People with hip osteoarthritis have reduced quadriceps voluntary activation and altered motor cortex function

Abstract

Aims: Compare quadriceps voluntary activation, corticospinal and intracortical excitability between people with and without hip osteoarthritis (OA). Exploratory objectives include quantifying the association of corticospinal/intracortical excitability with voluntary activation, corticospinal/intracortical excitability with hip related pain, and motor threshold with motor cortex inhibition and facilitation.

Methods: Case-control study including participants with clinically and radiologically confirmed hip OA and non-OA controls. Quadriceps voluntary activation was assessed using twitch interpolation via femoral nerve stimulation. Single- and paired-pulse transcranial magnetic stimulation over the motor cortex assessed resting motor threshold (RMT), active motor threshold (AMT), short-interval intracortical inhibition (SICI), intracortical facilitation (ICF) and silent period. Generalized linear models assessed outcomes (p < 0.05).

Results: We included 17 hip OA (76% female) and 24 controls (92% female) with a mean (standard deviation) age of 58.7 (7.9) years. Compared to controls, people with hip OA had reduced quadriceps voluntary activation (β= -5.29, 95% confidence intervals [CI], -0.79——-9.79) and increased ICF (β= 0.22, 95%CI, 0.01-0.43). People with hip OA did not differ from controls in RMT (β= 4.76, 95%CI, 14.08-4.56), AMT (β= 2.13, 95%CI, 7.12-2.86), SICI (β= 0.02, 95%CI, 0.15-0.006) or silent period (β= 8.72, 95%CI, 24.75-42.20). More facilitation was associated with increased hip pain (β= 24.55, 95%CI, 6.93-42.18), and more inhibition was associated with less voluntary activation (β= 10.50, 95%CI, 2.00-18.99).

Conclusion: People with hip OA demonstrate reduced quadriceps voluntary activation and complex changes in motor cortex excitability compared to controls. These findings suggest that hip OA can alter quadriceps neuromuscular function (facilitation associated with pain, inhibition associated with activation), thus having implications for rehabilitation.

Keywords

Muscle inhibition / Rehabilitation / Arthritis / Hip pain / Physiotherapy

Ethical approval statement

This research was reviewed and received approval by the Edith Cowan University Human Research Ethics Committee (2023-04080-MURPHY). The research was implemented in accordance with the Declaration of Helsinki. All participants provided informed, electronic consent.

CRediT authorship contribution statement

Myles C. Murphy: Writing - review & editing, Writing - original draft, Supervision, Project administration, Methodology, Funding acquisition, Formal analysis, Data curation, Conceptualization. Molly Coventry: Writing - review & editing, Formal analysis, Data curation. Janet L. Taylor: Writing - review & editing, Supervision, Methodology, Funding acquisition, Data curation, Conceptualization. Ebonie K. Rio: Writing - review & editing, Methodology. Andrea B. Mosler: Writing -review & editing. Jackie L. Whittaker: Writing - review & editing. Christopher Latella: Writing - review & editing, Supervision, Data curation.

Declaration of competing interest

None declared.

Acknowledgement Statement

The authors would like to acknowledge the Edith Cowan University Early-Mid Career Researcher Grant Scheme (G1006474), which sup-ported this research.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.smhs.2024.09.005.

References

[1] Ackerman IN, Buchbinder R, March L. Global burden of disease study 2019: an opportunity to understand the growing prevalence and impact of hip, knee, hand and other osteoarthritis in Australia. Intern Med J. 2023; 53(10):1875-1882. https://doi.org/10.1111/imj.15933.

[2] Australian Institute of Health and Welfare. Osteoarthritis. Canberra: AIHW; 2020. https://www.aihw.gov.au/reports/chronic-musculoskeletal-conditions/osteoarthritis. Accessed May 23, 2023.

[3] Ackerman IN, Bohensky MA, Zomer E, et al. The projected burden of primary total knee and hip replacement for osteoarthritis in Australia to the year 2030. BMC Muscoskel Disord. 2019; 20(1):90. https://doi.org/10.1186/s12891-019-2411-9.

[4] Murphy MC, Latella C, Rio EK, et al. Does lower-limb osteoarthritis alter motor cortex descending drive and voluntary activation? A systematic review and meta-analysis. EFORT Open Rev. 2023; 8(12):883-894. https://doi.org/10.1530/eor-23-0092.

[5] Pietrosimone BG, Saliba SA. Changes in voluntary quadriceps activation predict changes in quadriceps strength after therapeutic exercise in patients with knee osteoarthritis. Knee. 2012; 19(6):939-943. https://doi.org/10.1016/j.knee.2012.03.002.

[6] Simis M, Imamura M, de Melo PS, et al. Increased motor cortex inhibition as a marker of compensation to chronic pain in knee osteoarthritis. Sci Rep. 2021; 11(1):24011. https://doi.org/10.1038/s41598-021-03281-0.

[7] Luc-Harkey BA, Harkey MS, Pamukoff DN, et al. Greater intracortical inhibition associates with lower quadriceps voluntary activation in individuals with ACL reconstruction. Exp Brain Res. 2017; 235(4):1129-1137. https://doi.org/10.1007/s00221-017-4877-8.

[8] Schabrun SM, Hodges PW. Muscle pain differentially modulates short interval intracortical inhibition and intracortical facilitation in primary motor cortex. J Pain. 2012; 13(2):187-194. https://doi.org/10.1016/j.jpain.2011.10.013.

[9] Kittelson AJ, Thomas AC, Kluger BM, Stevens-Lapsley JE. Corticospinal and intracortical excitability of the quadriceps in patients with knee osteoarthritis. Exp Brain Res. 2014; 232(12):3991-3999. https://doi.org/10.1007/s00221-014-4079-6.

[10] Tarragó M, Deitos A, Brietzke AP, et al. Descending control of nociceptive processing in knee osteoarthritis is associated with intracortical disinhibition: an exploratory study. Medicine (Baltim). 2016; 95(17):e3353. https://doi.org/10.1097/md.0000000000003353.

[11] Lisee C, Lepley AS, Birchmeier T, O'Hagan K, Kuenze C. Quadriceps strength and volitional activation after anterior cruciate ligament reconstruction: a systematic review and meta-analysis. Sport Health. 2019; 11(2):163-179. https://doi.org/10.1177/1941738118822739.

[12] Culvenor AG, Collins NJ, Guermazi A, et al. Early patellofemoral osteoarthritis features one year after anterior cruciate ligament reconstruction: symptoms and quality of life at three years. Arthritis Care Res. 2016; 68(6):784-792. https://doi.org/10.1002/acr.22761.

[13] Patterson B, Culvenor AG, Barton CJ, et al. Poor functional performance 1 year after ACL reconstruction increases the risk of early osteoarthritis progression. Br J Sports Med. 2020; 54(9):546-553. https://doi.org/10.1136/bjsports-2019-101503.

[14] Murphy MC, Rio E, Whife C, Latella C. Maximising neuromuscular performance in people with pain and injury: moving beyond reps and sets to understand the challenges and embrace the complexity. BMJ Open Sport Exerc Med. 2024; 10(2): e001935. https://doi.org/10.1136/bmjsem-2024-001935.

[15] von Elm E, Altman DG, Egger M, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008; 61(4):344-349. https://doi.org/10.1016/j.jclinepi.2007.11.008.

[16] Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Screening questionnaire before TMS: an update. Clin Neurophysiol. 2011; 122(8):1686. https://doi.org/10.1016/j.clinph.2010.12.037.

[17] Impellizzeri FM, Jones DM, Griffin D, et al. Patient-reported outcome measures for hip-related pain: a review of the available evidence and a consensus statement from the international hip-related pain research network, Zurich 2018. Br J Sports Med. 2020; 54(14):848-857. https://doi.org/10.1136/bjsports-2019-101456.

[18] Thorborg K, Tijssen M, Habets B, et al. Patient-reported outcome (PRO) questionnaires for young to middle-aged adults with hip and groin disability: a systematic review of the clinimetric evidence. Br J Sports Med. 2015; 49(12):812. https://doi.org/10.1136/bjsports-2014-094224.

[19] Reijman M, Hazes JM, Pols HA, Bernsen RM, Koes BW, Bierma-Zeinstra SM. Validity and reliability of three definitions of hip osteoarthritis: cross sectional and longitudinal approach. Ann Rheum Dis. 2004; 63(11):1427-1433. https://doi.org/10.1136/ard.2003.016477.

[20] Nuzzo JL, Taylor JL, Gandevia SC. CORP: measurement of upper and lower limb muscle strength and voluntary activation. J Appl Physiol. 2019; 126(3):513-543. https://doi.org/10.1152/japplphysiol.00569.2018.

[21] Kean CO, Birmingham TB, Garland SJ, Bryant DM, Giffin JR. Minimal detectable change in quadriceps strength and voluntary muscle activation in patients with knee osteoarthritis. Arch Phys Med Rehabil. 2010; 91(9):1447-1451. https://doi.org/10.1016/j.apmr.2010.06.002.

[22] Skou ST, Grønne DT, Roos EM. Prevalence, severity, and correlates of pain flares in response to a repeated sit-to-stand activity: a cross-sectional study of 14 902 patients with knee and hip osteoarthritis in primary care. J Orthop Sports Phys Ther. 2020; 50(6):309-318. https://doi.org/10.2519/jospt.2019.9125.

[23] Alghadir AH, Anwer S, Iqbal A, Iqbal ZA. Test-retest reliability, validity, and minimum detectable change of visual analog, numerical rating, and verbal rating scales for measurement of osteoarthritic knee pain. J Pain Res. 2018; 11:851-856. https://doi.org/10.2147/jpr.S158847.

[24] Kuorinka I, Jonsson B, Kilbom A, et al. Standardised Nordic questionnaires for the analysis of musculoskeletal symptoms. Appl Ergon. 1987; 18(3):233-237. https://doi.org/10.1016/0003-6870(87)90010-x.

[25] Sutton VR, Chivers PT, Hart NH, et al. Persistent disability from preacademy injuries impairs physical performance in police force recruits: a cross-sectional study. JOSPT Open. 2024; 2(2):141-147. https://doi.org/10.2519/josptopen.2024.1025.

[26] Spitzer RL, Kroenke K, Williams JB, Löwe B.A brief measure for assessing generalized anxiety disorder: the GAD-7. Arch Intern Med. 2006; 166(10):1092-1097. https://doi.org/10.1001/archinte.166.10.1092.

[27] Kroenke K, Spitzer RL, Williams JB.The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med. 2001; 16(9):606-613. https://doi.org/10.1046/j.1525-1497.2001.016009606.x.

[28] Sinclair SJ, Siefert CJ, Slavin-Mulford JM, Stein MB, Renna M, Blais MA. Psychometric evaluation and normative data for the depression, anxiety, and stress scales-21 (DASS-21) in a nonclinical sample of U.S. adults. Eval Health Prof. 2012; 35(3):259-279. https://doi.org/10.1177/0163278711424282.

[29] Tang WT, Hsu MJ, Huang YM, Hsu YT, Chuang LL, Chang YJ. Low-intensity electrical stimulation to improve the neurological aspect of weakness in individuals with chronic anterior cruciate ligament lesion. BioMed Res Int. 2020;2020:7436274. https://doi.org/10.1155/2020/7436274.

[30] Schabrun SM, Christensen SW, Mrachacz-Kersting N, Graven-Nielsen T. Motor cortex reorganization and impaired function in the transition to sustained muscle pain. Cerebr Cortex. 2016; 26(5):1878-1890. https://doi.org/10.1093/cercor/bhu319.

[31] Chang WJ, O'Connell NE, Beckenkamp PR, Alhassani G, Liston MB, Schabrun SM. Altered primary motor cortex structure, organization, and function in chronic pain: a systematic review and meta-analysis. J Pain. 2018; 19(4):341-359. https://doi.org/10.1016/j.jpain.2017.10.007.

[32] O'Bryan SJ, Taylor JL, D'Amico JM, Rouffet DM. Quadriceps muscle fatigue reduces extension and flexion power during maximal cycling. Front Sports Act Living. 2021;3: 797288. https://doi.org/10.3389/fspor.2021.797288.

[33] Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000; 10(5):361-374. https://doi.org/10.1016/s1050-6411(00)00027-4.