Evaluation of grip strength in normal and obese Wistar rats submitted to swimming with overload after median nerve compression Laboratory of Endocrine Physiology and Metabolism; Laboratory for the Study of Injuries and Physical Therapy Resources, Universidade Estadual do Oeste do Paraná.

Josinéia Gresele Coradinia Camila Mayumi Martin Kakihata Regina Inês Kunz Tatiane Kamada Errero Maria Lúcia Bonfleur Gladson Ricardo Flor Bertolini About the authors

Abstracts

Objetivo

Verificar a funcionalidade por meio da força muscular de preensão em animais com obesidade induzida por glutamato monossódico (MSG) e animais controle, que sofreram compressão do nervo mediano direito, tendo como tratamento a natação com carga.

Métodos

Ratos Wistar neonatos durante os primeiros cinco dias de vida receberam injeções subcutâneas de MSG. O grupo controle recebeu solução salina hiperosmótica. Quarenta e oito ratos foram divididos em seis grupos: G1(controle); G2 (controle com lesão); G3 (controle com lesão + natação); G4 (obesos); G5 (obesos com lesão); G6 (obesos com lesão + natação). Os animais dos grupos G2, G3, G5 e G6 foram submetidos à compressão do nervo mediano e os dos grupos G3 e G6 foram tratados, após a lesão, com exercício de natação com carga durante três semanas. A natação teve duração progressiva conforme as semanas, de 20, 30 e 40 minutos. A força muscular foi avaliada por meio de um medidor de força de preensão no pré-operatório, no terceiro, sétimo, 14° e 21° dia pós-operatório. Os resultados foram expressos e analisados por estatística descritiva e inferencial.

Resultados

Quando comparada a força de preensão entre as avaliações, indiferentemente de grupos, na segunda avaliação os animais apresentaram menor força de preensão. Os grupos G1 e G4 apresentaram força de preensão maior, em comparação com os grupos G2, G3, G4 e G6.

Conclusão

O exercício de natação com sobrecarga não foi eficaz em promover melhoria na força muscular de preensão após lesão de compressão do nervo mediano direito em ratos controle e obesos-MSG.

Força muscular; Compressão nervosa; Obesidade; Natação


Objective

To verify the functionality through muscle grip strength in animals with obesity induced by monosodium glutamate (MSG) and in control animals, which suffered compression of the right median nerve, and treated with swimming with overload.

Methods

During the first five days of life, neonatal Wistar rats received subcutaneous injections of MSG. The control group received a hypertonic saline solution. Forty-eight rats were divided into six groups: G1 (control); G2 (control + injury); G3 (control + injury + swimming); G4 (obese); G5 (obese + injury); and G6 (obese + injury + swimming). The animals in groups G2, G3, G5 and G6 were submitted to compression of the median nerve and G3 and G6 groups were treated, after injury, with swimming exercise with load for three weeks. The swimming exercise had a progressive duration, according to the week, of 20, 30 and 40 min. Muscle strength was assessed using a grip strength meter preoperatively and on the 3rd, 7th, 14th and 21st days after surgery. The results were expressed and analyzed using descriptive and inferential statistics.

Results

When the grip strength was compared among assessments regardless of group, in the second assessment the animals exhibited lower grip strength. G1 and G4 groups had greater grip strength, compared to G2, G3, G4 and G6.

Conclusion

The swimming exercise with overload has not been effective in promoting improvement in muscle grip strength after compression injury of the right median nerve in control and in obese-MSG rats.

Muscle strength; Nerve compression; Obesity; Swimming


Introduction

Peripheral nerve lesions are commonly encountered in the clinical practice of physiotherapy, especially traumatic injuries such as crushing, compression or stretching, resulting in functional impairment, caused by the interruption in the proper transmission of nerve impulse.1Cavalcante VEV, Montenegro EJN, Pontes Filho NT de. Efeito da eletroestimulacão no músculo desnervado de animais: revisão sistemática. Fisioter Mov. 2012;25:669-78.,2Stafford MA, Peng P, Hill DA. Sciatica: a review of history, epidemiology, pathogenesis, and the role of epidural steroid injection in management. Br J Anaesth. 2007;99:461-73. The interruption of the nerve supply leads to a decreased muscle activity, causing muscular atrophy, and the main effect of this atrophy is the reduction of the area and diameter of the muscle fiber and consequent reduction in its strength.1Cavalcante VEV, Montenegro EJN, Pontes Filho NT de. Efeito da eletroestimulacão no músculo desnervado de animais: revisão sistemática. Fisioter Mov. 2012;25:669-78. Axons of injured peripheral nerves have the capacity to regenerate; however, this process is slow and the functional recovery is usually not complete.3Gordon T. The role of neurotrophic factors in nerve regeneration. Neurosurg Focus. 2009;26:E3. Studies involving disorders in peripheral nerves and obesity can be found in the literature;4Miscio G, Guastamacchia G, Brunani A, Priano L, Baudo S, Mauro A. Obesity and peripheral neuropathy risk: a dangerous liaison. J Peripher Nerv Syst. 2005;10:354-8.,5Ylitalo KR, Herman WH, Harlow SD. Serial anthropometry predicts peripheral nerve dysfunction in a community cohort. Diabetes Metab Res Rev. 2013;29:145-51. however, the approach of conservative treatment for peripheral nerve injury in obese subjects is still scarce.

Physical therapy seeks to repair the consequences of peripheral nerve injury, restoring functionality to the individual. The treatment can be performed by various therapeutic approaches, such as passive and active cinesiotherapy, electrotherapy, functional skills training, specific proprioceptive neuromuscular facilitation techniques and therapeutic exercise.

Animal studies demonstrate the efficacy of exercise on peripheral nerve regeneration.6Ilha J, Araujo RT, Malysz T, Hermel EES, Rigon P, Xavier LL, et al. Endurance and resistance exercise training programs elicit specific effects on sciatic nerve regeneration after experimental traumatic lesion in rats. Neurorehabil Neural Repair. 2008;22:355-66.,7Teodori RM, Betini J, Oliveira LS de, Sobral LL, Takeda SYM, Montebelo MI, et al. Swimming exercise in the acute or late phase after sciatic nerve crush accelerates nerve regeneration. Neural Plast. 2011;2011:8. The exercise practice promotes recovery of contractile and metabolic properties of muscle after denervation,8Tanaka S, Tsubaki A, Tachino K. Effect of exercise training after partial denervation in rat soleus muscles. J Phys Ther Sci. 2005;17:97-101. helps removing degenerated myelin and subsequent synthesis,9Sarikcioglu L, Oguz N. Exercise training and axonal regeneration after sciatic nerve injury. Int J Neurosci. 2001;109:173-7. aids in axonal diameter recovery1010 Oliveira LS, Sobral LL, Takeda SYM, Betini J, Guirro RRJ, Somazz MC, et al. Estimulación eléctrica y natación en la fase aguda de la axonotmesis: influencia sobre la regeneración nerviosa y la recuperación funcional. Rev Neurol. 2008;47:11-5. and axonal sprouting, favors the regeneration of injured nerves and functional recovery1111 Seo TB, Han IS, Yoon J-H, Hong K-E, Yoon S-J, Namgung UK. Involvement of Cdc2 in axonal regeneration enhanced by exercise training in rats. Med Sci Sport Exerc. 2006;38: 1267-76. and also increases the expression of nerve growth factors such as BDNF and NGF, stimulating the growth and development of new cells.1212 Dishman RK, Berthoud H-R, Booth FW, Cotman CW, Edgerton VR, Fleshner MR, et al. Neurobiology of exercise. Obesity. 2006;14:345-56. The physiological effects of exercise in the aquatic environment provide benefits to the cardiovascular, skeletal, muscular and nervous systems, increasing the tissue repair process.1313 Medeiros A, Oliveira EM, Gianolla R, Casarini DE, Negrão CE, Brum PC. Swimming training increases cardiac vagal activity and induces cardiac hypertrophy in rats. Br J Med Biol Res. 2004;37:1909-17. However, Oliveira et al.,1010 Oliveira LS, Sobral LL, Takeda SYM, Betini J, Guirro RRJ, Somazz MC, et al. Estimulación eléctrica y natación en la fase aguda de la axonotmesis: influencia sobre la regeneración nerviosa y la recuperación funcional. Rev Neurol. 2008;47:11-5. despite observing improvements in axonal diameter, report that the swimming practice did not affect the maturation of regenerated nerve fibers or their functionality, and when associated with electrical stimulation, delayed functional recovery. These findings disagree with what was observed by Teodori et al.,7Teodori RM, Betini J, Oliveira LS de, Sobral LL, Takeda SYM, Montebelo MI, et al. Swimming exercise in the acute or late phase after sciatic nerve crush accelerates nerve regeneration. Neural Plast. 2011;2011:8. who observed a significant effect of swimming exercise, with acceleration of nerve regeneration in post-axonotmesis of sciatic nerves of rats.

One way to evaluate the functionality of the individual is by the measurement of muscle strength, which enables a functional diagnosis by an evaluation of improvement or worsening during treatment, and as a predictive or prognostic measure.1414 Ferreira ACC, Shimano AC, Mazzer N, Barbieri CH, Elui VMC, Fonseca MCR. Grip and pinch strength in healthy children and adolescents. Acta Ortop Bras. 2011;19:92-7. In this context, the aim of this study was to assess the muscle grip strength in MSG-obese and in control animals, which suffered compression of the right median nerve and underwent swimming with load.

Materials and methods

Characterization of the study and sample

This is an experimental research approved by the Ethics Committee on Animal Experimentation and Practical Classes – CEEAAP, Universidade Estadual do Oeste do Paraná, under protocol number 01712.

Neonatal Wistar rats during the first five days of age received subcutaneous injections of monosodium glutamate (MSG) in a concentration of 4 g/kg body weight/day, forming the obese group. The control group received a hyperosmotic saline solution at a concentration of 1.25 g/kg body weight/day.1515 Balbo SL, Gravena C, Bonfleur ML, Mathias PC, de F. Insulin secretion and acetylcholinesterase activity in monosodium L-glutamate-induced obese mice. Horm Res. 2000;54:186-91. The animals were kept in a light/dark photoperiod of 12 h and at a temperature of 23 ± 2 °C, with food and water ad libitum.

At 68 days of life, 48 rats were divided into six experimental groups: G1 (control); G2 (control + injury); G3 (control + injury + swimming); G4 (MSG); G5 (MSG + injury); and G6 (MSG + injury + swimming). At 73 ± 4 days of life, the animals in groups G2, G3, G5 and G6 underwent surgery for median nerve compression.

Nerve compression

The compression of the right median nerve was based on the model presented by Chen et al.,1616 Chen J, Lue J, Lin L, Huang C, Chiang RP, Chen C, et al. Effects of pre-emptive drug treatment on astrocyte activation in the cuneate nucleus following rat median nerve injury. Pain. 2010;148:158-66. with nerve tie-down using 4.0 chromic catgut in 4 points, with an approximate distance of 1 mm in the median nerve, proximal to the elbow. To perform the surgical procedure for compression of the median nerve, the animals were anesthetized with ketamine hydrochloride solution (50 mg/kg) and xylazine (10 mg/kg).

Swimming

Five days prior to the surgery, the animals were adapted and trained in a gradual manner to swim, wherein in the first three days the rats swam for 15 min with an overload of 5% of body weight; in the following two days, they swam 20 min with an overload of 10% of body weight. The swimming exercise was held in an oval tank made of strong plastic material (200 l capacity, 60 cm deep) and containing water maintained at a controlled temperature of 32 ± 1 °C. The treatment began on the third day postoperatively; the exercises were performed once a day, five times a week, totaling 15 days of swimming. The animals were weighed every day for weight control and adjustment of their loads for the swimming exercise. In the first week, G3 and G6 groups started with 20 min of exercise; during the second week, 30 min; and in the third week, 40 min. In all practices, the animals supported a load of 10% of body weight. The other groups of animals were placed in water for 1 min.

Muscle strength

For muscle strength assessment, one grip strength meter described by Bertelli and Mira1717 Bertelli JA, Mira JC. The grasping test: a simple behavioral method assessment of peripheral nerve regeneration in the rat. J Neurosci Methods. 1995;58:151-5. was used. This assessment is a useful tool for analyzing the recovery of median nerve lesions, through the function of the flexor digitorum muscle. To perform the evaluation, the animal was pulled by the tail with increasing force. The rat could seize a grid attached to a force transducer, till the animal lost its grip. The anterior left limb was temporarily immobilized by wrapping with tape. Five days prior to surgery, the animals were adapted and trained on the equipment. The first evaluation (AV1) was performed before the compression of the median nerve, to obtain baseline values, i.e., preoperatively, followed by a second assessment on the 3rd postoperative day (AV2). The other assessments were carried out at the end of each week of treatment, i.e., the 7th (AV3), 14th (AV4) and 21st (AV5) day, with the aim to observe the evolution of the lesion and the type of treatment used. In each evaluation the test was repeated three times, and the mean value of repetitions was used.

Statistical analysis

The results were expressed and analyzed using descriptive and inferential statistics. To compare groups and times, one-way ANOVA with Tukey post-test was used, with a significance level of 5%.

Results

Both G1 and G4 showed no intragroup variations (P > 0.05), which was expected, since in these groups injuries were not inflicted. For the other groups, the values of AV1 were superior to the other assessments (P < 0.05), whereas G2 and G6 showed significant increases in AV4, when compared to AV2 (P < 0.05); the same was observed for G2, G3 and G6, when comparing AV5 versus AV2 (P < 0.05) (Table 1).

Table 1
Values found for handgrip of Wistar rats (mean and standard deviation), in grams, for different time points (AV1–AV5) in the different groups (G1–G6).

As for the comparison among groups, in AV1 (the pre-injury time) there were no significant differences (P > 0.05). However, from AV2 to AV5, differences between G1 versus G2, G3, G5 and G6 (P < 0.05) groups were observed, occurring the same with respect to G4 (Table 1), i.e., the values found revealed that the lesion reduced the grip strength, when comparing control groups (G1 and G4) with those which only underwent injury (G2 and G5), or those which underwent injury associated with swimming (G3 and G6). No significant differences were noted among groups of obese animals compared to eutrophic animals.

Discussion

Peripheral nerve injuries are responsible for high morbidity and functional loss, requiring therapeutic interventions1818 Taylor CA, Braza D, Rice JB, Dillingham T. The incidence of peripheral nerve injury in extremity trauma. Am J Phys Med Rehabil. 2008;87:381-5. to assist in the morphological and functional tissue repair, hence the importance of controlled experiments to evaluate the effectiveness of therapies. Most of the experimental studies in rats are carried out on models of sciatic nerve injury/compression. However, the most common injuries in humans occur in the upper limbs.1919 Daneyemez M, Solmaz I, Izci Y.Prognostic factors for the surgical management of peripheral nerve lesions. Tohoku J Exp Med. 2005;205:269-75. Thus, in the present study, we sought to find a model that could produce a compressive lesion in the median nerve. The nerve compression model used was presented by Bennett and Xie2020 Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 1988;33:87-107. for compressing the sciatic nerve; subsequently, the procedure was modified for the median nerve by Chen et al.,1616 Chen J, Lue J, Lin L, Huang C, Chiang RP, Chen C, et al. Effects of pre-emptive drug treatment on astrocyte activation in the cuneate nucleus following rat median nerve injury. Pain. 2010;148:158-66. which causes, besides hypernociception, muscle activity dysfunction. These changes begin from the 2nd day postoperatively (PO), reaching its maximum around the 10th to 14th PO day, disappearing after the 2nd month. Thus, in the present study, we began the treatment with swimming exercise in the 3rd PO, during which the changes arising from nerve compression had already been established. It was realized that the aquatic exercise could be important in recovering from paresis, both by decreasing the protein degradation2121 Lee Y, Kim J-H, Hong Y,Lee S-R, Chang KT, Hong Y. Prophylactic effects of swimming exercise on autophagy-induced muscle atrophy in diabetic rats. Lab Anim Res. 2012;28:171-9. and by functioning as a possible analgesia mediated by endogenous opioids,2222 Bertolini GRF, Rosa CT, Silva LI, Meireles A, Rocha BP. Uso do exercício resistido antagonizado por naloxone como fator de analgesia em sinovite aguda de joelho de ratos Wistar. Rev Bras Med Esporte. 2012;18:126-9. which could reduce the immobility of the limb due to pain.

When a peripheral nerve suffers compression (inducing local ischemia), some electrophysiological nerve conduction change occurs,2323 Ikemoto T, Tani T, Taniguchi S, Ikeuchi M, Kimura J. Effects of experimental focal compression on excitability of human median motor axons. Clin Neurophysiol. 2009;120:342-7. leading to muscle weakness.2424 Singh R, Singh Z, Bala R, Rana P Singh S. An unusual case of sciatic neuropraxia due to melorheostosis. J Bone Spine. 2010;77:614-5.,2525 Haflah NHM, Rashid AHA, Sapuan J. Partial anterior interosseous nerve palsy: isolated neuropraxia of the branch to flexor pollicis longus. Hand Surg. 2010;15:221-3. The results show that, at the first assessment (when the nerve compression had not yet been performed), the animals showed a significantly higher strength compared with the other results – which is consistent with normal standards. A reduction in muscle strength may be related to the hypernociception generated by nerve compression, producing muscle inhibition.2626 Yahia A, Ghroubi S, Kharrat O, Jribi S, Elleuch M, Elleuch MH. A study of isokinetic trunk and knee muscle strength in patients with chronic sciatica. Ann Phys Rehabil Med. 2010;53:239-49. Silva et al.2727 Silva LI, Meireles A, Rosa CT, Bertolini GRF. Avaliacão da dor em modelo experimental de compressão de nervo mediano em ratos. FIE Bull. 2014;81:565-8. warned that, after the surgical compression of the median nerve, a painful condition settles down, lasting at least until the 8th postoperative day, not decreasing in its intensity.

The results also revealed that there was no increase in grip strength in injured/swimming-treated animals versus injured/sedentary animals, suggesting that the swimming exercise was not efficient to produce an increase in muscle strength, after the injury by compression of the median nerve. In a study by Possamai, Siepko and Andrew,2828 Possamai F, Siepko CM, André ES. Investigacão dos efeitos do exercício terapêutico sobre a regeneracão nervosa periférica. Acta Fisiatr. 2010;17(4):142-7. 40 Wistar rats were functional and histologically evaluated, being divided into four groups according to the day the treatment would begin after an axonotmesis-type sciatic nerve injury. The animals were submitted to freestyle swimming for 30 min/day. The results show that there was no interference of physical exercise on peripheral nerve regeneration. Additionally, the treated groups showed no histological changes compared to sedentary rats. Accordingly, Oliveira et al.1010 Oliveira LS, Sobral LL, Takeda SYM, Betini J, Guirro RRJ, Somazz MC, et al. Estimulación eléctrica y natación en la fase aguda de la axonotmesis: influencia sobre la regeneración nerviosa y la recuperación funcional. Rev Neurol. 2008;47:11-5. noted that daily swimming exercise for 30 min, 5 times a week for 22 days, was ineffective with respect to nerve recovery in rats subjected to axonotmesis; when this was combined with electrical stimulation, the functional recovery was delayed. On the other hand, Teodori et al.,7Teodori RM, Betini J, Oliveira LS de, Sobral LL, Takeda SYM, Montebelo MI, et al. Swimming exercise in the acute or late phase after sciatic nerve crush accelerates nerve regeneration. Neural Plast. 2011;2011:8. evaluating functional and morphological characteristics of rats with sciatic axonotmesis, found that 30 min/day of swimming for two weeks accelerated nerve regeneration. Thus, a disagreement regarding the effects of exercise on aquatic recovery from nerve injury becomes evident.

This divergence is also found in the case of exercise outside the aquatic environment. Sobral et al.2929 Sobral LL, Oliveira LS, Takeda SYM, Somazz MC, Montebelo MIL, Teodori RM. Exercício imediato versus tardio na regeneracão do nervo isquiático de ratos após axoniotmese: análise histomorfométrica e funcional. Rev Bras Fisioter. 2008;12:311-6. performed histomorphometric and functional analyses to evaluate the influence of exercise on a treadmill, applied in early and late stages of sciatic nerve regeneration in rats following axonotmesis. The authors concluded that the treadmill exercise protocol applied to the immediate and late phases did not influence axonal sprouting, degree of maturation of the regenerated fibers, nor the functionality of the reinnervated muscles. Conversely, Seo et al.1111 Seo TB, Han IS, Yoon J-H, Hong K-E, Yoon S-J, Namgung UK. Involvement of Cdc2 in axonal regeneration enhanced by exercise training in rats. Med Sci Sport Exerc. 2006;38: 1267-76. reported that 30 min of walking on a treadmill between the 3rd and 14th day post-injury and with a speed of 18 m/min, played an important role in axonal regeneration. Ilha et al.6Ilha J, Araujo RT, Malysz T, Hermel EES, Rigon P, Xavier LL, et al. Endurance and resistance exercise training programs elicit specific effects on sciatic nerve regeneration after experimental traumatic lesion in rats. Neurorehabil Neural Repair. 2008;22:355-66. reported that, after two weeks of compression of the sciatic nerve in rats, the animals performed exercises during five weeks, namely: progressive treadmill exercises (about 9 m/min) in the first week and, in the remaining four weeks, 60 min/day. These authors noted improvement in nerve regeneration. However, animals that performed climbing-stair exercises (training against resistance) with body overload, with or without swimming, exhibited a delayed functional recovery.

The obesity model used in this study was the neonatal administration of MSG. Animals exposed to this substance undergo a neural reorganization that is reflected in a new metabolic structure, which predisposes to obesity in adulthood,3030 Lau A, Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010;460:525-42. and that also causes changes in the animal by application of MSG, such as a reduction in lean body mass.3131 Park S-Y, Kim Y-W, Dan J-M, Kim J-Y. Attenuated sympathetic activity and its relation to obesity in MSG injected and sympathectomized rats. Korean J Physiol Pharmacol. 2007;11:155-61. These animals have lower levels of growth hormone (GH), hence lower body weight and length, but with increased fat deposition.1515 Balbo SL, Gravena C, Bonfleur ML, Mathias PC, de F. Insulin secretion and acetylcholinesterase activity in monosodium L-glutamate-induced obese mice. Horm Res. 2000;54:186-91. In the results found at the end of the experiment, despite the MSG animals have presented lower means for grip strength, there were no significant differences in control and obese-MSG animals (independent of having been injured/treated, or not) with swimming – a fact that may be related to the nociception due to injury.

Because of the discrepancy in the literature regarding the optimal exercise time and about what is the better stage to start the practice, it is believed that swimming has been ineffective with respect to increasing grip strength as a result of some of these parameters, considering that the exercises were implemented in the immediate phase after injury, with progressive duration along the weeks. Additionally, an excessive load may have been generated in animals which swam, by virtue of the load of 10% of their body weight during the treatment – a factor identified as an important cause of delay in nerve regeneration.3232 Bar-shai M, Carmeli E, Ljubuncic P, Reznick AZ. Exercise and immobilization in aging animals: the involvement of oxidative stress and NF-kB activation. Free Radic Biol Med. 2008;44:202-14. We wish to emphasize, as a limitation of the present study, the absence of correlations with morphological findings of the median nerve and flexor carpi radialis muscle. This issue is suggested as a topic for future studies. Additionally, we also postponed the onset of physical exercise, with different protocols (i.e., with the addition of different overloads).

Conclusion

The swimming exercise with overload has not been effective in promoting improvement in muscle grip strength after compression injury of the right median nerve in control and obese-MSG rats.

References

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    Cavalcante VEV, Montenegro EJN, Pontes Filho NT de. Efeito da eletroestimulacão no músculo desnervado de animais: revisão sistemática. Fisioter Mov. 2012;25:669-78.
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    Stafford MA, Peng P, Hill DA. Sciatica: a review of history, epidemiology, pathogenesis, and the role of epidural steroid injection in management. Br J Anaesth. 2007;99:461-73.
  • 3
    Gordon T. The role of neurotrophic factors in nerve regeneration. Neurosurg Focus. 2009;26:E3.
  • 4
    Miscio G, Guastamacchia G, Brunani A, Priano L, Baudo S, Mauro A. Obesity and peripheral neuropathy risk: a dangerous liaison. J Peripher Nerv Syst. 2005;10:354-8.
  • 5
    Ylitalo KR, Herman WH, Harlow SD. Serial anthropometry predicts peripheral nerve dysfunction in a community cohort. Diabetes Metab Res Rev. 2013;29:145-51.
  • 6
    Ilha J, Araujo RT, Malysz T, Hermel EES, Rigon P, Xavier LL, et al. Endurance and resistance exercise training programs elicit specific effects on sciatic nerve regeneration after experimental traumatic lesion in rats. Neurorehabil Neural Repair. 2008;22:355-66.
  • 7
    Teodori RM, Betini J, Oliveira LS de, Sobral LL, Takeda SYM, Montebelo MI, et al. Swimming exercise in the acute or late phase after sciatic nerve crush accelerates nerve regeneration. Neural Plast. 2011;2011:8.
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    Tanaka S, Tsubaki A, Tachino K. Effect of exercise training after partial denervation in rat soleus muscles. J Phys Ther Sci. 2005;17:97-101.
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    Sarikcioglu L, Oguz N. Exercise training and axonal regeneration after sciatic nerve injury. Int J Neurosci. 2001;109:173-7.
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    Oliveira LS, Sobral LL, Takeda SYM, Betini J, Guirro RRJ, Somazz MC, et al. Estimulación eléctrica y natación en la fase aguda de la axonotmesis: influencia sobre la regeneración nerviosa y la recuperación funcional. Rev Neurol. 2008;47:11-5.
  • 11
    Seo TB, Han IS, Yoon J-H, Hong K-E, Yoon S-J, Namgung UK. Involvement of Cdc2 in axonal regeneration enhanced by exercise training in rats. Med Sci Sport Exerc. 2006;38: 1267-76.
  • 12
    Dishman RK, Berthoud H-R, Booth FW, Cotman CW, Edgerton VR, Fleshner MR, et al. Neurobiology of exercise. Obesity. 2006;14:345-56.
  • 13
    Medeiros A, Oliveira EM, Gianolla R, Casarini DE, Negrão CE, Brum PC. Swimming training increases cardiac vagal activity and induces cardiac hypertrophy in rats. Br J Med Biol Res. 2004;37:1909-17.
  • 14
    Ferreira ACC, Shimano AC, Mazzer N, Barbieri CH, Elui VMC, Fonseca MCR. Grip and pinch strength in healthy children and adolescents. Acta Ortop Bras. 2011;19:92-7.
  • 15
    Balbo SL, Gravena C, Bonfleur ML, Mathias PC, de F. Insulin secretion and acetylcholinesterase activity in monosodium L-glutamate-induced obese mice. Horm Res. 2000;54:186-91.
  • 16
    Chen J, Lue J, Lin L, Huang C, Chiang RP, Chen C, et al. Effects of pre-emptive drug treatment on astrocyte activation in the cuneate nucleus following rat median nerve injury. Pain. 2010;148:158-66.
  • 17
    Bertelli JA, Mira JC. The grasping test: a simple behavioral method assessment of peripheral nerve regeneration in the rat. J Neurosci Methods. 1995;58:151-5.
  • 18
    Taylor CA, Braza D, Rice JB, Dillingham T. The incidence of peripheral nerve injury in extremity trauma. Am J Phys Med Rehabil. 2008;87:381-5.
  • 19
    Daneyemez M, Solmaz I, Izci Y.Prognostic factors for the surgical management of peripheral nerve lesions. Tohoku J Exp Med. 2005;205:269-75.
  • 20
    Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 1988;33:87-107.
  • 21
    Lee Y, Kim J-H, Hong Y,Lee S-R, Chang KT, Hong Y. Prophylactic effects of swimming exercise on autophagy-induced muscle atrophy in diabetic rats. Lab Anim Res. 2012;28:171-9.
  • 22
    Bertolini GRF, Rosa CT, Silva LI, Meireles A, Rocha BP. Uso do exercício resistido antagonizado por naloxone como fator de analgesia em sinovite aguda de joelho de ratos Wistar. Rev Bras Med Esporte. 2012;18:126-9.
  • 23
    Ikemoto T, Tani T, Taniguchi S, Ikeuchi M, Kimura J. Effects of experimental focal compression on excitability of human median motor axons. Clin Neurophysiol. 2009;120:342-7.
  • 24
    Singh R, Singh Z, Bala R, Rana P Singh S. An unusual case of sciatic neuropraxia due to melorheostosis. J Bone Spine. 2010;77:614-5.
  • 25
    Haflah NHM, Rashid AHA, Sapuan J. Partial anterior interosseous nerve palsy: isolated neuropraxia of the branch to flexor pollicis longus. Hand Surg. 2010;15:221-3.
  • 26
    Yahia A, Ghroubi S, Kharrat O, Jribi S, Elleuch M, Elleuch MH. A study of isokinetic trunk and knee muscle strength in patients with chronic sciatica. Ann Phys Rehabil Med. 2010;53:239-49.
  • 27
    Silva LI, Meireles A, Rosa CT, Bertolini GRF. Avaliacão da dor em modelo experimental de compressão de nervo mediano em ratos. FIE Bull. 2014;81:565-8.
  • 28
    Possamai F, Siepko CM, André ES. Investigacão dos efeitos do exercício terapêutico sobre a regeneracão nervosa periférica. Acta Fisiatr. 2010;17(4):142-7.
  • 29
    Sobral LL, Oliveira LS, Takeda SYM, Somazz MC, Montebelo MIL, Teodori RM. Exercício imediato versus tardio na regeneracão do nervo isquiático de ratos após axoniotmese: análise histomorfométrica e funcional. Rev Bras Fisioter. 2008;12:311-6.
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*Corresponding author. E-mail: gladson_ricardo@yahoo.com.br (G.R.F. Bertolini).
  • Conflicts of interest
    The authors declare no conflicts of interest.
    • Laboratory of Endocrine Physiology and Metabolism; Laboratory for the Study of Injuries and Physical Therapy Resources, Universidade Estadual do Oeste do Paraná.

    Publication Dates

    • Publication in this collection
      Jan-Feb 2015

    History

    • Received
      16 Sept 2013
    • Accepted
      26 Aug 2014
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