Acute Improvement in Intraoperative EMG Following Common Fibular Nerve Decompression in Patients with Symptomatic Diabetic Sensorimotor Peripheral Neuropathy: 1. EMG Results

Abstract

Background and Study Aims Electromyographic (EMG) recordings of the fibularis longus (FL) and tibialis anterior (TA) muscles were performed intraoperatively during common fibular nerve (CFN) nerve decompression (ND) in patients with symptomatic diabetic sensorimotor peripheral neuropathy (DSPN) and clinical nerve compression.

Materials and Methods Forty-six legs in 40 patients underwent surgical ND by external neurolysis; FL and TA muscles were monitored intraoperatively. Evoked EMGs were recorded just prior to and within 1 minute after ND.

Results Thirty-eight legs (82.6%) demonstrated EMG improvement 1 minute after ND. Sixty muscles (31 FL, 29 TA) were monitored, with 44 (73.3%) improving in EMG amplitude. Mean change in EMG amplitude represented a 73.6% improvement (p < 0.0001). Changes in EMG amplitudes correlated with visual analog scale pain improvement (p = 0.03).

Conclusion This is the first report of acute changes in objective EMG responses during ND of CFN in DSPN patients and demonstrates that patients with symptomatic DSPN and clinical nerve entrapment have latent but functional axons that surgical ND can improve immediately.

Keywords

common fibular nerve decompression - intraoperative electromyography - motor evoked potentials - acute objective functional improvement

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Funding

No funding was received for this research.

• References

• 1 Centers for Disease Control and Prevention (CDC). National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United States. Available at: https://www.cdc.gov/diabetes/pubs/statsreport14/national-diabetes-report-web.pdf
• 2 Dyck PJ, Feldman EL, Vinik AI. Diabetic neuropathies: the nerve damage of diabetes. Available at: http://www.medhelp.org/gov/www11.htm
• 3 Margolis DJ, Malay DS, Hoffstad OJ. , et al. Incidence of diabetic foot ulcer and lower extremity amputation among Medicare beneficiaries, 2006 to 2008: Data points #2. Available at: http://www.ncbi.nlm.nih.gov/books/NBK65149/
• 4 Chaudhry V, Stevens JC, Kincaid J, So YT. ; Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Practice Advisory: utility of surgical decompression for treatment of diabetic neuropathy: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 2006; 66 (12) 1805-1808
• 5 Chaudhry V, Russell J, Belzberg A. Decompressive surgery of lower limbs for symmetrical diabetic peripheral neuropathy. Cochrane Database Syst Rev 2008; CD006152 (03) CD006152
• 6 Dellon AL. Neurosurgical prevention of ulceration and amputation by decompression of lower extremity peripheral nerves in diabetic neuropathy: update 2006. Acta Neurochir Suppl (Wien) 2007; 100: 149-151
• 7 Hawker GA, Mian S, Kendzerska T, French M. Measures of adult pain: Visual Analog Scale for Pain (VAS Pain), Numeric Rating Scale for Pain (NRS Pain), McGill Pain Questionnaire (MPQ), Short-Form McGill Pain Questionnaire (SF-MPQ), Chronic Pain Grade Scale (CPGS), Short Form-36 Bodily Pain Scale (SF-36 BPS), and Measure of Intermittent and Constant Osteoarthritis Pain (ICOAP). Arthritis Care Res (Hoboken) 2011; 63 (Suppl. 11) S240-S252
• 8 Tashjian RZ, Deloach J, Porucznik CA, Powell AP. Minimal clinically important differences (MCID) and patient acceptable symptomatic state (PASS) for visual analog scales (VAS) measuring pain in patients treated for rotator cuff disease. J Shoulder Elbow Surg 2009; 18 (06) 927-932
• 9 Tubach F, Ravaud P, Baron G. , et al. Evaluation of clinically relevant changes in patient reported outcomes in knee and hip osteoarthritis: the minimal clinically important improvement. Ann Rheum Dis 2005; 64 (01) 29-33
• 10 Aszmann OC, Kress KM, Dellon AL. Results of decompression of peripheral nerves in diabetics: a prospective, blinded study. Plast Reconstr Surg 2000; 106 (04) 816-822
• 11 Dellon AL. Treatment of symptomatic diabetic neuropathy by surgical decompression of multiple peripheral nerves. Plast Reconstr Surg 1992; 89 (04) 689-697; discussion 698–699
• 12 Dellon AL, Muse VL, Nickerson DS. , et al. Prevention of ulceration, amputation, and reduction of hospitalization: outcomes of a prospective multicenter trial of tibial neurolysis in patients with diabetic neuropathy. J Reconstr Microsurg 2012; 28 (04) 241-246
• 13 Dellon AL, Muse VL, Scott ND. , et al. A positive Tinel sign as predictor of pain relief or sensory recovery after decompression of chronic tibial nerve compression in patients with diabetic neuropathy. J Reconstr Microsurg 2012; 28 (04) 235-240
• 14 Ducic I, Short KW, Dellon AL. Relationship between loss of pedal sensibility, balance, and falls in patients with peripheral neuropathy. Ann Plast Surg 2004; 52 (06) 535-540
• 15 Ducic I, Taylor NS, Dellon AL. Relationship between peripheral nerve decompression and gain of pedal sensibility and balance in patients with peripheral neuropathy. Ann Plast Surg 2006; 56 (02) 145-150
• 16 Hollis Caffee H. Treatment of diabetic neuropathy by decompression of the posterior tibial nerve. Plast Reconstr Surg 2000; 106 (04) 813-815
• 17 Siemionow M, Alghoul M, Molski M, Agaoglu G. Clinical outcome of peripheral nerve decompression in diabetic and nondiabetic peripheral neuropathy. Ann Plast Surg 2006; 57 (04) 385-390
• 18 Zhang W, Zhong W, Yang M, Shi J, Guowei L, Ma Q. Evaluation of the clinical efficacy of multiple lower-extremity nerve decompression in diabetic peripheral neuropathy. Br J Neurosurg 2013; 27 (06) 795-799
• 19 Zhong W, Zhang W, Yang M, Li G, Ma Q, Yang X. Impact of diabetes mellitus duration on effect of lower extremity nerve decompression in 1,526 diabetic peripheral neuropathy patients. Acta Neurochir (Wien) 2014; 156 (07) 1329-1333
• 20 Baltodano PA, Basdag B, Bailey CR. , et al. The positive effect of neurolysis on diabetic patients with compressed nerves of the lower extremities: a systematic review and meta-analysis. Plast Reconstr Surg Glob Open 2013; 1 (04) e24
• 21 Dellon AL. The Dellon approach to neurolysis in the neuropathy patient with chronic nerve compression. Handchir Mikrochir Plast Chir 2008; 40 (06) 351-360
• 22 Liao C, Zhang W, Yang M, Ma Q, Li G, Zhong W. Surgical decompression of painful diabetic peripheral neuropathy: the role of pain distribution. PLoS ONE 2014; 9 (10) e109827
• 23 Parker RG. Dorsal foot pain due to compression of the deep peroneal nerve by exostosis of the metatarsocuneiform joint. J Am Podiatr Med Assoc 2005; 95 (05) 455-458
• 24 Rader AJ. Surgical decompression in lower-extremity diabetic peripheral neuropathy. J Am Podiatr Med Assoc 2005; 95 (05) 446-450
• 25 Sessions J, Nickerson DS. Biologic basis of nerve decompression surgery for focal entrapments in diabetic peripheral neuropathy. J Diabetes Sci Tech 2014; 8 (02) 412-418
• 26 Wieman TJ, Patel VG. Treatment of hyperesthetic neuropathic pain in diabetics. Decompression of the tarsal tunnel. Ann Surg 1995; 221 (06) 660-664; discussion 664–665
• 27 Zhang W, Li S, Zheng X. Evaluation of the clinical efficacy of multiple lower extremity nerve decompression in diabetic peripheral neuropathy. J Neurol Surg A Cent Eur Neurosurg 2013; 74 (02) 96-100
• 28 Fazan VPS, deVasconcelos CAC, Valenca MM. , et al. Diabetic peripheral neuropathies: a morphometric overview. Int J Morphol 2010; 28 (01) 51-64
• 29 Malik RA. The pathology of human diabetic neuropathy. Diabetes 1997; 46 (Suppl. 02) S50-S53
• 30 Yagihashi S, Matsunaga M. Ultrastructural pathology of peripheral nerves in patients with diabetic neuropathy. Tohoku J Exp Med 1979; 129 (04) 357-366
• 31 Falla D, Dall'Alba P, Rainoldi A, Merletti R, Jull G. Location of innervation zones of sternocleidomastoid and scalene muscles—a basis for clinical and research electromyography applications. Clin Neurophysiol 2002; 113 (01) 57-63
• 32 Guzman RA, Silvestre RA, Arriagada DA. Biceps brachii muscle innervation zone location in healthy subjects using high-density surface electromyography. int J Morphol 2011; 29 (02) 347-352
• 33 Malek MH, Coburn JW, Weir JP, Beck TW, Housh TJ. The effects of innervation zone on electromyographic amplitude and mean power frequency during incremental cycle ergometry. J Neurosci Methods 2006; 155 (01) 126-133
• 34 Saitou K, Masuda T, Michikami D, Kojima R, Okada M. Innervation zones of the upper and lower limb muscles estimated by using multichannel surface EMG. J Hum Ergol (Tokyo) 2000; 29 (1-2): 35-52
• 35 Lee CH, Dellon AL. Prognostic ability of Tinel sign in determining outcome for decompression surgery in diabetic and nondiabetic neuropathy. Ann Plast Surg 2004; 53 (06) 523-527
• 36 Macaré van Maurik JF, Franssen H, Millin DW, Peters EJ, Kon M. Nerve conduction studies after decompression in painful diabetic polyneuropathy. J Clin Neurophysiol 2015; 32 (03) 247-250
• 37 Bostock H, Sears TA. Continuous conduction in demyelinated mammalian nerve fibers. Nature 1976; 263 (5580): 786-787
• 38 Bostock H, Sears TA. The internodal axon membrane: electrical excitability and continuous conduction in segmental demyelination. J Physiol 1978; 280: 273-301
• 39 Felts PA, Baker TA, Smith KJ. Conduction in segmentally demyelinated mammalian central axons. J Neurosci 1997; 17 (19) 7267-7277
• 40 Shrager P. The distribution of sodium and potassium channels in single demyelinated axons of the frog. J Physiol 1987; 392: 587-602
• 41 Bostock H, Sears TA, Sherratt RM. The spatial distribution of excitability and membrane current in normal and demyelinated mammalian nerve fibres. J Physiol 1983; 341: 41-58
• 42 England JD, Gamboni F, Levinson SR, Finger TE. Changed distribution of sodium channels along demyelinated axons. Proc Natl Acad Sci U S A 1990; 87 (17) 6777-6780
• 43 Foster RE, Whalen CC, Waxman SG. Reorganization of the axon membrane in demyelinated peripheral nerve fibers: morphological evidence. Science 1980; 210 (4470): 661-663
• 44 Waxman SG, Kocsis JD, Black JA. Pathophysiology of demyelinated axons. In: Waxman SG, Kocsis JD, Stys PK. eds. The Axon: Structure, Function and Pathophysiology. New York, NY: Oxford University Press; 1995: 438-461
• 45 Black JA, Liu S, Tanaka M, Cummins TR, Waxman SG. Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain. Pain 2004; 108 (03) 237-247
• 46 Devor M. Sodium channels and mechanisms of neuropathic pain. J Pain 2006; 7 (01) (Suppl. 01) S3-S12
• 47 Dib-Hajj SD, Yang Y, Black JA, Waxman SG. The Na(V)1.7 sodium channel: from molecule to man. Nat Rev Neurosci 2013; 14 (01) 49-62
• 48 Rogers M, Tang L, Madge DJ, Stevens EB. The role of sodium channels in neuropathic pain. Semin Cell Dev Biol 2006; 17 (05) 571-581
• 49 Waxman SG. The molecular pathophysiology of pain: abnormal expression of sodium channel genes and its contributions to hyperexcitability of primary sensory neurons. Pain 1999; (Suppl. 06) S133-S140
• 50 Waxman SG. Acquired channelopathies in nerve injury and MS. Neurology 2001; 56 (12) 1621-1627
• 51 Waxman SG. Sodium channels, the electrogenisome and the electrogenistat: lessons and questions from the clinic. J Physiol 2012; 590 (11) 2601-2612
• 52 Waxman SG, Dib-Hajj S, Cummins TR, Black JA. Sodium channels and pain. Proc Natl Acad Sci U S A 1999; 96 (14) 7635-7639
• 53 Boroujerdi A, Zeng J, Sharp K, Kim D, Steward O, Luo ZD. Calcium channel alpha-2-delta-1 protein upregulation in dorsal spinal cord mediates spinal cord injury-induced neuropathic pain states. Pain 2011; 152 (03) 649-655
• 54 Cao YQ. Voltage-gated calcium channels and pain. Pain 2006; 126 (1-3): 5-9
• 55 Gribkoff VK. The role of voltage-gated calcium channels in pain and nociception. Semin Cell Dev Biol 2006; 17 (05) 555-564
• 56 Ohnami S, Tanabe M, Shinohara S, Takasu K, Kato A, Ono H. Role of voltage-dependent calcium channel subtypes in spinal long-term potentiation of C-fiber-evoked field potentials. Pain 2011; 152 (03) 623-631
• 57 Takahashi T, Aoki Y, Okubo K. , et al. Upregulation of Ca(v)3.2 T-type calcium channels targeted by endogenous hydrogen sulfide contributes to maintenance of neuropathic pain. Pain 2010; 150 (01) 183-191
• 58 Yaksh TL. Calcium channels as therapeutic targets in neuropathic pain. J Pain 2006; 7 (01) (Suppl. 01) S13-S30
• 59 Fan L, Guan X, Wang W. , et al. Impaired neuropathic pain and preserved acute pain in rats overexpressing voltage-gated potassium channel subunit Kv1.2 in primary afferent neurons. Mol Pain 2014; 10: 8
• 60 Jan LY, Jan YN. Voltage-gated potassium channels and the diversity of electrical signalling. J Physiol 2012; 590 (11) 2591-2599
• 61 He XH, Zang Y, Chen X. , et al. TNF-α contributes to up-regulation of Nav1.3 and Nav1.8 in DRG neurons following motor fiber injury. Pain 2010; 151 (02) 266-279
• 62 Bostock H, Sears TA, Sherratt RM. The effects of 4-aminopyridine and tetraethylammonium ions on normal and demyelinated mammalian nerve fibres. J Physiol 1981; 313: 301-315
• 63 Gustafson KJ, Grinberg Y, Joseph S, Triolo RJ. Human distal sciatic nerve fascicular anatomy: implications for ankle control using nerve-cuff electrodes. J Rehabil Res Dev 2012; 49 (02) 309-321
• 64 Kudoh H, Sakai T. Fascicular analysis at perineurial level of the branching pattern of the human common peroneal nerve. Anat Sci Int 2007; 82 (04) 218-226
• 65 Sunderland S, Ray LJ. The intraneural topography of the sciatic nerve and its popliteal divisions in man. Brain 1948; 71 (Pt. 3): 242-273
• 66 Tsuda M, Masuda T, Tozaki-Saitoh H, Inoue K. Microglial regulation of neuropathic pain. J Pharmacol Sci 2013; 121 (02) 89-94
• 67 Valdivia JM, Dellon AL, Weinand ME, Maloney Jr CT. Surgical treatment of peripheral neuropathy: outcomes from 100 consecutive decompressions. J Am Podiatr Med Assoc 2005; 95 (05) 451-454
• 68 Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009; 139 (02) 267-284
• 69 Jensen TS, Finnerupm NB. Neuropathic pain: peripheral and central mechanisms. Eur J Pain Suppl 2009; 3 (02) 33-36
• 70 Waxman SG, Cummins TR, Dib-Hajj S, Fjell J, Black JA. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 1999; 22 (09) 1177-1187
• 71 Devor M. Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp Brain Res 2009; 196 (01) 115-128
• 72 Nitzan-Luques A, Devor M, Tal M. Genotype-selective phenotypic switch in primary afferent neurons contributes to neuropathic pain. Pain 2011; 152 (10) 2413-2426
• 73 Amir R, Michaelis M, Devor M. Membrane potential oscillations in dorsal root ganglion neurons: role in normal electrogenesis and neuropathic pain. J Neurosci 1999; 19 (19) 8589-8596
• 74 Woolf CJ. Evidence for a central component of post-injury pain hypersensitivity. Nature 1983; 306 (5944): 686-688
• 75 Woolf CJ, Thompson SW. The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 1991; 44 (03) 293-299
• 76 Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 2001; 429 (1–3): 23-37
• 77 Detloff MR, Fisher LC, McGaughy V, Longbrake EE, Popovich PG, Basso DM. Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 2008; 212 (02) 337-347
• 78 Inoue K. The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol Ther 2006; 109 (1–2): 210-226
• 79 Lim TK, Shi XQ, Martin HC. , et al. Blood-nerve barrier dysfunction contributes to the generation of neuropathic pain and allows targeting of injured nerves for pain relief. Pain 2014; 155 (05) 954-967
• 80 Mika J, Zychowska M, Popiolek-Barczyk K, Rojewska E, Przewlocka B. Importance of glial activation in neuropathic pain. Eur J Pharmacol 2013; 716 (1–3): 106-119
• 81 Wang D, Couture R, Hong Y. Activated microglia in the spinal cord underlies diabetic neuropathic pain. Eur J Pharmacol 2014; 728: 59-66
• 82 Dilley A, Bove GM. Disruption of axoplasmic transport induces mechanical sensitivity in intact rat C-fibre nociceptor axons. J Physiol 2008; 586 (02) 593-604
• 83 Dilley A, Richards N, Pulman KG, Bove GM. Disruption of fast axonal transport in the rat induces behavioral changes consistent with neuropathic pain. J Pain 2013; 14 (11) 1437-1449
• 84 McCambridge J, Witton J, Elbourne DR. Systematic review of the Hawthorne effect: new concepts are needed to study research participation effects. J Clin Epidemiol 2014; 67 (03) 267-277
• 85 Biddinger KR, Amend KJ. The role of surgical decompression for diabetic neuropathy. Foot Ankle Clin 2004; 9 (02) 239-254
• 86 Cornblath DR, Vinik A, Feldman E, Freeman R, Boulton AJ. Surgical decompression for diabetic sensorimotor polyneuropathy. Diabetes Care 2007; 30 (02) 421-422
• 87 Vinik A, Mehrabyan A, Colen L, Boulton A. Focal entrapment neuropathies in diabetes. Diabetes Care 2004; 27 (07) 1783-1788
• 88 Levine TD, Barrett S, Hank N. , et al. A pilot trial of peripheral nerve decompression for painful diabetic neuropathy. In: Neurology 2013. :P01.125
• 89 Perkins BA, Olaleye D, Bril V. Carpal tunnel syndrome in patients with diabetic polyneuropathy. Diabetes Care 2002; 25 (03) 565-569
• 90 Taylor-Gjevre RM, Gjevre JA, Nair B. Suspected carpal tunnel syndrome: do nerve conduction study results and symptoms match?. Can Fam Physician 2010; 56 (07) e250-e254
• 91 Tetro AM, Evanoff BA, Hollstien SB, Gelberman RH. A new provocative test for carpal tunnel syndrome. Assessment of wrist flexion and nerve compression. J Bone Joint Surg Br 1998; 80 (03) 493-498
• 92 Brown A. Axonal transport of membranous and nonmembranous cargoes: a unified perspective. J Cell Biol 2003; 160 (06) 817-821