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http://ajs.sagepub.com/ Medicine The American Journal of Sports http://ajs.sagepub.com/content/44/3/609 The online version of this article can be found at: DOI: 10.1177/0363546515620583 2016 44: 609 originally published online January 21, 2016Am J Sports Med Troy N. Trumble, Jonathan J. Shuster, Flavia M. Cicuttini and Christiaan Leeuwenburgh Terese L. Chmielewski, Steven Z. George, Susan M. Tillman, Michael W. Moser, Trevor A. Lentz, Peter A. Indelicato, Ligament Reconstruction Low- Versus High-Intensity Plyometric Exercise During Rehabilitation After Anterior Cruciate Published by: http://www.sagepublications.com On behalf of: American Orthopaedic Society for Sports Medicine can be found at:The American Journal of Sports MedicineAdditional services and information for http://ajs.sagepub.com/cgi/alertsEmail Alerts: http://ajs.sagepub.com/subscriptionsSubscriptions: http://www.sagepub.com/journalsReprints.navReprints: http://www.sagepub.com/journalsPermissions.navPermissions: What is This? - Jan 21, 2016OnlineFirst Version of Record - Feb 29, 2016Version of Record >> at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from Low- Versus High-Intensity Plyometric Exercise During Rehabilitation After Anterior Cruciate Ligament Reconstruction Terese L. Chmielewski,*yz PT, PhD, Steven Z. George,y PT, PhD, Susan M. Tillman,§ PT, Michael W. Moser,|| MD, Trevor A. Lentz,§ PT, Peter A. Indelicato,|| MD, Troy N. Trumble,{ DVM, PhD, Jonathan J. Shuster,# PhD, Flavia M. Cicuttini,** PhD, and Christiaan Leeuwenburgh,yy PhD Investigation performed at the University of Florida, Gainesville, Florida, USA Background: Plyometric exercise is used during rehabilitation after anterior cruciate ligament (ACL) reconstruction to facilitate the return to sports participation. However, clinical outcomes have not been examined, and high loads on the lower extremity could be detrimental to knee articular cartilage. Purpose: To compare the immediate effect of low- and high-intensity plyometric exercise during rehabilitation after ACL recon- struction on knee function, articular cartilage metabolism, and other clinically relevant measures. Study Design: Randomized controlled trial; Level of evidence, 2. Methods: Twenty-four patients who underwent unilateral ACL reconstruction (mean, 14.3 weeks after surgery; range, 12.1-17.7 weeks) were assigned to 8 weeks (16 visits) of low- or high-intensity plyometric exercise consisting of running, jumping, and agility activities. Groups were distinguished by the expected magnitude of vertical ground-reaction forces. Testing was conducted before and after the intervention. Primary outcomes were self-reported knee function (International Knee Documentation Commit- tee [IKDC] subjective knee form) and a biomarker of articular cartilage degradation (urine concentrations of crosslinked C-telopeptide fragments of type II collagen [uCTX-II]). Secondary outcomes included additional biomarkers of articular cartilage metabolism (urinary concentrations of the neoepitope of type II collagen cleavage at the C-terminal three-quarter–length fragment [uC2C], serum concentrations of the C-terminal propeptide of newly formed type II collagen [sCPII]) and inflammation (tumor necrosis factor–a), functional performance (maximal vertical jump and single-legged hop), knee impairments (anterior knee laxity, average knee pain intensity, normalized quadriceps strength, quadriceps symmetry index), and psychosocial status (kinesiopho- bia, knee activity self-efficacy, pain catastrophizing). The change in each measure was compared between groups. Values before and after the intervention were compared with the groups combined. Results: The groups did not significantly differ in the change of any primary or secondary outcome measure. Of interest, sCPII concentrations tended to change in opposite directions (mean 6 SD: low-intensity group, 28.7 6 185.5 ng/mL; high-intensity group, –200.66 255.0 ng/mL; P = .097; Cohen d = 1.03). Across groups, significant changes after the intervention were increased the IKDC score, vertical jump height, normalized quadriceps strength, quadriceps symmetry index, and knee activity self-efficacy and decreased average knee pain intensity. Conclusion: No significant differences were detected between the low- and high-intensity plyometric exercise groups. Across both groups, plyometric exercise induced positive changes in knee function, knee impairments, and psychosocial status that would support the return to sports participation after ACL reconstruction. The effect of plyometric exercise intensity on articular cartilage requires further evaluation. Registration Number: Clinicaltrials.gov NCT01851655 Keywords: ACL; knee; articular cartilage; loading; psychosocial; outcomes An anterior cruciate ligament (ACL) rupture is a common injury in sports that involve cutting, jumping, or pivot- ing.18 Most people with an ACL injury require ACL recon- struction surgery to regain the knee stability necessary for resuming sports participation.24 ACL reconstruction is then followed by several months of supervised rehabilita- tion.1,60 Despite surgical advances and extensive rehabili- tation, recent literature has revealed less than optimal short- and long-term outcomes after ACL reconstruction. For example, up to two-thirds of those who undergo ACL reconstruction do not return to preinjury sport activities.3 Additionally, by 10 years after surgery, up to 80% of the ACL reconstruction population show radiographic signs The American Journal of Sports Medicine, Vol. 44, No. 3 DOI: 10.1177/0363546515620583 � 2016 The Author(s) 609 at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from of posttraumatic knee osteoarthritis (OA),40,48 which can lead to pain and limited ability to perform weightbearing activi- ties. Rehabilitation interventions that facilitate a return to sports participation and/or reduce the risk of posttraumatic knee OA after ACL reconstruction are highly desirable. Rehabilitation after ACL reconstruction is broadly divided into early and late phases. The early phase focuses on resolv- ing knee impairments (eg, pain, effusion, range of motion def- icit, quadriceps muscle weakness, and antalgic gait), and the late phase focuses on preparing the patient to return to sport activities.1,60 Running, jumping, and agility drills are typical interventions in the late phase of rehabilitation after ACL reconstruction.1,60 These interventions involve lower extrem- ity landing, followed by propulsion, which invokes the stretch-shortening cycle in extensor muscles (eg, quadriceps). The stretch-shortening cycle is an identifying feature of plyo- metric exercise.6 Therefore, running, jumping, and agility drills are all forms of plyometric exercise. In uninjured peo- ple, lower extremity plyometric exercise improves motor recruitment,5 increases muscle strength,5,47 and enhances sports-related performance.5,6,22,43 Plyometric exercise might assist the return to sports participation after ACL recon- struction by improving quadriceps muscle strength and knee function, but the intervention has not been examined in this population.1 Plyometric exercise produces vertical ground-reaction forces that range from 2 to over 6 times the body weight.12,29,57 The magnitude of vertical ground-reaction force indicates the intensity of plyometric exercise.13,28 Higher intensity plyometric exercise includes activities per- formed on a single leg, with greater effort, or from a higher box height.12,28,29,57 Posttraumatic knee OA is characterized by the loss of articular cartilage, which results when the metabolism of articular cartilagematrix molecules (eg, type II collagen) is imbalanced such that degradation outpaces synthesis.17 Excessive loads on articular cartilage increase degradation,51 but it is unclear how this translates to loads applied during rehabilitation after ACL reconstruction. It is of interest to know if plyometric exercise, especially high- intensity plyometric exercise, has negative effects on articu- lar cartilage after ACL reconstruction. Articular cartilage status may be monitored through biomarkers of articular cartilage metabolism in blood, urine, or synovial fluid.11 A widely studied articular carti- lage degradation biomarker is crosslinked C-telopeptide fragments of type II collagen in urine (uCTX-II).27 uCTX- II concentrations are elevated in patients with knee OA, those with focal articular cartilage lesions, and those who have undergone ACL reconstruction.7,8,46 Chronically high uCTX-II concentrations or increases over about a year are associated with the progression of knee OA on radio- graphs.45,49 While uCTX-II is generally considered an artic- ular cartilage biomarker, some studies suggest that concentrations also reflect changes at the bone-cartilage interface.37,56 Another biomarker of articular cartilage deg- radation is the neoepitope of type II collagen cleavage at the C-terminal three-quarter–length fragment in urine (uC2C). uC2C concentrations are elevated in patients with knee OA,8,19 and uC2C concentrations are elevated in synovial fluid after ACL injuries.31,61 Some research suggests that a ratio of articular cartilage degradation to synthesis (eg, serum concentrations of the C-terminal propeptide of newly formed type II collagen [sCPII]) better discriminates knee OA than individual biomarkers.8,55 The purpose of this study was to compare the immediate effects of low- and high-intensity plyometric exercise on knee function and articular cartilage metabolism in patients after ACL reconstruction. We hypothesized that self-reported knee function and articular cartilage degra- dation would increase based on the intensity of plyometric exercise. Because relatively little is known about plyomet- ric exercise during rehabilitation after ACL reconstruction, other clinically relevant measures were included as sec- ondary outcomes. METHODS Study Design This was a double-blind (participant and tester), random- ized controlled clinical trial comparing low- and high- intensity plyometric exercise during rehabilitation after ACL reconstruction. Testing was conducted before ran- domization and within 1 week after the intervention at the University of Florida and UF Health Rehab Center at the Orthopaedic and Sports Medicine Institute. Interven- tions were conducted at the UF Health Rehab Center at the Orthopaedic and Sports Medicine Institute. Setting and Participants Patients who underwent ACL reconstruction were recruited from the clinical practices of 2 board-certified orthopaedic *Address correspondence to Terese L. Chmielewski, PT, PhD, TRIA Orthopaedic Center, UF Health Orthopaedic and Sports Medicine Institute, 8100 Northland Drive, Bloomington, MN 55431, USA (email: terese.chmielewski@tria.com). yDepartment of Physical Therapy, University of Florida, Gainesville, Florida, USA. zTRIA Orthopaedic Center, Bloomington, Minnesota, USA. §UF Health Rehab Center at the Orthopaedics and Sports Medicine Institute, Gainesville, Florida, USA. ||Department of Orthopaedics & Rehabilitation, University of Florida, Gainesville, Florida, USA. {Veterinary Population Medicine, University of Minnesota, Minneapolis, Minnesota, USA. #Department of Health Outcomes and Policy, University of Florida, Gainesville, Florida, USA. **School of Public Health and Preventive Medicine, Monash University, Melbourne, Australia. yyInstitute on Aging, University of Florida, Gainesville, Florida, USA. One or more of the authors has declared the following potential conflict of interest or source of funding: This study was funded by NFL Charities. T.L.C.’s time and effort were supported by a grant from the National Institutes of Health (K01-HD052713). Support for the study was also provided by the Claude D. Pepper Older Americans Independence Center (OAIC) Metabolism and Translational Science Core. The OAIC is funded by a grant from the National Insti- tutes of Health/National Institute on Aging (1P30AG028740). 610 Chmielewski et al The American Journal of Sports Medicine at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from surgeons (M.W.M. and P.A.I.) at the University of Florida. Eligible participants were between 15 and 30 years of age, had undergone ACL reconstruction surgery no more than 6 months after injury, participated at least 50 hours per year in level 1 or 2 activities before injury (ie, sports that include cutting, jumping, or pivoting),10 and met clinical requirements for initiating advanced rehabilitation (at least 12 weeks after surgery, full active knee extension, active knee flexion within 5� of the nonsurgical side, pain rating no greater than 2 of 10 during activities of daily living, and quadriceps index of �60%). Exclusion criteria included a bilateral knee injury, prior knee ligament injury and/or surgery, concomitant ligamentous injury .grade 1, menis- cal repair, cartilage repair procedure, surgical complications requiring rehabilitation modification, and renal disease. The inclusion and exclusion criteria were meant to create a population of active participants with an acute, unilateral, and relatively isolated ACL injury. Patients gave written consent or assent (minor participants) to participate in this study on a form approved by the University of Florida Institutional Review Board. Randomization and Interventions After preintervention testing, participants were random- ized to the low- or high-intensity plyometric exercise group. The randomization scheme was computer gener- ated, balanced to ensure equal allocation to each treatment group, and further stratified by sex. The randomization scheme was maintained by the study coordinator and com- municated to the treating physical therapist when a partic- ipant entered the study. The mean time from surgery to the start of the intervention was 14.3 weeks (range, 12.1- 17.7 weeks). Participants were asked to refrain from par- ticipating in plyometric exercise outside of the study. Study interventions were administered 2 times per week for 8 weeks (16 visits) by a physical therapist with board-cer- tified credentialing in sports physical therapy (S.M.T.) or sports physical therapy residency training (T.A.L.). A brief warm-up on a stationary bicycle was performed at the start of the treatment session. Plyometric exercise consisted of running, jumping, and agility activities, and groups were dis- tinguished by the expected magnitude of vertical ground- reaction forces (Appendixes 1 and 2, available online at http://ajsm.sagepub.com/supplemental). Compared with the low-intensity group, the high-intensity group increased per- ceived effort at a faster rate and performed higher intensity activities such as sprinting, jump landing from boxes, single- legged drop land, and single-legged line jump (Table 1). Exercise volume was matched between groups, and the intensity, volume, and neuromuscular demands were grad- ually increased to minimize delayed-onset muscle soreness and knee joint inflammation. Verbal and visual cues were given during exercise performance to ensure the proper technique. All participants performed a standardized pro- gram of lower extremity strengthening (leg presses, machine squats, and knee extensions; 3 sets 3 10 repeti- tions each), flexibility (standing gastrocnemius and quadri- ceps stretches and long-sitting hamstring stretches; 2 3 30 seconds each), and proprioception (standing on foam or a tilt board; 3 3 30 seconds each). The starting resistancefor the plyometric leg press and lower extremity strengthen- ing was considered moderate by participants’ self-report. Cryotherapy was used after treatment as needed for knee symptoms. Before each treatment, participants reported any thigh muscle soreness or knee pain, and knee girth was mea- sured with a standard tape measure. The treatment ses- sion was rescheduled if muscle or joint soreness did not resolve after a warm-up on a stationary bicycle or knee TABLE 1 Differences in Plyometric Exercise Between the Low- and High-Intensity Groups Exercises Performed by Both Groups: Variable Manipulated Running � 10-minute walk:jog (greater jog time in high-intensity group) � 10-minute jog, 10-minute jog:run (initiated earlier in high-intensity group) Jumping � Leg press jump (high-intensity group progressed faster to alternating legs and surgical leg only) � Wall jump (initiated earlier in high-intensity group) � 2-legged forward hop (high-intensity group progressed to more demanding jumps) � 2-legged line jump (high-intensity group progressed to more demanding jumps) � Squat jump (initiated earlier in high-intensity group) Agility � Side shuffle, shuttle run, carioca, 45� cut, 90� cut (low-intensity group progressed to 50% effort, and high-intensity group progressed to 75% effort) Exercises Performed Only in High-Intensity Group Running � Run:sprint Jumping � 2-legged drop land, single-legged drop land, drop vertical jump, cone jump, tuck jump, single-legged line jump AJSM Vol. 44, No. 3, 2016 Plyometric Exercise Intensity After ACL Reconstruction 611 at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from girth increased more than 3 cm from the previous session. Otherwise, the protocol was implemented, and resistance was increased by 10% in the lower extremity strengthening program as long as a good technique was demonstrated. Demographic Information Demographic information was collected at testing before the intervention and included age, sex, body mass index, mechanism of injury, preinjury Tegner Activity Scale52 score, time from injury to surgery, time from surgery to pretesting, graft type, and meniscectomy procedures. A Tegner score of �5 indicates participation in sports.52 Outcome Measures Primary Outcomes. Knee function was assessed with the 2000 International Knee Documentation Committee (IKDC) subjective knee form, which includes items related to knee symptoms and functional activities. Scores range from 0 to 100, and a higher score indicates better knee function. The IKDC has good test-retest reliability (intra- class correlation coefficient [ICC] = 0.94).25 Articular cartilage metabolism was determined from bio- markers in urine and blood. Fasting, early morning (within 2 hours of waking), second-void urine and blood samples were collected and stored at –20�C until analysis. Biomarker concentrations were analyzed in duplicate with commercially available enzyme-linked immunosorbent assay (ELISA) kits. The primary biomarker of interest was uCTX-II (Urine Car- tiLaps; Nordic Bioscience). Urine samples were diluted as needed (range, 1:1 to 1:90). Urinary concentrations of creati- nine (Cayman Chemical Co) were determined and used to correct uCTX-II values according to the following formula: [corrected concentration (ng/mmol) = 1000 3 uncorrected concentration (ng/L)/creatinine (mmol/L)]. Intra- and inter- assay coefficients of variation were \6% and \12%, respectively. Secondary Outcomes. Functional performance was assessed with maximal vertical jump and single-legged for- ward hop test. A knee brace was not worn during testing. Participants performed 3 practice trials, followed by 3 maximal-effort test trials. The average of the test trials was analyzed. For the maximal vertical jump test, reach dis- tance was recorded with the arms raised overhead (Vertec; Power Systems). Next, participants performed a squat coun- termovement, jumped vertically as high as possible, touched the measuring arm, and landed solidly on both feet. The ver- tical jump height was calculated as the jump distance minus the reach distance (cm). The single-legged forward hop test was only performed after the intervention because of safety concerns. Participants stood on the test limb and hopped for- ward maximally, and the distance was recorded (cm). The nonsurgical limb was tested first. The single-legged forward hop test index was computed with the following formula: (surgical side distance/nonsurgical side distance) 3 100. Knee impairments included anterior knee laxity, average knee pain intensity, and quadriceps strength. Anterior knee laxity was measured with a knee arthrometer (KT-1000 arthrometer; MEDmetric Corp) using a manual maximum pull.44 Laxity was recorded on both sides (mm), and the dif- ference between sides (surgical – nonsurgical) was calcu- lated. For average knee pain intensity, participants verbally rated their worst and least knee pain intensity in the past week as well as their current knee pain intensity on the 11-point Numeric Pain Rating Scale (NPRS; 0 = no pain, 10 = worst pain imaginable),58 and the 3 ratings were averaged. The NPRS has been shown to be a reliable and valid method of measuring pain.23,58 Knee extensor tor- que (quadriceps strength) was measured with an isokinetic dynamometer (Biodex System 3; Biodex Medical Systems) and a test speed of 60 deg/s. Participants were seated and stabilized with their hips in 90� of flexion, and the dyna- mometer moved through a range of 100� to 10� of knee flex- ion. Testing was performed on the nonsurgical side first, followed by the surgical side. Participants performed 5 prac- tice trials and 5 maximal-effort test trials. The peak knee extensor torque (N�m) was determined from the test trials. Quadriceps strength variables included normalized peak knee extensor torque (peak knee extensor torque/body mass [kg]) and the quadriceps index: (peak knee extensor torque on surgical side/peak knee extensor torque on non- surgical side) 3 100. A secondary biomarker of articular cartilage degradation was uC2C (IB-C2C-HUSA; IBEX Pharmaceuticals Inc). Urine samples were diluted as needed (range, 1:2 to 1:15). uC2C values were corrected for urinary concentrations of creatinine. sCPII (Procollagen II C-Propeptide; IBEX Pharmaceuticals Inc) concentrations were used to assess articular cartilage synthesis. Ratios of articular cartilage degradation to synthesis (uCTX-II/sCPII and uC2C/sCPII) were created. Intra- and interassay coeffi- cients of variation across biomarkers were\6% and\12%, respectively. An inflammation biomarker was analyzed because high loads on articular cartilage can cause joint inflammation that contributes to articular cartilage degradation.14 Blood samples were collected (see Primary Outcomes section), and serum concentrations of tumor necrosis factor–a (TNF-a) were analyzed with a high-sensitivity ELISA (R&D Systems). Psychosocial status can influence the return to sports participation.9,15 Kinesiophobia, or fear of movement/ reinjury, impedes a return to sports participation4 and was measured with the shortened version of the Tampa Scale for Kinesiophobia (TSK-11).59 Items are scored from 1 (strongly disagree) to 4 (strongly agree) and summed to create a total score ranging from 11 to 44. Higher scores indicate higher kinesiophobia. The TSK-11 has shown good test-retest reliability (ICCs = 0.8159 and 0.9316) in patients with low back pain. Self-efficacy, or confidence, related to the knee can facilitate a return to sports partici- pation4 and was measured with a 10-item Knee Activity Self-efficacy questionnaire (KASE) (Appendix 3, available online) developed by us after considering a published ques- tionnaire53 and our clinical experience. Items are scored from 0 (strongly disagree) to 10 (strongly agree) and summed to createa total score ranging from 0 to 100. Higher scores indicate greater self-efficacy in knee-related activities. The test-retest reliability of the KASE question- naire was analyzed in 53 patients who had undergone 612 Chmielewski et al The American Journal of Sports Medicine at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from ACL reconstruction (29 male patients) and who completed the questionnaire at 8 and 9 weeks after surgery. The ICC (model 2,1) was 0.852. Pain catastrophizing, or negative thoughts about pain, can contribute to chronic pain develop- ment32 that might impede a return to sports participation34 and was measured with the Pain Catastrophizing Scale (PCS).50 Items on the PCS are scored from 0 (not at all) to 4 (all the time) and summed to create a total score ranging from 0 to 52. Higher scores indicate higher pain catastroph- izing. The PCS has good test-retest reliability (ICC = 0.93) in patients with low back pain.16 Statistical Analysis Power calculations were based on detecting group differen- ces in the 2 primary outcome measures (IKDC score and uCTX-II concentrations) with a 2-sided test, a level of .05, and power of 0.80. Group differences in the IKDC score were set at the minimal clinically important difference of 11 points,25,26 and the standard deviation was conserva- tively estimated at 11 points. Data on uCTX-II concentra- tions in an ACL reconstruction population were not available at the time of study planning. Therefore, uCTX- II concentrations in uninjured participants who perform running or swimming exercise (different loading intensi- ties) were used.41 A sample size of 13 participants per group was deemed necessary to satisfy power calculations. Statistical analysis was performed with SPSS version 21.0 (IBM Corp) and SAS version 9.3 (SAS Institute Inc). uCTX-II and uC2C values were log transformed before analysis because of a nonnormal distribution. uCTX-II/sCPII and uC2C/sCPII ratios were computed with raw values, and the result was log transformed. Descriptive statistics were gener- ated for demographic variables and the primary and second- ary outcome measures. To examine group differences, a univariate general linear model was created for each pri- mary and secondary outcome measure. Group assignment was the independent variable, and the change in the outcome measure (value after the intervention – value before the inter- vention) was the dependent variable. Values before the inter- vention were included as covariates, and age was also an additional covariate in models with uCTX-II and uC2C because past research37 and the present study show that these measures are negatively associated with age. For the single-legged forward hop test index, the value after the intervention was compared between groups with an indepen- dent-samples t test. Effect sizes were calculated for all out- come measures with Cohen d. The effect of plyometric exercise was examined by combining groups and comparing values before and after the intervention with paired-samples t tests. An a level of .05 was used for qualifying significance. RESULTS Study enrollment is shown in Figure 1. A total of 25 partic- ipants were enrolled; however, 1 participant was withdrawn after preintervention testing because of a quadriceps index \60%. Thus, 24 patients participated (12 participants in each treatment group). Demographic information can be found in Table 2. A participant in the high-intensity group injured her surgical knee in an accident outside of the study. The postinjury physical examination indicated that the graft was intact (ie, firm endpoint), and magnetic resonance imaging showed no further injury to the knee structures. The patient could not participate in further treatment ses- sions because of knee pain and swelling, but testing after the intervention was performed was consistent with an intent-to-treat analysis. Treatment logs were reviewed for compliance with the 16 treatment sessions. In the high-intensity group, the participant who sustained a knee injury completed 9 treat- ment sessions; additionally, 1 participant completed 14 treatment sessions, and 2 participants completed 15 treat- ment sessions, all because of missed appointments that were not rescheduled. In the low-intensity group, 1 partic- ipant completed 10 treatment sessions because of missed appointments that were not rescheduled. Therefore, the number of treatment sessions completed according to pro- tocol was 182 of 192 (95%) in the high-intensity group and 186 of 192 (97%) in the low-intensity group. Data on the articular cartilage metabolism biomarker were not analyzable at the preintervention time point for 1 participant in the high-intensity group. The creatinine con- centration was more than 75 times lower than the next low- est value in the sample, and the sCPII concentration was 10 times lower than the next lowest value in the sample. Thus, articular cartilage metabolism biomarkers were analyzed for 11 participants in the high-intensity group. The serum con- centrations of TNF-a after the intervention were below the threshold of detection in 6 participants (low-intensity group: n = 4; high-intensity group: n = 2). For these participants, the value of 0.203 pg/mL was substituted, which is half of the minimum value in the remaining sample. High-intensity group (n = 12) • Received allocated intervention (n =12) Low-intensity group (n = 12) • Received allocated intervention (n = 12) Allocation Excluded (n =1) • Did not meet inclusion criteria Enrolled in study (N = 25) Randomized (n = 24) Follow-up Lost to follow-up (n = 0) Missed appointments (n = 1) Lost to follow-up (n = 0) Discontinued intervention due to injury (n = 1) Missed appointments (n = 3) AnalysisAnalyzed (n = 12) • • • Analyzed (n = 12) Figure 1. Flow diagram of study participants. AJSM Vol. 44, No. 3, 2016 Plyometric Exercise Intensity After ACL Reconstruction 613 at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from Group differences were not found in the change of any outcome measure (Tables 3 and 4). However, sCPII concen- trations seemed to change in opposite directions between groups, with a positive mean value in the low-intensity group and a negative mean value in the high-intensity group (P = .097) (Table 4). Effect sizes were below 0.50 for all outcome measures, except for an effect size of 1.03 for sCPII concentrations (Table 4). Several clinical measures significantly changed in both groups after the intervention (Table 3). Measures that increased were the IKDC score (P \ .001), vertical jump height (P = .001), normalized knee extensor torque (P = .018), quadriceps index (P = .004), and KASE score (P \ .001); and the mean NPRS score decreased (P\ .001). DISCUSSION This study examined the effect of plyometric exercise inten- sity on knee function, articular cartilage metabolism, and other clinically relevant measures in patients who had undergone ACL reconstruction. We hypothesized that knee function and articular cartilage degradation would increase based on plyometric exercise intensity, but differences were not found between the low- and high-intensity groups. Signif- icant changes after the intervention were increased self- reported knee function, vertical jump height, normalized quadriceps strength, quadriceps symmetry index, and knee activity self-efficacy; and decreased average knee pain inten- sity. Thus, plyometric exercise had positive effects on knee function, knee impairments, and psychosocial status in patients who had undergone ACL reconstruction, regardless of intensity. Group differences were not found in the primary and sec- ondary outcomes possibly because of overlap in intensity between groups. Many plyometric activities form a common progressionduring rehabilitation after ACL reconstruction and were included in both groups. For these activities, perceived effort was increased more quickly in the high- TABLE 2 Demographic Information for Low- and High-Intensity Plyometric Exercise Groups Low-Intensity Group (n = 12) High-Intensity Group (n = 12) Male sex, n 7 8 Age, mean 6 SD, y 20.7 6 4.9 19.3 6 3.8 Body mass index, mean 6 SD, kg/m2 24.2 6 3.2 24.5 6 2.2 Mechanism of injury, n Contact 2 4 Noncontact 10 8 Time from injury to surgery, mean 6 SD (range), wk 5.8 6 3.9 (2-14) 11.7 6 9.5 (3-36) Time from surgery to preintervention testing, mean 6 SD (range), wk 14.6 6 1.6 (12-17) 14.0 6 0.9 (12-15) Preinjury Tegner activity rating, mean 6 SD 7.7 6 0.8 7.8 6 1.3 Graft type, n Allograft 5 3 Autograft 7 9 Meniscectomy, n None 4 11 Medial 3 0 Lateral 3 1 Medial and lateral 2 0 TABLE 3 Clinical Outcomes for Low- and High-Intensity Plyometric Exercise Groupsa Low-Intensity Group High-Intensity Group Before Intervention After Intervention Change Before Intervention After Intervention Change P Value Effect Size IKDC scoreb 70.0 6 13.1 82.1 6 12.9 12.1 6 7.5 72.2 6 10.9 87.7 6 8.4 15.5 6 6.8 .147 0.47 Single-legged hop test index, % — 88.7 6 9.1 — — 92.2 6 5.2 — .257 0.47 NPRS scoreb 1.0 6 0.9 0.6 6 0.6 –0.4 6 0.5 1.0 6 1.1 0.5 6 0.7 –0.5 6 0.6 .639 0.18 Knee laxity difference, mm 3.4 6 1.5 3.0 6 0.9 –0.4 6 1.0 2.0 6 0.9 1.9 6 0.9 –0.1 6 0.6 .219 0.09 Knee extensor torque,b N�m/kg 2.3 6 0.5 3.0 6 0.7 0.7 6 0.5 2.2 6 0.5 2.8 6 0.5 0.6 6 0.5 .751 0.20 Quadriceps index,b % 79.7 6 14.4 87.1 6 14.3 7.4 6 14.0 82.4 6 17.2 92.7 6 9.4 10.3 6 13.9 .311 0.21 TSK-11 score 17.8 6 6.9 17.6 6 5.2 –0.2 6 3.8 17.3 6 3.9 17.4 6 4.5 0.1 6 4.1 .964 0.08 KASE scoreb 67.2 6 23.5 87.9 6 15.1 20.7 6 20.1 80.3 6 12.2 93.3 6 6.1 13.0 6 10.0 .801 0.49 PCS score 3.7 6 4.5 2.5 6 4.2 –1.2 6 2.8 3.2 6 5.1 2.8 6 4.8 –0.4 6 2.0 .297 0.33 aData are reported as mean 6 SD. Group differences were not found in the magnitude of change from before intervention to after intervention. IKDC, Inter- national Knee Documentation Committee; KASE, Knee Activity Self-efficacy questionnaire; NPRS, Numeric Pain Rating Scale; PCS, Pain Catastrophizing Scale; TSK-11, shortened version of Tampa Scale for Kinesiophobia. bSignificant difference between scores before the intervention and after the intervention with the groups combined (P\ .05). 614 Chmielewski et al The American Journal of Sports Medicine at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from intensity group, but perception of effort was not measured. Also, individual movement patterns can affect the magni- tude of vertical ground-reaction force (eg, greater hip and knee flexion are associated with lower vertical ground- reaction force).20,35 Finally, high-intensity activities that were unique to the high-intensity group did not start until later in the protocol (eg, box jumps in week 3 or single- legged jumps in week 6) to allow time to progressively increase loads on the knee. Published ACL reconstruction protocols have not specified plyometric exercise prescrip- tion,1,21,38,62 so this study can inform protocol development for future research. Caution should be taken when general- izing the results of this study to other protocols that are sub- stantially lower or higher in intensity. Despite the possible overlap in plyometric exercise inten- sity between groups, it was of interest that sCPII concentra- tions changed in opposite directions (increase in low- intensity group and decrease in high-intensity group), which might be attributed to subtle differences in loading. Basic science research indicates that articular cartilage syn- thesis increases with moderate loading and shifts toward degradation with excessive loading.51 However, sCPII con- centrations were elevated in the high-intensity group com- pared with the low-intensity group at the preintervention time point; therefore, differences in the change in sCPII con- centrations could reflect a regression toward the mean in the high-intensity group. Exploratory post hoc analyses did not show that meniscectomy status or time from injury to surgery explained differences in sCPII concentrations. Subchondral bone injuries were not measured in this study but have the potential to influence articular cartilage sta- tus.30 Protecting knee joint health after ACL reconstruction is important but often overlooked in rehabilitation because of insufficient evidence to guide clinical decision making. Further research is warranted to better understand the effect of loading intensity on articular cartilage in patients who have undergone ACL reconstruction. Several measures changed favorably from before the intervention to after the intervention across groups. The IKDC score improved more than the minimal clinically important difference,26 and the value after the interven- tion approximated that of patients who return to sports at 1 year after surgery.33 Vertical jump height and quadri- ceps strength increased, mirroring the positive effects of plyometric exercise in uninjured participants.42 Moreover, mean single-legged hop test index and quadriceps index after intervention were 90%, which is a benchmark often used for clearance to return to sports.54 KASE scores increased, and while there is no previous research with which to compare, increased confidence bodes well for a return to sports participation.2 Finally, average knee pain intensity decreased after the intervention. Overall, changes after plyometric exercise would facilitate a return to sports participation after ACL reconstruction. Interestingly, the mean TSK-11 score, which indicates kinesiophobia or fear of reinjury, did not change after the intervention. A closer inspection of the data showed that TSK-11 scores after the intervention increased in about one-third of the sample, which agrees with reports of increased kinesiophobia at the time of return to sports after an injury.4,36 Plyometric exercise would seem appropriate to decrease kinesiophobia because it exposes patients to sports-related activities in a controlled setting,1 and graded exposure treatment is effective in patients with low back pain.39 However, graded exposure treatment focuses on activ- ities that cause fear, and plyometric activities in this study were selected to gradually increase loads on the lower extremity. The strengths of this study include a randomized con- trolled study design, a focus on a common rehabilitation intervention for which little is known,1 and a comprehensive testing protocol. The potential overlap in plyometric exer- cise intensity between groups is a study limitation that could be addressed by extending the protocol duration as tolerance to high-impact activity increases over time. It is unknown if plyometric exercise intensity has a differential effect in the long term because the study only had a short- term follow-up (immediately after the intervention). A short-term follow-up was appropriate for this study because exercise intensity and frequency would vary across patients after the return to sports. The study included a standardized program of strengthening, stretching, and proprioception exercises and did not have a control group (no plyometric exercise) for comparison. Therefore, the standardized TABLE 4 Biomarker Outcomes for Low- and High-Intensity Plyometric Exercise Groupsa Low-Intensity Group High-Intensity Group Before Intervention After Intervention Change Before Intervention After Intervention Change P Value Effect Size uCTX-II (log), ng/mmol 3.34 6 0.47 3.29 6 0.54 –0.05 6 0.13 3.45 6 0.48 3.36 6 0.46 –0.09 6 0.20 .856 0.24 uC2C (log), ng/mmol 2.62 6 0.29 2.65 6 0.44 0.03 6 0.43 2.78 6 0.44 2.72 6 0.45 –0.06 6 0.22 .694 0.26 sCPII, ng/mL 764.3 6 226.3 793.1 6 317.6 28.86 185.5 1007.2 6 317.4 806.6 6 279.0 –200.6 6 255.0 .097 1.03 Log uCTX-II/sCPII 0.48 6 0.45 0.42 6 0.52 –0.06 6 0.18 0.43 6 0.50 0.47 6 0.50 0.04 6 0.19 .237 0.49 Log uC2C/sCPII –0.25 6 0.29 –0.22 6 0.42 0.03 6 0.45 –0.20 6 0.42 –0.16 6 0.46 0.04 6 0.21 .859 0.03 TNF-a, pg/mL 2.3 6 3.2 1.7 6 3.9 –0.6 6 2.0 1.8 6 1.5 1.5 6 1.5 –0.3 6 1.6 .731 0.17 aData are reported as mean 6 SD. After accounting for baseline values, the magnitude of change in the biomarkers was not significantly different between groups. However, the effect size for change in sCPII was high. sCPII, serum concentrations of the C-terminal propeptide of newly formed type II collagen (a biomarker of articular cartilage synthesis); TNF-a, tumor necrosis factor–a (a biomarker of inflammation); uC2C, urine concentrations of the neoepitope of type II collagen cleavage at the C-terminal three-quarter–length fragment (a biomarker of articular cartilage degradation); uCTX-II, urine concentrations of crosslinked C-telopeptide fragments of type II collagen (a biomarker of articular cartilage degradation). AJSM Vol. 44, No. 3, 2016 Plyometric Exercise Intensity After ACL Reconstruction 615 at UNIV FEDERAL DA BAHIA on April 29, 2016ajs.sagepub.comDownloaded from program contributed to changes after the intervention, and it cannot be determined if the same outcomes would be achieved without plyometric exercise. The study had a mod- est sample of 12 participants per group. The sample size was estimated at 13 participants per group but was based on biomarker data reported for uninjured participants. We are cautious to interpret that plyometric exercise did not influence articular cartilage metabolism. Future research can be strengthened by a larger sample size and potentially using articular cartilage measures that are local to the knee. Preoperative differences were found between groups including the time from injury to surgery and the preva- lence of meniscectomy procedures, which may have con- founded the outcomes. Finally, participants in this study had an isolated, acute, and unilateral ACL injury, and reconstruction was performed with allograft or autograft tissue. Different results might be obtained with a multiple ligament injury, a chronic injury, revision ACL reconstruc- tion, or a sample with a homogeneous graft type. In summary, regardless of intensity, 8 weeks of plyo- metric exercise implemented during rehabilitation after ACL reconstruction had positive effects on knee function, knee impairments, and psychosocial status. These improvements should facilitate a return to sports partici- pation and possibly increase rates of return to sports after ACL reconstruction. Further research is needed to deter- mine if high-intensity plyometric exercise has negative effects on articular cartilage so that long-term knee joint health is not sacrificed for short-term functional gain. 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