counterparts without OA (Table 4).

**Study**

**PVF (BW)** 1.047 (0.077) 1.048 (0.05)

**Loading Rate (%BW/s)** 9.26 (3.46) 20.61 (2.34) 8.33 (1.44)

adduction moment.

and Radiographic Disease Severity in Knee Osteoarthritis 161

**Velocity (m/s)** 1.123 (0.190) 1.504 (0.301) **Stride Frequency** 0.903 (0.086) 1.111 (0.122) **Stride Length (m)** 1.193 (0.172) 1.374 (0.221) **Support Time (%)** 63.17 (3.37) 60.77 (3.77) **KROM (degrees)** 57.85 (9.36) 59.64(8.58) **PVF (BW)** 1.047 (0.077) 1.154 (0.126) **KAM(%BW\*HT)** 0.367(0.200) 0.380 (0.197) **Loading Rate (%BW/s)** 9.26 (3.46) 15.11 (7.47) **Time to Peak (s)** 0.204 (0.056) 0.137 (0.035) Table 2. Gait mechanics at self selected normal and fast speeds. All values are mean (SD). KROM: knee range of motion; PVF: peak vertical ground reaction force; KAM: knee

**Variable Normal Speed Fast Speed**

**Messier 1992**

**Velocity (m/s)** 1.123 (0.190) 1.097 (0.359) 1.090 (0.11)

**KROM (degrees)** 57.85 (9.36) 54.00 (7.00)

**KAM(%BW\*HT)** 0.367(0.20) 0.150 (0.03) 0.39 (0.28)

Table 3. Comparison of the gait mechanics from the current study, at a normal self-selected walking speed, to data from the literature (Kaufman et al., 2001; Messier et al., 1992; Zeni & Higginson, 2010). All values are mean (SD). KROM: knee range of motion; PVF: peak

**Velocity (m/s)** 1.123 (0.190) ↓ 1.296 (0.084)\* 1.17 (0.14)

**KROM (degrees)** 57.85 (9.36) 60.0 (4.0) **KAM (%BW\*HT)** 0.367(0.200) 0.360 (0.36)

Table 4. Comparison of gait mechanics of OA patients at a normal self-selected walking speed to control subject data from the literature (Kaufman et al., 2001; Messier et al., 2005a). All values are mean (SD). KROM: knee range of motion; PVF: peak vertical ground reaction force; KAM: knee adduction moment. Statistically significant differencs: † denotes p<0.05, \*

OA patients in this study walked slower, had a shorter stride length, smaller knee range of motion, spent more time in the support phase and had a smaller loading rate than their

**Variable Current Study Messier, 2005 Kaufman, 2001**

**Zeni 2009**

**Kaufman 2001**

Pearson's correlation coefficient (r), and significance level was adjusted accordingly to p<0.005 (Bonferroni's adjustment). This analysis was performed at each speed (normal and fast). A 1x3 analysis of variance was used to compare means for velocity and knee range of motion for the different levels of radiographic disease severity at each speed (α=0.05). Since it has been reported that support time is influenced by walking speed (Andriacchi et al., 1977), a 1x3 analysis of covariance was used to compare means for support time for the different levels of radiographic disease severity at each speed (α=0.05). Since previous research has also determined that the magnitude of the vertical ground reaction force is affected by walking speed (Andriacchi et al., 1977), means for peak vertical ground reaction force, loading rate, and time to peak were compared to level of radiographic disease severity at each speed level using an analysis of covariance as well. Post-hoc testing (LSD) was performed when necessary.

#### **3. Results**

Descriptive statistics for subject demographics are presented in Table 1 and gait characteristics for the OA subjects at both speeds are given in Table 2. Demographics and gait mechanics were characteristic of a population of overweight OA patients with varying degrees of radiographic severity (Table 3).

Table 1. Descriptive Statistics for Subject Demographics. BMI: Body Mass Index.

Pearson's correlation coefficient (r), and significance level was adjusted accordingly to p<0.005 (Bonferroni's adjustment). This analysis was performed at each speed (normal and fast). A 1x3 analysis of variance was used to compare means for velocity and knee range of motion for the different levels of radiographic disease severity at each speed (α=0.05). Since it has been reported that support time is influenced by walking speed (Andriacchi et al., 1977), a 1x3 analysis of covariance was used to compare means for support time for the different levels of radiographic disease severity at each speed (α=0.05). Since previous research has also determined that the magnitude of the vertical ground reaction force is affected by walking speed (Andriacchi et al., 1977), means for peak vertical ground reaction force, loading rate, and time to peak were compared to level of radiographic disease severity at each speed level using an analysis of covariance as well. Post-hoc testing (LSD)

Descriptive statistics for subject demographics are presented in Table 1 and gait characteristics for the OA subjects at both speeds are given in Table 2. Demographics and gait mechanics were characteristic of a population of overweight OA patients with varying

**Variable Mean (SD) % (n)**

**Female** 76 (143) **Male** 24 (46)

**Black** 35 (66) **White** 63 (119) **Other** 2 (4)

**Mild** 12 (23) **Moderate** 61 (116) **Severe** 27 (50)

Table 1. Descriptive Statistics for Subject Demographics. BMI: Body Mass Index.

was performed when necessary.

degrees of radiographic severity (Table 3).

**Age (years)** 58.54 (9.72) **Height (m)** 1.67 (0.081) **Weight (kg)** 94.74 (16.22) **BMI (kg/m2)** 34.17 (4.36)

**3. Results**

**Sex:**

**Race:**

**Disease severity:**

Table 2. Gait mechanics at self selected normal and fast speeds. All values are mean (SD). KROM: knee range of motion; PVF: peak vertical ground reaction force; KAM: knee adduction moment.

Table 3. Comparison of the gait mechanics from the current study, at a normal self-selected walking speed, to data from the literature (Kaufman et al., 2001; Messier et al., 1992; Zeni & Higginson, 2010). All values are mean (SD). KROM: knee range of motion; PVF: peak vertical ground reaction force; KAM: knee adduction moment.

Table 4. Comparison of gait mechanics of OA patients at a normal self-selected walking speed to control subject data from the literature (Kaufman et al., 2001; Messier et al., 2005a). All values are mean (SD). KROM: knee range of motion; PVF: peak vertical ground reaction force; KAM: knee adduction moment. Statistically significant differencs: † denotes p<0.05, \* denotes p<0.005 and denotes ‡ p<0.0001. \*\*For support time: p<0.06

OA patients in this study walked slower, had a shorter stride length, smaller knee range of motion, spent more time in the support phase and had a smaller loading rate than their counterparts without OA (Table 4).

The Relationship Between Gait Mechanics

and Radiographic Disease Severity in Knee Osteoarthritis 163

#, \*

**#, \***

**#, #, \* \***

Fig. 1. Analysis of variance results for velocity (# denotes a significant difference from mild

Fig. 2. Analysis of variance results for knee range of motion. # denotes significant difference

from mild OA, **\*** denotes significant difference from moderate OA

OA and **\*** denotes significant difference from moderate OA)

**#, \***

#### **3.1 Correlations**

None of the spatiotemporal variables showed a strong correlation with radiographic disease severity. However, a few variables had a weak statistically significant correlation with K/L grade (Table 4). Knee range of motion (KROM) was inversely correlated with radiographic disease severity (p<0.001) at both self selected speeds and peak vertical ground reaction force was inversely correlated with radiographic disease severity (p<0.005) at both speeds. Stated another way, subjects in this study with more severe radiographic disease severity walked with a smaller knee range of motion and had smaller ground reaction forces than their counterparts with less severe radiographic disease severity.

Table 5. Correlations of radiographic disease severity with gait data. All correlations were significant (p<0.005)\* and (p<0.001) †. KROM: knee range of motion; PVF: peak vertical ground reaction force.

#### **3.2 Analysis of variance**

The results of the analysis of variance for velocity by level of radiographic disease severity (Figure 1) demonstrated that there was a significant difference in walking velocity between mild and severe OA and moderate and severe OA at the fast speed. There were no significant differences in mean walking velocity by severity level at the normal walking speed. Differences in mean knee range of motion and mean peak vertical ground reaction force by level of OA severity existed at both speeds (Figures 2 and 3). Patients with severe OA had the smallest knee range of motion and the smallest peak vertical ground reaction force in all instances. The statistical analysis revealed significant differences in knee range of motion between patients with mild and severe OA at the normal and fast speeds as well as moderate and severe OA at the normal and fast speeds (Figure 2). The analysis of variance for stride length did not show any differences by OA severity level at either speed.

The results of the analyses of covariance for support time, knee adduction moment and loading rate did not reveal any significant differences between the different levels of radiographic disease severity at either speed. While not significantly different from the other groups, patients with moderate OA spent the least amount of time in the support phase of the gait cycle at the normal walking speed. At the fast speed, the more severe the level of OA, the more time spent in support. While these differences were not statistically significant, loading rate at the normal self selected speed was greater in patients with mild OA and decreased with increasing level of OA. At the fast speed, variation in loading rate by OA severity was inconsistent. Again, while not significantly different, mean knee adduction moment decreased with increasing radiographic severity at the normal walking speed and it increased with increasing radiographic severity at the fast speed. The analysis of covariance for peak vertical ground reaction force (Figure 3) determined that there was a statistically significant difference between moderate and mild OA and moderate and severe OA at the fast speed. Statistically significant differences in mean peak vertical ground reaction force also existed between the levels of radiographic OA at the normal speed.

The analysis of covariance for the time to peak vertical reaction force (Figure 4) did not reveal any differences in time to peak for the different levels of radiographic disease severity.

None of the spatiotemporal variables showed a strong correlation with radiographic disease severity. However, a few variables had a weak statistically significant correlation with K/L grade (Table 4). Knee range of motion (KROM) was inversely correlated with radiographic disease severity (p<0.001) at both self selected speeds and peak vertical ground reaction force was inversely correlated with radiographic disease severity (p<0.005) at both speeds. Stated another way, subjects in this study with more severe radiographic disease severity walked with a smaller knee range of motion and had smaller ground reaction forces than

**Variable Normal Speed Fast Speed**

The results of the analysis of variance for velocity by level of radiographic disease severity (Figure 1) demonstrated that there was a significant difference in walking velocity between mild and severe OA and moderate and severe OA at the fast speed. There were no significant differences in mean walking velocity by severity level at the normal walking speed. Differences in mean knee range of motion and mean peak vertical ground reaction force by level of OA severity existed at both speeds (Figures 2 and 3). Patients with severe OA had the smallest knee range of motion and the smallest peak vertical ground reaction force in all instances. The statistical analysis revealed significant differences in knee range of motion between patients with mild and severe OA at the normal and fast speeds as well as moderate and severe OA at the normal and fast speeds (Figure 2). The analysis of variance

for stride length did not show any differences by OA severity level at either speed.

any differences in time to peak for the different levels of radiographic disease severity.

The results of the analyses of covariance for support time, knee adduction moment and loading rate did not reveal any significant differences between the different levels of radiographic disease severity at either speed. While not significantly different from the other groups, patients with moderate OA spent the least amount of time in the support phase of the gait cycle at the normal walking speed. At the fast speed, the more severe the level of OA, the more time spent in support. While these differences were not statistically significant, loading rate at the normal self selected speed was greater in patients with mild OA and decreased with increasing level of OA. At the fast speed, variation in loading rate by OA severity was inconsistent. Again, while not significantly different, mean knee adduction moment decreased with increasing radiographic severity at the normal walking speed and it increased with increasing radiographic severity at the fast speed. The analysis of covariance for peak vertical ground reaction force (Figure 3) determined that there was a statistically significant difference between moderate and mild OA and moderate and severe OA at the fast speed. Statistically significant differences in mean peak vertical ground reaction force also existed between the levels of radiographic OA at the normal speed. The analysis of covariance for the time to peak vertical reaction force (Figure 4) did not reveal

**KROM (degrees)** r = -0.306† r = -0.307† **PVF (% BW)** r = -0.240\* r = -0.230\* Table 5. Correlations of radiographic disease severity with gait data. All correlations were significant (p<0.005)\* and (p<0.001) †. KROM: knee range of motion; PVF: peak vertical

their counterparts with less severe radiographic disease severity.

**3.1 Correlations**

ground reaction force.

**3.2 Analysis of variance**

Fig. 1. Analysis of variance results for velocity (# denotes a significant difference from mild OA and **\*** denotes significant difference from moderate OA)

Fig. 2. Analysis of variance results for knee range of motion. # denotes significant difference from mild OA, **\*** denotes significant difference from moderate OA

164 Principles of Osteoarthritis – Its Definition, Character, Derivation and Modality-Related Recognition

The Relationship Between Gait Mechanics

**4. Discussion**

characteristics.

their limbs less.

OA disease.

independent of walking speed.

and Radiographic Disease Severity in Knee Osteoarthritis 165

Given the conflicting results of previous studies, the purpose of this study was to further examine the relationship between radiographic disease severity and gait patterns in persons with knee OA by not only looking at radiographic grade, but by looking at gait patterns in subjects grouped by severity level. This study expanded on previous work by investigating differences in gait mechanics across all levels of radiographic severity (mild, moderate, and severe). The current study investigated joint mechanics, as well as spatiotemporal gait

It was predicted that more severe levels of knee OA would correlate positively with increased gait disability measured through slower walking velocity, shorter strides, lower peak vertical forces, greater knee adduction moments, smaller loading rates and a more limited knee range of motion. The results showed that four of these measures of gait disability differed significantly in patient groups having different levels of radiographic disease severity. It was further hypothesized that significant differences in gait mechanics would exist between the three radiographic disease severity levels, even after controlling for speed. This hypothesis was supported in that both peak vertical ground reaction force and time to peak vertical ground reaction force varied with radiographic disease severity

The gait biomechanics of the subjects in this study are consistent with previous reports. OA patients had a shorter stride length, slower walking velocity, lower stride frequency, a longer support time, and smaller loading rate than their counterparts without OA (Al-Zahrani & Bakheit, 2002; Brinkmann & Perry, 1985; Messier et al., 2005a; Messier et al., 1992). Furthermore, mean peak knee adduction moment and mean KROM were consistent with previous reported values in persons with OA (Baliunas et al., 2002; Kaufman et al., 2001; Messier et al., 2005a; Messier et al., 1992). When broken down by radiographic severity, subjects with more severe OA walked more slowly, with stiffer knees and loaded

Knee OA is the most common cause of disability in community dwelling elderly adults (Guccione et al., 1994) and these altered gait mechanics can potentially influence progression of OA and quality of life. For example, the typical mean walking speed for adults is 1.3 m/s and in general a reduction in walking velocity by 12% has clinical significance. The mean walking velocity in this study at the normal speed is at about a 14% reduction and for the patients with severe OA it is a 21% reduction. Given the increase in gait disability with increased OA severity found in this study, patients with severe radiographic disease may be unable to easily execute activities of daily living such as ambulation, and they may also be unable to complete the physical activities prescribed as part of the treatment plan for their

As others studies have reported (Nebel et al., 2009; White et al., 2010; Wilson et al., 2011), the present study found that there was only a modest relationship between K/L grade and gait mechanics. Knee range of motion and peak vertical ground reaction force was inversely correlated with radiographic disease severity at both speeds. Each of these variables, as well as velocity, stride frequency, loading rate, knee adduction moment and time to peak vertical ground reaction force, were also examined by level of severity. Statistically significant differences were seen in four of these gait variables. As predicted, patients with severe OA had the smallest knee range of motion and the smallest peak vertical ground reaction force at both speeds. The influence of radiographic disease

Fig. 3. Analysis of covariance results for peak vertical ground reaction force; # denotes significant difference from mild OA and **\*** denotes significant difference from moderate OA

Fig. 4. Analysis of covariance results for time to peak vertical ground reaction force; # denotes a significant difference from moderate OA at the normal speed, however at the fast speed there was a significant difference between mild and moderate and moderate and severe levels of radiographic disease severity.

### **4. Discussion**

164 Principles of Osteoarthritis – Its Definition, Character, Derivation and Modality-Related Recognition

Fig. 3. Analysis of covariance results for peak vertical ground reaction force; # denotes significant difference from mild OA and **\*** denotes significant difference from moderate OA

**#, \***

**# #**

**#, \***

Fig. 4. Analysis of covariance results for time to peak vertical ground reaction force; # denotes a significant difference from moderate OA at the normal speed, however at the fast speed there was a significant difference between mild and moderate and moderate and

severe levels of radiographic disease severity.

Given the conflicting results of previous studies, the purpose of this study was to further examine the relationship between radiographic disease severity and gait patterns in persons with knee OA by not only looking at radiographic grade, but by looking at gait patterns in subjects grouped by severity level. This study expanded on previous work by investigating differences in gait mechanics across all levels of radiographic severity (mild, moderate, and severe). The current study investigated joint mechanics, as well as spatiotemporal gait characteristics.

It was predicted that more severe levels of knee OA would correlate positively with increased gait disability measured through slower walking velocity, shorter strides, lower peak vertical forces, greater knee adduction moments, smaller loading rates and a more limited knee range of motion. The results showed that four of these measures of gait disability differed significantly in patient groups having different levels of radiographic disease severity. It was further hypothesized that significant differences in gait mechanics would exist between the three radiographic disease severity levels, even after controlling for speed. This hypothesis was supported in that both peak vertical ground reaction force and time to peak vertical ground reaction force varied with radiographic disease severity independent of walking speed.

The gait biomechanics of the subjects in this study are consistent with previous reports. OA patients had a shorter stride length, slower walking velocity, lower stride frequency, a longer support time, and smaller loading rate than their counterparts without OA (Al-Zahrani & Bakheit, 2002; Brinkmann & Perry, 1985; Messier et al., 2005a; Messier et al., 1992). Furthermore, mean peak knee adduction moment and mean KROM were consistent with previous reported values in persons with OA (Baliunas et al., 2002; Kaufman et al., 2001; Messier et al., 2005a; Messier et al., 1992). When broken down by radiographic severity, subjects with more severe OA walked more slowly, with stiffer knees and loaded their limbs less.

Knee OA is the most common cause of disability in community dwelling elderly adults (Guccione et al., 1994) and these altered gait mechanics can potentially influence progression of OA and quality of life. For example, the typical mean walking speed for adults is 1.3 m/s and in general a reduction in walking velocity by 12% has clinical significance. The mean walking velocity in this study at the normal speed is at about a 14% reduction and for the patients with severe OA it is a 21% reduction. Given the increase in gait disability with increased OA severity found in this study, patients with severe radiographic disease may be unable to easily execute activities of daily living such as ambulation, and they may also be unable to complete the physical activities prescribed as part of the treatment plan for their OA disease.

As others studies have reported (Nebel et al., 2009; White et al., 2010; Wilson et al., 2011), the present study found that there was only a modest relationship between K/L grade and gait mechanics. Knee range of motion and peak vertical ground reaction force was inversely correlated with radiographic disease severity at both speeds. Each of these variables, as well as velocity, stride frequency, loading rate, knee adduction moment and time to peak vertical ground reaction force, were also examined by level of severity. Statistically significant differences were seen in four of these gait variables. As predicted, patients with severe OA had the smallest knee range of motion and the smallest peak vertical ground reaction force at both speeds. The influence of radiographic disease

The Relationship Between Gait Mechanics

gait mechanics within each severity group.

**6. Acknowledgements**

AR50245 and AG15768.

3373.

280.

**7. References**

might be beneficial.

**5. Conclusion**

and Radiographic Disease Severity in Knee Osteoarthritis 167

catastrophizing explained a significant amount of variance in walking velocity and that pain catastrophizing was a significant individual predictor of walking velocity (Somers et al., 2009). Thus further investigation of the influence of pain and pain cognitions on the relationship between OA severity and additional gait variables (knee range of motion, peak vertical ground reaction force, and time to peak vertical ground reaction force),

The purpose of this study was to examine the relationship between radiographic disease severity and gait patterns in persons with knee OA by looking at gait mechanics and joint loading in subjects across all severity levels. The results indicate that variation in gait could not be fully explained by K/L grade; although, when K/L grade was used to form different levels of radiographic disease severity, significant differences did exist. The results showed that significant differences existed in peak vertical ground reaction force and time to peak vertical ground reaction force by level of radiographic severity, even after controlling for walking speed. This study continues to point to osteoarthritis of the knee as a multifactorial disease. While radiographic disease severity is related to changes in gait biomechanics, the aberrant gait patterns could be a combination of radiographic disease severity and the pain experienced at a given severity. It may even be related to a combination of pain cognitions and radiographic disease severity. The authors suggest that future work should be done to look at the influence of pain and pain related fear of movement or other pain cognitions on

The authors would like to thank Sarah Jaffe, Dr. Mary Beth Nebel, Alicia Abbey, and Bryan Gibson for their contributions to this work. This research was supported by NIH grants

Addison, S., Coleman, R., S Feng, McDaniel, G., & Kraus, V. (2009). Whole-body bone

Al-Zahrani, K.S., & Bakheit, A.M.O. (2002). A study of the gait characteristics of patients

Altman, R., Asch, E., Bloch, D., Bole, G., Borenstein, D., Brandt, K., Christy, W., Cooke, T.D.,

scintigraphy provides a measure of the total-body burden of osteoarthritis for the purpose of systemic biomarker validation. *Arthritis and Rheumatism, 60*(11), 3366-

with chronic osteoarthritis of the knee. *Disability and rehabilitation, 24*(5), 275-

Greenwald, R., Hochberg, M., Howell, D., Kaplan, D., Koopman, W., Longley III, S., Mankin, H., McShane, D.J., Medsger Jr, T., Meenan, R., Mikkelsen, W., Moskowitz, R., Murphy, W., Rothschild, B., Segal, M., Sokoloff, L., & Wolfe, F. (1986). Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria

severity on knee range of motion is understandable given that severe erosion of cartilage and presence of osteophytes as well as joint space narrowing could limit knee range of motion (Holla et al., 2011). It was expected that patients with severe OA would not load their limbs as much and load them more slowly to alleviate pain. Peak vertical ground reaction force decreased with increasing OA severity at both speeds. This alteration in gait mechanics is consistent with the notion that patients are seeking to reduce loading at the knee. Finally, time to peak vertical GRF was greatest in patients with moderate OA; the differences were statistically significant at the fast speed. It is important to note that, in this study, differences related to peak vertical ground reaction force were not a function of slower walking speed. This is in contrast to previous work that has suggested alterations in gait variables may arise partially as a result of altered walking speed (Mundermann et al., 2004; Zeni & Higginson, 2010). In this study, walking velocity did not differ as a function OA disease severity at the normal walking speed. However when challenged to walk at a fast speed, patients with severe OA walked significantly slower than patients with mild and moderate OA. Given that the external KAM during walking has been associated with radiographic disease severity (Sharma et al., 1998; Zeni & Higginson, 2010), it was expected that such a correlation would be observed in the current study, however, it was not. Some trends for knee adduction moment were revealed though. At the normal speed knee adduction moment decreased with increasing level of severity and the exact opposite was true at the fast walking speed; knee adduction moment increased with increasing radiographic severity. The trend at the fast speed was consistent with previous studies (Miyazaki et al., 2002; Wilson et al., 2011). A similar trend was observed for loading rate. While differences in loading rate were not statistically significant, loading rate decreased with increasing radiographic severity at the normal speed and it increased with increasing level of severity at the fast speed.

Based on the variables that differed by radiographic severity: velocity, knee range of motion, peak vertical ground reaction force, and time to peak vertical ground reaction force, it appears that subjects may have altered their gait mechanics as part of a compensatory strategy. These alterations may also be the result of altered control strategies (e.g. increased time to peak vertical ground reaction force) that may result in damaging gait patterns. Factors such as obesity, pain severity, and helplessness have been suggested to be important determinants of physical limitation in patients with knee OA (Creamer et al., 2000). Perhaps the compensatory strategies exhibited by the patients in this study are related to pain they experience with increasing disease severity. While the current study did not investigate the influence of pain on gait mechanics, a previous study by this group did find that pain accounted for as much as 24% of the variance in walking speed in patients with knee OA after controlling for demographics and disease severity (Somers et al., 2009). Another possible explanation for the compensatory gait mechanisms is kinesiophobia, or pain-related fear of movement, which refers to the fear of movement and injury due to consequent pain (Somers et al., 2009). If the patients with more severe OA are experiencing more pain, then it may be affecting their movement. Findings by Heuts et al., 2004 in which they found self-reported level of pain to be significantly correlated with functional limitations support this theory. Furthermore, there is increasing interest in the role of pain cognitions, specifically pain catastrophizing and pain-related fear in predicting adjustment to OA disease (Heuts et al., 2004; Somers et al., 2008; Somers et al., 2009). Somers and colleagues found that pain-related fear and pain catastrophizing explained a significant amount of variance in walking velocity and that pain catastrophizing was a significant individual predictor of walking velocity (Somers et al., 2009). Thus further investigation of the influence of pain and pain cognitions on the relationship between OA severity and additional gait variables (knee range of motion, peak vertical ground reaction force, and time to peak vertical ground reaction force), might be beneficial.

#### **5. Conclusion**

166 Principles of Osteoarthritis – Its Definition, Character, Derivation and Modality-Related Recognition

severity on knee range of motion is understandable given that severe erosion of cartilage and presence of osteophytes as well as joint space narrowing could limit knee range of motion (Holla et al., 2011). It was expected that patients with severe OA would not load their limbs as much and load them more slowly to alleviate pain. Peak vertical ground reaction force decreased with increasing OA severity at both speeds. This alteration in gait mechanics is consistent with the notion that patients are seeking to reduce loading at the knee. Finally, time to peak vertical GRF was greatest in patients with moderate OA; the differences were statistically significant at the fast speed. It is important to note that, in this study, differences related to peak vertical ground reaction force were not a function of slower walking speed. This is in contrast to previous work that has suggested alterations in gait variables may arise partially as a result of altered walking speed (Mundermann et al., 2004; Zeni & Higginson, 2010). In this study, walking velocity did not differ as a function OA disease severity at the normal walking speed. However when challenged to walk at a fast speed, patients with severe OA walked significantly slower than patients with mild and moderate OA. Given that the external KAM during walking has been associated with radiographic disease severity (Sharma et al., 1998; Zeni & Higginson, 2010), it was expected that such a correlation would be observed in the current study, however, it was not. Some trends for knee adduction moment were revealed though. At the normal speed knee adduction moment decreased with increasing level of severity and the exact opposite was true at the fast walking speed; knee adduction moment increased with increasing radiographic severity. The trend at the fast speed was consistent with previous studies (Miyazaki et al., 2002; Wilson et al., 2011). A similar trend was observed for loading rate. While differences in loading rate were not statistically significant, loading rate decreased with increasing radiographic severity at the normal speed and it

Based on the variables that differed by radiographic severity: velocity, knee range of motion, peak vertical ground reaction force, and time to peak vertical ground reaction force, it appears that subjects may have altered their gait mechanics as part of a compensatory strategy. These alterations may also be the result of altered control strategies (e.g. increased time to peak vertical ground reaction force) that may result in damaging gait patterns. Factors such as obesity, pain severity, and helplessness have been suggested to be important determinants of physical limitation in patients with knee OA (Creamer et al., 2000). Perhaps the compensatory strategies exhibited by the patients in this study are related to pain they experience with increasing disease severity. While the current study did not investigate the influence of pain on gait mechanics, a previous study by this group did find that pain accounted for as much as 24% of the variance in walking speed in patients with knee OA after controlling for demographics and disease severity (Somers et al., 2009). Another possible explanation for the compensatory gait mechanisms is kinesiophobia, or pain-related fear of movement, which refers to the fear of movement and injury due to consequent pain (Somers et al., 2009). If the patients with more severe OA are experiencing more pain, then it may be affecting their movement. Findings by Heuts et al., 2004 in which they found self-reported level of pain to be significantly correlated with functional limitations support this theory. Furthermore, there is increasing interest in the role of pain cognitions, specifically pain catastrophizing and pain-related fear in predicting adjustment to OA disease (Heuts et al., 2004; Somers et al., 2008; Somers et al., 2009). Somers and colleagues found that pain-related fear and pain

increased with increasing level of severity at the fast speed.

The purpose of this study was to examine the relationship between radiographic disease severity and gait patterns in persons with knee OA by looking at gait mechanics and joint loading in subjects across all severity levels. The results indicate that variation in gait could not be fully explained by K/L grade; although, when K/L grade was used to form different levels of radiographic disease severity, significant differences did exist. The results showed that significant differences existed in peak vertical ground reaction force and time to peak vertical ground reaction force by level of radiographic severity, even after controlling for walking speed. This study continues to point to osteoarthritis of the knee as a multifactorial disease. While radiographic disease severity is related to changes in gait biomechanics, the aberrant gait patterns could be a combination of radiographic disease severity and the pain experienced at a given severity. It may even be related to a combination of pain cognitions and radiographic disease severity. The authors suggest that future work should be done to look at the influence of pain and pain related fear of movement or other pain cognitions on gait mechanics within each severity group.

#### **6. Acknowledgements**

The authors would like to thank Sarah Jaffe, Dr. Mary Beth Nebel, Alicia Abbey, and Bryan Gibson for their contributions to this work. This research was supported by NIH grants AR50245 and AG15768.

#### **7. References**

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The Relationship Between Gait Mechanics

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*Pain, 110*(1-2), 228-235.

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fast walking speed. *J Biomech, 40*(8), 1754-1761.

and pain. *J Orthop Res, 20*(1), 101-107.

*Rheum. Disease, 16*, 494-501.

3145-3152.

*55*(1), 94-101.

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and Radiographic Disease Severity in Knee Osteoarthritis 169

Hart, D.J., & Spector, T.D. (1993). The relationship of obesity, fat distribution and

Helmick, C.G., D.T. Felson, Lawrence, R.C., Gabriel, S., R., H., & H., M.K. (2008). Estimates

Heuts, P.H., Vlaeyen, J.W., Roelofs, J., de Bie, R.A., Aretz, K., van Weel, C., & van Schayck,

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**9**

*Spain*

**Osteoarthritis in Sports and Exercise:**

*Department of Orthopedic Surgery, Hospital del Mar i l'Esperança,*

Eduard Alentorn-Geli and Lluís Puig Verdié

*Parc de Salut MAR, Barcelona,*

**Risk Factors and Preventive Strategies**

Osteoarthritis in people participating in sports have considerably increased over the last decades (Hunter DJ & Eckstein F, 2009; Wolf BR & Amendola A, 2005). Sports have many psychological, social and health benefits (Hunt A, 2003; Maffulli N et al., 2011), but individuals with past exposure to maintained vigorous exercise may have an increased risk of developing articular cartilage degeneration (Buckwalter JA, 2003; Kujala UM et al., 2003). Mechanical loading is crucial for an adequate growth and development of articular cartilage (Darling EM & Athanasiou KA, 2003). While too high of a mechanical load can damage normal articular cartilage, some stimulation is necessary to promote chondrogenesis (Darling EM & Athanasiou KA, 2003). Articular cartilage that is not mechanically stimulated will become thinner and will atrophy with time (Vanwanseele B et al., 2002). Given that the cartilage responses to mechanical loading, any type of physical activity may play a role in either the etiology or the protection against osteoarthritis. Where is the threshold at which exercise is no longer hazardous for articular cartilage but instead provides the exact stimulus for its homeostasis? There is no easy answer to this question as each individual has a unique response to each stimulus based on his own genetics but also on many associated

Osteoarthritis is a clinical syndrome caused by joint degeneration that results in permanent and often progressive joint pain and dysfunction (Buckwalter JA, 2003). Osteoarthritis has a multifactorial etiology with the influence of both systemic and local factors (Zhang Y & Jordan JM, 2010). Older age, female gender, obesity, osteoporosis, genetic factors, history of traumatic joint injuries, repetitive use of joints at high loads (either in sports, occupational work, or recreational exercise), muscle weakness, poor neuromuscular control, joint laxity, joint instability, lower extremity malalignment, or leglength discrepancy may contribute to osteoarthritis (Astephen Wilson JL et al., 2011; Blagojevic M et al., 2010; Bosomworth NJ, 2009; Harvey WF et al., 2010; Neogi T & Zhang Y, 2011; Pietrosimone BG et al., 2011; Roos EM et al., 2011; Sharma L et al., 2010; Zhang Y & Jordan JM, 2010). The knowledge of these risk factors is of great relevance to implement adequate preventive strategies for a highly debilitating disease with a clear impact on the patient's quality of life (Guccione AA et al., 1994). Prevention is also crucial because patients with osteoarthritis have an overall higher risk of death compared with the

**1. Introduction**

factors that have been linked to cartilage damage.

general population (Nüesch E et al., 2011).

Zeni, J.A., & Higginson, J.S. (2010). Differences in gait parameters between healthy subjects and persons with moderate and severe knee osteoarthritis: A result of altered walking speed? *Clinical Biomechanics, 24*(4), 372-378.

### **Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies**

Eduard Alentorn-Geli and Lluís Puig Verdié *Department of Orthopedic Surgery, Hospital del Mar i l'Esperança, Parc de Salut MAR, Barcelona, Spain*

#### **1. Introduction**

172 Principles of Osteoarthritis – Its Definition, Character, Derivation and Modality-Related Recognition

Wilson, J.L.A., Deluzio, K.J., Dunbar, M.J., Caldwell, G.E., & Hubley-Kozey, C.L. (2011). The

Zeni, J.A., & Higginson, J.S. (2010). Differences in gait parameters between healthy subjects

walking speed? *Clinical Biomechanics, 24*(4), 372-378.

*Cartilage, 19*, 186-193.

association between knee joint biomechanics and neuromuscular control and moderate knee osteoarthritis radiographic and pain severity. *Osteoarthritis and*

and persons with moderate and severe knee osteoarthritis: A result of altered

Osteoarthritis in people participating in sports have considerably increased over the last decades (Hunter DJ & Eckstein F, 2009; Wolf BR & Amendola A, 2005). Sports have many psychological, social and health benefits (Hunt A, 2003; Maffulli N et al., 2011), but individuals with past exposure to maintained vigorous exercise may have an increased risk of developing articular cartilage degeneration (Buckwalter JA, 2003; Kujala UM et al., 2003). Mechanical loading is crucial for an adequate growth and development of articular cartilage (Darling EM & Athanasiou KA, 2003). While too high of a mechanical load can damage normal articular cartilage, some stimulation is necessary to promote chondrogenesis (Darling EM & Athanasiou KA, 2003). Articular cartilage that is not mechanically stimulated will become thinner and will atrophy with time (Vanwanseele B et al., 2002). Given that the cartilage responses to mechanical loading, any type of physical activity may play a role in either the etiology or the protection against osteoarthritis. Where is the threshold at which exercise is no longer hazardous for articular cartilage but instead provides the exact stimulus for its homeostasis? There is no easy answer to this question as each individual has a unique response to each stimulus based on his own genetics but also on many associated factors that have been linked to cartilage damage.

Osteoarthritis is a clinical syndrome caused by joint degeneration that results in permanent and often progressive joint pain and dysfunction (Buckwalter JA, 2003). Osteoarthritis has a multifactorial etiology with the influence of both systemic and local factors (Zhang Y & Jordan JM, 2010). Older age, female gender, obesity, osteoporosis, genetic factors, history of traumatic joint injuries, repetitive use of joints at high loads (either in sports, occupational work, or recreational exercise), muscle weakness, poor neuromuscular control, joint laxity, joint instability, lower extremity malalignment, or leglength discrepancy may contribute to osteoarthritis (Astephen Wilson JL et al., 2011; Blagojevic M et al., 2010; Bosomworth NJ, 2009; Harvey WF et al., 2010; Neogi T & Zhang Y, 2011; Pietrosimone BG et al., 2011; Roos EM et al., 2011; Sharma L et al., 2010; Zhang Y & Jordan JM, 2010). The knowledge of these risk factors is of great relevance to implement adequate preventive strategies for a highly debilitating disease with a clear impact on the patient's quality of life (Guccione AA et al., 1994). Prevention is also crucial because patients with osteoarthritis have an overall higher risk of death compared with the general population (Nüesch E et al., 2011).

Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies 175

One of the most accepted risk factors for developing osteoarthritis is obesity (Hunter DJ & Sambrook PN, 2002). Increased weight may overload joints and alter the normal physiology of cartilage (Pallu S et al., 2010). Obesity is a clear modifiable risk factor, so there is an evident preventive measure that can be offer to patients. Weight loss would not only reduce the risk of osteoarthritis by unloading joints, but also by the fact that exercise would be of benefit for joints if performed through an adequate progression, beginning with non-weight-bearing exercises until the weight has been reduced (Felson DT et al., 1992). There are a lot of studies concluding on the increased risk of osteoarthritis in patients with obesity (Anderson JJ & Felson DT, 1988; Chaganti RK & Lane NE, 2011; Hart DJ & Spector TD, 1993; Kohatsu ND & Schurman DJ, 1990). The combination of risk factors may elicit a further increased risk of osteoarthritis, as exemplified by obesity and physical activity among elderly patients (odds ratio of 13 for developing knee osteoarthritis) (McAlindon TE et al., 1999), or obesity and female sex (Davis MA et al., 1988). The risk of osteoarthritis in obese patients is higher for knee and hand joints than for the hip joints (Grotle M et al., 2008). Interestingly, men with overweight during their 20's had higher rate than those who became overweight during their 40's on the incidence of self-reported osteoarthritis (Gelber AC et al., 1999). Hunter and Sambrook have concluded that there is consistent and conclusive evidence demonstrating the association between obesity and osteoarthritis (Hunter DJ &

Osteoporosis has been considered a risk factor for osteoarthritis (Bosomworth NJ, 2009; Hannan MT et al., 1993; Hunter DJ & Sambrook PN, 2002; Nevitt MC et al., 1995; Zhang Y et al., 2000). Although some initial studies suggested that osteoporosis would decrease the incidence of this disorder (Hunter DJ & Sambrook PN, 2002), more recent studies demonstrated that an increase in bone mineral density of 5%-10% is consistently related to both hip and knee osteoarthritis (Hannan MT et al., 1993; Nevitt MC et al., 1995). Low bone mineral density is associated with the incidence, but decreased progression of radiographic knee osteoarthritis (Zhang Y et al., 2000). The relationship between bone mineral density and osteoarthritis has been linked to vitamin D (McAlindon TE et al., 1996). Both low intake and low serum levels of vitamin D have been related to the progression of knee

Special attention is required for occupational osteoarthritis. Physical workload has been shown to be an important risk factor for the development of articular cartilage degeneration (Aluoch MA & Wao HO, 2009; Maetzel A et al., 1997). It is not the purpose of this chapter to review in detail the association between osteoarthritis and exposure to occupational physical activity. For a deeper knowledge of this risk factor, the reader is referred to the comprehensive review performed by Aluoch and Wao (Aluoch MA & Wao HO, 2009). Essentially, there is a strong relationship between high physical workload (frequent knee bending, heavy lifting, frequent stair climbing, and prolonged squatting) and risk of hand, hip, knee, and foot osteoarthritis (Aluoch MA & Wao HO, 2009). Jobs involved in occupational osteoarthritis include construction, agriculture, forestry, fishing, transportations, mining, and manufacturing (Aluoch MA & Wao HO, 2009). Occupational osteoarthritis is a modifiable risk factor. Measures aimed to prevent new cases of osteoarthritis or to decrease its progression should be taken (Hunter DJ & Sambrook PN,

Sambrook PN, 2002).

2002).

osteoarthritis (McAlindon TE et al., 1996).

The purpose of this chapter is to review the existing literature regarding the risk factors for osteoarthritis, paying special attention to past exposure to sports and exercise and also to prior joint injury and neuromuscular disorders. This chapter also reports proposed or potential preventive strategies for the development or progression of osteoarthritis.

#### **2. Overview of risk factors for osteoarthritis**

This chapter is focused on the risk of exercise and sports participation in the development and progression of osteoarthritis. In addition, there are many other identified risk factors that should be covered in order to better understand the problem of osteoarthritis and offer effective preventive measures. There are several recognized risk factors for developing osteoarthritis (Bosomworth NJ, 2009): older age, female sex, obesity, osteoporosis, occupation, sports activities, previous trauma, muscle weakness or dysfunction, proprioceptive deficit, lower limb malalignment, leg-length inequality, and genetic factors. Age, sex, and genetic factors are non-modifiable, whereas the others may be modified by an appropriate intervention. This chapter will be focused on the analysis of history of joint injury, neuromuscular dysfunction, and exercise and sports participation as risk factors for osteoarthritis.

Each body's tissue looses its optimum properties with ageing, which may contribute to any disorder. Older age is a well accepted risk factor for osteoarthritis (Bosomworth NJ, 2009; Hunter DJ & Sambrook PN, 2002; Stevens-Lapsley JE & Kohrt WM, 2010; Thelin N et al., 2006; Vrezas I et al., 2010; Ward MM et al., 1995). In fact, osteoarthritis is rare among young individuals. Articular cartilage changes with aging have been well documented both clinically and experimentally (Bosomworth NJ, 2009; Hardingham T & Bayliss M, 1990; Horton WE et al., 2006; Hunter DJ & Sambrook PN, 2002). This is a non-modifiable risk factor the prevention of its influence should begin in early ages and continue throughout the rest of the life. Obviously, this factor is always related to subject exercising or participating in sports. Thus, any investigation dealing with a certain risk factor must be adjusted for age. Females have been reported to have an increased risk of osteoarthritis (Bosomworth NJ, 2009; Hunter DJ & Sambrook PN, 2002; Jordan JM et al., 1996; Stevens-Lapsley JE & Kohrt WM, 2010). It was suggested that this difference from males would be explained by the influence of sex hormones, primarily estrogen (Hunter DJ & Sambrook PN, 2002; Riancho JA et al., 2010; Rosner IA et al., 1986; Stevens-Lapsley JE & Kohrt WM, 2010). The risk of osteoarthritis between males and females is similar under 50 years old, but significantly increases above this age in females (Felson DT et al., 1995; Oliveria SA et al., 1995). Thus, in postmenopausal women the risk of osteoarthritis is increased with respect to an age-matched cohort of males (Hunter DJ & Sambrook PN, 2002). A potential preventive pharmacological strategy with estrogen replacement therapy has been proposed for these patients (Spector TD et al., 1997). However, a recent systematic review concluded that there is some evidence for a protective effect of this therapy for hip, but not for knee osteoarthritis (de Klerk BM et al., 2009). De Klerk and colleagues stated that heterogeneity between the hormones used and outcome measurements made statistical data pooling impossible (de Klerk BM et al., 2009). Relationship between the exogenous hormone use and osteoarthritis was not clearly observed. They concluded that other aspects, yet to be determined, may play a role in the increased incidence in women aged over 50 years (de Klerk BM et al., 2009). Hunter and Sambrook suggested randomized, prospective clinical trials to clarify the effects of hormone replacement therapy on the development of osteoarthritis (Hunter DJ & Sambrook PN, 2002).

The purpose of this chapter is to review the existing literature regarding the risk factors for osteoarthritis, paying special attention to past exposure to sports and exercise and also to prior joint injury and neuromuscular disorders. This chapter also reports proposed or

This chapter is focused on the risk of exercise and sports participation in the development and progression of osteoarthritis. In addition, there are many other identified risk factors that should be covered in order to better understand the problem of osteoarthritis and offer effective preventive measures. There are several recognized risk factors for developing osteoarthritis (Bosomworth NJ, 2009): older age, female sex, obesity, osteoporosis, occupation, sports activities, previous trauma, muscle weakness or dysfunction, proprioceptive deficit, lower limb malalignment, leg-length inequality, and genetic factors. Age, sex, and genetic factors are non-modifiable, whereas the others may be modified by an appropriate intervention. This chapter will be focused on the analysis of history of joint injury, neuromuscular dysfunction, and exercise and sports participation as risk factors for

Each body's tissue looses its optimum properties with ageing, which may contribute to any disorder. Older age is a well accepted risk factor for osteoarthritis (Bosomworth NJ, 2009; Hunter DJ & Sambrook PN, 2002; Stevens-Lapsley JE & Kohrt WM, 2010; Thelin N et al., 2006; Vrezas I et al., 2010; Ward MM et al., 1995). In fact, osteoarthritis is rare among young individuals. Articular cartilage changes with aging have been well documented both clinically and experimentally (Bosomworth NJ, 2009; Hardingham T & Bayliss M, 1990; Horton WE et al., 2006; Hunter DJ & Sambrook PN, 2002). This is a non-modifiable risk factor the prevention of its influence should begin in early ages and continue throughout the rest of the life. Obviously, this factor is always related to subject exercising or participating in sports. Thus, any investigation dealing with a certain risk factor must be adjusted for age. Females have been reported to have an increased risk of osteoarthritis (Bosomworth NJ, 2009; Hunter DJ & Sambrook PN, 2002; Jordan JM et al., 1996; Stevens-Lapsley JE & Kohrt WM, 2010). It was suggested that this difference from males would be explained by the influence of sex hormones, primarily estrogen (Hunter DJ & Sambrook PN, 2002; Riancho JA et al., 2010; Rosner IA et al., 1986; Stevens-Lapsley JE & Kohrt WM, 2010). The risk of osteoarthritis between males and females is similar under 50 years old, but significantly increases above this age in females (Felson DT et al., 1995; Oliveria SA et al., 1995). Thus, in postmenopausal women the risk of osteoarthritis is increased with respect to an age-matched cohort of males (Hunter DJ & Sambrook PN, 2002). A potential preventive pharmacological strategy with estrogen replacement therapy has been proposed for these patients (Spector TD et al., 1997). However, a recent systematic review concluded that there is some evidence for a protective effect of this therapy for hip, but not for knee osteoarthritis (de Klerk BM et al., 2009). De Klerk and colleagues stated that heterogeneity between the hormones used and outcome measurements made statistical data pooling impossible (de Klerk BM et al., 2009). Relationship between the exogenous hormone use and osteoarthritis was not clearly observed. They concluded that other aspects, yet to be determined, may play a role in the increased incidence in women aged over 50 years (de Klerk BM et al., 2009). Hunter and Sambrook suggested randomized, prospective clinical trials to clarify the effects of hormone replacement therapy on

the development of osteoarthritis (Hunter DJ & Sambrook PN, 2002).

potential preventive strategies for the development or progression of osteoarthritis.

**2. Overview of risk factors for osteoarthritis**

osteoarthritis.

One of the most accepted risk factors for developing osteoarthritis is obesity (Hunter DJ & Sambrook PN, 2002). Increased weight may overload joints and alter the normal physiology of cartilage (Pallu S et al., 2010). Obesity is a clear modifiable risk factor, so there is an evident preventive measure that can be offer to patients. Weight loss would not only reduce the risk of osteoarthritis by unloading joints, but also by the fact that exercise would be of benefit for joints if performed through an adequate progression, beginning with non-weight-bearing exercises until the weight has been reduced (Felson DT et al., 1992). There are a lot of studies concluding on the increased risk of osteoarthritis in patients with obesity (Anderson JJ & Felson DT, 1988; Chaganti RK & Lane NE, 2011; Hart DJ & Spector TD, 1993; Kohatsu ND & Schurman DJ, 1990). The combination of risk factors may elicit a further increased risk of osteoarthritis, as exemplified by obesity and physical activity among elderly patients (odds ratio of 13 for developing knee osteoarthritis) (McAlindon TE et al., 1999), or obesity and female sex (Davis MA et al., 1988). The risk of osteoarthritis in obese patients is higher for knee and hand joints than for the hip joints (Grotle M et al., 2008). Interestingly, men with overweight during their 20's had higher rate than those who became overweight during their 40's on the incidence of self-reported osteoarthritis (Gelber AC et al., 1999). Hunter and Sambrook have concluded that there is consistent and conclusive evidence demonstrating the association between obesity and osteoarthritis (Hunter DJ & Sambrook PN, 2002).

Osteoporosis has been considered a risk factor for osteoarthritis (Bosomworth NJ, 2009; Hannan MT et al., 1993; Hunter DJ & Sambrook PN, 2002; Nevitt MC et al., 1995; Zhang Y et al., 2000). Although some initial studies suggested that osteoporosis would decrease the incidence of this disorder (Hunter DJ & Sambrook PN, 2002), more recent studies demonstrated that an increase in bone mineral density of 5%-10% is consistently related to both hip and knee osteoarthritis (Hannan MT et al., 1993; Nevitt MC et al., 1995). Low bone mineral density is associated with the incidence, but decreased progression of radiographic knee osteoarthritis (Zhang Y et al., 2000). The relationship between bone mineral density and osteoarthritis has been linked to vitamin D (McAlindon TE et al., 1996). Both low intake and low serum levels of vitamin D have been related to the progression of knee osteoarthritis (McAlindon TE et al., 1996).

Special attention is required for occupational osteoarthritis. Physical workload has been shown to be an important risk factor for the development of articular cartilage degeneration (Aluoch MA & Wao HO, 2009; Maetzel A et al., 1997). It is not the purpose of this chapter to review in detail the association between osteoarthritis and exposure to occupational physical activity. For a deeper knowledge of this risk factor, the reader is referred to the comprehensive review performed by Aluoch and Wao (Aluoch MA & Wao HO, 2009). Essentially, there is a strong relationship between high physical workload (frequent knee bending, heavy lifting, frequent stair climbing, and prolonged squatting) and risk of hand, hip, knee, and foot osteoarthritis (Aluoch MA & Wao HO, 2009). Jobs involved in occupational osteoarthritis include construction, agriculture, forestry, fishing, transportations, mining, and manufacturing (Aluoch MA & Wao HO, 2009). Occupational osteoarthritis is a modifiable risk factor. Measures aimed to prevent new cases of osteoarthritis or to decrease its progression should be taken (Hunter DJ & Sambrook PN, 2002).

Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies 177

in patients with no previous cartilage injuries. Long-term consequences of acute-traumatic meniscal tears in terms of osteoarthritis may be influenced by length of follow-up, age at the time of injury, sex, and associated injuries (Lohmander LS et al., 2007). In contrast, chronicdegenerative tears may affect one third of the general population over 50 years after no trauma at all (Englund M et al., 2008; Lohmander LS et al., 2007), and are associated with pre-existing and progression of knee osteoarthritis (Englund M et al., 2003). These meniscal injuries are more commonly associated with pre-existing joint cartilage damage than acutetraumatic tears (Christoforakis J et al., 2005; Englund M & Lohmander LS, 2004). The preexisting osteoarthritis is worsened by meniscal tears (Hunter DJ et al., 2006; Raynauld JP et al., 2006). Therefore, their risk of osteoarthritis in chronic-degenerative meniscal injuries is explained by two factors; that is, the presence of prior cartilage injury, and the meniscus tear itself. The "double" mechanism of osteoarthritis in these injuries may explain the worst long-term radiographic and clinical outcomes compared to acute-traumatic tears (Englund

Repetitive increased loading in a patient with unrepaired meniscal tear also increases the risk of developing knee osteoarthritis (Lohmander LS et al., 2007). Also, articular cartilage degeneration is produced when meniscectomy is performed. Partial or total meniscectomies increase the tibiofemoral contact area and increase the joint contact pressures (Baratz M et al., 1986; Burke DL et al., 1978; Fairbank TJ, 1948; Seedhom BB & Hargreaves DJ, 1979), thus explaining the early onset knee osteoarthritic changes (Hoser C et al., 2001; Jorgensen U et al., 1987; Roos H et al., 1998). The contralateral healthy knee is also affected although to a lesser degree (Englund M & Lohmander LS, 2004). The greater the area of meniscectomy, the greater the mechanical distress on the knee, and a greater chondral deterioration can be expected. Meniscal resection of only 15% to 34% increases the contact pressure more than a 350%, whereas a total meniscectomy increases the contact load on the cartilage up to a 700% (Ahmed AM & Burke DL, 1983; Fukubayashi TK & Kurosawa H, 1980). Roos and colleagues compared the risk of knee osteoarthritis in a cohort of 123 patients 21 years after total meniscectomy (Roos H et al., 1998). The relative risk of developing knee osteoarthritis after total meniscectomy was 14 (95% confidence interval 3.5-121.2), using age- and sexmatched pairs for comparison. Forty-eight percent of patients in the meniscectomy group had grade II or more radiographic osteoarthritis with the Kellegren-Lawrence classification compared to only a 7% in the control group. In addition, knee symptoms were reported twice as often in meniscectomized patients compared to controls (Roos H et al., 1998). The authors found no relationship with knee osteoarthritis depending on the localization of the compartment or type of meniscus tear. In contrast, Lohmander and colleagues stated in their review that the symptoms and functional outcomes of lateral meniscectomy in relation to knee osteoarthritis were worst compared to medial meniscectomy (Lohmander LS et al., 2007). In accordance with Roos and colleagues, Neuman and colleagues observed that the primary risk factor for tibiofemoral osteoarthritis was a prior meniscectomy after prospectively evaluating the occurrence of knee osteoarthritis 15 years after non-operative treatment of anterior cruciate ligament injury (Neuman P et al., 2008). Cooper and colleagues found that patients with previous knee injury had 3 times more risk of knee osteoarthritis compared to uninjured subjects. This risk was increased 4-fold if meniscectomy had to be performed (Cooper C et al., 1994). Specifically, meniscectomy was a strong risk factor for medial tibiofemoral osteoarthritis. In their excellent review article about the long-term consequences of anterior cruciate ligament and meniscal tears, Lohmander and colleagues found that some 50% of patients undergoing meniscectomy 15 to

M et al., 2001; 2003; 2004).

Lower limb malalignment and leg-length inequality would also be risk factors for progression, but not onset, of osteoarthritis (Brouwer GM et al., 2007; Golightly YM et al., 2007; 2010; Hunter DJ et al., 2007). Both factors may not initiate or cause osteoarthritis, but just worsen the already damaged articular cartilage. Knee varus malalignment but not knee valgus was associated with both onset and progression of osteoarthritis (Brouwer GM et al., 2007). This observation was particularly applicable to obese individuals, again showing the bad consequences of having various risk factors associated in the same subject. Unfortunately, this finding has not been reproducible (Hunter DJ et al., 2007). Leg-length inequality was associated with progression of radiographic knee osteoarthritis, but not with incident radiographic knee or hip osteoarthritis, progression of chronic knee symptoms, and incident and progression of chronic hip symptoms (Golightly YM et al., 2010). Both factors may be modifiable by surgery or raised insoles (Neogi T & Zhang Y, 2011).

Genetics, epigenetics, and genomics are probably the most promising areas to be developed in relation to the study of osteoarthritis. The study of these areas is yielding valuable insights into the etiology of osteoarthritis but there is still much to know (Meulenbelt I et al., 2011). It is likely that individuals with a genetic predisposition would have osteoarthritis in many joints (Felson DT et al., 2000). Genetic factors may account for at least 50% of cases of osteoarthritis in the hands and hips, and a smaller percentage in the knees (Spector TD et al., 1996a). Overall, Loughlin considers that the search for osteoarthritis susceptibility loci has been limited (Loughlin J, 2011). Genes affected for most common forms of osteoarthritis would include vitamin D receptor gene, insulin-like growth factor I gene, cartilage oligomeric protein genes, and HLA region (Felson DT et al., 2000). Genetics may contribute to osteoarthritis to a different extend depending on each individual. The heterogeneous nature of the disease in terms of potential causes and presentation may explain why genetics are not the only aspect to consider. In other words, genetic and environmental factors must be considered altogether for an adequate prevention of osteoarthritis.

#### **3. History of joint injury**

Any kind of physical activity implies a chance of injury. Former athletes have a high rate of joint injury (Krajnc Z et al., 2010). Individuals with a history of joint injury have a higher risk of developing osteoarthritis (Hunter DJ & Eckstein F, 2009). The role of joint injury in the development of osteoarthritis has been mainly studied in the knee joint. Previous knee injury may be one of the most important modifiable risk factors for subsequent knee osteoarthritis in men, and second only after obesity in women (Felson DT et al., 2000; Hunter DJ & Sambrook PN, 2002). Knee injuries typically occur in the younger population thus causing prolonged disability and high economic costs (Hunter DJ & Sambrook PN, 2002; Yelin E & Callahan LF, 1995). Knee joint injuries increase the risk of osteoarthritis by increasing tibiofemoral contact area and pressures in meniscal injuries, by causing joint instability in ligament injuries, by chondral lesions itself, or by impairing the neuromuscular system.

The menisci are responsible for load-bearing, shock-absorption, joint stability, joint lubrication, and joint congruity (King D, 1936). All these functions contribute to the preservation of articular cartilage, which may be injured whenever meniscal disorders develop. Meniscal tears may be classified in acute-traumatic or chronic-degenerative. Acutetraumatic tears mainly occur in young patients, usually participating in sports, and increase the risk of developing knee osteoarthritis (Englund M et al., 2003). Acute tears mainly occur

Lower limb malalignment and leg-length inequality would also be risk factors for progression, but not onset, of osteoarthritis (Brouwer GM et al., 2007; Golightly YM et al., 2007; 2010; Hunter DJ et al., 2007). Both factors may not initiate or cause osteoarthritis, but just worsen the already damaged articular cartilage. Knee varus malalignment but not knee valgus was associated with both onset and progression of osteoarthritis (Brouwer GM et al., 2007). This observation was particularly applicable to obese individuals, again showing the bad consequences of having various risk factors associated in the same subject. Unfortunately, this finding has not been reproducible (Hunter DJ et al., 2007). Leg-length inequality was associated with progression of radiographic knee osteoarthritis, but not with incident radiographic knee or hip osteoarthritis, progression of chronic knee symptoms, and incident and progression of chronic hip symptoms (Golightly YM et al., 2010). Both factors

Genetics, epigenetics, and genomics are probably the most promising areas to be developed in relation to the study of osteoarthritis. The study of these areas is yielding valuable insights into the etiology of osteoarthritis but there is still much to know (Meulenbelt I et al., 2011). It is likely that individuals with a genetic predisposition would have osteoarthritis in many joints (Felson DT et al., 2000). Genetic factors may account for at least 50% of cases of osteoarthritis in the hands and hips, and a smaller percentage in the knees (Spector TD et al., 1996a). Overall, Loughlin considers that the search for osteoarthritis susceptibility loci has been limited (Loughlin J, 2011). Genes affected for most common forms of osteoarthritis would include vitamin D receptor gene, insulin-like growth factor I gene, cartilage oligomeric protein genes, and HLA region (Felson DT et al., 2000). Genetics may contribute to osteoarthritis to a different extend depending on each individual. The heterogeneous nature of the disease in terms of potential causes and presentation may explain why genetics are not the only aspect to consider. In other words, genetic and environmental factors must

Any kind of physical activity implies a chance of injury. Former athletes have a high rate of joint injury (Krajnc Z et al., 2010). Individuals with a history of joint injury have a higher risk of developing osteoarthritis (Hunter DJ & Eckstein F, 2009). The role of joint injury in the development of osteoarthritis has been mainly studied in the knee joint. Previous knee injury may be one of the most important modifiable risk factors for subsequent knee osteoarthritis in men, and second only after obesity in women (Felson DT et al., 2000; Hunter DJ & Sambrook PN, 2002). Knee injuries typically occur in the younger population thus causing prolonged disability and high economic costs (Hunter DJ & Sambrook PN, 2002; Yelin E & Callahan LF, 1995). Knee joint injuries increase the risk of osteoarthritis by increasing tibiofemoral contact area and pressures in meniscal injuries, by causing joint instability in ligament injuries, by chondral lesions itself, or by impairing the neuromuscular

The menisci are responsible for load-bearing, shock-absorption, joint stability, joint lubrication, and joint congruity (King D, 1936). All these functions contribute to the preservation of articular cartilage, which may be injured whenever meniscal disorders develop. Meniscal tears may be classified in acute-traumatic or chronic-degenerative. Acutetraumatic tears mainly occur in young patients, usually participating in sports, and increase the risk of developing knee osteoarthritis (Englund M et al., 2003). Acute tears mainly occur

may be modifiable by surgery or raised insoles (Neogi T & Zhang Y, 2011).

be considered altogether for an adequate prevention of osteoarthritis.

**3. History of joint injury**

system.

in patients with no previous cartilage injuries. Long-term consequences of acute-traumatic meniscal tears in terms of osteoarthritis may be influenced by length of follow-up, age at the time of injury, sex, and associated injuries (Lohmander LS et al., 2007). In contrast, chronicdegenerative tears may affect one third of the general population over 50 years after no trauma at all (Englund M et al., 2008; Lohmander LS et al., 2007), and are associated with pre-existing and progression of knee osteoarthritis (Englund M et al., 2003). These meniscal injuries are more commonly associated with pre-existing joint cartilage damage than acutetraumatic tears (Christoforakis J et al., 2005; Englund M & Lohmander LS, 2004). The preexisting osteoarthritis is worsened by meniscal tears (Hunter DJ et al., 2006; Raynauld JP et al., 2006). Therefore, their risk of osteoarthritis in chronic-degenerative meniscal injuries is explained by two factors; that is, the presence of prior cartilage injury, and the meniscus tear itself. The "double" mechanism of osteoarthritis in these injuries may explain the worst long-term radiographic and clinical outcomes compared to acute-traumatic tears (Englund M et al., 2001; 2003; 2004).

Repetitive increased loading in a patient with unrepaired meniscal tear also increases the risk of developing knee osteoarthritis (Lohmander LS et al., 2007). Also, articular cartilage degeneration is produced when meniscectomy is performed. Partial or total meniscectomies increase the tibiofemoral contact area and increase the joint contact pressures (Baratz M et al., 1986; Burke DL et al., 1978; Fairbank TJ, 1948; Seedhom BB & Hargreaves DJ, 1979), thus explaining the early onset knee osteoarthritic changes (Hoser C et al., 2001; Jorgensen U et al., 1987; Roos H et al., 1998). The contralateral healthy knee is also affected although to a lesser degree (Englund M & Lohmander LS, 2004). The greater the area of meniscectomy, the greater the mechanical distress on the knee, and a greater chondral deterioration can be expected. Meniscal resection of only 15% to 34% increases the contact pressure more than a 350%, whereas a total meniscectomy increases the contact load on the cartilage up to a 700% (Ahmed AM & Burke DL, 1983; Fukubayashi TK & Kurosawa H, 1980). Roos and colleagues compared the risk of knee osteoarthritis in a cohort of 123 patients 21 years after total meniscectomy (Roos H et al., 1998). The relative risk of developing knee osteoarthritis after total meniscectomy was 14 (95% confidence interval 3.5-121.2), using age- and sexmatched pairs for comparison. Forty-eight percent of patients in the meniscectomy group had grade II or more radiographic osteoarthritis with the Kellegren-Lawrence classification compared to only a 7% in the control group. In addition, knee symptoms were reported twice as often in meniscectomized patients compared to controls (Roos H et al., 1998). The authors found no relationship with knee osteoarthritis depending on the localization of the compartment or type of meniscus tear. In contrast, Lohmander and colleagues stated in their review that the symptoms and functional outcomes of lateral meniscectomy in relation to knee osteoarthritis were worst compared to medial meniscectomy (Lohmander LS et al., 2007). In accordance with Roos and colleagues, Neuman and colleagues observed that the primary risk factor for tibiofemoral osteoarthritis was a prior meniscectomy after prospectively evaluating the occurrence of knee osteoarthritis 15 years after non-operative treatment of anterior cruciate ligament injury (Neuman P et al., 2008). Cooper and colleagues found that patients with previous knee injury had 3 times more risk of knee osteoarthritis compared to uninjured subjects. This risk was increased 4-fold if meniscectomy had to be performed (Cooper C et al., 1994). Specifically, meniscectomy was a strong risk factor for medial tibiofemoral osteoarthritis. In their excellent review article about the long-term consequences of anterior cruciate ligament and meniscal tears, Lohmander and colleagues found that some 50% of patients undergoing meniscectomy 15 to

Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies 179

2009). Although improvements in knee function were observed up to 15 years after ligament reconstruction, combined injuries (ACL, menisci, and chondral injuries) led to a higher risk of knee osteoarthritis compared with isolated anterior cruciate ligament tears (Oiestad BE et

The technique of anterior cruciate ligament reconstruction has conflicting evidence regarding the influence on the development of knee osteoarthritis (Keays SL et al., 2010; Vairo GL et al., 2010). The use of bone-patellar tendon bone would seem to increase the risk of knee osteoarthritis compared to the use of hamstring tendons autograft (Keays SL et al., 2010; Vairo GL et al., 2010). However, other authors have reported that at a median of 7 years after ligament reconstruction with either autograft, the prevalence of osteoarthritis as seen on standard weight-bearing radiographs and the clinical outcomes was comparable

Overall, there is a clear consensus that meniscal, ligament, and chondral injuries increase the risk of knee osteoarthritis (Ichiba A & Kishimoto I, 2009; Keays SL et al., 2010; Lidén M et al., 2008; Lohmander LS et al., 2007; Maffulli N et al., 2003; Magnussen RA et al., 2009; Neuman P et al., 2008; Oiestad BE et al., 2010a; 2010b; Roos H et al., 1998). Anterior cruciate ligament and menisci injuries increase the risk of joint degeneration whether or not being surgically treated (Lohmander LS et al., 2004; 2007; von Porat A et al., 2004). In addition, a past history of knee surgery is associated with a rapid progression to knee arthroplasty (Riddle DL et al., 2011). Therefore, prevention of injuries should be considered as one of the most important parts of training programs in athletes or subjects who wish to participate in sports (Roos H

The neuromuscular system is crucial to prevent joint damage. Muscles provide dynamic stability, aid in shock absorption, and provide adequate force transmission across joints (Brandt KD, 1997; Mikesky AE et al., 2000; Palmieri-Smith RM & Thomas AC, 2009). Therefore, deconditioned muscles or poor neuromuscular control may increase the risk of osteoarthritis (Roos EM et al., 2011). Impairment of the neuromuscular system may be caused by inadequate training or joint injuries. Preventive programs aimed to improve this system are essential to reduce the risk of osteoarthritis (Keays SL et al., 2010; Neuman P et al., 2008; Roos EM et al., 2011; Segal NA et al., 2010). Muscle weakness is considered a predictor of knee osteoarthritis onset, but there is no clear consensus regarding its role in osteoarthritis progression. In contrast, afferent sensory dysfunction has been related to

Anterior cruciate ligament injuries may cause muscle inhibition, muscle atrophy, and changes in activation patterns and knee kinematics (Berchuck M et al., 1990; Palmieri-Smith RM & Thomas AC, 2009; Snyder-Mackler L et al., 1993; Suter E & Herzog W, 2000). Oiestad and colleagues did not detect association between quadriceps weakness after anterior cruciate ligament reconstruction and knee osteoarthritis as measured 10-15 years later (Oiestad BE et al., 2010b). However, it is accepted that muscle weakness and neuromuscular impairment do exist after anterior cruciate ligament injuries (Berchuck M et al., 1990; Palmieri-Smith RM & Thomas AC, 2009; Roos EM et al., 2011). Palmieri-Smith and Thomas used the term arthrogenic inhibition to refer to the neurological "shutdown" of muscles surrounding an injured joint, preventing full activation, reducing strength, and promoting atrophy (Palmieri-Smith RM & Thomas AC, 2009). Neuromuscular impairment following

**4. Muscle weakness and afferent sensory dysfunction**

progression, but not onset, of osteoarthritis (Roos EM et al., 2011).

al., 2010a).

(Lidén M et al., 2008).

et al., 1998).

20 years earlier had radiographic knee osteoarthritis, with an odds ratio of about 10 compared to age- and sex-matched controls (Lohmander LS et al., 2007). The authors stated that symptoms and functional outcomes of meniscectomy were worst if other risk factors were present (i.e., women and obesity). Also, Hunter and Sambrook stated that older age at the time of injury predicts a more rapid progression to knee osteoarthritis (Hunter DJ & Sambrook PN, 2002). Patients with finger joint osteoarthritis at the time of meniscectomy had a higher risk of developing knee osteoarthritis compared to patients without finger osteoarthritis (Englund M et al., 2004). This may indicate the potential relationship between genetic predisposition and osteoarthritis. Lohmander and colleagues considered that studies assessing radiographic osteoarthritic changes after meniscus tears had large variations in sample sizes, patients lost at follow-up, age and sex distribution, and, overall, they had concerns on the quality of study designs. The review performed by Lohmander and colleagues did not provide support of meniscus suture or meniscus allograft transplantation to prevent future development of knee osteoarthritis (Lohmander LS et al., 2007).

Anterior cruciate ligament tears also occur more commonly in young patients, usually under 30 years old (Lohmander LS et al., 2007). Therefore, these injuries explain a large number of early-onset knee osteoarthritis cases with associated pain, functional limitations, and decreased quality of life in the individuals between 30 and 50 years (Lohmander LS et al., 2004; 2007; von Porat A et al., 2004). Radiographic knee osteoarthritis following an anterior cruciate ligament injury ranges from 10% to 90% at 10 to 20 years of follow-up (Gillquist J & Messner K, 1999; Lohmander LS & Roos H, 1994). Such a wide range may be explained by differences in the assessment method of radiographic osteoarthritis, sample size, loss of patients to, and length of, follow-up, sex distribution, age at the time of injury, and associated knee injuries (Lohmander LS et al., 2007). Lohmander and colleagues reported an approximate rate of radiographic knee osteoarthritis of more than 50% after 10 to 20 years of anterior cruciate ligament injury (Lohmander LS et al., 2007). The great majority of their reviewed studies using the Lysholm score had a mean follow-up values around 90 (good or excellent) (Lohmander LS et al., 2007). Scores for quality of life and sport and recreation after anterior cruciate ligament rehabilitation and/or surgery were found to be at its best at 1 to 2 years of follow-up, gradually deteriorating afterwards (Lohmander LS et al., 2007). After 12 years of an anterior cruciate ligament rupture with a mean age at follow-up of 31 years, 75% of female soccer players had a significant impairment of kneerelated quality of life and 42% symptomatic radiographic knee osteoarthritis (Lohmander LS et al., 2004). Similar consequences were reported in male soccer players 14 years after this injury, with a mean age at follow-up of 38 years (von Porat A et al., 2004).

Anterior cruciate ligament injuries are often associated with other knee injuries. Keays and colleagues found that concomitant meniscal and chondral damage significantly increased the risk of tibiofemoral osteoarthritis in patients undergoing anterior cruciate ligament reconstruction (Keays SL et al., 2010). Partial meniscectomy at the time of reconstruction significantly increases the risk of developing knee osteoarthritis compared to those with normal menisci (Magnussen RA et al., 2009). If complete meniscectomy is needed, then patients will develop radiographic knee osteoarthritis in near 100% of cases at 5-to-10-year follow-up (Magnussen RA et al., 2009). Meniscal repair was found to have inconsistent influence on the prevention of developing knee osteoarthritis after anterior cruciate ligament reconstruction (Magnussen RA et al., 2009). The presence of cartilage injury at the time of a meniscus tear requiring operation accelerates knee osteoarthritis in patients under 40 years old undergoing anterior cruciate ligament reconstruction (Ichiba A & Kishimoto I,

20 years earlier had radiographic knee osteoarthritis, with an odds ratio of about 10 compared to age- and sex-matched controls (Lohmander LS et al., 2007). The authors stated that symptoms and functional outcomes of meniscectomy were worst if other risk factors were present (i.e., women and obesity). Also, Hunter and Sambrook stated that older age at the time of injury predicts a more rapid progression to knee osteoarthritis (Hunter DJ & Sambrook PN, 2002). Patients with finger joint osteoarthritis at the time of meniscectomy had a higher risk of developing knee osteoarthritis compared to patients without finger osteoarthritis (Englund M et al., 2004). This may indicate the potential relationship between genetic predisposition and osteoarthritis. Lohmander and colleagues considered that studies assessing radiographic osteoarthritic changes after meniscus tears had large variations in sample sizes, patients lost at follow-up, age and sex distribution, and, overall, they had concerns on the quality of study designs. The review performed by Lohmander and colleagues did not provide support of meniscus suture or meniscus allograft transplantation

to prevent future development of knee osteoarthritis (Lohmander LS et al., 2007).

injury, with a mean age at follow-up of 38 years (von Porat A et al., 2004).

Anterior cruciate ligament injuries are often associated with other knee injuries. Keays and colleagues found that concomitant meniscal and chondral damage significantly increased the risk of tibiofemoral osteoarthritis in patients undergoing anterior cruciate ligament reconstruction (Keays SL et al., 2010). Partial meniscectomy at the time of reconstruction significantly increases the risk of developing knee osteoarthritis compared to those with normal menisci (Magnussen RA et al., 2009). If complete meniscectomy is needed, then patients will develop radiographic knee osteoarthritis in near 100% of cases at 5-to-10-year follow-up (Magnussen RA et al., 2009). Meniscal repair was found to have inconsistent influence on the prevention of developing knee osteoarthritis after anterior cruciate ligament reconstruction (Magnussen RA et al., 2009). The presence of cartilage injury at the time of a meniscus tear requiring operation accelerates knee osteoarthritis in patients under 40 years old undergoing anterior cruciate ligament reconstruction (Ichiba A & Kishimoto I,

Anterior cruciate ligament tears also occur more commonly in young patients, usually under 30 years old (Lohmander LS et al., 2007). Therefore, these injuries explain a large number of early-onset knee osteoarthritis cases with associated pain, functional limitations, and decreased quality of life in the individuals between 30 and 50 years (Lohmander LS et al., 2004; 2007; von Porat A et al., 2004). Radiographic knee osteoarthritis following an anterior cruciate ligament injury ranges from 10% to 90% at 10 to 20 years of follow-up (Gillquist J & Messner K, 1999; Lohmander LS & Roos H, 1994). Such a wide range may be explained by differences in the assessment method of radiographic osteoarthritis, sample size, loss of patients to, and length of, follow-up, sex distribution, age at the time of injury, and associated knee injuries (Lohmander LS et al., 2007). Lohmander and colleagues reported an approximate rate of radiographic knee osteoarthritis of more than 50% after 10 to 20 years of anterior cruciate ligament injury (Lohmander LS et al., 2007). The great majority of their reviewed studies using the Lysholm score had a mean follow-up values around 90 (good or excellent) (Lohmander LS et al., 2007). Scores for quality of life and sport and recreation after anterior cruciate ligament rehabilitation and/or surgery were found to be at its best at 1 to 2 years of follow-up, gradually deteriorating afterwards (Lohmander LS et al., 2007). After 12 years of an anterior cruciate ligament rupture with a mean age at follow-up of 31 years, 75% of female soccer players had a significant impairment of kneerelated quality of life and 42% symptomatic radiographic knee osteoarthritis (Lohmander LS et al., 2004). Similar consequences were reported in male soccer players 14 years after this 2009). Although improvements in knee function were observed up to 15 years after ligament reconstruction, combined injuries (ACL, menisci, and chondral injuries) led to a higher risk of knee osteoarthritis compared with isolated anterior cruciate ligament tears (Oiestad BE et al., 2010a).

The technique of anterior cruciate ligament reconstruction has conflicting evidence regarding the influence on the development of knee osteoarthritis (Keays SL et al., 2010; Vairo GL et al., 2010). The use of bone-patellar tendon bone would seem to increase the risk of knee osteoarthritis compared to the use of hamstring tendons autograft (Keays SL et al., 2010; Vairo GL et al., 2010). However, other authors have reported that at a median of 7 years after ligament reconstruction with either autograft, the prevalence of osteoarthritis as seen on standard weight-bearing radiographs and the clinical outcomes was comparable (Lidén M et al., 2008).

Overall, there is a clear consensus that meniscal, ligament, and chondral injuries increase the risk of knee osteoarthritis (Ichiba A & Kishimoto I, 2009; Keays SL et al., 2010; Lidén M et al., 2008; Lohmander LS et al., 2007; Maffulli N et al., 2003; Magnussen RA et al., 2009; Neuman P et al., 2008; Oiestad BE et al., 2010a; 2010b; Roos H et al., 1998). Anterior cruciate ligament and menisci injuries increase the risk of joint degeneration whether or not being surgically treated (Lohmander LS et al., 2004; 2007; von Porat A et al., 2004). In addition, a past history of knee surgery is associated with a rapid progression to knee arthroplasty (Riddle DL et al., 2011). Therefore, prevention of injuries should be considered as one of the most important parts of training programs in athletes or subjects who wish to participate in sports (Roos H et al., 1998).

#### **4. Muscle weakness and afferent sensory dysfunction**

The neuromuscular system is crucial to prevent joint damage. Muscles provide dynamic stability, aid in shock absorption, and provide adequate force transmission across joints (Brandt KD, 1997; Mikesky AE et al., 2000; Palmieri-Smith RM & Thomas AC, 2009). Therefore, deconditioned muscles or poor neuromuscular control may increase the risk of osteoarthritis (Roos EM et al., 2011). Impairment of the neuromuscular system may be caused by inadequate training or joint injuries. Preventive programs aimed to improve this system are essential to reduce the risk of osteoarthritis (Keays SL et al., 2010; Neuman P et al., 2008; Roos EM et al., 2011; Segal NA et al., 2010). Muscle weakness is considered a predictor of knee osteoarthritis onset, but there is no clear consensus regarding its role in osteoarthritis progression. In contrast, afferent sensory dysfunction has been related to progression, but not onset, of osteoarthritis (Roos EM et al., 2011).

Anterior cruciate ligament injuries may cause muscle inhibition, muscle atrophy, and changes in activation patterns and knee kinematics (Berchuck M et al., 1990; Palmieri-Smith RM & Thomas AC, 2009; Snyder-Mackler L et al., 1993; Suter E & Herzog W, 2000). Oiestad and colleagues did not detect association between quadriceps weakness after anterior cruciate ligament reconstruction and knee osteoarthritis as measured 10-15 years later (Oiestad BE et al., 2010b). However, it is accepted that muscle weakness and neuromuscular impairment do exist after anterior cruciate ligament injuries (Berchuck M et al., 1990; Palmieri-Smith RM & Thomas AC, 2009; Roos EM et al., 2011). Palmieri-Smith and Thomas used the term arthrogenic inhibition to refer to the neurological "shutdown" of muscles surrounding an injured joint, preventing full activation, reducing strength, and promoting atrophy (Palmieri-Smith RM & Thomas AC, 2009). Neuromuscular impairment following

Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies 181

radiographic knee osteoarthritis and a 29% reduction in the odds ratio of symptomatic knee osteoarthritis (Slemenda C et al., 1997). In an experimental animal model study, Longino and colleagues induced quadriceps muscle weakness by injecting botulinum toxin A into muscles (Longino D et al., 2005). Only 4 weeks after the induction of muscle weakness, the authors found retropatellar cartilage degeneration in the experimental rabbits compared to control rabbits. Segal and colleagues found that greater knee extensor strength protected against development of incident symptomatic, but not radiographic, knee osteoarthritis in both sexes (Segal NA et al., 2009; 2010). Subjects with greater quadriceps strength also had less knee pain and better physical function over follow-up (Amin S et al., 2009). Some of the benefits of neuromuscular training on knee osteoarthritis may be explained by induced changes in glycosaminoglycan content (Roos EM & Dahlberg LE, 2005). While there seems to be a protective effect of muscle strengthening against the onset of osteoarthritis, that seems to be controversial for osteoarthritis progression (Roos EM et al., 2011). Further welldesigned studies are needed to elucidate if muscle strengthening would prevent

The afferent somatosensory system comprises the receptors, afferent neurons and central processing centers that permit the detection of environmental sensory inputs, including the tactile sense, proprioception, temperature, and nociception (Roos EM et al., 2011). Proprioception, including the sense of position in space, underlies the ability to maintain erect posture, control joint movements and respond to perturbations (Roos EM et al., 2011). The link between proprioception and osteoarthritis is not only based on theoretical reasoning. Patients with knee osteoarthritis had significantly worse proprioceptive capacities than age-matched, normal individuals (Koralewicz LM & Engh GA, 2000; Pai YC et al., 1997; Roos EM et al., 2011; Sharma L, 1999). Impaired proprioception contributes to articular cartilage damage (Roos EM et al., 2011; Sharma L & Pai YC, 1997). Functional consequences of impaired proprioception include lower gait velocity, shorter stride length, and slower stair walking time (Sharma L & Pai YC, 1997). The study of long-term influence of proprioception impairment on osteoarthritis has a major confounding factor, as proprioception declines with age (Hurley MV et al., 1998; Pai YC et al., 1997), and older age is the most important risk factor for developing osteoarthritis (Roos EM et al., 2011). Proprioception would have a role as a risk factor for osteoarthritis progression (Roos EM et al., 2011), but not for osteoarthritis onset (Felson DT et al., 2009). Unfortunately, the relationship between afferent somatosensory system and protective or damaging muscle activity has been minimally evaluated in the setting of osteoarthritis (Sharma L & Pai YC,

Roos and colleagues summarized their extensive review of this factor in two main issues. First, exercise training interventions should address both muscle weakness and afferent sensory dysfunction (Roos EM et al., 2011). Second, exercise regimens that aim to achieve modification of joint loading or cartilage structure seem to be more promising in at-risk

Professor Joseph A. Buckwalter established a clear differentiation between the occurrences of osteoarthritis after exercise and sports exposition in normal or previously injured joints (Buckwalter JA, 2003; 2004). The investigation of the link between sports and osteoarthritis should not take into account athletes with significant joint injuries, as osteoarthritis may be a

individuals or those with early disease (Roos EM et al., 2011).

**5. Exercise and sports participation**

osteoarthritis progression.

1997).

anterior cruciate ligament injuries would also cause knee instability and a loss of smooth control of agonist and antagonist muscle interaction, contributing to the accelerated degeneration of the joint (Brandt KD, 1997; Herzog W & Longino D, 2007; Roos EM et al., 2011).

Neuman and colleagues observed the incidence of radiographic osteoarthritis in a cohort of patients with unilateral, acute anterior cruciate ligament tears undergoing non-operative treatment with neuromuscular training and early activity modification after 10-to-15 years (Neuman P et al., 2008). The authors found that all patients developing knee osteoarthritis were previously meniscectomized. None of the remaining non-meniscectomized patients had radiographic signs of knee osteoarthritis at 10-to-15 years of follow-up. Sixty-eight percent of patients had asymptomatic knees. The authors concluded that non-operative treatment of anterior cruciate ligament tears by means of neuromuscular training and early activity modification might also have been related to the low prevalence of radiographic knee osteoarthritis (Neuman P et al., 2008). Ageberg and colleagues reported a longitudinal prospective cohort study of 100 anterior cruciate ligament-deficient patients undergoing conservative treatment with neuromuscular training and activity modification (Ageberg E et al., 2007). The majority of patients in this study demonstrated good functional performance and knee muscle strength throughout the 15-year study with this treatment without undergoing reconstructive surgery. The main concern of this study was the lack of a matched comparative group. If reconstruction of anterior cruciate ligament is performed, Keays and colleagues found that the restoration of quadriceps-to-hamstring strength balance was associated with less osteoarthritis (Keays SL et al., 2010). Therefore, protection of articular cartilage when anterior cruciate ligament injury occurs may be more related to the neuromuscular training than the reconstruction of the torn ligament itself (Keays SL et al., 2010; Lohmander LS et al., 2007; Neuman P et al., 2008). Thus, early activity modification and neuromuscular knee rehabilitation after anterior cruciate ligament injury may be a very important aspect to decrease the impairment of the neuromuscular system.

Quadriceps and hip muscles weakness are common in patients with knee osteoarthritis (Felson DT et al., 2000; Hinman RS et al., 2010). Roos and colleagues suggested that muscle weakness might be a risk factor related to all of the most important risk factors for osteoarthritis, as muscle strength is lower in women than in men, is reduced following injury, decreases with age and is lower relative to overall body mass in obese individuals (Roos EM et al., 2011). Taking into account this relationship, the study of the isolated role of muscle weakness in osteoarthritis may be difficult. The combination of muscle weakness with other risk factors would increase the risk of osteoarthritis more than muscle weakness alone (Roos EM et al., 2011). It has been argued that muscle weakness would be the consequence of atrophy due to minimized use of painful joints (Felson DT et al., 2000). However, it is also present in patients with knee osteoarthritis who have no history of joint pain (Felson DT et al., 2000), so it would be a risk factor for structural damage to the joint and not only a consequence of a painful joint (Slemenda C et al., 1998). Thus, muscle weakness may be considered an independent risk factor for knee osteoarthritis (Roos EM et al., 2011). Slemenda and colleagues evaluated the baseline knee extensor strength in a cohort of women without radiographic knee osteoarthritis (Slemenda C et al., 1998). After 30 months, radiographs were taken from this sample and results demonstrated that those women with radiographic knee osteoarthritis had lower baseline strength values compared to subjects without it (Slemenda C et al., 1998). For each 10-lb-ft increase in knee extensor strength, Slemenda and colleagues found a 20% reduction in the odds ratio of prevalent

anterior cruciate ligament injuries would also cause knee instability and a loss of smooth control of agonist and antagonist muscle interaction, contributing to the accelerated degeneration of the joint (Brandt KD, 1997; Herzog W & Longino D, 2007; Roos EM et al.,

Neuman and colleagues observed the incidence of radiographic osteoarthritis in a cohort of patients with unilateral, acute anterior cruciate ligament tears undergoing non-operative treatment with neuromuscular training and early activity modification after 10-to-15 years (Neuman P et al., 2008). The authors found that all patients developing knee osteoarthritis were previously meniscectomized. None of the remaining non-meniscectomized patients had radiographic signs of knee osteoarthritis at 10-to-15 years of follow-up. Sixty-eight percent of patients had asymptomatic knees. The authors concluded that non-operative treatment of anterior cruciate ligament tears by means of neuromuscular training and early activity modification might also have been related to the low prevalence of radiographic knee osteoarthritis (Neuman P et al., 2008). Ageberg and colleagues reported a longitudinal prospective cohort study of 100 anterior cruciate ligament-deficient patients undergoing conservative treatment with neuromuscular training and activity modification (Ageberg E et al., 2007). The majority of patients in this study demonstrated good functional performance and knee muscle strength throughout the 15-year study with this treatment without undergoing reconstructive surgery. The main concern of this study was the lack of a matched comparative group. If reconstruction of anterior cruciate ligament is performed, Keays and colleagues found that the restoration of quadriceps-to-hamstring strength balance was associated with less osteoarthritis (Keays SL et al., 2010). Therefore, protection of articular cartilage when anterior cruciate ligament injury occurs may be more related to the neuromuscular training than the reconstruction of the torn ligament itself (Keays SL et al., 2010; Lohmander LS et al., 2007; Neuman P et al., 2008). Thus, early activity modification and neuromuscular knee rehabilitation after anterior cruciate ligament injury may be a very

important aspect to decrease the impairment of the neuromuscular system.

Quadriceps and hip muscles weakness are common in patients with knee osteoarthritis (Felson DT et al., 2000; Hinman RS et al., 2010). Roos and colleagues suggested that muscle weakness might be a risk factor related to all of the most important risk factors for osteoarthritis, as muscle strength is lower in women than in men, is reduced following injury, decreases with age and is lower relative to overall body mass in obese individuals (Roos EM et al., 2011). Taking into account this relationship, the study of the isolated role of muscle weakness in osteoarthritis may be difficult. The combination of muscle weakness with other risk factors would increase the risk of osteoarthritis more than muscle weakness alone (Roos EM et al., 2011). It has been argued that muscle weakness would be the consequence of atrophy due to minimized use of painful joints (Felson DT et al., 2000). However, it is also present in patients with knee osteoarthritis who have no history of joint pain (Felson DT et al., 2000), so it would be a risk factor for structural damage to the joint and not only a consequence of a painful joint (Slemenda C et al., 1998). Thus, muscle weakness may be considered an independent risk factor for knee osteoarthritis (Roos EM et al., 2011). Slemenda and colleagues evaluated the baseline knee extensor strength in a cohort of women without radiographic knee osteoarthritis (Slemenda C et al., 1998). After 30 months, radiographs were taken from this sample and results demonstrated that those women with radiographic knee osteoarthritis had lower baseline strength values compared to subjects without it (Slemenda C et al., 1998). For each 10-lb-ft increase in knee extensor strength, Slemenda and colleagues found a 20% reduction in the odds ratio of prevalent

2011).

radiographic knee osteoarthritis and a 29% reduction in the odds ratio of symptomatic knee osteoarthritis (Slemenda C et al., 1997). In an experimental animal model study, Longino and colleagues induced quadriceps muscle weakness by injecting botulinum toxin A into muscles (Longino D et al., 2005). Only 4 weeks after the induction of muscle weakness, the authors found retropatellar cartilage degeneration in the experimental rabbits compared to control rabbits. Segal and colleagues found that greater knee extensor strength protected against development of incident symptomatic, but not radiographic, knee osteoarthritis in both sexes (Segal NA et al., 2009; 2010). Subjects with greater quadriceps strength also had less knee pain and better physical function over follow-up (Amin S et al., 2009). Some of the benefits of neuromuscular training on knee osteoarthritis may be explained by induced changes in glycosaminoglycan content (Roos EM & Dahlberg LE, 2005). While there seems to be a protective effect of muscle strengthening against the onset of osteoarthritis, that seems to be controversial for osteoarthritis progression (Roos EM et al., 2011). Further welldesigned studies are needed to elucidate if muscle strengthening would prevent osteoarthritis progression.

The afferent somatosensory system comprises the receptors, afferent neurons and central processing centers that permit the detection of environmental sensory inputs, including the tactile sense, proprioception, temperature, and nociception (Roos EM et al., 2011). Proprioception, including the sense of position in space, underlies the ability to maintain erect posture, control joint movements and respond to perturbations (Roos EM et al., 2011). The link between proprioception and osteoarthritis is not only based on theoretical reasoning. Patients with knee osteoarthritis had significantly worse proprioceptive capacities than age-matched, normal individuals (Koralewicz LM & Engh GA, 2000; Pai YC et al., 1997; Roos EM et al., 2011; Sharma L, 1999). Impaired proprioception contributes to articular cartilage damage (Roos EM et al., 2011; Sharma L & Pai YC, 1997). Functional consequences of impaired proprioception include lower gait velocity, shorter stride length, and slower stair walking time (Sharma L & Pai YC, 1997). The study of long-term influence of proprioception impairment on osteoarthritis has a major confounding factor, as proprioception declines with age (Hurley MV et al., 1998; Pai YC et al., 1997), and older age is the most important risk factor for developing osteoarthritis (Roos EM et al., 2011). Proprioception would have a role as a risk factor for osteoarthritis progression (Roos EM et al., 2011), but not for osteoarthritis onset (Felson DT et al., 2009). Unfortunately, the relationship between afferent somatosensory system and protective or damaging muscle activity has been minimally evaluated in the setting of osteoarthritis (Sharma L & Pai YC, 1997).

Roos and colleagues summarized their extensive review of this factor in two main issues. First, exercise training interventions should address both muscle weakness and afferent sensory dysfunction (Roos EM et al., 2011). Second, exercise regimens that aim to achieve modification of joint loading or cartilage structure seem to be more promising in at-risk individuals or those with early disease (Roos EM et al., 2011).

#### **5. Exercise and sports participation**

Professor Joseph A. Buckwalter established a clear differentiation between the occurrences of osteoarthritis after exercise and sports exposition in normal or previously injured joints (Buckwalter JA, 2003; 2004). The investigation of the link between sports and osteoarthritis should not take into account athletes with significant joint injuries, as osteoarthritis may be a

Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies 183

consequence of the injury instead of the exposition to exercise itself. Professor Buckwalter differentiated between activities like running and others with higher impact and torsional loads (Buckwalter JA & Martin JA, 2004), as higher impact loads produce a higher cartilage deformation compared to lower loads (Eckstein F et al., 2005). Although running may be the main action of many sports, this type of exercise will be differentiated from cutting sports because of his different prognosis with respect to osteoarthritis (Buckwalter JA & Martin JA, 2004). Following this distinction, an up-to-date review of the existing literature is presented in chronological order throughout the coming paragraphs.

#### **5.1 Running**

All identified studies dealing with the association between running and osteoarthritis are summarized in Table 1. As shown, 39 articles were found but only 15 were specifically conducted to assess the risk of running in the development of osteoarthritis (Fries JF et al., 1994; Konradsen L et al., 1990; Kujala UM et al., 1999; Lane NE et al., 1986; Lane NE et al., 1987; Lane NE et al., 1990; Lane NE et al., 1993; Lane NE et al., 1998; Marti B et al., 1989; McDermott M & Freyne P, 1983; Panush RS et al., 1986; Panush RS et al., 1995; Puranen J et al., 1975; Wang BW et al., 2002; Ward MM et al., 1995). The other 24 studies have combined the exposure of running and other sports to assess the risk of osteoarthritis or general disability.  Of all studies dealing with running, 10.2% studied general disability and 10.2% spine, 7.7% hand, 46% hip, 74.3% knee, and 10.2% ankle osteoarthritis. All but 4 studies concluded that running was not associated with an increased risk of osteoarthritis. Four studies found that running increased the risk of hip and knee osteoarthritis (Cheng Y et al., 2000; Marti B et al., 1989; McDermott M & Freyne P, 1983; Spector TD et al., 1996b), but 2 of them involved subjects exposed to more physical activities (Cheng Y et al., 2000; Spector TD et al., 1996b). No studies have demonstrated a clear increase in the risk of spine, hand or ankle osteoarthritis after running exposure. Most common sources of bias in these reviewed studies were recall and selection bias, and lack of control of other potential risk factors for osteoarthritis. In fact, many of them did not adjusted the analysis for previous joint injury, body mass index or occupational workload (Table 1). Fifteen studies may be classified as Level II-evidence (38%), 19 as Level IIIevidence (49%), and 5 as Level IV-evidence (13%).

#### **5.2 Sports participation**

Sports with higher impact and torsional loads may increase the risk of osteoarthritis more than straight-ahead sports or exercise. Theoretically, sports such as cycling, swimming, or golf may not be considered among those with higher risk of osteoarthritis. For a complete classification of sports depending on the intensity of joint impact and torsional loads, the reader is directed towards the article by Buckwalter and Martin (Buckwalter JA & Martin JA, 2004).

consequence of the injury instead of the exposition to exercise itself. Professor Buckwalter differentiated between activities like running and others with higher impact and torsional loads (Buckwalter JA & Martin JA, 2004), as higher impact loads produce a higher cartilage deformation compared to lower loads (Eckstein F et al., 2005). Although running may be the main action of many sports, this type of exercise will be differentiated from cutting sports because of his different prognosis with respect to osteoarthritis (Buckwalter JA & Martin JA, 2004). Following this distinction, an up-to-date review of the existing literature is presented

All identified studies dealing with the association between running and osteoarthritis are summarized in Table 1. As shown, 39 articles were found but only 15 were specifically conducted to assess the risk of running in the development of osteoarthritis (Fries JF et al., 1994; Konradsen L et al., 1990; Kujala UM et al., 1999; Lane NE et al., 1986; Lane NE et al., 1987; Lane NE et al., 1990; Lane NE et al., 1993; Lane NE et al., 1998; Marti B et al., 1989; McDermott M & Freyne P, 1983; Panush RS et al., 1986; Panush RS et al., 1995; Puranen J et al., 1975; Wang BW et al., 2002; Ward MM et al., 1995). The other 24 studies have combined the exposure of running and other sports to assess the risk of osteoarthritis or general disability.  Of all studies dealing with running, 10.2% studied general disability and 10.2% spine, 7.7% hand, 46% hip, 74.3% knee, and 10.2% ankle osteoarthritis. All but 4 studies concluded that running was not associated with an increased risk of osteoarthritis. Four studies found that running increased the risk of hip and knee osteoarthritis (Cheng Y et al., 2000; Marti B et al., 1989; McDermott M & Freyne P, 1983; Spector TD et al., 1996b), but 2 of them involved subjects exposed to more physical activities (Cheng Y et al., 2000; Spector TD et al., 1996b). No studies have demonstrated a clear increase in the risk of spine, hand or ankle osteoarthritis after running exposure. Most common sources of bias in these reviewed studies were recall and selection bias, and lack of control of other potential risk factors for osteoarthritis. In fact, many of them did not adjusted the analysis for previous joint injury, body mass index or occupational workload (Table 1). Fifteen studies may be classified as Level II-evidence (38%), 19 as Level III-

Sports with higher impact and torsional loads may increase the risk of osteoarthritis more than straight-ahead sports or exercise. Theoretically, sports such as cycling, swimming, or golf may not be considered among those with higher risk of osteoarthritis. For a complete classification of sports depending on the intensity of joint impact and torsional loads, the reader is directed

towards the article by Buckwalter and Martin (Buckwalter JA & Martin JA, 2004).

in chronological order throughout the coming paragraphs.

evidence (49%), and 5 as Level IV-evidence (13%).

**5.2 Sports participation**

**5.1 Running**

y, years; OA, osteoarthritis; BMI, body mass index; min, minutes; JSN, joint space narrowing; vs, versus; SEM, Standard error of the mean; kg,

kilogram; TKA, total knee arthroplasty; Kcal, kilocalories; OR, odds ratio (95% interval confidence); RR, relative risk (95% interval confidence); SD,

standard deviation; WL, weight lifters; TF, tibiofemoral; PF, patellofemoral; h, hours; ERT, estrogen replacement therapy; HR, hazard ratio (95%

interval confidence); km, kilometre; MRI, magnetic resonance imaging. Table 1. Summary of studies evaluating the risk of osteoarthritis after exposure to running.

y, years; OA, osteoarthritis; BMI, body mass index; min, minutes; JSN, joint space narrowing; vs, versus; SEM, Standard error of the mean; kg,

Osteoarthritis in Sports and Exercise: Risk Factors and Preventive Strategies 197