1. Introduction
Both recreational and competitive distance running are associated with a plethora of physiological benefits [
1]. However, despite the physical improvements caused by running, it is also linked with a very high rate of overuse injuries [
2,
3]. Patellofemoral pain (PFP) is a common atraumatic knee pathology that typically manifests as retropatellar or peripatellar pain and inflammation, aggravated by activities that frequently load the joint [
4]. PFP has an incidence rate as high as 21% in runners [
5], with a much larger prevalence in females [
6]. The long-term prognosis is poor, with 71–91% of patients experiencing symptoms 20 years after diagnosis [
7]. PFP symptoms may later present with radiographic evidence of osteoarthritis at this joint [
8], and pain symptoms force many to reduce or even end their running training [
9], causing many to develop associated psychological disorders [
10].
The lack of treatment efficacy is attributed to the multifactorial nature and complex aetiology of PFP, which makes the identification of modifiable risk factors problematic [
11]. Given the high incidence of PFP in runners [
5], an enhanced comprehension of the parameters linked to PFP’s aetiology and its distinct incidence in differing populations is essential in order to prevent symptoms and improve management. Recent prospective pooled systematic reviews and meta-analyses have shown physiological indices of quadriceps weakness and hip abduction strength to be risk factors for PFP in military and adolescent populations, although no identifiable risk factors were evident in runners [
12].
There is a lack of prospective investigations exploring the biomechanical mechanisms linked to the aetiology of PFP in runners [
4]. Noehren et al. [
13] showed that female runners were at an increased risk of developing PFP in the presence of a statistically greater maximum hip adduction angle. Furthermore, in relation to asymptomatic controls, Fox et al. [
14] showed that PFP runners exhibited increased peak hip adduction, hip transverse plane range of motion (ROM), peak knee flexion, peak knee abduction, and peak dorsiflexion. Noehren et al. [
15,
16] revealed that in female PFP runners, increased hip adduction, hip internal rotation, and tibial internal rotation were evident compared to controls. Esculier et al. [
17] showed that runners with PFP exhibited higher hip adduction at toe-off, lower hip adduction ROM during late-stance, and longer soleus activation. Conversely, Dierks et al. [
18] showed that runners with PFP demonstrated reduced peak knee flexion, peak hip adduction, eversion ROM, peak knee flexion velocity, peak hip adduction velocity, and peak hip internal rotation velocity compared with controls. Finally, Willson and Davis [
19] revealed that females with PFP demonstrated greater hip adduction and contralateral pelvic drop compared to asymptomatic runners. Neal et al. [
12] proposed that these kinematic variations contribute to the development and persistence of PFP by way of increased patellofemoral joint stress, although patellofemoral joint loading has not yet been explored in runners with PFP in relation to asymptomatic controls.
Although previous analyses have explored the biomechanics of running in those with PFP compared to healthy controls, the majority utilized only female runners or a mixed-sex sample, without considering of the effects of sex. As such, the effects of sex on the biomechanics of running in those with PFP are poorly understood [
12]. Willy et al. [
20] compared the biomechanics of running in male and female runners with PFP, and showed that females exhibited greater peak hip adduction compared to both males with PFP and male controls, whereas males with PFP ran with a greater peak knee adduction compared to symptomatic females and male controls. A drawback of this investigation was the lack of a female control group, and Neal et al. [
4] undertook the only investigation examining male and female runners with PFP in relation to asymptomatic controls of both sexes. Mixed-sex comparisons showed that PFP runners exhibited greater peak hip adduction compared to controls. Females with PFP demonstrated significantly greater peak hip adduction compared to controls, but there were no differences between males with PFP and male controls.
Previous analyses concerning the biomechanical differences between runners with PFP and asymptomatic controls have examined only joint kinematics, ground reaction forces, and surface electromyography. Significant advances have been made in musculoskeletal simulation models [
21], leading to the development of bespoke software allowing skeletal muscle forces to be simulated during movement and utilized as inputs to calculate lower extremity joint reaction forces [
22]. Such approaches have been used extensively in running, but only one study has explored differences between those with PFP and healthy controls. Besier et al. [
23] showed that medial gastrocnemius forces were significantly greater in PFP runners, which they speculated may cause greater joint contact loads in comparison to pain-free runners, although joint loading indices were not undertaken in this investigation. With the high incidence of PFP in runners [
5], associated with a poor long-term prognosis [
7], further investigation is warranted in order to better understand the biomechanical variables associated with PFP and the increased incidence of this pathology in female runners, so as to enhance the quality of future evidence-based preventative strategies for both sexes.
This investigation, via a retrospective case–control study design, aimed firstly to evaluate the biomechanics of running in a pooled-sex sample of runners with and without PFP using a musculoskeletal simulation-based approach. Secondly, using the same experimental approach, this investigation sought to explore differences between runners with PFP and asymptomatic controls, when these cohorts were divided into subset comparisons of males and females with and without PFP, in order to investigate distinctions in PFP presentation between the sexes.
4. Discussion
Using a retrospective case–control approach, this study evaluated running biomechanics in patients with and without PFP via a musculoskeletal simulation-based approach, and also investigated potential distinctions in PFP presentation between the sexes. This study represents the first exploration of the biomechanical parameters linked to the aetiology of PFP using musculoskeletal simulation, and may yield important clinical information for efforts towards the cessation of symptom initiation and the improvement of PFP management.
Notably, patellofemoral stress indices were statistically greater in the PFP group compared to controls. This supports the notion that, in runners, PFP is mediated by increased joint loading, and is consistent with the findings of Brechter and Powers [
50], who found enhanced patellofemoral joint stress in those with PFP, using a mixed sample. The subset analyses from this study importantly revealed that enhanced patellofemoral joint stress in PFP runners was driven by female sex, as no differences were evident in males. The female PFP group exhibited more pronounced and coherent differences in patellofemoral joint loading, importantly highlighting potential sex differences in PFP aetiology. This emphasizes the need for different treatment approaches in male and female runners, and management strategies seeking to reduce patellofemoral joint stress are likely to be most efficacious in female runners. Patellofemoral joint loading is primarily caused by forces generated within the quadriceps [
51]; therefore, enhanced patellofemoral joint stress in the female PFP group was mediated as a function of the corresponding increases in forces that were observed consistently across all four quadriceps muscles.
A significantly more anterior footstrike position was shown in the control group in relation to the PFP group, which when contextualized via the strike index, revealed a rearfoot strike in the PFP group and a midfoot pattern in controls. The subset analyses again showed that this was mediated by female runners, and the chi-squared analyses support this, as significantly more rearfoot strikers were shown in the overall and female PFP groups. Daoud et al. [
52] showed that runners who habitually adopt a rearfoot strike pattern are more than twice as likely to experience a chronic running injury. Crucially, this investigation lends further precision to this observation, as in female runners the utilization of a rearfoot strike pattern makes runners significantly more likely to experience PFP. It is likely that the increased quadriceps muscle forces and patellofemoral loading shown overall and in the female PFP group were mediated by the rearfoot strike pattern adopted in relation to control runners. Utilization of a rearfoot strike pattern places increased demands on the knee extensors [
53], and patellofemoral stress is greater in rearfoot strikers [
54]. From a clinical perspective, transitioning from a rearfoot strike pattern has been shown to attenuate patellofemoral joint loading and improve pain symptoms in male runners, although no such intervention has been undertaken in females [
25]. Therefore, gait-retraining approaches that allow female PFP runners to modify their habitual footstrike pattern may be a particularly important clinical intervention.
From a kinematic and temporal perspective, peak knee flexion and step length were lower in the PFP group, while knee flexion was lower in male symptomatic runners compared to females with PFP. Individuals with PFP experience reduced knee flexion [
55,
56], which along with the reductions in step length may represent an attempt to minimise pain symptoms by mediating patellofemoral stress [
49,
55]. Reduced knee flexion in both the overall PFP and male PFP runners may be indicative of kinesiophobia—a renowned complaint in patients with PFP [
10,
56]. Kinesiophobia is more severe in males with chronic musculoskeletal pain [
57,
58]; therefore, as knee bracing [
59] and exercise therapy [
60] have been shown to improve kinesiophobia in PFP, this suggests that there is scope for targeted interventions towards male symptomatic runners.
The overall and male and female subset comparisons showed that peak eversion was significantly greater in PFP runners. Rearfoot eversion has been linked to the aetiology of PFP by theoretical modelling analyses [
61], and Dierks et al. [
18] showed significantly greater eversion in PFP runners in a mixed sample—though this investigation is the first to show increased eversion in sex-specific subset analyses. From a clinical standpoint, it appears that strategies centred around reducing rearfoot eversion are important for the treatment of PFP in both male and female runners. Conservative modalities such as foot orthoses and ankle braces have been shown to mediate statistical reductions in peak ankle eversion in both male and female runners [
62,
63]. No analyses have been undertaken using ankle bracing; however, previous intervention studies have shown foot orthoses to be effective in treating PFP, with greater rearfoot eversion angles at baseline predicting orthotic efficacy [
64,
65].
This investigation also revealed, in the comparisons of the overall and male and female subsets, that contralateral pelvic drop ROM was significantly greater in PFP runners. This is consistent with the findings of Bramah et al. [
66]—who showed that injured runners demonstrated greater contralateral pelvic drop—and those of Willson and Davis [
19], who indicated that runners with PFP exhibited significantly greater contralateral pelvic drop. Enhanced contralateral pelvic drop negatively influences patellofemoral joint biomechanics by elongating the ipsilateral iliotibial band, generating a greater laterally directed force on the patella [
67,
68]. Increased contralateral pelvic drop during weight-bearing activities and in PFP patients is considered a clinical sign of diminished strength or neuromuscular function at the hip [
66], which results in diminished capacity to stabilize the pelvis. This investigation supports this notion, as forces in the muscles primarily involved in stabilizing the pelvis were found to be statistically greater in the control group across all of the aforementioned group comparisons. Importantly, real-time gait retraining has been shown to significantly attenuate contralateral pelvic drop and pain symptoms in runners with PFP, and hip strengthening is able to mediate statistical improvements in PFP pain symptoms [
69]. The findings from the current investigation importantly support the collective utilization of these intervention modalities in runners of both sexes.
The overall as well as the male and female comparisons showed that % contributions of the rectus femoris were consistently greater in PFP runners, and that the same was true in symptomatic male runners. This suggests that overutilization of the rectus femoris is a potentially important biomechanical mechanism in PFP, and can be used to differentiate between sexes in symptomatic runners. Although, the mechanistic influence of this finding relating to the aetiology of PFP is not known, it is nevertheless a potentially clinically meaningful neuromuscular observation that may aid in the management of PFP in runners of both sexes. Furthermore, the overall and subgroup comparisons of symptomatic runners showed an enhanced co-contraction ratio in control runners and symptomatic females. This observation contrasts with those of Besier et al. [
23], who found no differences between PFP runners and healthy controls during running, although this investigation utilized electromyography rather than muscle forces. Nevertheless, it is proposed that these observations are mediated as a function of the enhanced hamstring and reduced rectus femoris muscle forces that were evident in the above overall and subgroup comparisons. It remains unknown whether these alterations in muscle kinetics are adaptive in response to pain or if they are causative, but it can be speculated that increased co-contraction might enhance knee joint stability and benefit the position of the patella within the trochlear groove [
70].
In contrast to the observations of both Willy et al. [
20] and Neal et al. [
4], our findings showed that females with PFP did not exhibit a greater peak hip adduction angle compared to controls. However, in agreement with Willy et al. [
20], our results showed that female runners with PFP ran with statistically larger hip adduction in relation to symptomatic males. Previous intervention trials have shown that targeted gait retraining reduces peak hip adduction during running and improves pain and function in runners with PFP [
71]. The observations from this investigation suggest that these interventions are likely to be most effective in females, and the implementation of gait retraining to attenuate hip adduction in symptomatic female runners is encouraged. Taking into account the range of sex-specific differences in the biomechanics of running between symptomatic runners demonstrates sex-specificity in terms of PFP presentation, indicating that future clinical investigations should present aetiological data for both sexes, and that treatment modalities should also be correspondingly sex-specific.
As with any investigation, there are limitations to the current study, and the findings should be contextualized in line with these limitations. Firstly, the retrospective nature of the study design means that it is not possible to determine whether the biomechanical differences between symptomatic runners and healthy controls are adaptations in the presence of anterior knee pain, or if they are causative parameters. Owing to the expense and difficulty of undertaking analyses of this nature, there is a lack of prospective analyses identifying risk factors for PFP, so this is a clear avenue for future research. In addition, PFP is a multifactorial condition; therefore, although the current investigation explored a plethora of parameters using musculoskeletal simulation, it was beyond the scope of this study to determine the non-biomechanical risk factors that may be important to the aetiology of PFP. Future analyses should seek to investigate additional measurements that may be important to the aetiology and clinical management of PFP.