Portable fixed dynamometry: towards remote muscle strength measurements in patients with motor neuron disease

Jaap N E Bakers, Leonard H van den Berg, Toju G Ajeks, Maxine J Holleman, Jill Verhoeven, Anita Beelen, Johanna M A Visser-Meily, Ruben P A van Eijk, Jaap N E Bakers, Leonard H van den Berg, Toju G Ajeks, Maxine J Holleman, Jill Verhoeven, Anita Beelen, Johanna M A Visser-Meily, Ruben P A van Eijk

Abstract

Background: We aimed to determine (1) the test-retest reliability of a newly developed portable fixed dynamometer (PFD) as compared to the hand-held dynamometer (HHD) in patients with motor neuron disease (MND) and (2) the PFD's ability to reduce possible examiner-induced ceiling effects.

Methods: Test-retest reliability of isometric muscle strength of the quadriceps was measured in patients with MND and non-neurological controls using the HHD and PFD. Reliability was estimated by the intraclass correlation coefficient (ICC) and standard error of measurement (SEM) using linear mixed effects models, and the Bland-Altman method of agreement.

Results: In total, 45 patients with MND and 43 healthy controls were enrolled in this study. The ICC of the PFD was excellent and similar in both patients and controls (ICC Patients 99.5% vs. ICC Controls 98.6%) with a SEM of 6.2%. A strong examiner-induced ceiling effect in HHD was found when the participant's strength exceeded that of examiner. Employing the PFD increased the range of muscle strength measurements across individuals nearly twofold from 414 to 783 N.

Conclusions: Portable fixed dynamometry may significantly reduce examiner-induced ceiling effects, optimize the standardization of muscle strength testing, and maximize reliability. Ultimately, PFD may improve the delivery of care due to its potential for unsupervised, home-based assessments and reduce the burden to the patient of participating in clinical trials for MND or other neuromuscular diseases.

Keywords: Fixed dynamometry; Motor neuron disease; Muscle strength; Reliability study; Remote monitoring.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Overview of study procedures
Fig. 2
Fig. 2
Prototype of the Portable Fixed Dynamometer. A rigid framework with two holders for the MicroFET dynamometers (*) was created to remove the need for an examiner when evaluating quadriceps strength. With the vertical arm (a), the height was adjusted to prevent the feet from touching the ground. The diagonal arm (b) enabled adjustment of the dynamometer pad to 1 centimeter proximal to the midline between the malleoli
Fig. 3
Fig. 3
Bland–Altman plots for test–retest reliability. Bland–Altman plots of the HHD (a–b) and PFD (cd) for non-neurological controls and patients with MND, respectively. Due to the heteroscedastic nature of the data, we applied a 10log-transformation. MD mean difference between trials 1 and 2, ICC intraclass correlation coefficient, SEM standard error of measurement, expressed as percentage of the mean on the original scale (Newton) [35]
Fig. 4
Fig. 4
Association between hand-held and portable fixed dynamometry. a Association between HHD and PFD measurements. The dotted line represents a correlation of 1 (i.e., HHD measurement = PFD measurement and vice-versa). The black solid line represents the observed association, estimated using a linear mixed effects model. The dots with crosses are data points classified as unable-to-break. b Muscle strength based on hand-held dynamometry data was categorized and per sub-group we determined the proportion unable-to-break A clear pattern emerges with the assessor no longer being able to measure the full muscle strength from 300 N upwards (i.e., a proportion of unable-to-break of 1)
Fig. 5
Fig. 5
Relationship between functional loss and muscle strength measurements. Boxplot of the HHD and PFD measurements in 45 patients with MND and 43 non-neurological controls (blue). Functional loss in MND patients was categorized using self-reported function scores of the ALS functional rating scale item 8 (walking); the score range was 0 to 4, where 0 indicates no leg muscle function (not included) and 4 indicates normal walking function

References

    1. National institute for health and care excellence: clinical guidelines; motor neurone disease: assessment and management (2016). In. national institute for health and care excellence: clinical guidelines. The National Institute of Health and Care Excellence (NICE), London.
    1. Cudkowicz M, Qureshi M, Shefner J. Measures and markers in amyotrophic lateral sclerosis. NeuroRx. 2004;1(2):273–283. doi: 10.1602/neurorx.1.2.273.
    1. Paganoni S, Cudkowicz M, Berry JD. Outcome measures in amyotrophic lateral sclerosis clinical trials. Clin Investig (Lond) 2014;4(7):605–618. doi: 10.4155/cli.14.52.
    1. Rutkove SB. Clinical measures of disease progression in amyotrophic lateral sclerosis. Neurotherapeutics. 2015;12(2):384–393. doi: 10.1007/s13311-014-0331-9.
    1. Cudkowicz ME, Titus S, Kearney M, Yu H, Sherman A, Schoenfeld D, Hayden D, Shui A, Brooks B, Conwit R, Felsenstein D, Greenblatt DJ, Keroack M, Kissel JT, Miller R, Rosenfeld J, Rothstein JD, Simpson E, Tolkoff-Rubin N, Zinman L, Shefner JM, Ceftriaxone Study I Safety and efficacy of ceftriaxone for amyotrophic lateral sclerosis: a multi-stage, randomised, double-blind, placebo-controlled trial. Lancet Neurol. 2014;13(11):1083–1091. doi: 10.1016/S1474-4422(14)70222-4.
    1. Cudkowicz ME, van den Berg LH, Shefner JM, Mitsumoto H, Mora JS, Ludolph A, Hardiman O, Bozik ME, Ingersoll EW, Archibald D, Meyers AL, Dong Y, Farwell WR, Kerr DA, investigators E Dexpramipexole versus placebo for patients with amyotrophic lateral sclerosis (EMPOWER): a randomised, double-blind, phase 3 trial. Lancet Neurol. 2013;12(11):1059–1067. doi: 10.1016/S1474-4422(13)70221-7.
    1. Meininger V, Genge A, van den Berg LH, Robberecht W, Ludolph A, Chio A, Kim SH, Leigh PN, Kiernan MC, Shefner JM, Desnuelle C, Morrison KE, Petri S, Boswell D, Temple J, Mohindra R, Davies M, Bullman J, Rees P, Lavrov A, Group NOGS Safety and efficacy of ozanezumab in patients with amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol. 2017;16(3):208–216. doi: 10.1016/S1474-4422(16)30399-4.
    1. Kolber MJ, Cleland JA. Strength testing using hand-held dynamometry. Phys Therapy Rev. 2005;10(2):99–112. doi: 10.1179/108331905X55730.
    1. Stark T, Walker B, Phillips JK, Fejer R, Beck R. Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: a systematic review. PM R J Injury Funct Rehabilit. 2011;3(5):472–479. doi: 10.1016/j.pmrj.2010.10.025.
    1. Keating JL, Matyas TA. The influence of subject and test design on dynamometric measurements of extremity muscles. Phys Ther. 1996;76(8):866–889. doi: 10.1093/ptj/76.8.866a.
    1. Lu TW, Hsu HC, Chang LY, Chen HL. Enhancing the examiner's resisting force improves the reliability of manual muscle strength measurements: comparison of a new device with hand-held dynamometry. J Rehabil Med. 2007;39(9):679–684. doi: 10.2340/16501977-0107.
    1. Wikholm JB, Bohannon RW. Hand-held dynamometer measurements: tester strength makes a difference. J Orthop Sports Phys Ther. 1991;13(4):191–198. doi: 10.2519/jospt.1991.13.4.191.
    1. Lu TW, Chien HL, Chang LY, Hsu HC. Enhancing the examiner's resisting force improves the validity of manual muscle strength measurements: application to knee extensors and flexors. J Strength Cond Res. 2012;26(9):2364–2371. doi: 10.1519/JSC.0b013e31823db080.
    1. Beck M, Giess R, Wurffel W, Magnus T, Ochs G, Toyka KV. Comparison of maximal voluntary isometric contraction and Drachman's hand-held dynamometry in evaluating patients with amyotrophic lateral sclerosis. Muscle Nerve. 1999;22(9):1265–1270. doi: 10.1002/(SICI)1097-4598(199909)22:9<1265::AID-MUS15>;2-F.
    1. Visser J, Mans E, de Visser M, van den Berg-Vos RM, Franssen H, de Jong JM, van den Berg LH, Wokke JH, de Haan RJ. Comparison of maximal voluntary isometric contraction and hand-held dynamometry in measuring muscle strength of patients with progressive lower motor neuron syndrome. Neuromuscul Disord. 2003;13(9):744–750. doi: 10.1016/S0960-8966(03)00135-4.
    1. Andres PL, Skerry LM, Munsat TL, Thornell BJ, Szymonifka J, Schoenfeld DA, Cudkowicz ME. Validation of a new strength measurement device for amyotrophic lateral sclerosis clinical trials. Muscle Nerve. 2012;45(1):81–85. doi: 10.1002/mus.22253.
    1. Bui KL, Mathur S, Dechman G, Maltais F, Camp P, Saey D. Fixed handheld dynamometry provides reliable and valid values for quadriceps isometric strength in people with chronic obstructive pulmonary disease: a multicenter study. Phys Ther. 2019 doi: 10.1093/ptj/pzz059.
    1. Kollock RO, Jr, Onate JA, Van Lunen B. The reliability of portable fixed dynamometry during hip and knee strength assessments. J Athl Train. 2010;45(4):349–356. doi: 10.4085/1062-6050-45.4.349.
    1. Mentiplay BF, Perraton LG, Bower KJ, Adair B, Pua YH, Williams GP, McGaw R, Clark RA. Assessment of lower limb muscle strength and power using hand-held and fixed dynamometry: a reliability and validity study. PLoS ONE. 2015;10(10):e0140822. doi: 10.1371/journal.pone.0140822.
    1. Andres PL, Allred MP, Stephens HE, Proffitt Bunnell M, Siener C, Macklin EA, Haines T, English RA, Fetterman KA, Kasarskis EJ, Florence J, Simmons Z, Cudkowicz ME. Fixed dynamometry is more sensitive than vital capacity or ALS rating scale. Muscle Nerve. 2017;56(4):710–715. doi: 10.1002/mus.25586.
    1. Martin HJ, Yule V, Syddall HE, Dennison EM, Cooper C, Aihie Sayer A. Is hand-held dynamometry useful for the measurement of quadriceps strength in older people? A comparison with the gold standard Bodex dynamometry. Gerontology. 2006;52(3):154–159. doi: 10.1159/000091824.
    1. Toonstra J, Mattacola CG. Test-retest reliability and validity of isometric knee-flexion and -extension measurement using 3 methods of assessing muscle strength. J Sport Rehabil. 2013;22:1. doi: 10.1123/jsr.2013.TR7.
    1. Sarabon N, Kozinc Z, Bishop C, Maffiuletti NA. Factors influencing bilateral deficit and inter-limb asymmetry of maximal and explosive strength: motor task, outcome measure and muscle group. Eur J Appl Physiol. 2020;120(7):1681–1688. doi: 10.1007/s00421-020-04399-1.
    1. Sarabon N, Rosker J, Fruhmann H, Burggraf S, Loefler S, Kern H. Reliability of maximal voluntary contraction related parameters measured by a novel portable isometric knee dynamometer. Phys Med Rehabilit Kurortmed. 2013;23(01):22–27. doi: 10.1055/s-0032-1331190.
    1. Helleman J, Van Eenennaam R, Kruitwagen ET, Kruithof WJ, Slappendel MJ, Van Den Berg LH, Visser-Meily JMA. Beelen A (2020) Telehealth as part of specialized ALS care: feasibility and user experiences with ALS home-monitoring and coaching. Amyotroph Lateral Scler Frontotemporal Degener. 2020 doi: 10.1080/216784211718712.
    1. Hobson EV, Baird WO, Bradburn M, Cooper C, Mawson S, Quinn A, Shaw PJ, Walsh T, McDermott CJ. Using telehealth in motor neuron disease to increase access to specialist multidisciplinary care: a UK-based pilot and feasibility study. BMJ Open. 2019;9(10):e028525. doi: 10.1136/bmjopen-2018-028525.
    1. Rutkove SB, Qi K, Shelton K, Liss J, Berisha V, Shefner JM. ALS longitudinal studies with frequent data collection at home: study design and baseline data. Amyotroph Lateral Scler Frontotemporal Degener. 2019;20(1–2):61–67. doi: 10.1080/21678421.2018.1541095.
    1. van Eijk RPA, Bakers JNE, Bunte TM, de Fockert AJ, Eijkemans MJC, van den Berg LH. Accelerometry for remote monitoring of physical activity in amyotrophic lateral sclerosis: a longitudinal cohort study. J Neurol. 2019;266(10):2387–2395. doi: 10.1007/s00415-019-09427-5.
    1. Rushton DJ, Andres PL, Allred P, Baloh RH, Svendsen CN. Patients with ALS show highly correlated progression rates in left and right limb muscles. Neurology. 2017;89(2):196–206. doi: 10.1212/WNL.0000000000004105.
    1. Shields RK, Ruhland JL, Ross MA, Saehler MM, Smith KB, Heffner ML. Analysis of health-related quality of life and muscle impairment in individuals with amyotrophic lateral sclerosis using the medical outcome survey and the Tufts Quantitative Neuromuscular Exam. Arch Phys Med Rehabil. 1998;79(7):855–862. doi: 10.1016/s0003-9993(98)90370-7.
    1. Shefner JM, Liu D, Leitner ML, Schoenfeld D, Johns DR, Ferguson T, Cudkowicz M. Quantitative strength testing in ALS clinical trials. Neurology. 2016;87(6):617–624. doi: 10.1212/WNL.0000000000002941.
    1. van Es MA, Hardiman O, Chio A, Al-Chalabi A, Pasterkamp RJ, Veldink JH, van den Berg LH. Amyotrophic lateral sclerosis. Lancet. 2017;390(10107):2084–2098. doi: 10.1016/S0140-6736(17)31287-4.
    1. van der Ploeg RJ, Oosterhuis HJ. The "make/break test" as a diagnostic tool in functional weakness. J Neurol Neurosurg Psychiatry. 1991;54(3):248–251. doi: 10.1136/jnnp.54.3.248.
    1. Ludbrook J. Confidence in Altman-Bland plots: a critical review of the method of differences. Clin Exp Pharmacol Physiol. 2010;37(2):143–149. doi: 10.1111/j.1440-1681.2009.05288.x.
    1. Euser AM, Dekker FW, le Cessie S. A practical approach to Bland-Altman plots and variation coefficients for log transformed variables. J Clin Epidemiol. 2008;61(10):978–982. doi: 10.1016/j.jclinepi.2007.11.003.
    1. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):48. 10.18637/jss.v067.i01
    1. Hogrel JY, Benveniste O, Bachasson D. Routine monitoring of isometric knee extension strength in patients with muscle impairments using a new portable device: cross-validation against a standard isokinetic dynamometer. Physiol Meas. 2020;41(1):015003. doi: 10.1088/1361-6579/ab6b49.
    1. Roussel MP, Hebert LJ, Duchesne E. Intra-rater reliability and concurrent validity of quantified muscle testing for maximal knee extensors strength in men with myotonic dystrophy type 1. J Neuromuscul Dis. 2019;6(2):233–240. doi: 10.3233/JND-190388.
    1. Andres PL, Hedlund W, Finison L, Conlon T, Felmus M, Munsat TL. Quantitative motor assessment in amyotrophic lateral sclerosis. Neurology. 1986;36(7):937–941. doi: 10.1212/wnl.36.7.937.
    1. Jackson SM, Cheng MS, Smith AR, Jr, Kolber MJ. Intrarater reliability of hand held dynamometry in measuring lower extremity isometric strength using a portable stabilization device. Musculoskelet Sci Pract. 2017;27:137–141. doi: 10.1016/j.math.2016.07.010.
    1. Koblbauer IF, Lambrecht Y, van der Hulst ML, Neeter C, Engelbert RH, Poolman RW, Scholtes VA. Reliability of maximal isometric knee strength testing with modified hand-held dynamometry in patients awaiting total knee arthroplasty: useful in research and individual patient settings? A reliability study. BMC Musculoskelet Disord. 2011;12:249. doi: 10.1186/1471-2474-12-249.
    1. Kolber MJ, Beekhuizen K, Cheng MS, Fiebert IM. The reliability of hand-held dynamometry in measuring isometric strength of the shoulder internal and external rotator musculature using a stabilization device. Physiother Theory Pract. 2007;23(2):119–124. doi: 10.1080/09593980701213032.
    1. Shin S, Lee K, Song C. Relationship of body composition, knee extensor strength, and standing balance to lumbar bone mineral density in postmenopausal females. J Phys Ther Sci. 2016;28(7):2105–2109. doi: 10.1589/jpts.28.2105.
    1. Thorborg K, Bandholm T, Holmich P. Hip- and knee-strength assessments using a hand-held dynamometer with external belt-fixation are inter-tester reliable. Knee Surg Sports Traumatol Arthrosc. 2013;21(3):550–555. doi: 10.1007/s00167-012-2115-2.
    1. Hansen EM, McCartney CN, Sweeney RS, Palimenio MR, Grindstaff TL. Hand-held dynamometer positioning impacts discomfort during quadriceps strength testing: a validity and reliability study. Int J Sports Phys Ther. 2015;10(1):62–68.
    1. Bohannon RW. Hand-held compared with isokinetic dynamometry for measurement of static knee extension torque (parallel reliability of dynamometers) Clin Phys Physiol Meas. 1990;11(3):217–222. doi: 10.1088/0143-0815/11/3/004.
    1. Reed RL, Den Hartog R, Yochum K, Pearlmutter L, Ruttinger AC, Mooradian AD. A comparison of hand-held isometric strength measurement with isokinetic muscle strength measurement in the elderly. J Am Geriatr Soc. 1993;41(1):53–56. doi: 10.1111/j.1532-5415.1993.tb05949.x.
    1. Kimura F, Fujimura C, Ishida S, Nakajima H, Furutama D, Uehara H, Shinoda K, Sugino M, Hanafusa T. Progression rate of ALSFRS-R at time of diagnosis predicts survival time in ALS. Neurology. 2006;66(2):265–267. doi: 10.1212/01.wnl.0000194316.91908.8a.
    1. Westeneng HJ, Debray TPA, Visser AE, van Eijk RPA, Rooney JPK, Calvo A, Martin S, McDermott CJ, Thompson AG, Pinto S, Kobeleva X, Rosenbohm A, Stubendorff B, Sommer H, Middelkoop BM, Dekker AM, van Vugt J, van Rheenen W, Vajda A, Heverin M, Kazoka M, Hollinger H, Gromicho M, Korner S, Ringer TM, Rodiger A, Gunkel A, Shaw CE, Bredenoord AL, van Es MA, Corcia P, Couratier P, Weber M, Grosskreutz J, Ludolph AC, Petri S, de Carvalho M, Van Damme P, Talbot K, Turner MR, Shaw PJ, Al-Chalabi A, Chio A, Hardiman O, Moons KGM, Veldink JH, van den Berg LH. Prognosis for patients with amyotrophic lateral sclerosis: development and validation of a personalised prediction model. Lancet Neurol. 2018;17(5):423–433. doi: 10.1016/S1474-4422(18)30089-9.

Source: PubMed

3
Tilaa