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Sports-Specific Illness and Injury: Section Articles

Development and Prevention of Running-Related Osteoarthritis

Ni, Guo-Xin MD, PhD

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Current Sports Medicine Reports: 9/10 2016 - Volume 15 - Issue 5 - p 342-349
doi: 10.1249/JSR.0000000000000294
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Abstract

Introduction

Because of its easy accessibility and low participation cost, running is becoming a prevalent activity in today’s health-conscious society. Running is well recognized to have a positive influence on an individual’s physical fitness and mood, as well as to reduce the incidence of obesity, cardiovascular disease, and many other chronic health problems. However, it also may cause injuries (29). More importantly, there is increasing concern that running may lead to osteoarthritis (OA) of lower limbs (16,37). Therefore, the benefits of participating in running need to be balanced against the risks of developing OA.

Although the association between running and OA has been investigated extensively, current evidence is insufficient to draw unequivocal conclusions (16,37). In addition to methodological issues associated with the assessment of joint structure and running programs, conflicting findings from those epidemiological studies also may be a result of individual variation in response to running (51). OA develops from a combination of joint vulnerability and joint loading (11). As such, there may be subgroups of individuals who differ in joint vulnerability and their responses to running. Some individuals may have specific characteristics that enable them to run without increasing their risk for OA, whereas others may require these individual factors and/or their running programs to be modified before they can commence or continue to run safely. In this review, the relation between running and OA was examined first, followed by exploring the effect of running on OA risk, as well as factors that may mediate such effect. Subsequently, a hypothesis is proposed for the cause of running-related OA. Finally, recommendations are provided to various individuals for safe running.

The Relation Between Running and OA

There are many difficulties to conducting and evaluating epidemiological studies exploring the association between running and OA, including the long time interval between exposure and outcomes, the large variability between individuals’ running patterns, innate predisposition to developing OA, and history of joint injuries (42). Nevertheless, a number of studies have examined the relationship between running and OA risk of lower limbs. Among them, some indeed suggested that running appears to increase OA risk (5,25,26,31,32,49), whereas others refuted a link between running and OA (3,13,37,57).

Not surprisingly, methodologic problems are common in these studies, including the lack of a control group (25), small sample size (25,32,37), potential selection bias by including only current runners (3), and the inability to randomly assign individuals to running and nonrunning groups (13,37,57). In addition, difficulty exists in reliably diagnosing OA (13,31,49) and in distinguishing between the effects of running and the presence of an injury (5,31). Indeed, these problems are, at least partially, responsible for the inconsistency in these studies. Therefore, further well-designed investigations are needed to clarify the relationship between running and the development of OA, as well as factors which may mediate this relationship. Nevertheless, these studies still can provide insight into such a relationship, and the following conclusions can be made:

  • The existing literature fails to support an association or causal relationship between low-level and moderate-level, or recreational running and OA.
  • Many factors have been associated with an increased risk of developing OA, including high-level or competitive running (5,31,49,54), increasing age (31,57), previous joint injury (5,25,26,32), and greater body mass index (BMI) (3,57).

General Effect of Running on Normal Joint Health

As a whole, running has many benefits to the body. It is well recognized that regular running is important for contributing to overall and musculoskeletal health. Ward et al. (55) used the Health Assessment Questionnaire Disability Index to measure physical disability of older individuals aged 50 yr or older and found that runners have less physical disability (49%) than their nonrunner counterparts (77%). Specific to joints of lower limbs, as noted above, moderate-level or recreational running is not likely detrimental to joint health.

Mechanical force has long been appreciated as a regulator of musculoskeletal tissues and may be the most important single environmental factor responsible for joint homeostasis. When considering the impact of running, a weight-bearing activity, on the joint tissues, there is a preponderant focus on cartilage because this pertains to OA. In addition to providing the articulating surface of synovial joints, one major function of articular cartilage is to transmit loading from one subchondral plate to the other. The biosynthetic activity of chondrocytes is responsive to mechanical stimuli and can alter the morphology and composition of cartilage (2). A biomechanical “window” has been suggested to maintain optimal cartilage homeostasis (36). Such concept also has been described by Dr. Scott Dye known as the “envelope of function” (8). Many animal (36) and human (2) studies demonstrated that physiological loading, induced by moderate-level or recreational running, can maintain the integrity of cartilage.

With the capability to directly visualize articular cartilage, magnetic resonance imaging (MRI) can provide a means to evaluate function in the intact human joint. Therefore, a few prospective studies have used MRI to assess the effect of running on articular cartilage. Krampla et al. (23) evaluated MRI on eight recreational long-distance runners before, immediately after, and 6 to 8 weeks after the Vienna City marathon. No new pathologic findings were found in six runners without major preexisting alterations. Later, seven of these athletes were followed up for 10 yr. Among them, six had no observable change in their MRI findings, and one had radiographic progression of arthrosis that was present 10 yr earlier (24). Many other studies (44) also largely confirmed that long-distance running causes neither edema in the medullar cavity nor joint effusion. These MRI studies suggest that, rather than detrimental effect, running may have a protective effect for healthy joints.

Nevertheless, running is usually considered a high-impact activity that can be hard on the knee/hip joint because impact forces during running can be as much as four to eight times higher than those during walking (52). Actually, the loading response of articular cartilage depends not only on the peak load but also on factors, such as the loading rate and duration (4), which should be considered when assessing knee OA risk and lower limb injury risk in general. A recent study compared knee joint loads between walking and running in healthy adults (33). Because of the relatively short duration of ground contact and the relatively long distance covered during a loading cycle, running in individuals with healthy knees does not induce per-unit-distance joint loads greater than those experienced during walking, which may offer a potential biomechanical explanation for why running does not seem to increase the risk of OA.

Running contributes to increased muscular strength, which can assist with distracting joint surfaces during running, controlling compressive forces on cartilage, and reducing the risk for injury (27). In addition, running can improve soft tissue extensibility, blood flow, and synovial fluid mobility, thus maintaining normal joint range of motion and providing essential nutrients to the cartilage matrix (15). Moreover, running is reported to promote weight loss directly, as well as attenuate middle-age weight gain (56). Although maintaining BMI within normal range significantly affects the risk of developing knee OA, the prevention of weight gain is an additional mechanism for limiting OA risk (57).

Factors Mediating the Relationship Between Running and OA Risk

OA develops from a combination of joint vulnerability and joint loading. In a review article, Felson (11) listed risk factors for OA disease separately as those increasing joint vulnerability (malalignment, muscle weakness, aging, etc.) and those that cause excessive loading (obesity, certain physical activities). Specific to running, many factors have been suggested to mediate its relationship with OA risk, as shown in the Table.

T1
Table:
Studies examining the effect of factors on the relationship between running and risk for developing OA.

High-Level or Competitive Running

It appears reasonable to conclude that there is a difference in the risk of OA between middle-level or recreational practice and high-level or competitive practice (28). To investigate if participation in sports increases the risk of developing OA of the hip, Vingård et al. (54) calculated relative risk (RR) according to a logistic regression analysis considering age, BMI, physical load from occupation, and different kinds of sports simultaneously. A lower RR of hip OA was revealed in those having practiced sport activities at middle level than those at high level. Specific to long distance running, the RR was 1.7 and 2.1, respectively. Among six studies suggesting a link between running and OA risk (5,25,26,31,32,49), four focused on ex-elite long-distance, or middle-distance runners (25,26,31,32,49). Even to nonelite runners (5), a significantly higher incidence of OA was found in men who were involved in high levels of walking or running.

One direct mechanism for the increased OA risk in high-level or elite runners may be due to the excessive running-induced loading. Although a closer examination is warranted, OA in high-level or competitive sport activities could be due to a threshold effect (47), which does not exist in recreational runners (17). Excessive mechanical stress can directly damage the cartilage extracellular matrix and shift the balance in chondrocytes to favor catabolic activity over anabolism, leading to the degradation of both collagen fibrils and proteoglycans. An animal study demonstrated that “strenuous” running may lead to OA-like changes of articular cartilage (36).

In addition, running at a high level may be linked with a higher incidence of joint injury, which may contribute to a higher risk of OA. Schueller-Weidekamm et al. (43) used MRI to evaluate the incidence of chronic knee changes in nonprofessional long-distance runners and found that the total score of all chronic knee lesions (including menisci lesion, cartilage lesion, and anterior cruciate ligament lesion) was significantly higher in high-trained runners (3.4 ± 2) than low-trained runners (1.8 ± 1.6).

When impacts are transmitted to the lower limb, normal strength and pace of periarticular muscular contraction may occur in correct time for protecting the joint. However, for elite runners, the high pain threshold (49) or the muscular fatigue could more or less inhibit proprioceptive reflexes and impair the subtle synchronization between the felt impact and the muscle response, probably leading to a higher risk for OA (28). Muscles can fatigue after repeated use and fail as dynamic stabilizers of the joint, leading to increased transarticular loading and joint injury. Hypothetically, muscles fatigued by a combination of long distance and fast running pace will have less ability to absorb shock transmitted to the skeleton, which over years of running might lead to increased wear and tear in weight-bearing joints. It is suggested that running pace tends to be associated with OA among ex-elite long-distance runners (31), but not among recreational runners (17). Besides, rapid acceleration of load does not allow sufficient time for the periarticular muscles, the major shock absorbers protecting the joint, to absorb the load (45).

Increasing Age

OA is a disease of aging, but age alone does not cause this disease. Rather, the vulnerabilities of a joint that occur as part of the aging process make it susceptible to this disease. Age-related changes in cartilage could increase the probability of tissue damage and decrease the ability of the tissue to repair damage. Furthermore, age-related changes in joint proprioception, joint capsules, ligaments, and muscle function also may contribute to the probability of articular cartilage damage from impact and torsional loading. Such changes may be reflected by the increased OA risk with increasing age in both recreational runners (57) and ex-elite runners (31).

After 30 min of running, Mosher et al. (34) reported a significantly smaller deformation of femoral and tibial cartilage in the older subjects. The increased stiffness of collagen matrix observed in older individuals would make the fibrils more prone to fatigue failure (7). Furthermore, aging may change kinematic and ground reaction force data during running. During running trials, older women produced significantly higher peak rearfoot eversion, knee internal rotation, external adductor moment, and loading rate of ground reaction force compared with their younger counterparts, suggesting relatively poor shock absorbency. High loading rates also can be harmful to the joint, if magnitudes exceed the physiologic tolerance level for an individual. Such running gait would make older female runners at higher risk of developing OA.

Joint Injury

In a review article (6), Conaghan suggested that the increased risk of lower limb OA in participants of repetitive and high impact sports is strongly associated with joint injury, such as ligament tears and meniscal injuries in the knee and fractures involving articular surfaces. Cheng et al. (5) reported a positive association between high-level running and the incidence of hip or knee OA in younger men but not in older men, probably because of a greater incidence of injury in younger individuals. Some researchers used MRI technique to explore the effect of marathon running on knee structures and found that no negative long-term effects were experienced in healthy individuals, and predisposing injury might be a predisposing risk for OA, triggered by the stress of long-distance running (23,24).

A number of studies demonstrated that the increased incidence of knee OA in the runners may be attributed to a higher incidence of knee injuries (25,26,32). Hootman et al. (17) pointed out that previous joint injury is a biologically plausible effect modifier of running-OA relationship because of the effects of injury on several potential mediators of cartilage degeneration, including secondary muscular weakness, joint asymmetry, biomechanical malalignments, ligamentous instability, and neurological deficits. These consequences may prevent normal distribution of compressive force and increased shear force on the articular surface. Some regions of articular surface experience higher peak loading, whereas others are minimally impacted. These abnormal loading patterns, coupled with impaired muscle function to absorb force, result in degenerative changes of the joint. The associated muscle dysfunction with injury leads to recurrent articular cartilage damage because the impact forces are no longer being absorbed appropriately (45). It was suggested that the loading rate of impact force is significantly greater among a group of previously injured runners compared with injury-free runners (18). Radin et al. (40) further found that the high rates of loading (knee pain group vs normal group: 67.6 vs 47.9 body weight [BW]/s) are significantly associated with levels of knee pain.

Joint Malalignment

As a local factor, joint malalignment increases joint vulnerability. McDermott and Freyne (32) reported 30% prevalence of radiographic knee OA in the runners complaining of knee pain and suggested a significant association between degenerative changes and both the presence of genu varum and the history of knee injury. In persons with normal joint mechanics and neuromuscular function, running-induced joint loading can be distributed over the entire articular surface and absorbed by muscle forces and therefore may not cause injury. By contrast, in those with joint malalignment, high-impact loading from running may increase articular contact stress and cause running-induced degeneration (1). It was recognized that the location of contact points within the joint during loading could be a key factor in the development of cartilage lesion. Although the knee malalignment itself may be a problem, the mechanism underlying pain onset and lesion formation may be the unaccustomed loading on areas of the articular cartilage that may not be adapted to accommodate it (39,48).

BMI

High BMI is a well-recognized risk factor for OA (12). Many studies confirmed that BMI can modify the relationship between running and OA risk (3,57). In a prospective study suggesting that long-distance running among healthy older individuals was not associated with accelerated radiographic knee OA, higher initial BMI was associated with worse radiographic OA at the final assessment (3). In a recent study with a large number of runners, Williams (57) found that the average risk for hip OA increased 5.0% per kilogram per square meter increase in BMI, and adjustment for BMI substantially diminished the risk reduction from 16.5% to 8.6% for OA. Nevertheless, it seems that BMI does not modify the relationship between running and risk of OA for those relatively lean participants (17).

Clearly, high BMI means greater loading on joints of lower limbs. Every pound of excess weight is multiplied three-fold to six-fold in terms of its effect on the loading (10). Excessive loading may lead to articular cartilage damage. In addition to greater loading, the added weight means that muscles must absorb even more force and therefore must be stronger and have greater endurance, though it is unknown of how much force to offset the negative effect of excessive loading. Unfortunately, individuals with a high BMI are usually associated with physical inactivity and therefore relative muscle dysfunction (9). Such “relative muscle dysfunction” in obese/overweight runners may explain their high OA risk (47).

Cause of Running-Related OA

Although it is well recognized that, under certain circumstances, running appears to increase OA risk, the cause of running-related OA is still no fully understood. Many health care professionals believe that the major cause of exercise-related OA is “wear and tear”—that is, gradual thinning of the articular cartilage because of repeated weight-bearing activity (53). This hypothesis predicts that any type of impact would increase OA, or worsen it, once developed. However, as stated earlier, only under certain circumstances can running increase OA risk. Recreational running does not increase the risk of OA, or is even beneficial to cartilage health. Clearly, the “wear and tear” hypothesis alone cannot explain the running-related OA. Shrier (47) thought OA in high-level or elite runners could be due to a threshold effect, and “wear and tear” only occurs after a threshold.

In 1999, Hurley (19) proposed that properly contracting muscles are the main force absorber for the joint, and that muscle dysfunction is the most important modifiable mediating factor for primary OA. Later, Shrier (47) provided additional literature to support the contention that muscle dysfunction is the primary cause of exercise-related OA. Muscle sensorimotor dysfunction may impair neuromuscular protective reflexes and shock absorption capacity. This could cause excessive, rapid, jarring joint loading during exercise, which is associated with OA pathogenesis (20). Nevertheless, in addition to muscle, many other tissues, such as tendons, ligaments, joint capsule, and mechanoreceptors, also are responsible for protecting cartilage from injury during daily activities. OA often occurs slowly and is attributable not just to failure of one joint protector, but the failure of several in combination. Hence, as a multifactorial disease, one mechanism alone might not fully explain the complex interaction between mechanical and neuromuscular factors in contributing to developing OA.

As noted above, with regard to running-related OA, factors often implicated in the development of OA comprise those that increase joint vulnerability (including increasing age, previous joint injury, joint malalignment, etc.) and those which increase joint loading (including obesity and high-level running). Therefore, it appears that running-related OA is a combined result of joint vulnerability and joint loading. Current evidence has demonstrated that moderate-level or recreational running is not likely detrimental or even beneficial to the integrity of healthy joint. Not surprisingly, with moderate loading, running-related OA is unlikely to develop on healthy joints (Fig.A). However, high-level or competitive running would increase joint loading, thus leading to an increased OA risk even for a healthy joint (Fig.B). On the other hand, joint vulnerability is increased under such conditions as increasing age, previous joint injury, joint malalignment, and so on. If a vulnerable joint is not loaded frequently and is only gently loaded when in use, OA does not necessarily develop. However, depending on the degree of joint vulnerability, moderate loading (recreational running and normal weight) may put vulnerable joints at risk for disease development (Fig.C). One feature of the vulnerable joint is cartilage unable to respond to healthy loading with matrix synthesis. In this setting, cartilage loss can occur with loading, and that can propel the disease process. Hence, if a vulnerable joint is loaded excessively, OA quite likely develops (Fig.D).

F1
Figure:
Schematic showing factors influencing the balance between joint vulnerability and joint loading. OA develops from a combination of joint vulnerability and joint loading (A). Moderate-level or recreational running is not likely detrimental, or even beneficial to the integrity of healthy joint. Under this circumstance, joint loading and joint vulnerability are in balance (B). However, high-level or competitive running and/or obesity would increase joint loading, thus leading to an increased OA risk even for healthy joint (C). On the other hand, joint vulnerability is increased under many conditions, such as increasing age, previous joint injury, joint malalignment, etc. Moderate loading (recreational running and normal weight) may put vulnerable joints at risk for disease development (D). Once a vulnerable joint is loaded excessively, OA quite likely develops (E).

Recommendations for Safe Participation in Running and Prevention of OA

Running-related OA appears to be a combined result of joint vulnerability and joint loading. A number of factors may increase joint vulnerability and/or cause excessive loading, thus leading to an increase in OA risk. Efforts should be made to identify those with joint vulnerability and joint loading, and measures should be taken to have those factors and/or their running programs modified before commencing or continuing to run safely.

Because people who have participated in high-level or competitive running appear to be at some risk of developing OA under certain circumstances, it is recommended to perform moderate-level running within the limits of comfort. According to the conditioning hypothesis proposed by Seedhom (46), the threshold at which cartilage fails is regulated by the prevalent stresses arising in a joint. A gradual increase in the level of running is therefore recommended. This is for individuals who intend to change from a sedentary lifestyle to an athletic one, or run from a lower level to a higher level. Luke et al. (30) reported elevated T1rho and T2 values in cartilage of early marathon runners after a marathon and elevated T1rho values after 3 months of reduced activity, suggesting the knee joint is at higher risk for degeneration. On the contrary, Kessler et al. (21) demonstrated that no differences in cartilage volume were found after running a marathon for those experienced runners. These findings highlight the importance of gradual increase in the level of running.

With aging, the vulnerabilities of a joint may occur and make it susceptible to OA. Therefore, a regular runner should lower his/her running level as he/she is getting older. Additionally, the higher value loading rate of ground reaction force in older individual suggests a relatively poor shock absorbency. It has been shown that rapid acceleration of load does not allow sufficient time for the periarticular muscles, the major shock absorbers protecting the joint, to absorb the load (45). In this regard, shoe cushioning is quite important for the older runner.

In a recent systematic review with only prospective cohort studies that studied risk factors for running-related injuries, 60 different predictive factors were investigated. The main risk factor was found to be previous injuries, usually in the past 12 months, reported in 62% of the articles that investigated this factor. Previous injury is usually associated with the development of a new injury or a similar injury of greater magnitude (41). Obviously, avoiding injuries is an important measure for reducing OA risk. Measures for this purpose include maintaining or improving muscle strength and tone, general fitness use of appropriate protective and playing equipment, adequate warm-up/cool-down, and education of runners. In the event of a sports injury, appropriate diagnosis, treatment and rehabilitation after injury should decrease the risk of subsequent joint OA (42). It is recommended to return to running slowly, lower the running level, or possibly wear a knee brace to provide joint stability and reduce the risk of meniscal damage. Rehabilitation programs currently recommended by physicians aim to restore muscular strength, power, endurance, flexibility, proprioception, and agility (22). It also is suggested to use a knee brace specifically for individuals with malalignment because it can alter knee joint loads through a combination of mechanisms (35).

As for an overweight/obese runner, it is advised to alternate running and non–weight-bearing activities, include muscle strengthening and flexibility exercises in an exercise program, promote a slow progression of running level, as well as teach and practice joint protection strategies (17). Weight loss appears to be crucial to lower the risk of disease. Higher-intensity exercise is suggested to promote a greater rate of fat burning. Unfortunately, it becomes difficult for people who are overweight to achieve, let alone sustain, the recommended levels of exercise. Lower body positive pressure partial body weight support may be an alternation, which allows the overweight individual to experience their preferred body weight as well as achieve meaningful calorie expenditure (14). Patil et al. (38) demonstrated that the lower body positive pressure treadmill allowed for a controlled decrease of the knee forces. This technology was even used safely and effectively on overweight knee OA patients to simulate weight loss and reduce acute knee pain during weight-bearing exercise (50).

Conclusions and Future Directions

Many competitive athletes, and an increasing number of the general population, often question whether participation in a running program increases their risk of developing OA. In the literature, studies investigating the effect of running on risk for developing OA at weight-bearing joints have reported with conflicting results (16,37), which are likely due to the existence of subgroups of individuals who differ in their response to running (51), as well as methodological issues associated with the assessment of joint structure and running programs (5,13,31,49). As such, a more comprehensive examination of joint structure and the implementation of objective and accurate assessments of running programs may enhance our understanding of the effect of running on knee/hip joint health with different parameters.

More importantly, addressing these methodological issues will allow studies to explore the role of biophysical factors within an individual that may influence the effect of running on risk for OA (51). It is suggested that factors, such as age, body mass, and previous knee injury, may influence knee/hip joint health in runners. There also are many other factors contributing to joint vulnerability (11). However, the causal relationships between these factors and the risk of OA are either unknown or speculative. Further research is needed to validate any causal relationship. A clear understanding of the implications of these risk factors should increase awareness in both competitive athletes and general population of the risks associated with running-related OA. Early identification of individuals at risk for OA provides an opportunity for interventions to modify risk factor or running program.

In this review, we propose that running-related OA is caused by a combination of joint vulnerability and joint loading, and subsequently, make some recommendations for safe running. Rather than a uniform approach to the implementation of running, it is suggested that running has different effects on different people and that individually tailored running programs are needed to allow running to commence safely. However, whether those prevention measures work effectively or not needs to be validated in the future.

The author declares no conflict of interest.

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