Ultrasound estimates of muscle quality in older adults: Reliability and comparison of Photoshop and ImageJ for the grayscale analysis of muscle echogenicity

PeerJ

Volumn 2016, Issue 2, 2016, Pages

  Harris Love, Michael O ^a,b   Seamon, Bryant A ^a   Teixeira, Carla ^a,c   Ismail, Catheeja ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

Geriatrics; Grayscale histogram analysis; ImageJ; Muscle echogenicity; Photoshop; Ultrasound

Indexed keywords

ADULT; ARTICLE; CLINICAL TRIAL; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CORRELATION COEFFICIENT; CROSS-SECTIONAL STUDY; ECHOGRAPHY; FEMALE; FREE HAND TOOL; HISTOGRAM; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MUSCLE; NORMAL HUMAN; OBSERVATIONAL STUDY; RECTANGULAR MARQUEE TOOL; RELIABILITY; TOOL USE; ULTRASOUND;

EID: 84963969089     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.1721     Document Type: Article

References (63)

1. Cardenas-Garcia J, Mayo PH. 2015. Bedside ultrasonography for the intensivist. Critical Care Clinics 31:43-66 DOI 10.1016/j.ccc.2014.08.003.
2. Caresio C, Molinari F, Emanuel G, Minetto MA. 2015. Muscle echo intensity: reliability and conditioning factors. Clinical Physiology and Functional Imaging 35:393-403 DOI 10.1111/cpf.12175.
3. Casella IB, Fukushima RB, Marques AB, De A, Cury MVM, Presti C. 2015. Comparison between a new computer program and the reference software for gray-scale median analysis of atherosclerotic carotid plaques. Journal of Clinical Ultrasound 43:194-198 DOI 10.1002/jcu.22178.
4. Cawthon PM, Blackwell TL, Cauley J, Kado DM, Barrett-Connor E, Lee CG, Hoffman AR, Nevitt M, Stefanick ML, Lane NE, Ensrud KE, Cummings SR, Orwoll ES. 2015. Evaluation of the usefulness of consensus definitions of sarcopenia in older men: results from the Observational Osteoporotic Fractures in Men Cohort Study. Journal of the American Geriatrics Society 63:2247-2259 DOI 10.1111/jgs.13788.
5. Cawthon PM, Fox KM, Gandra SR, Delmonico MJ, Chiou C-F, Anthony MS, Sewall A, Goodpaster B, Satterfield S, Cummings SR, Harris TB, for the Health, Aging and Body Composition Study. 2009. Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? Journal of the American Geriatrics Society 57:1411-1419 DOI 10.1111/j.1532-5415.2009.02366.x.
6. Clark DJ, Fielding RA. 2012. Neuromuscular contributions to age-related weakness. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 67A:41-47 DOI 10.1093/gerona/glr041.
7. Collins T. 2007. ImageJ for microscopy. BioTechniques 43:25-30 DOI 10.2144/000112505.
8. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel J-P, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older People. 2010. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in older people. Age and Ageing 39:412-423 DOI 10.1093/ageing/afq034.
9. Eliasziw M, Young SL, Woodbury MG, Fryday-Field K. 1994. Statistical methodology for the concurrent assessment of interrater and intrarater reliability: using goniometric measurements as an example. Physical Therapy 74:777-788.
10. Fortin M, Battié MC. 2012. Quantitative paraspinal muscle measurements: intersoftware reliability and agreement using OsiriX and ImageJ. Physical Therapy 92:853-864 DOI 10.2522/ptj.20110380.
11. Franchi MV, Atherton PJ, Reeves ND, Flück M, Williams J, Mitchell WK, Selby A, Beltran Valls RM, Narici MV. 2014. Architectural, functional and molecular responses to concentric and eccentric loading in human skeletal muscle. Acta Physiologica 210:642-654 DOI 10.1111/apha.12225.
12. Fukumoto Y, Ikezoe T, Yamada Y, Tsukagoshi R, Nakamura M, Mori N, Kimura M, Ichihashi N. 2012. Skeletal muscle quality assessed from echo intensity is associated with muscle strength of middle-aged and elderly persons. European Journal of Applied Physiology 112:1519-1525 DOI 10.1007/s00421-011-2099-5.
13. Fung AD, Collins JA, Campassi C, Ioffe OB, Staats PN. 2014. Performance characteristics of ultrasound-guided fine-needle aspiration of axillary lymph nodes for metastatic breast cancer employing rapid on-site evaluation of adequacy: analysis of 136 cases and review of the literature. Cancer Cytopathology 122:282-291 DOI 10.1002/cncy.21384.
14. Giavarina D. 2015. Understanding Bland Altman analysis. Biochemia Medica 25:141-151 DOI 10.11613/BM.2015.015.
15. Giggins OM, Persson U, Caulfield B. 2013. Biofeedback in rehabilitation. Journal of NeuroEngineering and Rehabilitation 10:60 DOI 10.1186/1743-0003-10-60.
16. Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R. 2000. Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. Journal of Applied Physiology 89:104-110.
17. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, Waite LM, Seibel MJ, Sambrook PN. 2010. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. Journal of the American Geriatrics Society 58:2055-2062 DOI 10.1111/j.1532-5415.2010.03145.x.
18. Hamaguchi Y, Kaido T, Okumura S, Fujimoto Y, Ogawa K, Mori A, Hammad A, Tamai Y, Inagaki N, Uemoto S. 2014. Impact of quality as well as quantity of skeletal muscle on outcomes after liver transplantation. Liver Transplantation 20:1413-1419 DOI 10.1002/lt.23970.
19. Harris-Love MO, Adams B, Hernandez HJ, DiPietro L, Blackman MR. 2014b. Disparities in the consequences of sarcopenia: implications for African American Veterans. Frontiers in Physiology 5:250.
20. Harris-Love MO, Monfaredi R, Ismail C, Blackman MR, Cleary K. 2014a. Quantitative ultrasound: measurement considerations for the assessment of muscular dystrophy and sarcopenia. Frontiers in Aging Neuroscience 6:172.
21. Harris-Love MO, Seamon BA, Teixeira C, Ismail C. 2015. Ultrasound estimates of myosteatosis: reliability and comparison of Adobe Photoshop R and ImageJ for grayscale analysis of muscle echogenicity. Journal of Frailty and Aging 4(Supplement 1):103 DOI 10.13140/RG.2.1.3275.3764.
22. Heckmatt J, Rodillo E, Doherty M, Willson K, Leeman S. 1989. Quantitative sonography of muscle. Journal of Child Neurology 4(Suppl):S101-S106.
23. Hernandez HJ, McIntosh V, Leland A, Harris-Love MO. 2015. Progressive resistance exercise with eccentric loading for the management of knee osteoarthritis. Frontiers in Medicine 2:45.
24. Iftekharuddin KM, Awwal AAS. 2012. Field guide to image processing. Bellingham: SPIE Press.
25. Ismail C, Zabal J, Hernandez HJ, Woletz P, Manning H, Teixeira C, DiPietro L, Blackman MR, Harris-Love M. 2015. Diagnostic ultrasound estimates of muscle mass and muscle quality discriminate between women with and without sarcopenia. Frontiers in Physiology 6:302.
26. Jansen M, Van Alfen N, Nijhuis van der Sanden MWG, Van Dijk JP, Pillen S, De Groot IJM. 2012. Quantitative muscle ultrasound is a promising longitudinal followup tool in Duchenne muscular dystrophy. Neuromuscular Disorders 22:306-317 DOI 10.1016/j.nmd.2011.10.020.
27. Klaastad Ø, Sauter AR, Dodgson MS. 2009. Brachial plexus block with or without ultrasound guidance. Current Opinion in Anaesthesiology 22:655-660 DOI 10.1097/ACO.0b013e32832eb7d3.
28. Krivickas LS, Dorer DJ, Ochala J, Frontera WR. 2011. Relationship between force and size in human single muscle fibres: muscle fibre size and force. Experimental Physiology 96:539-547 DOI 10.1113/expphysiol.2010.055269.
29. Kwah LK, Pinto RZ, Diong J, Herbert RD. 2013. Reliability and validity of ultrasound measurements of muscle fascicle length and pennation in humans: a systematic review. Journal of Applied Physiology 114:761-769 DOI 10.1152/japplphysiol.01430.2011.
30. Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB. 2010. Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. Journal of Bone and Mineral Research 25:513-519 DOI 10.1359/jbmr.090807.
31. Licata A. 2009. Bone density vs bone quality: what's a clinician to do? Cleveland Clinic Journal of Medicine 76:331-336 DOI 10.3949/ccjm.76a.08041.
32. Lieber RL. 2010. Skeletal muscle structure, function, and plasticity: the physiological basis of rehabilitation. Baltimore: Lippincott Williams & Wilkins.
33. Lowry R. 2004. VassarStats: Statistical Computation Web Site. Available at http://vassarstats.net/(accessed 27 November 2015).
34. Maly MR, Calder KM, Macintyre NJ, Beattie KA. 2013. Relationship of intermuscular fat volume in the thigh with knee extensor strength and physical performance in women at risk of or with knee osteoarthritis. Arthritis Care & Research 65:44-52 DOI 10.1002/acr.21868.
35. Marcus RL, Addison O, LaStayo PC. 2013. Intramuscular adipose tissue attenuates gains in muscle quality in older adults at high risk for falling. A brief report. The Journal of Nutrition, Health & Aging 17:215-218 DOI 10.1007/s12603-012-0377-5.
36. Munro BH. 2001. Statistical methods for health care research. Philadelphia: Lippincott,.
37. Nanes BA. 2015. Slide set: reproducible image analysis and batch processing with ImageJ. BioTechniques 59:269-278.
38. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB. 2006. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 61:72-77 DOI 10.1093/gerona/61.1.72.
39. Nodera H, Takamatsu N, Matsui N, Mori A, Terasawa Y, Shimatani Y, Osaki Y, Maruyama K, Izumi Y, Kaji R. 2015. Intramuscular dissociation of echogenicity in the triceps surae characterizes sporadic inclusion body myositis. European Journal of Neurology 23 Epub ahead of print DOI 10.1111/ene.12899.
40. Pillen S, Scholten RR, Zwarts MJ, Verrips A. 2003. Quantitative skeletal muscle ultrasonography in children with suspected neuromuscular disease. Muscle & Nerve 27:699-705 DOI 10.1002/mus.10385.
41. Pillen S, Van Alfen N. 2011. Skeletal muscle ultrasound. Neurological Research 33:1016-1024 DOI 10.1179/1743132811Y.0000000010.
42. Pillen S, Van Dijk JP, Weijers G, Raijmann W, De Korte CL, Zwarts MJ. 2009. Quantitative gray-scale analysis in skeletal muscle ultrasound: a comparison study of two ultrasound devices. Muscle & Nerve 39:781-786 DOI 10.1002/mus.21285.
43. Pillen S, Verrips A, Van Alfen N, Arts IMP, Sie LTL, Zwarts MJ. 2007. Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease. Neuromuscular Disorders 17:509-516 DOI 10.1016/j.nmd.2007.03.008.
44. Portney LG, Watkins MP. 2009. Foundations of clinical research: applications to practice. Upper Saddle River: Pearson/Prentice Hall,.
45. Rahemi H, Nigam N, Wakeling JM. 2015. The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese. Journal of The Royal Society Interface 12:20150365 DOI 10.1098/rsif.2015.0365.
46. Rasband WS. 1997. ImageJ. Bethesda: US National Institutes of Health.
47. Reeves ND, Maganaris CN, Longo S, Narici MV. 2009. Differential adaptations to eccentric versus conventional resistance training in older humans. Experimental Physiology 94:825-833 DOI 10.1113/expphysiol.2009.046599.
48. Reimers K, Reimers CD, Wagner S, Paetzke I, Pongratz DE. 1993. Skeletal muscle sonography: a correlative study of echogenicity and morphology. Journal of Ultrasound in Medicine 12:73-77.
49. Saad HA, Terry MA, Shamie N, Chen ES, Friend DF, Holiman JD, Stoeger C. 2008. An easy and inexpensive method for quantitative analysis of endothelial damage by using vital dye staining and Adobe Photoshop software. Cornea 27:818-824 DOI 10.1097/ICO.0b013e3181705ca2.
50. Sarwal A, Parry SM, Berry MJ, Hsu F-C, Lewis MT, Justus NW, Morris PE, Denehy L, Berney S, Dhar S, Cartwright MS. 2015. Interobserver reliability of quantitative muscle sonographic analysis in the critically ill population. Journal of Ultrasound in Medicine 34:1191-1200 DOI 10.7863/ultra.34.7.1191.
51. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9:671-675 DOI 10.1038/nmeth.2089.
52. Scott D, Blizzard L, Fell J, Ding C, Winzenberg T, Jones G. 2010. A prospective study of the associations between 25-hydroxy-vitamin D, sarcopenia progression and physical activity in older adults: vitamin D, sarcopenia and physical activity. Clinical Endocrinology 73:581-587 DOI 10.1111/j.1365-2265.2010.03858.x.
53. Shklyar I, Geisbush TR, Mijialovic AS, Pasternak A, Darras BT, Wu JS, Rutkove SB, Zaidman CM. 2015. Quantitative muscle ultrasound in Duchenne muscular dystrophy: a comparison of techniques. Muscle & Nerve 51:207-213 DOI 10.1002/mus.24296.
54. Singer FR, Eyre DR. 2008. Using biochemical markers of bone turnover in clinical practice. Cleveland Clinic Journal of Medicine 75:739-750 DOI 10.3949/ccjm.75.10.739.
55. Sipilä S, Suominen H. 1993. Muscle ultrasonography and computed tomography in elderly trained and untrained women. Muscle & Nerve 16:294-300 DOI 10.1002/mus.880160309.
56. Sipilä S, Suominen H. 1994. Knee extension strength and walking speed in relation to quadriceps muscle composition and training in elderly women. Clinical Physiology 14:433-442 DOI 10.1111/j.1475-097X.1994.tb00402.x.
57. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB. 2005. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 60:324-333 DOI 10.1093/gerona/60.3.324.
58. Watanabe Y, Yamada Y, Fukumoto Y, Ishihara T, Yokoyama K, Yoshida M, Yamagata E, Kimura M. 2013. Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clinical Interventions in Aging 8:993-998.
59. Whittaker J, Teyhen D, Elliott J, Cook K, Langevin H, Dahl H, Stokes M. 2007. Rehabilitative ultrasound imaging: understanding the technology and its applications. Journal of Orthopaedic & Sports Physical Therapy 37:434-449 DOI 10.2519/jospt.2007.2350.
60. Wroblewski AP, Amati F, Smiley MA, Goodpaster B, Wright V. 2011. Chronic exercise preserves lean muscle mass in masters athletes. The Physician and Sportsmedicine 39:172-178 DOI 10.3810/psm.2011.09.1933.
61. Zaidman CM, Connolly AM, Malkus EC, Florence JM, Pestronk A. 2010. Quantitative ultrasound using backscatter analysis in Duchenne and Becker muscular dystrophy. Neuromuscular Disorders 20:805-809 DOI 10.1016/j.nmd.2010.06.019.
62. Zaidman CM, Holland MR, Anderson CC, Pestronk A. 2008. Calibrated quantitative ultrasound imaging of skeletal muscle using backscatter analysis. Muscle & Nerve 38:893-898 DOI 10.1002/mus.21052.
63. Zaidman CM, Holland MR, Hughes MS. 2012. Quantitative ultrasound of skeletal muscle: reliable measurements of calibrated muscle backscatter from different ultrasound systems. Ultrasound in Medicine & Biology 38:1618-1625 DOI 10.1016/j.ultrasmedbio.2012.04.020.