Changes in Spinal and Corticospinal Excitability in Patients with Chronic Ankle Instability: A Systematic Review with Meta-Analysis
Abstract
:1. Introduction
2. Experimental Section
2.1. Eligibility Criteria
2.2. Literature Search Strategy
2.3. Study Selection and Data Extraction
2.4. Assessment of Methodological Quality
2.5. Data Analysis
3. Results
3.1. Search Findings
3.2. Methodological Quality
3.3. Study Characteristics
3.3.1. Study Design
3.3.2. Participants
3.3.3. Outcome Measures
3.4. Neural Excitability Meta-Analysis
3.4.1. Soleus Hmax/Mmax Ratio
3.4.2. Fibular Longus Hmax/Mmax Ratio
3.4.3. Soleus Cortical Motor Threshold
3.4.4. Fibularis Longus Cortical Motor Threshold
3.5. Risk of Bias across Studies
4. Discussion
4.1. Spinal Reflex Excitability Associated with CAI
4.1.1. Functional Consequences of Reflex Inhibition in CAI Patients
4.1.2. Mechanisms of Reflex Inhibition in CAI Patients
4.1.3. Reduced Spinal Reflex Excitability as a Sign of “Arthrogenic Muscle Inhibition” in CAI Patients?
4.2. Corticospinal Excitability Associated with CAI
4.3. Limitations
4.4. Recommendations for Future Research
5. Conclusions
Author Contributions
Conflicts of Interest
References
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Author (Year) | Study Design | Inclusion Criteria | Participant Characteristics | Stimulation Settings | Outcome | ||
---|---|---|---|---|---|---|---|
CAI Group | Comparison Group | CAI Group | Comparison Group | ||||
McVey (2005) | Case- control | ≥5 “yes” responses on AII | Uninjured: No history of ankle injury or significant lower extremity injury or surgery | 15 unilateral CAI patients (8 females, 26.5 ± 126.5 years, 173 ± 6.8 cm, 70 ± 7.2 kg) | 14 uninjured (13 females, 21.3 ± 2.5 years,166 ± 5.4 cm, 61 ± 6.4 kg) | Unipolar stimulating electrode to stimulate the sciatic nerve with 1 ms squared wave pulse that were 10 s apart by increasing stimulus intensity in 0.2 V until Hmax and Mmax were obtained | Hmax:Mmax ratios of soleus, fibularis longus, and tibialis anterior measured in a prone position |
Sefton (2008) | Case- control | >1 ankle sprain in the previous year, recurring symptoms, and difficulty in >1 area in the FADI or 2 areas in the FADI-Sport | Uninjured: No history of ankle injury and no incidence of acute or chronic lower extremity injuries | 22 CAI patients (17 females, 22.3 years, 167.6 cm, 69.8 kg) Measures of standard deviation were not reported | 21 uninjured (16 females, 21.9 years, 166.0 cm, 64.1 kg) Measures of standard deviation were not reported | Unipolar stimulating electrode placed over the popliteal fossa to stimulate the posterior tibial nerve with 1 ms squared wave pulse that were 10 to 20 s apart by slowly increasing stimulus intensity | Hmax:Mmax ratio of soleus during bipedal stance and percent changes in paired reflex depression and recurrent inhibition of soleus measured both in unipedal and bipedal stances |
Doeringer (2009) | Case-control with crossover | A history of ankle sprain, episodes of “giving way” and feelings of instability (≥3 “yes” responses on AII) | Uninjured: No history of ankle sprain or other lower extremity injuries to the tested limb | 12 CAI patients (9 females, 23 ± 1 years, 168.7 ± 9.8 cm, 73.4 ± 20.0 kg) | 12 uninjured (7 females, 23 ± 1 years, 171.7 ± 7.0 cm, 77.9 ± 14.9 kg) | Bipolar (bar) stimulating electrode placed over the popliteal fossa to stimulate the posterior tibial nerve with 1 ms squared wave pulses that were 20 s apart by increasing stimulus intensity in 0.2 to 0.5 V increments until Hmax and Mmax were obtained | Hmax:Mmax ratio of soleus measured in a reclining position with 120° of hip flexion and 60° of knee flexion, and the neutral position of the ankle |
Palmieri-Smith (2009) | Case-control | All CAI subjects that were physically active (Tegner score of 5 or 6) met the criteria set forth by both Functional Ankle Instability Questionnaire and AII. | Uninjured: All control subjects were physically active (Tegner score of 5 or 6), but other criteria were not specified. | 21 unilateral CAI patients (18 females, 21 ± 2 years, 171 ± 7 cm, 65 ± 9 kg) | 21 uninjured (18 females, 21 ± 3 years, 169 ± 9 cm, 64 ± 10 kg) | Unipolar stimulating electrode placed over the popliteal fossa to stimulate the sciatic nerve with 1 ms squared wave pulses that were 10 s apart by increasing stimulus intensity in 0.2 V increments until Hmax and Mmax were obtained | Hmax:Mmax ratio of fibularis longus measured in prone position |
Doeringer (2010) | Case-control with crossover | A history of ankle sprain, episodes of “giving way” and feelings of instability (≥3 “yes” responses on AII) | Uninjured: No history of ankle sprain or other lower extremity injuries to the tested limb | 12 CAI patients (9 females, 23 ± 1 years, 168.7 ± 9.8 cm, 73.4 ± 20.0 kg) | 12 uninjured (7 females, 23 ± 1 years, 171.7 ± 7.0 cm, 77.9 ± 14.9 kg) | Bipolar (bar) stimulating electrode placed over the popliteal fossa to stimulate the sciatic nerve with 1 ms squared wave pulses that were 20 s apart by increasing stimulus intensity in 0.2 to 0.5 V increments until Hmax and Mmax were obtained | Hmax:Mmax ratio of fibularis longus and tibialis anterior measured in a reclining position with 120° of hip flexion, 60° of knee flexion, and the neutral position of the ankle |
Sefton (2011) | Case- control with repeated measures | >1 ankle sprain in the previous year, recurring symptoms, and difficulty in >1 area in the FADI or 2 areas in the FADI-Sport | Uninjured: No history of ankle injury and no incidence of acute or chronic lower extremity injuries | 12 CAI patients (8 females, 21.2 ± 2.1 years, 165.1 ± 8.9 cm, 67.2 ± 9.4 kg) | 9 uninjured (6 females, 20.8 ± 1.3 years, 167.3 ± 7.9 cm, 62.8 ± 10.3 kg) | Unipolar stimulating electrode placed over the popliteal fossa to stimulate the posterior tibial nerve with 1 ms squared wave pulse that were 10 to 20 s apart by slowly increasing stimulus intensity | Hmax:Mmax ratio of soleus during bipedal stance and percent changes in paired reflex depression and recurrent inhibition of soleus measured both in unipedal and bipedal stances |
Kim (2012) | Case-control | A history of at least 1 lateral ankle sprain (1-yr old or greater), episodes of “giving way”, feelings of instability (≥4 “yes” responses on AII), and self-reported ankle disability (≤90% on FAAM and ≤80% on the FAAM-Sport) | Uninjured: No history of ankle injury or significant lower extremity injury or surgery, and any limitation of ankle function | 16 unilateral CAI patients (6 females, 21.0 ± 6.9 years, 173.9 ± 7.4 cm, 72.6 ± 11.9 kg) | 15 uninjured (6 females 19.9 ± 4.3 years, 175.8 ± 9.7 cm, 71.3 ± 17.8 kg) | Unipolar stimulating electrode placed over the superior popliteal fossa to stimulate the sciatic nerve with 1 ms squared wave pulses that were at least 12 s apart by increasing stimulus intensity in 0.2 V increments until Hmax was obtained, then 1.0 V increments until Mmax plateaued | Hmax:Mmax ratio of soleus and fibularis longus measured in 3 body positions: prone, bipedal, and unipedal stances |
Pietro- simone (2012) | Case-control | A history of at least 2 unilateral ankle sprains and self-reported function (<90% on FADI, <80% on FADI-Sport) | Uninjured: No ankle instability and self-reported functions (>95% on FADI, >85% on FADI-Sport) | 10 unilateral CAI patients (6 females, 21.2 ± 1.2 years, 175.1 ± 9.7 cm, 77.1 ± 13.6 kg) | 10 uninjured (6 females 21.2 ± 2.3 years, 172.3 ± 8.9 cm, 73.4 ± 7.2 kg) | Double-cone coil placed over the contralateral vertex of the cranium relative to the involved limb to deliver a single magnetic pulse of a maximum magnetic stimulus of 1.4 Tesla that were 15 s apart between trials | Resting motor threshold expressed as a percentage of 2 Tesla of fibularis longus measured in the seated position with 85° of hip flexion, 10° of knee flexion, and 10° of ankle plantar flexion |
Needle (2013) | Case- control | A history of at least 1 unilateral ankle sprain (≤25 on CAIT) | Uninjured: No history of ankle injury and a score of >27 on CAIT) | 12 unilateral CAI patients (6 females, 20.9 ± 4.1 years, 170.6 ± 10.1 cm, 72.5 ± 15.0 kg) | 12 uninjured (6 females 21.2 ± 2.6 years, 172.7 ± 8.5 cm, 70.0 ± 15.0 kg) | A figure-8 coil placed over the contralateral vertex of the cranium relative to the involved limb to deliver a single magnetic pulse of a maximum magnetic stimulus of 1.4 Tesla that were 5 s apart between trials | AMT of soleus, fibularis longus, and tibialis anterior measured in the seated position with pronation of ankle at 15% of maximal effort of fibularis longus activity |
Kim (2015) | Case-control with crossover | A history of at least 1 lateral ankle sprain (1-yr old or greater), episodes of “giving way”, feelings of instability (≥4 “yes” responses on AII), and self-reported ankle disability (≤90% on FAAM and ≤80% on the FAAM-Sport) | Uninjured: No history of ankle injury or lower extremity injury or surgery and any limitation of ankle function | 15 CAI patients (6 females, 22.6 ± 5.8 years, 174.7 ± 8.1 cm, 74.9 ± 12.8 kg) | 15 uninjured (6 females, 23.8 ± 5.8 years, 171.9 ± 9.9 cm, 68.9 ± 15.5 kg) | Unipolar stimulating electrode placed over the superior popliteal fossa to stimulate the sciatic nerve with 1 ms squared wave pulses that were at least 12 s apart by increasing stimulus intensity in 0.2 V increments until Hmax was obtained, then 1.0 V increments until Mmax plateaued | Hmax:Mmax ratio of soleus and fibularis longus measured in 3 body positions: prone, bipedal and unipedal stances |
McLeod (2015) | Case-control | A history of at least 1 acute lateral ankle sprain, resulting in swelling, pain, and/or temporary loss of function but not within the 3 months) and >2 episodes of the ankle “giving way” in the 6 months (≤80% on the FAAM-Sport) | Uninjured: No history of ankle injury and a score of 100% on the FAAM-Sport | 21 CAI patients (12 females, 20.8 ± 1.6 years, 171.6 ± 11.4 cm, 68.8 ± 11.9 kg) | 24 uninjured (17 females, 22.5 ± 2.9 years, 172.4 ± 10.9 cm, 69.2 ± 12.3 kg) | For H-reflex testing, the unipolar stimulating electrode to stimulate (1) the sciatic nerve for fibularis longus and (2) the femoral nerve for vastus medialis separately by increasing stimulus intensity in 0.2 V increments until Hmax was obtained For TMS testing, the double-cone coil placed over the contralateral vertex of the cranium relative to the involved limb to deliver a brief magnetic stimulus of a maximum magnetic stimulus of 1.4 Tesla | Hmax:Mmax ratios of both fibularis longus and vastus medialis measured in a supine position For the fibularis longus AMT and 5 MEP responses at varying levels of intensity, measured in the seated position with 85° of hip flexion, 10° of knee flexion, and 10° of ankle plantar flexion For the vastus medialis, AMT and 5 MEP responses at varying levels of intensity, measured in the seated position with 85° of hip flexion and 90° of knee flexion |
Bowker (2016) | Case-control | A history of at least 1 ankle sprain, resulting in swelling, pain, and/or temporary loss of function), ≥2 episodes of the ankle “giving way” within the 6 months, perceived ankle instability, and dysfunction during daily living activities (≥5 “yes” responses on AII and scores of ≥11 on IdFAI) | Uninjured: No history of ankle sprain and a score of 0 on both AII and IdFAI Copers: History of ankle sprains, but no reported episode of the ankle “giving way”, perceived instability, or loss of function without modifying physical activity, <5 “yes” responses on AII, and scores of <11 on IdFAI | 37 CAI patients (19 females, 22 ± 3.5 years, 25.2 ± 3.8 body mass index) | 26 uninjured (17 females, 21.6 ± 3.2 years, 23.7 ± 2.8 body mass index 30 copers (17 females, 21.9 ± 4.3 years, 26.2 ± 6.3 body mass index) | Unipolar stimulating electrode placed over the proximal lateral popliteal fossa to stimulate the posterior tibial nerve with 1 ms squared wave pulse that were 10 s apart by increasing or decreasing the stimulus intensity in 0.2 V increments until Hmax was obtained, then 1.0 V increments until Mmax plateaued | Hmax:Mmax ratio of soleus measured in the seated position with 90° of hip flexion, 90° of knee flexion, 90° of ankle plantar flexion |
Terada (2016) | Case-control | A history of at least 2 significant ankle sprains, resulting in swelling, pain, and/or temporary loss of function, ≥2 episodes of the ankle “giving way” within the 6 months, perceived ankle instability, and dysfunction during daily living activities (≥4 “yes” responses on AII and scores of ≥11 on IdFAI) | Uninjured: No history of ankle sprain and a score of 0 on both the AII and IdFAI | 16 CAI patients (6 females, 22.2 ± 3.6 years, 25.8 ± 2.5 body mass index) | 17 uninjured (9 females, 21.2 ± 3.0 years, 24.7 ± 3.1 body mass index) | For Mmax of the fibularis longus, the unipolar stimulating electrode placed over the proximal lateral popliteal fossa to stimulate the posterior tibial nerve with 1 ms squared wave pulse by increasing the stimulus intensity in 1.0 V increments until Mmax plateaued For TMS testing, the double-cone coil placed over the contralateral vertex of the cranium relative to the involved limb to deliver a series of magnetic stimuli of 1.0 Tesla | AMT, MEP120%:Mmax ratio, and CSP: MEP120% ratio of soleus measured in the seated position with 90° of knee flexion, 90° of ankle dorsiflexion |
Kosik (2017) | Case-control | A history of at least 1 acute lateral ankle sprain, resulting in swelling, pain, and/or temporary loss of function and ≥2 episodes of the ankle “giving way” within the 6 months (≥5 “yes” responses on AII and scores of ≥11 on IdFAI ≤24 on CAIT) | Uninjured: No history of lower extremity injuries and a score 0 on both the AII and IdFAI, and 30 on CAIT | 18 CAI patients (14 females, 23.8 ± 3.6 years, 169.6 ± 7.5 cm, 73.1 ± 12.0 kg) | 16 uninjured (10 females, 21.1 ± 2.2 years, 168.6 ± 13.4 cm, 66.5 ± 10.2 kg) | For H-reflex testing, the unipolar stimulating electrode to stimulate the proximal common fibular nerve with 1 ms squared wave pulse by increasing or decreasing the stimulus intensity in 0.2 V increments until Hmax was obtained, then 1.0 V increments until Mmax plateaued For TMS testing, The double-cone coil placed over the contralateral vertex of the cranium relative to the involved limb to deliver a series of magnetic stimuli of 1 Tesla that were 10 s apart | Hmax:Mmax ratio of fibularis longus measured in the prone position MEP100%:Mmax ratio and corticomotor map outcomes for fibularis longus: (1) size of corticomotor map area, (2) volume of corticomotor map, (3) location of cortical representation, measured in the seated position with 75° of hip flexion, 60° of knee flexion, 80° of ankle plantar flexion |
Terada (2017) | Case- control | CAI subgroups: (1) PI-RAS: A history of at least 2 previous ankle sprains and ≥2 episodes of the ankle “giving way” within the 6 months (≥5 “yes” responses on AII and scores of ≥11 on IdFAI) (2) PI: A history of one previous ankle sprain and ≥2 episodes of the ankle “giving way” within the 6 months (≥5 “yes” responses on AII and scores of ≥11 on IdFAI) (3) RAS: A history of at least 2 previous ankle sprains, but no episode of the ankle “giving way”, <5 “yes” responses on AII, and scores of <11 on IdFAI | Uninjured: No history of ankle sprain and a score 0 on both the AII and IdFAI Copers: A history of one previous ankle sprain, report of returning to full activity for at least 12 months following an initial ankle sprain without recurrent injury, no reported episode of the ankle “giving way”, perceived instability, or loss of function without modifying physical activity, <5 “yes” responses on AII, and scores of <11 on IdFAI | 25 PI-RAS patients (11 females, 22.5 ± 4.0 years, 171.4 ± 8.7 cm, 76.2 ± 14.8 kg, 25.8 ± 3.6 body mass index) 13 PI patients (9 females, 20.8 ± 1.6 years, 165.8 ± 6.5 cm, 65.7 ± 11.8 kg, 23.9 ± 3.8 body mass index) 12 RAS patients (6 females, 22.2 ± 4.8 years, 171.0 ± 10.3 cm, 79.1 ± 7.8 kg, 26.7 ± 7.6 body mass index) | 26 uninjured (17 females, 21.6 ± 3.2 years, 166.1 ± 8.1 cm, 66.2 ± 13.1 kg, 23.8 ± 3.0 body mass index) 18 copers (11 females, 21.6 ± 4.0 years, 169.6 ± 11.3 cm, 72.4 ± 17.3 kg, 24.9 ± 3.8 body mass index) | For H-reflex testing, the unipolar stimulating electrode to stimulate the posterior tibial nerve with 1 ms squared wave pulse that were 10 s apart by increasing the stimulus intensity in 0.2 V increments until Hmax was obtained, then 1.0 V increments until Mmax plateau | Hmax:Mmax ratio of soleus measured in the seated position with 90° of hip flexion, 90° of knee flexion, and 90° of ankle plantar flexion |
Otzel (2019) | Case-control with crossover | A history of at least 1 moderate ankle sprain requiring immobilization, no formal rehabilitation, at least one recurrent ankle sprain 3-6 months prior to participation, perceived pain, ankle instability or weakness, and self-reported functional limitations (≤90% on FADI and ≤80% on the FADI-Sport) | Uninjured age-matched control Specific inclusion criteria not reported | 10 CAI patients (6 females, 20.7 ± 1.3 years, 169.4 ± 10.7 cm, 66.0 ± 10.1 kg) | 10 uninjured (7 females, 19.8 ± 0.7 years, 165.6 ± 9.2 cm, 59.1 ± 10.7 kg) | For H-reflex testing, the unipolar stimulating electrode to stimulate the posterior tibial nerve with 1 ms squared wave pulse that were 10 s apart by increasing the stimulus intensity in 0.2 V increments until Hmax was obtained, then continued until Mmax plateau | Hmax:Mmax ratio of soleus measured in the seated position with 30° of hip flexion, 90° of knee flexion, 90° of ankle plantar flexion |
Thompson (2019) | Case-control | A history of at least 1 significant ankle sprain, causing inflammatory symptoms and disrupted activity), the most recent ankle sprain occurred less than 3 months prior to study participation, reports of episodes of the ankle “giving way” and/or recurrent pain and/or perceived ankle instability, and dysfunction during daily living activities (≥5 “yes” responses on AII and scores <24 on CAIT) | Uninjured: No history of an ankle sprain Copers: History of ankle sprains, but no report of recurrent injuries, episode of the ankle “giving way”, and/or perceived instability | 12 CAI patients (4 females, 25.2 ± 3.7 years, 177.7 ± 8.1 cm, 75.8 ± 14.8 kg) | 12 uninjured (4 females, 23.3 ± 4.5 years, 171.6 ± 6.2 cm, 74.3 ± 10.2 kg) 12 copers (4 females, 24.2 ± 4.7 years, 172.7 ± 8.2 cm, 71.4 ± 6.9 kg) | For H-reflex testing, the unipolar stimulating electrode to stimulate the posterior tibial nerve with 1 ms squared wave pulse that was 10–15 s apart | Soleus Hmax:Mmax ratio and slope of recruitment curve during bipedal stance Soleus H50%:Mmax ratio and percent changes in presynaptic inhibition and recurrent inhibition, measured both in unipedal and bipedal stances |
Study | Reporting | External Validity | Internal Validity Bias | Internal Validity Confounding | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Quality Index Score (%) | 1. Hypothesis Clearly Described? | 2. Main Outcomes Clearly Described? | 3. Characteristics of the Patients included Clearly Described? | 5. Distribution of Principle Confounder of Each Group Clearly Described? | 6. Main Findings Clearly Described? | 7. Estimates of Random Variability Provided for the Main Outcomes? | 10. Actual Probability Values Reported for Main Outcomes? | 11. Were the Subjects Asked to Participate Representative of the Entire Population? | 12. Were the Subjects who Were Prepared to Participate Representative of the Entire Population? | 16. Was it Clear if the Results Were Based on “Data Dredging’? | 18. Were the Statistical Tests Appropriate? | 20. Were the Main Outcome Measures Valid and Reliable? | 21. Were all Patients and Controls Recruited from the Same Population? | 22. Were all Patients and Controls Recruited over the Same Time Period? | |
McVey (2005) | 60.0 | + | + | - | + | + | + | + | - | - | + | + | + | - | - |
Sefton (2008) | 66.7 | - | + | - | ++ | + | + | + | - | - | + | + | + | + | - |
Doeringer (2009) | 66.7 | + | + | - | + | + | + | + | - | - | + | + | + | + | - |
Palmieri-Smith (2009) | 66.7 | + | + | - | ++ | + | + | + | - | - | + | + | + | - | - |
Doeringer (2010) | 66.7 | + | + | - | + | + | + | + | - | - | + | + | + | + | - |
Sefton (2011) | 60.0 | + | + | - | + | + | + | + | - | - | + | + | + | - | - |
Kim (2012) | 73.3 | + | + | + | ++ | + | + | + | - | - | + | + | + | - | - |
Pietro- simone (2012) | 66.7 | + | + | - | ++ | + | + | + | - | - | + | + | + | - | - |
Needle (2013) | 46.7 | - | - | - | ++ | - | + | + | - | - | + | + | - | + | - |
Kim (2015) | 73.3 | + | + | + | ++ | + | + | + | - | - | + | + | + | - | - |
McLeod (2015) | 60.0 | + | + | - | + | + | + | + | - | - | + | + | + | - | - |
Bowker (2016) | 73.3 | + | + | + | + | + | + | + | - | - | + | + | + | + | - |
Terada (2016) | 73.3 | + | + | + | + | + | + | + | - | - | + | + | + | + | - |
Kosik (2017) | 73.3 | + | + | + | + | + | + | + | - | - | + | + | + | + | - |
Terada (2017) | 73.3 | + | + | + | + | + | + | + | - | - | + | + | + | + | - |
Otzel (2019) | 60.0 | + | + | + | + | + | + | + | - | - | + | + | - | - | - |
Thompson (2019) | 60.0 | + | + | + | + | + | + | + | - | - | + | + | - | - | - |
Average (SD) | 65.9 (7.4) |
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Kim, K.-M.; Kim, J.-S.; Cruz-Díaz, D.; Ryu, S.; Kang, M.; Taube, W. Changes in Spinal and Corticospinal Excitability in Patients with Chronic Ankle Instability: A Systematic Review with Meta-Analysis. J. Clin. Med. 2019, 8, 1037. https://doi.org/10.3390/jcm8071037
Kim K-M, Kim J-S, Cruz-Díaz D, Ryu S, Kang M, Taube W. Changes in Spinal and Corticospinal Excitability in Patients with Chronic Ankle Instability: A Systematic Review with Meta-Analysis. Journal of Clinical Medicine. 2019; 8(7):1037. https://doi.org/10.3390/jcm8071037
Chicago/Turabian StyleKim, Kyung-Min, Joo-Sung Kim, David Cruz-Díaz, Seungho Ryu, Minsoo Kang, and Wolfgang Taube. 2019. "Changes in Spinal and Corticospinal Excitability in Patients with Chronic Ankle Instability: A Systematic Review with Meta-Analysis" Journal of Clinical Medicine 8, no. 7: 1037. https://doi.org/10.3390/jcm8071037