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Functional Performance and Inflammatory Cytokines After Squat Exercises and Whole-Body Vibration in Elderly Individuals With Knee Osteoarthritis

  • Adriano P. Simão
    Affiliations
    Exercise Physiology Laboratory, School of Health and Biological Sciences, Federal University of the Jequitinhonha and Mucuri Valleys, Diamantina, Minas Gerais, Brazil

    Multicenter Post Graduation Program in Physiological Sciences, Brazilian Society of Physiology, São Paulo, Brazil
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  • Núbia C. Avelar
    Affiliations
    Exercise Physiology Laboratory, School of Health and Biological Sciences, Federal University of the Jequitinhonha and Mucuri Valleys, Diamantina, Minas Gerais, Brazil

    Multicenter Post Graduation Program in Physiological Sciences, Brazilian Society of Physiology, São Paulo, Brazil
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  • Rosalina Tossige-Gomes
    Affiliations
    Exercise Physiology Laboratory, School of Health and Biological Sciences, Federal University of the Jequitinhonha and Mucuri Valleys, Diamantina, Minas Gerais, Brazil
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  • Camila D. Neves
    Affiliations
    Exercise Physiology Laboratory, School of Health and Biological Sciences, Federal University of the Jequitinhonha and Mucuri Valleys, Diamantina, Minas Gerais, Brazil
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  • Vanessa A. Mendonça
    Affiliations
    Exercise Physiology Laboratory, School of Health and Biological Sciences, Federal University of the Jequitinhonha and Mucuri Valleys, Diamantina, Minas Gerais, Brazil

    Multicenter Post Graduation Program in Physiological Sciences, Brazilian Society of Physiology, São Paulo, Brazil
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  • Aline S. Miranda
    Affiliations
    Immunopharmacology Laboratory, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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  • Mauro M. Teixeira
    Affiliations
    Immunopharmacology Laboratory, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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  • Antônio L. Teixeira
    Affiliations
    Immunopharmacology Laboratory, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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  • André P. Andrade
    Affiliations
    Physical Education School, Occupational Therapy and Physiotherapy, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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  • Cândido C. Coimbra
    Affiliations
    Endocrinology Laboratory, Biological Sciences Institute, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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  • Ana Cristina Lacerda
    Correspondence
    Reprint requests to Ana Cristina R. Lacerda, PhD, School of Health and Biological Sciences, Exercise Physiology Laboratory, Federal University of the Jequitinhonha and Mucuri Valleys, Gloria's St #187, DownTown, 39100-000 Diamantina, Minas Gerais, Brazil
    Affiliations
    Exercise Physiology Laboratory, School of Health and Biological Sciences, Federal University of the Jequitinhonha and Mucuri Valleys, Diamantina, Minas Gerais, Brazil

    Multicenter Post Graduation Program in Physiological Sciences, Brazilian Society of Physiology, São Paulo, Brazil
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Published:April 30, 2012DOI:https://doi.org/10.1016/j.apmr.2012.04.017

      Abstract

      Simão AP, Avelar NC, Tossige-Gomes R, Neves CD, Mendonça VA, Miranda AS, Teixeira MM, Teixeira AL, Andrade AP, Coimbra CC, Lacerda AC. Functional performance and inflammatory cytokines after squat exercises and whole-body vibration in elderly individuals with knee osteoarthritis.

      Objective

      To investigate the effects of squat exercises combined with whole-body vibration on the plasma concentration of inflammatory markers and the functional performance of elderly individuals with knee osteoarthritis (OA).

      Design

      Clinical, prospective, randomized, single-blinded study.

      Setting

      Exercise physiology laboratory.

      Participants

      Elderly subjects with knee OA (N=32) were divided into 3 groups: (1) squat exercises on a vibratory platform (platform group, n=11); (2) squat exercises without vibration (squat group, n=10); and (3) the control group (n=11).

      Interventions

      The structured program of squat exercises in the platform and squat groups was conducted 3 times per week, on alternate days, for 12 weeks.

      Main Outcome Measures

      Plasma soluble tumor necrosis factor-α receptors 1 (sTNFR1) and 2 (sTNFR2) were measured using immunoassays (the enzyme-linked immunosorbent assay method). The Western Ontario and McMaster Universities Osteoarthritis Index questionnaire was used to evaluate self-reported physical function, pain, and stiffness. The 6-minute walk test, the Berg Balance Scale, and gait speed were used to evaluate physical function.

      Results

      In the platform group, there were significant reductions in the plasma concentrations of the inflammatory markers sTNFR1 and sTNFR2 (P<.001 and P<.05, respectively) and self-reported pain (P<.05) compared with the control group, and there was an increase in balance (P<.05) and speed and distance walked (P<.05 and P<.001, respectively). In addition, the platform group walked faster than the squat group (P<.01).

      Conclusions

      The results suggest that whole-body vibration training improves self-perception of pain, balance, gait quality, and inflammatory markers in elderly subjects with knee OA.

      Key Words

      List of Abbreviations:

      BMI (body mass index), g (gravity), IL (interleukin), OA (osteoarthritis), sTNFR1 (soluble tumor necrosis factor-α receptor-1), sTNFR2 (soluble tumor necrosis factor-α receptor-2), sTNFRs (soluble receptors of tumor necrosis factor-α), TNF-α (tumor necrosis factor-α), TNFR1 (cell surface tumor necrosis factor-α receptor-1), TNFR2 (cell surface tumor necrosis factor-α receptor-2), WOMAC (Western Ontario and McMaster Universities Osteoarthritis Index)
      OSTEOARTHRITIS (OA) IS a slow and progressive disease that is characterized by the degradation of articular cartilage and subchondral bone.
      • Kuettner K.E.
      • Cole A.A.
      Cartilage degeneration in different human joints.
      • Miller G.D.
      • Nicklas B.J.
      • Loeser R.F.
      Inflammatory biomarkers and physical function in older, obese adults with knee pain and self-reported osteoarthritis after intensive weight-loss therapy.
      The degradation of articular knee cartilage in OA causes an inflammatory process (ie, the release of cytokines and the endogenous mediators of inflammatory reactions) that is responsible for the proteolytic digestion of articular cartilage.
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      • Englund M.
      The role of biomechanics in the initiation and progression of OA of the knee.
      Studies have shown that OA is associated with high serum levels of inflammatory markers, including tumor necrosis factor-α (TNF-α) and the soluble receptors of TNF-α (sTNFR1 and sTNFR2).
      • Kuettner K.E.
      • Cole A.A.
      Cartilage degeneration in different human joints.
      • Miller G.D.
      • Nicklas B.J.
      • Loeser R.F.
      Inflammatory biomarkers and physical function in older, obese adults with knee pain and self-reported osteoarthritis after intensive weight-loss therapy.
      • Fernandes J.C.
      • Martel-Pelletier J.
      • Pelletier J.P.
      The role of cytokines in osteoarthritis pathophysiology.
      According to Penninx et al,
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      high levels of soluble TNF-α receptors were associated with decreased physical function, increased OA symptoms (eg, pain and stiffness), and worse radiographic scores in elderly, obese individuals with knee OA.
      Although the process of articular cartilage degradation is considered to be irreversible, it is known that it can be stabilized or slowed with physical activities that build strength and proprioception in the lower limbs.
      • Englund M.
      The role of biomechanics in the initiation and progression of OA of the knee.
      • Jan M.H.
      • Lin C.H.
      • Lin Y.F.
      • Lin J.J.
      • Lin D.H.
      Effects of weight-bearing versus nonweight-bearing exercise on function, walking speed, and position sense in participants with knee osteoarthritis: a randomized controlled trial.
      • Dunlop D.D.
      • Semanik P.
      • Song J.
      • et al.
      Moving to maintain function in knee osteoarthritis: evidence from the osteoarthritis initiative.
      The greatest challenge of conservative OA treatment in the elderly is to find physical activities that act within the therapeutic window (ie, the load is high enough to be effective but not high enough to cause joint deterioration). Within this perspective, whole-body vibration training has been recommended as an efficient and safe tool for building muscle strength
      • Verschueren S.M.
      • Roelants M.
      • Delecluse C.
      • Swinnen S.
      • Vanderschueren D.
      • Boonen S.
      Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study.
      • Roelants M.
      • Delecluse C.
      • Verschueren S.M.
      Whole-body-vibration training increases knee-extension strength and speed of movement in older women.
      and proprioception
      • Verschueren S.M.
      • Roelants M.
      • Delecluse C.
      • Swinnen S.
      • Vanderschueren D.
      • Boonen S.
      Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study.
      in older women with knee OA.
      • Trans T.
      • Aaboe J.
      • Henriksen M.
      • Christensen R.
      • Bliddal H.
      • Lund H.
      Effect of whole body vibration exercise on muscle strength and proprioception in females with knee osteoarthritis.
      Whole-body vibration training is achieved on a vibratory platform, and the amplitude is varied while the patient is either positioned orthostatically or performing dynamic movements (eg, squats with unipedal or bipedal support, or plantar flexion movements with feet supported over the platform).
      • Bogaerts A.
      • Verschueren S.
      • Delecluse C.
      • Claessens A.L.
      • Boonen S.
      Effects of whole body vibration training on postural control in older individuals: a 1 year randomized controlled trial.
      • Delecluse C.
      • Roelants M.
      • Verschueren S.
      Strength increase after whole-body vibration compared with resistance training.
      There is a gap in the literature concerning the capacity of whole-body vibration training to minimize inflammatory components or to prevent functional decline and disease progression in elderly individuals with knee OA. The purpose of this study was to investigate the effects of squat exercises combined with whole-body vibration on the plasma concentration of inflammatory markers and the functional performance of elderly individuals with knee OA. Because the vibratory stimulus strengthens the lower limbs
      • Verschueren S.M.
      • Roelants M.
      • Delecluse C.
      • Swinnen S.
      • Vanderschueren D.
      • Boonen S.
      Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study.
      • Roelants M.
      • Delecluse C.
      • Verschueren S.M.
      Whole-body-vibration training increases knee-extension strength and speed of movement in older women.
      and improves proprioception
      • Verschueren S.M.
      • Roelants M.
      • Delecluse C.
      • Swinnen S.
      • Vanderschueren D.
      • Boonen S.
      Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study.
      in elderly patients with knee OA by inducing isometric, concentric, and eccentric contractions of the hip and knee extensor muscle groups and the plantar flexors, it was hypothesized that the subjects in the platform group, which involved squat exercise training along with whole-body vibration, would have better control and execution of functional movements, such as those required for balance and gait performance, compared with the control (which did not receive training) and the squat (which involved squat exercise training without whole-body vibration) groups. In addition, the combination of squat exercises and whole-body vibration would improve the stability of the knee affected by OA by reducing the inflammatory joint process and, consequently, the self-perception of pain.

      Methods

      This prospective, randomized, single-blinded study assessed variables immediately before and after a 12-week training program. For the allocation of participants, a 1:1 ratio randomization was performed using opaque envelopes for the concealment of allocation. To minimize the chance of bias, opaque, sealed, and serial-numbered envelopes were used that were opened sequentially (only after the participant's name and further details were written on the envelope) and kept in a locked, secure place. The allocation sequence was concealed from the researcher who enrolled and assessed participants. Only 1 researcher was aware of the group assignments when performing the randomization. This study was approved by the Scientific Ethics Committee of the Federal University of Jequitinhonha and Mucuri Valleys (protocol n° 001/08).
      To participate in the study, patients had to be 60 years or older and have a diagnosis of OA in at least 1 knee based on the clinical and radiographic criteria of the American College of Rheumatology
      • Hinton R.
      • Moody R.L.
      • Davis A.W.
      • Thomas S.F.
      Osteoarthritis: diagnosis and therapeutic considerations.
      : (1) knee pain for most of the days in the previous month; (2) osteophytes at the joint margins on radiographs; (3) synovial fluid typical of OA (laboratory); (4) age 40 years or older; (5) crepitus on active joint motion; and (6) morning stiffness lasting 30 minutes or less. The subjects could only receive a diagnosis of knee OA if the following American College of Rheumatology criteria were present: criteria 1 and 2; criteria 1, 3, 5, and 6; or criteria 1, 4, 5, and 6.
      The severity of the knee OA was classified radiographically according to the Kellgren-Lawrence scale (grades 0–4: 0, normal; 4, severe OA). Grade 2 (definite osteophytes and possible narrowing of the joint space) was used as a cutoff to classify knee OA.
      • Kellgren J.H.
      • Lawrence J.S.
      Radiological assessment of osteo-arthrosis.
      • Schiphof D.
      • de Klerk B.M.
      • Koes B.W.
      • Bierma-Zeinstra S.
      Good reliability, questionable validity of 25 different classification criteria of knee osteoarthritis: a systematic appraisal.
      Exclusion criteria were the following: (1) recent knee trauma; (2) use of any device to assist locomotion (eg, walking sticks, crutches, walkers); (3) physiotherapy treatment or any other rehabilitation procedure in the last 3 months; (4) the absence of the minimum clinical and cognitive conditions for performing physical activities; and (5) use of glucocorticoids for at least 2 months before beginning the study. Patients were also excluded if they had the following: orthopedic disease; neurologic, respiratory, or acute cardiac issues that prevented the performance of the required exercises; vestibular disorders; immunosuppression or immunodeficiency; lack of sphincter control (anal and bladder); or cognitive deficits, as determined by a lower score on the Mini-Mental State Examination than obtained by other patients with the same education level.
      • Bertolucci P.H.
      • Brucki S.M.
      • Campacci S.R.
      • Juliano Y.
      [The Mini-Mental State Examination in a general population: impact of educational status] [Portuguese].
      This examination consists of 6 categories, which include memory, spatial orientation, temporal orientation, judgment, problem solving, and reasoning. Each category is scored from 0 to 3. The sum of the scores obtained in each category is determined, and higher scores signify lower cognitive impairment. The cutoff point was 13 for illiterate subjects, 18 for subjects with 1 to 3 years of education, 23 for subjects with 4 to 7 years of education, and 26 for subjects with more than 7 years of education.
      A total of 125 elderly patients were evaluated, and 35 (4 men, 31 women) met the criteria for inclusion and participated in the research. Once included in the study, volunteers were randomly distributed into 1 of 3 groups: the platform group (n=12), which involved squat exercise training along with whole-body vibration; the squat group (n=11), which involved squat exercise training without whole-body vibration; and the control group (n=12), in which the members did not receive training and were instructed not to change their lifestyle during the study or engage in any new type of physical activity. To ensure the maintenance of patients in the control group, weekly phone calls were made to each group member to confirm his/her routine activities. Thirty-two of the 35 elderly individuals completed the study and were reassessed after the 12-week training period (fig 1).
      Figure thumbnail gr1
      Fig 1Study flowchart. Pretest and posttest correspond to the periods immediately before and after the training, respectively.

      Procedures

      Clinical and demographic data related to the participants were initially collected, and all study patients (platform, squat, and control groups) underwent a clinical evaluation and blood sample collection before the initiation of the 12-week intervention program for the platform and squat groups. The blood draws were always collected at 8 am for the volunteers of all the groups, followed by the clinical tests. At the end of the training period, the volunteers of the 3 groups were reassessed.
      The structured program of squat exercises in the platform and squat groups was conducted 3 times per week, on alternate days, for 12 weeks. The squat exercise was performed starting at approximately 10° of knee flexion and continuing until 60° of knee flexion was reached. For each volunteer, a knee angle of 60° was measured before the series of exercises, and a barrier was imposed on the buttocks to limit the degree of knee flexion.
      For temporal control during the squat, an examiner provided verbal encouragement to standardize the length of maintaining the semifull position (3s) and the flexed position (3s of isometric contraction) of the knees in each squat repetition. In addition, a predetermined distance from the feet (14cm to the right and 14cm to the left of the vibration center of the platform) was set to ensure that each of the lower limbs received the same amount of vibration stimulus. Moreover, with the aim of maintaining control of the body's center of gravity behind the base of the support, the positioning of the spine, arms, and head and the type of squat (simulating the motion of sitting in a chair) were standardized.
      The platform group subjects received a vertical sinusoidal vibration at a preestablished frequency (FitVibea).
      The parameters of the vibration in the platform group were based on the principles of training load progression: the frequency was varied from 35 to 40Hz, the amplitude was 4mm, and the acceleration ranged from 2.78 to 3.26g. The choice of vibratory frequencies and the amplitude were set in order to obtain an acceleration range between 2 and 5g (gravity), which was suggested to be sufficient by Delecluse et al
      • Delecluse C.
      • Roelants M.
      • Verschueren S.
      Strength increase after whole-body vibration compared with resistance training.
      for achieving the desired physiologic effects. Before the data collection, the acceleration values of the platform were measured using the accelerometer Megab (ZPP1-3D-BC The Acceleration Measuring Kit).
      The volume of the squat training for the squat and platform groups was increased systematically during the 12-week intervention by increasing the time and number of sets and reducing the rest time (table 1). For patients in the platform group, the vibration acceleration was also increased by varying the vibratory frequency (35–40Hz).
      • Trans T.
      • Aaboe J.
      • Henriksen M.
      • Christensen R.
      • Bliddal H.
      • Lund H.
      Effect of whole body vibration exercise on muscle strength and proprioception in females with knee osteoarthritis.
      • Bogaerts A.
      • Verschueren S.
      • Delecluse C.
      • Claessens A.L.
      • Boonen S.
      Effects of whole body vibration training on postural control in older individuals: a 1 year randomized controlled trial.
      • Rees S.S.
      • Murphy A.J.
      • Watsford M.L.
      Effects of whole body vibration on postural steadiness in an older population.
      • Avelar N.C.
      • Simao A.P.
      • Tossige-Gomes R.
      • et al.
      The effect of adding whole-body vibration to squat training on the functional performance and self-report of disease status in elderly patients with knee osteoarthritis: a randomized, controlled clinical study.
      The protocol was designed in accordance with the International Organization for Standardization 2631-1 guidelines for the prescription of training intensity, in which the ideal parameters of frequency, amplitude, and time of exposure to whole-body vibration are defined based on the acceleration values.
      • Griffin M.J.
      Minimum health and safety requirements for workers exposed to hand-transmitted vibration and whole-body vibration in the European Union; a review.
      In addition, an effort was made to use training parameters that were similar to the parameters implemented in previous studies.
      • Trans T.
      • Aaboe J.
      • Henriksen M.
      • Christensen R.
      • Bliddal H.
      • Lund H.
      Effect of whole body vibration exercise on muscle strength and proprioception in females with knee osteoarthritis.
      • Bogaerts A.
      • Verschueren S.
      • Delecluse C.
      • Claessens A.L.
      • Boonen S.
      Effects of whole body vibration training on postural control in older individuals: a 1 year randomized controlled trial.
      • Kawanabe K.
      • Kawashima A.
      • Sashimoto I.
      • Takeda T.
      • Sato Y.
      • Iwamoto J.
      Effect of whole-body vibration exercise and muscle strengthening, balance, and walking exercises on walking ability in the elderly.
      Table 1Progression of Training in Platform and Squat Groups
      WeeksParameters of the Vibration
      Only for platform group.
      Time (s)/No. of Series of the Squat
      Platform and squat groups.
      Rest Time Between Series (s)
      Platform and squat groups.
      Frequency of Vibration (Hz)Vibration Amplitude (mm)Acceleration (g)
      1354220/620
      2354220/620
      3354225/725
      4354230/825
      5354230/830
      6354240/830
      74042.6140/840
      84042.6140/840
      94042.6140/830
      104042.6140/830
      114042.6140/825
      124042.6140/825
      low asterisk Only for platform group.
      Platform and squat groups.
      Before the squat exercise, the intervention groups (squat and platform) warmed up on exercise bikesc for 10 uninterrupted minutes at 70% of maximum cardiac frequency, which was predicted for age and was monitored with a cardiofrequency meter (Polar model F4d).

      Analysis of Inflammatory Markers With Enzyme-Linked Immunosorbent Assay

      For plasma processing, 10-mL blood samples were collected from the antecubital vein using aseptic technique and heparin as an anticoagulant. The blood was immediately centrifuged twice at 3.000g for 10 minutes, and the plasma was kept frozen at –70°C until assayed. Plasma sTNFR1 and sTNFR2 levels were measured according to the procedures supplied by the manufacturer and using ELISA kits for sTNFR1 and sTNFR2 (DuoSete). The detection limit was 5pg/mL for both soluble receptors.

      Radiographic Evaluation

      To confirm the diagnosis of knee OA, digital radiographic evaluations were performed on all participants. Anteroposterior oblique and lateral images of the knees were collected with subjects in the orthostatic position bearing weight on the lower limbs.
      • Harada N.
      • Chiu V.
      • Damronrodriguez J.
      • Fowler E.
      • Siu A.
      • Reuben D.B.
      Screening for balance and mobility impairment in elderly individuals living in residential care facilities.
      The radiologic classification of OA severity, which was based on the Kellgren-Lawrence scale,
      • Kellgren J.H.
      • Lawrence J.S.
      Radiological assessment of osteo-arthrosis.
      was performed by 2 examiners who were blinded to the clinical status of the participants. There was 100% agreement on the assessments of radiographic images by the examiners.

      Clinical Tests

      In all cases, the clinical tests were administered by the same examiner who was blinded to the group assignments of the participants. The order of testing was always the same for the physical function tests both before and after the intervention period.

      Western Ontario and McMaster Universities Osteoarthritis Index

      Self-reported functional performance was evaluated using the Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC), validated for Brazilian populations.
      • Fernandes M.I.
      Tradução e validação do questionário de qualidade de vida específico para a osteoartrose WOMAC (Western Ontario and McMaster Universities Osteoarthritis Index) para a língua portuguesa [dissertação].
      The WOMAC, which is composed of 24 items, was developed to measure health status and assess a patient's self-perception of pain (5 questions), joint stiffness (2 questions), and functional performance (17 questions) during the previous 72 hours. The WOMAC score was presented on a Likert-type scale where questions received a score of 0, 25, 50, 75, or 100 for no pain, a little pain, moderate pain, intense pain, and very intense pain, respectively.
      • Bellamy N.
      • Buchanan W.W.
      • Goldsmith C.H.
      • Campbell J.
      • Stitt L.W.
      Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee.

      Functional performance tests

      Before the functional performance tests, the participants were instructed to use the bathroom, dress in comfortable clothing and shoes, drink 500 mL of water, eat a light meal, and avoid arduous activity for at least 2 hours.
      Functional performance was evaluated based on the Berg Balance Scale,
      • Miyamoto S.T.
      • Lombardi Junior I.
      • Berg K.O.
      • Ramos L.R.
      • Natour J.
      Brazilian version of the Berg Balance Scale.
      • Berg K.O.
      • Maki B.E.
      • Williams J.I.
      • Holliday P.J.
      • Wood-Dauphinee S.L.
      Clinical and laboratory measures of postural balance in an elderly population.
      the gait speed test, and the 6-minute walk test.
      • Harada N.
      • Chiu V.
      • Damronrodriguez J.
      • Fowler E.
      • Siu A.
      • Reuben D.B.
      Screening for balance and mobility impairment in elderly individuals living in residential care facilities.
      All tests were performed on the same day, and the WOMAC questionnaire was administered before the tests. There was a 5-minute break between each functional performance test.

      Berg Balance Scale

      The Berg Balance Scale evaluates balance using 14 tasks that involve static and dynamic balance (ie, reach, turn, transfer, remain standing, and get up).
      • Miyamoto S.T.
      • Lombardi Junior I.
      • Berg K.O.
      • Ramos L.R.
      • Natour J.
      Brazilian version of the Berg Balance Scale.
      Performance was evaluated by direct observation, and scores ranged from 0 (unable to perform the task) to 4 (performs the task independently), with a maximum of 56 points. A score below 45 indicates poor balance.
      • Miyamoto S.T.
      • Lombardi Junior I.
      • Berg K.O.
      • Ramos L.R.
      • Natour J.
      Brazilian version of the Berg Balance Scale.
      • Berg K.O.
      • Maki B.E.
      • Williams J.I.
      • Holliday P.J.
      • Wood-Dauphinee S.L.
      Clinical and laboratory measures of postural balance in an elderly population.

      Gait speed test

      To evaluate gait speed, individuals were instructed to walk at a normal pace along a 10-m route. The first 2m and the last 2m were not evaluated because they were considered to correspond to acceleration and deceleration periods. Thus, the time required to complete the middle 6m was measured. The average time of 3 trials was used to calculate the gait speed in meters per second.
      • Abreu S.S.E.
      • Caldas C.P.
      Gait speed, balance and age: a correlational study among elderly women with and without participation in a therapeutic exercise program.

      Six-minute walk test

      The objective of the 6-minute walk test was to evaluate walking function. This test measures the greatest distance that the individual is able to walk in 6 minutes. On hearing a standardized verbal command, the individual walked as fast as possible (without running) from one end of the route to the other. After 6 minutes, the individual being evaluated was instructed to stop, and the distance traveled was recorded. Two tests were performed with an interval of at least 15 minutes between tests.
      ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories
      ATS statement: guidelines for the six-minute walk test.
      • Steffen T.M.
      • Hacker T.A.
      • Mollinger L.
      Age- and gender-related test performance in community-dwelling elderly people: Six-Minute Walk Test, Berg Balance Scale, Timed Up & Go Test, and gait speeds.

      Statistical Analysis

      Statistical analyses were performed with Prism 4.0 software.f The normality of the data distribution was assessed by the Shapiro-Wilk test.
      Nonparametric tests were used for the outcome analysis. The analysis between the groups was performed through variation (Δ) within each group, where postvalue – prevalue = Δ value.
      The sample characterization data were normally distributed and are presented as the mean and SD.
      The inflammatory markers and physical performance data were not normally distributed and are presented as the median and interquartile range. To evaluate the baseline and Δ value differences between groups, the Kruskal-Wallis test with Dunn's post hoc test was used for all the variables. The statistical significance was set at P<.05.

      Sample size

      Sample size was calculated according to the gait speed test. The gait speed test evaluates the ability of subjects to increase or decrease their walking speed above or below a “comfortable” pace, which can vary depending on the environment and task demands (eg, crossing streets and avoiding obstacles). To calculate the sample size, SD of .22 (obtained from the article by Penninx
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      ), a minimum difference of 0.5m/s between the groups, a significance level of 99%, and a statistical power of 80% were considered. As a result, the minimum number of subjects for each study group needed to be 5 participants. To compensate for possible losses in the study, 10% was added to this sample size for a total of 6 participants for each group.
      The following formula was used to calculate the sample size required for the gait speed test (comparison of quantitative measures between different groups):
      (Zα+Zβ)2×2×dp2d2


      where Zα is the critical value to avoid a type I error (99% significance level) = 2.575; Zβ is the critical value to avoid a type II error (80% statistical power) = .84; dp2 is the SD for the gait speed, obtained from Penninx
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      ; and d is the minimum difference to be detected between groups (0.5m/s in the gait speed).
      For the biomarkers studied (sTNFR1, sTNFR2), the statistical power of the study was calculated from the results of the effect size of the Δ values obtained from the comparisons before and after training.
      • Cohen J.
      A power primer.
      • Cohen J.
      The earth is round (p < .05).
      A comparison between the control and platform groups demonstrated that the magnitude of the effect was high for both sTNFR1 (Cohen's d=2.19) and sTNFR2 (Cohen's d=1.37), indicating that the study has a statistical power above 84% for these variables, and the minimum sample size to obtain a statistical power of 80% would be 7 individuals per group.
      • Portney L.G.
      • Watkins M.P.
      Foundations of clinical research: applications to practice.
      The following formula was used to calculate the effect size (Cohen
      • Cohen J.
      A power primer.
      ):
      d=(X1X2)/S


      where X1 = the mean of the result of the first group; X2 = the mean of the result of the second group; and S' = the common SD, which was calculated from the SD of the 2 groups.

      Results

      The characteristics of the sample population are shown in table 2. There were no significant differences in age, sex distribution, body height or weight, body mass index (BMI), or the OA grade among the 3 groups (P>.05), which confirmed the baseline homogeneity of the groups. The average age of the participants was 72 years, and the mean BMI was 28.7kg/m2. Most of the sample (87.5%) were women.
      Table 2Sample Characterization
      CharacteristicsControl Group (n= 11)Squat Group (n=10)Platform Group (n=10)P
      Age (y)71±5.369±3.775±7.4.063
      Body mass (kg)65.1±10.573.4±9.774.2±10.7.371
      Height (m)1.56±0.071.57±0.081.56±0.05.935
      BMI (kg/m2)26.7±2.7429.8±2.5327.4±9.7.456
      Sex: M/W (%)9/9110/9018/82NA
      Severity of knee OA
      Classified radiographically according to Kellgren-Lawrence scale.14
      (%)
      234234234NA
      462727501040203050
      NOTE. Values are mean ± SD or as otherwise indicated.
      Abbreviations: M, men; NA, not applicable W, women.
      low asterisk Classified radiographically according to Kellgren-Lawrence scale.
      • Kellgren J.H.
      • Lawrence J.S.
      Radiological assessment of osteo-arthrosis.
      All participants in both intervention groups complied with the full intervention program. The overall attendance was 99.7% in the platform group and 98.6% in the squat group. There was no statistically significant difference between the groups with respect to compliance (P<.05).
      The pretest and posttest values from the physical-functional evaluation and the plasma concentrations of sTNFR1 and sTNFR2 are shown in table 3.
      Table 3Values Pretest and Posttest From the Performance Evaluation and Plasma Concentrations of sTNFR1 and sTNFR2
      VariablesControl Group (n=12)Squat Group (n=11)Platform Group (n=12)Baseline P
      PretestPosttestΔPretestPosttestΔPretestPosttestΔ
      sTNFR1 (pg/mL)682.8 (617–849)1072.0 (879–1252)389.2 (102 to 638)722.4 (522–1052)742.5 (373–1492)155.0 (−720 to 536)1033.0 (718–1281)709.2 (379–1281)−146.0 (−826 to 183).09
      sTNFR2 (pg/mL)3568.0 (3319–5002)4673.0 (3266–5371)35.4 (−1206 to 2104)4141.0 (3329–4993)3650.0 (2949–4719)−497.7 (−1351 to 2219)4944.0 (3819–5862)3987.0 (2964–5067)−996.5 (−1750 to 147.3).20
      Self-reported pain (score)175.0 (125–350)175.0 (100–250)0 (−125 to 125)275.0 (150–350)150.0 (75–250)−62.5 (−325 to 75)312.5 (238–400)175.0 (75–275)−137.5 (−200 to 0).20
      Self-reported stiffness (score)75 (50–100)75 (25.0–150)0 (−75 to 125)100 (37.5–125)50 (0–137.5)−25 (−100 to 50)100 (75–137.5)75 (50–87.5)−25 (−125 to 50).28
      Self-reported function (score)625 (525–675)650 (450–950)75 (−225 to 400)900 (737.5–1213)847.5 (387.5–1088)−100 (−725 to 275)975 (600–1325)725 (350–1000)−175 (−550 to 100).07
      Berg Balance Scale (score)51.0 (50–55)54.0 (51–56)0 (−2 to 5)53.5 (50–55)54.5 (53–56)1.5 (−1 to 4)48.0 (45–55)54.0 (52–56)4.5 (0 to 14).24
      6-minute walk test (m)423.5 (384–443)430.0 (397–450)6 (−28 to 33)392.0 (361–454)410.6 (379–444)17.5 (−28 to 72)415.7 (377–488)438.0 (412–522)37.5 (−18 to 78).62
      Gait speed test (m/s)1.26 (1.12–1.41)1.33 (1.08–1.54)0.07 (−0.14 to 0.31)1.20 (1.13–1.47)1.38 (1.24–1.52)0.16 (−0.07 to 0.25)1.10 (0.99–1.28)1.37 (1.33–1.63)0.33 (0.23 to 0.42).31
      NOTE. Values are median (interquartile range) or as otherwise indicated.
      The variation (Δ) in the plasma concentrations of sTNFR1 and sTNFR2 showed a significant reduction in the platform group compared with the control group (P<.01 and P<.05, respectively) (fig 2).
      Figure thumbnail gr2
      Fig 2Variation of sTNFR1 (A) and sTNFR2 (B) plasma concentrations before and after the intervention period (delta = Δ). *Significant difference for platform group versus control group (P<.01 for sTNFR1 and P<.05 for sTNFR2).
      The data from the physical-functional evaluation, which were analyzed through variations in postintervention and preintervention (Δ) results, showed significant differences between the control and platform groups for self-reported pain (WOMAC: P<.05), balance (Berg Balance Scale: P<.05), and gait performance, which was evaluated by the gait speed and 6-minute walk tests (P<.05 and P<.001, respectively). Interestingly, the gait speed in the platform group was faster than in the squat group (P<.01) after training (fig 3).
      Figure thumbnail gr3
      Fig 3Variations of self-reported pain (A), balance, which was evaluated by the Berg Balance Scale (B), distance traveled in the 6-minute walk test (C), and gait speed (D) before and after the intervention period (Δ). *P<.05 for platform group vs control group. **P<.01 for platform group vs squat group. ***P<.001 for platform group vs control group.
      With respect to the baseline values of the 3 groups, the statistical analysis (Kruskal-Wallis test with Dunn's post hoc test) did not show any significant differences for all the variables (table 3).
      Table 4 gives the post hoc test (Δ values) results from the performance evaluation and the plasma concentrations of sTNFR1 and sTNFR2.
      Table 4Post Hoc Test (Δ Values) From the Performance Evaluation and Plasma Concentrations of sTNFR1 and sTNFR2
      VariablesDunn's Multiple Comparison TestP
      sTNFR1 (pg/mL)Control vs squat>.05
      Control vs platform<.01
      Squat vs platform>.05
      sTNFR2 (pg/mL)Control vs squat>.05
      Control vs platform<.01
      Squat vs platform>.05
      Self-reported pain (score)Control vs squat>.05
      Control vs platform<.05
      Squat vs platform>.05
      Self-reported stiffness (score)Control vs squat>.05
      Control vs platform>.05
      Squat vs platform>.05
      Self-reported function (score)Control vs squat>.05
      Control vs platform>.05
      Squat vs platform>.05
      Berg Balance Scale (score)Control vs squat>.05
      Control vs platform<.05
      Squat vs platform>.05
      6-minute walk test (m)Control vs squat>.05
      Control vs platform<.05
      Squat vs platform>.05
      Gait speed test (m/s)Control vs squat>.05
      Control vs platform<.001
      Squat vs platform<.01

      Discussion

      The results of this study showed that the addition of vibration to squat exercise training improved gait performance and static and dynamic balance and decreased biomarkers and self-perception of pain in elderly patients with knee OA.
      The addition of whole-body vibration to squat exercise training generates vertical sinusoidal vibrations that stimulate the primary endings of the muscle spindles, activating α-motor neurons that result in muscle contractions that are comparable to the tonic vibration reflex.
      • Trans T.
      • Aaboe J.
      • Henriksen M.
      • Christensen R.
      • Bliddal H.
      • Lund H.
      Effect of whole body vibration exercise on muscle strength and proprioception in females with knee osteoarthritis.
      As a result, the vibration stimulus strengthens the lower limbs
      • Verschueren S.M.
      • Roelants M.
      • Delecluse C.
      • Swinnen S.
      • Vanderschueren D.
      • Boonen S.
      Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study.
      • Roelants M.
      • Delecluse C.
      • Verschueren S.M.
      Whole-body-vibration training increases knee-extension strength and speed of movement in older women.
      and improves proprioception
      • Verschueren S.M.
      • Roelants M.
      • Delecluse C.
      • Swinnen S.
      • Vanderschueren D.
      • Boonen S.
      Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study.
      in elderly patients with knee OA by inducing isometric, concentric, and eccentric contractions of the hip and knee extensor muscle groups and the plantar flexors, thereby improving the control and execution of functional movements such as those required for static and dynamic balance and gait performance. As a consequence, whole-body vibration may be useful to stabilize and/or minimize the symptoms and consequences of knee OA in elderly patients by reducing the inflammatory joint process and the self-perception of pain.
      The present study observed that the addition of whole-body vibration to squat exercise training improved the gait performance of the subjects, as evaluated by the gait speed and the distance walked. Although no studies have investigated the distance walked in elderly individuals with OA after whole-body vibration training, improvements in gait speed have been observed in elderly individuals after a training program on a vibratory platform.
      • Kawanabe K.
      • Kawashima A.
      • Sashimoto I.
      • Takeda T.
      • Sato Y.
      • Iwamoto J.
      Effect of whole-body vibration exercise and muscle strengthening, balance, and walking exercises on walking ability in the elderly.
      Moreover, several researchers
      • Abreu S.S.E.
      • Caldas C.P.
      Gait speed, balance and age: a correlational study among elderly women with and without participation in a therapeutic exercise program.
      • Montero-Odasso M.
      • Schapira M.
      • Soriano E.R.
      • et al.
      Gait velocity as a single predictor of adverse events in healthy seniors aged 75 years and older.
      have suggested that balance improvements can positively influence gait speed in the elderly. Indeed, deteriorations in balance lead to an increased risk for falls,
      • Avdic D.
      • Pecar D.
      Significance of specificity of Tinetti B-POMA test and fall risk factor in third age of life.
      • Madureira M.M.
      • Takayama L.
      • Gallinaro A.L.
      • Caparbo V.F.
      • Costa R.A.
      • Pereira R.M.
      Balance training program is highly effective in improving functional status and reducing the risk of falls in elderly women with osteoporosis: a randomized controlled trial.
      and elderly individuals compensate for their lack of balance by increasing the double-support phase of their gait, which decreases gait speed.
      • Mbourou G.A.
      • Lajoie Y.
      • Teasdale N.
      Step length variability at gait initiation in elderly fallers and non-fallers, and young adults.
      As far as we know, there is no study that had evaluated the effect of vibration training on balance in elderly individuals with knee OA. However, Bautmans et al
      • Bautmans I.
      • Van Hees E.
      • Lemper J.C.
      • Mets T.
      The feasibility of Whole Body Vibration in institutionalised elderly persons and its influence on muscle performance, balance and mobility: a randomised controlled trial [ISRCTN62535013].
      used a randomized controlled trial to investigate the viability and impact of using whole-body vibration in institutionalized elderly individuals and observed a significant improvement in the balance of the group that trained on the vibratory platform compared with the placebo group.
      A decrease in self-reported pain (WOMAC) was observed in the platform group compared with the control group, which is a finding that is consistent with the literature. Indeed, studies have shown a decrease in self-reported pain immediately after a training period.
      • van Baar M.E.
      • Dekker J.
      • Oostendorp R.A.
      • Bijl D.
      • Voorn T.B.
      • Bijlsma J.W.
      Effectiveness of exercise in patients with osteoarthritis of hip or knee: nine months' follow up.
      • Murphy S.L.
      • Strasburg D.M.
      • Lyden A.K.
      • et al.
      Effects of activity strategy training on pain and physical activity in older adults with knee or hip osteoarthritis: a pilot study.
      • Liu C.J.
      • Latham N.K.
      Progressive resistance strength training for improving physical function in older adults.
      To our knowledge, this study was the first randomized study that investigated the effects of adding whole-body vibration to squat exercise training on the plasma concentrations of inflammatory markers in elderly individuals with knee OA. Compared with the control group, the plasma concentrations of the soluble receptors of TNF-α (sTNFRs) in the platform group were reduced, which coincided with improvements in static and dynamic balance, gait performance, and self-reported pain.
      TNF-α is a potent cytokine that is predominantly proinflammatory and catabolic. Interestingly, TNF-α, which is primarily produced by stimulated phagocytes,
      • Aderka D.
      • Engelmann H.
      • Maor Y.
      • Brakebusch C.
      • Wallach D.
      Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors.
      is involved in the initiation and progression of OA.
      • Goekoop R.J.
      • Kloppenburg M.
      • Kroon H.M.
      • et al.
      Low innate production of interleukin-1beta and interleukin-6 is associated with the absence of osteoarthritis in old age.
      • Goldring S.R.
      • Goldring M.B.
      The role of cytokines in cartilage matrix degeneration in osteoarthritis.
      The intracellular signals for the response to TNF-α are mediated by 2 distinct species of cell surface receptors (ie, cell surface TNF-α receptors 1 [TNFR1] and 2 [TNFR2]), which bind TNF-α with high affinity. TNFR1 is expressed by most cell types, whereas TNFR2 is primarily expressed by hematopoietic cells and endothelial cells.
      • Waetzig G.H.
      • Rosenstiel P.
      • Arlt A.
      • et al.
      Soluble tumor necrosis factor (TNF) receptor-1 induces apoptosis via reverse TNF signaling and autocrine transforming growth factor-beta1.
      Both TNF-α receptors also exist in soluble forms (ie, sTNFR1 and sTNFR2). Interestingly, the cleavage of tumor necrosis factor receptors on the cell surface by TNF-α–converting enzyme results in appreciable serum levels of sTNFR1 and sTNFR2. These sTNFRs may compete with cell surface receptors and block TNF-α activity.
      • Waetzig G.H.
      • Rosenstiel P.
      • Arlt A.
      • et al.
      Soluble tumor necrosis factor (TNF) receptor-1 induces apoptosis via reverse TNF signaling and autocrine transforming growth factor-beta1.
      • Gokhale R.
      • Chandrashekara S.
      • Vasanthakumar K.C.
      Cytokine response to strenuous exercise in athletes and non-athletes—an adaptive response.
      Because the sTNFRs can compete with the cell-associated tumor necrosis factor receptors for TNF-α, they have been suggested to function as inhibitors of TNF-α activity. It is important to emphasize that TNF-α is a proinflammatory cytokine that is very sensitive to subtle changes in endogenous glucocorticoid levels, such as circadian-mediated variations, and it has a rather short half-life. According to Kaneyama
      • Kaneyama K.
      • Segami N.
      • Yoshimura H.
      • Honjo M.
      • Demura N.
      Increased levels of soluble cytokine receptors in the synovial fluid of temporomandibular joint disorders in relation to joint effusion on magnetic resonance images.
      and Cope
      • Cope A.P.
      • Aderka D.
      • Doherty M.
      • et al.
      Increased levels of soluble tumor necrosis factor receptors in the sera and synovial fluid of patients with rheumatic diseases.
      and colleagues, the expression of sTNFR1 and sTNFR2 reflects changes in the catabolic activity of TNF-α toward the cartilage matrix. Moreover, there is scientific evidence that the stimuli that increase cytokine concentrations may also induce increases in the production of soluble receptors, some of which decrease cytokine activity.
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      Because soluble receptors are generally more stable in the circulation than are cytokines,
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      they could potentially be more reliable markers of chronic inflammation. Given this possibility, it was hypothesized that the significant reduction in plasma concentrations of both sTNFR1 and sTNFR2 in the platform group compared with the control group could reflect a reduction in the inflammatory joint process of the knee.
      Penninx
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      investigated the association between the serum concentrations of soluble markers (interleukin [IL]-6, C-reactive protein, TNF-α), and soluble receptors (soluble receptors of IL-6 and IL-2, sTNFR1, sTNFR2) and the functional performance and disease severity in elderly, obese individuals with knee OA. The results of the Penninx
      • Penninx B.W.
      • Abbas H.
      • Ambrosius W.
      • et al.
      Inflammatory markers and physical function among older adults with knee osteoarthritis.
      study showed that particularly high levels of sTNFR1 and sTNFR2 were associated with a decrease in physical function, an increase in OA symptoms, and worse radiographic scores of the knee.
      There were no significant differences between the squat and the control groups, even in the plasma concentrations of sTNFR1 and sTNFR2. It is believed that the subjects' own body mass overload during the training with squat exercises was not sufficient to promote improvements in the physical-functional evaluation tests used in the present study, or changes in the plasma concentrations of sTNFR1 and sTNFR2 or the self-perception of pain. Interestingly, compared with the controls, the association of the squat with whole-body vibration stimulation was sufficient to induce significant alterations, which suggests that the whole-body vibration stimulus provided an additional overload to the squat exercise. Moreover, a comparison of the 3 groups showed a trend toward improvement for the platform group compared with the squat group in all of the analyzed variables. This finding was confirmed by the significant differences that were observed between the squat and platform groups in the gait speed test.

      Study Limitations

      The addition of whole-body vibration to squat exercise training was designed to strengthen the lower limbs
      • Roelants M.
      • Delecluse C.
      • Verschueren S.M.
      Whole-body-vibration training increases knee-extension strength and speed of movement in older women.
      in elderly patients with OA by inducing isometric, concentric, and eccentric contractions of the hip and knee extensor muscle groups and the plantar flexors. One limitation of the present results is that they cannot be extrapolated to other physical activity modalities. Other studies are necessary to evaluate the alterations in sTNFRs in other exercise modalities.

      Conclusions

      The addition of vibration training to squat exercise training improves static and dynamic balance and gait performance. Also, the addition of vibration training reduces the self-perception of pain and inflammatory markers in elderly patients with knee OA.
      • a
        FitVibe; GymnaUniphy NV, Pasweg 6a, 3740 Bilzen, Belgium.
      • b
        Mega Accelerometer, ZPP1-3D-BC The Acceleration Measuring Kit; Mega Electronics Ltd, PO Box 1199 (Microkatu 1) FI-70211, Kuopio, Finland.
      • c
        Stone Fitness Equipment, PO Box 494, Huntertown, IN 46748-0494.
      • d
        Polar F4 Heart Rate Monitor Watch; Polar Electro Oy, Professorintie 5, FIN-90440 Kempele, Finland.
      • e
        ELISA Kit; R&D Systems, Inc, 614 McKinley Place NE, Minneapolis, MN 55413.
      • f
        Prism 4.0; GraphPad Software, Inc, 2236 Avenida de la Playa, La Jolla, CA 92037.

      Acknowledgments

      We thank the Santa Casa of Diamantina, Minas Gerais, Brazil.

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