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Effects of Exercise on Patellar Cartilage in Women with Mild Knee Osteoarthritis ¨ KKINEN1,2, MIIKA T. NIEMINEN3,4,5, JARMO KOLI1, JUHANI MULTANEN1,2, URHO M. KUJALA1, ARJA HA 6,7 3,4 ¨ MSA ¨ 3,4,8, RIIKKA AHOLA4,8, HANNU KAUTIAINEN , EVELIINA LAMMENTAUSTA , TIMO JA 9 10 1 ¨ HARRI SELANNE , ILKKA KIVIRANTA , and ARI HEINONEN Department of Health Sciences, University of Jyva¨skyla¨, Jyva¨skyla¨, FINLAND; 2Department of Physical Medicine and Rehabilitation, Central Finland Central Hospital, Jyva¨skyla¨, FINLAND; 3Department of Diagnostic Radiology, Oulu University Hospital, Oulu, FINLAND; 4Medical Research Center Oulu, University of Oulu and Oulu University Hospital, Oulu, FINLAND; 5Department of Radiology, University of Oulu, Oulu, FINLAND; 6Department of General Practice and Primary Healthcare, University of Helsinki, Helsinki, FINLAND; 7Unit of Primary Healthcare, Kuopio University Hospital, Kuopio, FINLAND; 8Department of Medical Technology, Institute of Biomedicine, University of Oulu, Oulu, Finland; 9LIKES Research Center, Jyva¨skyla¨, FINLAND; and 10Department of Orthopedics and Traumatology, University of Helsinki and Helsinki University Hospital, Helsinki, FINLAND 1
ABSTRACT ¨ KKINEN, M. T. NIEMINEN, H. KAUTIAINEN, E. LAMMENTAUSTA, KOLI, J., J. MULTANEN, U. M. KUJALA, A. HA ¨ ¨ ¨ T. JAMSA, R. AHOLA, H. SELANNE, I. KIVIRANTA, and A. HEINONEN. Effects of Exercise on Patellar Cartilage in Women with Mild Knee Osteoarthritis. Med. Sci. Sports Exerc., Vol. 47, No. 9, pp. 1767–1774, 2015. Purpose: This study aims to investigate the effects of exercise on patellar cartilage using T2 relaxation time mapping of magnetic resonance imaging in postmenopausal women with mild patellofemoral joint osteoarthritis (OA). Methods: Eighty postmenopausal women (mean age, 58 (SD, 4.2) yr) with mild knee OA were randomized to either a supervised progressive impact exercise program three times a week for 12 months (n = 40) or a nonintervention control group (n = 40). Biochemical properties of cartilage were estimated using T2 relaxation time mapping, a parameter sensitive to collagen integrity, collagen orientation, and tissue hydration. Leg muscle strength and power, aerobic capacity, and self-rated assessment with the Knee Injury and Osteoarthritis Outcome Score were also measured. Results: After intervention, full-thickness patellar cartilage T2 values had medium-size effect (d = 0.59; 95% confidence interval, 0.16 to 0.97; P = 0.018); the change difference was 7% greater in the exercise group compared with the control group. In the deep half of tissue, the significant exercise effect size was medium (d = 0.56; 95% confidence interval, 0.13 to 0.99; P = 0.013); the change difference was 8% greater in the exercise group compared with controls. Furthermore, significant medium-size T2 effects were found in the total lateral segment, lateral deep, and lateral superficial zones in favor of the exercise group. Extension force was 11% greater (d = 0.63, P = 0.006) and maximal aerobic capacity was 4% greater (d = 0.55, P = 0.028) in the exercise group than in controls. No changes in Knee Injury and Osteoarthritis Outcome Score emerged between the groups. Conclusions: Progressively implemented high-impact and intensive exercise creates enough stimuli and exerts favorable effects on patellar cartilage quality and physical function in postmenopausal women with mild knee OA. Key Words: PHYSICAL FUNCTIONING, REHABILITATION, MAGNETIC RESONANCE IMAGING, PHYSICAL THERAPY
K
nee osteoarthritis (OA) is an age-related joint disease commonly present in postmenopausal women, causing pain and disability. Knee OA is characterized by loss and degeneration of hyaline cartilage (6,11). The knee joint has three compartments: medial tibiofemoral, lateral tibiofemoral, and patellofemoral. The biomechanics of the patellofemoral joint differs from that of the tibiofemoral compartment in mechanical loading (35). Although knee OA exerts influence on all three compartments of the knee, evidence indicates that radiographically isolated patellofemoral OA plays an independent and important role in knee pain and disability in mild knee OA (10,15,23). Radiographic and symptom
Address for correspondence: Ari Heinonen, Ph.D., Department of Health Sciences, University of Jyva¨skyla¨, PO Box 35, Jyva¨skyla¨ 40014, Finland; E-mail: [email protected]. Submitted for publication August 2014. Accepted for publication January 2015. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.acsm-msse.org). 0195-9131/15/4709-1767/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2015 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000629
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changes may be more prevalent in the patellofemoral joint than in the tibiofemoral joint (10,34). More than a third of women older than 60 yr have been reported to have radiographic patellofemoral OA (9). To date, there is no cure for OA (12). It is important, therefore, to find prophylactic means to prevent or at least decelerate the processes of cartilage degeneration (6). Regular exercise is a promising nonpharmacological method that can positively influence cartilage morphology (24,35,38) and biochemical composition (24,28). In addition, exercise has been shown to be effective in reducing pain and in promoting physical functioning in people with knee OA (12). On the other hand, sports-related knee injuries in persons with extremely high physical activity levels and older age are associated with higher knee OA risk and elevated magnetic resonance imaging (MRI) T2 mapping values (3,18,32,35). High T2 values correlate with histological degeneration of cartilage, implying increased free water content and collagen disorientation (8,22). However, in subjects with high OA risk, light exercise has been associated with better cartilage quality (16). In our recently published randomized controlled trial (RCT), we reported that aerobic/step-aerobic exercise had a beneficial effect on bone but did not have a major positive or negative effect on tibiofemoral cartilage (24). In sports, knee injury is the strongest predictor of knee OA (18). In an observational study of the occurrence of tibiofemoral and patellofemoral OA among former athletes, both types of radiographic OA were more common among former weightlifters than among former runners (18). Based on knowledge on patellofemoral biomechanics (5,19), moderate dynamic exercise loading—excluding high injury risk at early knee extension and deep squats with high loads (such as in weightlifting)—should be a favorable stimulus for improving patellar cartilage quality. So far, no RCT has reported on the effects of moderate dynamic exercise on patellar cartilage. Consequently, we investigated the effects of a 12-month supervised aerobic/step-aerobic exercise program on patellar cartilage, using T2 relaxation time mapping, in postmenopausal women with mild tibiofemoral joint OA and usually lacking significant deep cartilage defects of the patella. In addition, we studied the effects of the exercise intervention on physical performance and knee-related symptoms.
MATERIALS AND METHODS Design and Participants This study was a 12-month RCT with two experimental arms: 1) an aerobic/step-aerobic training group and 2) a nontraining control group. The assigned training frequency was three times a week for 12 months. All measurements were performed at baseline (before the intervention) and at the end of the 12-month intervention. All outcome assessors, except for J. Multanen (in patellar cartilage segmentation), were blinded to treatment group assignment. The trial profile is shown in Figure 1.
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Voluntary participants from the Jyva¨skyla¨ region in Central Finland were recruited through a local newspaper advertisement. A total of 298 women responded; after assessment of eligibility by telephone interview, 208 women were then invited for anteroposterior knee x-rays. After the knee x-rays, dual-energy x-ray absorptiometry and clinical examinations were conducted on 80 subjects who met the inclusion criteria. Eligibility criteria were as follows: postmenopause, age 50–65 yr, knee pain on most days, regular intensive exercise no more than twice a week, no illnesses that contraindicated exercise or would limit participation in the exercise program, and grade 1–2 Kellgren–Lawrence (K–L) radiographic tibiofemoral joint OA. Exclusion criteria were as follows: femoral neck bone and lumbar spine bone mineral density (gIcmj2) T-score lower than j2.5 (i.e., indicating osteoporosis), measured with dual-energy x-ray absorptiometry (GE Medical Systems, Lunar Prodigy, Madison, WI, USA); body mass index e35 kgImj2; knee instability or surgery of the knee caused by trauma; inflammatory joint disease; intra-articular steroid injections in the knee in the preceding 12 months; and contraindications to MRI (allergies to contrast agents or renal insufficiency). A statistician randomly allocated each participant to the exercise group (n = 40) or the control group (n = 40) according to a computer-generated blocked randomization list. We used a block size of 10, stratified according to tibiofemoral joint K–L grades 1 and 2. Immediately after randomization, two exercisers withdrew; consequently, baseline data were reported for 78 participants. During the intervention, two participants dropped out (Fig. 1). The study protocol was approved by the Ethics Committee of the Central Finland Health Care District. A written informed consent form was obtained from all participants before enrolment. Exercise Program High-impact multidirectional modified aerobic and stepaerobic jumping exercise programs alternated every 2 wk. Supervised group exercise classes, lasting 55 min, were carried out three times a week for 12 months. Loading was gradually increased after 3 months by progressively raising the height of foam fences from 5 to 20 cm in aerobic exercises, and the height of step benches from 10 to 20 cm in jumping exercises (14,17,36). During exercise sessions, the estimated knee flexion angle varied from 70- to 5-; thus, no deep squats were performed. The exercise protocol is described in more detail in Supplementary Digital Content (see document, Supplemental Digital Content 1, Exercise protocol: training quality, alternation, frequency, time, span and quantity, http://links.lww.com/MSS/A514). Exercise instructors systematically recorded possible injuries and knee pain after every exercise session. The mean knee pain during exercise sessions was 5 mm (SD, 10) (visual analog scale score, 0–100 mm). Measurement of exercise loading. High-impact exercise was quantified by recording the number and intensity of
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FIGURE 1—Flowchart of recruitment process and inclusion of participants. DXA, dual-energy x-ray absorptiometry.
acceleration peaks (impacts) with accelerometers fixed to the waist (Newtest, Oulu, Finland) during one exercise session in each of the 3-month exercise periods (37). The distribution of the number and intensity of impacts is shown in Figure 2, with the impacts being proportional to the number of jumps, steps, and patellar movements made during the exercise sessions. Zero acceleration (g) corresponded to standing. Categorization and labeling are based on Vainionpaa et al. (37), with modifications. They proposed 3.9g as the osteogenic threshold.
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Daily physical activity. Outside intervention sessions, the number and intensity of acceleration peaks (impacts) attributable to daily physical activities from all participants (intervention training classes not included) were measured with accelerometers and are described in detail elsewhere (1,24,37). Daily physical activity was described as daily impact score (DISlog) (1). The mean DISlog outside the intervention sessions was 163 (SD, 43) in the exercise group and 168 (SD, 46) in the control group. There were no
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Muscle power. Leg extensor power in each leg was measured with the Nottingham Power Rig. In each case, the best value (i.e., maximum) performance was taken for analysis (27). Cardiorespiratory fitness. Cardiorespiratory fitness ˙ O2max; mLIkgj1Iminj1) was assessed with a standardized (V ˙ O2max 2-km walk test (UKK Institute, Tampere, Finland). V was estimated based on sex, age, weight, height, heart rate, and measured walking time (20). Questionnaires
FIGURE 2—Number of impacts at four acceleration levels during the intervention. Bars indicate interquartile range. *Indicates zero acceleration (g) is equated to standing still and g = 9.81 mIsj2.
intergroup differences in physical activity or knee loading outside the intervention sessions.
General health and habitual physical activity were assessed with questionnaires at baseline. Baseline habitual physical activity was converted into MET-hours per week (2,17). Perceived pain, knee symptoms, self-rated physical function, sports/recreation, and knee-related quality of life were assessed with the Knee Injury and Osteoarthritis Outcome Score (KOOS) (29). Adverse Events
Controls were requested to maintain their usual activities and were offered the possibility of participating in a social group meeting every third month. Seventy percent of control group participants took part in the meetings, which included lectures on healthy lifestyles (not physical activity or exercise) and stretching exercises.
During the 12-month exercise intervention, only six exercisers consulted the study physician for musculoskeletal injuries or other symptoms (24). Participants whose pain symptoms increased during the intervention were advised to take a short individualized break from training. All these trainees returned to the exercise regimen within 5 to 21 d. In the control group, two visits to the attending physician were made for previous meniscal tear injury and cardiac dysrhythmia. The number of visits to the attending physician did not differ statistically between the groups (P = 0.15).
Primary Outcome Measure
Statistical Methods
Cartilage measurements. Measurement protocol is described in Supplemental Digital Content (see document, Supplemental Digital Content 1, page 1; MRI protocol: participants preparation, MRI–measurement parameters, http://links.lww.com/MSS/A514). T2 relaxation time (T2) (13,25) was determined using a Siemens Magnetom Symphony Quantum 1.5-T scanner (Siemens AG, Medical Solutions, Erlangen, Germany) with a standard transmit/ receive knee array coil. Participants had been lying in the tube for about 40 min before axial T2 series were imaged. Cartilage regions of interest (ROI) from a single transversal slice in the patella were manually segmented using an inhouse MATLAB application (Mathworks, Inc., Natick, MA, USA) (Fig. 3). Cartilage ROI are shown in Figure 3. In our laboratory, the (mean) interobserver error (CVRMS) for T2 full-thickness ROI was 2%.
All analyses were based on intention-to-treat principles. Results were expressed as mean (SD) or median (interquartile range). Statistical comparison between groups was made by chi-square test or Fisher’s exact test and t-test. Statistical comparison of changes in outcome measurements was performed by paired t-test or ANCOVA. Confidence intervals
Control Group
Secondary Outcome Measures Physical performance. Muscle force. Maximal isometric knee extension was measured in sitting position with a knee angle of 60-, using a dynamometer chair (Good Strength; Metitur Oy, Jyva¨skyla¨, Finland) (31). We used the best value (i.e., maximum) of the test attempts of force measurements.
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FIGURE 3—Illustration of ROI in patellar cartilage. ROI are shown in covered areas outlined by continuous lines in a single transversal slice from the middle of the patella. The broken line divides the full-thickness cartilage into the superficial half and the deep half.
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TABLE 1. Baseline demographic and clinical characteristics of the participants. Characteristics
Control Group (n = 40)
58 (4) 165 (6) 73.4 (9.4) 27.1 (3.1) 24 (63) 8 (21) 10 (14) 18.1 (13.1)
59 (4) 161 (5) 69.4 (11.7) 26.7 (4.2) 17 (42) 13 (32) 10 (13) 18.9 (17.2)
18 (47) 5 (13) 15 ( 40)
21 (52) 1 (3) 18 (45)
12 (32) 26 (68)
13 (32) 27 (68)
(CI; 95% CI) for MRI outcome means were obtained by biascorrected bootstrapping (3000 replications). Group differences in MRI, physical performance, and clinical symptom outcomes were adjusted for baseline values. Effect size (d) was calculated using the method of Cohen. An effect size of 0.20 was considered small, 0.50 was medium, and 0.80 was large. CI for effect sizes were obtained by bias-corrected bootstrapping (5000 replications). Statistical analyses were performed using statistical software (Stata, release 13.1; StataCorp, College Station, TX). Before the study, the estimated sample size for power calculation was based on the primary hypothesis. A sample size of 70 subjects (35 in each group) was required to detect a 0.08-g (~2%) difference in femoral neck bone mineral content between the intervention group and the control group (> = 0.05, power, 80%), assuming a dropout rate of approximately 10%. For T2, we were unable to reliably
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Exercise Group (n = 38)
Age, mean (SD), yr Height, mean (SD), cm Body mass, mean (SD), kg Body mass index, mean (SD), kgImj2 Pain killers, n (%) Occasional use of glucosamine, n (%) Knee pain during the last week, mean (SD), mm Habitual physical activity, mean (SD), METIhIwkj1 Patellofemoral K–L grade, n (%) K–L grade 0 K–L grade 1 K–L grade 2 Tibiofemoral K–L grade, n (%) K–L grade 1 K–L grade 2
calculate the intended sample sizes, as previous long-term exercise interventions for cartilage change did not exist.
RESULTS Baseline clinical characteristics of the study groups are given in Table 1. At baseline, no statistically significant differences in any characteristics were observed between the groups, except that the subjects in the exercise group were slightly taller. During the study, two trainees in the exercise group dropped out on weeks 3 and 5; there were no dropouts in the control group. Patellofemoral K–L grading was similar in both groups at baseline (P = 0.21). The mean training compliance was 68%, and the mean training frequency was 2.1 (SD, 0.9) per week (including dropouts). The mean number of measured impacts, and thus patellar movements, during one training class was 2 275 (SD, 343).
TABLE 2. Baseline values, changes, treatment effects, and effects sizes of patellar cartilage T2 relaxation time, KOOS, and physical function measures. Baseline
Quantitative MRI T2 Patella total, ms Superficial, ms Deep, ms Lateral segment Bulk, ms Deep, ms Superficial, ms Medial segment Bulk, ms Deep, ms Superficial, ms Clinical outcomes KOOS (0–100) Pain Symptoms Physical functioning Sport and recreation Quality of life Physical function Knee extension force, Nc Leg power, WIkgj1c V˙O2max, mLIkgj1Iminj1
Changes at 12-Month Time Point
Exercise Group (n = 36)
Control Group (n = 40)
Exercise Group (n = 36)
Control Group (n = 40)
Treatment Effect
Effect Size
Mean (SD)
Mean (SD)
Mean (95% CI)
Mean (95% CI)
Mean (95% CI)
d (95% CI)a
47.9 (7.9) 52.5 (8.2) 43.2 (9.3)
45.7 (6.0) 50.1 (7.1) 41.1 (7.2)
j3.8 (j6.4 to j1.9) j3.9 (j6.9 to j1.7) j3.6 (j6.0 to j1.5)
0.03 (j1.8 to 2.1) 0.1 (j2.4 to 2.5) 0.3 (j1.9 to 2.4)
j3.8 (j6.8 to j0.9) j4.0 (j7.6 to j0.4) j3.9 (j7.0 to j0.8)
49.6 (9.0) 45.1 (11.0) 54.0 (9.1)
46.0 (6.2) 41.3 (8.0) 50.8 (7.5)
j4.9 (j8.0 to j2.4) j4.9 (j7.7 to j2.3) j4.6 (j7.8 to j1.8)
0.6 (j1.6 to 3.2) 0.7 (j2.0 to 3.8) 0.6 (j1.9 to 3.4)
45.9 (8.1) 40.8 (8.8) 50.7 (9.3)
45.7 (8.0) 41.2 (8.4) 49.8 (9.4)
j2.6 (j4.9 to j0.8) j1.9 (j4.5 to 0.01) j3.3 (j6.2 to j1.0)
j0.3 (j2.4 to 2.0) 0.1 (j2.1 to 2.3) 0.4 (j2.3 to 3.0)
86 79 92 78 76
(10) (12) (8) (16) (15)
401 (95) 2.2 (0.5) 29 (3)
87 83 93 78 78
(7) (10) (6) (12) (15)
414 (70) 2.1 (0.5) 29 (4)
4.4 (1 to 8) 1.8 (1 to 8) 1 (j2 to 3) 4 (j2 to 9) 7 (2 to 12)
1.8 1 j0.2 j1 4
(j1 to 4 ) (j3 to 4) (j2 to 1) (j5 to 3) (j0.1 to 8)
21 (j1 to 44) 0.3 (0.1 to 0.4) 1.4 (0.7 to 2.1)
j14 (j29 to 1) 0.2 (0.03 to 0.3) 0.3 (j0.4 to 1)
P Value Crude
Adjustedb
0.59 (0.16 to 0.97) 0.50 (0.09 to 0.91) 0.56 (0.13 to 0.99)
0.010 0.028 0.014
0.018 0.062 0.013
j5.5 (j9.2 to j1.9) j5.6 (j9.5 to j1.6) j5.2 (j9.4 to j1.1)
0.67 (0.26 to 1.06) 0.62 (0.18 to 1.05) 0.58 (0.16 to 0.97)
0.003 0.006 0.013
0.021 0.031 0.047
j2.3 (j5.4 to 0.7) j2.1 (j5.2 to 1.0) j3.6 (j7.3 to 0.06)
0.34 (j0.12 to 0.74) 0.43 (j0.03 to 0.82) 0.29 (j0.16 to 0.70)
0.138 0.192 0.054
0.077 0.047 0.052
0.29 0.36 0.14 0.35 0.20
0.22 0.12 0.53 0.14 0.39
0.22 0.36 0.59 0.14 0.51
0.009 0.24 0.027
0.006 0.20 0.028
2.6 3.8 0.9 5 2.8
(j1 to 4) (j1.5 to 9 ) (j2 to 4) (j2 to 12) (j4 to 9)
35 (9 to 61) j0.1 (j0.3 to 0.04) 1.0 (0.1 to 2.0 )
(j0.18 to (j0.09 to (j0.64 to (j0.16 to (j0.26 to
0.74) 0.13) 0.31) 0.89) 0.64)
0.63 (0.20 to 1.12) 0.28 (j0.18 to 0.79) 0.55 (0.10 to 1.03)
a
Effect size (d ) was calculated using the method of Cohen. Adjusted to baseline values. c Mean of both legs (best attempt). b
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Cartilage measurements. Table 2 gives T2 values at baseline, changes, group differences (i.e., treatment effects), and effect sizes at the end of the 12-month intervention. Differences between T2 values in the superficial layer and T2 values in the deep layer were attributable to natural collagen orientation (high T2 values correspond to cartilage structure degeneration). The exercise intervention had medium-size effect (d = 0.59, P = 0.018) on total patellar cartilage T2 values, and the group change difference was 7%, indicating improved cartilage quality. In the total deep zone, the effect size was medium (d = 0.56, P = 0.013), and the group change difference was 8%. Figure 4 shows group changes in T2 values at the lateral and medial segments of the patellofemoral joint. In the total lateral segment, the effect size was medium (d = 0.67, P = 0.021), and the group change difference was 10%. In addition, the exercise intervention had medium-size effects on the lateral deep zone (d = 62, P = 0.031) and on the lateral superficial zone (d = 0.58, P = 0.047). In these zones, the group change differences were 12% and 9%, respectively. In the medial deep zone, the exercise intervention had a small but significant effect (d = 0.29, P = 0.047), and the group change difference was 4%. Physical performance, perceived pain, knee stiffness, and self-rated physical functioning. Isometric extension force was 11% greater (d = 0.63, P = 0.006) and maximal aerobic capacity was 4% greater (d = 0.55, P = 0.028) in the exercise group than in controls. The exercise group showed significant positive changes in leg power and some KOOS subscales (pain, OA symptoms, and quality of life), but no between-group differences were observed (Table 2).
DISCUSSION Our 12-month randomized controlled high-impact exercise trial in postmenopausal women with mild OA showed decreased mean T2 relaxation time, indicating improved patellar cartilage quality. In addition, physical performance improved, although we observed no between-group difference in self-rated knee OA symptoms.
FIGURE 4—Group changes in T2 relaxation time in different parts of patellar cartilage after the 12-month intervention. Bars indicate 95% CI.
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In our recent report on the very same group and intervention, we showed that the studied exercise program increased femoral neck bone mineral content (g) but did not have negative or positive effects on tibiofemoral cartilage biochemical composition, assessed using quantitative MRI measures (24). In addition, the exercise program promoted physical performance and thus reduced multiple-fall risk factors for osteoporotic fractures among postmenopausal women (24). Our results are in line, at least in part, with those of Teichtahl et al. (35), who found that vigorous physical activity was beneficial for patellofemoral cartilage volume in men and women without pre-existing cartilage damage, but not for people with baseline cartilage defects. In our RCT, the exercise program comprised intensive long-term training with moderate patellofemoral load in flexion–extension exercises and close-to-optimal knee flexion angles. Our exercise program had positive effects on patellar cartilage quality, that is, on the structural properties of the collagenous fiber architecture and water content (T2 relaxation time) in postmenopausal women with mild tibiofemoral and patellofemoral OA. Thus, these results highlight the importance of physical activity for knee cartilage characteristics. In daily activities, patellofemoral joint loading (equal to tibiofemoral joint loading) has been shown to be two to nine times the body weight during flexion movements (4,7,15,22,33). In addition, when ascending and descending stairs, the force vector of the patella is mostly directed against the femur and is about half of the force induced during running (7). Furthermore, running causes moderate impacts from three to five accelerations of gravity (g; zero corresponds to standing), depending on running speed (30), whereas in our exercise program, the highest impacts were higher (from 5g to 9g) than those in running. Thus, during knee flexion, the patellofemoral cartilage loading forces in our study could have been of the same order as previously measured in running (7). Nevertheless, we have recently suggested that although knee forces occasionally seemed to be rather high in our exercise program, the total number of highest impacts remained at a reasonable level (an average number of 44 in the exercise sessions); thus, loading remained within the physiological ‘‘safe loading range’’ in terms of cartilage health (24). The bigger is the force produced by the knee extensors, the more the patella is pressed into the trochlear groove, thereby widening the cartilage contact area and decreasing the pressure per centimeter squared (4). Widening the area of compression decreases the peak loading (i.e., compressive and shear loading) of patellofemoral cartilage against that of femoral cartilage. This is in line with our finding of an increase in knee extension force, indicating increased loading of the patellofemoral joint, during the training program. Altogether, the aforementioned loading environment in patellar cartilage may explain the positive exercise loading adaptation in the patellofemoral joint as compared with our previous findings on the response of the tibiofemoral joint to the same high-impact exercise in the same postmenopausal women with mild OA (24).
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down the progression of these diseases. However, high-impact exercise may not provide the optimal loading modality for patients with knee OA. Future studies should evaluate whether low-impact or nonimpact loading modalities, such as cycling or aquatic training, have beneficial effects on articular cartilage and also may reduce the risk factors of falling. In conclusion, progressively implemented high-impact and intensive exercise provides adequate stimuli and thus has favorable effects on patellar cartilage quality and general health/physical function in patients with mild knee OA. The exercise protocol is also well tolerated. Future studies need to address whether low-impact or nonimpact loading modalities, such as cycling or aquatic training, have beneficial effects on articular cartilage in both sexes and how long the effects last after exercise. The authors thank all of the personnel involved in the ‘ Bone Exercise to Cartilage’’ project, in particular Katriina Ojala, M.Sc. (UKK Institute), for designing and tutoring the exercise programs; Katri Lihavainen, Ph.D., for her contribution as exercise instructor in charge; and Timo Rantalainen, Ph.D. (University of Jyva¨skyla¨ and Center for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, Melbourne, Australia), for helping assemble the dataset used in this analysis. The authors gratefully acknowledge Dr. Risto Ojala, M.D. (Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland), for reading the radiographs. The present study was funded by the Academy of Finland, the Ministry of Education and Culture, the Finnish Cultural Foundation, the Finnish Rheumatism Foundation, the Juho Vainio Foundation, the Emil Aaltonen Foundation, the Yrjo¨ Jahnsson Foundation, the Central Finland Health Care District, the Finnish Doctoral Program of Musculoskeletal Disorders and Biomaterials, and the executive committee of the alliance between Rehabilitation Center Peurunka and the University of Jyva¨skyla¨. The authors declare no conflicts of interest and no financial/ personal relationships with other people or organizations. Clinical Trial Registration: ISRCTN58314639. A. Heinonen, A. Ha¨kkinen, I. Kiviranta, M. T. Nieminen, T. Ja¨msa¨, and J. Multanen designed the study. J. Koli, J. Multanen, E. Lammentausta, and H. Sela¨nne conducted the study. J. Koli, J. Multanen, and R. Ahola collected the data. H. Kautiainen, A. Heinonen, J. Koli, and J. Multanen analyzed the data. A. Heinonen, M. T. Nieminen, J. Koli, J. Multanen, H. Kautiainen, E. Lammentausta, A. Ha¨kkinen, U. M. Kujala, and I. Kiviranta interpreted the data. J. Koli, J. Multanen, A. Heinonen, and A. Ha¨kkinen drafted the manuscript. J. Koli, A. Heinonen, A. Ha¨kkinen, J. Multanen, U. M. Kujala, I. Kiviranta, M. T. Nieminen, E. Lammentausta, T. Ja¨msa¨, H. Kautiainen, R. Ahola, and H. Sela¨nne revised the content of the manuscript. J. Koli, J. Multanen, A. Heinonen, A. Ha¨kkinen, U. M. Kujala, I. Kiviranta, M. T. Nieminen, E. Lammentausta, T. Ja¨msa¨, H. Kautiainen, R. Ahola, and H. Sela¨nne approved the final version of the manuscript. A. Heinonen and J. Koli are responsible for the integrity of data analyses. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
REFERENCES 1. Ahola R, Korpelainen R, Vainionpaa A, Jamsa T. Daily impact score in long-term acceleration measurements of exercise. J Biomech. 2010; 43(10):1960–4. 2. Ainsworth BE, Haskell WL, Herrmann SD, et al. 2011 Compendium of Physical Activities: a second update of codes and MET values. Med Sci Sports Exerc. 2011;43(8):1575–81. 3. Baum T, Stehling C, Joseph GB, et al. Changes in knee cartilage T2 values over 24 months in subjects with and without risk factors for knee osteoarthritis and their association with focal knee lesions at baseline: data from the osteoarthritis initiative. J Magn Reson Imaging. 2012;35(2):370–8.
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4. Besier TF, Draper CE, Gold GE, Beaupre´ GS, Delp SL. Patellofemoral joint contact area increases with knee flexion and weight-bearing. J Orthopaed Res. 2005;23(2):345–50. 5. Borotikar BS, Sheehan FT. In vivo patellofemoral contact mechanics during active extension using a novel dynamic MRI-based methodology. Osteoarthritis Cartilage. 2013;21:1886–94. 6. Brandt KD, Doherty ME, Doherty M, Lohmander LS. Osteoarthritis. Oxford: Oxford University Press, 2003:511. 7. Chen YJ, Scher I, Powers CM. Quantification of patellofemoral joint reaction forces during functional activities using a subject-specific three-dimensional model. J Appl Biomech. 2010;26(4):415–23.
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In the present study, the significant improvements in superficial and deep patellar cartilage T2 parameters, indicated by decreased T2 values in the exercise group compared with the control group, may indicate a positive effect on the biochemical properties of cartilage, particularly those of the collagen network and/or tissue hydration maintained by collagen distribution, increased by bound water content, and not disorientated by matrix structure (22). These changes in T2 relaxation time have been suggested to be related to alteration in collagen fiber orientation and water content (21). All in all, it seems that long-term bone-beneficial impact exercise (24) is also advantageous to patellar cartilage and thus emphasizes the role of exercise in OA rehabilitation. However, in our recent analysis of the effects of the same exercise regimen on tibiofemoral joint cartilage in the same group, we did not find any positive or negative cartilage response (24). However, high-impact exercise may not provide the optimal loading modality for patients with knee OA. As we have pointed out previously (24), this research project has several strengths, including a long-term randomized controlled exercise intervention, high training compliance, and only a few dropouts. In addition, we were able to divide patellar cartilage into deep and superficial zones. Furthermore, all of the important quality criteria of RCT were carefully applied. Furthermore, supervised group exercises are cost-effective (26) because one exercise leader can supervise several participants at the same time and because group exercise demands on space and equipment are typically modest. However, a lack of means to differentiate pain symptoms originating from the tibiofemoral compartment from pain symptoms originating from the patellofemoral compartment limited us to confirming that the pain was in the patellofemoral joint. Another limitation is that we do not have knowledge on the long-term maintenance of the positive changes induced in cartilage. In addition to previously known benefits on knee function and relief of OA knee pain (12), the most important novel finding was that patellar cartilage quality can be improved with the kind of high-impact jumping exercise that has been shown to be beneficial for bone integrity. Importantly, this kind of impact exercise is well tolerated and, in addition, is not harmful to tibiofemoral cartilage, as we have shown previously (24). Because osteoporosis and OA often occur in the same population (i.e., postmenopausal women), the same kind of exercise program could be beneficial for slowing
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8. David-Vaudey E, Ghosh S, Ries M, Majumdar S. T2 relaxation time measurements in osteoarthritis. Magn Reson Imaging. 2004; 22(5):673–82. 9. Davies AP, Vince AS, Shepstone L, Donell ST, Glasgow MM. The radiologic prevalence of patellofemoral osteoarthritis. Clin Orthop Relat Res. 2002;402(402):206–12. 10. Duncan R, Peat G, Thomas E, Wood L, Hay E, Croft P. How do pain and function vary with compartmental distribution and severity of radiographic knee osteoarthritis? Rheumatology. 2008; 47(11):1704–7. 11. Felson DT. The epidemiology of knee osteoarthritis: results from the Framingham Osteoarthritis Study. Semin Arthritis Rheum. 1990;20(3 Suppl 1):42–50. 12. Fransen M, McConnell S. Exercise for osteoarthritis of the knee. Cochrane Database Syst Rev. 2008;(4):CD004376. 13. Hannila I, Raina SS, Tervonen O, Ojala R, Nieminen MT. Topographical variation of T2 relaxation time in the young adult knee cartilage at 1.5 T. Osteoarthritis Cartilage. 2009;17(12):1570–5. 14. Heinonen A, Kannus P, Sievanen H, et al. Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet. 1996;348(9038):1343–7. 15. Hinman RS, Crossley KM. Patellofemoral joint osteoarthritis: an important subgroup of knee osteoarthritis. Rheumatology. 2007; 46(7):1057–62. 16. Hovis KK, Stehling C, Souza RB, et al. Physical activity is associated with magnetic resonance imaging-based knee cartilage T2 measurements in asymptomatic subjects with and those without osteoarthritis risk factors. Arthritis Rheum. 2011;63(8):2248–56. 17. Karinkanta S, Heinonen A, Sievanen H, et al. A multi-component exercise regimen to prevent functional decline and bone fragility in home-dwelling elderly women: randomized, controlled trial. Osteoporos Int. 2007;18(4):453–62. 18. Kujala UM, Kettunen J, Paananen H, et al. Knee osteoarthritis in former runners, soccer players, weight lifters, and shooters. Arthritis Rheum. 1995;38(4):539–46. 19. Kujala UM, Osterman K, Kormano M, Nelimarkka O, Hurme M, Taimela S. Patellofemoral relationships in recurrent patellar dislocation. J Bone Joint Surg Br. 1989;71(5):788–92. 20. Laukkanen RM, Kukkonen-Harjula TK, Oja P, Pasanen ME, Vuori IM. Prediction of change in maximal aerobic power by the 2-km walk test after walking training in middle-aged adults. Int J Sports Med. 2000;21(2):113–6. 21. Li X, Majumdar S. Quantitative MRI of articular cartilage and its clinical applications. J Magn Reson Imaging. 2013;38(5):991–1008. 22. Li X, Pai A, Blumenkrantz G, et al. Spatial distribution and relationship of T1Q and T2 relaxation times in knee cartilage with osteoarthritis. Magn Reson Med. 2009;61(6):1310–8. 23. McAlindon TE, Snow S, Cooper C, Dieppe PA. Radiographic patterns of osteoarthritis of the knee joint in the community: the importance of the patellofemoral joint. Ann Rheum Dis. 1992; 51(7):844–9.
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24. Multanen J, Nieminen MT, Hakkinen A, et al. Effects of highimpact training on bone and articular cartilage: 12-month randomized controlled quantitative MRI study. J Bone Miner Res. 2014;29(1): 192–201. 25. Multanen J, Rauvala E, Lammentausta E, et al. Reproducibility of imaging human knee cartilage by delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) at 1.5 Tesla. Osteoarthritis Cartilage. 2009;17(5):559–64. 26. Patel G, Walsh N, Gooberman-Hill R. Managing osteoarthritis in primary care: exploring healthcare professionals’ views on a multiple-joint intervention designed to facilitate self-management. Musculoskelet Care. 2014;12(4):199–209. 27. Portegijs E, Sipila¨ S, Alen M, et al. Leg extension power asymmetry and mobility limitation in healthy older women. Arch Phys Med Rehabil. 2005;86(9):1838–42. 28. Roos EM, Dahlberg L. Positive effects of moderate exercise on glycosaminoglycan content in knee cartilage: a four-month, randomized, controlled trial in patients at risk of osteoarthritis. Arthritis Rheum. 2005;52(11):3507–14. 29. Roos EM, Lohmander LS. The Knee injury and Osteoarthritis Outcome Score (KOOS): from joint injury to osteoarthritis. Health Qual Life Outcomes. 2003;1:64. 30. Roos PE, Barton N, van Deursen RW. Patellofemoral joint compression forces in backward and forward running. J Biomech. 2012;45(9):1656–60. 31. Sipila S, Multanen J, Kallinen M, Era P, Suominen H. Effects of strength and endurance training on isometric muscle strength and walking speed in elderly women. Acta Physiol Scand. 1996;156(4):457–64. 32. Stehling C. Patellar cartilage: T2 values and morphologic abnormalities at 3.0-T MR imaging in relation to physical activity in asymptomatic subjects from the osteoarthritis initiative. Radiology. 2010;254(2):509–20. 33. Subburaj K, Kumar D, Souza RB, et al. The acute effect of running on knee articular cartilage and meniscus magnetic resonance relaxation times in young healthy adults. Am J Sports Med. 2012;40(9):2134–41. 34. Szebenyi B, Hollander AP, Dieppe P, et al. Associations between pain, function, and radiographic features in osteoarthritis of the knee. Arthritis Rheum. 2006;54(1):230–5. 35. Teichtahl AJ, Wluka AE, Forbes A, et al. Longitudinal effect of vigorous physical activity on patella cartilage morphology in people without clinical knee disease. Arthritis Rheum. 2009;61(8):1095–102. 36. Uusi-Rasi K, Kannus P, Cheng S, et al. Effect of alendronate and exercise on bone and physical performance of postmenopausal women: a randomized controlled trial. Bone. 2003;33(1):132–43. 37. Vainionpaa A, Korpelainen R, Vihriala E, Rinta-Paavola A, Leppaluoto J, Jamsa T. Intensity of exercise is associated with bone density change in premenopausal women. Osteoporos Int. 2006;17(3):455–63. 38. Wijayaratne SP, Teichtahl AJ, Wluka AE, et al. The determinants of change in patella cartilage volume—a cohort study of healthy middle-aged women. Rheumatology. 2008;47(9):1426–9.
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Effects of Exercise on Patellar Cartilage in Women with Mild Knee Osteoarthritis ¨ KKINEN1,2, MIIKA T. NIEMINEN3,4,5, JARMO KOLI1, JUHANI MULTANEN1,2, URHO M. KUJALA1, ARJA HA 6,7 3,4 ¨ MSA ¨ 3,4,8, RIIKKA AHOLA4,8, HANNU KAUTIAINEN , EVELIINA LAMMENTAUSTA , TIMO JA 9 10 1 ¨ HARRI SELANNE , ILKKA KIVIRANTA , and ARI HEINONEN Department of Health Sciences, University of Jyva¨skyla¨, Jyva¨skyla¨, FINLAND; 2Department of Physical Medicine and Rehabilitation, Central Finland Central Hospital, Jyva¨skyla¨, FINLAND; 3Department of Diagnostic Radiology, Oulu University Hospital, Oulu, FINLAND; 4Medical Research Center Oulu, University of Oulu and Oulu University Hospital, Oulu, FINLAND; 5Department of Radiology, University of Oulu, Oulu, FINLAND; 6Department of General Practice and Primary Healthcare, University of Helsinki, Helsinki, FINLAND; 7Unit of Primary Healthcare, Kuopio University Hospital, Kuopio, FINLAND; 8Department of Medical Technology, Institute of Biomedicine, University of Oulu, Oulu, Finland; 9LIKES Research Center, Jyva¨skyla¨, FINLAND; and 10Department of Orthopedics and Traumatology, University of Helsinki and Helsinki University Hospital, Helsinki, FINLAND 1
ABSTRACT ¨ KKINEN, M. T. NIEMINEN, H. KAUTIAINEN, E. LAMMENTAUSTA, KOLI, J., J. MULTANEN, U. M. KUJALA, A. HA ¨ ¨ ¨ T. JAMSA, R. AHOLA, H. SELANNE, I. KIVIRANTA, and A. HEINONEN. Effects of Exercise on Patellar Cartilage in Women with Mild Knee Osteoarthritis. Med. Sci. Sports Exerc., Vol. 47, No. 9, pp. 1767–1774, 2015. Purpose: This study aims to investigate the effects of exercise on patellar cartilage using T2 relaxation time mapping of magnetic resonance imaging in postmenopausal women with mild patellofemoral joint osteoarthritis (OA). Methods: Eighty postmenopausal women (mean age, 58 (SD, 4.2) yr) with mild knee OA were randomized to either a supervised progressive impact exercise program three times a week for 12 months (n = 40) or a nonintervention control group (n = 40). Biochemical properties of cartilage were estimated using T2 relaxation time mapping, a parameter sensitive to collagen integrity, collagen orientation, and tissue hydration. Leg muscle strength and power, aerobic capacity, and self-rated assessment with the Knee Injury and Osteoarthritis Outcome Score were also measured. Results: After intervention, full-thickness patellar cartilage T2 values had medium-size effect (d = 0.59; 95% confidence interval, 0.16 to 0.97; P = 0.018); the change difference was 7% greater in the exercise group compared with the control group. In the deep half of tissue, the significant exercise effect size was medium (d = 0.56; 95% confidence interval, 0.13 to 0.99; P = 0.013); the change difference was 8% greater in the exercise group compared with controls. Furthermore, significant medium-size T2 effects were found in the total lateral segment, lateral deep, and lateral superficial zones in favor of the exercise group. Extension force was 11% greater (d = 0.63, P = 0.006) and maximal aerobic capacity was 4% greater (d = 0.55, P = 0.028) in the exercise group than in controls. No changes in Knee Injury and Osteoarthritis Outcome Score emerged between the groups. Conclusions: Progressively implemented high-impact and intensive exercise creates enough stimuli and exerts favorable effects on patellar cartilage quality and physical function in postmenopausal women with mild knee OA. Key Words: PHYSICAL FUNCTIONING, REHABILITATION, MAGNETIC RESONANCE IMAGING, PHYSICAL THERAPY
K
nee osteoarthritis (OA) is an age-related joint disease commonly present in postmenopausal women, causing pain and disability. Knee OA is characterized by loss and degeneration of hyaline cartilage (6,11). The knee joint has three compartments: medial tibiofemoral, lateral tibiofemoral, and patellofemoral. The biomechanics of the patellofemoral joint differs from that of the tibiofemoral compartment in mechanical loading (35). Although knee OA exerts influence on all three compartments of the knee, evidence indicates that radiographically isolated patellofemoral OA plays an independent and important role in knee pain and disability in mild knee OA (10,15,23). Radiographic and symptom
Address for correspondence: Ari Heinonen, Ph.D., Department of Health Sciences, University of Jyva¨skyla¨, PO Box 35, Jyva¨skyla¨ 40014, Finland; E-mail: [email protected]. Submitted for publication August 2014. Accepted for publication January 2015. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.acsm-msse.org). 0195-9131/15/4709-1767/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2015 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000629
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changes may be more prevalent in the patellofemoral joint than in the tibiofemoral joint (10,34). More than a third of women older than 60 yr have been reported to have radiographic patellofemoral OA (9). To date, there is no cure for OA (12). It is important, therefore, to find prophylactic means to prevent or at least decelerate the processes of cartilage degeneration (6). Regular exercise is a promising nonpharmacological method that can positively influence cartilage morphology (24,35,38) and biochemical composition (24,28). In addition, exercise has been shown to be effective in reducing pain and in promoting physical functioning in people with knee OA (12). On the other hand, sports-related knee injuries in persons with extremely high physical activity levels and older age are associated with higher knee OA risk and elevated magnetic resonance imaging (MRI) T2 mapping values (3,18,32,35). High T2 values correlate with histological degeneration of cartilage, implying increased free water content and collagen disorientation (8,22). However, in subjects with high OA risk, light exercise has been associated with better cartilage quality (16). In our recently published randomized controlled trial (RCT), we reported that aerobic/step-aerobic exercise had a beneficial effect on bone but did not have a major positive or negative effect on tibiofemoral cartilage (24). In sports, knee injury is the strongest predictor of knee OA (18). In an observational study of the occurrence of tibiofemoral and patellofemoral OA among former athletes, both types of radiographic OA were more common among former weightlifters than among former runners (18). Based on knowledge on patellofemoral biomechanics (5,19), moderate dynamic exercise loading—excluding high injury risk at early knee extension and deep squats with high loads (such as in weightlifting)—should be a favorable stimulus for improving patellar cartilage quality. So far, no RCT has reported on the effects of moderate dynamic exercise on patellar cartilage. Consequently, we investigated the effects of a 12-month supervised aerobic/step-aerobic exercise program on patellar cartilage, using T2 relaxation time mapping, in postmenopausal women with mild tibiofemoral joint OA and usually lacking significant deep cartilage defects of the patella. In addition, we studied the effects of the exercise intervention on physical performance and knee-related symptoms.
MATERIALS AND METHODS Design and Participants This study was a 12-month RCT with two experimental arms: 1) an aerobic/step-aerobic training group and 2) a nontraining control group. The assigned training frequency was three times a week for 12 months. All measurements were performed at baseline (before the intervention) and at the end of the 12-month intervention. All outcome assessors, except for J. Multanen (in patellar cartilage segmentation), were blinded to treatment group assignment. The trial profile is shown in Figure 1.
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Voluntary participants from the Jyva¨skyla¨ region in Central Finland were recruited through a local newspaper advertisement. A total of 298 women responded; after assessment of eligibility by telephone interview, 208 women were then invited for anteroposterior knee x-rays. After the knee x-rays, dual-energy x-ray absorptiometry and clinical examinations were conducted on 80 subjects who met the inclusion criteria. Eligibility criteria were as follows: postmenopause, age 50–65 yr, knee pain on most days, regular intensive exercise no more than twice a week, no illnesses that contraindicated exercise or would limit participation in the exercise program, and grade 1–2 Kellgren–Lawrence (K–L) radiographic tibiofemoral joint OA. Exclusion criteria were as follows: femoral neck bone and lumbar spine bone mineral density (gIcmj2) T-score lower than j2.5 (i.e., indicating osteoporosis), measured with dual-energy x-ray absorptiometry (GE Medical Systems, Lunar Prodigy, Madison, WI, USA); body mass index e35 kgImj2; knee instability or surgery of the knee caused by trauma; inflammatory joint disease; intra-articular steroid injections in the knee in the preceding 12 months; and contraindications to MRI (allergies to contrast agents or renal insufficiency). A statistician randomly allocated each participant to the exercise group (n = 40) or the control group (n = 40) according to a computer-generated blocked randomization list. We used a block size of 10, stratified according to tibiofemoral joint K–L grades 1 and 2. Immediately after randomization, two exercisers withdrew; consequently, baseline data were reported for 78 participants. During the intervention, two participants dropped out (Fig. 1). The study protocol was approved by the Ethics Committee of the Central Finland Health Care District. A written informed consent form was obtained from all participants before enrolment. Exercise Program High-impact multidirectional modified aerobic and stepaerobic jumping exercise programs alternated every 2 wk. Supervised group exercise classes, lasting 55 min, were carried out three times a week for 12 months. Loading was gradually increased after 3 months by progressively raising the height of foam fences from 5 to 20 cm in aerobic exercises, and the height of step benches from 10 to 20 cm in jumping exercises (14,17,36). During exercise sessions, the estimated knee flexion angle varied from 70- to 5-; thus, no deep squats were performed. The exercise protocol is described in more detail in Supplementary Digital Content (see document, Supplemental Digital Content 1, Exercise protocol: training quality, alternation, frequency, time, span and quantity, http://links.lww.com/MSS/A514). Exercise instructors systematically recorded possible injuries and knee pain after every exercise session. The mean knee pain during exercise sessions was 5 mm (SD, 10) (visual analog scale score, 0–100 mm). Measurement of exercise loading. High-impact exercise was quantified by recording the number and intensity of
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FIGURE 1—Flowchart of recruitment process and inclusion of participants. DXA, dual-energy x-ray absorptiometry.
acceleration peaks (impacts) with accelerometers fixed to the waist (Newtest, Oulu, Finland) during one exercise session in each of the 3-month exercise periods (37). The distribution of the number and intensity of impacts is shown in Figure 2, with the impacts being proportional to the number of jumps, steps, and patellar movements made during the exercise sessions. Zero acceleration (g) corresponded to standing. Categorization and labeling are based on Vainionpaa et al. (37), with modifications. They proposed 3.9g as the osteogenic threshold.
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Daily physical activity. Outside intervention sessions, the number and intensity of acceleration peaks (impacts) attributable to daily physical activities from all participants (intervention training classes not included) were measured with accelerometers and are described in detail elsewhere (1,24,37). Daily physical activity was described as daily impact score (DISlog) (1). The mean DISlog outside the intervention sessions was 163 (SD, 43) in the exercise group and 168 (SD, 46) in the control group. There were no
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Muscle power. Leg extensor power in each leg was measured with the Nottingham Power Rig. In each case, the best value (i.e., maximum) performance was taken for analysis (27). Cardiorespiratory fitness. Cardiorespiratory fitness ˙ O2max; mLIkgj1Iminj1) was assessed with a standardized (V ˙ O2max 2-km walk test (UKK Institute, Tampere, Finland). V was estimated based on sex, age, weight, height, heart rate, and measured walking time (20). Questionnaires
FIGURE 2—Number of impacts at four acceleration levels during the intervention. Bars indicate interquartile range. *Indicates zero acceleration (g) is equated to standing still and g = 9.81 mIsj2.
intergroup differences in physical activity or knee loading outside the intervention sessions.
General health and habitual physical activity were assessed with questionnaires at baseline. Baseline habitual physical activity was converted into MET-hours per week (2,17). Perceived pain, knee symptoms, self-rated physical function, sports/recreation, and knee-related quality of life were assessed with the Knee Injury and Osteoarthritis Outcome Score (KOOS) (29). Adverse Events
Controls were requested to maintain their usual activities and were offered the possibility of participating in a social group meeting every third month. Seventy percent of control group participants took part in the meetings, which included lectures on healthy lifestyles (not physical activity or exercise) and stretching exercises.
During the 12-month exercise intervention, only six exercisers consulted the study physician for musculoskeletal injuries or other symptoms (24). Participants whose pain symptoms increased during the intervention were advised to take a short individualized break from training. All these trainees returned to the exercise regimen within 5 to 21 d. In the control group, two visits to the attending physician were made for previous meniscal tear injury and cardiac dysrhythmia. The number of visits to the attending physician did not differ statistically between the groups (P = 0.15).
Primary Outcome Measure
Statistical Methods
Cartilage measurements. Measurement protocol is described in Supplemental Digital Content (see document, Supplemental Digital Content 1, page 1; MRI protocol: participants preparation, MRI–measurement parameters, http://links.lww.com/MSS/A514). T2 relaxation time (T2) (13,25) was determined using a Siemens Magnetom Symphony Quantum 1.5-T scanner (Siemens AG, Medical Solutions, Erlangen, Germany) with a standard transmit/ receive knee array coil. Participants had been lying in the tube for about 40 min before axial T2 series were imaged. Cartilage regions of interest (ROI) from a single transversal slice in the patella were manually segmented using an inhouse MATLAB application (Mathworks, Inc., Natick, MA, USA) (Fig. 3). Cartilage ROI are shown in Figure 3. In our laboratory, the (mean) interobserver error (CVRMS) for T2 full-thickness ROI was 2%.
All analyses were based on intention-to-treat principles. Results were expressed as mean (SD) or median (interquartile range). Statistical comparison between groups was made by chi-square test or Fisher’s exact test and t-test. Statistical comparison of changes in outcome measurements was performed by paired t-test or ANCOVA. Confidence intervals
Control Group
Secondary Outcome Measures Physical performance. Muscle force. Maximal isometric knee extension was measured in sitting position with a knee angle of 60-, using a dynamometer chair (Good Strength; Metitur Oy, Jyva¨skyla¨, Finland) (31). We used the best value (i.e., maximum) of the test attempts of force measurements.
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FIGURE 3—Illustration of ROI in patellar cartilage. ROI are shown in covered areas outlined by continuous lines in a single transversal slice from the middle of the patella. The broken line divides the full-thickness cartilage into the superficial half and the deep half.
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TABLE 1. Baseline demographic and clinical characteristics of the participants. Characteristics
Control Group (n = 40)
58 (4) 165 (6) 73.4 (9.4) 27.1 (3.1) 24 (63) 8 (21) 10 (14) 18.1 (13.1)
59 (4) 161 (5) 69.4 (11.7) 26.7 (4.2) 17 (42) 13 (32) 10 (13) 18.9 (17.2)
18 (47) 5 (13) 15 ( 40)
21 (52) 1 (3) 18 (45)
12 (32) 26 (68)
13 (32) 27 (68)
(CI; 95% CI) for MRI outcome means were obtained by biascorrected bootstrapping (3000 replications). Group differences in MRI, physical performance, and clinical symptom outcomes were adjusted for baseline values. Effect size (d) was calculated using the method of Cohen. An effect size of 0.20 was considered small, 0.50 was medium, and 0.80 was large. CI for effect sizes were obtained by bias-corrected bootstrapping (5000 replications). Statistical analyses were performed using statistical software (Stata, release 13.1; StataCorp, College Station, TX). Before the study, the estimated sample size for power calculation was based on the primary hypothesis. A sample size of 70 subjects (35 in each group) was required to detect a 0.08-g (~2%) difference in femoral neck bone mineral content between the intervention group and the control group (> = 0.05, power, 80%), assuming a dropout rate of approximately 10%. For T2, we were unable to reliably
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Exercise Group (n = 38)
Age, mean (SD), yr Height, mean (SD), cm Body mass, mean (SD), kg Body mass index, mean (SD), kgImj2 Pain killers, n (%) Occasional use of glucosamine, n (%) Knee pain during the last week, mean (SD), mm Habitual physical activity, mean (SD), METIhIwkj1 Patellofemoral K–L grade, n (%) K–L grade 0 K–L grade 1 K–L grade 2 Tibiofemoral K–L grade, n (%) K–L grade 1 K–L grade 2
calculate the intended sample sizes, as previous long-term exercise interventions for cartilage change did not exist.
RESULTS Baseline clinical characteristics of the study groups are given in Table 1. At baseline, no statistically significant differences in any characteristics were observed between the groups, except that the subjects in the exercise group were slightly taller. During the study, two trainees in the exercise group dropped out on weeks 3 and 5; there were no dropouts in the control group. Patellofemoral K–L grading was similar in both groups at baseline (P = 0.21). The mean training compliance was 68%, and the mean training frequency was 2.1 (SD, 0.9) per week (including dropouts). The mean number of measured impacts, and thus patellar movements, during one training class was 2 275 (SD, 343).
TABLE 2. Baseline values, changes, treatment effects, and effects sizes of patellar cartilage T2 relaxation time, KOOS, and physical function measures. Baseline
Quantitative MRI T2 Patella total, ms Superficial, ms Deep, ms Lateral segment Bulk, ms Deep, ms Superficial, ms Medial segment Bulk, ms Deep, ms Superficial, ms Clinical outcomes KOOS (0–100) Pain Symptoms Physical functioning Sport and recreation Quality of life Physical function Knee extension force, Nc Leg power, WIkgj1c V˙O2max, mLIkgj1Iminj1
Changes at 12-Month Time Point
Exercise Group (n = 36)
Control Group (n = 40)
Exercise Group (n = 36)
Control Group (n = 40)
Treatment Effect
Effect Size
Mean (SD)
Mean (SD)
Mean (95% CI)
Mean (95% CI)
Mean (95% CI)
d (95% CI)a
47.9 (7.9) 52.5 (8.2) 43.2 (9.3)
45.7 (6.0) 50.1 (7.1) 41.1 (7.2)
j3.8 (j6.4 to j1.9) j3.9 (j6.9 to j1.7) j3.6 (j6.0 to j1.5)
0.03 (j1.8 to 2.1) 0.1 (j2.4 to 2.5) 0.3 (j1.9 to 2.4)
j3.8 (j6.8 to j0.9) j4.0 (j7.6 to j0.4) j3.9 (j7.0 to j0.8)
49.6 (9.0) 45.1 (11.0) 54.0 (9.1)
46.0 (6.2) 41.3 (8.0) 50.8 (7.5)
j4.9 (j8.0 to j2.4) j4.9 (j7.7 to j2.3) j4.6 (j7.8 to j1.8)
0.6 (j1.6 to 3.2) 0.7 (j2.0 to 3.8) 0.6 (j1.9 to 3.4)
45.9 (8.1) 40.8 (8.8) 50.7 (9.3)
45.7 (8.0) 41.2 (8.4) 49.8 (9.4)
j2.6 (j4.9 to j0.8) j1.9 (j4.5 to 0.01) j3.3 (j6.2 to j1.0)
j0.3 (j2.4 to 2.0) 0.1 (j2.1 to 2.3) 0.4 (j2.3 to 3.0)
86 79 92 78 76
(10) (12) (8) (16) (15)
401 (95) 2.2 (0.5) 29 (3)
87 83 93 78 78
(7) (10) (6) (12) (15)
414 (70) 2.1 (0.5) 29 (4)
4.4 (1 to 8) 1.8 (1 to 8) 1 (j2 to 3) 4 (j2 to 9) 7 (2 to 12)
1.8 1 j0.2 j1 4
(j1 to 4 ) (j3 to 4) (j2 to 1) (j5 to 3) (j0.1 to 8)
21 (j1 to 44) 0.3 (0.1 to 0.4) 1.4 (0.7 to 2.1)
j14 (j29 to 1) 0.2 (0.03 to 0.3) 0.3 (j0.4 to 1)
P Value Crude
Adjustedb
0.59 (0.16 to 0.97) 0.50 (0.09 to 0.91) 0.56 (0.13 to 0.99)
0.010 0.028 0.014
0.018 0.062 0.013
j5.5 (j9.2 to j1.9) j5.6 (j9.5 to j1.6) j5.2 (j9.4 to j1.1)
0.67 (0.26 to 1.06) 0.62 (0.18 to 1.05) 0.58 (0.16 to 0.97)
0.003 0.006 0.013
0.021 0.031 0.047
j2.3 (j5.4 to 0.7) j2.1 (j5.2 to 1.0) j3.6 (j7.3 to 0.06)
0.34 (j0.12 to 0.74) 0.43 (j0.03 to 0.82) 0.29 (j0.16 to 0.70)
0.138 0.192 0.054
0.077 0.047 0.052
0.29 0.36 0.14 0.35 0.20
0.22 0.12 0.53 0.14 0.39
0.22 0.36 0.59 0.14 0.51
0.009 0.24 0.027
0.006 0.20 0.028
2.6 3.8 0.9 5 2.8
(j1 to 4) (j1.5 to 9 ) (j2 to 4) (j2 to 12) (j4 to 9)
35 (9 to 61) j0.1 (j0.3 to 0.04) 1.0 (0.1 to 2.0 )
(j0.18 to (j0.09 to (j0.64 to (j0.16 to (j0.26 to
0.74) 0.13) 0.31) 0.89) 0.64)
0.63 (0.20 to 1.12) 0.28 (j0.18 to 0.79) 0.55 (0.10 to 1.03)
a
Effect size (d ) was calculated using the method of Cohen. Adjusted to baseline values. c Mean of both legs (best attempt). b
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Cartilage measurements. Table 2 gives T2 values at baseline, changes, group differences (i.e., treatment effects), and effect sizes at the end of the 12-month intervention. Differences between T2 values in the superficial layer and T2 values in the deep layer were attributable to natural collagen orientation (high T2 values correspond to cartilage structure degeneration). The exercise intervention had medium-size effect (d = 0.59, P = 0.018) on total patellar cartilage T2 values, and the group change difference was 7%, indicating improved cartilage quality. In the total deep zone, the effect size was medium (d = 0.56, P = 0.013), and the group change difference was 8%. Figure 4 shows group changes in T2 values at the lateral and medial segments of the patellofemoral joint. In the total lateral segment, the effect size was medium (d = 0.67, P = 0.021), and the group change difference was 10%. In addition, the exercise intervention had medium-size effects on the lateral deep zone (d = 62, P = 0.031) and on the lateral superficial zone (d = 0.58, P = 0.047). In these zones, the group change differences were 12% and 9%, respectively. In the medial deep zone, the exercise intervention had a small but significant effect (d = 0.29, P = 0.047), and the group change difference was 4%. Physical performance, perceived pain, knee stiffness, and self-rated physical functioning. Isometric extension force was 11% greater (d = 0.63, P = 0.006) and maximal aerobic capacity was 4% greater (d = 0.55, P = 0.028) in the exercise group than in controls. The exercise group showed significant positive changes in leg power and some KOOS subscales (pain, OA symptoms, and quality of life), but no between-group differences were observed (Table 2).
DISCUSSION Our 12-month randomized controlled high-impact exercise trial in postmenopausal women with mild OA showed decreased mean T2 relaxation time, indicating improved patellar cartilage quality. In addition, physical performance improved, although we observed no between-group difference in self-rated knee OA symptoms.
FIGURE 4—Group changes in T2 relaxation time in different parts of patellar cartilage after the 12-month intervention. Bars indicate 95% CI.
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In our recent report on the very same group and intervention, we showed that the studied exercise program increased femoral neck bone mineral content (g) but did not have negative or positive effects on tibiofemoral cartilage biochemical composition, assessed using quantitative MRI measures (24). In addition, the exercise program promoted physical performance and thus reduced multiple-fall risk factors for osteoporotic fractures among postmenopausal women (24). Our results are in line, at least in part, with those of Teichtahl et al. (35), who found that vigorous physical activity was beneficial for patellofemoral cartilage volume in men and women without pre-existing cartilage damage, but not for people with baseline cartilage defects. In our RCT, the exercise program comprised intensive long-term training with moderate patellofemoral load in flexion–extension exercises and close-to-optimal knee flexion angles. Our exercise program had positive effects on patellar cartilage quality, that is, on the structural properties of the collagenous fiber architecture and water content (T2 relaxation time) in postmenopausal women with mild tibiofemoral and patellofemoral OA. Thus, these results highlight the importance of physical activity for knee cartilage characteristics. In daily activities, patellofemoral joint loading (equal to tibiofemoral joint loading) has been shown to be two to nine times the body weight during flexion movements (4,7,15,22,33). In addition, when ascending and descending stairs, the force vector of the patella is mostly directed against the femur and is about half of the force induced during running (7). Furthermore, running causes moderate impacts from three to five accelerations of gravity (g; zero corresponds to standing), depending on running speed (30), whereas in our exercise program, the highest impacts were higher (from 5g to 9g) than those in running. Thus, during knee flexion, the patellofemoral cartilage loading forces in our study could have been of the same order as previously measured in running (7). Nevertheless, we have recently suggested that although knee forces occasionally seemed to be rather high in our exercise program, the total number of highest impacts remained at a reasonable level (an average number of 44 in the exercise sessions); thus, loading remained within the physiological ‘‘safe loading range’’ in terms of cartilage health (24). The bigger is the force produced by the knee extensors, the more the patella is pressed into the trochlear groove, thereby widening the cartilage contact area and decreasing the pressure per centimeter squared (4). Widening the area of compression decreases the peak loading (i.e., compressive and shear loading) of patellofemoral cartilage against that of femoral cartilage. This is in line with our finding of an increase in knee extension force, indicating increased loading of the patellofemoral joint, during the training program. Altogether, the aforementioned loading environment in patellar cartilage may explain the positive exercise loading adaptation in the patellofemoral joint as compared with our previous findings on the response of the tibiofemoral joint to the same high-impact exercise in the same postmenopausal women with mild OA (24).
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down the progression of these diseases. However, high-impact exercise may not provide the optimal loading modality for patients with knee OA. Future studies should evaluate whether low-impact or nonimpact loading modalities, such as cycling or aquatic training, have beneficial effects on articular cartilage and also may reduce the risk factors of falling. In conclusion, progressively implemented high-impact and intensive exercise provides adequate stimuli and thus has favorable effects on patellar cartilage quality and general health/physical function in patients with mild knee OA. The exercise protocol is also well tolerated. Future studies need to address whether low-impact or nonimpact loading modalities, such as cycling or aquatic training, have beneficial effects on articular cartilage in both sexes and how long the effects last after exercise. The authors thank all of the personnel involved in the ‘ Bone Exercise to Cartilage’’ project, in particular Katriina Ojala, M.Sc. (UKK Institute), for designing and tutoring the exercise programs; Katri Lihavainen, Ph.D., for her contribution as exercise instructor in charge; and Timo Rantalainen, Ph.D. (University of Jyva¨skyla¨ and Center for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, Melbourne, Australia), for helping assemble the dataset used in this analysis. The authors gratefully acknowledge Dr. Risto Ojala, M.D. (Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland), for reading the radiographs. The present study was funded by the Academy of Finland, the Ministry of Education and Culture, the Finnish Cultural Foundation, the Finnish Rheumatism Foundation, the Juho Vainio Foundation, the Emil Aaltonen Foundation, the Yrjo¨ Jahnsson Foundation, the Central Finland Health Care District, the Finnish Doctoral Program of Musculoskeletal Disorders and Biomaterials, and the executive committee of the alliance between Rehabilitation Center Peurunka and the University of Jyva¨skyla¨. The authors declare no conflicts of interest and no financial/ personal relationships with other people or organizations. Clinical Trial Registration: ISRCTN58314639. A. Heinonen, A. Ha¨kkinen, I. Kiviranta, M. T. Nieminen, T. Ja¨msa¨, and J. Multanen designed the study. J. Koli, J. Multanen, E. Lammentausta, and H. Sela¨nne conducted the study. J. Koli, J. Multanen, and R. Ahola collected the data. H. Kautiainen, A. Heinonen, J. Koli, and J. Multanen analyzed the data. A. Heinonen, M. T. Nieminen, J. Koli, J. Multanen, H. Kautiainen, E. Lammentausta, A. Ha¨kkinen, U. M. Kujala, and I. Kiviranta interpreted the data. J. Koli, J. Multanen, A. Heinonen, and A. Ha¨kkinen drafted the manuscript. J. Koli, A. Heinonen, A. Ha¨kkinen, J. Multanen, U. M. Kujala, I. Kiviranta, M. T. Nieminen, E. Lammentausta, T. Ja¨msa¨, H. Kautiainen, R. Ahola, and H. Sela¨nne revised the content of the manuscript. J. Koli, J. Multanen, A. Heinonen, A. Ha¨kkinen, U. M. Kujala, I. Kiviranta, M. T. Nieminen, E. Lammentausta, T. Ja¨msa¨, H. Kautiainen, R. Ahola, and H. Sela¨nne approved the final version of the manuscript. A. Heinonen and J. Koli are responsible for the integrity of data analyses. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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In the present study, the significant improvements in superficial and deep patellar cartilage T2 parameters, indicated by decreased T2 values in the exercise group compared with the control group, may indicate a positive effect on the biochemical properties of cartilage, particularly those of the collagen network and/or tissue hydration maintained by collagen distribution, increased by bound water content, and not disorientated by matrix structure (22). These changes in T2 relaxation time have been suggested to be related to alteration in collagen fiber orientation and water content (21). All in all, it seems that long-term bone-beneficial impact exercise (24) is also advantageous to patellar cartilage and thus emphasizes the role of exercise in OA rehabilitation. However, in our recent analysis of the effects of the same exercise regimen on tibiofemoral joint cartilage in the same group, we did not find any positive or negative cartilage response (24). However, high-impact exercise may not provide the optimal loading modality for patients with knee OA. As we have pointed out previously (24), this research project has several strengths, including a long-term randomized controlled exercise intervention, high training compliance, and only a few dropouts. In addition, we were able to divide patellar cartilage into deep and superficial zones. Furthermore, all of the important quality criteria of RCT were carefully applied. Furthermore, supervised group exercises are cost-effective (26) because one exercise leader can supervise several participants at the same time and because group exercise demands on space and equipment are typically modest. However, a lack of means to differentiate pain symptoms originating from the tibiofemoral compartment from pain symptoms originating from the patellofemoral compartment limited us to confirming that the pain was in the patellofemoral joint. Another limitation is that we do not have knowledge on the long-term maintenance of the positive changes induced in cartilage. In addition to previously known benefits on knee function and relief of OA knee pain (12), the most important novel finding was that patellar cartilage quality can be improved with the kind of high-impact jumping exercise that has been shown to be beneficial for bone integrity. Importantly, this kind of impact exercise is well tolerated and, in addition, is not harmful to tibiofemoral cartilage, as we have shown previously (24). Because osteoporosis and OA often occur in the same population (i.e., postmenopausal women), the same kind of exercise program could be beneficial for slowing
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