Abstract
Purpose
Patellofemoral pain syndrome (PFPS) is twice as prevalent in females as males, yet a few studies have evaluated differences in quadriceps muscle control between sexes or across force levels. This study investigated sex differences in quadriceps EMG onset times and amplitude at different force levels during isometric knee extension in asymptomatic males and females and in females with PFPS.
Methods
Thirteen healthy males, 12 healthy females, and 10 females with PFPS performed isometric knee extension ramp contractions at 25%, 50%, and 75% of maximal voluntary contraction (MVC). Surface EMG was recorded from the vastus lateralis (VL), vastus medialis oblique (VMO), vastus medialis (VM), and rectus femoris (RF).
Results
Healthy females showed delayed VL (222 ± 67 ms, p = 0.002), VMO (357 ± 101 ms, p = 0.001), and VM (258 ± 62 ms, p < 0.001) recruitment in comparison with healthy males. Healthy males activated the VL earlier than the VM (156 ± 51 ms, p = 0.02) and RF (379 ± 74 ms, p < 0.001), and at a similar time as the VMO; healthy females activated the VL earlier than the VM (192 ± 53 ms, p = 0.004) and VMO (239 ± 73 ms, p = 0.01). A lower VMO:VL activation ratio was found at 25% MVC (p < 0.001) than at higher force levels.
Conclusions
Delayed activation of the VMO relative to the VL has been proposed as a risk factor for PFPS. This study confirms a delay in VMO onset time in females.
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Abbreviations
- ANOVA:
-
Analysis of variance
- EMG:
-
Electromyography
- ICC:
-
Intraclass correlation coefficient
- MVC:
-
Maximal voluntary contraction
- PFPS:
-
Patellofemoral pain syndrome
- RF:
-
Rectus femoris
- RMS:
-
Root mean square
- VAS:
-
Visual analog scale
- VL:
-
Vastus lateralis
- VM:
-
Vastus medialis
- VMO:
-
Vastus medialis oblique
References
Aminaka N, Pietrosimone BG, Armstrong CW, Meszaros A, Gribble PA (2011) Patellofemoral pain syndrome alters neuromuscular control and kinetics during stair ambulation. J Electromyogr Kinesiol 21(4):645–651. https://doi.org/10.1016/j.jelekin.2011.03.007
Baur H, Hirschmüller A, Cassel M, Müller S, Mayer F (2010) Gender-specific neuromuscular activity of the M. peroneus longus in healthy runners—A descriptive laboratory study. Clin Biomech 25(9):938–943. https://doi.org/10.1016/j.clinbiomech.2010.06.009
Bennett WF, Doherty N, Hallisey MJ, Fulkerson JP (1993) Insertion orientation of terminal vastus lateralis obliquus and vastus medialis obliquus muscle fibers in human knees. Clin Anat 6(3):129–134. https://doi.org/10.1002/ca.980060302
Bigham HJ, Flaxman TE, Smith AJJ, Benoit DL (2018) Neuromuscular adaptations in older males and females with knee osteoarthritis during weight-bearing force control. Knee 25(1):40–50. https://doi.org/10.1016/j.knee.2017.06.004
Boling MC, Bolgla LA, Mattacola CG, Uhl TL, Hosey RG (2006) Outcomes of a weight-bearing rehabilitation program for patients diagnosed with patellofemoral pain syndrome. Arch Phys Med Rehabil 87(11):1428–1435. https://doi.org/10.1016/j.apmr.2006.07.264
Boling M, Padua D, Marshall S, Guskiewicz K, Pyne S, Beutler A (2010) Gender differences in the incidence and prevalence of patellofemoral pain syndrome. Scand J Med Sci Sports 20(5):725–730. https://doi.org/10.1111/j.1600-0838.2009.00996.x
Bowyer D, Armstrong M, Dixon J, Smith TO (2008) The vastus medialis oblique: vastus lateralis electromyographic intensity ratio does not differ by gender in young participants without knee pathology. Physiotherapy 94(2):168–173. https://doi.org/10.1016/j.physio.2007.08.007
Briani RV, de Oliveira SD, Pazzinatto MF, Ferreira AS, Ferrari D, de Azevedo FM (2016) Delayed onset of electromyographic activity of the vastus medialis relative to the vastus lateralis may be related to physical activity levels in females with patellofemoral pain. J Electromyogr Kinesiol 26:137–142. https://doi.org/10.1016/j.jelekin.2015.10.012
Brindle TJ, Mattacola C, McCrory J (2003) Electromyographic changes in the gluteus medius during stair ascent and descent in subjects with anterior knee pain. Knee Surg Sports Traumatol Arthrosc 11(4):244–251. https://doi.org/10.1007/s00167-003-0353-z
Cavazzuti L, Merlo A, Orlandi F, Campanini I (2010) Delayed onset of electromyographic activity of vastus medialis obliquus relative to vastus lateralis in subjects with patellofemoral pain syndrome. Gait Posture 32(3):290–295. https://doi.org/10.1016/j.gaitpost.2010.06.025
Chester R, Smith TO, Sweeting D, Dixon J, Wood S, Song F (2008) The relative timing of VMO and VL in the aetiology of anterior knee pain: a systematic review and meta-analysis. BMC Musculoskelet Disord 9:64. https://doi.org/10.1186/1471-2474-9-64
Cowan SM, Crossley KM (2009) Does gender influence neuromotor control of the knee and hip? J Electromyogr Kinesiol 19(2):276–282. https://doi.org/10.1016/j.jelekin.2007.07.009
Cowan SM, Hodges PW, Bennell KL (2001) Anticipatory activity of vastus lateralis and vastus medialis obliquus occurs simultaneously in voluntary heel and toe raises. Phys Ther Sport 2:71–79. https://doi.org/10.1054/ptsp.2001.0056
Cowan SM, Hodges PW, Bennell KL, Crossley KM (2002) Altered vastii recruitment when people with patellofemoral pain syndrome complete a postural task. Arch Phys Med Rehabil 83(7):989–995. https://doi.org/10.1053/apmr.2002.33234
Crossley KM, Cowan SM, Bennell KL, McConnell J (2004) Knee flexion during stair ambulation is altered in individuals with patellofemoral pain. J Orthop Res 22:267–274. https://doi.org/10.1016/j.orthres.2003.08.014
Dieter BP, McGowan CP, Stoll SK, Vella CA (2014) Muscle activation patterns and patellofemoral pain in cyclists. Med Sci Sports Exerc 46(4):753–761. https://doi.org/10.1249/MSS.0000000000000153
Farahmand F, Senavongse W, Amis AA (1998) Quantitative study of the quadriceps muscles and trochlear groove geometry related to instability of the patellofemoral joint. J Orthop Res 16(1):136–143. https://doi.org/10.1002/jor.1100160123
Felicio LR, Do Prado BA, Liporacci RF, Saad MC, De Oliveria AS, Bevilaqua-Grossi D (2011) Analysis of patellar stabilizers muscles and patellar kinematics in anterior knee pain subjects. J Electromyogr Kinesiol 21(1):148–153. https://doi.org/10.1016/j.jelekin.2010.09.001
Foss KD, Myer GD, Magnussen RA, Hewett TE (2014) Diagnostic differences for anterior knee pain between sexes in adolescent basketball players. J Athl Enhanc 3(1):1814. https://doi.org/10.4172/2324-9080.1000139
Gilleard W, McConnell J, Parsons D (1998) The effect of patellar taping on the onset of vastus medialis obliquus and vastus lateralis muscle activity in persons with patellofemoral pain. Phys Ther 78(1):25–32. https://doi.org/10.1093/ptj/78.1.25
Herrington L, Blacker M, Enjuanes N, Smith P, Worthington D (2006) The effect of limb position, exercise mode and contraction type on overall activity of VMO and VL. Phys Ther Sport 7(2):87–92. https://doi.org/10.1016/j.ptsp.2006.01.003
IBM Corp (2017) IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY: IBM Corp. Released 2017.
Konrad P (2005) The ABC of EMG: a practical introduction to kinesiological electromyography. Version 1.0. https://hermanwallace.com/download/The_ABC_of_EMG_by_Peter_Konrad.pdf. Accessed Apr 2005.
Karst GM, Willett GM (1995) Onset timing of electromyographic activity in the vastus medialis oblique and vastus lateralis muscles in subjects with and without patellofemoral pain syndrome. Phys Ther 75(9):813–823. https://doi.org/10.1093/ptj/75.9.813
Kujala UM, Jaakkola LH, Koskinen SK, Taimela S, Hurme M, Nelimarkka O (1993) Scoring of patellofemoral disorders. Arthroscopy 9(2):159–163. https://doi.org/10.1016/S0749-8063(05)80366-4
Laprade J, Culham E, Brouwer B (1998) Comparison of five isometric exercises in the recruitment of the vastus medialis oblique in persons with and without patellofemoral pain syndrome. J Orthop Sports Phys Ther 27(3):197–204. https://doi.org/10.2519/jospt.1998.27.3.197
Lieb FJ, Perry J (1968) Quadriceps function. An anatomical and mechanical study using amputated limbs. J Bone Jt Surg Am 50(8):1535–1548. https://doi.org/10.2106/00004623-196850080-00003
Lin F, Wang G, Koh JL, Hendrix RW, Zhang LQ (2004) In vivo and noninvasive three-dimensional patellar tracking induced by individual heads of quadriceps. Med Sci Sports Exerc 36(1):93–101. https://doi.org/10.1249/01.MSS.0000106260.45656.CC
Martinez-Valdes E, Negro F, Falla D, De Nunzio AM, Farina D (2018) Surface electromyographic amplitude does not identify differences in neural drive to synergistic muscles. J Appl Physiol 124(4):1071–1079. https://doi.org/10.1152/japplphysiol.01115.2017
McConnell J (1996) Management of patellofemoral problems. Man Ther 1(2):60–66. https://doi.org/10.1054/math.1996.0251
Miller AE, MacDougall JD, Tarnopolsky MA, Sale DG (1993) Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol 66(3):254–262
Morrish GM, Woledge RC (1997) A comparison of the activation of muscles moving the patella in normal subjects and in patients with chronic patellofemoral problems. Scand J Rehabil Med 29(1):43–48
Myer GD, Ford KR, Hewett TE (2005) The effects of gender on quadriceps muscle activation strategies during a maneuver that mimics a high ACL injury risk position. J Electromyogr Kinesiol 15(2):181–189. https://doi.org/10.1016/j.jelekin.2004.08.006
Narici MV, Roi GS, Landoni L, Minetti AE, Cerretelli P (1989) Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur J Appl Physiol Occup Physiol 59(4):310–319. https://doi.org/10.1007/bf02388334
Neptune RR, Wright IC, van den Bogert AJ (2000) The influence of orthotic devices and vastus medialis strength and timing on patellofemoral loads during running. Clin Biomech 15(8):611–618. https://doi.org/10.1016/S0268-0033(00)00028-0
Owings TM, Grabiner MD (2002) Motor control of the vastus medialis oblique and vastus lateralis muscles is disrupted during eccentric contractions in subjects with patellofemoral pain. Am J Sports Med 30(4):483–487. https://doi.org/10.1177/03635465020300040601
Pal S, Besier TF, Draper CE, Fredericson M, Gold GE, Beaupre GS, Delp SL (2012) Patellar tilt correlates with vastus lateralis:vastus medialis activation ratio in maltracking patellofemoral pain patients. J Orthop Res 30(6):927–933. https://doi.org/10.1002/jor.22008
Peng YL, Tenan MS, Griffin L (2018) Hip position and sex differences in motor unit firing patterns of the vastus medialis and vastus medialis oblique in healthy individuals. J Appl Physiol 124(6):1438–1446. https://doi.org/10.1152/japplphysiol.00702.2017
Powers CM (1998) Rehabilitation of patellofemoral joint disorders: a critical review. J Orthop Sports Phys Ther 28(5):345–354. https://doi.org/10.2519/jospt.1998.28.5.345
Powers CM, Bolgla LA, Callaghan MJ, Collins N, Sheehan FT (2012) Patellofemoral pain: proximal, distal, and local factors, 2nd International Research Retreat. J Orthop Sports Phys Ther 42(6):A1–54
Powers CM, Landel R, Perry J (1996) Timing and intensity of vastus muscle activity during functional activities in subjects with and without patellofemoral pain. Phys Ther 76(9):946–955. https://doi.org/10.1093/ptj/76.9.946
Rainoldi A, Falla D, Mellor R, Bennell K, Hodges P (2008) Myoelectric manifestations of fatigue in vastus lateralis, medialis obliquus and medialis longus muscles. J Electromyogr Kinesiol 18(6):1032–1037. https://doi.org/10.1016/j.jelekin.2007.05.008
Simoneau JA, Bouchard C (1989) Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol Endocrinol Metab 257(4 Pt 1):E567–E572. https://doi.org/10.1152/ajpendo.1989.257.4.E567
Spairani L, Barbero M, Cescon C, Combi F, Gemelli T, Giovanetti G, Magnani B, D’Antona G (2012) An electromyographic study of the vastii muscles during open and closed kinetic chain submaximal isometric exercises. Int J Sports Phys Ther 7(6):617–626
Sung PS, Lee DC (2009) Gender differences in onset timing and activation of the muscles of the dominant knee during stair climbing. Knee 16(5):375–380. https://doi.org/10.1016/j.knee.2009.02.003
Van Tiggelen D, Cowan S, Coorevits P, Duvigneaud N, Witvrouw E (2009) Delayed vastus medialis obliquus to vastus lateralis onset timing contributes to the development of patellofemoral pain in previously healthy men: a prospective study. Am J Sports Med 37(6):1099–1105. https://doi.org/10.1177/0363546508331135
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LG and YP conceived and designed research. YP conducted experiments and analyzed the data. LG and AJ assisted with data interpretation. All authors read and approved the manuscript.
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Peng, YL., Johnson, A.E. & Griffin, L. Sex differences in neuromuscular control of quadriceps. Eur J Appl Physiol 120, 2193–2202 (2020). https://doi.org/10.1007/s00421-020-04443-0
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DOI: https://doi.org/10.1007/s00421-020-04443-0