Association of Squatting With Increased Prevalence of Radiographic Tibiofemoral Knee Osteoarthritis

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1 ARTHRITIS & RHEUMATISM Vol. 50, No. 4, April 2004, pp DOI /art , American College of Rheumatology Association of Squatting With Increased Prevalence of Radiographic Tibiofemoral Knee Osteoarthritis The Beijing Osteoarthritis Study Yuqing Zhang, 1 David J. Hunter, 1 Michael C. Nevitt, 2 Ling Xu, 3 Jingbo Niu, 1 Li-Yung Lui, 2 Wei Yu, 3 Piran Aliabadi, 4 and David T. Felson 1 Objective. To examine the association between squatting, a common daily posture in China, and the prevalence of radiographic osteoarthritis (OA) in different knee compartments among Chinese subjects from Beijing, and to estimate how much of the difference in prevalence of knee OA between Chinese subjects in Beijing and white subjects in Framingham, Massachusetts is accounted for by the impact of squatting. Methods. We recruited a random sample of Beijing residents age >60 years. Subjects answered questions on joint symptoms, and knee radiographs were obtained. Subjects were also asked to recall the average amount of time spent squatting each day at age 25 years. Radiographic films (weight-bearing anteroposterior and skyline views) were read for Kellgren/Lawrence (K/L) grade and individual radiographic features. Medial disease was defined when radiographs showed a K/L grade of >2 at the tibiofemoral joint and a medial joint space narrowing score of >1, and lateral disease was assessed in a comparable manner in the lateral compartments. We examined the association of squatting with the prevalence of tibiofemoral OA as well as with the prevalence of patellofemoral knee OA, while adjusting for age and other potential confounding factors. We Supported by NIH grants AR and AR Yuqing Zhang, DSc, David J. Hunter, MD, PhD, Jingbo Niu, MD, David T. Felson, MD, MPH: Boston University School of Medicine, Boston, Massacusetts; 2 Michael C. Nevitt, PhD, Li-Yung Lui, MS: University of California, San Francisco; 3 Ling Xu, MD, Wei Yu, MD: Peking Union Medical College Hospital, Beijing, China; 4 Piran Aliabadi, MD: Brigham and s Hospital, Boston, Massacusetts. Address correspondence and reprint requests to Yuqing Zhang, DSc, A203, Boston University School of Medicine, 715 Albany Street, Boston, MA Submitted for publication March 14, 2003; accepted in revised form December 17, used the same approach to assess the relationship between squatting and tibiofemoral OA in the medial compartment and in the lateral compartment. Finally, we estimated the impact of squatting at age 25 on the difference in prevalence of knee OA between Chinese subjects in Beijing and white subjects in the Framingham OA Study. Results. Squatting was very common among the Chinese subjects: 40% of men and 68% of women reported squatting >1 hour per day at age 25. The prevalence of tibiofemoral OA increased as the time spent squatting at age 25 increased in both the men and the women. Compared with subjects who squatted <30 minutes per day at age 25, the multivariable-adjusted prevalence odds ratios of tibiofemoral OA were 1.1 for time spent squatting of minutes/day, 1.0 for minutes/day, 1.7 for minutes/day, and 2.0 for >120 minutes/day among the men (P for trend 0.074), and the respective odds ratios among the women were 1.4, 1.3, 1.2, and 2.4 (P for trend 0.077). A weaker association with patellofemoral OA was found. Prolonged squatting in daily life was more strongly associated with medial knee OA than with lateral disease in the men, but had a similar effect on both knee compartments in the women. After adjusting for the impact of squatting, the age-adjusted difference in prevalence of tibiofemoral OA was reduced from an excess of 14.4% to 9.5% in the Chinese women, but the difference in prevalence of tibiofemoral OA in the Chinese men increased after adjustment for age and squatting, from 2.9% lower to 7.0% lower as compared with their white counterparts. Conclusion. Prolonged squatting is a strong risk factor for tibiofemoral knee OA among elderly Chinese subjects in Beijing, and accounts for a substantial 1187

2 1188 ZHANG ET AL proportion of the difference in prevalence of tibiofemoral OA between Chinese subjects in Beijing and white subjects in Framingham. Although elderly residents of Beijing, China are thinner than white subjects in Framingham, Massachusetts, the prevalence of knee osteoarthritis (OA) in elderly Chinese men is similar to, and in elderly Chinese women even higher than, that in the white men and women of the Framingham cohort (1). This finding prompted us to investigate the risk factors that may increase the prevalence of knee OA among Chinese subjects, especially the Chinese women. Several investigators have reported that occupational squatting is a strong risk factor for knee OA (2 6), and biomechanical studies suggest that deep squatting increases contact force across the tibiofemoral joints (7) more so than across the patellofemoral joints (8). Other investigators have also found that the distribution of contact forces between the medial tibiofemoral compartment and the lateral tibiofemoral compartment is different depending on the angle of flexion (7). The maximum contact force at the medial compartment is greater than that at the lateral compartment when the flexion angle of the knee is 90 (9 11); however, such data are unavailable for deep squatting. In Western societies, squatting in occupational activities often occurs in conjunction with other heavy labor. Any of these activities may increase the risk of knee OA, thus confounding the relationship between squatting and knee OA. Nonoccupational squatting is a common posture in daily living among Chinese men and women (12), and this phenomenon is also prevalent in other Asian countries. Thus, Asian populations provide a unique opportunity to assess the effect of squatting during daily living on the risk of knee OA. Using data collected from the Beijing OA Study, we examined the association between squatting in daily living and the prevalence of knee OA. We assessed whether squatting has a different effect on OA in different knee compartments. We also estimated the proportion of the difference in prevalence of knee OA that is accounted for by the impact of squatting among the Chinese subjects in Beijing as compared with that among the white subjects in Framingham. SUBJECTS AND METHODS The Beijing OA Study. The study design has been described in detail previously (1,13). Briefly, we recruited a random sample of men and women age 60 years from 4 central districts of Beijing, China. Subjects were interviewed at their homes by trained health professional interviewers. We administered a standardized questionnaire that focused on joint symptoms, previous diagnoses of arthritis, and possible risk factors for OA. Subjects were asked to recall how much time they spent squatting per day, on average, at age 25 years, including squatting while using the toilet, talking, cooking, eating, doing housework, washing clothes, and working. At the end of the interview, subjects were invited to the central examination site at Peking Union Medical College Hospital for clinical evaluation. Each subject s height was measured using the wallmounted Harpenden stadiometer (Holtain, Crosswell, Wales, UK), and weight was assessed using a balanced beam scale with a precision to 0.1 kg. Calibration of the scale and stadiometer was checked regularly using external standards. Quadriceps strength was tested isometrically on each leg separately using a spring-loaded strain gauge attached to a specially constructed chair. Bone mineral density was assessed at the proximal femur using a dual x-ray absorptiometer (GE-Lunar Corporation, Madison, WI). Using the Framingham OA Study protocol, all subjects were assessed with a single anteroposterior (AP) radiograph of both knees, with the knee joints fully extended and in a weight-bearing position, and a weight-bearing skyline view was obtained using the protocol of Buckland-Wright (14). Radiograph reading. A single bone and joint radiologist (PA), who is the reader for the Framingham OA Study, read all knee films, including the AP and skyline views, using the Kellgren/Lawrence (K/L) scale (15) and by identifying individual radiographic features of OA. Joint space narrowing (JSN) on the AP view was read in the medial and lateral compartments and scored on a 0 3 scale using the Osteoarthritis Research Society International Atlas (16). The weighted kappa for the K/L grade (scale 0 4) for intrareader reliability was 0.79 (95% confidence interval [95% CI] ). The small number of disagreements was not in any particular direction, suggesting that there was little likelihood of bias in estimates. Radiographic tibiofemoral OA was defined as a K/L grade of 2 on the AP view. Medial OA in the tibiofemoral knee joint was defined as a K/L grade of 2 and medial JSN score of 1 on a 0 3 scale. Lateral OA in the tibiofemoral joint was also defined as a K/L grade of 2 and lateral JSN score of 1. For the skyline view, we adopted the scoring criteria previously described by one of the authors (DTF) and his colleagues (16). Briefly, individual radiographic features and overall grades of OA in the patellofemoral compartment on the skyline view were read according to the following schemes: osteophytes on a 0 3 scale, JSN on a 0 3 scale, sclerosis on a 0 3 scale, and cysts as present or absent. A knee was defined as having patellofemoral OA if either an osteophyte of severity grade 2 was present or moderate to severe JSN ( 2 ona0 3 scale) with concurrent grade 1 osteophytes in the patellofemoral joint was present. Statistical analysis. We excluded subjects with rheumatoid arthritis (RA) from the present analysis. To identify subjects with RA, we asked all subjects whether they had ever been diagnosed as having RA. In the Beijing OA Study, we also asked subjects about another diagnosis, rheumatic arthritis, which we thought might be reported as RA by the

3 SQUATTING AND RADIOGRAPHIC TIBIOFEMAL KNEE OA 1189 subjects. If the subjects reported having RA and taking secondline drugs for RA, we characterized them as having RA. In addition, if a subject s hand radiographs revealed typical radiographic evidence of RA, even if that person did not report RA or rheumatic arthritis during the interview, he or she was excluded. We divided time spent squatting at age 25 into 5 categories: 30, 30 59, , , and 180 minutes/ day. For each sex, we calculated the prevalence of tibiofemoral knee OA according to the time spent squatting at age 25. We then examined the association of squatting at age 25 with the prevalence of tibiofemoral OA, using generalized estimating equations with each knee as an observation unit. Variables included in the generalized estimating equation model were age, years of education (1 6 years, 7 9 years, years, and 13 years), smoking status (nonsmoker, ex-smoker, and current smoker), body mass index, history of knee injury (yes versus no), Physical Activity Index, bone density at the femoral neck, and isometric quadriceps strength. We tested the significance of the trend in the prevalence of tibiofemoral OA by including in the model a single variable for time spent squatting. We used the same approach to assess the association between squatting at age 25 and the prevalence of patellofemoral OA. We also explored whether the impact of squatting at Table 1. Study* Characteristics of participants in the Beijing Osteoarthritis Characteristic (n 755) (n 1,103) Age, years Height, meters BMI, kg/m Bone density at femoral neck, gm/cm Quadriceps strength, kg Physical Activity Index Smoking status, no. (%) Current smoker 265 (35.1) 190 (17.2) Past smoker 242 (32.0) 99 (9.0) Never smoker 248 (32.9) 813 (73.8) Years of education, no. (%) (73.0) 970 (87.9) (9.5) 57 (5.2) (13.3) 60 (5.4) (4.2) 16 (1.5) History of knee injury, no. (%) No 718 (95.1) 1034 (93.8) Yes 37 (4.9) 68 (6.2) Squatting at age 25 by minutes/day, no. (%) (28.5) 147 (13.5) (31.0) 191 (17.6) (29.2) 445 (40.9) (6.9) 234 (21.5) (4.4) 71 (6.5) * Except where indicated otherwise, values are the mean SD. BMI body mass index. The Physical Activity Index is a Framingham Study measure translated into Chinese, which sums the energy expenditure of each hour s activities in a typical day. Twelve men and 15 women had missing values on the time spent squatting at age 25 years. Table 2. Association between squatting at age 25 and prevalence of radiographic tibiofemoral osteoarthritis (TFOA) among Chinese subjects from Beijing* Sex, squatting at age 25 by minutes/day No. of subjects Prevalence of TFOA, % Ageadjusted Multivariableadjusted (95% CI) ( ) ( ) ( ) ( ) P for trend ( ) ( ) ( ) ( ) P for trend * odds ratio; 95% CI 95% confidence interval. age 25 on prevalence of tibiofemoral OA differed between the medial and lateral compartments. To estimate how much of the difference in the prevalence of knee OA between Chinese subjects in Beijing and white subjects in Framingham, Massachusetts was accounted for by the impact of squatting, we calculated both age-adjusted and age- and squatting-adjusted differences in the prevalence of knee OA between the Chinese subjects and the white subjects (17); we then assessed the impact of squatting on the difference in prevalence of knee OA between the 2 racial groups by comparing the prevalence differences before and after adjustment for squatting. In this analysis, we assumed that all white subjects in the Framingham population squatted 30 minutes per day at age 25. RESULTS Of 2,269 age-eligible Chinese subjects contacted during door-to-door canvassing, 2,031 (89.5%) completed the home interview, and 1,858 (81.9%) had a clinical examination and knee radiographs. Three subjects with RA were excluded from the present analysis. The characteristics of the participants in the Beijing Osteoarthritis Study are presented in Table 1. The average body mass index was 25.2 kg/m 2 in the male Chinese subjects and 26.0 kg/m 2 in the female Chinese subjects in Beijing. These elderly Chinese subjects were thinner compared with their elderly white counterparts (both in the Framingham cohort and in many other white populations). Smoking was very common among the Chinese men, whereas about onequarter of the Chinese women had a history of smoking. About three-quarters of the Chinese men and almost

4 1190 ZHANG ET AL Table 3. Association between squatting at age 25 and prevalence of medial and lateral TFOA among Chinese subjects from Beijing* Sex, squatting Multivariable-adjusted (95% CI) at age 25 by minutes/day Medial TFOA Lateral TFOA ( ) 1.2 ( ) ( ) 0.7 ( ) ( ) 1.3 ( ) ( ) 1.2 ( ) P for trend ( ) 1.2 ( ) ( ) 1.4 ( ) ( ) 1.3 ( ) ( ) 2.2 ( ) P for trend * See Table 2 for definitions. 90% of the Chinese women had not graduated from high school. Among the study subjects, squatting was very common. About 40% of the men and 68% of the women in Beijing reported that they had squatted 1 hour per day, on average, at age 25. Table 2 presents the association between squatting at age 25 and the prevalence of tibiofemoral knee OA. Among the Chinese men, the prevalence of tibiofemoral OA increased with longer time spent squatting. After adjustment for age and other risk factors, in comparison with the men who reported squatting 30 minutes per day, those squatting minutes per day had a 70% increased likelihood of having tibiofemoral OA, whereas those squatting 180 minutes per day Table 4. Association between squatting at age 25 and prevalence of radiographic patellofemoral osteoarthritis (PFOA) among Chinese subjects from Beijing* Sex, squatting at age 25 by minutes/day No. of subjects Prevalence of PFOA, % Ageadjusted Multivariableadjusted (95% CI) ( ) ( ) ( ) ( ) ( ) ( ) ( ) ( ) * See Table 2 for other definitions. Table 5. Impact of squatting at age 25 on the difference in prevalence of tibiofemoral osteoarthritis (TFOA) between Chinese subjects in Beijing and white subjects in Framingham, Massachussetts Difference in prevalence of TFOA, % Adjustment for age Adjustment for age and squatting Absolute change in prevalence after adjustment for squatting had an almost 2 times greater likelihood of having the disease. The test for trend showed borderline statistical significance (P 0.074). Squatting at age 25 also increased the prevalence of tibiofemoral OA among the Chinese women (P for trend 0.077), especially among those who squatted 180 minutes per day at age 25 (odds ratio 2.4, 95% CI ). The effect of squatting on the likelihood of developing medial tibiofemoral OA appeared greater than that for lateral tibiofemoral OA (Table 3). However, prolonged squatting appeared to increase the prevalence of OA at both the medial and lateral compartments in women. When an alternate definition was used to define medial and lateral OA, i.e., medial or lateral JSN score of 2 on a 0 3 scale, similar results were obtained. The association between squatting and the prevalence of patellofemoral OA is shown in Table 4. Although prolonged time spent squatting was also associated with an increased prevalence of patellofemoral OA in both Chinese men and Chinese women, the magnitude of the association was smaller than that for tibiofemoral OA. Table 5 presents the impact of squatting on the difference in prevalence of tibiofemoral OA between the Chinese subjects from Beijing and the white subjects from Framingham. After adjustment for age, the absolute prevalence of tibiofemoral OA in the Chinese women was higher than in the white women, by 14.4%. However, with further adjustment for the time spent squatting at age 25, the difference in prevalence was reduced to 9.5%. Among the men, the age-adjusted prevalence of tibiofemoral OA was only slightly lower in the Chinese subjects compared with the white subjects, by 2.9%. However, after adding the impact of squatting into the model, the difference became greater, with the adjusted prevalence of tibiofemoral OA in the Chinese men being 7.0% less than in the white men.

5 SQUATTING AND RADIOGRAPHIC TIBIOFEMAL KNEE OA 1191 DISCUSSION Using data collected from the Beijing OA Study, we found that squatting is a common posture among Chinese men and women, and prolonged squatting in daily life is associated with an increased prevalence of knee OA, especially tibiofemoral knee OA. The time spent squatting at age 25 accounts for a substantial proportion of the difference in the prevalence of tibiofemoral OA between the Chinese subjects in Beijing and the white subjects in Framingham. Several studies have shown that occupational squatting is associated with an increased risk of knee OA (2 6). Jobs involving squatting often require other types of activities as well, such as kneeling or lifting heavy loads, and persons with these kinds of jobs may also differ from others by having other risk factors for knee OA, such as knee injury. In the present study, squatting assessed at age 25 included that performed in both nonoccupational and occupational settings; thus, we were unable to separate the effect of occupational squatting from that of nonoccupational squatting. Nevertheless, the results of this study corroborate previous findings, in that we provided additional evidence that prolonged squatting is a risk factor for tibiofemoral knee OA. We found a greater effect of squatting on medial tibiofemoral OA than on lateral tibiofemoral OA in the Chinese men, but a similar effect of squatting was observed on both knee compartments in the Chinese women. Several investigators have reported that the maximum value of the medial contact force is larger than the maximum lateral contact force at a knee flexion angle of 90 (9 11); such findings, however, are lacking when the flexion angle is more than 120 (deep squatting). Typically, the medial compartment absorbs 60 70% of the force across the knee during weight bearing (18). This disproportionate medial transmission of load results from an adduction moment (18) and reflects the magnitude of intrinsic compressive load on the medial compartment (19). Although the adduction moment in a deep squat may be less than that experienced during walking, the adduction moment remains predominant (20) and likely explains the predilection for OA in the medial compartment in Chinese men. Several factors that differ between men and women may influence the sex-specific effect of squatting on the tibiofemoral compartments. These include pelvic dimensions, knee morphology, Q-angle, and neuromuscular strength (21). For instance, disproportionate loading of the lateral compartment in women likely arises from differences in knee stability/stiffness, which is reduced in women as a result of decreased neuromuscular strength and increased ligamentous laxity (21 23). The greater effect of squatting on tibiofemoral OA than on patellofemoral OA is interesting. Most squatting observed in Chinese subjects is often a deep squat, i.e., 120. As mentioned above, studies have suggested that the contact force on knee joints during squatting varies according to the angle of flexion. During deep squatting, the contact area in the patellofemoral joint shifts to the proximal pole of the patella, and the femoral trochlea articulates with the quadriceps tendon (8,24). Biomechanical data support the notion that the patellofemoral contact force is markedly reduced beyond a flexion angle of 90 (25,26). On the other hand, Dahlkvist et al found that the tibiofemoral joint compression forces during a deep squat are 5 times body weight, and the shear force is 3 4 times body weight (7). This large load is applied over a smaller contact area, since the tibiofemoral contact area decreases by about half in deep flexion (27). Others also demonstrated that the tibiofemoral adduction moments generated from deep squatting are significantly larger than those from walking or stair climbing (20). All these might explain why the relationship of squatting at age 25 with the prevalence of tibiofemoral OA is stronger than that with patellofemoral OA. The present study has several limitations. First, although our data showed that squatting at age 25 was associated with an increased prevalence of tibiofemoral knee OA, the trend was of only borderline statistical significance. The effect was mostly seen among subjects with a history of prolonged squatting, but the percentage of subjects who reported prolonged squatting was relatively small. Furthermore, since very few elderly Chinese subjects in this study did not squat at all at age 25, we used those who squatted less than one-half hour per day as the reference category, and this will certainly dilute the effect of any squatting on knee OA. Second, recall bias for the time spent squatting at age 25 might explain the current positive findings. For example, subjects with symptoms of knee OA may be more likely to report their history of squatting than those without knee symptoms. However, when we excluded subjects with a history of knee pain from the analysis, the association did not change substantially. Third, since we did not collect data on squatting at age 25 from subjects in the Framingham OA Study, we assumed that all of the white subjects had squatted for fewer than 30 minutes each day at age 25. It is quite possible that some subjects in the Framingham OA

6 1192 ZHANG ET AL Study squatted for more than 30 minutes per day at age 25. If so, the magnitude of the difference in prevalence of tibiofemoral OA accounted for by the impact of squatting between the 2 racial groups may be smaller than that reported in the present study. However, it is unlikely that a large proportion of the white subjects in the Framingham cohort would have reported prolonged squatting at age 25. Finally, the unavailability of skyline films in the Framingham OA Study prevented us from comparing racial differences in the prevalence of patellofemoral OA, an important joint from both a clinical and an epidemiologic point of view. In conclusion, we found that squatting at age 25 is a risk factor for knee OA among elderly Chinese subjects in Beijing. Its effect was much stronger on tibiofemoral knee OA than on patellofemoral knee OA. 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