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Research Article| Volume 25, ISSUE 8, P1238-1246, August 2017

Effects of high intensity resistance aquatic training on body composition and walking speed in women with mild knee osteoarthritis: a 4-month RCT with 12-month follow-up

Open ArchivePublished:March 03, 2017DOI:https://doi.org/10.1016/j.joca.2017.02.800

      Summary

      Objective

      To investigate the effects of 4-months intensive aquatic resistance training on body composition and walking speed in post-menopausal women with mild knee osteoarthritis (OA), immediately after intervention and after 12-months follow-up. Additionally, influence of leisure time physical activity (LTPA) will be investigated.

      Design

      This randomised clinical trial assigned eighty-seven volunteer postmenopausal women into two study arms. The intervention group (n = 43) participated in 48 supervised intensive aquatic resistance training sessions over 4-months while the control group (n = 44) maintained normal physical activity. Eighty four participants continued into the 12-months' follow-up period. Body composition was measured with dual-energy X-ray absorptiometry (DXA). Walking speed over 2 km and the knee injury and osteoarthritis outcome score (KOOS) were measured. LTPA was recorded with self-reported diaries.

      Results

      After the 4-month intervention there was a significant decrease (P = 0.002) in fat mass (mean change: −1.17 kg; 95% CI: −2.00 to −0.43) and increase (P = 0.002) in walking speed (0.052 m/s; 95% CI: 0.018 to 0.086) in favour of the intervention group. Body composition returned to baseline after 12-months. In contrast, increased walking speed was maintained (0.046 m/s; 95% CI 0.006 to 0.086, P = 0.032). No change was seen in lean mass or KOOS. Daily LTPA over the 16-months had a significant effect (P = 0.007) on fat mass loss (f2 = 0.05) but no effect on walking speed.

      Conclusions

      Our findings show that high intensity aquatic resistance training decreases fat mass and improves walking speed in post-menopausal women with mild knee OA. Only improvements in walking speed were maintained at 12-months follow-up. Higher levels of LTPA were associated with fat mass loss.
      Trial registration number: ISRCTN65346593.

      Keywords

      Introduction

      Knee osteoarthritis (OA) is a common cause of pain and activity limitations causing significant burden on healthcare services
      • McAlindon T.
      • Bannuru R.
      • Sullivan M.
      • Arden N.
      • Berenbaum F.
      • Bierma-Zeinstra S.
      • et al.
      OARSI guidelines for the non-surgical management of knee osteoarthritis.
      . While there is no known treatment that prevents or reverses OA, traditional management of OA focuses on reducing the symptoms, i.e., pain and activity limitations, associated with the disease. Recently focus has shifted from treatment of end-stage OA to preventing progression of the disease, especially in early knee OA
      • Roos E.M.
      • Arden N.K.
      Strategies for the prevention of knee osteoarthritis.
      . One possible approach could be to use interventions that address known risk factors for progression of OA. Risk factors predicting worsening in symptoms and activity limitations include slow walking speeds, obesity, older age and decreased leisure time physical activity (LTPA)
      • van Dijk G.M.
      • Veenhof C.
      • Spreeuwenberg P.
      • Coene N.
      • Burger B.J.
      • van Schaardenburg D.
      • et al.
      Prognosis of limitations in activities in osteoarthritis of the hip or knee: a 3-year cohort study.
      • Pisters M.F.
      • Veenhof C.
      • van Dijk G.M.
      • Heymans M.W.
      • Twisk J.W.
      • Dekker J.
      The course of limitations in activities over 5 years in patients with knee and hip osteoarthritis with moderate functional limitations: risk factors for future functional decline.
      . Obesity is associated with knee OA progression through sub-optimal biomechanical loading and low-grade systematic inflammation related to high body fat-mass
      • Roos E.M.
      • Arden N.K.
      Strategies for the prevention of knee osteoarthritis.
      • Murray I.R.
      • Benke M.T.
      • Mandelbaum B.R.
      Management of knee articular cartilage injuries in athletes: chondroprotection, chondrofacilitation, and resurfacing.
      . Further, people with knee OA have been shown to walk slower and adapt their gait patterns in order to avoid pain and to redistribute joint loading
      • Mundermann A.
      • Dyrby C.O.
      • Hurwitz D.E.
      • Sharma L.
      • Andriacchi T.P.
      Potential strategies to reduce medial compartment loading in patients with knee osteoarthritis of varying severity: reduced walking speed.
      • Zeni Jr., J.A.
      • Higginson J.S.
      Differences in gait parameters between healthy subjects and persons with moderate and severe knee osteoarthritis: a result of altered walking speed?.
      .
      Exercise has been shown to evoke positive changes on symptoms and functional capacity as well as facilitate weight loss
      • Fransen M.
      • McConnell S.
      • Harmer A.R.
      • van der Esch M.
      • Simic M.
      • Bennell K.L.
      Exercise for osteoarthritis of the knee: a Cochrane systematic review.
      • Messier S.P.
      • Mihalko S.L.
      • Legault C.
      • Miller G.D.
      • Nicklas B.J.
      • DeVita P.
      • et al.
      Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial.
      and is therefore strongly recommended in the management of knee OA
      • McAlindon T.
      • Bannuru R.
      • Sullivan M.
      • Arden N.
      • Berenbaum F.
      • Bierma-Zeinstra S.
      • et al.
      OARSI guidelines for the non-surgical management of knee osteoarthritis.
      • Hochberg M.C.
      • Altman R.D.
      • April K.T.
      • Benkhalti M.
      • Guyatt G.
      • McGowan J.
      • et al.
      American College of Rheumatology 2012 recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee.
      . However, pain is a major modulator for activity avoidance in patients with OA and may limit compliance with land-based exercise
      • Holla J.F.
      • Sanchez-Ramirez D.C.
      • van der Leeden M.
      • Ket J.C.
      • Roorda L.D.
      • Lems W.F.
      • et al.
      The avoidance model in knee and hip osteoarthritis: a systematic review of the evidence.
      . The aquatic environment allows the individual to exercise with reduced weight bearing and impact on the affected joints
      • Harrison R.A.
      • Hillman M.
      • Bulstrode S.
      Loading of the lower limb when walking partially immersed: implications for clinical practice.
      . Recent studies have shown that individuals with lower-limb OA experience significantly less pain during aquatic compared to land-based exercise of equivalent intensity
      • Denning W.M.
      • Bressel E.
      • Dolny D.G.
      Underwater treadmill exercise as a potential treatment for adults with osteoarthritis.
      • Roper J.A.
      • Bressel E.
      • Tillman M.D.
      Acute aquatic treadmill exercise improves gait and pain in people with knee osteoarthritis.
      . Our recent systematic reviews revealed that aquatic exercise evokes both a small and a moderate effect on physical functioning in people with lower limb OA
      • Waller B.
      • Ogonowska-Slodownik A.
      • Vitor M.
      • Lambeck J.
      • Daly D.
      • Kujala U.M.
      • et al.
      Effect of therapeutic aquatic exercise on symptoms and function associated with lower limb osteoarthritis: systematic review with meta-analysis.
      and healthy older people
      • Waller B.
      • Ogonowska-Słodownik A.
      • Vitor M.
      • Rodionova K.
      • Lambeck J.
      • Heinonen A.
      • et al.
      The effect of aquatic exercise on physical functioning in the older adult: a systematic review with meta-analysis.
      , respectively. The difference in effect size is thought, in part, to be due to the higher intensity of training implemented with the healthy older adults
      • Lim J.Y.
      • Tchai E.
      • Jang S.N.
      Effectiveness of aquatic exercise for obese patients with knee osteoarthritis: a randomized controlled trial.
      . Further, lack of reporting of actual training intensities achieved in all the included aquatic exercise studies, limits interpretation of the results. Moreover, higher levels LTPA can have a positive impact on body composition and also predict a slower progression of OA related symptoms and activity limitations
      • van Dijk G.M.
      • Veenhof C.
      • Spreeuwenberg P.
      • Coene N.
      • Burger B.J.
      • van Schaardenburg D.
      • et al.
      Prognosis of limitations in activities in osteoarthritis of the hip or knee: a 3-year cohort study.
      • Pisters M.F.
      • Veenhof C.
      • van Dijk G.M.
      • Heymans M.W.
      • Twisk J.W.
      • Dekker J.
      The course of limitations in activities over 5 years in patients with knee and hip osteoarthritis with moderate functional limitations: risk factors for future functional decline.
      . LTPA levels have not been reported in any previous aquatic exercise studies and therefore the effect of this important cofounding factor has not been previously investigated.
      In order to prevent knee OA progression, the exercise intervention should be prescribed early in the disease progression
      • Roos E.M.
      • Arden N.K.
      Strategies for the prevention of knee osteoarthritis.
      . To the authors knowledge only one previous study has investigated the effect evoked by aquatic exercise in the early stage of knee OA development
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      . Our study, a randomised controlled trial (RCT), indicated that 4-months of aquatic resistance training improved estimated cardiovascular fitness and had a small significant impact on tibiofemoral cartilage as measured with quantitative magnetic resonance imaging (qMRI)
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      . Therefore, aims of this study are to report the effect of 4-months intensive aquatic resistance training program on body composition and functional capacity in postmenopausal women with mild knee OA, and whether possible changes are maintained after 12-months' follow-up. The effect of LTPA on the results and the training intensities achieved during the aquatic resistance training will also be investigated.

      Materials and methods

      Study design

      This study uses previously unreported outcome data collected from the registered AquaRehab research project (ISRCTN65346593), a RCT consisting of a 4-month aquatic intervention with a 12-month follow-up period. Data was collected from January 2012 to April 2014. The full description of the protocol can be found on open access
      • Waller B.
      • Munukka M.
      • Multanen J.
      • Rantalainen T.
      • Pöyhönen T.
      • Nieminen M.T.
      • et al.
      Effects of a progressive aquatic resistance exercise program on the biochemical composition and morphology of cartilage in women with mild knee osteoarthritis: protocol for a randomised controlled trial.
      , which was followed without changes and a full report of participant recruitment can be found from our previous study
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      . This study has two experimental arms: (1) aquatic resistance training and (2) control. Included participants were women aged 60–68 years old with mild knee OA. In this study we classify mild knee OA as experiencing knee pain on most days, not exceeding 5/10 VAS, with radiographic changes in tibiofemoral joint grades I (possible osteophytes) or II (definite osteophytes, possible joint space narrowing) according to the Kellgren–Lawrence (K/L) classification
      • Altman R.
      • Asch E.
      • Bloch D.
      • Bole G.
      • Borenstein D.
      • Brandt K.
      • et al.
      Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association.
      . Pre- and post-intervention results for the qMRI outcomes and patient reported symptoms have been previously reported
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      . This current study, in addition to patient reported symptoms, will report the outcomes for body composition and walking speed taken pre- and post-intervention as well as after the 12-months follow-up
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      . The study design and reporting follows the CONSORT recommendations for the conducting and reporting of randomized controlled trials
      • Moher D.
      • Hopewell S.
      • Schulz K.F.
      • Montori V.
      • Gotzsche P.C.
      • Devereaux P.J.
      • et al.
      CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials.
      . The study protocol (Dnro 19U/2011) was approved by the Ethics Committee of the Central Finland Health Care District and conforms to the Declaration of Helsinki. Written informed consent was obtained from all participants prior to enrolment.

      Subject recruitment

      Participants were recruited from the county of Central Finland using newspaper advertisements and telephone recruitment methods. Eligibility criteria was female aged 60–68 years old, body mass index (BMI) <35, experiences knee pain almost daily, K/L grades I or II and no medical reason preventing full participation in intensive exercise. Full eligibility criteria are described elsewhere
      • Waller B.
      • Munukka M.
      • Multanen J.
      • Rantalainen T.
      • Pöyhönen T.
      • Nieminen M.T.
      • et al.
      Effects of a progressive aquatic resistance exercise program on the biochemical composition and morphology of cartilage in women with mild knee osteoarthritis: protocol for a randomised controlled trial.
      .

      Randomisation and blinding

      The subjects were randomly allocated into one of the two arms of the study by a blinded external statistician, provided only with randomisation number and OA severity, using a computer generated block randomization of size of ten, stratified according to K/L grading. The first author performed the dual-energy X-ray absorptiometry (DXA) imaging but analysis was performed using the manufactures' in-built software without modification. Physical therapists providing the intervention also performed the physical performance measures. Principal investigators were blinded to group allocation.

      Interventions

      Those participants in the intervention group participated in an aquatic resistance training sessions lasting 1 h, 3 times a week for 16 weeks (48 sessions in total). Variable resistance equipment was used to progress training intensity with three resistance levels; barefoot, small resistance fins (Theraband products, The Hygienic Corporation, Akron, OH 44310 USA) and large resistance boots (Hydro-boots, Hydro-Tone Fitness Systems, Inc. Orange, CA 92865-2760, USA). Training intensity was set at as “hard and fast as possible”: A full description of the training program, its progression and daily training program can be found elsewhere
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      . The control group maintained usual care and were asked to continue their usual leisure time activities. They were offered the possibility of participating in two sessions consisting of 1 h of light stretching, relaxation and social interaction during the 4-month intervention period.

      Measures of exercise intensity and perceived exertion

      Maximum training intensity was ensured by measuring the maximum and average heartrates and rating of perceived exertion (RPE) for every training session using heart rate monitors (Polar Oy, Kemble. Finland). Maximum heartrate was estimated using the Karvonen formula (220 − age = maxHR) with no adjustments made for the possible effects of immersion. During the twelfth week capillary blood lactates and repetitions completed for all three training situations were measured. Self-reported emotional state felt during the aquatic resistance training was measured with a 1–5 Likert scale (1-Poor, 2-Tolerable, 3-Satisfactory, 4-Good, 5-Excellent).

      Outcome measures

      Outcomes for this study are body composition, walking speed and self-reported symptoms. Body composition (total body fat and lean body mass (kg)) was measured with dual-energy X-ray absorptiometry (DXA, Lunar Prodigy; GE Lunar Healthcare, Madison, WI, USA). All full body and regional images were analysed as per manufacturers' protocols using enCORE software (enCORE 2011, version 13.60.033). In vivo precision of these measurements has been reported to be high (CV 1.3–2.2%)
      • Uusi-Rasi K.
      • Rauhio A.
      • Kannus P.
      • Pasanen M.
      • Kukkonen-Harjula K.
      • Fogelholm M.
      • et al.
      Three-month weight reduction does not compromise bone strength in obese premenopausal women.
      . Walking speed was calculated from the UKK 2 km walking test. This test requires the subject to walk 2 km around a 200 m flat track as quickly as possible without running
      • Laukkanen R.
      • Oja R.
      • Pasanen M.
      • Vuori I.
      Criterion validity of a two-kilometer walking test for predicting the maximal oxygen uptake of moderately to highly active middle-aged adults.
      . Walking speed was calculated in metres per second (m/s) and describes walking ability and is a surrogate for aerobic fitness. Self-report pain (Pain), symptoms (Sym), activities of daily living (ADL), sports and recreation (Sport&Rec) and quality of life (QoL) were measured using be the five domains of the Finnish version of the knee injury and osteoarthritis outcome score (KOOS)
      • Koli J.
      • Multanen J.
      • Häkkinen A.
      • Kiviranta I.
      • Kujala U.
      • Heinonen A.
      Reliability of the Finnish versions of WOMAC and KOOS forms for knee osteoarthritis.
      . Scores are transformed into a score 0–100 with a score of 0 indicating extreme knee problems and 100 no knee problems
      • Bekkers J.E.
      • de Windt T.S.
      • Raijmakers N.J.
      • Dhert W.J.
      • Saris D.B.
      Validation of the knee injury and osteoarthritis outcome score (KOOS) for the treatment of focal cartilage lesions.
      .

      LTPA

      LTPA for each participant was calculated for the whole 4-month intervention and 12-month follow-up period using a daily physical activity diary. Participants recorded type of activity and self-perceived intensity of each activity, i.e., low, moderate or high, from which metabolic equivalent task hours (MET/h) per month was calculated
      • Ainsworth B.E.
      • Haskell W.L.
      • Herrmann S.D.
      • Meckes N.
      • Bassett Jr., D.R.
      • Tudor-Locke C.
      • et al.
      2011 Compendium of physical activities: a second update of codes and MET values.
      . The LTPA for the intervention group was calculated by combining the MET/h calculated from the aquatic resistance training and the physical activity diary.

      Statistical methods

      Results are displayed as mean and standard deviation (SD) unless otherwise stated. Between group baseline comparisons were performed using a bootstrap type t-test and Chi-squared. Repeated measures for walking speed, body composition and all domains of the KOOS were analysed using generalised linear mixed-models with unstructured correlation structure. Fixed effects were group, time and group-time interaction. Effect size, standardised beta coefficient (Beta (β)) adjusted for baseline values, was calculated for post intervention and at 12-month follow-up. Cohen's standard for Beta values above 0.10, 0.30 and 0.50 represent small, moderate and large effects respectively
      • Cohen J.
      A power primer.
      . Between group differences in average monthly LTPA during the 4 month intervention and 12-months period was tested using a Fisher–Pitman permutation test for two independent samples. The relationship between average monthly LTPA and body composition and walking speed, after removal of group allocation, was calculated using a mixed-effects regression model and represented as Cohen's f2, were 0.02, 0.15 and 0.35 indicate a small, moderate and large effect respectively
      • Cohen J.
      Statistical Power Analysis for the Behavioral Sciences.
      . Repeated analysis of variance (ANOVA) was used to compare the differences between the three training intensities (barefoot, small fins and large boots) and measures of training response i.e., RPE, heart rates, blood lactates, number of repetition performed per session and emotional state. Statistical analyses were performed using statistical software (Stata, release 13.1, StataCorp, College Station, Texas).
      This study is a post hoc analysis of original data thus the target sample size (n = 70, 35 per research arm) was calculated based on expect change in the qMRI outcome
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      .

      Results

      In total, 87 participants fulfilled the eligibility criteria and after attending baseline measurement were randomised into the two treatment arms of the study. There were no significant differences between the groups in any descriptive variables at baseline (Table I). Eighty five participants completed the intervention and 84 agreed to participate in the 12-month follow-up. In total 76 participants attended measurement at 12-months follow-up. Participant recruitment and reasons for loss to follow-up are shown in Fig. 1.
      Table IBaseline demographic and clinical characteristics
      Exercise group (n = 43)Control group (n = 44)
      Age (years)63.8 (2.4)63.9 (2.4)
      Height (cm)161.7 (5)161.6 (5)
      Body mass (kg)69.6 (10.3)71.0 (11.2)
      BMI (kg/m2)26.6 (3.8)27.1 (3.5)
      Affected knee (right/left)36/734/10
      K/L grade, n (%)
       Grade 123 (53.5)24 (54.5)
       Grade 220 (46.5)20 (45.5)
      Analgesia, n (%)
      Number of participants using analgesia for knee pain on inclusion to study.
      11 (26)9 (20)
      LTPA (MET/h/week)29 (31)36 (33)
      Smoker n (%)
       Never1713
       Current33
       Previous2328
      Blood pressure, n (%)
       Normal2314
       Elevated911
       Medical management1119
      Values are means (SD) unless otherwise noted.
      Number of participants using analgesia for knee pain on inclusion to study.
      Fig. 1
      Fig. 1Flow chart showing participant recruitment, randomisation and retention.

      Training intensities achieved during aquatic resistance training

      Adherence to the aquatic training program was high (88%), with only three subjects attending less than 70%. Pain during aquatic resistance training in the affected knee was reported more frequently during the first month (37 times), followed by a gradual decrease in frequency as the training progressed, with a three-fold reduction in the frequency (12 times) by the fourth month. Pain experienced in affected knee during the intervention was mild 14 (16) (visual analogue scale (VAS) 0–100 mm). Training intensity recorded from each complete training session is shown in Table II. There was a gradual increase in RPE when progressing from barefoot to large resistance boots while no significant differences in heart rates were measured. A full description of the daily training intensities measured and pain experienced during training can be found from the Supplemental material Appendix A. The attendance for the control group sessions was 68%.
      Table IIDescription of training intensities achieved during the aquatic resistance training and psychological feelings experienced per progression
      BarefootSmall FinsLarge boots
      No. Sessions81426
      RPE
      RPE = Rating of perceived exertion (BORG 6–20).
      13.7 (1.0)14.9 (1.3)15.0 (1.5)
      Bare vs Large (P < 0.001).
      Average HR (%)61 (5.9)61 (5.3)61 (6.3)
      Max HR (%)85 (7.8)84 (8.9)84 (8.0)
      Blood lactates (mmol/L)
      Measured directly after sessions 35–37.
      4.9 (2.1)4.5 (1.9)4.0 (1.8)
      Repetitions per session481 (66)408 (71)376 (65)
      Bare vs Large (P < 0.001).
      Self-reported emotional state4.2 (0.33)4.2 (0.36)4.3 (0.40)
      Mean and (SD) unless otherwise stated.
      RPE = Rating of perceived exertion (BORG 6–20).
      Measured directly after sessions 35–37.
      Bare vs Large (P < 0.001).

      Treatment effects and maintenance at 12-months

      Summaries of the treatment effects after 4-months and their maintenance at 12-months follow-up are presented in Fig. 2 and Table III. After 4-months aquatic resistance training there was a significant (P = 0.002) moderate (Beta (β): 0.32; 95% CI: 0.14 to 0.51) decrease in fat mass (−4.7% and 0.25% in training and control group respectively) and over-all moderate (β: 0.34; 0.15 to 0.52) decrease (−1.4% and 0.21%) in body weight (P = 0.004), both in favour of the intervention group. There was a significant (P < 0.001) decrease in fat mass in both legs −0.47 kg (−0.74 to −0.20) or a loss of −4.5% in the training group compared to 1.1% increase in the control group. There was a similar significant change (P = 0.007) in the trunk −0.63 kg (−1.1 to −0.17) or a loss of −3.1% compared to a 1.0% increase in the control group. Both significant findings were lost at 12-months follow-up. No localised change in lean mass was seen at any time point. After the intervention, a significant increase in walking speed (P = 0.002) was observed in favour of the intervention group (β: 0.3; 0.12 to 0.50). At 12-months follow-up walking speed (P = 0.032) in the intervention group remained significantly faster compared to the control group (β: 0.2; 0.01 to 0.44). No other significant between group differences could be seen in any domain of the KOOS questionnaire.
      Fig. 2
      Fig. 2Changes in A) fat and lean mass (kg) and B) walking speed (m/s) following a 4-months aquatic resistance training and 12-month follow-up period.
      Table IIIEffect of aquatic resistance training on walking speed, body composition and clinical symptoms
      VariablenAquatic training (AT)ControlMean difference (95% CI)P-value*nATControlMean difference (95% CI)P-value**
      BL mean (SD)FU mean (SD)BL mean (SD)FU mean (SD)12-FU mean (SD)12-FU mean (SD)
      Walking speed (m/s)871.74 (0.15)1.83 (0.16)1.73 (0.17)1.76 (0.17)0.052 (0.018 to 0.086)0.002731.82 (0.14)1.77 (0.13)0.046 (0.006 to 0.90)0.032
      Body composition
       Body mass (Kg)8769.2 (10.3)68.2 (10.4)70.8 (11.2)70.9 (11.3)−1.11 (−1.85 to −0.42)0.0047668.6 (10.6)70.8 (11.5)−0.39 (−1.51 to 0.64)0.543
       BMI8726.6 (3.8)26.2 (3.9)27.1 (3.5)27.1 (3.6)−0.46 (−0.74 to −0.19)0.0017626.4 (4.0)26.9 (3.7)0.001 (−0.47 to 0.47)0.892
       Lean mass (kg)8740.3 (3.9)40.6 (3.9)41.4 (4.4)41.7 (4.4)0.083 (−0.29 to 0.45)0.5907640.1 (4.0)41.9 (4.2)−0.30 (−0.79 to 0.12)0.410
       Fat mass (Kg)8726.0 (8.6)24.8 (8.8)26.5 (8.0)26.4 (8.1)−1.17 (−2.00 to −0.43)0.0027625.7 (8.8)26.1 (8.5)−0.14 (−1.24 to 0.90)0.700
      KOOS (0–100)
       Pain8780.6 (10.4)84.3 (10.5)82.1 (11.8)83.3 (11.7)2.3 (−1.93 to 6.31)0.1847686.8 (10.5)85.1 (12.4)1.45 (−2.72 to 5.66)0.187
       Symptoms8774.4 (12.9)80.9 (12.1)74.8 (14.1)77.5 (14.9)4.07 (−0.43 to 8.54)0.0917681.4 (11.4)77.9 (14.5)3.31 (−1.19 to 7.30)0.119
       ADL8784.5 (10.4)87.7 (9.7)85.2 (11.0)86.0 (14.6)3.36 (−0.38 to 7.118)0.1057489.2 (11.2)88.3 (11.0)0.97 (−2.64 to 4.32)0.397
       Sport&Rec8763.6 (20.5)70.6 (21.7)64.8 (22.2)67.6 (26.5)4.81 (−3.00 to 12.61)0.2237671.0 (20.7)68.7 (24.6)2.45 (−4.76 to 8.96)0.396
       QoL8766.0 (17.5)72.6 (18.1)70.6 (20.1)74.1 (23.1)2.76 (−3.51 to 8.66)0.2487575.0 (18.2)76.4 (24.4)1.21 (−5.97 to 7.98)0.308
      LTPA (MET/h)85160 (53)104 (63)56 (−81.4 to −31.1)<0.001†76100 (57)107 (56)−7.3 (−31.5 to 16.9)0.56†
      BL = baseline, FU = post-intervention (4-months), 12-FU = 12-months follow-up, *post-intervention follow-up compared to baseline (mixed model), **12-month follow-up compared to baseline (mixed-model).
      LTPA = average monthly total leisure time physical activity. †Fisher–Pitman permutation test.

      Effects of physical activity

      There was a significant (P < 0.001) between group difference in average monthly LTPA during the intervention period 160 (53) vs 104 (63) MET/h for intervention and control groups respectively. This difference was immediately lost following cessation of the aquatic training (Table III), monthly group averages are depicted in Fig. 3. After removal of group allocation there was a small (Cohen's f2 = 0.05) statistically significant (P = 0.007) relationship between higher average monthly LTPA (MET/h) and greater loss of fat mass. There was no relationship between LTPA (P = 0.52) and lean mass (f2 = 0.002) and a small (f2 = 0.02) but non-significant (P = 0.25) relationship with walking speed. While walking was the most popular form of LTPA (40.1%) there was no difference seen in activity type or intensities between the control and intervention group at any time point.
      Fig. 3
      Fig. 3Monthly leisure time physical activity (MET/h).

      Harms

      As previously reported
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      , one subject stopped the intervention following pain experienced after the first use of the large resistance boot (session 16). One subject complained of dyspnoea. After education training the participant was able to complete the intervention and attend follow-up measurements. The results of both participants are included as per intention-to-treat analysis. No subjects at pre- or post-intervention measurements were unable to walk the 2 km. At 12 months' follow-up two subjects, one from each group could not complete the 2 km; both due to a lower-limb injury unrelated to their knee OA.

      Discussion

      Our study indicates that an intensive aquatic resistance training program is effective at decreasing fat mass as well as improving walking speed in post-menopausal women with mild knee OA. This is the first randomised controlled study investigating the effects of aquatic resistance training on individuals with mild knee OA with a 12-month follow-up period. While, our results show that the improvements in body composition are lost at 12-months' follow-up, the improvements in walking speed were maintained. Importantly, higher average monthly LTPA was related with greater loss of fat mass over the 16-month study period. Further, this is the first study to report the actual training intensities achieved by the subjects during an aquatic exercise intervention and the effect of LTPA during the intervention and follow-up period.
      Increased fat mass is linked to knee OA through biomechanical
      • Browning R.C.
      • Kram R.
      Effects of obesity on the biomechanics of walking at different speeds.
      and low-grade inflammatory mechanisms
      • Vincent H.K.
      • Heywood K.
      • Connelley J.
      • Hurley R.W.
      Weight loss and obesity in the treatment and prevention of osteoarthritis.
      , and is associated with an increased risk of suffering from knee OA as well as a more rapid progression of the disease
      • Houard X.
      • Goldring M.B.
      • Berenbaum F.
      Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis.
      • Vuolteenaho K.
      • Koskinen A.
      • Moilanen E.
      Leptin – a link between obesity and osteoarthritis. applications for prevention and treatment.
      • Ding C.
      • Stannus O.
      • Cicuttini F.
      • Antony B.
      • Jones G.
      Body fat is associated with increased and lean mass with decreased knee cartilage loss in older adults: a prospective cohort study.
      . A change of −1% in body weight has been shown to have a significant association with slower loss of tibial cartilage volume and improvement in symptoms suggesting our 1.4% weight change could have a meaningful impact on both cartilage health and OA related symptoms
      • Teichtahl A.J.
      • Wluka A.E.
      • Tanamas S.K.
      • Wang Y.
      • Strauss B.J.
      • Proietto J.
      • et al.
      Weight change and change in tibial cartilage volume and symptoms in obese adults.
      . Our findings indicate a superior improvement in body composition compared with the two previous studies investigating the effects of aquatic exercise on body and fat mass in persons with OA
      • Lim J.Y.
      • Tchai E.
      • Jang S.N.
      Effectiveness of aquatic exercise for obese patients with knee osteoarthritis: a randomized controlled trial.
      • Kim I.S.
      • Chung S.H.
      • Park Y.J.
      • Kang H.Y.
      The effectiveness of an aquarobic exercise program for patients with osteoarthritis.
      . The respective −1.17 kg and −1.1 kg decreases in fat and body mass evoked in our study are larger than the non-significant decrease in fat mass (−0.7 kg) reported by Lim et al.
      • Lim J.Y.
      • Tchai E.
      • Jang S.N.
      Effectiveness of aquatic exercise for obese patients with knee osteoarthritis: a randomized controlled trial.
      and significant reduction in body mass (−0.76 kg) reported by Kim et al.
      • Kim I.S.
      • Chung S.H.
      • Park Y.J.
      • Kang H.Y.
      The effectiveness of an aquarobic exercise program for patients with osteoarthritis.
      . While this could be due our slightly longer duration i.e., 4 weeks longer, we also utilised a much higher training intensities. Lim et al.
      • Lim J.Y.
      • Tchai E.
      • Jang S.N.
      Effectiveness of aquatic exercise for obese patients with knee osteoarthritis: a randomized controlled trial.
      set intensity at 65% Max HR, while Kim et al.
      • Kim I.S.
      • Chung S.H.
      • Park Y.J.
      • Kang H.Y.
      The effectiveness of an aquarobic exercise program for patients with osteoarthritis.
      set intensity at RPE 12–13 (Borg 6–20), approximately 60% Max HR
      . In our study, average maximum heartrates during the main set were close to 85% with measured maximum HR up to 105%. Further, our finding demonstrate that high intensity aquatic exercise, appears to have similar effects as land-based exercise programs on body and fat mass. Messier et al.
      • Messier S.P.
      • Mihalko S.L.
      • Legault C.
      • Miller G.D.
      • Nicklas B.J.
      • DeVita P.
      • et al.
      Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial.
      , for example, reported that an 18-month, 3 times a week land-based exercise-only program produced a (−1.8 kg) loss in total body weight. However, the decrease in fat mass was only 1% (−0.4 kg) and loss of lean mass was 1% (−2.6 kg) in the exercise-only group. A loss of lean-mass and therefore reduction in muscle strength, is a common negative side effect of weight loss. Reduction in muscle mass and strength is associated with the development and faster progression of knee OA
      • van der Esch M.
      • Holla J.F.
      • van der Leeden M.
      • Knol D.L.
      • Lems W.F.
      • Roorda L.D.
      • et al.
      Decrease of muscle strength is associated with increase of activity limitations in early knee osteoarthritis: 3-year results from the cohort hip and cohort knee study.
      • Oiestad B.E.
      • Juhl C.B.
      • Eitzen I.
      • Thorlund J.B.
      Knee extensor muscle weakness is a risk factor for development of knee osteoarthritis. A systematic review and meta-analysis.
      , therefore preserving muscle mass during periods of weight loss is vital in this population
      • Ding C.
      • Stannus O.
      • Cicuttini F.
      • Antony B.
      • Jones G.
      Body fat is associated with increased and lean mass with decreased knee cartilage loss in older adults: a prospective cohort study.
      . Our study showed no change in lean mass and previously reported muscle strength
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      , indicating that while the training was intensive enough to evoke a decrease in fat mass it was also sufficient to preserve strength and lean mass.
      Improvements in walking speed after 4-months aquatic resistance training, and its maintenance, after a 12-month follow-up period, are in contrast to the results for body composition changes. Slower walking speeds are associated with faster progression of OA related symptoms and activity limitations and the small but sustained improvement of 0.05 m/s achieved in our study indicate a meaningful and lasting improvement in functional capacity
      • Perera S.
      • Mody S.H.
      • Woodman R.C.
      • Studenski S.A.
      Meaningful change and responsiveness in common physical performance measures in older adults.
      . Given that the weight lost during the intervention was regained during follow-up, our findings suggest that the effect on walking speed may not have been weight related. The results could indicate an improvement in cardiovascular fitness; however, the lack of between group differences in LTPA over the 12-months' follow-up period and at a level that had no effect on cardiovascular fitness in controls during the intervention period, suggests that this alone cannot explain the maintenance of walking speed. While there were no improvements in muscle strength of the knee extensors and flexors (previously reported
      • Munukka M.
      • Waller B.
      • Rantalainen T.
      • Hakkinen A.
      • Nieminen M.T.
      • Lammentausta E.
      • et al.
      Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
      ), we cannot rule out improvements in the un-measured ankle plantar flexors or hip abductors which could improve gait biomechanics and efficiency
      • Kulmala J.P.
      • Korhonen M.T.
      • Kuitunen S.
      • Suominen H.
      • Heinonen A.
      • Mikkola A.
      • et al.
      Which muscles compromise human locomotor performance with age?.
      . Further, strength alone is not a marker of improved gait biomechanics with efficient gait requiring co-ordination between agonist and antagonist muscles
      • Zeni Jr., J.A.
      • Higginson J.S.
      Differences in gait parameters between healthy subjects and persons with moderate and severe knee osteoarthritis: a result of altered walking speed?.
      • Mills K.
      • Hettinga B.A.
      • Pohl M.B.
      • Ferber R.
      Between-limb kinematic asymmetry during gait in unilateral and bilateral mild to moderate knee osteoarthritis.
      • Mills K.
      • Hunt M.A.
      • Leigh R.
      • Ferber R.
      A systematic review and meta-analysis of lower limb neuromuscular alterations associated with knee osteoarthritis during level walking.
      . Immersion results in a decrease in nociceptor stimulation and afferent feedback
      • Cronin N.J.
      • Valtonen A.M.
      • Waller B.
      • Poyhonen T.
      • Avela J.
      Effects of short term water immersion on peripheral reflex excitability in hemiplegic and healthy individuals: a preliminary study.
      • Pöyhönen T.
      • Avela J.
      Effect of head-out water immersion on neuromuscular function of the plantarflexor muscles.
      , and reduces the sensation of pain
      • Denning W.M.
      • Bressel E.
      • Dolny D.G.
      Underwater treadmill exercise as a potential treatment for adults with osteoarthritis.
      • Roper J.A.
      • Bressel E.
      • Tillman M.D.
      Acute aquatic treadmill exercise improves gait and pain in people with knee osteoarthritis.
      • Hall J.
      • Swinkels A.
      • Briddon J.
      • McCabe C.S.
      Does aquatic exercise relieve pain in adults with neurologic or musculoskeletal disease? A systematic review and meta-analysis of randomized controlled trials.
      • Fisken A.
      • Waters D.L.
      • Hing W.A.
      • Steele M.
      • Keogh J.W.
      Perception and responses to different forms of aqua-based exercise among older adults with osteoarthritis.
      . These conditions may create a suitable training condition for improving gait biomechanics
      • Roper J.A.
      • Bressel E.
      • Tillman M.D.
      Acute aquatic treadmill exercise improves gait and pain in people with knee osteoarthritis.
      . Alternatively, the high intensity intervention exposed the subjects to the sensation of high physical exertion. This could have taught the participants that it was safe for them to exert themselves at a higher intensity than previously thought. It is feasible to speculate that this exercise pedagogy was retained 12-months after intervention cessation. However, walking frequency and intensity as part of the monthly LTPA did not differ between groups suggesting the improvement in walking speed was not utilised. Ultimately, the mechanisms behind the effect of aquatic resistance training on walking speed, deserves further investigation.
      Education on life-style changes has been suggested as a vital part of management of both early and late-stage OA, in order to sustain improved levels of physical activity following an intervention study
      • Filardo G.
      • Kon E.
      • Longo U.G.
      • Madry H.
      • Marchettini P.
      • Marmotti A.
      • et al.
      Non-surgical treatments for the management of early osteoarthritis.
      . Participants in the training group did not have higher LTPA after the intervention than the control group therefore it is plausible to conclude that they returned back to pre-intervention level. Therefore, the increased walking speed may only describe improved functional capacity and may not be associated with increased walking speeds utilised in daily life. In combination with the possible exercise pedagogical effect of the high intensity exercise and implementation of a life-style education program, including dietary and advice, may have maintained or even continued the improvements in body composition and walking speed. Importantly, our results showed an association between higher levels LTPA and loss of fat mass irrespective of group allocation. Our results suggest that involvement in the intervention did not increase LTPA during the 12-months' follow-up period. However, LTPA was measured using self-reported questionnaires and it is plausible to hypothesise that after the intervention the participants in the training group may have changed their perception of activity intensities. Further, inclusion in a study may have caused a general increase in LTPA explaining the results. No acute worsening of clinical symptoms, as measured with the KOOS, was seen, possibility a result of the low impairment at baseline, the fluctuating nature of OA symptoms and the relatively short follow-up period
      • Roos E.M.
      • Arden N.K.
      Strategies for the prevention of knee osteoarthritis.
      .
      The strengths of this study included the randomised control design. The high adherence to the intervention and small number of drop-outs optimised the treatment response and shows motivation to participate in such an aquatic resistance exercise intervention. This is the first study to monitor LTPA, in addition to the exercise intervention, during an aquatic exercise intervention in participants with knee OA
      • Waller B.
      • Ogonowska-Slodownik A.
      • Vitor M.
      • Lambeck J.
      • Daly D.
      • Kujala U.M.
      • et al.
      Effect of therapeutic aquatic exercise on symptoms and function associated with lower limb osteoarthritis: systematic review with meta-analysis.
      , controlling an important confounding factor. The main limitation of this study was the use of strict inclusion criteria, essential for the original primary qMRI outcomes, which resulted in a homogeneous sample limiting direct application of our results to persons with more severe knee OA. However, it is conceivable to assume that, adapted, this program, would be suitable to improve functional capacity and decrease weight in subjects with more severe knee OA. Further studies are needed to confirm its efficacy in subjects with hip OA. The use of un-equal interventions i.e., only two sessions in the control group, introduces at least some degree of bias in favour of the intervention. Therefore, these results only indicate that aquatic resistance training is effective compared to no intervention and not more effective than another intervention. The lack of assessor blinding to the intervention may have resulted in bias, however, assessors had no vested interest in the results of this study and primary investigator was blinded throughout. Dietary intake was not measured or controlled for. Inclusion in a study has been shown to affect participants' dietary habits as well as physical activity and therefore we cannot directly attribute all the changes as a pure effect of the intervention. Diet alone, however, would not have accounted for the maintenance of lean body mass
      • Messier S.P.
      • Mihalko S.L.
      • Legault C.
      • Miller G.D.
      • Nicklas B.J.
      • DeVita P.
      • et al.
      Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial.
      . Further, greater increases in lean mass and decreases in fat mass may have occurred with appropriate diet
      • Thomas D.M.
      • Bouchard C.
      • Church T.
      • Slentz C.
      • Kraus W.E.
      • Redman L.M.
      • et al.
      Why do individuals not lose more weight from an exercise intervention at a defined dose? An energy balance analysis.
      . Intensity of the self-reported LTPA may have been affected after the intervention therefore use of objective measure after the intervention, e.g., accelerometers, would have given more accurate information
      • Ainsworth B.E.
      • Caspersen C.J.
      • Matthews C.E.
      • Masse L.C.
      • Baranowski T.
      • Zhu W.
      Recommendations to improve the accuracy of estimates of physical activity derived from self report.
      . It is not known if the mechanisms improving walking ability occurred earlier during the intervention therefore, future studies could look at the effectiveness of a shorter intensive aquatic exercise intervention.

      Conclusion

      To conclude, our findings show that a relatively short high intensity aquatic resistance training program decreases fat mass and improves walking speed in post-menopausal women with mild knee OA. Only improvements in walking speed were maintained at 12-months follow-up. Further, LTPA appeared more important for controlling body composition than walking speed. Therefore, future research should investigate if lifestyle education following an intensive aquatic resistance training intervention optimises long term benefits for people with knee OA. Additionally, research is needed to discover through which mechanism aquatic resistance training improves walking speed.

      Author contributions

      Waller, Benjamin: Analysis and interpretation of the data, drafting of the article, critical revision of the article for important intellectual content, final approval of the article, obtaining of funding, collection and assembly of data.
      Munukka, Matti: Analysis and interpretation of the data, drafting of the article, critical revision of the article for important intellectual content, final approval of the article, obtaining of funding, collection and assembly of data.
      Rantalainen, Timo: Analysis and interpretation of the data, critical revision of the article for important intellectual content, final approval of the article, administrative, technical, or logistic support, collection and assembly of data.
      Lammentausta, Eveliina: Conception and design, analysis and interpretation of the data, critical revision of the article for important intellectual content, final approval of the article, administrative, technical, or logistic support.
      Nieminen, Miika: Conception and design, analysis and interpretation of the data, critical revision of the article for important intellectual content, final approval of the article, administrative, technical, or logistic support.
      Kiviranta, Ilkka: Conception and design, analysis and interpretation of the data, critical revision of the article for important intellectual content, final approval of the article.
      Kautiainen, Hannu: Conception and design, analysis and interpretation of the data, drafting of the article, critical revision of the article for important intellectual content, final approval of the article, statistical expertise, collection and assembly of data.
      Häkkinen, Arja: Conception and design, analysis and interpretation of the data, drafting of the article, critical revision of the article for important intellectual content, final approval of the article.
      Kujala, Urho: Conception and design, analysis and interpretation of the data, drafting of the article, critical revision of the article for important intellectual content, final approval of the article.
      Heinonen, Ari: Conception and design, analysis and interpretation of the data, drafting of the article, critical revision of the article for important intellectual content, final approval of the article, obtaining of funding.

      Conflict of interest

      There is no conflict of interest for any authors.

      Role of funding sources

      Financial supporters were: Academy of Finland (ref: 253198), The Social Insurance Institution of Finland (KELA) (ref: 34/26/2011), Finnish Cultural Foundation and Yrjö Jahnsson Foundation (ref: 6699). None of these had a role in study design, collection, analysis and interpretation of data; in the writing of the manuscript; and in the decision to submit the manuscript for publication.

      Appendix A. Supplementary data

      The following is the supplementary data related to this article:

      References

        • McAlindon T.
        • Bannuru R.
        • Sullivan M.
        • Arden N.
        • Berenbaum F.
        • Bierma-Zeinstra S.
        • et al.
        OARSI guidelines for the non-surgical management of knee osteoarthritis.
        Osteoarthritis Cartilage. 2014; 22: 363-388
        • Roos E.M.
        • Arden N.K.
        Strategies for the prevention of knee osteoarthritis.
        Nat Rev Rheumatol. 2016; 12: 92-101https://doi.org/10.1038/nrrheum.2015.135
        • van Dijk G.M.
        • Veenhof C.
        • Spreeuwenberg P.
        • Coene N.
        • Burger B.J.
        • van Schaardenburg D.
        • et al.
        Prognosis of limitations in activities in osteoarthritis of the hip or knee: a 3-year cohort study.
        Arch Phys Med Rehabil. 2010; 91: 58-66https://doi.org/10.1016/j.apmr.2009.08.147
        • Pisters M.F.
        • Veenhof C.
        • van Dijk G.M.
        • Heymans M.W.
        • Twisk J.W.
        • Dekker J.
        The course of limitations in activities over 5 years in patients with knee and hip osteoarthritis with moderate functional limitations: risk factors for future functional decline.
        Osteoarthritis Cartilage. 2012; 20: 503-510https://doi.org/10.1016/j.joca.2012.02.002
        • Murray I.R.
        • Benke M.T.
        • Mandelbaum B.R.
        Management of knee articular cartilage injuries in athletes: chondroprotection, chondrofacilitation, and resurfacing.
        Knee Surg Sports Traumatol Arthrosc. 2016; 24: 1617-1626https://doi.org/10.1007/s00167-015-3509-8
        • Mundermann A.
        • Dyrby C.O.
        • Hurwitz D.E.
        • Sharma L.
        • Andriacchi T.P.
        Potential strategies to reduce medial compartment loading in patients with knee osteoarthritis of varying severity: reduced walking speed.
        Arthritis Rheum. 2004; 50: 1172-1178https://doi.org/10.1002/art.20132
        • Zeni Jr., J.A.
        • Higginson J.S.
        Differences in gait parameters between healthy subjects and persons with moderate and severe knee osteoarthritis: a result of altered walking speed?.
        Clin Biomech. 2009; 24: 372-378https://doi.org/10.1016/j.clinbiomech.2009.02.001
        • Fransen M.
        • McConnell S.
        • Harmer A.R.
        • van der Esch M.
        • Simic M.
        • Bennell K.L.
        Exercise for osteoarthritis of the knee: a Cochrane systematic review.
        Br J Sports Med. 2015; 49 (10.1136/bjsports-2015-095424): 1554-1557https://doi.org/10.1002/14651858.CD004376.pub3
        • Messier S.P.
        • Mihalko S.L.
        • Legault C.
        • Miller G.D.
        • Nicklas B.J.
        • DeVita P.
        • et al.
        Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial.
        JAMA. 2013; 310: 1263-1273https://doi.org/10.1001/jama.2013.277669
        • Hochberg M.C.
        • Altman R.D.
        • April K.T.
        • Benkhalti M.
        • Guyatt G.
        • McGowan J.
        • et al.
        American College of Rheumatology 2012 recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee.
        Arthritis Care Res. 2012; 64: 465-474
        • Holla J.F.
        • Sanchez-Ramirez D.C.
        • van der Leeden M.
        • Ket J.C.
        • Roorda L.D.
        • Lems W.F.
        • et al.
        The avoidance model in knee and hip osteoarthritis: a systematic review of the evidence.
        J Behav Med. 2014; 37: 1226-1241https://doi.org/10.1007/s10865-014-9571-8
        • Harrison R.A.
        • Hillman M.
        • Bulstrode S.
        Loading of the lower limb when walking partially immersed: implications for clinical practice.
        Physiotherapy. 1992; 78: 164-166
        • Denning W.M.
        • Bressel E.
        • Dolny D.G.
        Underwater treadmill exercise as a potential treatment for adults with osteoarthritis.
        Int J Aquat Res Educ. 2010; 4: 70-80
        • Roper J.A.
        • Bressel E.
        • Tillman M.D.
        Acute aquatic treadmill exercise improves gait and pain in people with knee osteoarthritis.
        Arch Phys Med Rehabil. 2013; 94: 419-425https://doi.org/10.1016/j.apmr.2012.10.027
        • Waller B.
        • Ogonowska-Slodownik A.
        • Vitor M.
        • Lambeck J.
        • Daly D.
        • Kujala U.M.
        • et al.
        Effect of therapeutic aquatic exercise on symptoms and function associated with lower limb osteoarthritis: systematic review with meta-analysis.
        Phys Ther. 2014; 94: 1383-1395https://doi.org/10.2522/ptj.20130417
        • Waller B.
        • Ogonowska-Słodownik A.
        • Vitor M.
        • Rodionova K.
        • Lambeck J.
        • Heinonen A.
        • et al.
        The effect of aquatic exercise on physical functioning in the older adult: a systematic review with meta-analysis.
        Age Ageing. 2016; https://doi.org/10.1093/ageing/afw102
        • Lim J.Y.
        • Tchai E.
        • Jang S.N.
        Effectiveness of aquatic exercise for obese patients with knee osteoarthritis: a randomized controlled trial.
        PM R. 2010; 2: 723-731
        • Munukka M.
        • Waller B.
        • Rantalainen T.
        • Hakkinen A.
        • Nieminen M.T.
        • Lammentausta E.
        • et al.
        Efficacy of progressive aquatic resistance training for tibiofemoral cartilage in postmenopausal women with mild knee osteoarthritis: a randomised controlled trial.
        Osteoarthritis Cartilage. 2016; 24: 1708-1717https://doi.org/10.1016/j.joca.2016.05.007
        • Waller B.
        • Munukka M.
        • Multanen J.
        • Rantalainen T.
        • Pöyhönen T.
        • Nieminen M.T.
        • et al.
        Effects of a progressive aquatic resistance exercise program on the biochemical composition and morphology of cartilage in women with mild knee osteoarthritis: protocol for a randomised controlled trial.
        BMC Musculoskelet Disord. 2013; 14: 82https://doi.org/10.1186/1471-2474-14-82
        • Altman R.
        • Asch E.
        • Bloch D.
        • Bole G.
        • Borenstein D.
        • Brandt K.
        • et al.
        Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association.
        Arthritis Rheum. 1986; 29: 1039-1049
        • Moher D.
        • Hopewell S.
        • Schulz K.F.
        • Montori V.
        • Gotzsche P.C.
        • Devereaux P.J.
        • et al.
        CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials.
        Int J Surg. 2012; 10: 28-55https://doi.org/10.1016/j.ijsu.2011.10.001
        • Uusi-Rasi K.
        • Rauhio A.
        • Kannus P.
        • Pasanen M.
        • Kukkonen-Harjula K.
        • Fogelholm M.
        • et al.
        Three-month weight reduction does not compromise bone strength in obese premenopausal women.
        Bone. 2010; 46: 1286-1293https://doi.org/10.1016/j.bone.2009.10.013
        • Laukkanen R.
        • Oja R.
        • Pasanen M.
        • Vuori I.
        Criterion validity of a two-kilometer walking test for predicting the maximal oxygen uptake of moderately to highly active middle-aged adults.
        Scand J Med Sci Sports. 1993; 3: 267-272
        • Koli J.
        • Multanen J.
        • Häkkinen A.
        • Kiviranta I.
        • Kujala U.
        • Heinonen A.
        Reliability of the Finnish versions of WOMAC and KOOS forms for knee osteoarthritis.
        Physiotherapy. 2011; 97: D203-D204
        • Bekkers J.E.
        • de Windt T.S.
        • Raijmakers N.J.
        • Dhert W.J.
        • Saris D.B.
        Validation of the knee injury and osteoarthritis outcome score (KOOS) for the treatment of focal cartilage lesions.
        Osteoarthritis Cartilage. 2009; 17: 1434-1439
        • Ainsworth B.E.
        • Haskell W.L.
        • Herrmann S.D.
        • Meckes N.
        • Bassett Jr., D.R.
        • Tudor-Locke C.
        • et al.
        2011 Compendium of physical activities: a second update of codes and MET values.
        Med Sci Sports Exerc. 2011; 43: 1575-1581https://doi.org/10.1249/MSS.0b013e31821ece12
        • Cohen J.
        A power primer.
        Psychol Bull. 1992; 112: 155-159
        • Cohen J.
        Statistical Power Analysis for the Behavioral Sciences.
        Lawrence Erlbaum, Hillsdale, N.J1988
        • Browning R.C.
        • Kram R.
        Effects of obesity on the biomechanics of walking at different speeds.
        Med Sci Sports Exerc. 2007; 39: 1632-1641https://doi.org/10.1249/mss.0b013e318076b54b
        • Vincent H.K.
        • Heywood K.
        • Connelley J.
        • Hurley R.W.
        Weight loss and obesity in the treatment and prevention of osteoarthritis.
        PM R. 2012; 4: S59-S67https://doi.org/10.1016/j.pmrj.2012.01.005
        • Houard X.
        • Goldring M.B.
        • Berenbaum F.
        Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis.
        Curr Rheumatol Rep. 2013; 15: 375https://doi.org/10.1007/s11926-013-0375-6
        • Vuolteenaho K.
        • Koskinen A.
        • Moilanen E.
        Leptin – a link between obesity and osteoarthritis. applications for prevention and treatment.
        Basic Clin Pharmacol Toxicol. 2014; 114: 103-108https://doi.org/10.1111/bcpt.12160
        • Ding C.
        • Stannus O.
        • Cicuttini F.
        • Antony B.
        • Jones G.
        Body fat is associated with increased and lean mass with decreased knee cartilage loss in older adults: a prospective cohort study.
        Int J Obes. 2013; 37: 822-827
        • Teichtahl A.J.
        • Wluka A.E.
        • Tanamas S.K.
        • Wang Y.
        • Strauss B.J.
        • Proietto J.
        • et al.
        Weight change and change in tibial cartilage volume and symptoms in obese adults.
        Ann Rheum Dis. 2015; 74: 1024-1029https://doi.org/10.1136/annrheumdis-2013-204488
        • Kim I.S.
        • Chung S.H.
        • Park Y.J.
        • Kang H.Y.
        The effectiveness of an aquarobic exercise program for patients with osteoarthritis.
        Appl Nurs Res. 2012; 25: 181-189https://doi.org/10.1016/j.apnr.2010.10.001
      1. Whaley M.H. Brubaker P.H. Otto R.M. ACSM's Guidelines for Exercise Testing and Prescription. Lippin cott Williams and Wilkins, Philadelphia2006
        • van der Esch M.
        • Holla J.F.
        • van der Leeden M.
        • Knol D.L.
        • Lems W.F.
        • Roorda L.D.
        • et al.
        Decrease of muscle strength is associated with increase of activity limitations in early knee osteoarthritis: 3-year results from the cohort hip and cohort knee study.
        Arch Phys Med Rehabil. 2014; 95: 1962-1968https://doi.org/10.1016/j.apmr.2014.06.007
        • Oiestad B.E.
        • Juhl C.B.
        • Eitzen I.
        • Thorlund J.B.
        Knee extensor muscle weakness is a risk factor for development of knee osteoarthritis. A systematic review and meta-analysis.
        Osteoarthritis Cartilage. 2015; 23: 171-177https://doi.org/10.1016/j.joca.2014.10.008
        • Perera S.
        • Mody S.H.
        • Woodman R.C.
        • Studenski S.A.
        Meaningful change and responsiveness in common physical performance measures in older adults.
        J Am Geriatr Soc. 2006; 54: 743-749
        • Kulmala J.P.
        • Korhonen M.T.
        • Kuitunen S.
        • Suominen H.
        • Heinonen A.
        • Mikkola A.
        • et al.
        Which muscles compromise human locomotor performance with age?.
        J R Soc Interface. 2014; 11: 20140858https://doi.org/10.1098/rsif.2014.0858
        • Mills K.
        • Hettinga B.A.
        • Pohl M.B.
        • Ferber R.
        Between-limb kinematic asymmetry during gait in unilateral and bilateral mild to moderate knee osteoarthritis.
        Arch Phys Med Rehabil. 2013; 94: 2241-2247https://doi.org/10.1016/j.apmr.2013.05.010
        • Mills K.
        • Hunt M.A.
        • Leigh R.
        • Ferber R.
        A systematic review and meta-analysis of lower limb neuromuscular alterations associated with knee osteoarthritis during level walking.
        Clin Biomech. 2013; 28: 713-724https://doi.org/10.1016/j.clinbiomech.2013.07.008
        • Cronin N.J.
        • Valtonen A.M.
        • Waller B.
        • Poyhonen T.
        • Avela J.
        Effects of short term water immersion on peripheral reflex excitability in hemiplegic and healthy individuals: a preliminary study.
        J Musculoskelet Neuronal Interact. 2016; 16: 58-62
        • Pöyhönen T.
        • Avela J.
        Effect of head-out water immersion on neuromuscular function of the plantarflexor muscles.
        Aviat Space Environ Med. 2002; 73: 1215-1218
        • Hall J.
        • Swinkels A.
        • Briddon J.
        • McCabe C.S.
        Does aquatic exercise relieve pain in adults with neurologic or musculoskeletal disease? A systematic review and meta-analysis of randomized controlled trials.
        Arch Phys Med Rehabil. 2008; 89: 873-883https://doi.org/10.1016/j.apmr.2007.09.054
        • Fisken A.
        • Waters D.L.
        • Hing W.A.
        • Steele M.
        • Keogh J.W.
        Perception and responses to different forms of aqua-based exercise among older adults with osteoarthritis.
        Int J Aquat Res Educ. 2014; 8: 32-52
        • Filardo G.
        • Kon E.
        • Longo U.G.
        • Madry H.
        • Marchettini P.
        • Marmotti A.
        • et al.
        Non-surgical treatments for the management of early osteoarthritis.
        Knee Surg Sports Traumatol Arthrosc. 2016; 26: 1775-1785https://doi.org/10.1007/s00167-016-4089-y
        • Thomas D.M.
        • Bouchard C.
        • Church T.
        • Slentz C.
        • Kraus W.E.
        • Redman L.M.
        • et al.
        Why do individuals not lose more weight from an exercise intervention at a defined dose? An energy balance analysis.
        Obes Rev. 2012; 13: 835-847https://doi.org/10.1111/j.1467-789X.2012.01012.x
        • Ainsworth B.E.
        • Caspersen C.J.
        • Matthews C.E.
        • Masse L.C.
        • Baranowski T.
        • Zhu W.
        Recommendations to improve the accuracy of estimates of physical activity derived from self report.
        J Phys Act Health. 2012; 9: S76-S84