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Laboratory- and Clinician-Oriented Measures of Sensory Organization Strategies in Those With and Without Chronic Ankle Instability

2020; Volume: 12; Issue: 6 Linguagem: Inglês

10.3928/19425864-20200821-01

1942-5872

Kyeongtak Song, Erik A. Wikstrom,

Tendon Structure and Treatment

Original Research freeLaboratory- and Clinician-Oriented Measures of Sensory Organization Strategies in Those With and Without Chronic Ankle Instability Kyeongtak Song, PhD, ATC, CSCS, , and , PhD, ATC, CSCS Erik A. Wikstrom, PhD, ATC, , PhD, ATC Kyeongtak Song, PhD, ATC, CSCS and Erik A. Wikstrom, PhD, ATC Published Online:August 21, 2020https://doi.org/10.3928/19425864-20200821-01PDFAbstract ToolsAdd to favoritesDownload CitationsTrack CitationsCopy LTI LinkHTMLAbstractPDF ShareShare onFacebookTwitterLinkedInRedditEmail SectionsMoreAbstractPurpose:To quantify laboratory- and clinician-oriented measures of sensory organization strategies in those with chronic ankle instability (CAI) relative to controls.Methods:Fifteen individuals with CAI and 15 uninjured controls volunteered. All participants completed the sensory organization test (SOT) in a double- and single-limb stance and a single-limb assessment of the Clinical Test of Sensory Integration in Balance (CTSIB).Results:For double-limb SOT, the CAI group had significantly lower scores under conditions 1, 2, and 5 and lower composite, somatosensory, and vestibular scores (P ≤ .042). For single-limb SOT, the CAI group had significantly lower scores under conditions 1, 2, and 3, and lower composite and somatosensory scores (P ≤ .039). For the CTSIB, the CAI group showed significantly lower time in balance under conditions 2 and 6 and lower composite and somatosensory scores (P ≤ .012).Conclusions:Laboratory- and clinician-oriented assessments tools detect impaired balance and altered sensory organization strategies in CAI participants.[Athletic Training & Sports Health Care. 2020;12(6):257–264.]IntroductionA lateral ankle sprain is one of the most common injuries in all sports,1 accounting for approximately 15% of all reported injuries in collegiate athletics.2 Following a lateral ankle sprain, 30% to 74% of patients report long-term residual symptoms including pain, swelling, weakness, feelings of instability, and health-related quality of life deficits.3–7 In addition to residual symptoms, reinjury often occurs and has been reported in as many as 73% of individuals who initially sustain a lateral ankle sprain.6 Recurrent ankle injury and the presence of residual symptoms are key characteristics of chronic ankle instability (CAI),8 a condition that has been linked to post-traumatic osteoarthritis of the ankle,9,10 and decrease the physical activity levels of those with CAI.5,11 Although the exact neurophysiologic mechanism of CAI remains unclear, sensorimotor alterations have been hypothesized to play a role.12–14Individuals with CAI have known postural control impairments.12–14 Maintaining postural control is a continuous task that requires integration of three major sensory systems (visual, vestibular, and somatosensory systems).15,16 The contribution of each sensory modality is internally modulated depending on the available sensory systems, called sensory reweighting.17,18 Recent research suggests that CAI-associated postural control impairments might be due to an inability to appropriately reweight sensory and/or somatosensory information.19–21 Indeed, a recent systematic review suggests that individuals with CAI place a greater emphasis on visual information while balancing than uninjured controls.22 However, this conclusion was based on postural control scores under two conditions (ie, eyes open and closed) that only manipulated vision. Therefore, further research is needed to determine whether the reweighting abilities of those with CAI, under a more complex set of conditions, differs from uninjured controls.The Sensory Organization Test (SOT) is a laboratory-oriented assessment technique that quantifies the contribution of somatosensory, visual, and vestibular inputs on an individual's ability to maintain balance. During an SOT protocol, the participant's sensory information is altered or removed by using a sway-referencing force plate and/or visual surround. Similarly, the Clinical Test for Sensory Interaction and Balance (CTSIB) is a clinician-oriented alternative that was designed based on the same conceptual framework of the SOT.23 These assessment techniques have been used to study patients with concussion,24,25 older adults,26,27 and patients with vestibular disorders,28 but have not been applied to those with CAI despite evidence that those with CAI have altered sensory organization strategies.Therefore, the primary purpose of this study was to quantify sensory organization strategies in those with CAI relative to uninjured controls using the laboratory-based SOT and clinician-based CTSIB. We hypothesized that those with CAI would have a reduced ability to reweight sensory information, particularly in those conditions where visual information is removed or altered. The secondary purpose was to determine the association among corresponding SOT and CTSIB scores to test the face validity of the CTSIB in this population. Our hypothesis was that the performance on corresponding conditions between SOT and CTSIB would demonstrate moderate to high associations.MethodsStudy DesignThis study employed a cross-sectional study design to compare sensory organization strategies between CAI and healthy control groups. The independent variable was group (CAI and control) and dependent variables included the SOT scores and stance times in the CTSIB.Sample size estimates were based on CTSIB pilot data because of its clinical nature. The calculated between-group effect sizes averaged 0.5 across the stance conditions. Using this effect size, 1−β = 0.80, and α = 0.05 or less, a total of 22 participants (11 per group) are needed to determine whether group differences exist. Therefore, we planned to enroll 30 participants (15 per group) to ensure that participant attrition did not hurt the statistical power of the investigation.ParticipantsFifteen individuals with CAI and 15 uninjured controls who were between 18 and 35 years of age volunteered. Inclusion criteria for participants with CAI included: (1) having a history of at least one lateral ankle sprain, (2) experiencing at least two episodes of giving way within the past 6 months, (3) a score of greater than 11 on the Identification of Functional Ankle Instability (IdFAI), (4) having self-assessed disability scores of 90% or less on the Foot and Ankle Ability Measure (FAAM), and (5) having self-assessed disability scores of 80% or less on the FAAM Sport (FAAM-S). These inclusion criteria are in agreement with the International Ankle Consortium guidelines.29 If an individual has bilateral instability, the limb with lower FAAM and FAAM-S scores was used as the involved limb. For uninjured controls, the inclusion criteria included: (1) no history of ankle sprains and giving way episodes, (2) a score of less than 11 on the IdFAI, (3) a score of greater than 98% on the FAAM, and (4) a score of 98% or greater on the FAAM-S. Exclusion criteria for both groups included: (1) acute lower extremity and head injuries for the previous 3 months, (2) symptomatic musculoskeletal and head injuries sustained at any time, (3) known equilibrium disorders, and (4) chronic lower extremity pathologies (eg, ACL tears).29 The dominant limb was used for single-limb assessments within the control group. All participants provided written informed consent approved by an institutional review board at the University of North Carolina at Chapel Hill for all study elements prior to any data collection.ProceduresParticipants completed a single test session in which the SOT and the CTSIB were assessed in a counter-balanced order within each group and 10 minutes of rest was provided between SOT and CTSIB assessments. The SOT was administered using the Neuro-Com SMART EquiTest system Smart Balance System (NeuroCom International, Inc). This instrument is equipped with a dual force plate, which is set into a platform base and a movable visual surround. The SOT protocol produces sensory conflicts by systematically altering or removing visual and support-surface information. During SOT sway-referenced conditions, the visual surround (conditions 3 and 6) and the support surface (conditions 4 through 6) move in the sagittal plane to distort optical flow and somatosensory stimulation, respectively. This movement is controlled by the system software and the amount of motion is in proportion to the participant's magnitude of postural sway.25,30 All SOT testing was done barefoot with participants completing the double-limb protocol first. The participants performed three 20-second trials under six different conditions while they were asked to stand as still as possible with their arms relaxed at their sides and looking straight forward.30 All six of the SOT conditions are listed in Table 1. At the completion of the double-limb protocol, 3 minutes of rest was provided before the single-limb protocol was initiated. The order of trial completion (n = 18) for both the double-and single-limb assessment was randomized for each participant.Table 1 Six Sensory Conditions for the Sensory Organization Test and the Clinical Test of Sensory Integration in BalanceSensory InputsCondition 1Condition 2Condition 3Condition 4Condition 5Condition 6EyesOpenClosedOpenOpenClosedOpenVisual surroundFixedFixedSway-referencedFixedFixedSway-referencedSupport surfaceFixed SupportFixed SupportFixed SupportSway-referencedSway-referencedSway-referencedThe NeuroCom system automatically calculated the equilibrium scores under each condition and the overall composite scores. In brief, the equilibrium score from each trial represents a nondimensional percentage comparing participants' peak amplitude of sway to their theoretical limits of stability in the anterior-posterior direction. The overall composite equilibrium score was calculated based on the weighted average of all scores.30 A higher equilibrium score indicates better postural control. The NeuroCom system also calculated sensory analysis ratio scores for the somatosensory (SOM), visual (VIS), and vestibular (VEST) system by dividing the equilibrium score in conditions 2, 4, or 5 by the score in condition 1, respectively.30 This ratio score indicates the participant's ability to use those specific inputs. The preference ratio (PREF), calculated by dividing the sum of scores in conditions 3 and 6 by the sum of scores in conditions 2 and 5, reflects the degree to which a participant relies on visual information to maintain postural control when inaccurate visual input is present.30For the CTSIB, we followed the protocol developed by Shumway-Cook and Horak.23 The CTISB consists of three trials under three conditions (eyes open, eyes closed, and visual-conflict dome) and two surface conditions (fixed and foam Airex balance pad [AIREX]) (Table 1). CTSIB testing was initiated with condition testing order randomized for each participant. As previous reported,23 the visual-conflict dome was made from a paper lantern (cut in half) and secured to a headband to provide a visual sway-referencing effect. The foam pad was used as a sway-referenced surface to reduce somatosensory information accuracy. The primary CTSIB outcome is the time (seconds) that a participant remains in balance (maximum duration of 30 seconds).23 The time was stopped if the participants shifted/slid their involved foot over the pad, put their uninvolved limb down, removed their hands from their hips, or opened their eyes during the eyes closed trials.31 The overall composite time score and sensory analysis ratios (SOM, VIS, VEST, and PREF) were calculated using the same equations as for the SOT outcomes.30 All CTSIB testing was done barefoot. Only the single limb CTSIB protocol was assessed because pilot testing revealed that all participants were able to maintain balance for the full duration (30 seconds) during all double-limb CTSIB trials.Statistical AnalysisDescriptive statistics for performance on the SOT and CTSIB for both groups were calculated. Normality was assessed using a Shapiro-Wilk test. We employed separate multivariate analyses of variances (MANOVAs) and subsequent univariate ANOVAs, when appropriate, to compare SOT and CTSIB scores between groups. Bias-corrected Hedge's g effect sizes with their corresponding 95% confidence intervals (95% CI) were also used to confirm group differences. Hedge's g effect sizes were interpreted as follows: less than 0.3 as small, 0.31 to 0.7 as moderate, and greater than 0.71 as large. Pearson product-moment (r) or Spearman rank (ρ) correlations, based on data normality, were used to determine the associations among corresponding SOT and CTSIB conditions. The strength of the relationship was interpreted as: less than 0.20 as very weak, 0.20 to 0.39 as weak, 0.40 to 0.59 as moderate, 0.60 to 0.79 as strong, and 0.80 to 1.00 as very strong.32 All statistical analyses were performed using SPSS software (version 25.0; SPSS, Inc) and the level of statistical significance was set a priori at a P value of less than .05.ResultsThere were no significant differences between the CAI and control group demographics (ie, sex, age, height, and weight). As expected, the CAI group had significantly more ankle sprains and giving way episodes, as well as worse IdFAI, FAAM, and FAAM-S scores. Mean, standard deviations, and P values for participant demographics and injury characteristics are reported in Table 2.Table 2 Participant Demographics, Injury History Characteristics, and Self-reported FunctionCharacteristicCAI (n = 15)Control (n = 15)PSex (males/females)4/112/13.651Age (years)20.13 ± 1.0620.20 ± 0.77.846Height (cm)170.01 ± 11.85167.30 ± 9.40.494Weight (kg)70.58 ± 15.2861.63 ± 7.15.053Identification of Functional Ankle Instability24.87 ± 7.001.33 ± 1.99< .001Foot & Ankle Ability Measure Activities of Daily Living subscale (%)82.90 ± 7.60100.00 ± 0.00< .001Foot & Ankle Ability Measure Sport subscale (%)70.84 ± 10.21100.00 ± 0.00< .001Number of ankle sprains3.60 ± 2.13–< .001Number of giving way episodes within 6 months4.27 ± 3.45–< .001CAI = chronic ankle instabilitySOTFor double-leg stance, there was a significant group effect (P = .006). The CAI group had worse scores in all outcomes with significantly lower equilibrium scores under conditions 1, 2, and 5. Similarly, the CAI group had lower composite and lower SOM and VEST ratio scores compared to the control group. These results were associated with large effect sizes and 95% CIs that did not cross zero (Table 3). However, no statistical differences were seen in conditions 3, 4, and 6, or VIS and PREF ratios.Table 3 SOT Scores, Mean ± SD, and Effect SizesaParameterDouble-limb StanceSingle-limb StanceCAIControlPEffect Sizes (95% CI)CAIControlPEffect Sizes (95% CI)SOT191.4 ± 2.4593.80 ± 1.88.005−1.07 (−1.83 to −0.30)86.92 ± 4.4889.73 ± 2.20.038−0.77 (−1.52 to −0.03)SOT287.00 ± 3.2791.00 ± 1.55< .001−1.52 (−2.33 to −0.71)69.00 ± 6.6976.91 ± 4.95.001−1.31 (−2.10 to −0.52)SOT387.22 ± 4.1788.87 ± 3.84.271−0.40 (−1.12 to 0.32)79.76 ± 3.4383.27 ± 4.05.016−0.91 (−1.66 to −0.16)SOT478.38 ± 6.2381.53 ± 7.87.234−0.43 (−1.16 to 0.29)79.58 ± 6.6480.87 ± 6.04.583−0.20 (−0.92 to 0.52)SOT559.62 ± 10.5468.49 ± 7.02.011−0.96 (−1.72 to −0.21)53.56 ± 7.7959.89 ± 9.74.059−0.70 (−1.44 to 0.04)SOT652.27 ± 9.3958.42 ± 15.66.202−0.46 (−1.19 to 0.26)59.27 ± 7.7664.51 ± 7.89.077−0.65 (−1.39 to 0.08)Composite72.27 ± 5.6876.93 ± 6.30.042−0.76 (−1.50 to −0.02)69.60 ± 4.1073.67 ± 4.24.012−0.95 (−1.70 to −0.19)SOM ratio95.13 ± 2.9297.27 ± 1.87.024−0.85 (−1.60 to −0.10)79.93 ± 9.2885.80 ± 4.95.039−0.77 (−1.51 to −0.03)VIS ratio85.73 ± 5.2787.00 ± 7.58.599−0.19 (−0.91 to 0.53)91.40 ± 6.2490.20 ± 6.70.6160.18 (−0.54 to 0.90)VEST ratio65.2 ± 10.5373.00 ± 6.95.024−0.85 (−1.60 to −0.10)61.47 ± 7.9866.67 ± 9.85.123−0.56 (−1.29 to 0.17)PREF ratio95.2 ± 5.2192.27 ± 8.88.2790.39 (−0.33 to 1.11)114.33 ± 14.12108.47 ± 11.66.2250.44 (−0.28 to 1.16)SOT = Sensory Organization Test; SD = standard deviation; CAI = chronic ankle instability; SOM = somatosensory; VIS = visual; VEST = vestibular; PREF = preferenceaBold indicates a significant difference between CAI and control groups. A negative effect size for all outcomes except the PREF ratio indicates a worse score is present in the CAI group.For single-leg stance, there was a significant group effect (P = .044) because the CAI group had worse scores in all but one outcome. More specifically, individuals with CAI showed significantly lower equilibrium scores under conditions 1, 2, and 3, as well as lower composite and SOM ratio scores. These results were associated with large effect sizes and 95% CIs that did not cross zero. However, no significant differences were noted in conditions 4, 5, and 6, as well as VIS, VEST, and PREF ratio scores. Means, standard deviations, and effect sizes, and corresponding 95% CIs for SOT results can be seen in Table 3.CTSIBThere was a significant group effect for CTSIB testing (P = .035). The CAI group had worse scores in all outcomes and showed significantly lower time in balance under conditions 2 and 6, as well as lower composite and SOM ratio scores. These results were associated with large effect sizes and 95% CIs that did not include zero. However, no differences were noted in conditions 1, 3, 4, and 5, as well as VIS, VEST, and PREF ratio scores. A summary of CTSIB scores for each group is provided in Table 4.Table 4 CTSIB Scores for Single-limb Stance, Mean ± SDaParameterCAIControlPEffect Sizes (95% CI)CTSIB1 (s)29.83 ± 0.6530.00 ± 0.00.326−0.36 (−1.08 to 0.36)CTSIB2 (s)16.80 ± 7.2723.57 ± 4.81.005−1.07 (−1.83 to −0.30)CTSIB3 (s)18.13 ± 7.4422.71 ± 6.09.076−0.66 (−1.39 to 0.08)CTSIB4 (s)27.14 ± 4.0428.43 ± 3.89.378−0.32 (−1.04 to 0.40)CTSIB5 (s)4.69 ± 1.525.86 ± 2.21.104−0.60 (−1.33 to 0.13)CTSIB6 (s)3.48 ± 1.675.81 ± 2.20.003−1.16 (−1.93 to −0.39)CTSIB_Composite (s)14.78 ± 2.9617.29 ± 2.10.012−0.95 (−1.71 to −0.20)CTSIB_SOM ratio56.60 ± 25.4078.58 ± 16.05.008−1.01 (−1.77 to −0.25)CTSIB_VIS ratio90.94 ± 13.2094.77 ± 12.95.429−0.28 (−1.00 to 0.43)CTSIB_VEST ratio15.80 ± 5.3919.53 ± 7.36.125−0.56 (−1.29 to 0.17)CTSIB_PREF ratio104.08 ± 39.6994.15 ± 33.99.4680.26 (−0.46 to 0.98)CTSIB = Clinical Test of Sensory Integration in Balance; SD = standard deviation; CAI = chronic ankle instability; SOM = somatosensory; VIS = visual; VEST = vestibular; PREF = preferenceaBold indicates significant difference between CAI and control groups. A negative effect size for all outcomes except the PREF ratio indicates a worse score is present in the CAI group.SOT and CTSIB AssociationsSignificant moderate to strong relationships between single-limb SOT and CTSIB were identified in condition 2 (r = 0.645, P < .001), condition 5 (r = 0.498, P = .005), composite score (r = 0.402, P = .038), SOM ratio score (r = 0.479, P = .007), and VEST ratio score (ρ = 0.493, P = .006). Associations were not identified for condition 1 (ρ = 0.054, P = .778), condition 3 (r = 0.161, P = .395), condition 4 (ρ = 0.021, P = .912), condition 6 (r = −0.079, P = .677), VIS ratio score (r = 0.003, P = .988), and PREF ratio score (r = 0.134, P = .481).DiscussionTo our knowledge, we are the first to present SOT and CTSIB scores in those with CAI relative to uninjured healthy controls. The results indicate that both laboratory-oriented (ie, SOT) and clinician-oriented (ie, CTSIB) assessments can detect postural instability in patients with CAI, consistent with the existing literature.12–14,21 Most important, both the laboratory-oriented (SOT) and clinician-oriented (CTSIB) assessments detected altered sensory organization strategies in those with CAI, which is also consistent with the literature.21,22 Although the exact mechanisms causing these postural control impairments and sensory organization alterations remain unknown, our results suggest three possibilities: (1) a decreased ability to use somatosensory information, (2) a reduced ability to reweight among sources of sensory information, and (3) an increased reliance on visual information.Those with CAI have an impaired ability to detect ankle joint position33 and have increased plantar light-touch thresholds.34,35 These impairments may be due to altered/decreased input from damaged mechanoreceptors,36 which are also hypothesized to be a causal factor of the observed postural control deficits in those with CAI. The lower SOM ratio scores in those with CAI, from both the SOT and CTSIB, support this premise and further suggest that patients with CAI are less able to use somatosensory information during both double-and single-limb balance tasks.Those with CAI also demonstrated lower composite SOT and CTSIB scores compared to healthy controls. These results may indicate that patients with CAI are less able to compensate for the removal of multiple sources of sensory information compared to those without CAI. This deficit may be due, in part, to the observed inability to use somatosensory information. As expected, both groups demonstrated greater postural sway as additional sources of sensory information are removed or made inaccurate. However, uninjured controls demonstrated a smaller sway response during the SOT protocols and a longer time in balance during the CTSIB protocol. These findings suggest that a healthy sensorimotor system is better able to adapt to changing task constraints, consistent with the existing literature.37 Similarly, healthy individuals appear better able to adapt to the removal of specific somatosensory inputs. For example, anesthetizing the lateral ankle ligaments38,39 and disrupting the afferent signals from the plantar surface of the foot via textured insoles40 does not alter postural control performance in uninjured healthy controls. However, patients with CAI demonstrate significant declines in balance performance under similar experimental conditions (ie, textured insoles).20Altering (conditions 3 and 6) or removing (conditions 2 and 5) visual information also caused greater postural control declines in patients with CAI compared to uninjured individuals. PREF ratio scores, which indicate the degree of visual reliance, were increased in those with CAI, although the difference was not statistically different. These results are also consistent with the existing literature.21,22 Although these results suggest that those with CAI rely more on visual information, the result may be a natural compensation because of the inability to use somatosensory information while balancing and/or the inability to reweight among sensory sources.Cumulatively, the published literature and our current results suggest that those with CAI, relative to controls, have altered sensory organization strategies that appears to manifest as an inability to dynamically re-weight to available sources of sensory input and worse postural control.19,20 These impairments may help explain the functional consequences that are hallmarks of CAI, such as repeated ankle sprains and episodes of giving way,7 because poor postural control is a risk factor for musculoskeletal injuries (ie, ankle, knee, and low back).41–43 However, further research on the impact of altered sensory organization strategies directly on injury risk remains unknown in those with CAI. Future research is also needed to determine if and how sensory organization strategies can be modified and when the post-injury time frame offers the best opportunity to modify an individual's sensory organization strategy. To date, only one systematic review has investigated the modifiability of sensory organization strategies in those with CAI. In brief, the authors noted that traditional balance training improves postural control but does not reduce reliance on visual information.44Our secondary results partially support our a priori hypothesis because some but not all SOT and CTSIB conditions and ratio scores associated with each other. We believe that the lack of consistent associations was due, in part, to a ceiling effect in conditions 1 and 4 of the CTSIB (ie, the majority of participants were able to maintain balance for the duration of the assessment). Despite this limitation, the identified associations suggest that the CTSIB could be a clinician-oriented option to quantify sensory organization strategies. However, further research is needed to improve the assessment tool (eg, wearable sensors) to accurately quantify abnormal postural sway or sensory integration with better precision.This investigation is not without limitations. First, our participants were young recreationally active volunteers who were not seeking medical treatment for their CAI. Thus, the results may have limited generalizability to other subsamples of CAI. Second, this investigation used a small sample size but our study was powered appropriately, which suggests that a type II error was not made. Although the demographic and injury history data are representative of the larger CAI population, future research should confirm these initial results in a larger sample. Finally, although our results are consistent with the existing literature, the connection between sensory organization strategies and injury history or self-reported disability has yet to be established.Implications for Clinical PracticeThe primary implication is that the CTSIB is a clinician-oriented assessment tool capable of detecting postural control impairments and altered sensory organization strategies in those with CAI. Thus, the results suggest that providers now have a clinician-based outcome measure to help them discern whether their intervention strategies are able to modify a patient's sensory organization strategy. Unfortunately, the current research design is not able to address ways to modify sensory organization strategies in those with CAI. However, poor sensory organization strategies in those with CAI may indicate the importance of challenging various sensory systems during the rehabilitation after ankle injuries. 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Sports Med. 2018; 48(4):893–905.10.1007/s40279-017-0850-8 CrossrefGoogle Scholar Previous article Next article FiguresReferencesRelatedDetails Request Permissions InformationCopyright 2020, SLACK IncorporatedPDF downloadCorrespondence: Kyeongtak Song, PhD, ATC, CSCS, Department of Exercise and Sport Science, University of North Carolina at Chapel Hill, 311 Woollen Gym, Chapel Hill, NC 27599. Email: [email protected]unc.eduFrom the Department of Exercise and Sport Science, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.The authors have no financial or proprietary interest in the materials presented herein. Received2/01/20Accepted8/13/20