The Relation of Body Mass Index to Muscular Viscoelastic Properties in Normal and Overweight Individuals

Serkan Usgu, Engin Ramazanoğlu, Yavuz Yakut, Serkan Usgu, Engin Ramazanoğlu, Yavuz Yakut

Abstract

Background: The body mass index (BMI) is closely related to fat tissue, which may have direct or indirect effects on muscle function. Previous studies have evaluated BMI and muscle viscoelastic properties in vivo in older people or individual sexes; however, the relationship between BMI and muscular viscoelastic properties is still unknown. Aims: The purpose of this study was to determine the correlation of BMI with muscular viscoelastic properties, and to compare these properties in a young sedentary population with normal and overweight individuals. Methods: A total of 172 healthy sedentary individuals (mean age, 26.00 ± 5.45 years) were categorized by sex (male and female) and BMI classification (normal (BMI, 18.50-24.99 kg/m2), overweight (BMI = 25.00-29.99 kg/m2)). Body weight was evaluated using an electronic scale, while height was measured using a standard stadiometer. BMI was calculated by dividing the weight in kilograms by the square of height in meters. The viscoelastic properties (tone, stiffness, and elasticity) of the biceps brachii (BB) and biceps femoris (BF) muscles were measured bilaterally using the MyotonPRO device at rest. Results: The bilateral BF tone and stiffness, right BB stiffness, and elasticity showed weak correlations with BMI in all participants. Furthermore, the bilateral BF tone and stiffness, right BB stiffness and elasticity, and left BB stiffness were weakly positively correlated with male sex. Only the right BB elasticity was weakly positively correlated with BMI in females (p < 0.05). No correlation with BMI was determined for other viscoelastic properties (p > 0.05). The overweight group showed increased bilateral BF stiffness and tone, right BB stiffness, and reduced bilateral BB elasticity compared to the normal-weight group (p < 0.05), while other viscoelastic properties were similar (p > 0.05). Greater bilateral BB tone, BF tone and stiffness, and lower BF elasticity were observed in males than in females (p < 0.05), but other viscoelastic properties were not significantly different (p < 0.05). No effect of BMI-sex interactions was found on viscoelastic properties (p > 0.05). Conclusions: The BB and BF viscoelastic properties were weakly correlated with BMI. Males showed greater muscle tone and stiffness, and lower elasticity. The overweight individuals showed increased stiffness and tone, particularly in lower extremities, and reduced elasticity in upper extremities. The effect of BMI-sex interactions on the viscoelastic properties was not clear. Higher BMI (increased mechanical load) might cause the human body to develop different muscular viscoelastic adaptations in the extremities.

Keywords: body mass index; elasticity; overweight; stiffness; tone.

Conflict of interest statement

All authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
The reference points of muscles for myotonometric assessment: (a) biceps femoris; (b) biceps brachii.

References

    1. Flegal K.M., Carroll M.D., Kit B.K., Ogden C.L. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA. 2012;307:491–497. doi: 10.1001/jama.2012.39.
    1. Wang F., McDonald T., Champagne L.J., Edington D.W. Relationship of body mass index and physical activity to health care costs among employees. J. Occup. Med. 2004;46:428–436. doi: 10.1097/.
    1. Hilton T.N., Tuttle L.J., Bohnert K.L., Mueller M.J., Sinacore D.R. Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: Association with performance and function. Phys. Ther. 2008;88:1336–1344. doi: 10.2522/ptj.20080079.
    1. Hamaguchi Y., Kaido T., Okumura S., Kobayashi A., Shirai H., Yagi S., Naoko K., Hideaki O., Shinji U. Impact of skeletal muscle mass index, intramuscular adipose tissue content, and visceral to subcutaneous adipose tissue area ratio on early mortality of living donor liver transplantation. Transplantation. 2017;101:565–574. doi: 10.1097/TP.0000000000001587.
    1. Šarabon N., Kozinc Ž., Podrekar N. Using shear-wave elastography in skeletal muscle: A repeatability and reproducibility study on biceps femoris muscle. PLoS ONE. 2019;14:e0222008.
    1. Feng Y., Li Y., Liu C., Zhang Z. Assessing the elastic properties of skeletal muscle and tendon using shearwave ultrasound elastography and MyotonPRO. Sci. Rep. 2018;8:1–9.
    1. Gapeyeva H., Vain A. Methodical Guide: Principles of Applying Myoton in Physical Medicine and Rehabilitation. Müomeetria Ltd.; Tartu, Estonia: 2008.
    1. Agyapong-Badu S., Warner M., Samuel D., Stokes M. Practical considerations for standardized recording of muscle mechanical properties using a myometric device: Recording site, muscle length, state of contraction and prior activity. J. Musculoskelet Res. 2018;21:1850010. doi: 10.1142/S0218957718500100.
    1. Faria A., Gabriel R., Abrantes J., Brás R., Moreira H. Triceps-surae musculotendinous stiffness: Relative differences between obese and non-obese postmenopausal women. Clin. Biomech. 2009;24:866–871. doi: 10.1016/j.clinbiomech.2009.07.015.
    1. Kuo W.H., Jian D.W., Wang T.G., Wang Y.C. Neck muscle stiffness quantified by sonoelastography is correlated with body mass index and chronic neck pain symptoms. Ultrasound Med. Biol. 2013;39:1356–1361. doi: 10.1016/j.ultrasmedbio.2012.11.015.
    1. Seo A., Lee J.H., Kusaka Y. Estimation of trunk muscle parameters for a biomechanical model by age, height and weight. J. Occup. Health. 2003;45:197–201. doi: 10.1539/joh.45.197.
    1. Wood S., Pearsall D., Ross R., Reid J. Trunk muscle parameters determined from MRI for lean to obese males. Clin. Biomech. 1996;11:139–144. doi: 10.1016/0268-0033(95)00018-6.
    1. Bailey L., Samuel D., Warner M., Stokes M. Parameters representing muscle tone, elasticity and stiffness of biceps brachii in healthy older males: Symmetry and within-session reliability using the MyotonPRO. J. Neurol. Disord. 2013;1:1–7. doi: 10.4172/2329-6895.1000116.
    1. Leonard C.T., Deshner W.P., Romo J.W., Suoja E.S., Fehrer S.C., Mikhailenok E.L. Myotonometer intra-and interrater reliabilities. Arch. Phys. Med. Rehabil. 2003;84:928–932. doi: 10.1016/S0003-9993(03)00006-6.
    1. Agyapong-Badu S., Aird L., Bailey L., Mooney K., Mullix J., Warner M., Samuel D., Stokes M. Interrater reliability of muscle tone, stiffness and elasticity measurements of rectus femoris and biceps brachii in healthy young and older males. Work Pap. Health Sci. 2013;4:1–11.
    1. Chuang L.L., Wu C.Y., Lin K.C. Reliability, validity, and responsiveness of myotonometric measurement of muscle tone, elasticity, and stiffness in patients with stroke. Arch. Phys. Med. Rehabil. 2012;93:532–540. doi: 10.1016/j.apmr.2011.09.014.
    1. Drenth H., Zuidema S.U., Krijnen W.P., Bautmans I., van der Schans C., Hobbelen H. Psychometric properties of the MyotonPRO in dementia patients with paratonia. Gerontology. 2018;64:401–412. doi: 10.1159/000485462.
    1. Lidström Å., Ahlsten G., Hirchfeld H., Norrlin S. Intrarater and interrater reliability of myotonometer measurements of muscle tone in children. J. Child. Neurol. 2009;24:267–274. doi: 10.1177/0883073808323025.
    1. Kocur P., Tomczak M., Wiernicka M., Goliwąs M., Lewandowski J., Łochyński D. Relationship between age, BMI, head posture and superficial neck muscle stiffness and elasticity in adult women. Sci. Rep. 2019;9:1–10.
    1. Saris W., Blair S., Van Baak M., Eaton S., Davies p Di Pietro L., Fogelholm M., Rissanen A., Schoeller D., Swinburn B., Tremblay A., et al. How much physical activity is enough to prevent unhealthy weight gain? Outcome of the IASO 1st Stock Conference and consensus statement. Obes. Rev. 2003;4:101–114. doi: 10.1046/j.1467-789X.2003.00101.x.
    1. Gervasi M., Sisti D., Amatori S., Andreazza M., Benelli P., Sestili P., Rocchi M.B.L., Calavalle A.R. Muscular viscoelastic characteristics of athletes participating in the European Master Indoor Athletics Championship. Eur. J. Appl. Physiol. 2017;117:1739–1746. doi: 10.1007/s00421-017-3668-z.
    1. Saglam M., Arikan H., Savci S., Inal I.D., Bosnak G.M., Karabulut E., Tokgozoglu L. International physical activity questionnaire: Reliability and validity of the Turkish version. Percept. Mot. Skills. 2010;111:278–284. doi: 10.2466/06.08.PMS.111.4.278-284.
    1. Zinder S.M., Padua D.A. Reliability, validity, and precision of a handheld myometer for assessing in vivo muscle stiffness. J. Sport Rehabil. 2011;20 doi: 10.1123/jsr.2010-0051.
    1. Schneebeli A., Falla D., Clijsen R., Barbero M. Myotonometry for the evaluation of Achilles tendon mechanical properties: A reliability and construct validity study. BMJ Open Sport Exerc. Med. 2020;6:e000726. doi: 10.1136/bmjsem-2019-000726.
    1. Liu C.L., Li Y.P., Wang X.Q., Zhang Z.J. Quantifying the stiffness of Achilles tendon: Intra-and inter-operator reliability and the effect of ankle joint motion. Med. Sci. Monit. Med. Sci. Mon. Int. Med. J. Exp. Clin. Res. 2018;24:4876. doi: 10.12659/MSM.909531.
    1. Gavronski G., Veraksitš A., Vasar E., Maaroos J. Evaluation of viscoelastic parameters of the skeletal muscles in junior triathletes. Physiol. Meas. 2007;28:625. doi: 10.1088/0967-3334/28/6/002.
    1. Myoton [(accessed on 12 August 2021)]. [updated 23 July 2021] Available online:
    1. Agyapong-Badu S., Warner M., Samuel D., Stokes M. Measurement of ageing effects on muscle tone and mechanical properties of rectus femoris and biceps brachii in healthy males and females using a novel hand-held myometric device. Arch. Gerontol. Geriatr. 2016;62:59–67. doi: 10.1016/j.archger.2015.09.011.
    1. Rihvk I., Clough A., Clough P. Investigation to compare static stretching and proprioceptive neuromuscular facilitation contract–relax stretching effects on the visco-elastic parameters of the biceps femoris muscle. Int. Musculoskelet. Med. 2010;32:157–162. doi: 10.1179/1753615410Y.0000000004.
    1. Lee Y., Kim M., Lee H. The measurement of stiffness for major muscles with shear wave elastography and myoton: A quantitative analysis study. Diagnostics. 2021;11:524. doi: 10.3390/diagnostics11030524.
    1. Schober P., Boer C., Schwarte L.A. Correlation coefficients: Appropriate use and interpretation. Anesth. Analg. 2018;126:1763–1768. doi: 10.1213/ANE.0000000000002864.
    1. Altman D.G. Practical Statistics for Medical Research. CRC Press; Boca Raton, FL, USA: 1990.
    1. Hoffman L.R., Koppenhaver S.L., MacDonald C.W., Herrera J.M., Streuli J., Visco Z.L., Wildermuth N., Albin S.R. Normative Parameters of Gastrocnemius Muscle Stiffness and Associations with Patient Characteristics and Function. Int. J. Sports Phys. Ther. 2021;16:41.
    1. White A., Abbott H., Masi A.T., Henderson J., Nair K. Biomechanical properties of low back myofascial tissue in younger adult ankylosing spondylitis patients and matched healthy control subjects. Clin. Biomech. 2018;57:67–73. doi: 10.1016/j.clinbiomech.2018.06.006.
    1. Kawai T., Takamoto K., Bito I. Previous hamstring muscle strain injury alters passive tissue stiffness and vibration sense. J. Bodyw. Mov. Ther. 2021;27:573–578. doi: 10.1016/j.jbmt.2021.05.002.
    1. Blackburn J.T., Padua D.A., Weinhold P.S., Guskiewicz K.M. Comparison of triceps surae structural stiffness and material modulus across sex. Clin. Biomech. 2006;21:159–167. doi: 10.1016/j.clinbiomech.2005.08.012.
    1. Deng L., Zhang X., Xiao S., Wang B., Fu W. Gender Difference in Architectural and Mechanical Properties of Medial Gastrocnemius–Achilles Tendon Unit In Vivo. Life. 2021;11:569. doi: 10.3390/life11060569.
    1. Morse C.I. Gender differences in the passive stiffness of the human gastrocnemius muscle during stretch. Eur. J. Appl. Physiol. 2011;111:2149–2154. doi: 10.1007/s00421-011-1845-z.
    1. Chino K., Takahashi H. Association of gastrocnemius muscle stiffness with passive ankle joint stiffness and sex-related difference in the joint stiffness. J. Appl. Biomech. 2018;34:169–174. doi: 10.1123/jab.2017-0121.
    1. Saeki J., Ikezoe T., Yoshimi S., Nakamura M., Ichihashi N. Menstrual cycle variation and gender difference in muscle stiffness of triceps surae. Clin. Biomech. 2019;61:222–226. doi: 10.1016/j.clinbiomech.2018.12.013.
    1. Eby S.F., Cloud B.A., Brandenburg J.E., Giambini H., Song P., Chen S., LeBrasseur N.K., An K.-N. Shear wave elastography of passive skeletal muscle stiffness: Influences of sex and age throughout adulthood. Clinl. Biomech. 2015;30:22–27. doi: 10.1016/j.clinbiomech.2014.11.011.
    1. Miller A.E.J., MacDougall J., Tarnopolsky M., Sale D. Gender differences in strength and muscle fiber characteristics. Eur. J. Appl. Physiol. 1993;66:254–262. doi: 10.1007/BF00235103.
    1. Staron R.S., Hagerman F.C., Hikida R.S., Murray T.F., Hostler D.P., Crill M.T., Ragg K.E., Toma K. Fiber type composition of the vastus lateralis muscle of young men and women. J. Histochem. Cytochem. 2000;48:623–629. doi: 10.1177/002215540004800506.
    1. Shorten M.R. Muscle elasticity and human performance. Med. Sport Sci. 1987;25:1–18.
    1. Abe T., Brechue W.F., Fujita S., Brown J.B. Gender differences in FFM accumulation and architectural characteristics of muscle. Med. Sci. Sports Exerc. 1998;30:1066–1070. doi: 10.1097/00005768-199807000-00007.
    1. Gajdosik R., Giuliani C., Bohannon R. Passive compliance and length of the hamstring muscles of healthy men anc women. Clin. Biomech. 1990;5:23–29. doi: 10.1016/0268-0033(90)90028-5.
    1. Chleboun G.S., Howell J.N., Conatser R.R., Giesey J.J. The relationship between elbow flexor volume and angular stiffness at the elbow. Clin. Biomech. 1997;12:383–392. doi: 10.1016/S0268-0033(97)00027-2.
    1. Komi P.V. Physiological and biomechanical correlates of muscle function: Effects of muscle structure and stretch—Shortening cycle on force and speed. Exerc. Sport Sci. Rev. 1984;12:81–122. doi: 10.1249/00003677-198401000-00006.
    1. Garaulet M., Perez-Llamas F., Fuente T., Zamora S., Tebar F.J. Anthropometric, computed tomography and fat cell data in an obese population: Relationship with insulin, leptin, tumor necrosis factor-alpha, sex hormone-binding globulin and sex hormones. Eur. J. Endocrinol. 2000;143:657–666. doi: 10.1530/eje.0.1430657.
    1. Fröhlich-Zwahlen A., Casartelli N., Item-Glatthorn J., Maffiuletti N. Validity of resting myotonometric assessment of lower extremity muscles in chronic stroke patients with limited hypertonia: A preliminary study. J. Electromyogr. Kinesiol. 2014;24:762–769. doi: 10.1016/j.jelekin.2014.06.007.
    1. Geer E.B., Shen W. Gender differences in insulin resistance, body composition, and energy balance. Gend. Med. 2009;6:60–75. doi: 10.1016/j.genm.2009.02.002.
    1. Kvist H., Chowdhury B., Grangård U., Tylen U., Sjöström L. Total and visceral adipose-tissue volumes derived from measurements with computed tomography in adult men and women: Predictive equations. Am. J. Clin. Nutr. 1988;48:1351–1361. doi: 10.1093/ajcn/48.6.1351.
    1. Bell D.R., Blackburn J.T., Ondrak K.S., Hackney A.C., Hudson J.D., Norcross M.F., Padua D.A. The effects of oral contraceptive use on muscle stiffness across the menstrual cycle. Clin. J. Sport Med. 2011;21:467–473. doi: 10.1097/JSM.0b013e318230f50a.
    1. Bell D.R., Blackburn J.T., Norcorss M.F., Ondrak K.S., Hudson J.D., Hackney A., Padua D.A. Estrogen and muscle stiffness have a negative relationship in females. Knee Surg. Sports Traumatol. Arthrosc. 2012;20:361–367. doi: 10.1007/s00167-011-1577-y.
    1. Maffiuletti N.A., Ratel S., Sartorio A., Martin V. The impact of obesity on in vivo human skeletal muscle function. Curr. Obes. Rep. 2013;2:251–260. doi: 10.1007/s13679-013-0066-7.
    1. Brady A.O., Straight C., Schmidt M., Evans E. Impact of body mass index on the relationship between muscle quality and physical function in older women. J. Nutr. Health Aging. 2014;18:378–382. doi: 10.1007/s12603-013-0421-0.
    1. Mullix J., Warner M., Stokes M. Testing muscle tone and mechanical properties of rectus femoris and biceps femoris using a novel hand held MyotonPRO device: Relative ratios and reliability. Work. Pap. Health Sci. 2012;1:1–8.
    1. Chuang L.L., Wu C.Y., Lin K.C., Lur S.Y. Quantitative mechanical properties of the relaxed biceps and triceps brachii muscles in patients with subacute stroke: A reliability study of the myoton-3 myometer. Stroke Res. Treat. 2012;2012:617694. doi: 10.1155/2012/617694.
    1. Chuang L.L., Lin K.C., Wu C.Y., Chang C.W., Chen H.C., Yin H.P., Wang L. Relative and absolute reliabilities of the myotonometric measurements of hemiparetic arms in patients with stroke. Arch. Phys. Med. Rehabil. 2013;94:459–466. doi: 10.1016/j.apmr.2012.08.212.
    1. Bizzini M., Mannion A.F. Reliability of a new, hand-held device for assessing skeletal muscle stiffness. Clin. Biomech. 2003;18:459–461. doi: 10.1016/S0268-0033(03)00042-1.
    1. Rahemi H., Nigam N., Wakeling J.M. The effect of intramuscular fat on skeletal muscle mechanics: Implications for the elderly and obese. J. R. Soc. Interface. 2015;12:20150365. doi: 10.1098/rsif.2015.0365.
    1. Ryu M., Jo J., Lee Y., Chung Y.S., Kim K.M., Baek W.C. Association of physical activity with sarcopenia and sarcopenic obesity in community-dwelling older adults: The Fourth Korea National Health and Nutrition Examination Survey. Age Ageing. 2013;42:734–740. doi: 10.1093/ageing/aft063.
    1. Garcia-Vicencio S., Coudeyre E., Kluka V., Cardenoux C., Jegu A., Fourot A.V., Ratel S., Martin V. The bigger, the stronger? Insights from muscle architecture and nervous characteristics in obese adolescent girls. Int. J. Obesity. 2016;40:245–251. doi: 10.1038/ijo.2015.158.
    1. Tomlinson D.J., Erskine R., Winwood K., Morse C., Onambélé G. The impact of obesity on skeletal muscle architecture in untrained young vs. old women. J. Anat. 2014;225:675–684. doi: 10.1111/joa.12248.
    1. Maffiuletti N.A., Jubeau M., Agosti F., De Col A., Sartorio A. Quadriceps muscle function characteristics in severely obese and nonobese adolescents. Eur. J. Appl. Physiol. 2008;103:481–484. doi: 10.1007/s00421-008-0737-3.
    1. Barbat-Artigas S., Pion C.H., Leduc-Gaudet J.P., Rolland Y., Aubertin-Leheudre M. Exploring the role of muscle mass, obesity, and age in the relationship between muscle quality and physical function. J. Am. Med. Dir. Assoc. 2014;15:303.e13–303.e20. doi: 10.1016/j.jamda.2013.12.008.
    1. Pruyn E.C., Watsford M.L., Murphy A.J. Validity and reliability of three methods of stiffness assessment. J. Sport Health Sci. 2016;5:476–483. doi: 10.1016/j.jshs.2015.12.001.

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