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Original article| Volume 75, 104772, July 2023

Establishment of regression-based normative isometric strength values for major lower limb muscle groups in persons with multiple sclerosis

  • Heather M. DelMastro
    Correspondence
    Corresponding author.
    Affiliations
    Mandell Center for Multiple Sclerosis, Mount Sinai Rehabilitation Hospital, Trinity Health Of New England, 490 Blue Hills Avenue, Hartford, CT, 06112, United States

    Department of Rehabilitative Medicine, Frank H. Netter MD School of Medicine at Quinnipiac University, 370 Bassett Road, North Haven, CT, 06473, United States
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  • Laura B. Simaitis
    Affiliations
    Department of Physical Therapy, School of Health Sciences at Quinnipiac University, 370 Bassett Road, North Haven, CT, 06473, United States
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  • Elizabeth S. Gromisch
    Affiliations
    Mandell Center for Multiple Sclerosis, Mount Sinai Rehabilitation Hospital, Trinity Health Of New England, 490 Blue Hills Avenue, Hartford, CT, 06112, United States

    Department of Rehabilitative Medicine, Frank H. Netter MD School of Medicine at Quinnipiac University, 370 Bassett Road, North Haven, CT, 06473, United States

    Department of Medical Sciences, Frank H. Netter MD School of Medicine at Quinnipiac University, 370 Bassett Road, North Haven, CT, 06473, United States

    Department of Neurology, University of Connecticut School of Medicine, 263 Farmington Avenue, Farmington, CT, 06030, United States
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  • Author Footnotes
    # at the time of the study
    Kayla Gomes
    Footnotes
    # at the time of the study
    Affiliations
    Mandell Center for Multiple Sclerosis, Mount Sinai Rehabilitation Hospital, Trinity Health Of New England, 490 Blue Hills Avenue, Hartford, CT, 06112, United States

    Rehabilitation Medicine, Department of Veterans Affairs, 555 Willard Avenue, Newington, CT, 06111 United States
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  • Jennifer A. Ruiz
    Affiliations
    Mandell Center for Multiple Sclerosis, Mount Sinai Rehabilitation Hospital, Trinity Health Of New England, 490 Blue Hills Avenue, Hartford, CT, 06112, United States

    Department of Rehabilitative Medicine, Frank H. Netter MD School of Medicine at Quinnipiac University, 370 Bassett Road, North Haven, CT, 06473, United States

    Department of Medical Sciences, Frank H. Netter MD School of Medicine at Quinnipiac University, 370 Bassett Road, North Haven, CT, 06473, United States
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  • Author Footnotes
    # at the time of the study

      Highlights

      • Regression-based norms were provided for lower limb strength in PwMS.
      • 94.9–100% mildly disabled PwMS had ankle dorsiflexion weakness.
      • 98.3% PwMS had weakness in at least one lower limb muscle group.
      • Lower limb weakness was most prevalent in ankle dorsiflexion and hip extension.

      Abstract

      Background

      Limb weakness is a major impairment that affects mobility in persons with multiple sclerosis (PwMS). Specifically, lower limb (LL) weakness can greatly affect gait and balance, while increasing fall risk and decreasing quality of life. Numerous studies have compared LL strength of PwMS to healthy controls, however none have objectively measured strength in all major LL joints (hip, knee, and ankle) in a large number of PwMS. Additionally, while discrete normative values exist for knee extensors in PwMS, there has yet to be regression-based normative isometric strength values for all major LL muscle groups. Therefore, this study aimed to develop gender-specific regression-based normative prediction equations, with 95% confidence intervals, for maximal isometric peak torque of major LL muscles in PwMS. A secondary aim was to characterize the prevalence of LL weakness in PwMS, defined as ≥ 2 SD below values reported for healthy individuals.

      Methods

      A convenience sample of 175 (women: n = 135) PwMS participated in a prospective, cross-sectional study where isometric peak torque of hip flexors, extensors, and abductors, knee flexors and extensors, and ankle plantarflexors and dorsiflexors were measured using the Biodex System 4 Pro-Dynamometer®. Demographics (age, height, and weight) and disease characteristics (disease duration and disability) were collected. Performances were separated for each muscle group into strongest limb and weakest limb. For each gender, regression-based equations were generated for the LL muscle groups by limb with age, height, weight, disability, and disease duration as the covariates. Descriptive statistics were used to examine the frequency of LL weakness by gender and disability level. For comparison purposes, age-stratified (<30, 30–39, 40–49, 50–59, 60–69, >70 years) and disability-stratified (mild, moderate, and severe ambulant) discrete peak torque values were also generated for each gender.

      Results

      Regression-based normative data are presented for men and women, accounting for age, height, weight, disability, and disease duration. Men were significantly stronger (P < 0.001) than women for all LL, with the men's models accounting for a greater percent of muscle strength variation than women's models for all muscle groups, except for hip extension. Disability was inversely related to strength in all of the models. LL weakness was prevalent in hip flexion (m: 47.5%; w: 63.0%) and extension (m: 92.5%; w: 88.1%), knee extension (m: 30.0%; w: 33.3%) and flexion (m: 25.0%; w: 34.8%), and ankle plantarflexion (m: 15.0%; w: 10.4%) and dorsiflexion (m: 100.0%; w: 96.3%). PwMS with mild disability had a high prevalence of ankle dorsiflexion (94.9–100.0%) and hip extension (81.4–90.0%) weakness.

      Conclusions

      This study is the first to provide regression-based normative data of bilateral strength in all major LL muscle groups and clinically useful prevalence data on the occurrence of weakness in these muscles. Of note, PwMS had a high prevalence of ankle dorsiflexion and hip extension weakness even when they were only mildly disabled. These findings can help guide the direction of future interventions and treatments to improve muscle function in PwMS.

      Keywords

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      References

        • Multiple Sclerosis Rehabilitation
        From Impairment to Participation.
        CRC Press, Boca Raton, FL2013
        • ACSM
        ACSM's Guidelines for Exercise Testing and Prescription.
        9th ed. Lippincott Willliams & Williams, Wolters Kluwer2014
        • Andrews J.S.
        • Trupin L.
        • Schmajuk G.
        • Barton J.
        • Margaretten M.
        • Yazdany J.
        • Yelin E.H.
        • Katz P.P.
        Muscle strength, muscle mass, and physical disability in women with systemic lupus erythematosus.
        Arthritis Care Res. (Hoboken). 2015; 67: 120-127
        • Armstrong L.E.
        • Winant D.M.
        • Swasey P.R.
        • Seidle M.E.
        • Carter A.L.
        • Gehlsen G.
        Using isokinetic dynamometry to test ambulatory patients with multiple sclerosis.
        Phys. Ther. 1983; 63: 1274-1279
        • Bertoni R.
        • Lamers I.
        • Chen C.C.
        • Feys P.
        • Cattaneo D.
        Unilateral and bilateral upper limb dysfunction at body functions, activity and participation levels in people with multiple sclerosis.
        Mult. Scler. 2015; 21: 1566-1574
      1. Biodex, Biodex Multi-Joint Sytem-PRO: Setup/Operation Manual. Biodex Medical Systems, Inc., Shirley, New York.

        • Broekmans T.
        • Gijbels D.
        • Eijnde B.O.
        • Alders G.
        • Lamers I.
        • Roelants M.
        • Feys P.
        The relationship between upper leg muscle strength and walking capacity in persons with multiple sclerosis.
        Mult. Scler. 2013; 19: 112-119
        • Broekmans T.
        • Roelants M.
        • Feys P.
        • Alders G.
        • Gijbels D.
        • Hanssen I.
        • Stinissen P.
        • Eijnde B.O.
        Effects of long-term resistance training and simultaneous electro-stimulation on muscle strength and functional mobility in multiple sclerosis.
        Mult. Scler. 2011; 17: 468-477
        • Cagnie B.
        • Cools A.
        • De Loose V.
        • Cambier D.
        • Danneels L.
        Differences in isometric neck muscle strength between healthy controls and women with chronic neck pain: the use of a reliable measurement.
        Arch. Phys. Med. 2007; 88: 1441-1445
        • Cameron M.H.
        • Nilsagard Y.
        Balance, gait, and falls in multiple sclerosis.
        Handb. Clin. Neurol. 2018; 159: 237-250
        • Cameron M.H.
        • Wagner J.M.
        Gait abnormalities in multiple sclerosis: pathogenesis, evaluation, and advances in treatment.
        Curr. Neurol. Neurosci. Rep. 2011; 11: 507-515
        • Checchia G.A.
        • Giannone F.
        • Miccoli B.
        • Cantafora N.
        • Gazzi A.
        Isokinetic testing of muscular function and fatigue in patients with multiple sclerosis.
        Isokinet. Exerc. Sci. 1993; 3: 101-110
        • Chung L.H.
        • Remelius J.G.
        • Van Emmerik R.E.
        • Kent-Braun J.A.
        Leg power asymmetry and postural control in women with multiple sclerosis.
        Med. Sci. Sports. 2008; 40: 1717-1724
        • Citaker S.
        • Guclu-Gunduz A.
        • Yazici G.
        • Bayraktar D.
        • Nazliel B.
        • Irkec C.
        Relationship between lower extremity isometric muscle strength and standing balance in patients with multiple sclerosis.
        NeuroRehabilitation. 2013; 33: 293-298
        • Compston A.
        • McDonald I.
        • Noseworthy J.
        • Lassmann H.
        • Miller D.
        • Smith K.
        • Wekerle H.
        • Confavreux C.
        McAlpine's Multiple Sclerosis.
        4th ed. Churchill Livingstone Elsevier, Philadelphia, PA2005
        • Coote S.
        • Hogan N.
        • Franklin S.
        Falls in people with multiple sclerosis who use a walking aid: prevalence, factors, and effect of strength and balance interventions.
        Arch Phys Med. 2013; 94: 616-621
        • Cruickshank T.M.
        • Reyes A.R.
        • Ziman M.R.
        A systematic review and meta-analysis of strength training in individuals with multiple sclerosis or Parkinson disease.
        Medicine (Baltimore).Medicine (Baltimore). 2015; 94: e411
        • Dalgas U.
        • Stenager E.
        • Jakobsen J.
        • Petersen T.
        • Hansen H.J.
        • Knudsen C.
        • Overgaard K.
        • Ingemann-Hansen T.
        Resistance training improves muscle strength and functional capacity in multiple sclerosis.
        NeurologyNeurology. 2009; 73: 1478-1484
        • Dalgas U.
        • Stenager E.
        • Jakobsen J.
        • Petersen T.
        • Overgaard K.
        • Ingemann-Hansen T.
        Muscle fiber size increases following resistance training in multiple sclerosis.
        Mult. Scler. 2010; 16: 1367-1376
        • Dalgas U.
        • Stenager E.
        • Lund C.
        • Rasmussen C.
        • Petersen T.
        • Sorensen H.
        • Ingemann-Hansen T.
        • Overgaard K.
        Neural drive increases following resistance training in patients with multiple sclerosis.
        J. Neurol. 2013; 260: 1822-1832
        • Davies B.L.
        • Arpin D.J.
        • Volkman K.G.
        • Corr B.
        • Reelfs H.
        • Harbourne R.T.
        • Healey K.
        • Zabad R.
        • Kurz M.J.
        Neurorehabilitation strategies focusing on ankle control improve mobility and posture in persons with multiple sclerosis.
        J. Neurol. Phys. Ther. 2015; 39: 225-232
        • Davies B.L.
        • Hoffman R.M.
        • Healey K.
        • Zabad R.
        • Kurz M.J.
        Errors in the ankle plantarflexor force production are related to the gait deficits of individuals with multiple sclerosis.
        Hum. Mov. Sci. 2017; 51: 91-98
        • Federation
        Atlas of MS.
        3rd ed. 2020
        • Fox R.J.
        • Bacon T.E.
        • Chamot E.
        • Salter A.R.
        • Cutter G.R.
        • Kalina J.T.
        • Kister I.
        Prevalence of multiple sclerosis symptoms across lifespan: data from the NARCOMS Registry.
        Neurodegener. Dis. Manag. 2015; 5 (Suppl): 3-10
        • Gianni C.
        • Prosperini L.
        • Jonsdottir J.
        • Cattaneo D.
        A systematic review of factors associated with accidental falls in people with multiple sclerosis: a meta-analytic approach.
        Clin. Rehabil. 2014; 28: 704-716
        • Green S.B.
        How many subjects does it take to do a regression analysis.
        Multivariate Behav. Res. 1991; 26: 499-510
        • Gross M.T.
        • Brugnolotti J.C.
        Relationship between multiple predictor variables and normal biodex eversion-inversion peak torque and angular work.
        J. Orthop. Sports Phys. Ther. 1992; 15: 24-31
        • Harbo T.
        • Brincks J.
        • Andersen H.
        Maximal isokinetic and isometric muscle strength of major muscle groups related to age, body mass, height, and sex in 178 healthy subjects.
        Eur. J. Appl. Physiol. 2012; 112: 267-275
        • Heesen C.
        • Bohm J.
        • Reich C.
        • Kasper J.
        • Goebel M.
        • Gold S.M.
        Patient perception of bodily functions in multiple sclerosis: gait and visual function are the most valuable.
        Mult. Scler. 2008; 14: 988-991
        • Hoang P.D.
        • Gandevia S.C.
        • Herbert R.D.
        Prevalence of joint contractures and muscle weakness in people with multiple sclerosis.
        Disabil. Rehabil. 2014; 36: 1588-1593
        • Hohol M.J.
        • Orav E.J.
        • Weiner H.L.
        Disease steps in multiple sclerosis: a simple approach to evaluate disease progression.
        Neurology. 1995; 45: 251-255
        • Hohol M.J.
        • Orav E.J.
        • Weiner H.L.
        Disease steps in multiple sclerosis: a longitudinal study comparing disease steps and EDSS to evaluate disease progression.
        Mult. Scler. 1999; 5: 349-354
        • Jeng B.
        • Sandroff B.M.
        • Motl R.W.
        Energetic cost of walking and spasticity in persons with multiple sclerosis with moderate disability.
        NeuroRehabilitation. 2018; 43: 483-489
        • Jorgensen M.
        • Dalgas U.
        • Wens I.
        • Hvid L.G.
        Muscle strength and power in persons with multiple sclerosis - A systematic review and meta-analysis.
        J Neurol Sci. 2017; 376: 225-241
        • Kjolhede T.
        • Vissing K.
        • Dalgas U.
        Multiple sclerosis and progressive resistance training: a systematic review.
        Mult. Scler. 2012; 18: 1215-1228
        • Koushyar H.
        • Nussbaum M.A.
        • Davy K.P.
        • Madigan M.L.
        Relative strength at the hip, knee, and ankle is lower among younger and older females who are obese.
        J. Geriatr. Phys. Ther. 2017; 40: 143-149
        • Lambert C.P.
        • Archer R.L.
        • Evans W.J.
        Muscle strength and fatigue during isokinetic exercise in individuals with multiple sclerosis.
        Med. Sci. Sports. 2001; 33: 1613-1619
        • Larocca N.G.
        Impact of walking impairment in multiple sclerosis: perspectives of patients and care partners.
        Patient. 2011; 4: 189-201
        • Liebensteiner M.C.
        • Krismer M.
        • Koller A.
        • Semenitz B.
        • Mayr E.
        Does minimally invasive total knee arthroplasty improve isokinetic torque?.
        Clin. Orthop. Relat. Res. 2012; 470: 3233-3239
        • Lindle R.S.
        • Metter E.J.
        • Lynch N.A.
        • Fleg J.L.
        • Fozard J.L.
        • Tobin J.
        • Roy T.A.
        • Hurley B.F.
        Age and gender comparisons of muscle strength in 654 women and men aged 20–93 yr.
        J. Appl. Physiol. 1997; 83: 1581-1587
        • Mañago M.M.
        • Callesen J.
        • Dalgas U.
        • Kittelson J.
        • Schenkman M.
        Does disability level impact the relationship of muscle strength to walking performance in people with multiple sclerosis? a cross-sectional analysis.
        Mult. Scler. Relat. Disord. 2020; 42102052
        • Mañago M.M.
        • Hebert J.R.
        • Kittelson J.
        • Schenkman M.
        Contributions of ankle, knee, hip, and trunk muscle function to gait performance in people with multiple sclerosis: a cross-sectional analysis.
        Phys. Ther. 2018; 98: 595-604
        • Manca A.
        • Dvir Z.
        • Deriu F.
        Strength and work parameters in people with multiple sclerosis and in healthy individuals: a responsiveness study of the ankle dorsiflexors.
        Isokinet. Exerc. Sci. 2018; 26: 53-61
        • Manca A.
        • Martinez G.
        • Cereatti A.
        • Della Croce U.
        • Ventura L.
        • Dvir Z.
        • Deriu F.
        Isokinetic predictors of gait speed increase following high-intensity resistance training of the ankle dorsiflexors in people with multiple sclerosis: a pilot study.
        Clin. Biomech. 2019; 67: 102-106
        • Marrie R.A.
        • Goldman M.
        Validity of performance scales for disability assessment in multiple sclerosis.
        Mult. Scler. 2007; 13: 1176-1182
        • Marrie R.A.
        • Whitehouse C.E.
        • Patel R.
        • Figley C.R.
        • Kornelsen J.
        • Bolton J.M.
        • Graff L.A.
        • Mazerolle E.L.
        • Marriott J.J.
        • Bernstein C.N.
        • Fisk J.D.
        Performance of regression-based norms for cognitive functioning of persons with multiple sclerosis in an independent sample.
        Front. Neurol. 2020; 11621010
        • Mazumder R.
        • Murchison C.
        • Bourdette D.
        • Cameron M.
        Falls in people with multiple sclerosis compared with falls in healthy controls.
        PLoS ONE. 2014; 9e107620
        • Motl R.W.
        • McAuley E.
        Pathways between physical activity and quality of life in adults with multiple sclerosis. Health psychology : official journal of the Division of Health Psychology.
        Am. Psychol. Assoc. 2009; 28: 682-689
        • Newsome S.D.
        • Wang J.I.
        • Kang J.Y.
        • Calabresi P.A.
        • Zackowski K.M.
        Quantitative measures detect sensory and motor impairments in multiple sclerosis.
        J Neurol Sci. 2011; 305: 103-111
        • Oosterhuis H.E.
        • van der Ark L.A.
        • Sijtsma K.
        Sample size requirements for traditional and regression-based norms.
        AssessmentAssessment. 2016; 23: 191-202
        • Ozkul C.
        • Eldemir K.
        • Eldemir S.
        • Yildirim M.S.
        • Saygili F.
        • Guclu-Gunduz A.
        • Irkec C.
        Functional performance, leg muscle strength, and core muscle endurance in multiple sclerosis patients with mild disability: a cross-sectional study.
        Motor Control. 2022; 26: 729-747
        • Pisa M.
        • Ruiz J.A.
        • DeLuca G.C.
        • de Andres Crespo M.
        • DelMastro H.M.
        • Olson K.M.
        • Triche E.W.
        • Lo A.C.
        Quantification of upper limb dysfunction in the activities of the daily living in persons with multiple sclerosis.
        Mult. Scler. Relat. Disord. 2022; 63103917
        • Portilla-Cueto K.
        • Medina-Perez C.
        • Romero-Perez E.M.
        • Hernandez-Murua J.A.
        • Oliveira C.E.P.
        • de Souza-Teixeira F.
        • Gonzalez-Bernal J.J.
        • Vila-Cha C.
        • de Paz J.A.
        Reference values for isometric, dynamic, and asymmetry leg extension strength in patients with multiple sclerosis.
        Int. J. Environ. Res. Public Health. 2020; 17
        • Ramari C.
        • Hvid L.G.
        • David A.C.
        • Dalgas U.
        The importance of lower-extremity muscle strength for lower-limb functional capacity in multiple sclerosis: systematic review.
        Ann Phys Rehabil Med. 2020; 63: 123-137
        • Ramari C.
        • Moraes A.G.
        • Tauil C.B.
        • von Glehn F.
        • Motl R.
        • de David A.C.
        Knee flexor strength and balance control impairment may explain declines during prolonged walking in women with mild multiple sclerosis.
        Mult. Scler. Relat. Disord. 2018; 20: 181-185
        • Ramskov D.
        • Pedersen M.B.
        • Kastrup K.
        • Lonbro S.
        • Jacobsen J.S.
        • Thorborg K.
        • Nielsen R.O.
        • Rasmussen S.
        Normative values of eccentric hip abduction strength in novice runners: an equation adjusting for age and gender.
        Int. J. Sports Phys. Ther. 2014; 9: 68-75
        • Schwartz C.E.
        • Vollmer T.
        • Lee H.
        Reliability and validity of two self-report measures of impairment and disability for MS. North American research consortium on multiple sclerosis outcomes study group.
        NeurologyNeurology. 1999; 52: 63-70
        • Scott S.M.
        • Hughes A.R.
        • Galloway S.D.
        • Hunter A.M.
        Surface EMG characteristics of people with multiple sclerosis during static contractions of the knee extensors.
        Clin. Physiol. Funct. Imaging. 2011; 31: 11-17
        • Stevens J.A.
        • Lee R.
        The potential to reduce falls and avert costs by clinically managing fall risk.
        Am. J. Prev. Med. 2018; 55: 290-297
        • Stevens V.
        • Goodman K.
        • Rough K.
        • Kraft G.H.
        Gait impairment and optimizing mobility in multiple sclerosis.
        Phys. Med. Rehabil. Clin. N Am. 2013; 24: 573-592
        • Thoumie P.
        • Lamotte D.
        • Cantalloube S.
        • Faucher M.
        • Amarenco G.
        Motor determinants of gait in 100 ambulatory patients with multiple sclerosis.
        Mult. Scler. 2005; 11: 485-491
        • Versteegh T.
        • Beaudet D.
        • Greenbaum M.
        • Hellyer L.
        • Tritton A.
        • Walton D.
        Evaluating the reliability of a novel neck-strength assessment protocol for healthy adults using self-generated resistance with a hand-held dynamometer.
        Physiother. Can. 2015; 67: 58-64
        • Wagner J.M.
        • Kremer T.R.
        • Van Dillen L.R.
        • Naismith R.T.
        Plantarflexor weakness negatively impacts walking in persons with multiple sclerosis more than plantarflexor spasticity.
        Arch. Phys. Med. 2014; 95: 1358-1365
        • Wens I.
        • Dalgas U.
        • Vandenabeele F.
        • Krekels M.
        • Grevendonk L.
        • Eijnde B.O.
        Multiple sclerosis affects skeletal muscle characteristics.
        PLoS ONE. 2014; 9e108158
        • White L.J.
        • McCoy S.C.
        • Castellano V.
        • Gutierrez G.
        • Stevens J.E.
        • Walter G.A.
        • Vandenborne K.
        Resistance training improves strength and functional capacity in persons with multiple sclerosis.
        Mult. Scler. 2004; 10: 668-674
        • Wiggin M.
        • Wilkinson K.
        • Habetz S.
        • Chorley J.
        • Watson M.
        Percentile values of isokinetic peak torque in children six through thirteen years old.
        Pediatr. Phys. Ther. 2006; 18: 3-18
        • Yang F.
        • Qiao M.
        • Su X.
        • Lazarus J.
        Relative importance of physical and psychological factors to slowness in people with mild to moderate multiple sclerosis.
        Mult. Scler. Relat. Disord. 2019; 27: 81-90