Ultrasonic Evaluation of Muscle Echogenicity in the Lower Limbs for the Detection of Diabetic Peripheral Neuropathy
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Abstract
Purpose: This study aimed to test the ability of high-frequency muscle ultrasound in detecting changes in muscle Echo Intensity (EI) in patients with type 2 Diabetes Mellitus (T2DM) and to correlate muscle ultrasonography findings with Nerve Conduction Study (NCS) parameters in those patients. Additionally, we aimed to assess the usefulness of muscle ultrasound in diagnosing diabetic peripheral neuropathy.
Materials and Methods: In this case-control study, 26 diabetic patients with Diabetic Peripheral Neuropathy (DPN) and 25 controls were enrolled. Among the controls, 15 were healthy individuals, and the remaining 10 were diabetic patients without DPN. All participants underwent Nerve Conduction Studies (NCS) of the peroneal and tibial motor nerves, as well as quantitative muscle ultrasound. Ultrasound (US) images of the Abductor Hallucis (AH) muscle, Tibialis Anterior (TA) muscle, and Rectus Femoris (RF) muscle were taken and analyzed using grayscale analysis to measure quantitative Echo Intensity (EI). A comparison between the groups regarding EI was made, and correlations between NCS and quantitative US results were assessed.
Results: Our Study unveiled a statistically significant augmentation in muscular EI within two of the scrutinized muscle groups among individuals afflicted by DPN, relative to the control cohorts. Moreover, a noteworthy correlation was discerned between the parameters of NCS and muscular EI.
Conclusion: Quantitating muscle EI using grayscale analysis of US images is a useful supplementary test for the detection of DPN.
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2- Numan Salman Dawood, Numan S Dawood, and Maan H Al-khalisy, "Evaluation of the effect of type II diabetes mellitus on Bone Mineral Density of Upper and Lower Limbs by Dual-Energy X-Ray Absorptiometry." Journal of the Faculty of Medicine Baghdad, Vol. 65 (No. 1), pp. 27-33, (2023).
3- Hailun Huang and Shan Wu, "Application of high-resolution ultrasound on diagnosing diabetic peripheral neuropathy." Diabetes, Metabolic Syndrome and Obesity, pp. 139-52, (2021).
4- Kamakshi Patel, Holli Horak, and Ezgi Tiryaki, "Diabetic neuropathies." Muscle & Nerve, Vol. 63 (No. 1), pp. 22-30, (2021).
5- Caitlin W Hicks and Elizabeth Selvin, "Epidemiology of peripheral neuropathy and lower extremity disease in diabetes." Current diabetes reports, Vol. 19pp. 1-8, (2019).
6- Jennifer Miller, Henrik Gollee, and Mariel Purcell, "Ultrasound imaging as a diagnostic tool to assess the functional status of muscles after a spinal cord injury." Ultrasound in Medicine & Biology, Vol. 47 (No. 3), pp. 386-97, (2021).
7- Natalia L Gonzalez and Lisa D Hobson-Webb, "Neuromuscular ultrasound in clinical practice: A review." Clinical neurophysiology practice, Vol. 4pp. 148-63, (2019).
8- A.J.A. Al-Sarray, "Molecular and electronic properties of Schiff bases derived from different aniline derivatives: density functional theory study." Eurasian Chemical Communications, Vol. 5 (No. 4), pp. 317-26, (2023).
9- Arne Schwennicke, Meikel Bargfrede, and Carl D Reimers, "Clinical, electromyographic, and ultrasonographic assessment of focal neuropathies." Journal of neuroimaging, Vol. 8 (No. 3), pp. 136-43, (1998).
10- Ilse MP Arts, Sigrid Pillen, H Jurgen Schelhaas, Sebastiaan Overeem, and Machiel J Zwarts, "Normal values for quantitative muscle ultrasonography in adults." Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, Vol. 41 (No. 1), pp. 32-41, (2010).
11- Natalia Maria Maurits, Anna Elizabeth Bollen, Alphons Windhausen, Aeiko Eppo Jurjen De Jager, and Johannes Harmen Van Der Hoeven, "Muscle ultrasound analysis: normal values and differentiation between myopathies and neuropathies." Ultrasound in Medicine & Biology, Vol. 29 (No. 2), pp. 215-25, (2003).
12- Zenji Makita et al., "Advanced glycosylation end products in patients with diabetic nephropathy." New England Journal of Medicine, Vol. 325 (No. 12), pp. 836-42, (1991).
13- Cheng-Yin Tan, Thaarani Arumugam, Siti Nur Omaira Razali, Mohd Azly Yahya, Khean-Jin Goh, and Nortina Shahrizaila, "Nerve ultrasound can distinguish chronic inflammatory demyelinating polyneuropathy from demyelinating diabetic sensorimotor polyneuropathy." Journal of Clinical Neuroscience, Vol. 57pp. 198-201, (2018).
14- Ali J. A. Al-Sarray, Tarik Al-Kayat, Borhan Mustafa Mohammed, Mohammed Jassim Bader Al-assadi, and Yousif Abu-Zaid, "Dielectric and Electrical Properties of Intercalated 1-(4-nitrophenyl)-N-(p-tolyl) methanimine into the Interlayers of Bentonite Clay." Journal of Medicinal and Chemical Sciences, Vol. 5 (No. 7 (Special Issue)), pp. 1321-30, (2022).
15- Ihsan M Ajeena, "Effect of hypertension on diabetic peripheral neuropathy." Journal of the Faculty of Medicine Baghdad, Vol. 50 (No. 2), pp. 160-65, (2008).
16- Steven J Brown, Joseph C Handsaker, Frank L Bowling, Costantinos N Maganaris, Andrew JM Boulton, and Neil D Reeves, "Do patients with diabetic neuropathy use a higher proportion of their maximum strength when walking?" Journal of biomechanics, Vol. 47 (No. 15), pp. 3639-44, (2014).
17- Omar Farooq Nafea Al-Azzawi, Mohammed Waheeb Alobaidy, and Momtaz M Saham, "Nephrotic range proteinuria; does it predict lung involvement in patients with type 2 diabetes." Diabetes & Metabolic Syndrome: Clinical Research & Reviews, Vol. 13 (No. 1), pp. 622-25, (2019).
18- Giorgio Orlando, Stefano Balducci, Andrew JM Boulton, Hans Degens, and Neil D Reeves, "Neuromuscular dysfunction and exercise training in people with diabetic peripheral neuropathy: a narrative review." Diabetes Research and Clinical Practice, Vol. 183p. 109183, (2022).
19- Tatiana Y Kostrominova, "Skeletal Muscle Denervation: Past, Present and Future." International Journal of Molecular Sciences, Vol. 23 (No. 14), p. 7489, (2022).
20- Gerd Gunreben and Ulrich Bogdahn, "Real‐time sonography of acute and chronic muscle denervation." Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, Vol. 14 (No. 7), pp. 654-64, (1991).
21- Karim Reimers, Carl D Reimers, Stefen Wagner, I Paetzke, and DE Pongratz, "Skeletal muscle sonography: a correlative study of echogenicity and morphology." Journal of Ultrasound in Medicine, Vol. 12 (No. 2), pp. 73-77, (1993).
22- Sigrid Pillen et al., "Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity." Ultrasound in Medicine & Biology, Vol. 35 (No. 3), pp. 443-46, (2009).
23- David Mayans, Michael S Cartwright, and Francis O Walker, "Neuromuscular ultrasonography: quantifying muscle and nerve measurements." Physical Medicine and Rehabilitation Clinics, Vol. 23 (No. 1), pp. 133-48, (2012).
24- H Andersen, PC Gadeberg, B Brock, and J Jakobsen, "Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study." Diabetologia, Vol. 40pp. 1062-69, (1997).
25- Steven B Soliman et al., "The hyperechoic appearance of the deltoid muscle on shoulder ultrasound imaging as a predictor of diabetes and prediabetes." Journal of Ultrasound in Medicine, Vol. 39 (No. 2), pp. 323-29, (2020).
26- F Zidan Howayda, E Hanan, Amr M Gamil, S Soad, and H Agyad, "Correlation between Quantitative Ultrasonography on Small Muscles of the Foot in Diabetic Peripheral Neuropathy and Electrodiagnostic Study." The Medical Journal of Cairo University, Vol. 88 (No. December), pp. 1975-84, (2020).
27- Hyewon Lee, Sungju Jee, Soo Ho Park, Seung-Chan Ahn, Juneho Im, and Min Kyun Sohn, "Quantitative muscle ultrasonography in carpal tunnel syndrome." Annals of Rehabilitation Medicine, Vol. 40 (No. 6), pp. 1048-56, (2016).
28- S Pillen, A Verrips, N Van Alfen, IMP Arts, LTL Sie, and MJ Zwarts, "Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease." Neuromuscular disorders, Vol. 17 (No. 7), pp. 509-16, (2007).
29- Ji-Sun Kim, Hung Youl Seok, and Byung-Jo Kim, "The significance of muscle echo intensity on ultrasound for focal neuropathy: the median-to ulnar-innervated muscle echo intensity ratio in carpal tunnel syndrome." Clinical Neurophysiology, Vol. 127 (No. 1), pp. 880-85, (2016).
30- Keiichi Hokkoku et al., "Quantitative muscle ultrasound is useful for evaluating secondary axonal degeneration in chronic inflammatory demyelinating polyneuropathy." Brain and Behavior, Vol. 7 (No. 10), p. e00812, (2017).
31- Felix Klawitter, Uwe Walter, Robert Patejdl, Josefine Endler, Daniel A Reuter, and Johannes Ehler, "Sonographic evaluation of muscle echogenicity for the detection of intensive care unit-acquired weakness: a pilot single-center prospective cohort study." Diagnostics, Vol. 12 (No. 6), p. 1378, (2022).
32- N Shahrizaila et al., "Quantitative muscle ultrasound as a biomarker in Charcot-Marie-Tooth neuropathy." Clinical Neurophysiology, Vol. 128 (No. 1), pp. 227-32, (2017).
2- Numan Salman Dawood, Numan S Dawood, and Maan H Al-khalisy, "Evaluation of the effect of type II diabetes mellitus on Bone Mineral Density of Upper and Lower Limbs by Dual-Energy X-Ray Absorptiometry." Journal of the Faculty of Medicine Baghdad, Vol. 65 (No. 1), pp. 27-33, (2023).
3- Hailun Huang and Shan Wu, "Application of high-resolution ultrasound on diagnosing diabetic peripheral neuropathy." Diabetes, Metabolic Syndrome and Obesity, pp. 139-52, (2021).
4- Kamakshi Patel, Holli Horak, and Ezgi Tiryaki, "Diabetic neuropathies." Muscle & Nerve, Vol. 63 (No. 1), pp. 22-30, (2021).
5- Caitlin W Hicks and Elizabeth Selvin, "Epidemiology of peripheral neuropathy and lower extremity disease in diabetes." Current diabetes reports, Vol. 19pp. 1-8, (2019).
6- Jennifer Miller, Henrik Gollee, and Mariel Purcell, "Ultrasound imaging as a diagnostic tool to assess the functional status of muscles after a spinal cord injury." Ultrasound in Medicine & Biology, Vol. 47 (No. 3), pp. 386-97, (2021).
7- Natalia L Gonzalez and Lisa D Hobson-Webb, "Neuromuscular ultrasound in clinical practice: A review." Clinical neurophysiology practice, Vol. 4pp. 148-63, (2019).
8- A.J.A. Al-Sarray, "Molecular and electronic properties of Schiff bases derived from different aniline derivatives: density functional theory study." Eurasian Chemical Communications, Vol. 5 (No. 4), pp. 317-26, (2023).
9- Arne Schwennicke, Meikel Bargfrede, and Carl D Reimers, "Clinical, electromyographic, and ultrasonographic assessment of focal neuropathies." Journal of neuroimaging, Vol. 8 (No. 3), pp. 136-43, (1998).
10- Ilse MP Arts, Sigrid Pillen, H Jurgen Schelhaas, Sebastiaan Overeem, and Machiel J Zwarts, "Normal values for quantitative muscle ultrasonography in adults." Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, Vol. 41 (No. 1), pp. 32-41, (2010).
11- Natalia Maria Maurits, Anna Elizabeth Bollen, Alphons Windhausen, Aeiko Eppo Jurjen De Jager, and Johannes Harmen Van Der Hoeven, "Muscle ultrasound analysis: normal values and differentiation between myopathies and neuropathies." Ultrasound in Medicine & Biology, Vol. 29 (No. 2), pp. 215-25, (2003).
12- Zenji Makita et al., "Advanced glycosylation end products in patients with diabetic nephropathy." New England Journal of Medicine, Vol. 325 (No. 12), pp. 836-42, (1991).
13- Cheng-Yin Tan, Thaarani Arumugam, Siti Nur Omaira Razali, Mohd Azly Yahya, Khean-Jin Goh, and Nortina Shahrizaila, "Nerve ultrasound can distinguish chronic inflammatory demyelinating polyneuropathy from demyelinating diabetic sensorimotor polyneuropathy." Journal of Clinical Neuroscience, Vol. 57pp. 198-201, (2018).
14- Ali J. A. Al-Sarray, Tarik Al-Kayat, Borhan Mustafa Mohammed, Mohammed Jassim Bader Al-assadi, and Yousif Abu-Zaid, "Dielectric and Electrical Properties of Intercalated 1-(4-nitrophenyl)-N-(p-tolyl) methanimine into the Interlayers of Bentonite Clay." Journal of Medicinal and Chemical Sciences, Vol. 5 (No. 7 (Special Issue)), pp. 1321-30, (2022).
15- Ihsan M Ajeena, "Effect of hypertension on diabetic peripheral neuropathy." Journal of the Faculty of Medicine Baghdad, Vol. 50 (No. 2), pp. 160-65, (2008).
16- Steven J Brown, Joseph C Handsaker, Frank L Bowling, Costantinos N Maganaris, Andrew JM Boulton, and Neil D Reeves, "Do patients with diabetic neuropathy use a higher proportion of their maximum strength when walking?" Journal of biomechanics, Vol. 47 (No. 15), pp. 3639-44, (2014).
17- Omar Farooq Nafea Al-Azzawi, Mohammed Waheeb Alobaidy, and Momtaz M Saham, "Nephrotic range proteinuria; does it predict lung involvement in patients with type 2 diabetes." Diabetes & Metabolic Syndrome: Clinical Research & Reviews, Vol. 13 (No. 1), pp. 622-25, (2019).
18- Giorgio Orlando, Stefano Balducci, Andrew JM Boulton, Hans Degens, and Neil D Reeves, "Neuromuscular dysfunction and exercise training in people with diabetic peripheral neuropathy: a narrative review." Diabetes Research and Clinical Practice, Vol. 183p. 109183, (2022).
19- Tatiana Y Kostrominova, "Skeletal Muscle Denervation: Past, Present and Future." International Journal of Molecular Sciences, Vol. 23 (No. 14), p. 7489, (2022).
20- Gerd Gunreben and Ulrich Bogdahn, "Real‐time sonography of acute and chronic muscle denervation." Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, Vol. 14 (No. 7), pp. 654-64, (1991).
21- Karim Reimers, Carl D Reimers, Stefen Wagner, I Paetzke, and DE Pongratz, "Skeletal muscle sonography: a correlative study of echogenicity and morphology." Journal of Ultrasound in Medicine, Vol. 12 (No. 2), pp. 73-77, (1993).
22- Sigrid Pillen et al., "Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity." Ultrasound in Medicine & Biology, Vol. 35 (No. 3), pp. 443-46, (2009).
23- David Mayans, Michael S Cartwright, and Francis O Walker, "Neuromuscular ultrasonography: quantifying muscle and nerve measurements." Physical Medicine and Rehabilitation Clinics, Vol. 23 (No. 1), pp. 133-48, (2012).
24- H Andersen, PC Gadeberg, B Brock, and J Jakobsen, "Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study." Diabetologia, Vol. 40pp. 1062-69, (1997).
25- Steven B Soliman et al., "The hyperechoic appearance of the deltoid muscle on shoulder ultrasound imaging as a predictor of diabetes and prediabetes." Journal of Ultrasound in Medicine, Vol. 39 (No. 2), pp. 323-29, (2020).
26- F Zidan Howayda, E Hanan, Amr M Gamil, S Soad, and H Agyad, "Correlation between Quantitative Ultrasonography on Small Muscles of the Foot in Diabetic Peripheral Neuropathy and Electrodiagnostic Study." The Medical Journal of Cairo University, Vol. 88 (No. December), pp. 1975-84, (2020).
27- Hyewon Lee, Sungju Jee, Soo Ho Park, Seung-Chan Ahn, Juneho Im, and Min Kyun Sohn, "Quantitative muscle ultrasonography in carpal tunnel syndrome." Annals of Rehabilitation Medicine, Vol. 40 (No. 6), pp. 1048-56, (2016).
28- S Pillen, A Verrips, N Van Alfen, IMP Arts, LTL Sie, and MJ Zwarts, "Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease." Neuromuscular disorders, Vol. 17 (No. 7), pp. 509-16, (2007).
29- Ji-Sun Kim, Hung Youl Seok, and Byung-Jo Kim, "The significance of muscle echo intensity on ultrasound for focal neuropathy: the median-to ulnar-innervated muscle echo intensity ratio in carpal tunnel syndrome." Clinical Neurophysiology, Vol. 127 (No. 1), pp. 880-85, (2016).
30- Keiichi Hokkoku et al., "Quantitative muscle ultrasound is useful for evaluating secondary axonal degeneration in chronic inflammatory demyelinating polyneuropathy." Brain and Behavior, Vol. 7 (No. 10), p. e00812, (2017).
31- Felix Klawitter, Uwe Walter, Robert Patejdl, Josefine Endler, Daniel A Reuter, and Johannes Ehler, "Sonographic evaluation of muscle echogenicity for the detection of intensive care unit-acquired weakness: a pilot single-center prospective cohort study." Diagnostics, Vol. 12 (No. 6), p. 1378, (2022).
32- N Shahrizaila et al., "Quantitative muscle ultrasound as a biomarker in Charcot-Marie-Tooth neuropathy." Clinical Neurophysiology, Vol. 128 (No. 1), pp. 227-32, (2017).
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| Issue | Vol 11 No 3 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/fbt.v11i3.15889 | |
| Keywords | ||
| Diabetic Peripheral Neuropathy Muscle Ultrasound Echo Intensity Nerve Conduction Study Greyscale Analysis | ||
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How to Cite
1.
Abdulkareem SH, H. Ameer A. Ultrasonic Evaluation of Muscle Echogenicity in the Lower Limbs for the Detection of Diabetic Peripheral Neuropathy. Frontiers Biomed Technol. 2024;11(3):462-470.
