JCLB-04001; No of Pages 5 Clinical Biomechanics xxx (2015) xxx–xxx
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Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain Danilo de Oliveira Silva a, Ronaldo Valdir Briani a, Marcella Ferraz Pazzinatto a, Deisi Ferrari b, Fernando Amâncio Aragão c, Fábio Mícolis de Azevedo a,⁎ a b c
Physical Therapy Department, School of Science and Technology, University of São Paulo State, Presidente Prudente, Brazil Post-Graduation Program Interunits Bioengineering EESC/FMRP/IQSC-USP, University of São Paulo, São Carlos, Brazil Physical Therapy Department, State University of West Parana, Cascavel, Parana, Brazil
a r t i c l e
i n f o
Article history: Received 21 January 2015 Accepted 29 June 2015 Keywords: Kinetics Reproducibility of results Anterior knee pain Kinematics Patellofemoral joint
a b s t r a c t Background: Stair ascent is an activity that exacerbates symptoms of individuals with patellofemoral pain. The discomfort associated with this activity usually results in gait modification such as reduced knee flexion in an attempt to reduce pain. Although such compensatory strategy is a logical approach to decrease pain, it also reduces the normal active shock absorption increasing loading rates and may lead to deleterious and degenerative changes of the knee joint. Thus, the aims of this study were (i) to investigate whether there is reduced knee flexion in adults with PFP compared to healthy controls; and (ii) to analyze loading rates in these subjects, during stair climbing. Method: Twenty-nine individuals with patellofemoral pain and twenty-five control individuals (18–30 years) participated in this study. Each subject underwent three-dimensional kinematic and kinetic analyses during stair climbing on two separate days. Between-groups analyses of variance were performed to identify differences in peak knee flexion and loading rates. Intraclass correlation coefficient was performed to verify the reliability of the variables. Findings: On both days, the patellofemoral pain group demonstrated significantly reduced peak knee flexion and increased loading rates. In addition, the two variables obtained high to very high reliability. Interpretation: Reduced knee flexion during stair climbing as a strategy to avoid anterior knee pain does not seem to be healthy for lower limb mechanical distributions. Repeated loading at higher loading rates may be damaging to lower limb joints. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction One of the most common knee disorders affecting young individuals is patellofemoral pain (PFP) (Briani et al., 2015). Studies have suggested that females have a greater risk of developing this condition (Rathleff et al., 2013). The percentage of young females who initiate physical activity programs and are diagnosed with PFP is up to 10% (Rathleff et al., 2013). Furthermore, PFP affects 1 in 4 subjects in the general population (Ferrari et al., 2014). Clinically, individuals with PFP report limitations in gait, especially during ascending stairs (De Oliveira Silva et al., 2015). The discomfort associated with these activities usually results in gait modification, which attempts to reduce pain (Powers et al., 1999). A retrospective study design has shown that individuals with PFP may use protection strategies to avoid anterior knee pain (Powers et al., 1999). This is highlighted by (Crossley et al. (2004), who reported
⁎ Corresponding author at: Rua Roberto Simonsen, 305, Presidente Prudente, Sao Paulo 19060-900, Brazil. E-mail address: [email protected] (F.M. de Azevedo).
reduced peak knee flexion during stair ascent in individuals with PFP, possibly indicating a compensatory strategy to reduce pain which must be considered when interpreting findings. In general, decreased knee flexion excursion during the stance phase increases the peak vertical forces experienced by the lower extremities (Cook et al., 1997; Farrokhi et al., 2015). Strenuous impact loading can evoke joint damage and contribute to the development of knee joint injuries (Buckwalter et al., 2013). It has been suggested that vertical ground reaction force loading rates (loading rate) are an important parameter for assessing the overload of lower limb musculoskeletal tissues (Cook et al., 1997; Liikavainio et al., 2007, 2010; Radin et al., 1991). Loading rates are thought to describe the “intensity” with which the force develops at touchdown (Stacoff et al., 2005). In addition, repeated loading at higher physiological loading rates, such as those occurring during stair negotiation, are damaging to lower limb joints (Liikavainio et al., 2007, 2010; Loy and Voloshin, 1991; Stacoff et al., 2005). One study (McNitt-Gray et al., 1994) reported reductions in loading rates when individuals produced “soft landings” through increased knee flexion excursion, which is believed to be a shockattenuating mechanism.
http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021 0268-0033/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
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D. de Oliveira Silva et al. / Clinical Biomechanics xxx (2015) xxx–xxx
The relationship between knee flexion and ground reaction forces was studied by Cook et al. (1997), who found that restricted knee flexion during walking resulted in greater vertical ground reaction forces and rates of lower limb loading in normal subjects. Radin et al. (1986) have shown that one in every three asymptomatic pre-stage knee osteoarthritis adults are exposed to repetitive increased loading rates during walking. The loading rates affecting the musculoskeletal system during stair negotiation can be even more forceful (Loy and Voloshin, 1991; Stacoff et al., 2005). Interestingly, it has been recently speculated that PFP in younger individuals may be a precursor to knee osteoarthritis later in life (Crossley, 2014; Utting et al., 2005). Given the plausible mechanistic link between PFP and knee osteoarthritis, it stands to reason that biomechanical examination of usual locomotion patterns in individuals with PFP may provide valuable information regarding potential deviations and compensations adopted by these individuals (Farrokhi et al., 2015). Although such a compensatory strategy is a logical approach to decrease pain, it also reduces the normal active shock absorption increasing loading rates and may lead to deleterious and degenerative changes of the knee joint (Liikavainio et al., 2010; Powers et al., 1999; Radin et al., 1991). Thus, we hypothesized that individuals with PFP would present reduced knee flexion and increased loading rates. To further investigate this hypothesis, the aims of this study were (i) to investigate whether there is reduced knee flexion in adults with PFP compared to healthy controls; and (ii) to analyze the loading rates of these subjects during stair climbing. 2. Methods This cross-sectional study was performed at the Laboratory of Biomechanics and Motor Control of the University of São Paulo State. The sample was recruited from gyms, parks and universities between January and September 2014. The study was approved by the University of São Paulo State Human Ethics Committee, and each participant gave written informed consent prior to participation. 2.1. Participants Twenty-nine females with PFP and twenty-five pain free females (control group) were recruited. Mean (SD) age, height and mass are presented in Table 1. Power calculations for this study were performed using preliminary data (8 individuals) from a pilot study for peak knee flexion and loading rate. The parameter (peak knee flexion) with the highest standard deviation and the smallest difference between groups was used. Sample size was determined based on predicted power to detect a difference of 2° between the groups with an alpha of 0.05 and 80% power. Based on calculations made in sample power (SPSS Inc. Chicago, IL, USA), a minimum sample size of 22 subjects per group was indicated. Diagnosis of PFP was based on definitions used in previous PFP studies (Briani et al., 2015; De Oliveira Silva et al., 2015; Ferrari et al., 2014). The inclusion criteria were (1) anterior knee pain during at least 2 of the following activities: remaining seated, squatting, kneeling, running, climbing stairs and jumping; (2) pain during patellar palpation; (3) symptoms for at least 1 month with an insidious beginning; (4) pain level in the previous month of up to 3 cm on a 10 cm visual
Table 1 Demographics. Variable
Age Mass (kg) Height (m) Cadence (steps/min)
Pain-free
PFP
Mean (SD)
Mean (SD)
22.01 (3.05) 62.12 (7.31) 1.64 (0.06) 80.78 (6.93)
21.5 (2.98) 63.25 (10.76) 1.65 (0.02) 76.12 (6.04)
Mean (SD): mean and standard deviation.
p-value
0.572 0.201 0.636 0.198
analog scale (VAS); and (5) 3 or more positive clinical signs in the following tests: Clarke’s sign, McConnell test, Noble compression, Waldron test and patella in the medial or lateral position. The participants were required to fulfill all 5 requirements to be allocated to the PFP group and could not present any signs or symptoms of PFP or other diseases to be allocated to the CG. The presence of any of the following conditions was considered an exclusion criterion: events of patellar subluxation or dislocation, lower limb inflammatory process, osteoarthritis, patellar tendon or meniscus tears, bursitis, ligament tears or the presence of neurological diseases. Those who had undergone knee surgery or knee treatments such as arthroscopy, steroid injections, oral steroids, opiate treatment, acupuncture or physiotherapy during the preceding 6 months were excluded from this study. All the participants were evaluated according to the exclusion and inclusion criteria by two investigators with five years of clinical practice and were only allocated into the PFP group or control group if these two investigators were in agreement about the criteria. 2.2. Kinematic and kinetic analysis Data collection included lower-limb kinetic and kinematic evaluation of each participant’s symptomatic limb (those with unilateral symptoms) or most symptomatic limb (in those with bilateral symptoms) during stair climbing. Motion analysis was collected using a three-dimensional motion-analysis system (VICON MX, Vicon Motion Systems Inc.; Denver—EUA) combined with 4 cameras (type Bonita® B10) operating at a sampling frequency of 100 Hz with a resolution of 1 megapixel. Ground reaction forces were collected using a force plate (AMTI, OR6, Watertown, MA, USA) at a sampling frequency of 2000 Hz, synchronized with the motion capture system. To perform kinematic evaluation of each participant during stair climbing, a lower limb model was used associated with a plug-in gait model (PIG-SACR) to perform static calibration (Kadaba et al., 1990). Each participant’s height, mass, inter-anterior superior iliac spine distance (ASIS), ASIS to lateral malleolus distance, knee width and ankle width were recorded. Retro-reflective markers (9.5 mm) were placed by the same investigator on specific anatomical landmarks (outlined below) to form foot, shank, thigh and pelvis segments on both limbs: Markers were placed on the right and left ASIS; top of the sacrum (L4–L5), over the greater trochanter, lateral and medial knee at the level of the lateral femoral epicondyle, lateral and medial ankle at the level of the lateral malleolus, first and fifth metatarsal heads and the tip of the toe. A relaxed standing calibration trial was then captured, after which the participants performed practice stair climbing trials to allow familiarization with the instrumentation and environment, it is important to state that the subjects were not able to use handrails. Evaluation of motor tasks that are more challenging in terms of mechanical and muscular demands, such as managing stairs, may further contribute to the understanding of compensatory mechanisms generated by subjects with PFP which are not observed during walking (De Oliveira Silva et al., 2015). Because of this, the experimental design included a seven-step staircase, each step being 18 cm high and 28 cm deep, with a 2 m walkway in front of and behind the staircase. Once participants felt they were comfortable, and the investigator deemed they were climbing the stairs with consistent velocity, data collection commenced. Each participant was asked to climb the staircase at their natural comfortable speed. Five successful trials were collected for each participant. To ensure a natural stair-climbing pattern, participants were not aware of the force plate which was hidden within the fourth step; only the investigator knew of its existence and position, the force plate was mechanically coupled to the ground (i.e. independent and uncoupled from the stair structure). The starting positions prior to each trial were the same to optimize the likelihood of a successful trial. For the reliability analysis, the trials were performed in the same manner on separate days, with an interval of 2 to 7 days between the
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
D. de Oliveira Silva et al. / Clinical Biomechanics xxx (2015) xxx–xxx
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2 collection periods. The investigator was blind concerning group allocation.
Loading rate was found to be significantly greater in the PFP group compared to control group (Fig. 2) t(52) = 2.908 p-value = 0.018.
2.3. Data analysis
4. Discussion
Each trial was filtered with a fourth-order Butterworth low-pass filter with a cutoff frequency of 6 Hz for kinematic data and 10 Hz for kinetic data (Winter, 2009). The retro-reflective markers were identified and labeled within the Vicon Nexus® 1.8 (Vicon Motion Systems Inc., EUA) for reconstruction. Heel strike and toe off were identified using force plate data to allow cadence measurement. Data were then exported to a specifically developed Excel template for analysis. The variable of interest was peak knee flexion. Loading rate was calculated as between 20% and 80% of the period between footstrike and first peak of vertical ground reaction force; and the loading rate calculation was the total change in vertical ground reaction force divided by the total change in time over this period (Stacoff et al., 2005), vertical ground reaction force was normalized by the body weight of each individual. The reliability results of this study seem adequate. For a relative measure of reliability, the intraclass correlation coefficient (ICC) (2, k) model (confidence intervals) was used and the standard error of the mean (SEM) was used to express the precision of the measurement in absolute values. For the control group, the ICC values were 0.91 (0.80; 0.95) and 0.93 (0.81; 0.97) to peak knee flexion e loading rates, respectively, and the SEM values were 0.77 and 0.09 (N/s, normalized by body weight). For the PFP group, the ICC values were 0.84 (0.67; 0.90) and 0.86 (0.68; 0.93) to peak knee flexion e loading rate, respectively, the SEM values were 0.92 and 0.12 (N/s, normalized by body weight).
There were no significant differences between groups for age, height, mass or cadence (Table 1). Peak knee flexion was statistically 2.51° less in the PFP group (Fig. 1) t(52) = 2.355 p-value = 0.020.
Several theoretical hypotheses have been proposed in an attempt to explain the pathomechanisms underlying PFP development (Lankhorst et al., 2013). Our findings indicate that during stair ascent, reduced peak knee flexion and increased loading rates exist in individuals with PFP compared to asymptomatic individuals. We previously hypothesized that subjects with PFP would present reduced knee flexion and increased loading rates. Our findings demonstrate a reduction of 2.51° in knee flexion of individuals with PFP compared to controls during stair climbing. This result is consistent with previously reported findings of a 6.8° reduction in peak knee flexion during stair ascent (Crossley et al., 2004) in individuals with PFP. The 4.2° difference between the studies may be partly explained by differences in step height, which was lower in our study, or could reflect the greater pain severity reported on a 10 cm VAS reported in Crossley et al.’s study (7.5 cm) compared to ours (4.9 cm), highlighting the reduced knee flexion as a protection mechanism of individuals with PFP. It is difficult to confront our kinetic findings with the PFP literature. To the best of our knowledge, this is the first study to approach such perspective. However, our findings indicate a difference of 0.57 (N/s, normalized by body weight) between groups. Another study (Hamel et al., 2005), aimed at identifying differences in loading rate between healthy young females and older females during stair ascent reported a 1.64 (N/s, normalized by body weight) difference magnitude between groups. This higher difference (Hamel et al., 2005) may have occurred due to sample characteristics being quite different and, in our study, there were no differences concerning anthropometric data. Moreover, another possible reason for the slight difference in our findings is that perhaps some individuals were not in pain at the time of data collection due to the intermittent characteristic of pain in individuals with PFP (Grenholm et al., 2009). As we hypothesized, individuals with PFP demonstrated reduced knee flexion compared to pain-free individuals during stair climbing. On the other hand, no study has demonstrated increased loading rates in individuals with PFP during stair climbing. There is some evidence that compensatory reduced knee flexion could generate increased loading rates (Cook et al., 1997; Farrokhi et al., 2015; Radin et al., 1982, 1991) and this suggestion was supported by the results of the present study. The total range of motion sustained by the lower extremity during the loading phase may influence the forces experienced by the body (McNitt-Gray et al., 1994). Assuming a given impulse, greater excursions probably result in lower loading rates. A study demonstrated this principle by reporting that lower loading rates were associated
Fig. 1. Peak knee flexion means and standard deviations of the control group (CG) and patellofemoral pain group (PFP).* represents statistical difference p b 0.05.
Fig. 2. Loading rate means and standard deviations of the control group (CG) and patellofemoral pain group (PFP).* represents statistical difference p b 0.05.
2.4. Statistical analysis Statistical analysis was performed using SPSS (version 18.0, SPSS Inc., Chicago, IL), with an a priori level of significance of 0.05. Prior to statistical analysis, all variables were assessed for normality and were found to be normally distributed based on graphical observation (kurtosis and skewness) and obtainment of p N 0.05 in the Shapiro–Wilk test. Mean age, height, mass and cadence were compared between groups using independent-samples t tests. Due to adequate values of reliability, data used for subsequent analyses were from the first day of data collection, the day was chosen randomly. Independent t tests were used to compare peak knee flexion and loading rate between control group and PFP group during stair ascent. 3. Results
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
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with greater hip and knee flexion excursions in controlled landings (McNitt-Gray et al., 1994). These increased excursions may, therefore, reduce the risk of stress on lower limb joints. Since individuals with PFP have been shown to limit knee flexion and active shock absorbing action of the quadriceps (Cook et al., 1997), this population may be susceptible to increased vertical ground reaction forces and the consequences of an increased rate of lower limb loading. Thus, compensatory behavior to accommodate for PFP may have effect on the tibiofemoral joint, as a result of its horizontal orientation, through axial compression (Powers et al., 1999). On the other hand, loading rate would not have strong effects on the patellofemoral joint by nature of its vertical alignment and the fact that patellofemoral compression is primarily dependent on the magnitude of quadriceps force (Maquet, 1984; Powers et al., 1999) and the femur orientation (Liao et al., 2015). Additionally, reduced knee flexion angles in both asymptomatic individuals and individuals with tibiofemoral osteoarthritis have also been linked with a more rapid increase in the ground reaction forces and greater rates of lower limb loading, which make the tibiofemoral joint especially susceptible to disease development and/or progression through increased axial compression and impulse loading (Cook et al., 1997; Mündermann et al., 2005; Radin et al., 1991). Given our results, compensatory mechanisms of individuals with PFP to reduce knee pain may have a deleterious effect on the tibiofemoral joint. Our findings seem to be reasonable because it has been recently shown that PFP in younger individuals may be a precursor to knee osteoarthritis later in life (Crossley, 2014; Utting et al., 2005). In addition, another study has found a correlation between increases in the loading rates with the progression of pain and knee osteoarthritis (Radin et al., 1982). Therefore, reducing knee flexion during stair climbing as a strategy to avoid anterior knee pain does not seem to be healthy for the lower limb mechanics of females with PFP (Liikavainio et al., 2010; Radin et al., 1982, 1991; Salsich et al., 2001).
4.1. Clinical implications The results presented above suggest that therapists need to focus on knee flexion compensations during functional movement tasks in individuals with PFP. Individuals who systematically present reduced knee flexion have demonstrated increased loading rates (Cook et al., 1997; Farrokhi et al., 2015; Radin et al., 1986, 1991). This alteration may exacerbate the dysfunction in the long-term, and moreover, may contribute to other lower limb diseases: further research is now needed to explore this possibility. As there is an association between PFP and the development of knee osteoarthritis (Crossley, 2014; Utting et al., 2005), the potential for repeatedly performed, altered lower limb kinematics to damage lower limb joints should be further investigated. This is important clinically because once the relationship between kinetic/kinematic alterations and functional movement mechanics are clarified, stair climbing retraining methods to alter ambulation mechanics can be developed.
4.2. Limitations A limitation of this study was the inclusion of individuals with both unilateral and bilateral PFP, being a potential confounding factor. In addition, this study was unable to show a comparison with other activities like gait, running and stair descent. It would aid to understand if this adaptation appears only during stair ascent or also in other functional movement tasks. Due to the retrospective nature of the study, our results do not allow differentiation between cause and effect in relation to the kinematic and kinetic variables evaluated. Further prospective research is needed to evaluate if increased loading rate is caused by reduced knee flexion and if loading rate increases in individuals with PFP experiencing greater pain.
5. Conclusion The results of this study support the author’s hypothesis that individuals with PFP presented reduced knee flexion and increased values of loading rates compared to pain-free individuals during stair climbing.
Conflict of interest statement No author has any financial or personal relationship with people or organizations that could inappropriately influence this work.
References Briani, R.V., De Oliveira Silva, D., Pazzinatto, M.F., De Albuquerque, C.E., Ferrari, D., Aragão, F.A., et al., 2015. Comparison of frequency and time domain electromyography parameters in women with patellofemoral pain. Clin. Biomech. 30, 302–307. http:// dx.doi.org/10.1016/j.clinbiomech.2014.12.014. Buckwalter, J.A., Anderson, D.D., Brown, T.D., Tochigi, Y., Martin, J.A., 2013. The roles of mechanical stresses in the pathogenesis of osteoarthritis: Implications for treatment of joint injuries. Cartilage 4, 286–294. http://dx.doi.org/10.1177/1947603513495889. Cook, T.M., Farrell, K.P., Carey, I., Gibbs, J.M., Wiger, G.E., 1997. Effects of restricted knee flexion and walking speed on the vertical ground reaction force during gait. J. Orthop. Sports Phys. Ther. 25, 236–244. http://dx.doi.org/10.2519/jospt.1997.25.4. 236. Crossley, K., 2014. Is patellofemoral osteoarthritis a common sequela of patellofemoral pain? Br. J. Sports Med. 48, 409–410. http://dx.doi.org/10.1136/bjsports-2014093445. Crossley, K.M., Cowan, S.M., Bennell, K.L., McConnell, J., 2004. Knee flexion during stair ambulation is altered in individuals with patellofemoral pain. J. Orthop. Res. 22, 267–274. http://dx.doi.org/10.1016/j.orthres.2003.08.014. De Oliveira Silva, D., Briani, R.V., Pazzinatto, M.F., Ferrari, D., Aragão, F.A., Albuquerque, C.E., et al., 2015. Reliability and differentiation capability of dynamic and static kinematic measurements of rearfoot eversion in patellofemoral pain. Clin. Biomech. 30, 144–148. http://dx.doi.org/10.1016/j.clinbiomech.2014.12.009. Farrokhi, S., O’Connell, M., Fitzgerald, G.K., 2015. Altered gait biomechanics and increased knee-specific impairments in patients with coexisting tibiofemoral and patellofemoral osteoarthritis. Gait Posture 41, 81–85. http://dx.doi.org/10.1016/j.gaitpost.2014.08. 014. Ferrari, D., Kuriki, H.U., Silva, C.R., Alves, N., Mícolis de Azevedo, F., 2014. Diagnostic accuracy of the electromyography parameters associated with anterior knee pain in the diagnosis of patellofemoral pain syndrome. Arch. Phys. Med. Rehabil. 95, 1521–1526. http://dx.doi.org/10.1016/j.apmr.2014.03.028. Grenholm, A., Stensdotter, A.K., Häger-Ross, C., 2009. Kinematic analyses during stair descent in young women with patellofemoral pain. Clin. Biomech. 24, 88–94. http://dx. doi.org/10.1016/j.clinbiomech.2008.09.004. Hamel, K. a, Okita, N., Bus, S. a, Cavanagh, P.R., 2005. A comparison of foot/ground interaction during stair negotiation and level walking in young and older women. Ergonomics 48, 1047–1056. http://dx.doi.org/10.1080/00140130500193665. Kadaba, M.P., Ramakrishnan, H.K., Wootten, M.E., 1990. Measurement of lower extremity kinematics during level walking. J. Orthop. Res. 8, 383–392. http://dx.doi.org/10. 1002/jor.1100080310. Lankhorst, N.E., Bierma-Zeinstra, S.M. a, van Middelkoop, M., 2013. Factors associated with patellofemoral pain syndrome: A systematic review. Br. J. Sports Med. 47, 193–206. http://dx.doi.org/10.1136/bjsports-2011-090369. Liao, T., Yang, N., Ho, K., Farrokhi, S., Powers, C.M., Perry, J., et al., 2015. Femur rotation increases patella cartilage stress in females with patellofemoral pain. Med. Sci. Sports Exerc. http://dx.doi.org/10.1249/MSS.0000000000000617 (Epub ahead of print). Liikavainio, T., Isolehto, J., Helminen, H.J., Perttunen, J., Lepola, V., Kiviranta, I., et al., 2007. Loading and gait symmetry during level and stair walking in asymptomatic subjects with knee osteoarthritis: Importance of quadriceps femoris in reducing impact force during heel strike? Knee 14, 231–238. http://dx.doi.org/10.1016/j.knee.2007.03.001. Liikavainio, T., Bragge, T., Hakkarainen, M., Karjalainen, P.a., Arokoshi, J.P., 2010. Gait and muscle activation changes in men with knee osteoarthritis. Knee 17, 69–76. http://dx. doi.org/10.1016/j.knee.2009.05.003. Loy, D.J., Voloshin, A.S., 1991. Biomechanics of stair walking and jumping. J. Sports Sci. 9, 137–149. Maquet, P.G., 1984. Biomechanics of the Knee, 2nd ed. Springer, New York. McNitt-Gray, J.L., Yokoi, T., Millward, C., 1994. Landing strategies used by gymnasts on different surfaces. J. Appl. Biomech. 10, 237–252. Mündermann, A., Dyrby, C.O., Andriacchi, T.P., 2005. Secondary gait changes in patients with medial compartment knee osteoarthritis: Increased load at the ankle, knee, and hip during walking. Arthritis Rheum. 52, 2835–2844. http://dx.doi.org/10.1002/ art.21262. Powers, C.M., Heino, J.G., Rao, S., Perry, J., 1999. The influence of patellofemoral pain on lower limb loading during gait. Clin. Biomech. 14, 722–728. Radin, E.L., Eyre, D., Kelman, J.L., Schiller a L, 1982. Effect of prolonged walking on the joints of sheep. J. Biomech. 15, 487–492. Radin, E.L., Whittle, M.W., Yang, K.H., Jefferson, R.J., Rodgers, M.M., Kish, V.L., 1986. The heel strike transient, its relationship with the angular velocity of the shank, and the effect of quadriceps paralysis. Advances in Bioengineering, first edition, pp. 121–123 (New York).
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
D. de Oliveira Silva et al. / Clinical Biomechanics xxx (2015) xxx–xxx Radin, E.L., Yang, K.H., Riegger, C., Kish, V.L., O’Connor, J.J., 1991. Relationship between lower limb dynamics and knee joint pain. J. Orthop. Res. 9, 398–405. http://dx.doi. org/10.1002/jor.1100090312. Rathleff, M.S., Roos, E.M., Olesen, J.L., Rasmussen, S., Arendt-Nielsen, L., 2013. Lower mechanical pressure pain thresholds in female adolescents with patellofemoral pain syndrome. J. Orthop. Sports Phys. Ther. 43, 414–421. http://dx.doi.org/10.2519/ jospt.2013.4383. Salsich, G.B., Brechter, J.H., Powers, C.M., 2001. Lower extremity kinetics during stair ambulation in patients with and without patellofemoral pain. Clin. Biomech. 16, 906–912. http://dx.doi.org/10.1016/S0268-0033(01)00085-7.
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Stacoff, A., Diezi, C., Luder, G., Stüssi, E., Kramers-De Quervain, I. a, 2005. Ground reaction forces on stairs: Effects of stair inclination and age. Gait Posture 21, 24–38. http://dx. doi.org/10.1016/j.gaitpost.2003.11.003. Utting, M.R., Davies, G., Newman, J.H., 2005. Is anterior knee pain a predisposing factor to patellofemoral osteoarthritis? Knee 12, 362–365. http://dx.doi.org/10.1016/j.knee. 2004.12.006. Winter, D., 2009. Biomechanics and Motor Control of Human Movement, 4th ed. (New York).
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
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Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain Danilo de Oliveira Silva a, Ronaldo Valdir Briani a, Marcella Ferraz Pazzinatto a, Deisi Ferrari b, Fernando Amâncio Aragão c, Fábio Mícolis de Azevedo a,⁎ a b c
Physical Therapy Department, School of Science and Technology, University of São Paulo State, Presidente Prudente, Brazil Post-Graduation Program Interunits Bioengineering EESC/FMRP/IQSC-USP, University of São Paulo, São Carlos, Brazil Physical Therapy Department, State University of West Parana, Cascavel, Parana, Brazil
a r t i c l e
i n f o
Article history: Received 21 January 2015 Accepted 29 June 2015 Keywords: Kinetics Reproducibility of results Anterior knee pain Kinematics Patellofemoral joint
a b s t r a c t Background: Stair ascent is an activity that exacerbates symptoms of individuals with patellofemoral pain. The discomfort associated with this activity usually results in gait modification such as reduced knee flexion in an attempt to reduce pain. Although such compensatory strategy is a logical approach to decrease pain, it also reduces the normal active shock absorption increasing loading rates and may lead to deleterious and degenerative changes of the knee joint. Thus, the aims of this study were (i) to investigate whether there is reduced knee flexion in adults with PFP compared to healthy controls; and (ii) to analyze loading rates in these subjects, during stair climbing. Method: Twenty-nine individuals with patellofemoral pain and twenty-five control individuals (18–30 years) participated in this study. Each subject underwent three-dimensional kinematic and kinetic analyses during stair climbing on two separate days. Between-groups analyses of variance were performed to identify differences in peak knee flexion and loading rates. Intraclass correlation coefficient was performed to verify the reliability of the variables. Findings: On both days, the patellofemoral pain group demonstrated significantly reduced peak knee flexion and increased loading rates. In addition, the two variables obtained high to very high reliability. Interpretation: Reduced knee flexion during stair climbing as a strategy to avoid anterior knee pain does not seem to be healthy for lower limb mechanical distributions. Repeated loading at higher loading rates may be damaging to lower limb joints. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction One of the most common knee disorders affecting young individuals is patellofemoral pain (PFP) (Briani et al., 2015). Studies have suggested that females have a greater risk of developing this condition (Rathleff et al., 2013). The percentage of young females who initiate physical activity programs and are diagnosed with PFP is up to 10% (Rathleff et al., 2013). Furthermore, PFP affects 1 in 4 subjects in the general population (Ferrari et al., 2014). Clinically, individuals with PFP report limitations in gait, especially during ascending stairs (De Oliveira Silva et al., 2015). The discomfort associated with these activities usually results in gait modification, which attempts to reduce pain (Powers et al., 1999). A retrospective study design has shown that individuals with PFP may use protection strategies to avoid anterior knee pain (Powers et al., 1999). This is highlighted by (Crossley et al. (2004), who reported
⁎ Corresponding author at: Rua Roberto Simonsen, 305, Presidente Prudente, Sao Paulo 19060-900, Brazil. E-mail address: [email protected] (F.M. de Azevedo).
reduced peak knee flexion during stair ascent in individuals with PFP, possibly indicating a compensatory strategy to reduce pain which must be considered when interpreting findings. In general, decreased knee flexion excursion during the stance phase increases the peak vertical forces experienced by the lower extremities (Cook et al., 1997; Farrokhi et al., 2015). Strenuous impact loading can evoke joint damage and contribute to the development of knee joint injuries (Buckwalter et al., 2013). It has been suggested that vertical ground reaction force loading rates (loading rate) are an important parameter for assessing the overload of lower limb musculoskeletal tissues (Cook et al., 1997; Liikavainio et al., 2007, 2010; Radin et al., 1991). Loading rates are thought to describe the “intensity” with which the force develops at touchdown (Stacoff et al., 2005). In addition, repeated loading at higher physiological loading rates, such as those occurring during stair negotiation, are damaging to lower limb joints (Liikavainio et al., 2007, 2010; Loy and Voloshin, 1991; Stacoff et al., 2005). One study (McNitt-Gray et al., 1994) reported reductions in loading rates when individuals produced “soft landings” through increased knee flexion excursion, which is believed to be a shockattenuating mechanism.
http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021 0268-0033/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
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The relationship between knee flexion and ground reaction forces was studied by Cook et al. (1997), who found that restricted knee flexion during walking resulted in greater vertical ground reaction forces and rates of lower limb loading in normal subjects. Radin et al. (1986) have shown that one in every three asymptomatic pre-stage knee osteoarthritis adults are exposed to repetitive increased loading rates during walking. The loading rates affecting the musculoskeletal system during stair negotiation can be even more forceful (Loy and Voloshin, 1991; Stacoff et al., 2005). Interestingly, it has been recently speculated that PFP in younger individuals may be a precursor to knee osteoarthritis later in life (Crossley, 2014; Utting et al., 2005). Given the plausible mechanistic link between PFP and knee osteoarthritis, it stands to reason that biomechanical examination of usual locomotion patterns in individuals with PFP may provide valuable information regarding potential deviations and compensations adopted by these individuals (Farrokhi et al., 2015). Although such a compensatory strategy is a logical approach to decrease pain, it also reduces the normal active shock absorption increasing loading rates and may lead to deleterious and degenerative changes of the knee joint (Liikavainio et al., 2010; Powers et al., 1999; Radin et al., 1991). Thus, we hypothesized that individuals with PFP would present reduced knee flexion and increased loading rates. To further investigate this hypothesis, the aims of this study were (i) to investigate whether there is reduced knee flexion in adults with PFP compared to healthy controls; and (ii) to analyze the loading rates of these subjects during stair climbing. 2. Methods This cross-sectional study was performed at the Laboratory of Biomechanics and Motor Control of the University of São Paulo State. The sample was recruited from gyms, parks and universities between January and September 2014. The study was approved by the University of São Paulo State Human Ethics Committee, and each participant gave written informed consent prior to participation. 2.1. Participants Twenty-nine females with PFP and twenty-five pain free females (control group) were recruited. Mean (SD) age, height and mass are presented in Table 1. Power calculations for this study were performed using preliminary data (8 individuals) from a pilot study for peak knee flexion and loading rate. The parameter (peak knee flexion) with the highest standard deviation and the smallest difference between groups was used. Sample size was determined based on predicted power to detect a difference of 2° between the groups with an alpha of 0.05 and 80% power. Based on calculations made in sample power (SPSS Inc. Chicago, IL, USA), a minimum sample size of 22 subjects per group was indicated. Diagnosis of PFP was based on definitions used in previous PFP studies (Briani et al., 2015; De Oliveira Silva et al., 2015; Ferrari et al., 2014). The inclusion criteria were (1) anterior knee pain during at least 2 of the following activities: remaining seated, squatting, kneeling, running, climbing stairs and jumping; (2) pain during patellar palpation; (3) symptoms for at least 1 month with an insidious beginning; (4) pain level in the previous month of up to 3 cm on a 10 cm visual
Table 1 Demographics. Variable
Age Mass (kg) Height (m) Cadence (steps/min)
Pain-free
PFP
Mean (SD)
Mean (SD)
22.01 (3.05) 62.12 (7.31) 1.64 (0.06) 80.78 (6.93)
21.5 (2.98) 63.25 (10.76) 1.65 (0.02) 76.12 (6.04)
Mean (SD): mean and standard deviation.
p-value
0.572 0.201 0.636 0.198
analog scale (VAS); and (5) 3 or more positive clinical signs in the following tests: Clarke’s sign, McConnell test, Noble compression, Waldron test and patella in the medial or lateral position. The participants were required to fulfill all 5 requirements to be allocated to the PFP group and could not present any signs or symptoms of PFP or other diseases to be allocated to the CG. The presence of any of the following conditions was considered an exclusion criterion: events of patellar subluxation or dislocation, lower limb inflammatory process, osteoarthritis, patellar tendon or meniscus tears, bursitis, ligament tears or the presence of neurological diseases. Those who had undergone knee surgery or knee treatments such as arthroscopy, steroid injections, oral steroids, opiate treatment, acupuncture or physiotherapy during the preceding 6 months were excluded from this study. All the participants were evaluated according to the exclusion and inclusion criteria by two investigators with five years of clinical practice and were only allocated into the PFP group or control group if these two investigators were in agreement about the criteria. 2.2. Kinematic and kinetic analysis Data collection included lower-limb kinetic and kinematic evaluation of each participant’s symptomatic limb (those with unilateral symptoms) or most symptomatic limb (in those with bilateral symptoms) during stair climbing. Motion analysis was collected using a three-dimensional motion-analysis system (VICON MX, Vicon Motion Systems Inc.; Denver—EUA) combined with 4 cameras (type Bonita® B10) operating at a sampling frequency of 100 Hz with a resolution of 1 megapixel. Ground reaction forces were collected using a force plate (AMTI, OR6, Watertown, MA, USA) at a sampling frequency of 2000 Hz, synchronized with the motion capture system. To perform kinematic evaluation of each participant during stair climbing, a lower limb model was used associated with a plug-in gait model (PIG-SACR) to perform static calibration (Kadaba et al., 1990). Each participant’s height, mass, inter-anterior superior iliac spine distance (ASIS), ASIS to lateral malleolus distance, knee width and ankle width were recorded. Retro-reflective markers (9.5 mm) were placed by the same investigator on specific anatomical landmarks (outlined below) to form foot, shank, thigh and pelvis segments on both limbs: Markers were placed on the right and left ASIS; top of the sacrum (L4–L5), over the greater trochanter, lateral and medial knee at the level of the lateral femoral epicondyle, lateral and medial ankle at the level of the lateral malleolus, first and fifth metatarsal heads and the tip of the toe. A relaxed standing calibration trial was then captured, after which the participants performed practice stair climbing trials to allow familiarization with the instrumentation and environment, it is important to state that the subjects were not able to use handrails. Evaluation of motor tasks that are more challenging in terms of mechanical and muscular demands, such as managing stairs, may further contribute to the understanding of compensatory mechanisms generated by subjects with PFP which are not observed during walking (De Oliveira Silva et al., 2015). Because of this, the experimental design included a seven-step staircase, each step being 18 cm high and 28 cm deep, with a 2 m walkway in front of and behind the staircase. Once participants felt they were comfortable, and the investigator deemed they were climbing the stairs with consistent velocity, data collection commenced. Each participant was asked to climb the staircase at their natural comfortable speed. Five successful trials were collected for each participant. To ensure a natural stair-climbing pattern, participants were not aware of the force plate which was hidden within the fourth step; only the investigator knew of its existence and position, the force plate was mechanically coupled to the ground (i.e. independent and uncoupled from the stair structure). The starting positions prior to each trial were the same to optimize the likelihood of a successful trial. For the reliability analysis, the trials were performed in the same manner on separate days, with an interval of 2 to 7 days between the
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
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2 collection periods. The investigator was blind concerning group allocation.
Loading rate was found to be significantly greater in the PFP group compared to control group (Fig. 2) t(52) = 2.908 p-value = 0.018.
2.3. Data analysis
4. Discussion
Each trial was filtered with a fourth-order Butterworth low-pass filter with a cutoff frequency of 6 Hz for kinematic data and 10 Hz for kinetic data (Winter, 2009). The retro-reflective markers were identified and labeled within the Vicon Nexus® 1.8 (Vicon Motion Systems Inc., EUA) for reconstruction. Heel strike and toe off were identified using force plate data to allow cadence measurement. Data were then exported to a specifically developed Excel template for analysis. The variable of interest was peak knee flexion. Loading rate was calculated as between 20% and 80% of the period between footstrike and first peak of vertical ground reaction force; and the loading rate calculation was the total change in vertical ground reaction force divided by the total change in time over this period (Stacoff et al., 2005), vertical ground reaction force was normalized by the body weight of each individual. The reliability results of this study seem adequate. For a relative measure of reliability, the intraclass correlation coefficient (ICC) (2, k) model (confidence intervals) was used and the standard error of the mean (SEM) was used to express the precision of the measurement in absolute values. For the control group, the ICC values were 0.91 (0.80; 0.95) and 0.93 (0.81; 0.97) to peak knee flexion e loading rates, respectively, and the SEM values were 0.77 and 0.09 (N/s, normalized by body weight). For the PFP group, the ICC values were 0.84 (0.67; 0.90) and 0.86 (0.68; 0.93) to peak knee flexion e loading rate, respectively, the SEM values were 0.92 and 0.12 (N/s, normalized by body weight).
There were no significant differences between groups for age, height, mass or cadence (Table 1). Peak knee flexion was statistically 2.51° less in the PFP group (Fig. 1) t(52) = 2.355 p-value = 0.020.
Several theoretical hypotheses have been proposed in an attempt to explain the pathomechanisms underlying PFP development (Lankhorst et al., 2013). Our findings indicate that during stair ascent, reduced peak knee flexion and increased loading rates exist in individuals with PFP compared to asymptomatic individuals. We previously hypothesized that subjects with PFP would present reduced knee flexion and increased loading rates. Our findings demonstrate a reduction of 2.51° in knee flexion of individuals with PFP compared to controls during stair climbing. This result is consistent with previously reported findings of a 6.8° reduction in peak knee flexion during stair ascent (Crossley et al., 2004) in individuals with PFP. The 4.2° difference between the studies may be partly explained by differences in step height, which was lower in our study, or could reflect the greater pain severity reported on a 10 cm VAS reported in Crossley et al.’s study (7.5 cm) compared to ours (4.9 cm), highlighting the reduced knee flexion as a protection mechanism of individuals with PFP. It is difficult to confront our kinetic findings with the PFP literature. To the best of our knowledge, this is the first study to approach such perspective. However, our findings indicate a difference of 0.57 (N/s, normalized by body weight) between groups. Another study (Hamel et al., 2005), aimed at identifying differences in loading rate between healthy young females and older females during stair ascent reported a 1.64 (N/s, normalized by body weight) difference magnitude between groups. This higher difference (Hamel et al., 2005) may have occurred due to sample characteristics being quite different and, in our study, there were no differences concerning anthropometric data. Moreover, another possible reason for the slight difference in our findings is that perhaps some individuals were not in pain at the time of data collection due to the intermittent characteristic of pain in individuals with PFP (Grenholm et al., 2009). As we hypothesized, individuals with PFP demonstrated reduced knee flexion compared to pain-free individuals during stair climbing. On the other hand, no study has demonstrated increased loading rates in individuals with PFP during stair climbing. There is some evidence that compensatory reduced knee flexion could generate increased loading rates (Cook et al., 1997; Farrokhi et al., 2015; Radin et al., 1982, 1991) and this suggestion was supported by the results of the present study. The total range of motion sustained by the lower extremity during the loading phase may influence the forces experienced by the body (McNitt-Gray et al., 1994). Assuming a given impulse, greater excursions probably result in lower loading rates. A study demonstrated this principle by reporting that lower loading rates were associated
Fig. 1. Peak knee flexion means and standard deviations of the control group (CG) and patellofemoral pain group (PFP).* represents statistical difference p b 0.05.
Fig. 2. Loading rate means and standard deviations of the control group (CG) and patellofemoral pain group (PFP).* represents statistical difference p b 0.05.
2.4. Statistical analysis Statistical analysis was performed using SPSS (version 18.0, SPSS Inc., Chicago, IL), with an a priori level of significance of 0.05. Prior to statistical analysis, all variables were assessed for normality and were found to be normally distributed based on graphical observation (kurtosis and skewness) and obtainment of p N 0.05 in the Shapiro–Wilk test. Mean age, height, mass and cadence were compared between groups using independent-samples t tests. Due to adequate values of reliability, data used for subsequent analyses were from the first day of data collection, the day was chosen randomly. Independent t tests were used to compare peak knee flexion and loading rate between control group and PFP group during stair ascent. 3. Results
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
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with greater hip and knee flexion excursions in controlled landings (McNitt-Gray et al., 1994). These increased excursions may, therefore, reduce the risk of stress on lower limb joints. Since individuals with PFP have been shown to limit knee flexion and active shock absorbing action of the quadriceps (Cook et al., 1997), this population may be susceptible to increased vertical ground reaction forces and the consequences of an increased rate of lower limb loading. Thus, compensatory behavior to accommodate for PFP may have effect on the tibiofemoral joint, as a result of its horizontal orientation, through axial compression (Powers et al., 1999). On the other hand, loading rate would not have strong effects on the patellofemoral joint by nature of its vertical alignment and the fact that patellofemoral compression is primarily dependent on the magnitude of quadriceps force (Maquet, 1984; Powers et al., 1999) and the femur orientation (Liao et al., 2015). Additionally, reduced knee flexion angles in both asymptomatic individuals and individuals with tibiofemoral osteoarthritis have also been linked with a more rapid increase in the ground reaction forces and greater rates of lower limb loading, which make the tibiofemoral joint especially susceptible to disease development and/or progression through increased axial compression and impulse loading (Cook et al., 1997; Mündermann et al., 2005; Radin et al., 1991). Given our results, compensatory mechanisms of individuals with PFP to reduce knee pain may have a deleterious effect on the tibiofemoral joint. Our findings seem to be reasonable because it has been recently shown that PFP in younger individuals may be a precursor to knee osteoarthritis later in life (Crossley, 2014; Utting et al., 2005). In addition, another study has found a correlation between increases in the loading rates with the progression of pain and knee osteoarthritis (Radin et al., 1982). Therefore, reducing knee flexion during stair climbing as a strategy to avoid anterior knee pain does not seem to be healthy for the lower limb mechanics of females with PFP (Liikavainio et al., 2010; Radin et al., 1982, 1991; Salsich et al., 2001).
4.1. Clinical implications The results presented above suggest that therapists need to focus on knee flexion compensations during functional movement tasks in individuals with PFP. Individuals who systematically present reduced knee flexion have demonstrated increased loading rates (Cook et al., 1997; Farrokhi et al., 2015; Radin et al., 1986, 1991). This alteration may exacerbate the dysfunction in the long-term, and moreover, may contribute to other lower limb diseases: further research is now needed to explore this possibility. As there is an association between PFP and the development of knee osteoarthritis (Crossley, 2014; Utting et al., 2005), the potential for repeatedly performed, altered lower limb kinematics to damage lower limb joints should be further investigated. This is important clinically because once the relationship between kinetic/kinematic alterations and functional movement mechanics are clarified, stair climbing retraining methods to alter ambulation mechanics can be developed.
4.2. Limitations A limitation of this study was the inclusion of individuals with both unilateral and bilateral PFP, being a potential confounding factor. In addition, this study was unable to show a comparison with other activities like gait, running and stair descent. It would aid to understand if this adaptation appears only during stair ascent or also in other functional movement tasks. Due to the retrospective nature of the study, our results do not allow differentiation between cause and effect in relation to the kinematic and kinetic variables evaluated. Further prospective research is needed to evaluate if increased loading rate is caused by reduced knee flexion and if loading rate increases in individuals with PFP experiencing greater pain.
5. Conclusion The results of this study support the author’s hypothesis that individuals with PFP presented reduced knee flexion and increased values of loading rates compared to pain-free individuals during stair climbing.
Conflict of interest statement No author has any financial or personal relationship with people or organizations that could inappropriately influence this work.
References Briani, R.V., De Oliveira Silva, D., Pazzinatto, M.F., De Albuquerque, C.E., Ferrari, D., Aragão, F.A., et al., 2015. Comparison of frequency and time domain electromyography parameters in women with patellofemoral pain. Clin. Biomech. 30, 302–307. http:// dx.doi.org/10.1016/j.clinbiomech.2014.12.014. Buckwalter, J.A., Anderson, D.D., Brown, T.D., Tochigi, Y., Martin, J.A., 2013. The roles of mechanical stresses in the pathogenesis of osteoarthritis: Implications for treatment of joint injuries. Cartilage 4, 286–294. http://dx.doi.org/10.1177/1947603513495889. Cook, T.M., Farrell, K.P., Carey, I., Gibbs, J.M., Wiger, G.E., 1997. Effects of restricted knee flexion and walking speed on the vertical ground reaction force during gait. J. Orthop. Sports Phys. Ther. 25, 236–244. http://dx.doi.org/10.2519/jospt.1997.25.4. 236. Crossley, K., 2014. Is patellofemoral osteoarthritis a common sequela of patellofemoral pain? Br. J. Sports Med. 48, 409–410. http://dx.doi.org/10.1136/bjsports-2014093445. Crossley, K.M., Cowan, S.M., Bennell, K.L., McConnell, J., 2004. Knee flexion during stair ambulation is altered in individuals with patellofemoral pain. J. Orthop. Res. 22, 267–274. http://dx.doi.org/10.1016/j.orthres.2003.08.014. De Oliveira Silva, D., Briani, R.V., Pazzinatto, M.F., Ferrari, D., Aragão, F.A., Albuquerque, C.E., et al., 2015. Reliability and differentiation capability of dynamic and static kinematic measurements of rearfoot eversion in patellofemoral pain. Clin. Biomech. 30, 144–148. http://dx.doi.org/10.1016/j.clinbiomech.2014.12.009. Farrokhi, S., O’Connell, M., Fitzgerald, G.K., 2015. Altered gait biomechanics and increased knee-specific impairments in patients with coexisting tibiofemoral and patellofemoral osteoarthritis. Gait Posture 41, 81–85. http://dx.doi.org/10.1016/j.gaitpost.2014.08. 014. Ferrari, D., Kuriki, H.U., Silva, C.R., Alves, N., Mícolis de Azevedo, F., 2014. Diagnostic accuracy of the electromyography parameters associated with anterior knee pain in the diagnosis of patellofemoral pain syndrome. Arch. Phys. Med. Rehabil. 95, 1521–1526. http://dx.doi.org/10.1016/j.apmr.2014.03.028. Grenholm, A., Stensdotter, A.K., Häger-Ross, C., 2009. Kinematic analyses during stair descent in young women with patellofemoral pain. Clin. Biomech. 24, 88–94. http://dx. doi.org/10.1016/j.clinbiomech.2008.09.004. Hamel, K. a, Okita, N., Bus, S. a, Cavanagh, P.R., 2005. A comparison of foot/ground interaction during stair negotiation and level walking in young and older women. Ergonomics 48, 1047–1056. http://dx.doi.org/10.1080/00140130500193665. Kadaba, M.P., Ramakrishnan, H.K., Wootten, M.E., 1990. Measurement of lower extremity kinematics during level walking. J. Orthop. Res. 8, 383–392. http://dx.doi.org/10. 1002/jor.1100080310. Lankhorst, N.E., Bierma-Zeinstra, S.M. a, van Middelkoop, M., 2013. Factors associated with patellofemoral pain syndrome: A systematic review. Br. J. Sports Med. 47, 193–206. http://dx.doi.org/10.1136/bjsports-2011-090369. Liao, T., Yang, N., Ho, K., Farrokhi, S., Powers, C.M., Perry, J., et al., 2015. Femur rotation increases patella cartilage stress in females with patellofemoral pain. Med. Sci. Sports Exerc. http://dx.doi.org/10.1249/MSS.0000000000000617 (Epub ahead of print). Liikavainio, T., Isolehto, J., Helminen, H.J., Perttunen, J., Lepola, V., Kiviranta, I., et al., 2007. Loading and gait symmetry during level and stair walking in asymptomatic subjects with knee osteoarthritis: Importance of quadriceps femoris in reducing impact force during heel strike? Knee 14, 231–238. http://dx.doi.org/10.1016/j.knee.2007.03.001. Liikavainio, T., Bragge, T., Hakkarainen, M., Karjalainen, P.a., Arokoshi, J.P., 2010. Gait and muscle activation changes in men with knee osteoarthritis. Knee 17, 69–76. http://dx. doi.org/10.1016/j.knee.2009.05.003. Loy, D.J., Voloshin, A.S., 1991. Biomechanics of stair walking and jumping. J. Sports Sci. 9, 137–149. Maquet, P.G., 1984. Biomechanics of the Knee, 2nd ed. Springer, New York. McNitt-Gray, J.L., Yokoi, T., Millward, C., 1994. Landing strategies used by gymnasts on different surfaces. J. Appl. Biomech. 10, 237–252. Mündermann, A., Dyrby, C.O., Andriacchi, T.P., 2005. Secondary gait changes in patients with medial compartment knee osteoarthritis: Increased load at the ankle, knee, and hip during walking. Arthritis Rheum. 52, 2835–2844. http://dx.doi.org/10.1002/ art.21262. Powers, C.M., Heino, J.G., Rao, S., Perry, J., 1999. The influence of patellofemoral pain on lower limb loading during gait. Clin. Biomech. 14, 722–728. Radin, E.L., Eyre, D., Kelman, J.L., Schiller a L, 1982. Effect of prolonged walking on the joints of sheep. J. Biomech. 15, 487–492. Radin, E.L., Whittle, M.W., Yang, K.H., Jefferson, R.J., Rodgers, M.M., Kish, V.L., 1986. The heel strike transient, its relationship with the angular velocity of the shank, and the effect of quadriceps paralysis. Advances in Bioengineering, first edition, pp. 121–123 (New York).
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
D. de Oliveira Silva et al. / Clinical Biomechanics xxx (2015) xxx–xxx Radin, E.L., Yang, K.H., Riegger, C., Kish, V.L., O’Connor, J.J., 1991. Relationship between lower limb dynamics and knee joint pain. J. Orthop. Res. 9, 398–405. http://dx.doi. org/10.1002/jor.1100090312. Rathleff, M.S., Roos, E.M., Olesen, J.L., Rasmussen, S., Arendt-Nielsen, L., 2013. Lower mechanical pressure pain thresholds in female adolescents with patellofemoral pain syndrome. J. Orthop. Sports Phys. Ther. 43, 414–421. http://dx.doi.org/10.2519/ jospt.2013.4383. Salsich, G.B., Brechter, J.H., Powers, C.M., 2001. Lower extremity kinetics during stair ambulation in patients with and without patellofemoral pain. Clin. Biomech. 16, 906–912. http://dx.doi.org/10.1016/S0268-0033(01)00085-7.
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Stacoff, A., Diezi, C., Luder, G., Stüssi, E., Kramers-De Quervain, I. a, 2005. Ground reaction forces on stairs: Effects of stair inclination and age. Gait Posture 21, 24–38. http://dx. doi.org/10.1016/j.gaitpost.2003.11.003. Utting, M.R., Davies, G., Newman, J.H., 2005. Is anterior knee pain a predisposing factor to patellofemoral osteoarthritis? Knee 12, 362–365. http://dx.doi.org/10.1016/j.knee. 2004.12.006. Winter, D., 2009. Biomechanics and Motor Control of Human Movement, 4th ed. (New York).
Please cite this article as: de Oliveira Silva, D., et al., Reduced knee flexion is a possible cause of increased loading rates in individuals with patellofemoral pain, Clin. Biomech. (2015), http://dx.doi.org/10.1016/j.clinbiomech.2015.06.021
