Stiffness of the Masseter Muscle in Children—Establishing the Reference Values in the Pediatric Population Using Shear-Wave Elastography
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bertini, E.; D’Amico, A.; Gualandi, F.; Petrini, S. Congenital muscular dystrophies: A brief review. Semin. Pediatr. Neurol. 2011, 18, 277–288. [Google Scholar] [CrossRef] [Green Version]
- Kruse, A.; Schranz, C.; Tilp, M.; Svehlik, M. Muscle and tendon morphology alterations in children and adolescents with mild forms of spastic cerebral palsy. BMC Pediatr. 2018, 18, 156. [Google Scholar] [CrossRef] [Green Version]
- Hemke, R.; Herregods, N.; Jaremko, J.L.; Åström, G.; Avenarius, D.; Becce, F.; Bielecki, D.K.; Boesen, M.; Dalili, D.; Giraudo, C.; et al. Imaging assessment of children presenting with suspected or known juvenile idiopathic arthritis: ESSR-ESPR points to consider. Eur. Radiol. 2020, 30, 5237. [Google Scholar] [CrossRef]
- Parent, S.; Mac-Thiong, J.M.; Roy-Beaudry, M.; Sosa, J.F.; Labelle, H. Spinal cord injury in the pediatric population: A systematic review of the literature. J. Neurotrauma 2011, 28, 1515–1524. [Google Scholar] [CrossRef] [Green Version]
- Wahlund, K. Temporomandibular disorders in adolescents. Epidemiological and methodological studies and a randomized controlled trial. Swed. Dent. J. Suppl. 2003, 164, 2–64. [Google Scholar]
- Goo, M.; Johnston, L.M.; Hug, F.; Tucker, K. Systematic Review of Instrumented Measures of Skeletal Muscle Mechanical Properties: Evidence for the Application of Shear Wave Elastography with Children. Ultrasound Med. Biol. 2020, 46, 1831–1840. [Google Scholar] [CrossRef]
- Al-Khotani, A.; Naimi-Akbar, A.; Gjelset, M.; Albadawi, E.; Bello, L.; Hedenberg-Magnusson, B.; Christidis, N. The associations between psychosocial aspects and TMD-pain related aspects in children and adolescents. J. Headache Pain 2016, 17, 30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Christidis, N.; Lindström Ndanshau, E.; Sandberg, A.; Tsilingaridis, G. Prevalence and treatment strategies regarding temporomandibular disorders in children and adolescents-A systematic review. J. Oral Rehabil. 2019, 46, 291–301. [Google Scholar] [CrossRef] [PubMed]
- Wieckiewicz, M.; Grychowska, N.; Nahajowski, M.; Hnitecka, S.; Kempiak, K.; Charemska, K.; Balicz, A.; Chirkowska, A.; Zietek, M.; Winocur, E. Prevalence and Overlaps of Headaches and Pain-Related Temporomandibular Disorders Among the Polish Urban Population. J. Oral Facial Pain Headache 2020, 34, 31–39. [Google Scholar] [CrossRef] [PubMed]
- List, T.; Wahlund, K.; Wenneberg, B.; Dworkin, S.F. TMD in children and adolescents: Prevalence of pain, gender differences, and perceived treatment need. J. Orofac. Pain 1999, 13, 9–20. [Google Scholar]
- Franco-Micheloni, A.L.; Fernandes, G.; de Godoi Gonçalves, D.A.; Camparis, C.M. Temporomandibular Disorders in a Young Adolescent Brazilian Population: Epidemiologic Characterization and Associated Factors. J. Oral Facial Pain Headache 2015, 29, 242–249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Melo Júnior, P.C.; Aroucha, J.; Arnaud, M.; Lima, M.G.S.; Gomes, S.G.F.; Ximenes, R.; Rosenblatt, A.; Caldas, A.F., Jr. Prevalence of TMD and level of chronic pain in a group of Brazilian adolescents. PLoS ONE 2019, 14, e0205874. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scrivani, S.J.; Khawaja, S.N.; Bavia, P.F. Nonsurgical Management of Pediatric Temporomandibular Joint Dysfunction. Oral Maxillofac. Surg. Clin. N. Am. 2018, 30, 35–45. [Google Scholar] [CrossRef]
- Dietsch, A.M.; Clark, H.M.; Steiner, J.N.; Solomon, N.P. Effects of Age, Sex, and Body Position on Orofacial Muscle Tone in Healthy Adults. J. Speech Lang. Hear. Res. 2015, 58, 1145–1150. [Google Scholar] [CrossRef] [Green Version]
- Carroll, K.; Yiu, E.M.; Ryan, M.M.; Kennedy, R.A.; de Valle, K. The effects of calf massage in boys with Duchenne muscular dystrophy: A prospective interventional study. Disabil. Rehabil. 2020, 1–7. [Google Scholar] [CrossRef]
- Gagnat, Y.; Brændvik, S.M.; Roeleveld, K. Surface Electromyography Normalization Affects the Interpretation of Muscle Activity and Coactivation in Children With Cerebral Palsy During Walking. Front. Neurol. 2020, 11, 202. [Google Scholar] [CrossRef] [PubMed]
- Díaz-Serrano, K.V.; Dias, T.M.; Vasconcelos, P.; Sousa, L.G.; Siéssere, S.; Regalo, S.; Palinkas, M. Impact of temporomandibular disorders on the stomatognathic system in children. Med. Oral Patol. Oral Cir. Bucal. 2017, 22, e723–e729. [Google Scholar] [CrossRef] [PubMed]
- Bohannon, R.W.; Smith, M.B. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys. Ther. 1987, 67, 206–207. [Google Scholar] [CrossRef] [PubMed]
- Akbaş, A.N. Assessments and outcome measures of cerebral palsy. In Cerebral Palsy—Current Steps; Gunel, M.K., Ed.; IntechOpen: London, UK, 2016. [Google Scholar]
- Ariji, Y.; Nakayama, M.; Nishiyama, W.; Ogi, N.; Sakuma, S.; Katsumata, A.; Kurita, K.; Ariji, E. Can sonographic features be efficacy predictors of robotic massage treatment for masseter and temporal muscle in patients with temporomandibular disorder with myofascial pain? Cranio 2016, 34, 13–19. [Google Scholar] [CrossRef]
- Kishimoto, R.; Suga, M.; Koyama, A.; Omatsu, T.; Tachibana, Y.; Ebner, D.K.; Obata, T. Measuring shear-wave speed with point shear-wave elastography and MR elastography: A phantom study. BMJ Open 2017, 7, e013925. [Google Scholar] [CrossRef]
- Calvete, A.C.; Rodriguez, J.M.; de Dios Berna-Mestre, J.; Rios, A.; Abellan-Rivero, D.; Reus, M. Interobserver agreement for thyroid elastography: Value of the quality factor. J. Ultrasound Med. 2013, 32, 495–504. [Google Scholar] [CrossRef]
- Garcovich, M.; Di Stasio, E.; Zocco, M.A.; Riccardi, L.; Elena Ainora, M.; Annicchiarico, B.E.; Gibiino, G.; Santopaolo, F.; Gasbarrini, A.; Pompili, M. Assessing Baveno VI criteria with liver stiffness measured using a new point-shear wave elastography technique (BAVElastPQ study). Liver Int. 2020, 40, 1952–1960. [Google Scholar] [CrossRef]
- Xu, B.; Jiang, G.; Ye, J.; He, J.; Xie, W. Research on pediatric glomerular disease and normal kidney with shear wave based elastography point quantification. JPN J. Radiol. 2016, 34, 738–746. [Google Scholar] [CrossRef]
- Brandenburg, J.E.; Eby, S.F.; Song, P.; Kingsley-Berg, S.; Bamlet, W.; Sieck, G.C.; An, K.-N. Quantifying passive muscle stiffness in children with and without cerebral palsy using ultrasound shear wave elastography. Dev. Med. Child. Neurol. 2016, 58, 1288–1294. [Google Scholar] [CrossRef] [Green Version]
- Lacourpaille, L.; Gross, R.; Hug, F.; Guével, A.; Péréon, Y.; Magot, A.; Hogrel, J.-Y.; Nordez, A. Effects of Duchenne muscular dystrophy on muscle stiffness and response to electrically-induced muscle contraction: A 12-month follow-up. Neuromuscul. Disord. 2017, 27, 214–220. [Google Scholar] [CrossRef] [PubMed]
- Linek, P.; Wolny, T.; Sikora, D.; Klepek, A. Supersonic Shear Imaging for Quantification of Lateral Abdominal Muscle Shear Modulus in Pediatric Population with Scoliosis: A Reliability and Agreement Study. Ultrasound Med. Biol. 2019, 45, 1551–1561. [Google Scholar] [CrossRef]
- Thomas, K.; Shankar, H. Targeting myofascial taut bands by ultrasound. Curr. Pain Headache Rep. 2013, 17, 349. [Google Scholar] [CrossRef] [PubMed]
- Olchowy, C.; Olchowy, A.; Hadzik, J.; Dąbrowski, P.; Mierzwa, D. Dentists can provide reliable shear wave elastography measurements of the stiffness of masseter muscles: A possible scenario for a faster diagnostic process. Adv. Clin. Exp. Med. 2021, 30, 575–580. [Google Scholar] [CrossRef] [PubMed]
- Raadsheer, M.C.; Van Eijden, T.M.; Van Spronsen, P.H.; Van Ginkel, F.C.; Kiliaridis, S.; Prahl-Andersen, B. A comparison of human masseter muscle thickness measured by ultrasonography and magnetic resonance imaging. Arch. Oral Biol. 1994, 39, 1079–1084. [Google Scholar] [CrossRef]
- Botticchio, A.; Mourad, F.; Fernández-Carnero, S.; Arias-Buría, J.L.; Santodomingo Bueno, A.; Mesa Jiménez, J.; Gobbo, M. Short-Term Morphological Changes in Asymptomatic Perimandibular Muscles after Dry Needling Assessed with Rehabilitative Ultrasound Imaging: A Proof-of-Concept Study. J. Clin. Med. 2021, 10, 209. [Google Scholar] [CrossRef]
- Öztürk, M.; Çalışkan, E.; Habibi, H.A. Shear wave elastography of temporomandibular joint disc and masseter muscle stiffness in healthy children and adolescents: A preliminary study. Oral Radiol. 2021. [Google Scholar] [CrossRef]
- Lacourpaille, L.; Hug, F.; Guével, A.; Péréon, Y.; Magot, A.; Hogrel, J.-Y.; Nordez, A. Non-invasive assessment of muscle stiffness in patients with duchenne muscular dystrophy. Muscle Nerve 2015, 51, 284–286. [Google Scholar] [CrossRef]
- Olchowy, C.; Więckiewicz, M.; Sconfienza, L.M.; Łasecki, M.; Seweryn, P.; Smardz, J.; Hnitecka, S.; Dominiak, M.; Olchowy, A. Potential of Using Shear Wave Elastography in the Clinical Evaluation and Monitoring of Changes in Masseter Muscle Stiffness. Pain Res. Manag. 2020, 2020, 4184268. [Google Scholar] [CrossRef]
- Olchowy, C.; Grzech-Leśniak, K.; Hadzik, J.; Olchowy, A.; Łasecki, M. Monitoring of Changes in Masticatory Muscle Stiffness after Gum Chewing Using Shear Wave Elastography. J. Clin. Med. 2021, 10, 2480. [Google Scholar] [CrossRef] [PubMed]
- Olchowy, A.; Wieckiewicz, M.; Winocur, E.; Dominiak, M.; Dekkers, I.; Łasecki, M.; Olchowy, C. Great potential of ultrasound elastography for the assessment of the masseter muscle in patients with temporomandibular disorders. A systematic review. Dentomaxillofac. Radiol. 2020, 49, 20200024. [Google Scholar] [CrossRef]
- Arda, K.; Ciledag, N.; Aktas, E.; Aribas, B.K.; Kose, K. Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography. AJR Am. J. Roentgenol. 2011, 197, 532–536. [Google Scholar] [CrossRef]
- Herman, J.; Sedlackova, Z.; Vachutka, J.; Furst, T.; Salzman, R.; Vomacka, J. Shear wave elastography parameters of normal soft tissues of the neck. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc. Czech Repub. 2017, 161, 320–325. [Google Scholar] [CrossRef] [Green Version]
- Olchowy, A.; Więckiewicz, M.; Malysa, A.; Olchowy, C. Determination of Reference Values of the Masseter Muscle Stiffness in Healthy Adults Using Shear Wave Elastography. Int. J. Environ. Res. Public Health 2021, 18, 9371. [Google Scholar] [CrossRef] [PubMed]
- Pavan, P.; Monti, E.; Bondí, M.; Fan, C.; Stecco, C.; Narici, M.; Reggiani, C.; Marcucci, L. Alterations of Extracellular Matrix Mechanical Properties Contribute to Age-Related Functional Impairment of Human Skeletal Muscles. Int. J. Mol. Sci. 2020, 21, 3992. [Google Scholar] [CrossRef]
- Ochala, J.; Lambertz, D.; Pousson, M.; Goubel, F.; Hoecke, J.V. Changes in mechanical properties of human plantar flexor muscles in ageing. Exp. Gerontol. 2004, 39, 349–358. [Google Scholar] [CrossRef] [PubMed]
- Chodock, E.; Hahn, J.; Setlock, C.A.; Lipps, D.B. Identifying predictors of upper extremity muscle elasticity with healthy aging. J. Biomech. 2020, 103, 109687. [Google Scholar] [CrossRef] [PubMed]
- Şendur, H.N.; Cindil, E.; Cerit, M.N.; Kılıç, P.; Gültekin, I.; Oktar, S. Evaluation of effects of aging on skeletal muscle elasticity using shear wave elastography. Eur. J. Radiol. 2020, 128, 109038. [Google Scholar] [CrossRef] [PubMed]
- Takashima, M.; Arai, Y.; Kawamura, A.; Hayashi, T.; Takagi, R. Quantitative evaluation of masseter muscle stiffness in patients with temporomandibular disorders using shear wave elastography. J. Prosthodont. Res. 2017, 61, 432–438. [Google Scholar] [CrossRef] [PubMed]
- Perez, C. Temporomandibular disorders in children and adolescents. Gen. Dent. 2018, 66, 51–55. [Google Scholar]
Group | Mean ± SD | Median (IQR) |
---|---|---|
Total | ||
Age (year) | 10.87 ± 3.38 | 12.00 (9.25–13.00) |
Left masseter (kPa) | 6.47 ± 0.78 | 6.33 (6.11–7.04) |
SD of left masseter | 1.45 ± 0.42 | 1.41 (1.11–1.63) |
Right masseter (kPa) | 6.24 ± 0.76 | 6.30 (5.58–6.71) |
SD of right masseter | 1.41 ± 0.52 | 1.40 (0.91–1.83) |
Girls | ||
Age (year) | 10.28 ± 4.16 | 11.50 (8.25–13.00) |
Total value (kPa) | 6.63 ± 0.80 | 6.68 (6.10–7.13) |
Left masseter (kPa) | 6.72 ± 0.85 | 6.87 (6.17–7.13) |
SD of left masseter | 1.62 ± 0.42 | 1.60 (1.37–1.70) |
Right masseter (kPa) | 6.54 ± 0.77 | 6.63 (5.87–6.77) |
SD of right masseter | 1.61 ± 0.53 | 1.73 (1.00–2.03) |
Boys | ||
Age (year) | 11.75 ± 1.42 | 12.00 (11.00–13.00) |
Total value (kPa) | 5.94 ± 0.50 | 6.12 (5.55–6.30) |
Left masseter (kPa) | 6.09 ± 0.46 | 6.17 (6.10–6.31) |
SD of left masseter | 1.20 ± 0.30 | 1.12 (1.06–1.31) |
Right masseter (kPa) | 5.80 ± 0.52 | 5.67 (5.50–6.30) |
SD of right masseter | 1.10 ± 0.33 | 0.92 (0.86–1.40) |
Comparison | p-Value |
---|---|
Age boys/age girls (year) | 0.5354 |
Left masseter total/right masseter total | 0.3546 |
Masseters boys/masseters girls | 0.0006 |
Left masseter girls/right masseter girls | 0.3420 |
Left masseter boys/right masseter boys | 0.2973 |
Left masseter girls/left masseters boys | 0.0416 |
Right masseter girls/right masseters boys | 0.0030 |
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Olchowy, C.; Olchowy, A.; Pawluś, A.; Więckiewicz, M.; Sconfienza, L.M. Stiffness of the Masseter Muscle in Children—Establishing the Reference Values in the Pediatric Population Using Shear-Wave Elastography. Int. J. Environ. Res. Public Health 2021, 18, 9619. https://doi.org/10.3390/ijerph18189619
Olchowy C, Olchowy A, Pawluś A, Więckiewicz M, Sconfienza LM. Stiffness of the Masseter Muscle in Children—Establishing the Reference Values in the Pediatric Population Using Shear-Wave Elastography. International Journal of Environmental Research and Public Health. 2021; 18(18):9619. https://doi.org/10.3390/ijerph18189619
Chicago/Turabian StyleOlchowy, Cyprian, Anna Olchowy, Aleksander Pawluś, Mieszko Więckiewicz, and Luca Maria Sconfienza. 2021. "Stiffness of the Masseter Muscle in Children—Establishing the Reference Values in the Pediatric Population Using Shear-Wave Elastography" International Journal of Environmental Research and Public Health 18, no. 18: 9619. https://doi.org/10.3390/ijerph18189619