kornegay JN. Comparative genomics of X-linked muscular dystrophies: the golden retriever model. Curr Genomics. 2013;14(5):330-342.
Lerario A, Bonfiglio S, Sormani M, et al. Quantitative muscle strength assessment in Duchenne muscular dystrophy: longitudinal study and correlation with functional measures. BMC Neurol. 2012;12(91):1-8.
Thibaud JL, Azzabou N, Barthelemy I, et al. Comprehensive longitudinal characterization of canine muscular dystrophy by serial NMR imaging of GRMD dogs. Neuromuscul Disord. 2012;22:S85-S99.
Kostrominova TY, Reiner DS, Haas RH, Ingermanson R, McDonough PM. Automated Methods for the analysis of skeletal muscle fiber size and metabolic type. In: Jeon KW, ed. International Review of Cell and Molecular Biology. Vol 306. Academic Press; 2013:275-332.
Hollingsworth KG, Garrood P, Eagle M, Bushby K, Straub V. Magnetic resonance imaging in Duchenne muscular dystrophy: longitudinal assessment of natural history over 18 months. Muscle Nerve. 2013;48(4):586-588.
Martins-Bach AB, Malheiros J, Matot B, et al. Quantitative T2 combined with texture analysis of nuclear magnetic resonance images identify different degrees of muscle involvement in three mouse models of muscle dystrophy: mdx, Largemyd and mdx/Largemyd. PLoS One. 2015;10(2):e0117835.
Mathur S, Vohra RS, Germain SA, et al. Changes in muscle T2 and tissue damage after downhill running in mdx Mice. Muscle Nerve. 2011;43(6):878-886.
Aherne W. A method of determining the cross sectional area of muscle fibres. J Neurol Sci. 1968;7(3):519-528.
Maxwell LC, McNamara JA, Carlson DS, Faulkner JA. Histochemistry of fibres of masseter and temporalis muscles of edentulous monkeys Macaca mulatta. Arch Oral Biol. 1980;25(2):87-93.
Shorey CD, Cleland KW. Problems associated with the morphometric measurement of transverse skeletal muscle fibers: I. Analysis of frozen sections. Anat Rec. 1983;207(3):523-531.
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671-675.
Liu F, Mackey AL, Srikuea R, Esser KA, Yang L. Automated image segmentation of haematoxylin and eosin stained skeletal muscle cross-sections. J Microsc. 2013;252(3):275-285.
Kornegay JN, Bogan JR, Bogan DJ, et al. Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome. 2012;23:85-108.
Vohra RS, Mathur S, Bryant ND, Forbes SC, Vandenborne K, Walter GA. Age-related T2 changes in hindlimb muscles of mdx mice. Muscle Nerve. 2016;53(1):84-90.
Qin EC, Jugé L, Lambert SA, Paradis V, Sinkus R, Bilston LE. In vivo anisotropic mechanical properties of dystrophic skeletal muscles measured by anisotropic MR elastographic imaging: the mdx mouse model of muscular dystrophy. Radiology. 2014;273(3):726-735.
Park J, Wicki J, Knoblaugh SE, Chamberlain JS, Lee D. Multi-parametric MRI at 14T for muscular dystrophy mice treated with AAV vector-mediated gene therapy. PLoS One. 2015;10(4):e0124914.
Yokota T, Q-l L, Partridge T, et al. Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol. 2009;65(6):667-676.
Fan Z, Wang J, Ahn M, et al. Characteristics of magnetic resonance imaging biomarkers in a natural history study of golden retriever muscular dystrophy. Neuromuscul Disord. 2014;24(2):178-191.
Wokke BH, Van Den Bergen JC, Hooijmans MT, Verschuuren JJ, Niks EH, Kan HE. T2 relaxation times are increased in Skeletal muscle of DMD but not BMD patients. Muscle Nerve. 2016;53(1):38-43.
Hooijmans MT, Doorenweerd N, Baligand C, et al. Spatially localized phosphorous metabolism of skeletal muscle in Duchenne muscular dystrophy patients: 24-month follow-up. PLoS One. 2017;12(8):e0182086.
Willcocks RJ, Arpan IA, Forbes SC, et al. Longitudinal measurements of MRI-T2 in boys with Duchenne muscular dystrophy: effects of age and disease progression. Neuromuscul Disord. 2014;24(5):393-401.
Arpan I, Willcocks RJ, Forbes SC, et al. Examination of effects of corticosteroids on skeletal muscles of boys with DMD using MRI and MRS. Neurology. 2014;83(11):974-980.
Ponrartana S, Ramos-Platt L, Wren TA, et al. Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol. 2015;45:582-589.
Mankodi A, Bishop CA, Auh S, Newbould RD, Fischbeck KH, Janiczek RL. Quantifying disease activity in fatty-infiltrated skeletal muscle by IDEAL-CPMG in Duchenne muscular dystrophy. Neuromuscul Disord. 2016;26(10):650-658.
Hooijmans MT, Damon BM, Froeling M, et al. Evaluation of skeletal muscle DTI in patients with Duchenne muscular dystrophy. NMR Biomed. 2015;28(11):1589-1597.
Vohra R, Accorsi A, Kumar A, Walter G, Girgenrath M. Magnetic resonance imaging is sensitive to pathological amelioration in a model for laminin-deficient congenital muscular dystrophy (MDC1A). PLoS One. 2015;10(9):e0138254.
Bonati U, Hafner P, Schädelin S, et al. Quantitative muscle MRI: a powerful surrogate outcome measure in Duchenne muscular dystrophy. Neuromuscul Disord. 2015;25(9):679-685.
Gaeta M, Messina S, Mileto A, et al. Muscle fat-fraction and mapping in Duchenne muscular dystrophy: evaluation of disease distribution and correlation with clinical assessments. Skeletal Radiol. 2012;41(8):955-961.
Bish LT, Sleeper MM, Forbes SC, et al. Long-term systemic myostatin inhibition via liver-targeted gene transfer in golden retriever muscular dystrophy. Hum Gene Ther. 2011;22(12):1499-1509.
Heier CR, Guerron AD, Korotcov A, et al. Non-invasive MRI and spectroscopy of mdx mice reveal temporal changes in dystrophic muscle imaging and in energy deficits. PLoS One. 2014;9(11):e112477.
Wang J, Fan Z, Vandenborne K, et al. A computerized MRI biomarker quantification scheme for a canine model of Duchenne muscular dystrophy. Int J Comput Assist Radiol Surg. 2013;8(5):763-774.
Wokke BH, van den Bergen JC, Versluis MJ, et al. Quantitative MRI and strength measurements in the assessment of muscle quality in Duchenne muscular dystrophy. Neuromuscul Disord. 2014;24(5):409-416.
Mathur S, Lott DJ, Senesac C, et al. Age-related differences in lower-limb muscle cross-sectional area and torque production in boys with Duchenne muscular dystrophy. Arch Phys Med Rehabil. 2010;91(7):1051-1058.
Richards P, Saywell WR, Heywood P. Pseudohypertrophy of the temporalis muscle in Xp21 muscular dystrophy. Dev Med Child Neurol. 2000;42(11):786-787.
Akima H, Lott D, Senesac C, et al. Relationships of thigh muscle contractile and non-contractile tissue with function, strength, and age in boys with Duchenne muscular dystrophy. Neuromuscul Disord. 2012;22(1):16-25.
Godi C, Ambrosi A, Nicastro F, et al. Longitudinal MRI quantification of muscle degeneration in Duchenne muscular dystrophy. Ann Clin Transl Neurol. 2016;3(8):607-622.
Roberts TC, Blomberg KEM, McClorey G, et al. Expression analysis in multiple muscle groups and serum reveals complexity in the microRNA transcriptome of the mdx mouse with implications for therapy. Mol Ther Nucleic Acids. 2012;1(8):e39.
Willcocks RJ, Rooney WD, Triplett WT, et al. Multicenter prospective longitudinal study of magnetic resonance biomarkers in a large Duchenne muscular dystrophy cohort. Ann Neurol. 2016;79(4):535-547.
Kornegay JN. The golden retriever model of Duchenne muscular dystrophy. Skelet Muscle. 2017;7(9):1-21.
Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press; 2011.
National Institutes of Health. Office of Laboratory Animal Welfare - Public Health Service Policy on Humane Care and Use of Laboratory Animals. Volume 20172015.
Kiernan JA. Histological and Histochemical Methods. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2008.
Wikeley DM. Manual of Histological and Histochemical Methods used for Larval Evaluation. Hobart, Tasmania: Marine Resources Division, Marine Research Laboratories-Taroona, Department of Primary Industry and Fisheries; 1994.
Eresen A, McConnell S, Birch SM, Griffin JF, Kornegay JN, Ji JX. Localized MRI and histological image correlation in a canine model of Duchenne muscular dystrophy. Conf Proc IEEE Eng Med Biol Soc. 2016;2016:4083-4086.
Eresen A, McConnell S, Birch SM, Griffin JF, Kornegay JN, Ji JX. Tissue classification in a canine model of Duchenne Muscular Dystrophy using quantitative MRI parameters. Conf Proc IEEE Eng Med Biol Soc. 2017;2017:4066-4069.
Hales PW, Burton RAB, Bollesdorff C, et al. Progressive changes in T1, T2 and left-ventricular histo-architecture in the fixed and embedded rat heart. NMR Biomed. 2010;24:836-843.
Hellerbach A, Schuster V, Jansen A, Sommer J. MRI phantoms - are there alternatives to agar? PLoS One. 2013;8(8):e70343.
Thelwall PE, Shepherd TM, Stanisz GJ, Blackband SJ. Effects of temperature and aldehyde fixation on tissue water diffusion properties, studied in an erythrocyte ghost tissue model. Magn Reson Med. 2006;56:282-289.
Pomfret R, Sillay K, Miranpuri G. Investigation of the electrical properties of agarose gel: characterization of concentration using nyquist plot phase angle and the implications of a more comprehensive in vitro model of the brain. Ann Neurosci. 2013;20(3):99-107.
McConnell S. Automatic Canine Muscle Histology Image Segmentation Based on RGB Histogram [Master's Thesis]. College Station, TX: Texas A&M University; 2016.
Deoni SC, Rutt BK, Peters TM. Rapid combined T1 and T2 mapping using gradient recalled acquisition in the steady state. Magn Reson Med. 2003;49(3):515-526.
Glover GH, Schneider E. Three-point Dixon technique for true water/fat decomposition with B0 inhomogeneity correction. Magn Reson Med. 1991;18(2):371-383.
Reeder S, Hines C, Yu H, McKenzie C, Brittain J. On the definition of fat-fraction for in vivo fat quantifi cation with magnetic resonance imaging. In: Proceedings of the 17th Annual Meeting of ISMRM. Hawaii, 2009. Abstract 211.
Cook PA, Bai Y, Nedjati-Gilani S, et al. Camino: open-source diffusion-MRI reconstruction and processing. In: Proceedings of the 14th Annual Meeting of ISMRM, Seattle, Washington, 2006. Abstract 2759.
Eresen A, McConnell S, Birch S, Friedeck W, Griffin J, Kornegay J, Ji JX. Correlating MRI and histological parameters in GRMD muscles: a comparison between 3T and 4.7T acquisitions. In: Proceedings of the 25th Annual Meeting of ISMRM, Honolulu, Hawaii, 2017. Abstract 1572.
Ojala T, Pietikäinen M, Harwood D. A comparative study of texture measures with classification based on featured distributions. Pattern Recognit. 1996;29(1):51-59.
Ojala T, Pietikainen M, Maenpaa T. Multiresolution gray-scale and rotation invariant texture classification with local binary patterns. IEEE Trans Pattern Anal Mach Intell. 2002;24(7):971-987.
Haralick RM, Shanmugam K, Dinstein IH. Textural features for image classification. IEEE Trans Syst Man Cybern. 1973;SMC-3(6):610-621.
Galloway MM. Texture analysis using gray level run lengths. Comput Graph Image Process. 1975;4(2):172-179.
McConnell RK. Method of and apparatus for pattern recognition. Google Patent US4567610A; 1986.
Freeman WT, Roth M; Mitsubishi Electric Research Laboratories, assignee. Orientation Histograms for Hand Gesture Recognition. USA1994.
Dalal N, Triggs B. Histograms of oriented gradients for human detection. In: Proceedings of the 2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR'05) - Vol 1: IEEE Computer Society; 2005:886-893.
Eresen A, Birch SM, Alic L, Friffin Iv JF, Kornegay JN, Ji JX. New similarity metric for registration of MRI to histology: golden retriever muscular dystrophy imaging. IEEE Trans Biomed Eng. 2019;66(5):1222-1230.
Breiman L. Random Forests. Mach Learn. 2001;45(1):5-32.
R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2017.
Alic L, Haeck JC, Bol K, et al. Facilitating tumor functional assessment by spatially relating 3D tumor histology and in vivo MRI: image registration approach. PLoS One. 2011;6(8):e22835.

Auteurs

Aydin Eresen (A)

Department of Electrical and Computer Engineering, Texas A&M University, College Station, Texas.

Noor E Hafsa (NE)

Department of Electrical and Computer Engineering, Texas A&M University, Doha, Qatar.

Lejla Alic (L)

Department of Electrical and Computer Engineering, Texas A&M University, Doha, Qatar.
Magnetic Detection & Imaging Group, Faculty of Science & Technology, University of Twente, Enschede, The Netherlands.

Sharla M Birch (SM)

College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas.

John F Griffin (JF)

College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas.

Joe N Kornegay (JN)

College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas.

Jim X Ji (JX)

Department of Electrical and Computer Engineering, Texas A&M University, College Station, Texas.
Department of Electrical and Computer Engineering, Texas A&M University, Doha, Qatar.

Articles similaires

Humans Ketamine Propofol Pulmonary Atelectasis Female
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH