Effect of walking and resting after three cryotherapy modalities

Effect of walking and resting after three cryotherapy modalities on the recovery of sensory and motor nerve conduction velocity in healthy subjects

Efeito da marcha e do repouso após aplicação de três protocolos de crioterapia na recuperação da velocidade de condução sensorial e motora em sujeitos saudáveis

Esperanza Herrera^I; Maria Cristina Sandoval^I; Diana M. Camargo^I; Tania F. Salvini^II

^ISchool of Physical Therapy, Health Faculty, Universidad Industrial de Santander (UIS), Bucaramanga, Santander, Colômbia
^IILaboratory of Muscle Plasticity, Department of Physical Therapy, Universidade Federal de São Carlos (UFSCar), São Carlos, SP, Brazil

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ABSTRACT

BACKGROUND: Different cryotherapy modalities have distinct effects on sensory and motor nerve conduction parameters. However, it is unclear how these parameters change during the post-cooling period and how the exercise carried out in this period would influence the recovery of nerve conduction velocity (NCV).
OBJECTIVES: To compare the effects of three cryotherapy modalities on post-cooling NCV and to analyze the effect of walking on the recovery of sensory and motor NCV.
METHODS: Thirty six healthy young subjects were randomly allocated into three groups: ice massage (n=12), ice pack (n=12) and cold water immersion (n=12). The modalities were applied to the right leg. The subjects of each modality group were again randomized to perform a post-cooling activity: a) 30min rest, b) walking 15 min followed by 15 min rest. The NCV of sural (sensory) and posterior tibial (motor) nerves was evaluated. Initial (pre-cooling) and final (30 min post-cooling) NCV were compared using a paired t-test. The effects of the modalities and the post-cooling activities on NCV were evaluated by an analysis of covariance. The significance level was α=0.05.
RESULTS: There was a significant difference between immersion and ice massage on final sensory NCV (p=0.009). Ice pack and ice massage showed similar effects (p>0.05). Walking accelerated the recovery of sensory and motor NCV, regardless of the modality previously applied (p<0.0001).
CONCLUSIONS: Cold water immersion was the most effective modality for maintaining reduced sensory nerve conduction after cooling. Walking after cooling, with any of the three modalities, enhances the recovery of sensory and motor NCV.

Keywords: cryotherapy; cold therapy; nerve conduction; cooling agents; sural nerve; tibial nerve.

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RESUMO

CONTEXTUALIZAÇÃO: Diferentes protocolos de crioterapia têm ação distinta nos parâmetros de condução neural sensorial e motora. No entanto, não se sabe como é o comportamento desses parâmetros no período pós-resfriamento e como o exercício físico realizado nesse período atuaria na recuperação da velocidade de condução nervosa (VCN).
OBJETIVOS: Comparar o efeito de três protocolos de crioterapia na VCN pós-resfriamento e analisar o efeito da marcha pós-resfriamento na recuperação da VCN sensorial e motora.
MÉTODOS: Trinta e seis sujeitos jovens e saudáveis foram alocados aleatoriamente em três grupos: criomassagem (n=12), pacote de gelo (n=12); imersão em água gelada (n=12). As modalidades foram aplicadas na perna direita. Os sujeitos de cada grupo foram novamente aleatorizados para realizar uma atividade pós-resfriamento: a) 30 min de repouso; b) 15 min de marcha seguidos de 15 min de repouso. Avaliou-se a VCN nos nervos sural (sensorial) e tibial posterior (motor). Comparações entre VCN inicial e final (30 min pós-resfriamento) foram realizadas com teste t de Student pareado. Os efeitos das modalidades e das atividades pós-resfriamento na VCN foram avaliados mediante análise de covariância. O nível de significância foi α=0,05.
RESULTADOS: Houve efeito diferente entre imersão e criomassagem na VCN sensorial final (p=0,009). Pacote de gelo e criomassagem apresentaram efeitos similares (p>0,05). A marcha acelerou a recuperação da VCN sensorial e motora, independente da modalidade previamente aplicada (p<0,0001).
CONCLUSÕES: Imersão em água gelada foi o procedimento mais eficaz para manter diminuída a condução nervosa sensorial após o resfriamento. A marcha pós-crioterapia, com qualquer um dos três protocolos, acelera a recuperação da VCN sensorial e motora.

Palavras-chave: crioterapia; terapia por frio; condução nervosa; agentes de resfriamento; nervo sural; nervo tibial.

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Introduction

Cryotherapy is a modality often used in clinical and sports environments for treating musculoskeletal injuries both in the acute phase and during rehabilitation. In the acute phase of the injury, the cryotherapy is used mainly to reduce metabolism, cellular hypoxia, pain and edema^1-6. During the rehabilitation phase, cryotherapy accelerates the process of tissue repair and reduces pain, facilitating the performance of therapeutic exercises and shortening the subject's functional recovery^1,3,4,6,7.

A reduction in tissue temperature is the primary effect of cryotherapy, which leads to other physiological changes such as a reduction in metabolic activity and nerve conduction velocity (NCV)^3,8. Several studies have analyzed the efficacy of cryotherapy modalities for reducing cutaneous^8-14, intramuscular^7,9,14-16 and articular¹⁷ temperature. Previous studies have identified that a crushed ice pack, ice massage and cold water immersion are the most effective modalities for inducing greater and faster cooling^9-12. Other studies^7,12,15have compared the efficacy of different modalities of cryotherapy in the maintenance of tissue cooling after the end of cryotherapy, i.e., during the rewarming period. Rewarming is understood as the recovery of a tissue temperature level similar to that of pre-cooling⁷. After cryotherapy the temperature of the skin recovers quickly¹², while intramuscular temperature remains reduced for some minutes¹⁵. In two of the above-mentioned studies^12,15, tissue rewarming was analyzed while the subjects were at rest.

More recently, the effects of exercise after cryotherapy on tissue rewarming have been analyzed. Myrer, Measom and Fellingham⁷ identified that moderate walking, when compared to rest, accelerates the rewarming of triceps surae muscle that had been previously cooled with a crushed ice pack.

A possible explanation for this result is that exercise increases metabolism, blood flow and heat production⁷. As a consequence, post-cryotherapy exercise could reduce the duration of other physiological effects of cooling such as a reduction in NCV.

There is a direct and linear relationship between tissue temperature and NCV^18-24. As a consequence, cooling causes a significant reduction in sensory and motor NCV^23-25. It is also known that the hypoalgesic effect of cryotherapy, evidenced by the increase in the threshold and tolerance of pain, is associated with a reduction in cooling- induced sensory NCV²⁴. In spite of the importance of NCV for hypoalgesic effects, few studies^23,25 have compared the efficacy of distinct modalities of cryotherapy for reducing neural conduction. A recent study by our group²⁵, which evaluated the immediate effects of ice pack, ice massage and cold water immersion on the NCV of sural and posterior tibial nerves, showed that the three modalities of cooling significantly reduced the NCV of both nerves. However, the sensory nervous fibers were most affected by cooling, and cold water immersion was the most effective modality for reducing NCV (mainly motor NCV), probably because it involved a greater area.

The literature on the late effects (post-cooling) of distinct modalities of cryotherapy on sensory and motor NCV is scarce. Consequently, it is unknown if the distinct modalities of cryotherapy are associated with differences in the recovery of basal levels (pre-cooling) of sensory and motor NCV. Furthermore, no study has analyzed the effect of exercise performed immediately after cooling on the recovery of NCV.

In light of the above-mentioned considerations, this study was developed to answer the following questions: a) Are distinct modalities of cryotherapy associated with differences in the recovery of basal levels (pre-cooling) of sensory and motor NCV? b) Does post-cooling exercise (walking) accelerate the recovery of NCV?

This information would be important for recommending different cryotherapy modalities to obtain therapeutic effects associated with reduced NCV, such as hypoalgesia. This type of study would have important clinical applications regarding therapeutic exercise performed after cryotherapy (cryokinetics)⁷ or in situations where the athlete returns to physical activity immediately after being treated with cryotherapy.

The objectives of the present study were to compare the effects of three modalities of cryotherapy (ice massage, ice pack and cold water immersion) on NCV recorded 30 min post-cooling and to analyze the effect of post-cooling physical exercise (walking) on sensory and motor NCV. Considering that cold water immersion is more efficient than other modalities for reducing NCV²⁵, as well as for keeping muscle cool during rewarming¹⁵, the hypothesis of this study was that cold water immersion would also be more effective for maintaining the changes in NCV during the post-cooling period than either ice massage or an ice pack. Moreover, considering that it has already been identified that post-cooling physical exercise accelerates muscular rewarming⁷, another hypothesis of the present study was that post-cooling walking would also accelerate the recovery of motor and sensory NCV.

Methods

An experimental study was conducted with 3 randomly assigned intervention groups (ice massage, ice pack and cold water immersion). For the post-cooling phase, the subjects from each intervention group were randomized again for one of the two post-cooling activity groups: a) 30 min of rest;

b) 15 min of walking followed by 15 min of rest (Figure 1). This post-cooling protocol is similar to the one used by Myrer, Measom and Fellingham⁷ to analyze the effects of exercise on muscular rewarming after cryotherapy. The independent variables analyzed were: modality of cooling, post-cooling activity and assessment time (pre-cooling and 30 min post-cooling). The dependent variables were motor and sensory NCV (m/s).

Subjects

This research project was approved by the Ethics Committee for Human Research of the Universidad Industrial de Santander, Bucaramanga, Santander, Colombia under protocol nº 18/2006. The subjects signed an informed consent form after having the experimental procedures, risks and benefits of the research explained to them. All the participants filled out a questionnaire on health aiming to determine the presence of some of the following exclusion criteria: BMI<18.5 or >24.9, history of alcoholism or smoking, cardiovascular or peripheral vascular disease, diabetes, neurological or musculoskeletal disease, recent trauma or loss of sensitivity, adverse reactions to cold, Raynaud's Phenomenon and pregnancy²⁵.

The calculation of the sample size for each intervention group was determined by the sampsi command in Stata9.0 according to the following criteria: α=0.05; (1-β)= 0.9; ratio 1:1. The calculation method was repeated measures analysis of covariance (ANCOVA), with one initial and other final measures and a correlation between the measures of r=0.2. This method defined a sample of 10-12 participants for each intervention group.

Thirty six healthy subjects (18 women and 18 men) were enrolled in this study. The mean±SD age was 20.5±1.9 years, mass 60.2±8.4 kg, height 1.63±0.1 m and BMI 22.4±1.6 kg/m².

Instruments

The nerve conduction studies were carried out with Nicolet Compass Meridian^TM (Nicolet Biomedical Company, USA) equipment.

The cooling modalities were chosen because they are considered the most effective for reducing tissue temperature^9-14,16,25. For ice massage, an 8×10×5 cm 279 g block of ice was used. The ice pack was an 18×8 cm vacuum-sealed plastic sac containing 279 g of ice. Immersion was carried out in a 20×35×30 cm acrylic tank containing water and ice with a temperature of approximately 10°C. The tank's temperature was measured throughout the intervention and presented initial and final means of 8.9±1.0 and 7.8±1.2°C, respectively. There was no change or addition of ice during any of the cryotherapy modalities.

Procedures

To minimize any circadian effects on body temperature, all experiments were performed between 2:00 pm and 6:00 pm. The subjects were allocated in the cooling and post-cooling activity groups by random computer sequencing²⁶. Considering that the post-cooling measurements had to be taken immediately after the administration of the modalities, the same room was used for all interventions and assessment procedures. Thus, the evaluator knew which intervention had been performed with each subject. Room temperature was maintained at 24±0.08°C without variation during the tests (p=0.29). The subjects were instructed to wear comfortable clothes during the experiment. The experimental protocol was developed in three phases: acclimation (15 min), cooling (15 min) and post-cooling (30 min) as shown in Figure 1.

Acclimation phase

During this phase, which lasted 15 min, the subjects rested in a prone position on a standard exam table. Meanwhile, the exact area to be cooled was determined and the electrodes for studying nerve conduction were attached. At the end of this phase, the NCV pre-cooling data were obtained (Figure 1).

Cooling phase

The cooling modalities were applied for 15 min on the right calf of each participant by a physical therapist trained for this activity. This specific length of application was chosen since it is commonly used in clinical practice and avoids adverse cryotherapy effects²⁷. The length of time allotted for participant adaptation to the cold was not considered before the experimental protocol. All participants completed their cooling protocol with no adverse reactions to the cold.

The procedures for determining the area for cooling treatment are detailed in a previous study ²⁵. In brief, for the ice massage and ice pack interventions, the subjects remained lying in a prone position and these modalities were applied to a rectangular area (18×8 cm) on the right calf; compression was not used during the administration of the ice pack. The ice massage was performed with continuous longitudinal displacement. For cold water immersion, the participants remained seated while immersing their leg in a tank to the upper edge of the rectangle that has been drawn for the previous modalities (Figure 2). At the end of the intervention, the leg was quickly dried without friction, and the participant returned to the prone position for post-cooling NCV measurements (Figure 1). These data have already been published recently²⁵ and were not considered in the analysis of the present study.

Post-cooling phase

In this phase, the subjects performed one of the randomly determined activities. Half of the subjects from each modality group (n=6) remained resting and lying prone on an exam table for 30 min. The other half (n=6) walked for 15 min and then rested for 15 min in the prone position. NCV was then reassessed at 30 min post-cooling (Figure 1). The walking exercise was carried out in a 9.45 m² area at a frequency of 90 steps/min, which was controlled by a metronome, i.e., the subjects stepped at each "click" of the device.

Nerve conduction studies

NCV was registered in the posterior tibial nerve (motor) and in the sural nerve (sensory) at the previously-mentioned times (Figure 1). These nerves were selected because they are located superficially within the treatment area and their recording techniques have been well described^25,28. Furthermore, the posterior tibial nerve has a high quantity of motor ûbers, and the sural nerve is a pure sensory nerve^18,28 allowing assessment of the cooling and post-cooling activity effects in both motor and sensory nerves.

All nerve conduction studies were performed by same experienced examiner. The good reliability of these recording techniques repeatedly administered by the same examiner has been previously established^25,29. Surface electrodes were used to stimulate and record nerve responses. In order to reduce technical variations between repeated measurements, the stimulation and recording sites were outlined with a waterproof marker during the pre-cooling measurement and the recording electrodes were not removed during the intervention, except for the participants who received cold water immersion. For this procedure, the recording electrodes were removed after the pre-cooling measurement and replaced at the sites previously marked for post-cooling measurements. To calculate the NCV, the peak latency of the negative wave²⁵ was determined.

The sural nerve recordings were obtained with a bandwidth of 20 Hz to 3 kHz, a gain of 20V/division, and a sweep speed of 1 ms/division. A surface recording bar electrode was placed immediately behind the lateral malleolus. The stimulating electrode was placed about 14 cm proximal to the active recording electrode, just lateral to the posterior midline of the calf²⁵. The stimuli were 100 µs rectangular pulses whose amplitude whose amplitude was adjusted slightly higher than necessary to ensure a maximum response. The nerve signals were obtained by averaging 20 responses.

The tibial motor nerve recordings were obtained with a bandwidth of 2 Hz to 10 kHz, a gain of 2mV/division, and a sweep speed of 2 ms/division. The active disc recording electrode was placed over the abductor hallucis muscle, and the reference disc recording electrode was placed at the base of the hallucis. The ground electrode was positioned on the calf muscle. The distal stimulation site was on the ankle immediately behind the medial malleolus, and the proximal stimulation site was at the popliteal fossa²⁵.

Statistical analysis

Descriptive statistics were used to summarize population characteristics and NCV data, which are presented as mean±SD³⁰. Baseline characteristics by intervention group were compared by analysis of variance (ANOVA) or the Χ2 test, depending of the measurement scale of each variable²⁶. NCV normality was determined by the Shapiro-Wilk test^26,30. The initially-recorded NCV and the 30 min post-cooling NCV were then compared for each post-cooling activity group with a paired t-test. The purpose of this comparison was to determine whether there was a complete recovery of NCV 30 min after cooling.

Finally, ANCOVA³¹ was performed to compare the effects of the three modalities and the post-cooling activities on the 30 min post-cooling NCV, adjusting for the NCV measured immediately after cooling. The group that received ice massage and rested after cooling was the reference group for assessing the modality effect. Stata9.0 was used for statistical analysis with a significance level of α=0.05

Results

There were no significant differences between participant characteristics in either the three modality groups or the post-cooling activity groups (p>0.05, Table 1).

Table 2 presents the results of the initial and final NCV (30 min post-cooling) comparisons. There was a significant difference between the initial and final NCV of the posterior tibial nerve in the groups that rested, regardless of the previously-used modality (p<0.01). The cold water immersion group that walked and rested also showed a significant difference (p=0.019).

Significant differences were observed between the initial and final NCV (30 min post-cooling) of the sensory nerve in all groups (p<0.03), except for the group that walked and then rested after having been treated with an ice pack (p=0.07). In general, greater magnitudes of difference were observed in the sensory nerve and in the groups that remained at rest (Table 2).

The ANCOVA showed a significant difference between the cold water immersion group and the group the received ice massage on the sural nerve 30 min post-cooling NCV (p=0.009, Table 3). This difference was not observed in the motor signals of the posterior tibial nerve (p=0.60, Table 3). There were no observed differences in effect between ice pack and ice massage on 30 min post-cooling NCV (P>0.05, Table 3). Regarding the effect of post-cooling activity on the recovery of motor and sensory NCV, it was observed that, compared to 30 min of rest, 15 min of walking followed by 15 min of rest accelerated the recovery of 30 min post-cooling NCV in both nerves (p<0.0001, Table 3). This effect was more evident in the sensory nerve, and the coefficient for the sural nerve was higher (β=7.12) than that determined for the posterior tibial motor nerve (β=3.99), although the 95% confidence intervals were not statistically different (Table 3).

Discussion

The results of the present study showed that, compared to only resting, the combination of post-cooling walking and resting accelerates the recovery of NCV in both sensory and motor nerves, regardless of the cooling modality used (Table 3). Moreover, cold water immersion was the most effective modality for maintaining decreased NCV 30 min after cooling, especially in the sensory nerve, which was observed in a previous study²⁵. These results confirm the hypotheses of this study.

In the literature reviewed, no previous studies were found that evaluated the effect of the post-cooling activity on NCV. However, considering the direct and linear relationship identified between tissue temperature and NCV^18-24, we can compare our results with the findings of Myrer, Measom and Fellingham⁷, who investigated the effect of exercise (10 min of walking on a treadmill at 5.63 km/h followed by 20 min of resting) on the recovery of intramuscular temperature after applying an ice pack for 20 min. The main finding of this study was that exercise accelerated muscle rewarming. It is known that exercise increases muscle metabolism, blood flow and the production of heat^7,32,33. Therefore, the subjects who exercised after cooling activated the physiological processes that induce a faster recovery of intramuscular temperature and, hence, NCV.

The immediate effect of cooling on NCV had been previously evaluated by our group, showing that sensory nerve fibers are more sensitive to cooling than motor fibers²⁵. The results of this study also show that the magnitude of differences between initial and final NCV (30 min post-cooling) in the sensory nerve was highest when the subjects remained at rest (Table 2). However, there were no significant differences in these variables in either nerve after the application of the three modalities (Table 2), which shows that, especially when subjects only rested, 30 minutes was not a sufficient period of time to fully recover the initial values of sensory and motor NCV.

Several studies^8,10-12 have compared the effectiveness of these modalities by measuring skin temperature, assuming that changes in skin temperature are closely related to subcutaneous and intramuscular temperature changes. However, it has also been reported that this assumption is not entirely correct since skin temperature does not adequately represent changes in deeper tissues or cooling efficiency; skin temperature decreases faster and at a greater magnitude than muscle temperature^34,35.

Our results support this assertion due to the different cooling effect observed in the two nerves situated at different depths. We consider that since the sensory nerve is located more superficially, its changes may be more associated with variations in skin temperature^9,15, while the observed changes in the NCV of motor nerve fibers, which are located more deeply, may be more associated with a reduction of intramuscular temperature.

Cold water immersion was significantly more effective in maintaining changes in sensory nerve NCV 30 min after cooling than the other modalities (Table 3). Moreover, the two groups treated with this modality showed differences between initial and final NCV, which shows that there was an incomplete recovery of sensory and motor NCV, regardless of post-treatment activity (Table 2). This result is consistent with the greater effectiveness of cold water immersion for reducing sensory and motor NCV immediately after cooling, which had been previously verified by Herrera et al.²⁵. The greater effectiveness of immersion for reducing and maintaining reductions in NCV for 30 min is probably due to the fact that this modality cools a larger area in comparison with the other two modalities, since almost the entire surface of the leg and foot are immersed.

The technique of cold water immersion presents another difference in relation to ice massage and ice packs in that it is the only modality applied with the lower limb aligned in opposition to the treatment. In the other modalities, the limb was positioned at the same level as the heart. Further studies are necessary to investigate the importance of the extremity's position on the effectiveness of cryotherapy modalities.

We believe that our results provide additional information for both scientific purposes and clinical practice regarding the selection and implementation of cryotherapy modalities. For example, the results show that when it is desired to keep decreasing the sensory and motor NCV by cryotherapy, the subject should remain at rest after the intervention. Cold water immersion, as used in this study, is the modality most recommended for maintaining the therapeutic effects of sensory nerve conduction changes, such as hypoalgesia. Our results also support the use of cryokinetics, since the three modalities were able to alter sensory conduction at levels recommended to produce hypoalgesia²⁵, which would allow the better performance of therapeutic exercise after cooling. However, such exercise limits the duration of the exercise hypoalgesic effect and requires either the repetition of cryotherapy or the use of another modality after exercise to increase the hypoalgesic effect.

Finally, it is important to point out that a continued decrease in NCV (30 min post-cooling), mainly in resting conditions and without adequate supervision, involves a possible risk of nerve damage in areas where the nerve passes superficially. The literature has shown cases of neuropathy due to the application of cryotherapy along the course of more superficial peripheral nerves^27,36.

When analyzing the present study's results, some methodological limitations deserve consideration: the ice massage and ice pack cooling area was smaller than that of cold water immersion; the study population was composed of young and healthy subjects, and it is possible that cooling causes different effects in elderly and medically compromised subjects; the fact that the examiner was aware of the modality used in each group could affect the internal validity of the study; and the absence of another NCV evaluation performed immediately after walking (in the walking/resting group) did not allow verification of whether the subsequent 15 min of rest masked larger effects of walking on NCV recovery.

Conclusion

Walking after cooling accelerated the recovery of sensory and motor nerve conduction. Cold water immersion, as administered, was the most effective modality for maintaining reduced sensory nerve conduction.

Acknowledgments

To the Coordenação de Aperfeiçoamento do Pessoal de Nível Superior (Capes, Brasil) for doctorate funding and to the Universidad Industrial de Santander for financing this research.

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Muscular activity of patella and hip stabilizers of healthy subjects during squat exercises

Muscular activity of patella and hip stabilizers of healthy subjects during squat exercises

Lilian R. Felício^I; Luiza A. Dias^II; Ana P. M. C. Silva^II; Anamaria S. Oliveira^III; Débora Bevilaqua-Grossi^III

^IPostgraduate Program of Health Science Applied of Locomotor Apparatus, School of Medicine from Ribeirão Preto (FMRP), Universidade de São Paulo (USP), Ribeirão Preto, SP, Brazil
^IICourse of Physical Therapy, FMRP, USP
^IIIDepartment of Biomechanics, Medicine and Rehabilitation of the Locomotor System, FMRP, USP

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ABSTRACT

BACKGROUND: Hip and knee muscle weaknesses have been associated with the onset of anterior knee pain (AKP). Therefore, the understanding of how squats exercises can be performed in order to optimize the electrical activity of these muscles is relevant for physical therapy treatments.
OBJECTIVE: To compare the electromyographic activity of patella and pelvic stabilizers during traditional squat and squat associated with isometric hip adduction or abduction in subjects without AKP.
METHODS: Electromyography signals were captured using double-differential electrodes at the vastus medialis obliquus (VMO), vastus lateralis obliquus (VLO), vastus lateralis longus (VLL) and gluteus medium (GMed) in 15 healthy and sedentary women during squats exercises: traditional and associated with hip adduction and hip abduction with load of 25% of body weight. Linear mixed models with significance level of 5% were used for data analysis.
RESULTS: Squat associated with hip adduction and abduction produced electromyographic activity of GMed of 0.47 (0.2) and 0.59 (0.22) respectively, while conventional squat produced an electromyiographic activity of 0.33 (0.27). The higher VMO activity was 0.59 (0.27) during the isometric contraction in the squat associated with hip adduction. The higher VLO activity was 0.60 (0.32) during isometric contraction in the squat associated with hip abduction.
CONCLUSION: Squat exercise associated with hip adduction increased VMO muscle activity as well as the activity of GMed activity.

Keywords: exercise therapy; kinesiology; electromyography; knee; hip.

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Introduction

Squat exercises are often prescribed in physiotherapy practice for several knee impairments because when properly administered, it promotes an increase in knee and pelvic muscles strenght^1-3. In addition, this exercise in closed kinetic chain is an integral part of functional activities and these exercises are often related with pain in patient with anterior knee pain (AKP) such as sport practices and going up and down stairs¹.

Exercises in closed kinetic chain associated to isometric contractions of hip abductors generate a higher electrical activation of the gluteus medium muscle (GMed) in healthy subjects when compared to the exercises done in opened kinetic chain. Additionally, the bipodal squat produces a better pelvic stabilization when compared to the unipodal squat⁴. Furthermore, although the associations of isometric hip adduction and abduction have been reported to produce an increased activity of GMed during bipodal squats, the same has been found not to be true when considering unipodal squats.

The squat with the association of isometric contraction of hip adduction has been shown to promote values of electromyographic amplitude similar for the medial and lateral portions of the quadriceps. Therefore, this squat modality promotes a better balance of the patellofemoral joint in comparison to the conventional squat (CS)⁶. However, these studies⁶ did not evaluate the pelvic musculature.

Understanding how squats can be performed in order to promote a higher activation of patella and hip stabilizers is relevant because in addition to the dynamic stability of the patella, weaknesses of pelvic stabilizer are related to patellofemoral dysfunction^7-11.

There is no description in the literature regarding the most efficient way to perform squat exercises in order to promote balanced activation of the dynamic stabilizers of the patella and a higher electrical activity of the pelvic stabilizers. This information will help provide scientific basis and justification for the prescription of squat exercise for patients with AKP or patellofemoral dysfunction.

In this context, the purpose of the present study was to compare the electromyographyc activity of the patella and hip stabilizers between the positions of conventional squat and squats associated with isometric contraction of hip adduction and abduction in subjects with no complaint of AKP. The hypothesis of the present study is that squat associated with isometric contractions of hip abduction generates an increase in the electromyographic activity of the patella stabilizers when compared to the conventional squats and squats with hip adduction.

Methods

Fifteen sedentary women with no AKP complain were recruited through verbal invitation and participated in this study. Inclusion criteria were women that presented with a maximum of two clinical signals of misalignment in the lower limb¹², with no complains of AKP¹³, and no history of orthopedic or neurological conditions, trauma or previous surgery of bones, muscles and joints of the lower limb or spine, since pain is the main complain associated to AKP. Exclusion criteria was complain of pain in any part of the lower limb and performance of any type of physical activity, recreational or sportive, twice or more frequently per week⁶.

All of the participants were properly informed about the study procedures and signed a free informed consent approved by the Ethics Research Committee of the Clinical Hospital of the Medical School of Ribeirão Preto, Ribeirão Preto, SP, Brazil (protocol nº. HCFMRP 14102/2006).

The surface electromygraphic signals were collected bilaterally from eight double-differentials active electrodes with three Ag/AgCl bars (dimensions 23x21x5 mm and distance between electrodes of 10 mm), with gain of 20x, input impedance of 10GΩ and band-pass filter and the common mode rejection ratio of the 130dB. The active electrodes were positioned on the vastus medialis obliquus (VMO), vastus lateralis obliquus (VLO), vastus lateralis longus (VLL) (Figure 1A)¹⁴ and GMed (Figure 1B)¹⁵. They were fixed with a double-sided adhesive tape to the skin previously prepared and the connections were tested according to the rules of the Surface EMG for Non Invasive Assessment of Muscles Project¹⁵. The stainless steel ground electrode (diameter of 3 cm) was fixed to the sternum.

The signals were analogically amplified and digitalized with simultaneous frequency of sampling of 2 KHz by channel, in the range of 0.01-1.5 kHz, by the convertor board of 16 bits of resolution of dynamic range from the portable device Myosystem BR-1P84, from the brand Datahominis (Uberlândia, Minas Gerais, Brazil). TheMyosystem Program, version 3.5, was used for visualizing and processing the electromyographic signal.

The electromygraphic signals of the VMO, VLO and VL were collected during three maximal isometric voluntary contractions (MIVC) of shank extension, with the knee fixed at 90° of flexion (extensor chair), since this position facilitates a higher electrical activity of the quadriceps muscles¹. The MIVC of the GMed was collected in the manual muscle testing position¹⁶; with the hips in 20º of abduction and 10º of extension. Pelvic stabilization and the resistance imputed to the distal portion of the leg were applied manually by the same evaluator¹⁷. The MIVC of these activities were maintained for six seconds, and were later used as reference values for normalization of the electromygraphic data obtained in the squat exercises studied.

All isometric positions of squats were performed with an additional load of 25% of each subject body weight. This additional load was determined by trial and error, in a pilot study. This load was identified as the minimal capable load to intensify the myoelectric activity, especially of the muscle GMed, to an acceptable level of signal-noise relation using double-differential electrodes^9,14.

The electromygraphic data of the CS was collected with the participants with their back supported on a ball of 45 cm diameter, of the brand Carci^®, and maintaining it against a wall, with 60° of knee flexion¹⁸, feet apart and hips in neutral position of the frontal and transversal planes (Figure 2A). The squat exercises associated to the MIVC of hip adduction (CS-ADD)⁶ were performed in the same position of the CS a support positioned between the legs, in the height of the medial femoral epicondyle (Figure 2B). The squat exercises with hip abduction (CS-ABD) were performed on the same position as the CS with addition of MIVC of hip abduction resisted by an non elastic band, adjustable with Velcro^®, positioned leveled with lateral femoral epicondyle (Figure 2C). Pelvic movements in transversal and frontal planes were visually controlled by the evaluators. The squat contractions were recorded in isometric position to guarantee that the electromygraphic surfaces were not affected by the variations in tension-length and tension-velocity relation or even by the number of motor units active in the area of caption¹⁹.

The sequences of the exercises were determined by a simple draw and were recorded for six seconds of three contractions for each squats condition. All participants were verbally motivated during the contractions by the same examiner. A minimal resting time of two minutes between each contraction was established to minimize the effects of muscle fatigue²⁰.

The raw electromyographic signals were digitally filtered in the band of 20 to 500 Hz, and the root square of the mean squares (RMS, root mean square) was calculated to represent the amplitude of muscle activation.

The mean value of RMS of each muscle was normalized by the mean value of the RMS obtained in the contractions of reference of the same muscle²¹. In other words the RMS was normalized by the relation between the mean value of the studied contractions and the mean value obtained from the recordings of MIVCs. Thus, the values of amplitude of myoelectric activation are presented in arbitrary unit (AU). The muscle activity was characterized as minimal (between 0 and 0.39), moderate (between 0.40 and 0.74) and strong (between 0.75 and 1)²².

Means and standard-deviations of the RMS normalized values were used to verify statistically significant differences between the dominant and non-dominant sides and between the different squat conditions. Mixed linear model²³ is a test of variance and was used in this study as it takes into account both the source of variations intra- and inter-subjects. This statistical method is recommended when the values of the same subject are grouped, and the assumption of independence between the observations in the group is not adequate²³. The random effect was considered as being the muscles assessed, VMO, VLO, VLL and GMed, and the fixed effect was considered as being the exercises, CS, CS-ABD and CS- ADD.

The adjustment of the model for a normal distribution was done through the procedure PROC MIXED uinsg SAS^®9.0.

Results

Demographic data and clinical parameters of sedentary women are presented on Table 1.

There were no statistical significant differences between the values of muscle activation of dominant and non dominant lower limbs. The associations both of hip adduction and abduction favored the activation of the muscle GMed (Table 2) in relation to the CS (p<0.05). In relation to the patellar stabilizers, the results showed that the VMO was more active in the squat associated with hip adduction in relation to the other squats tested (p<0.05). The VLL muscle, presented a higher electrical activity in the squat with hip adduction and abduction when compared to the CS (p<0.05) (Table 2). The comparison between the electromyographyic activities of the stabilizers of the patella did not show statistically significant differences.

Discussion

The results of the present study revealed that the muscle activation produced by the proposed squats ranged between 26 and 60% of the activation achieved in the reference contractions, that were actually considered to be from weak to moderate²². The muscle GMed showed higher electrical activity in the squat with hip abduction or adduction when compared to conventional squat, which produced similar muscle activation for all of the muscles studied.

It is worth noting that even with the addition of a load equal to 25% of the body weight and the association of hip abduction or adduction the activation of the GMed in squat exercises were at most 59% of the amplitude generated at the reference position. Thus, when a muscle weakness is evidenced in the clinical assessment of patients, we must consider that the squat exercise, as proposed in this study may not be enough to improve the strength of these muscle and therefore, specific exercises may be included in the protocol.

Unlike the initial hypothesis, both the squat with hip adduction and the squat with hip abduction produced moderate activations that were larger than those achieved with the CS for the patella and pelvic stabilizer. However, despite all the squats presenting with balanced activity of the patella stabilizer muscles, the squat with hip adduction provided a larger electrical activity of the VMO compared to the CS-ABD. The contraction of GMed in these situations is due, probably, to its function as pelvic stabilizer and to the control of the internal rotation of the femur^24-26. These data agree with the findings of Hertel et al.⁵ that found that the addition of isometric contraction of hip adduction and abduction to unipodal squat have no effect on the electrical activity of GMed. However, despite the similarities of the result, the experimental conditions of the studies were different since in the present study volunteers kept both feet on the ground, had the back supported by a ball and had an added load of 25% of the body weight.

In addition to finding a moderate activation of GMed in squat contractions with hip adduction and abduction, the squat contraction with hip adduction provided greater activation of the electric VMO muscle, which are desirable activations in the rehabilitation of meniscal²⁷ and ligament²⁸ of the knee and in the AKP^29,30.

Moreover, the results of this study revealed that squat with hip abduction stimulated the activation of the GMed but also provided higher activity of the VLL. This greater activation of the VLL should not be advocated in the intervention of patellar dislocations and patellofemoral dysfunctions, since it could favor the lateralization of the patella¹.

Coqueiro et al.⁶ reported that the prescription of exercises that promote muscle synergism of the patella lateral stabilizer musculature are as important as promoting the contraction of the medial portion of the quadriceps. Our data do not differ with regards to the activation of GMed and indicate a balanced activity between the stabilizers of the patella in the exercises CS-ADD and CS-ABD, but the squat exercise associated with adduction of the hip showed an increase in the myoelectric activity of the muscle VMO. It is suggested, therefore, that this exercise is the most suitable in the rehabilitation of patients with AKP, since it emphasizes the GMed activation and the activity of VMO.

The results of this study are limited by the lack of information about the kinematics of the pelvis and lower limb segments and the exact change of the patella positioning caused by the muscle contractions proposed. Another aspect that was not addressed is the relationship between the muscle tensor fasciae latae and its function of pelvic stabilizer together with the hip abductors muscles. Furthermore, the tensor fasciae latae muscle is an anterior-lateral stabilizer of the knee, and a weakness in this musculature can lead to increased shear forces and hence an increase in patellofemoral stress³¹.

Finally, it is important to consider that this is an exploratory study and its results, as the variance of the average EMG amplitude, can be used as a basis for further studies that seek to replicate this method with a larger number of participants, as well as with AKP patients, highlighting the therapeutic value of these exercises.

Conclusion

The results of this study showed that the squat exercise associated with hip adduction produced higher activation of the VMO muscle, and produced an increase in the activity of the GMed.

Acknowledgements

To the Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP (process number 2007/08461-6), for the financial support, and to the Center of Quantitative Methods- CEMEQ/Clinical Hospital, FMRP, for the statistical analysis

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