Login Register Cart 0
Generic placeholder image

Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Adaptive Autonomic and Neuroplastic Control in Diabetic Neuropathy: A Narrative Review

Author(s): Francesca Marsili, Paul Potgieter and Corlius Fourie Birkill*

Volume 20, Issue 8, 2024

Published on: 24 November, 2023

Article ID: e241123223803 Pages: 17

DOI: 10.2174/0115733998253213231031050044

Price: $65

Abstract

Background: Type 2 diabetes mellitus (T2DM) is a worldwide socioeconomic burden, and is accompanied by a variety of metabolic disorders, as well as nerve dysfunction referred to as diabetic neuropathy (DN). Despite a tremendous body of research, the pathogenesis of DN remains largely elusive. Currently, two schools of thought exist regarding the pathogenesis of diabetic neuropathy: a) mitochondrial-induced toxicity, and b) microvascular damage. Both mechanisms signify DN as an intractable disease and, as a consequence, therapeutic approaches treat symptoms with limited efficacy and risk of side effects.

Objective: Here, we propose that the human body exclusively employs mechanisms of adaptation to protect itself during an adverse event. For this purpose, two control systems are defined, namely the autonomic and the neural control systems. The autonomic control system responds via inflammatory and immune responses, while the neural control system regulates neural signaling, via plastic adaptation. Both systems are proposed to regulate a network of temporal and causative connections which unravel the complex nature of diabetic complications.

Results: A significant result of this approach infers that both systems make DN reversible, thus opening the door to novel therapeutic applications.

[1]
Khan MAB, Hashim MJ, King JK, Govender RD, Mustafa H, Al Kaabi J. Epidemiology of type 2 diabetes-global burden of disease and forecasted trends. J Epidemiol Glob Health 2019; 10(1): 107-11.
[http://dx.doi.org/10.2991/jegh.k.191028.001] [PMID: 32175717]
[2]
International Diabetes Federation. IDF Diabetes Atlas. (10th ed.), 2021. Available from: https://www.diabetesatlas.org
[3]
Bo A, Thomsen RW, Nielsen JS, et al. Early‐onset type 2 diabetes: Age gradient in clinical and behavioural risk factors in 5115 persons with newly diagnosed type 2 diabetes-results from the DD2 study. Diabetes Metab Res Rev 2018; 34(3): e2968.
[http://dx.doi.org/10.1002/dmrr.2968] [PMID: 29172021]
[4]
Fonseca VA. Defining and characterizing the progression of type 2 diabetes. Diabetes Care 2009; 32 (Suppl. 2): S151-6.
[http://dx.doi.org/10.2337/dc09-S301] [PMID: 19875543]
[5]
Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev 2013; 93(1): 137-88.
[http://dx.doi.org/10.1152/physrev.00045.2011] [PMID: 23303908]
[6]
Hicks CW, Selvin E. Epidemiology of peripheral neuropathy and lower extremity disease in diabetes. Curr Diab Rep 2019; 19(10): 86.
[http://dx.doi.org/10.1007/s11892-019-1212-8] [PMID: 31456118]
[7]
Kobayashi M, Zochodne DW. Diabetic neuropathy and the sensory neuron: New aspects of pathogenesis and their treatment implications. J Diabetes Investig 2018; 9(6): 1239-54.
[http://dx.doi.org/10.1111/jdi.12833] [PMID: 29533535]
[8]
Feldman EL, Callaghan BC, Pop-Busui R, et al. Diabetic neuropathy. Nat Rev Dis Primers 2019; 5(1): 41.
[http://dx.doi.org/10.1038/s41572-019-0092-1] [PMID: 31197153]
[9]
Gundogdu BM. Diabetic peripheral neuropathy: An update on pathogenesis and management. Curr Neurol Neurosci Rep 2006; 6(1): 1-4.
[http://dx.doi.org/10.1007/s11910-996-0001-3] [PMID: 16469264]
[10]
Rahman MS, Hossain KS, Das S, et al. Role of insulin in health and disease: An update. Int J Mol Sci 2021; 22(12): 6403.
[http://dx.doi.org/10.3390/ijms22126403] [PMID: 34203830]
[11]
Ohishi M. Hypertension with diabetes mellitus: Physiology and pathology. Hypertens Res 2018; 41(6): 389-93.
[http://dx.doi.org/10.1038/s41440-018-0034-4] [PMID: 29556093]
[12]
Clark MG, Wallis MG, Barrett EJ, et al. Blood flow and muscle metabolism: A focus on insulin action. Am J Physiol Endocrinol Metab 2003; 284(2): E241-58.
[http://dx.doi.org/10.1152/ajpendo.00408.2002] [PMID: 12531739]
[13]
Limberg JK, Soares RN, Power G, et al. Hyperinsulinemia blunts sympathetic vasoconstriction: A possible role of β-adrenergic activation. Am J Physiol Regul Integr Comp Physiol 2021; 320(6): R771-9.
[http://dx.doi.org/10.1152/ajpregu.00018.2021] [PMID: 33851554]
[14]
Kim J, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction. Circulation 2006; 113(15): 1888-904.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.105.563213] [PMID: 16618833]
[15]
Scherrer U, Sartori C. Insulin as a vascular and sympathoexcitatory hormone: Implications for blood pressure regulation, insulin sensitivity, and cardiovascular morbidity. Circulation 1997; 96(11): 4104-13.
[http://dx.doi.org/10.1161/01.CIR.96.11.4104] [PMID: 9403636]
[16]
Feldman EL, Nave KA, Jensen TS, Bennett DLH. New horizons in diabetic neuropathy: Mechanisms, bioenergetics, and pain. Neuron 2017; 93(6): 1296-313.
[http://dx.doi.org/10.1016/j.neuron.2017.02.005] [PMID: 28334605]
[17]
Hadi HAR, Suwaidi JA. Endothelial dysfunction in diabetes mellitus. Vasc Health Risk Manag 2007; 3(6): 853-76.
[PMID: 18200806]
[18]
Zhou MS, Schulman IH, Zeng Q. Link between the renin–angiotensin system and insulin resistance: Implications for cardiovascular disease. Vasc Med 2012; 17(5): 330-41.
[http://dx.doi.org/10.1177/1358863X12450094] [PMID: 22814999]
[19]
Rask-Madsen C, King GL. Vascular complications of diabetes: Mechanisms of injury and protective factors. Cell Metab 2013; 17(1): 20-33.
[http://dx.doi.org/10.1016/j.cmet.2012.11.012] [PMID: 23312281]
[20]
Ramasamy R, Yan SF, Schmidt AM. Receptor for AGE (RAGE): Signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 2011; 1243(1): 88-102.
[http://dx.doi.org/10.1111/j.1749-6632.2011.06320.x] [PMID: 22211895]
[21]
Pongratz G, Straub RH. The sympathetic nervous response in inflammation. Arthritis Res Ther 2014; 16(6): 504.
[http://dx.doi.org/10.1186/s13075-014-0504-2] [PMID: 25789375]
[22]
Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta Mol Cell Res 2011; 1813(5): 878-88.
[http://dx.doi.org/10.1016/j.bbamcr.2011.01.034] [PMID: 21296109]
[23]
Akbari M, Hassan-Zadeh V. IL-6 signalling pathways and the development of type 2 diabetes. Inflammopharmacology 2018; 26(3): 685-98.
[http://dx.doi.org/10.1007/s10787-018-0458-0] [PMID: 29508109]
[24]
Rothaug M, Becker-Pauly C, Rose-John S. The role of interleukin-6 signaling in nervous tissue. Biochimica et Biophysica Acta (BBA) -. Molecular Cell Research 2016; 1863(6): 1218-27.
[25]
Cox AA, Sagot Y, Hedou G, et al. Low-dose pulsatile interleukin-6 as a treatment option for diabetic peripheral neuropathy. Front Endocrinol 2017; 8: 89.
[http://dx.doi.org/10.3389/fendo.2017.00089] [PMID: 28512447]
[26]
Chen L, Deng H, Cui H, et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 2018; 9(6): 7204-18.
[http://dx.doi.org/10.18632/oncotarget.23208] [PMID: 29467962]
[27]
Tsalamandris S, Antonopoulos AS, Oikonomou E, et al. The role of inflammation in diabetes: Current concepts and future perspectives. Eur Cardiol 2019; 14(1): 50-9.
[http://dx.doi.org/10.15420/ecr.2018.33.1] [PMID: 31131037]
[28]
Banerjee M, Saxena M. Interleukin-1 (IL-1) family of cytokines: Role in type 2 diabetes. Clin Chim Acta 2012; 413(15-16): 1163-70.
[http://dx.doi.org/10.1016/j.cca.2012.03.021] [PMID: 22521751]
[29]
Lyra e Silva NM, Gonçalves RA, Pascoal TA, et al. Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease. Transl Psychiatry 2021; 11(1): 251.
[http://dx.doi.org/10.1038/s41398-021-01349-z] [PMID: 33911072]
[30]
Zhou J, Zhou S. Inflammation: Therapeutic targets for diabetic neuropathy. Mol Neurobiol 2014; 49(1): 536-46.
[http://dx.doi.org/10.1007/s12035-013-8537-0] [PMID: 23990376]
[31]
Feigerlová E, Battaglia-Hsu SF. IL-6 signaling in diabetic nephropathy: From pathophysiology to therapeutic perspectives. Cytokine Growth Factor Rev 2017; 37: 57-65.
[http://dx.doi.org/10.1016/j.cytogfr.2017.03.003] [PMID: 28363692]
[32]
Lieb DC, Parson HK, Mamikunian G, Vinik AI. Cardiac autonomic imbalance in newly diagnosed and established diabetes is associated with markers of adipose tissue inflammation. Exp Diabetes Res 2012; 2012: 1-8.
[http://dx.doi.org/10.1155/2012/878760] [PMID: 22110481]
[33]
Weitz J, Diaz RR, Almaca J, Makhmutova M, Caicedo A. Anti-inflammatory cholinergic signals inhibit islet resident macrophage responses to ATP in living pancreatic tissue slices. Diabetes 2018; 67(Supplement_1)
[http://dx.doi.org/10.2337/db18-197-OR]
[34]
White UA, Stephens JM. The gp130 receptor cytokine family: Regulators of adipocyte development and function. Curr Pharm Des 2011; 17(4): 340-6.
[http://dx.doi.org/10.2174/138161211795164202] [PMID: 21375496]
[35]
Qu D, Liu J, Lau CW, Huang Y. IL-6 in diabetes and cardiovascular complications. Br J Pharmacol 2014; 171(15): 3595-603.
[http://dx.doi.org/10.1111/bph.12713] [PMID: 24697653]
[36]
Montgomery A, Tam F, Gursche C, et al. Overlapping and distinct biological effects of IL-6 classic and trans-signaling in vascular endothelial cells. Am J Physiol Cell Physiol 2021; 320(4): C554-65.
[http://dx.doi.org/10.1152/ajpcell.00323.2020] [PMID: 33471622]
[37]
Zhang XL, Topley N, Ito T, Phillips A. Interleukin-6 regulation of transforming growth factor (TGF)-β receptor compartmentalization and turnover enhances TGF-β1 signaling. J Biol Chem 2005; 280(13): 12239-45.
[http://dx.doi.org/10.1074/jbc.M413284200] [PMID: 15661740]
[38]
Robinson R, Srinivasan M, Shanmugam A, et al. Interleukin-6 trans-signaling inhibition prevents oxidative stress in a mouse model of early diabetic retinopathy. Redox Biol 2020; 34: 101574.
[http://dx.doi.org/10.1016/j.redox.2020.101574] [PMID: 32422539]
[39]
Campbell IL, Erta M, Lim SL, et al. Trans-signaling is a dominant mechanism for the pathogenic actions of interleukin-6 in the brain. J Neurosci 2014; 34(7): 2503-13.
[http://dx.doi.org/10.1523/JNEUROSCI.2830-13.2014] [PMID: 24523541]
[40]
Recasens M, Almolda B, Pérez-Clausell J, Campbell IL, González B, Castellano B. Chronic exposure to IL-6 induces a desensitized phenotype of the microglia. J Neuroinflammation 2021; 18(1): 31.
[http://dx.doi.org/10.1186/s12974-020-02063-1] [PMID: 33482848]
[41]
Lamagna C, Aurrand-Lions M, Imhof BA. Dual role of macrophages in tumor growth and angiogenesis. J Leukoc Biol 2006; 80(4): 705-13.
[http://dx.doi.org/10.1189/jlb.1105656] [PMID: 16864600]
[42]
Galli SJ, Grimbaldeston M, Tsai M. Immunomodulatory mast cells: Negative, as well as positive, regulators of immunity. Nat Rev Immunol 2008; 8(6): 478-86.
[http://dx.doi.org/10.1038/nri2327] [PMID: 18483499]
[43]
Castilla MÁ, Caramelo C, Gazapo RM, et al. Role of vascular endothelial growth factor (VEGF) in endothelial cell protection against cytotoxic agents. Life Sci 2000; 67(9): 1003-13.
[http://dx.doi.org/10.1016/S0024-3205(00)00693-7] [PMID: 10954034]
[44]
Vinik AI, Maser RE, Mitchell BD, Freeman R. Diabetic autonomic neuropathy. Diabetes Care 2003; 26(5): 1553-79.
[http://dx.doi.org/10.2337/diacare.26.5.1553] [PMID: 12716821]
[45]
Xiao J, Li J, Cai L, Chakrabarti S, Li X. Cytokines and diabetes research. J Diabetes Res 2014; 2014: 1-2.
[http://dx.doi.org/10.1155/2014/920613] [PMID: 24551859]
[46]
Kim H, Zamel R, Bai XH, Liu M. PKC activation induces inflammatory response and cell death in human bronchial epithelial cells. PLoS One 2013; 8(5): e64182.
[http://dx.doi.org/10.1371/journal.pone.0064182] [PMID: 23691166]
[47]
Sabio G, Davis RJ. TNF and MAP kinase signalling pathways. Semin Immunol 2014; 26(3): 237-45.
[http://dx.doi.org/10.1016/j.smim.2014.02.009] [PMID: 24647229]
[48]
Yung JHM, Giacca A. Role of c-Jun N-terminal Kinase (JNK) in obesity and type 2 Diabetes. Cells 2020; 9(3): 706.
[http://dx.doi.org/10.3390/cells9030706] [PMID: 32183037]
[49]
Casqueiro J, Casqueiro J, Alves C. Infections in patients with diabetes mellitus: A review of pathogenesis. Indian J Endocrinol Metab 2012; 16 (Suppl. 1): S27-36.
[PMID: 22701840]
[50]
Guo W, Li M, Dong Y, et al. Diabetes is a risk factor for the progression and prognosis of COVID‐19. Diabetes Metab Res Rev 2020; 36(7): e3319.
[http://dx.doi.org/10.1002/dmrr.3319] [PMID: 32233013]
[51]
Bril V, Blanchette CM, Noone JM, Runken MC, Gelinas D, Russell JW. The dilemma of diabetes in chronic inflammatory demyelinating polyneuropathy. J Diabetes Complications 2016; 30(7): 1401-7.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.05.007] [PMID: 27389526]
[52]
Park HT, Kim YH, Lee KE, Kim JK. Behind the pathology of macrophage-associated demyelination in inflammatory neuropathies: demyelinating Schwann cells. Cell Mol Life Sci 2020; 77(13): 2497-506.
[http://dx.doi.org/10.1007/s00018-019-03431-8] [PMID: 31884566]
[53]
Koike H, Katsuno M. Macrophages and autoantibodies in demyelinating diseases. Cells 2021; 10(4): 844.
[http://dx.doi.org/10.3390/cells10040844] [PMID: 33917929]
[54]
Traka M, Podojil JR, McCarthy DP, Miller SD, Popko B. Oligodendrocyte death results in immune-mediated CNS demyelination. Nat Neurosci 2016; 19(1): 65-74.
[http://dx.doi.org/10.1038/nn.4193] [PMID: 26656646]
[55]
Peschl P, Bradl M, Höftberger R, Berger T, Reindl M. Myelin oligodendrocyte glycoprotein: Deciphering a target in inflammatory demyelinating diseases. Front Immunol 2017; 8: 529.
[http://dx.doi.org/10.3389/fimmu.2017.00529] [PMID: 28533781]
[56]
Skaper SD. Oligodendrocyte precursor cells as a therapeutic target for demyelinating diseases. Prog Brain Res 2019; 245: 119-44.
[http://dx.doi.org/10.1016/bs.pbr.2019.03.013]
[57]
Höftberger R, Guo Y, Flanagan EP, et al. The pathology of central nervous system inflammatory demyelinating disease accompanying myelin oligodendrocyte glycoprotein autoantibody. Acta Neuropathol 2020; 139(5): 875-92.
[http://dx.doi.org/10.1007/s00401-020-02132-y] [PMID: 32048003]
[58]
Velikova TV, Kabakchieva PP, Assyov YS, Georgiev T. Targeting inflammatory cytokines to improve type 2 diabetes control. BioMed Res Int 2021; 2021: 1-12.
[http://dx.doi.org/10.1155/2021/7297419] [PMID: 34557550]
[59]
Zhou YQ, Liu Z, Liu ZH, et al. Interleukin-6: An emerging regulator of pathological pain. J Neuroinflammation 2016; 13(1): 141.
[http://dx.doi.org/10.1186/s12974-016-0607-6] [PMID: 27267059]
[60]
Payne SC, Ward G, MacIsaac RJ, Hyakumura T, Fallon JB, Villalobos J. Differential effects of vagus nerve stimulation strategies on glycemia and pancreatic secretions. Physiol Rep 2020; 8(11): e14479.
[http://dx.doi.org/10.14814/phy2.14479] [PMID: 32512650]
[61]
Caravaca AS, Gallina AL, Tarnawski L, et al. An Effective method for acute vagus nerve stimulation in experimental inflammation. Front Neurosci 2019; 13: 877.
[http://dx.doi.org/10.3389/fnins.2019.00877] [PMID: 31551672]
[62]
Tsaava T, Datta-Chaudhuri T, Addorisio ME, et al. Specific vagus nerve stimulation parameters alter serum cytokine levels in the absence of inflammation. Bioelectron Med 2020; 6(1): 8.
[http://dx.doi.org/10.1186/s42234-020-00042-8] [PMID: 32309522]
[63]
Pavlov VA, Wang H, Czura CJ, Friedman SG, Tracey KJ. The cholinergic anti-inflammatory pathway: A missing link in neuroimmunomodulation. Mol Med 2003; 9(5-8): 125-34.
[http://dx.doi.org/10.1007/BF03402177] [PMID: 14571320]
[64]
Koopman FA, Chavan SS, Miljko S, et al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis. Proc Natl Acad Sci USA 2016; 113(29): 8284-9.
[http://dx.doi.org/10.1073/pnas.1605635113] [PMID: 27382171]
[65]
Staats P, Giannakopoulos G, Blake J, Liebler E, Levy RM. The use of non-invasive vagus nerve stimulation to treat respiratory symptoms associated with COVID-19: A theoretical hypothesis and early clinical experience. Neuromodulation 2020; 23(6): 784-8.
[http://dx.doi.org/10.1111/ner.13172] [PMID: 32342609]
[66]
Kaniusas E, Szeles JC, Kampusch S, et al. Non-invasive auricular vagus nerve stimulation as a potential treatment for COVID-19 originated acute respiratory distress syndrome. Front Physiol 2020; 11: 890.
[http://dx.doi.org/10.3389/fphys.2020.00890] [PMID: 32848845]
[67]
Asad ZUA, Przebinda A, Chaudhary AMD, Farooqui S, Youness H, Stavrakis S. The role of vagus nerve stimulation in sepsis. Bioelectron Med 2020; 3(4): 51-62.
[http://dx.doi.org/10.2217/bem-2020-0010]
[68]
Boezaart AP, Botha DA. Treatment of Stage 3 COVID-19 with transcutaneous auricular vagus nerve stimulation drastically reduces interleukin-6 blood levels: A report on two cases. Neuromodulation 2021; 24(1): 166-7.
[http://dx.doi.org/10.1111/ner.13293] [PMID: 33063409]
[69]
Pavlov VA. The evolving obesity challenge: Targeting the vagus nerve and the inflammatory reflex in the response. Pharmacol Ther 2021; 222: 107794.
[http://dx.doi.org/10.1016/j.pharmthera.2020.107794] [PMID: 33310156]
[70]
Dubin AE, Patapoutian A. Nociceptors: The sensors of the pain pathway. J Clin Invest 2010; 120(11): 3760-72.
[http://dx.doi.org/10.1172/JCI42843] [PMID: 21041958]
[71]
Muramatsu K. Diabetes mellitus-related dysfunction of the motor system. Int J Mol Sci 2020; 21(20): 7485.
[http://dx.doi.org/10.3390/ijms21207485] [PMID: 33050583]
[72]
Sung JY, Tani J, Chang TS, Lin CSY. Uncovering sensory axonal dysfunction in asymptomatic type 2 diabetic neuropathy. PLoS One 2017; 12(2): e0171223.
[http://dx.doi.org/10.1371/journal.pone.0171223] [PMID: 28182728]
[73]
Sohn JW. Ion channels in the central regulation of energy and glucose homeostasis. Front Neurosci 2013; 7: 85.
[http://dx.doi.org/10.3389/fnins.2013.00085] [PMID: 23734095]
[74]
De Bernardis Murat C, Leão RM. A voltage‐dependent depolarization induced by low external glucose in neurons of the nucleus of the tractus solitarius: interaction with KATP channels. J Physiol 2019; 597(9): 2515-32.
[http://dx.doi.org/10.1113/JP277729] [PMID: 30927460]
[75]
de Campos Lima T, Santos DO, Lemes JBP, Chiovato LM, Lotufo CMC. Hyperglycemia induces mechanical hyperalgesia and depolarization of the resting membrane potential of primary nociceptive neurons: Role of ATP-sensitive potassium channels. J Neurol Sci 2019; 401: 55-61.
[http://dx.doi.org/10.1016/j.jns.2019.03.025] [PMID: 31015148]
[76]
Ågren R, Nilsson J, Århem P. Closed and open state dependent block of potassium channels cause opposing effects on excitability-a computational approach. Sci Rep 2019; 9(1): 8175.
[http://dx.doi.org/10.1038/s41598-019-44564-x] [PMID: 31160624]
[77]
Lin YC, Lin CSY, Chang TS, et al. Early sensory neurophysiological changes in prediabetes. J Diabetes Investig 2020; 11(2): 458-65.
[http://dx.doi.org/10.1111/jdi.13151] [PMID: 31563156]
[78]
Bönhof GJ, Strom A, Püttgen S, et al. Patterns of cutaneous nerve fibre loss and regeneration in type 2 diabetes with painful and painless polyneuropathy. Diabetologia 2017; 60(12): 2495-503.
[http://dx.doi.org/10.1007/s00125-017-4438-5] [PMID: 28914336]
[79]
Wendelschafer-Crabb G, Kennedy WR, Walk D. Morphological features of nerves in skin biopsies. J Neurol Sci 2006; 242(1-2): 15-21.
[http://dx.doi.org/10.1016/j.jns.2005.11.010] [PMID: 16448669]
[80]
Cheng HT, Dauch JR, Porzio MT, et al. Increased axonal regeneration and swellings in intraepidermal nerve fibers characterize painful phenotypes of diabetic neuropathy. J Pain 2013; 14(9): 941-7.
[http://dx.doi.org/10.1016/j.jpain.2013.03.005] [PMID: 23685187]
[81]
Lauria G, Lombardi R, Camozzi F, Devigili G. Skin biopsy for the diagnosis of peripheral neuropathy. Histopathology 2009; 54(3): 273-85.
[http://dx.doi.org/10.1111/j.1365-2559.2008.03096.x] [PMID: 18637969]
[82]
Galosi E, La Cesa S, Di Stefano G, et al. A pain in the skin. Regenerating nerve sprouts are distinctly associated with ongoing burning pain in patients with diabetes. Eur J Pain 2018; 22(10): 1727-34.
[http://dx.doi.org/10.1002/ejp.1259] [PMID: 29885017]
[83]
Li S, Liu N, Zhang X, Zhou D, Cai D. Bilinearity in spatiotemporal integration of synaptic inputs. PLOS Comput Biol 2014; 10(12): e1004014.
[http://dx.doi.org/10.1371/journal.pcbi.1004014] [PMID: 25521832]
[84]
Hao J, Wang X, Dan Y, Poo M, Zhang X. An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons. Proc Natl Acad Sci USA 2009; 106(51): 21906-11.
[http://dx.doi.org/10.1073/pnas.0912022106] [PMID: 19955407]
[85]
Moulin TC, Rayêe D, Williams MJ, Schiöth HB. The synaptic scaling literature: A systematic review of methodologies and quality of reporting. Front Cell Neurosci 2020; 14: 164.
[http://dx.doi.org/10.3389/fncel.2020.00164] [PMID: 32612512]
[86]
Hossain MJ, Kendig MD, Wild BM, et al. Evidence of altered peripheral nerve function in a rodent model of diet-induced prediabetes. Biomedicines 2020; 8(9): 313.
[http://dx.doi.org/10.3390/biomedicines8090313] [PMID: 32872256]
[87]
Sango K, Mizukami H, Horie H, Yagihashi S. Impaired axonal regeneration in diabetes. perspective on the underlying mechanism from in vivo and in vitro experimental studies. Front Endocrinol 2017; 8: 12.
[http://dx.doi.org/10.3389/fendo.2017.00012] [PMID: 28203223]
[88]
Sakai J. How synaptic pruning shapes neural wiring during development and, possibly, in disease. Proc Natl Acad Sci USA 2020; 117(28): 16096-9.
[http://dx.doi.org/10.1073/pnas.2010281117] [PMID: 32581125]
[89]
Faust TE, Gunner G, Schafer DP. Mechanisms governing activity-dependent synaptic pruning in the developing mammalian CNS. Nat Rev Neurosci 2021; 22(11): 657-73.
[http://dx.doi.org/10.1038/s41583-021-00507-y] [PMID: 34545240]
[90]
Riccomagno MM, Kolodkin AL. Sculpting neural circuits by axon and dendrite pruning. Annu Rev Cell Dev Biol 2015; 31(1): 779-805.
[http://dx.doi.org/10.1146/annurev-cellbio-100913-013038] [PMID: 26436703]
[91]
Geloso MC, D’Ambrosi N. Microglial Pruning: Relevance for synaptic dysfunction in multiple sclerosis and related experimental models. Cells 2021; 10(3): 686.
[http://dx.doi.org/10.3390/cells10030686] [PMID: 33804596]
[92]
Plant LD. A role for K2P channels in the operation of somatosensory nociceptors. Front Mol Neurosci 2012; 5: 21.
[http://dx.doi.org/10.3389/fnmol.2012.00021] [PMID: 22403526]
[93]
Yaron A, Schuldiner O. Common and divergent mechanisms in developmental neuronal remodeling and dying back neurodegeneration. Curr Biol 2016; 26(13): R628-39.
[http://dx.doi.org/10.1016/j.cub.2016.05.025] [PMID: 27404258]
[94]
Alrabayah M, Qaswal AB, Suleiman A, Khreesha L. Role of potassium ions quantum tunneling in the pathophysiology of phantom limb pain. Brain Sci 2020; 10(4): 241.
[http://dx.doi.org/10.3390/brainsci10040241] [PMID: 32325702]
[95]
Flor H. Maladaptive plasticity, memory for pain and phantom limb pain: review and suggestions for new therapies. Expert Rev Neurother 2008; 8(5): 809-18.
[http://dx.doi.org/10.1586/14737175.8.5.809] [PMID: 18457537]
[96]
Meyers EC, Kasliwal N, Solorzano BR, et al. Enhancing plasticity in central networks improves motor and sensory recovery after nerve damage. Nat Commun 2019; 10(1): 5782.
[http://dx.doi.org/10.1038/s41467-019-13695-0] [PMID: 31857587]
[97]
Schwartzman RJ, Grothusen J, Kiefer TR, Rohr P. Neuropathic central pain: Epidemiology, etiology, and treatment options. Arch Neurol 2001; 58(10): 1547-50.
[http://dx.doi.org/10.1001/archneur.58.10.1547] [PMID: 11594911]
[98]
Meacham K, Shepherd A, Mohapatra DP, Haroutounian S. Neuropathic pain: Central vs. peripheral mechanisms. Curr Pain Headache Rep 2017; 21(6): 28.
[http://dx.doi.org/10.1007/s11916-017-0629-5] [PMID: 28432601]
[99]
Drewes AM, Søfteland E, Dimcevski G, et al. Brain changes in diabetes mellitus patients with gastrointestinal symptoms. World J Diabetes 2016; 7(2): 14-26.
[http://dx.doi.org/10.4239/wjd.v7.i2.14] [PMID: 26839652]
[100]
Selvarajah D, Wilkinson ID, Fang F, et al. Structural and functional abnormalities of the primary somatosensory cortex in diabetic peripheral neuropathy: A multimodal MRI study. Diabetes 2019; 68(4): 796-806.
[http://dx.doi.org/10.2337/db18-0509] [PMID: 30617218]
[101]
Daffada PJ, Walsh N, McCabe CS, Palmer S. The impact of cortical remapping interventions on pain and disability in chronic low back pain: A systematic review. Physiotherapy 2015; 101(1): 25-33.
[http://dx.doi.org/10.1016/j.physio.2014.07.002] [PMID: 25442672]
[102]
Vartiainen N, Kirveskari E, Kallio-Laine K, Kalso E, Forss N. Cortical reorganization in primary somatosensory cortex in patients with unilateral chronic pain. J Pain 2009; 10(8): 854-9.
[http://dx.doi.org/10.1016/j.jpain.2009.02.006] [PMID: 19638329]
[103]
Ferris JK, Peters S, Brown KE, Tourigny K, Boyd LA. Type-2 diabetes mellitus reduces cortical thickness and decreases oxidative metabolism in sensorimotor regions after stroke. J Cereb Blood Flow Metab 2018; 38(5): 823-34.
[http://dx.doi.org/10.1177/0271678X17703887] [PMID: 28401788]
[104]
Fried PJ, Pascual-Leone A, Bolo NR. Diabetes and the link between neuroplasticity and glutamate in the aging human motor cortex. Clin Neurophysiol 2019; 130(9): 1502-10.
[http://dx.doi.org/10.1016/j.clinph.2019.04.721] [PMID: 31295719]
[105]
Zhang Y, Qu M, Yi X, et al. Sensorimotor and pain‐related alterations of the gray matter and white matter in type 2 diabetic patients with peripheral neuropathy. Hum Brain Mapp 2020; 41(3): 710-25.
[http://dx.doi.org/10.1002/hbm.24834] [PMID: 31663232]
[106]
Koike H, Katsuno M. Pathophysiology of chronic inflammatory demyelinating polyneuropathy: Insights into classification and therapeutic strategy. Neurol Ther 2020; 9(2): 213-27.
[http://dx.doi.org/10.1007/s40120-020-00190-8] [PMID: 32410146]
[107]
Lund JP, Donga R, Widmer CG, Stohler CS. The pain-adaptation model: A discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 1991; 69(5): 683-94.
[http://dx.doi.org/10.1139/y91-102] [PMID: 1863921]
[108]
Hodges PW, Moseley GL. Pain and motor control of the lumbopelvic region: Effect and possible mechanisms. J Electromyogr Kinesiol 2003; 13(4): 361-70.
[http://dx.doi.org/10.1016/S1050-6411(03)00042-7] [PMID: 12832166]
[109]
Bansal V, Kalita J, Misra UK. Diabetic neuropathy. Postgrad Med J 2006; 82(964): 95-100.
[http://dx.doi.org/10.1136/pgmj.2005.036137] [PMID: 16461471]
[110]
Henry DE, Chiodo AE, Yang W. Central nervous system reorganization in a variety of chronic pain states: A review. PM R 2011; 3(12): 1116-25.
[http://dx.doi.org/10.1016/j.pmrj.2011.05.018] [PMID: 22192321]
[111]
Sweetnam D, Holmes A, Tennant KA, et al. Diabetes impairs cortical plasticity and functional recovery following ischemic stroke. J Neurosci 2012; 32(15): 5132-43.
[http://dx.doi.org/10.1523/JNEUROSCI.5075-11.2012] [PMID: 22496559]
[112]
Andersen H. Motor neuropathy. In: Elsevier BV, Ed. Diabetes and the Nervous System 3rd series. 2014; pp. 81-95.
[http://dx.doi.org/10.1016/B978-0-444-53480-4.00007-2]
[113]
Morgalla MH, de Barros Filho MF, Chander BS, Soekadar SR, Tatagiba M, Lepski G. Neurophysiological effects of Dorsal Root Ganglion Stimulation (DRGS) in pain processing at the cortical level. Neuromodulation 2019; 22(1): 36-43.
[http://dx.doi.org/10.1111/ner.12900] [PMID: 30561852]
[114]
Snyder MJ, Gibbs LM, Lindsay TJ. Treating painful diabetic peripheral neuropathy: An update. Am Fam Physician 2016; 94(3): 227-34.
[PMID: 27479625]
[115]
Weintraub MI, Cole SP. Pulsed magnetic field therapy in refractory neuropathic pain secondary to peripheral neuropathy: electrodiagnostic parameters-pilot study. Neurorehabil Neural Repair 2004; 18(1): 42-6.
[http://dx.doi.org/10.1177/0888439003261024] [PMID: 15035963]
[116]
Lei T, Jing D, Xie K, et al. Therapeutic effects of 15 Hz pulsed electromagnetic field on diabetic peripheral neuropathy in streptozotocin-treated rats. PLoS One 2013; 8(4): e61414.
[http://dx.doi.org/10.1371/journal.pone.0061414] [PMID: 23637830]
[117]
Berger P, Landau S. Can an electrical pulsed radio frequency device relieve pain and improve function in patients with pedal diabetic neuropathy? A single blind randomized placebo-controlled trial. Johannesburg. 2016.
[118]
Goroszeniuk T, Kothari S. External stimulation: simplistic solution to intractable pain. London 2015.
[119]
Weintraub MI, Herrmann DN, Smith AG, Backonja MM, Cole SP. Pulsed electromagnetic fields to reduce diabetic neuropathic pain and stimulate neuronal repair: A randomized controlled trial. Arch Phys Med Rehabil 2009; 90(7): 1102-9.
[http://dx.doi.org/10.1016/j.apmr.2009.01.019] [PMID: 19577022]
[120]
Liu H, Zhou J, Gu L, Zuo Y. The change of HCN1/HCN2 mRNA expression in peripheral nerve after chronic constriction injury induced neuropathy followed by pulsed electromagnetic field therapy. Oncotarget 2017; 8(1): 1110-6.
[http://dx.doi.org/10.18632/oncotarget.13584] [PMID: 27901476]
[121]
Battecha K. Efficacy of pulsed electromagnetic field on pain and nerve conduction velocity in patients with diabetic neuropathy. Bull Fac Phys Ther 2017; 22(1): 9-14.
[http://dx.doi.org/10.4103/1110-6611.209877]
[122]
Veves A, Backonja M, Malik RA. Painful diabetic neuropathy: Epidemiology, natural history, early diagnosis, and treatment options. Pain Med 2008; 9(6): 660-74.
[http://dx.doi.org/10.1111/j.1526-4637.2007.00347.x] [PMID: 18828198]
[123]
Shillo P, Sloan G, Greig M, et al. Painful and painless diabetic neuropathies: What is the difference? Curr Diab Rep 2019; 19(6): 32.
[http://dx.doi.org/10.1007/s11892-019-1150-5] [PMID: 31065863]
[124]
Baskozos G, Themistocleous AC, Hebert HL, et al. Classification of painful or painless diabetic peripheral neuropathy and identification of the most powerful predictors using machine learning models in large cross-sectional cohorts. BMC Med Inform Decis Mak 2022; 22(1): 144.
[http://dx.doi.org/10.1186/s12911-022-01890-x] [PMID: 35644620]
[125]
Llorián-Salvador M, González-Rodríguez S. Painful understanding of VEGF. Front Pharmacol 2018; 9: 1267.
[http://dx.doi.org/10.3389/fphar.2018.01267] [PMID: 30459621]
[126]
Ponirakis G, Abdul-Ghani MA, Jayyousi A, et al. Painful diabetic neuropathy is associated with increased nerve regeneration in patients with type 2 diabetes undergoing intensive glycemic control. J Diabetes Investig 2021; 12(9): 1642-50.
[http://dx.doi.org/10.1111/jdi.13544] [PMID: 33714226]
[127]
Shillo P, Yiangou Y, Donatien P, Greig M, Selvarajah D, Wilkinson ID, et al. Nerve and vascular biomarkers in skin biopsies differentiate painful from painless peripheral neuropathy in type 2 diabetes. Frontiers in Pain Research 2021; 2.
[128]
Herder C, Bongaerts BWC, Rathmann W, et al. Differential association between biomarkers of subclinical inflammation and painful polyneuropathy: results from the KORA F4 study. Diabetes Care 2015; 38(1): 91-6.
[http://dx.doi.org/10.2337/dc14-1403] [PMID: 25325880]
[129]
Hammi C, Yeung B. StatPearls. Neuropathy 2022.
[130]
Zajączkowska R, Kocot-Kępska M, Leppert W, Wrzosek A, Mika J, Wordliczek J. Mechanisms of chemotherapy-induced peripheral neuropathy. Int J Mol Sci 2019; 20(6): 1451.
[http://dx.doi.org/10.3390/ijms20061451] [PMID: 30909387]
[131]
Kaeley N, Ahmad S, Pathania M, Kakkar R. Prevalence and patterns of peripheral neuropathy in patients of rheumatoid arthritis. J Family Med Prim Care 2019; 8(1): 22-6.
[http://dx.doi.org/10.4103/jfmpc.jfmpc_260_18] [PMID: 30911476]
[132]
Motwani L, Asif N, Patel A, Vedantam D, Poman DS. Neuropathy in human immunodeficiency virus: A review of the underlying pathogenesis and treatment. Cureus 2022; 14(6): e25905.
[http://dx.doi.org/10.7759/cureus.25905] [PMID: 35844323]
[133]
Wulff EA, Wang AK, Simpson DM. HIV-associated peripheral neuropathy: Epidemiology, pathophysiology and treatment. Drugs 2000; 59(6): 1251-60.
[http://dx.doi.org/10.2165/00003495-200059060-00005] [PMID: 10882161]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy