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Current Pharmaceutical Biotechnology

Author(s): Rafał Staszkiewicz*, Dawid Sobański, Kamil Bryś, Waldemar Och, Michał Garczarek, Uladzislau Ulasavets, Michał Stasiowski, Werner Dammermann, Damian Strojny and Beniamin Oskar Grabarek

DOI: 10.2174/0113892010262904230919073351

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Effect of Glycemic Disorders and Habits on the Concentration of Selected Neurotrophic Factors in Patients with Lumbosacral Intervertebral Disc Degeneration

Page: [908 - 923] Pages: 16

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Abstract

Background: Unhealthy habits, such as overeating processed and high-calorie foods, alcohol abuse, and smoking, negatively impact human health. It has been suggested that the inflammatory process and the resulting growth of nerve fibers within the intervertebral disc (IVD) fissures is the main reason for the pain accompanying IVD degeneration (IVDD).

Objectives: The aim of this study was to determine whether smoking, alcohol consumption, overweight/obesity, or diabetes comorbidity contribute to the development of IVDD and how the aforementioned factors affect the levels of brain-derived neurotrophic factor (BDNF), glial cell-derived neurotrophic factor (GDNF), and growth associated protein 43 (GAP-43) in the study and control groups (intervertebral discs, IVDs from cadavers, and serum samples from voluntary blood donors).

Methods: The study group comprised 113 patients diagnosed with IVDD who qualified for microdiscectomy. Two control groups (I and II) were used in this study. The first included 81 IVDs obtained from Caucasian human cadavers. Control group II, on the other hand, included serum samples obtained from 113 voluntary blood donors. The expression profiles of BDNF, GDNF, and GAP-43 were determined by enzyme-linked immunosorbent assay (ELISA).

Results: Our statistical analysis confirmed that patients who were overweight/obese, smoked tobacco, consumed alcohol, or had diabetes had a higher risk of IVDD (OR > 1). Statistical analysis showed that BDNF, GAP-43, and GDNF concentrations were significantly higher in the IVDs and serum samples obtained from the study group compared to the control group (p < 0.05). In addition, higher levels of BDNF, GDNF, and GAP-43 were noted in IVDD patients who consumed alcohol, smoked tobacco, were overweight/obese, or had comorbid diabetes compared to patients without these risk factors (p < 0.05).

Conclusion: We showed that changes in energy metabolism, habits, and lifestyle, as well as the degenerative process of IVD in the lumbosacral spine contribute to changing the concentration profile of the analyzed neurotrophic factors.

Graphical Abstract

[1]
Urban, J.P.G.; Roberts, S. Degeneration of the intervertebral disc. Arthritis Res., 2003, 5(3), 120-130.
[http://dx.doi.org/10.1186/ar629] [PMID: 12723977]
[2]
Boxberger, J.I.; Orlansky, A.S.; Sen, S.; Elliott, D.M. Reduced nucleus pulposus glycosaminoglycan content alters intervertebral disc dynamic viscoelastic mechanics. J. Biomech., 2009, 42(12), 1941-1946.
[http://dx.doi.org/10.1016/j.jbiomech.2009.05.008] [PMID: 19539936]
[3]
Kos, N.; Gradisnik, L.; Velnar, T. A brief review of the degenerative intervertebral disc disease. Med. Arh., 2019, 73(6), 421-424.
[http://dx.doi.org/10.5455/medarh.2019.73.421-424] [PMID: 32082013]
[4]
Clouet, J.; Vinatier, C.; Merceron, C.; Pot-Vaucel, M.; Hamel, O.; Weiss, P.; Grimandi, G.; Guicheux, J. The intervertebral disc: From pathophysiology to tissue engineering. Joint Bone Spine, 2009, 76(6), 614-618.
[http://dx.doi.org/10.1016/j.jbspin.2009.07.002] [PMID: 19819178]
[5]
Mardonova, S.M. The influence of bad habits on the human body. Themat. J. Phys. Educ., 2021.
[6]
Hossain, S.; Hossain, S.; Ahmed, F.; Islam, R.; Sikder, T.; Rahman, A. Prevalence of tobacco smoking and factors associated with the initiation of smoking among university students in Dhaka, Bangladesh. Cent Asian J Glob Health, 2017, 6(1), 244.
[http://dx.doi.org/10.5195/cajgh.2017.244]
[7]
Ho, J.S.Y.; Fernando, D.I.; Chan, M.Y.; Sia, C.H. Obesity in COVID-19: A systematic review and meta-analysis. Ann. Acad. Med. Singap., 2020, 49(12), 996-1008.
[http://dx.doi.org/10.47102/annals-acadmedsg.2020299] [PMID: 33463658]
[8]
Teraguchi, M.; Yoshimura, N.; Hashizume, H.; Yamada, H.; Oka, H.; Minamide, A.; Nagata, K.; Ishimoto, Y.; Kagotani, R.; Kawaguchi, H.; Tanaka, S.; Akune, T.; Nakamura, K.; Muraki, S.; Yoshida, M. Progression, incidence, and risk factors for intervertebral disc degeneration in a longitudinal population-based cohort: The Wakayama Spine Study. Osteoarthritis Cartilage, 2017, 25(7), 1122-1131.
[http://dx.doi.org/10.1016/j.joca.2017.01.001] [PMID: 28089899]
[9]
Lotz, J.C.; Ulrich, J.A. Innervation, inflammation, and hypermobility may characterize pathologic disc degeneration: Review of animal model data. J. Bone Joint Surg. Am., 2006, 88(S2), 76-82.
[http://dx.doi.org/10.2106/00004623-200604002-00016] [PMID: 16595449]
[10]
Benowitz, L.I.; Routtenberg, A. GAP-43: An intrinsic determinant of neuronal development and plasticity. Trends Neurosci., 1997, 20(2), 84-91.
[http://dx.doi.org/10.1016/S0166-2236(96)10072-2] [PMID: 9023877]
[11]
Aarts, L.H.J.; Schotman, P.; Verhaagen, J.; Schrama, L.H.; Gispen, W.H. The role of the neural growth associated protein B-50/Gap-43 in morphogenesis. In: In Molecular and Cellular Mechanisms of Neuronal Plasticity; Ehrlich, Y.H; Springer US: Boston, MA, 1998; Vol. 446, pp. 85-106.
[12]
Peng, B.; Hao, J.; Hou, S.; Wu, W.; Jiang, D.; Fu, X.; Yang, Y. Possible pathogenesis of painful intervertebral disc degeneration. Spine, 2006, 31(5), 560-566.
[http://dx.doi.org/10.1097/01.brs.0000201324.45537.46] [PMID: 16508552]
[13]
Purmessur, D.; Freemont, A.J.; Hoyland, J.A. Expression and regulation of neurotrophins in the nondegenerate and degenerate human intervertebral disc. Arthritis Res. Ther., 2008, 10(4), R99.
[http://dx.doi.org/10.1186/ar2487] [PMID: 18727839]
[14]
Krock, E.; Rosenzweig, D.H.; Chabot-Doré, A.J.; Jarzem, P.; Weber, M.H.; Ouellet, J.A.; Stone, L.S.; Haglund, L. Painful, degenerating intervertebral discs up regulate neurite sprouting and CGRP through nociceptive factors. J. Cell. Mol. Med., 2014, 18(6), 1213-1225.
[http://dx.doi.org/10.1111/jcmm.12268] [PMID: 24650225]
[15]
LA Binch, A.; Cole, A.A.; Breakwell, L.M.; Michael, A.L.R.; Chiverton, N.; Cross, A.K.; Le Maitre, C.L. Expression and regulation of neurotrophic and angiogenic factors during human intervertebral disc degeneration. Arthritis Res. Ther., 2014, 16(4), 416.
[http://dx.doi.org/10.1186/s13075-014-0416-1] [PMID: 25209447]
[16]
Henderson, C.E.; Phillips, H.S.; Pollock, R.A.; Davies, A.M.; Lemeulle, C.; Armanini, M.; Simmons, L.; Moffet, B.; Vandlen, R.A.; Koliatsos, V.E.; Rosenthal, A.; Rosenthal, A. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science, 1994, 266(5187), 1062-1064.
[http://dx.doi.org/10.1126/science.7973664] [PMID: 7973664]
[17]
Morcuende, S.; Muñoz-Hernández, R.; Benítez-Temiño, B.; Pastor, A.M.; de la Cruz, R.R. Neuroprotective effects of NGF, BDNF, NT-3 and GDNF on axotomized extraocular motoneurons in neonatal rats. Neuroscience, 2013, 250, 31-48.
[http://dx.doi.org/10.1016/j.neuroscience.2013.06.050] [PMID: 23827308]
[18]
Yamada, J.; Akeda, K.; Sano, T.; Iwasaki, T.; Takegami, N.; Sudo, A. Expression of glial cell line-derived neurotrophic factor in the human intervertebral disc. Spine, 2020, 45(13), E768-E775.
[http://dx.doi.org/10.1097/BRS.0000000000003418] [PMID: 32049932]
[19]
Jung, W.W.; Kim, H.S.; Shon, J.R.; Lee, M.; Lee, S.H.; Sul, D.; Na, H.S.; Kim, J.H.; Kim, B.J. Intervertebral disc degenerationinduced expression of pain-related molecules: Glial cell-derived neurotropic factor as a key factor. J. Neurosurg. Anesthesiol., 2011, 23(4), 329-334.
[http://dx.doi.org/10.1097/ANA.0b013e318220f033] [PMID: 21659885]
[20]
Yang, Y.; Xie, B.; Ju, C.; Jin, H.; Ye, X.; Yao, L.; Jia, M.; Sun, Z.; Yuan, Y. The association of decreased serum gdnf level with hyperglycemia and depression in type 2 diabetes mellitus. Endocr. Pract., 2019, 25(9), 951-965.
[http://dx.doi.org/10.4158/EP-2018-0492] [PMID: 31170370]
[21]
Rosskothen-Kuhl, N.; Illing, R.B. Gap43 transcription modulation in the adult brain depends on sensory activity and synaptic cooperation. PLoS One, 2014, 9(3), e92624.
[http://dx.doi.org/10.1371/journal.pone.0092624] [PMID: 24647228]
[22]
Carriel, V.; Garzón, I.; Campos, A.; Cornelissen, M.; Alaminos, M. Differential expression of GAP-43 and neurofilament during peripheral nerve regeneration through bio-artificial conduits. J. Tissue Eng. Regen. Med., 2017, 11(2), 553-563.
[http://dx.doi.org/10.1002/term.1949] [PMID: 25080900]
[23]
Jiang, H.; Wang, J.; Xu, B.; Yang, Q.; Liu, Y. Study on the expression of nerve growth associated protein-43 in rat model of intervertebral disc degeneration. J. Musculoskelet. Neuronal Interact., 2017, 17(2), 104-107.
[PMID: 28574417]
[24]
Staszkiewicz, R.; Gładysz, D.; Gralewski, M.; Bryś, K.; Garczarek, M.; SGadzieliński, M.; Marcol, W.; Sobański, D.; Grabarek, B.O. Usefulness of detecting brain-derived neurotrophic factor in intervertebral disc degeneration of the lumbosacral spine. Med. Sci. Monit., 2023, 29, e938663.
[http://dx.doi.org/10.12659/MSM.938663] [PMID: 36642939]
[25]
Staszkiewicz, R.; Gralewski, M.; Gładysz, D.; Bryś, K.; Garczarek, M.; Gadzieliński, M.; Marcol, W.; Sobański, D.; Grabarek, B.O. Evaluation of the concentration of growth associated protein-43 and glial cell-derived neurotrophic factor in degenerated intervertebral discs of the lumbosacral region of the spine. Mol. Pain, 2023, 19.
[http://dx.doi.org/10.1177/17448069231158287] [PMID: 36733259]
[26]
Staszkiewicz, R.; Bryś, K.; Gładysz, D.; Gralewski, M.; Garczarek, M.; Gadzieliński, M.; Wieczorek, J.; Marcol, W.; Ostenda, A.; Grabarek, B.O. Changes in elements and relationships among elements in intervertebral disc degeneration. Int. J. Environ. Res. Public Health, 2022, 19(15), 9042.
[http://dx.doi.org/10.3390/ijerph19159042] [PMID: 35897416]
[27]
Staszkiewicz, R.; Sobański, D.; Ulasavets, U.; Wieczorek, J.; Golec, E.; Marcol, W.; Grabarek, B.O. Evaluation of the concentration of selected elements in serum patients with intervertebral disc degeneration. J. Trace Elem. Med. Biol., 2023, 77, 127145.
[http://dx.doi.org/10.1016/j.jtemb.2023.127145] [PMID: 36921371]
[28]
Regulation of the Minister of Health of May 4, 2021 amending the regulation on the list of medicines for a beneficiary with the title of "Distinguished Honorary Blood Donor" or "Distinguished Transplant Donor" 2021. Available from: https://isap.sejm.gov.pl/isap.nsf/DocDetails.xsp?id=WDU20210000883 (Accessed on: 31 August 2022).
[29]
Stasiowski, M.; Missir, A.; Pluta, A.; Szumera, I.; Stasiak, M.; Szopa, W.; Błaszczyk, B.; Możdżyński, B.; Majchrzak, K.; Tymowski, M.; Niewiadomska, E.; Ładziński, P.; Krawczyk, L.; Kaspera, W. Influence of infiltration anaesthesia on perioperative outcomes following lumbar discectomy under surgical pleth index-guided general anaesthesia: A preliminary report from a randomised controlled prospective trial. Adv. Med. Sci., 2020, 65(1), 149-155.
[http://dx.doi.org/10.1016/j.advms.2019.12.006] [PMID: 31945659]
[30]
Jackson, A.R.; Dhawale, A.A.; Brown, M.D. Association between intervertebral disc degeneration and cigarette smoking: Clinical and experimental findings. JBJS Rev., 2015, 3(3), e2.
[http://dx.doi.org/10.2106/JBJS.RVW.N.00057] [PMID: 27490888]
[31]
Elmasry, S.; Asfour, S.; de Rivero Vaccari, J.P.; Travascio, F. Effects of tobacco smoking on the degeneration of the intervertebral disc: A finite element study. PLoS One, 2015, 10(8), e0136137.
[http://dx.doi.org/10.1371/journal.pone.0136137] [PMID: 26301590]
[32]
Chen, Z.; Li, X.; Pan, F.; Wu, D.; Li, H. A retrospective study: Does cigarette smoking induce cervical disc degeneration? Int. J. Surg., 2018, 53, 269-273.
[http://dx.doi.org/10.1016/j.ijsu.2018.04.004] [PMID: 29649666]
[33]
Kiraz, M.; Demir, E. Relationship of lumbar disc degeneration with hemoglobin value and smoking. Neurochirurgie, 2020, 66(5), 373-377.
[http://dx.doi.org/10.1016/j.neuchi.2020.06.133] [PMID: 32866500]
[34]
Trevisan, C.; Alessi, A.; Girotti, G.; Zanforlini, B.M.; Bertocco, A.; Mazzochin, M.; Zoccarato, F.; Piovesan, F.; Dianin, M.; Giannini, S.; Manzato, E.; Sergi, G. The impact of smoking on bone metabolism, bone mineral density and vertebral fractures in postmenopausal women. J. Clin. Densitom., 2020, 23(3), 381-389.
[http://dx.doi.org/10.1016/j.jocd.2019.07.007] [PMID: 31350204]
[35]
Even Dar, R.; Mazor, Y.; Karban, A.; Ish-Shalom, S.; Segal, E. Risk factors for low bone density in inflammatory bowel disease: Use of glucocorticoids, low body mass index, and smoking. Dig. Dis., 2019, 37(4), 284-290.
[http://dx.doi.org/10.1159/000496935] [PMID: 30799399]
[36]
Khan, J.S.; Hah, J.M.; Mackey, S.C. Effects of smoking on patients with chronic pain: A propensity-weighted analysis on the Collaborative Health Outcomes Information Registry. Pain, 2019, 160(10), 2374-2379.
[http://dx.doi.org/10.1097/j.pain.0000000000001631] [PMID: 31149975]
[37]
Veilleux, J.C. The relationship between distress tolerance and cigarette smoking: A systematic review and synthesis. Clin. Psychol. Rev., 2019, 71, 78-89.
[http://dx.doi.org/10.1016/j.cpr.2019.01.003] [PMID: 30691959]
[38]
Kapetanakis, S.; Gkantsinikoudis, N.; Chaniotakis, C.; Charitoudis, G.; Givissis, P. Percutaneous transforaminal endoscopic discectomy for the treatment of lumbar disc herniation in obese patients: Health-related quality of life assessment in a 2-year follow-up. World Neurosurg., 2018, 113, e638-e649.
[http://dx.doi.org/10.1016/j.wneu.2018.02.112] [PMID: 29499422]
[39]
Wilson, Z.R.; Kendall, R. Obesity, vascular disease, and lumbar disk degeneration: Associations of comorbidities in low back pain. PM R, 2017, 9(4), 398-402.
[http://dx.doi.org/10.1016/j.pmrj.2016.09.011] [PMID: 27721006]
[40]
Özcan-Ekşi, E.E.; Kara, M.; Berikol, G.; Orhun, Ö.; Turgut, V.U.; Ekşi, M.Ş. A new radiological index for the assessment of higher body fat status and lumbar spine degeneration. Skeletal Radiol., 2022, 51(6), 1261-1271.
[http://dx.doi.org/10.1007/s00256-021-03957-8] [PMID: 34792625]
[41]
Lee, S.Y.; Kim, W.; Lee, S.U.; Choi, K.H. Relationship between obesity and lumbar spine degeneration: A cross-sectional study from the fifth korean national health and nutrition examination survey, 2010–2012. Metab. Syndr. Relat. Disord., 2019, 17(1), 60-66.
[http://dx.doi.org/10.1089/met.2018.0051] [PMID: 30300077]
[42]
Jakoi, A.M.; Pannu, G.; D’Oro, A.; Buser, Z.; Pham, M.H.; Patel, N.N.; Hsieh, P.C.; Liu, J.C.; Acosta, F.L.; Hah, R.; Wang, J.C. The clinical correlations between diabetes, cigarette smoking and obesity on intervertebral degenerative disc disease of the lumbar spine. Asian Spine J., 2017, 11(3), 337-347.
[http://dx.doi.org/10.4184/asj.2017.11.3.337] [PMID: 28670401]
[43]
Kakar, R.S.; Simpson, K.J.; Das, B.M.; Brown, C.N. Review of physical activity benefits and potential considerations for individuals with surgical fusion of spine for scoliosis. Int. J. Exerc. Sci., 2017, 10(2), 166-177.
[PMID: 28344731]
[44]
Tieland, M.; Trouwborst, I.; Clark, B.C. Skeletal muscle performance and ageing. J. Cachexia Sarcopenia Muscle, 2018, 9(1), 3-19.
[http://dx.doi.org/10.1002/jcsm.12238] [PMID: 29151281]
[45]
Wu, H.; Ballantyne, C.M. Metabolic inflammation and insulin resistance in obesity. Circ. Res., 2020, 126(11), 1549-1564.
[http://dx.doi.org/10.1161/CIRCRESAHA.119.315896] [PMID: 32437299]
[46]
Wondmkun, Y.T. Obesity, insulin resistance, and type 2 diabetes: Associations and therapeutic implications. Diabetes Metab. Syndr. Obes., 2020, 13, 3611-3616.
[http://dx.doi.org/10.2147/DMSO.S275898] [PMID: 33116712]
[47]
Wu, H.; Ballantyne, C.M. Skeletal muscle inflammation and insulin resistance in obesity. J. Clin. Invest., 2017, 127(1), 43-54.
[http://dx.doi.org/10.1172/JCI88880] [PMID: 28045398]
[48]
Zhang, N.; Yin, Y.; Chen, W.S.; Xu, S.J. Moderate alcohol consumption may decrease risk of intervertebral disc degeneration. Med. Hypotheses, 2008, 71(4), 501-504.
[http://dx.doi.org/10.1016/j.mehy.2008.05.024] [PMID: 18632213]
[49]
Shin, B.J. Risk factors for recurrent lumbar disc herniations. Asian Spine J., 2014, 8(2), 211-215.
[http://dx.doi.org/10.4184/asj.2014.8.2.211] [PMID: 24761206]
[50]
Rasmussen, C. Lumbar disc herniation: Favourable outcome associated with intake of wine. Eur. Spine J., 1998, 7(1), 24-28.
[http://dx.doi.org/10.1007/s005860050022] [PMID: 9548354]
[51]
García-Arroyo, F.E.; Cristóbal, M.; Arellano-Buendía, A.S.; Osorio, H.; Tapia, E.; Soto, V.; Madero, M.; Lanaspa, M.A.; Roncal-Jiménez, C.; Bankir, L.; Johnson, R.J.; Sánchez-Lozada, L.G. Rehydration with soft drink-like beverages exacerbates dehydration and worsens dehydration-associated renal injury. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2016, 311(1), R57-R65.
[http://dx.doi.org/10.1152/ajpregu.00354.2015] [PMID: 27053647]
[52]
Sampara, P.; Banala, R.R.; Vemuri, S.K.; Av, G.R.; Gpv, S. Understanding the molecular biology of intervertebral disc degeneration and potential gene therapy strategies for regeneration: A review. Gene Ther., 2018, 25(2), 67-82.
[http://dx.doi.org/10.1038/s41434-018-0004-0] [PMID: 29567950]
[53]
Năsui, B.A.; Ungur, R.A.; Talaba, P.; Varlas, V.N.; Ciuciuc, N.; Silaghi, C.A.; Silaghi, H.; Opre, D.; Pop, A.L. Is alcohol consumption related to lifestyle factors in romanian university students? Int. J. Environ. Res. Public Health, 2021, 18(4), 1835.
[http://dx.doi.org/10.3390/ijerph18041835] [PMID: 33668631]
[54]
Liu, C.; Ran, J.; Hou, B.; Li, Y.; Morelli, J.N.; Li, X. Causal effects of body mass index, education, and lifestyle behaviors on intervertebral disc disorders: Mendelian randomization study. J. Orthop. Res., 2023, jor.25656.
[http://dx.doi.org/10.1002/jor.25656] [PMID: 37408137]
[55]
Boissoneault, J.; Lewis, B.; Nixon, S.J. Characterizing chronic pain and alcohol use trajectory among treatment-seeking alcoholics. Alcohol, 2019, 75, 47-54.
[http://dx.doi.org/10.1016/j.alcohol.2018.05.009] [PMID: 30359794]
[56]
Karimi, R.; Mallah, N.; Nedjat, S.; Beasley, M.J.; Takkouche, B. Association between alcohol consumption and chronic pain: A systematic review and meta-analysis. Br. J. Anaesth., 2022, 129(3), 355-365.
[http://dx.doi.org/10.1016/j.bja.2022.03.010] [PMID: 35410791]
[57]
Mahmoud, M.; Kokozidou, M.; Auffarth, A.; Schulze-Tanzil, G. The relationship between diabetes mellitus type ii and intervertebral disc degeneration in diabetic rodent models: A systematic and comprehensive review. Cells, 2020, 9(10), 2208.
[http://dx.doi.org/10.3390/cells9102208] [PMID: 33003542]
[58]
Russo, F.; Ambrosio, L.; Ngo, K.; Vadalà, G.; Denaro, V.; Fan, Y.; Sowa, G.; Kang, J.D.; Vo, N. The role of type I diabetes in intervertebral disc degeneration. Spine, 2019, 44(17), 1177-1185.
[http://dx.doi.org/10.1097/BRS.0000000000003054] [PMID: 30973512]
[59]
Park, C.H.; Min, K.B.; Min, J.Y.; Kim, D.H.; Seo, K.M.; Kim, D.K. Strong association of type 2 diabetes with degenerative lumbar spine disorders. Sci. Rep., 2021, 11(1), 16472.
[http://dx.doi.org/10.1038/s41598-021-95626-y] [PMID: 34389750]
[60]
Ruiz-Fernández, C.; Francisco, V.; Pino, J.; Mera, A.; González-Gay, M.A.; Gómez, R.; Lago, F.; Gualillo, O. Molecular relationships among obesity, inflammation and intervertebral disc degeneration: Are adipokines the common link? Int. J. Mol. Sci., 2019, 20(8), 2030.
[http://dx.doi.org/10.3390/ijms20082030] [PMID: 31027158]
[61]
Mateos-Valenzuela, A.G.; González-Macías, M.E.; Ahumada-Valdez, S.; Villa-Angulo, C.; Villa-Angulo, R. Risk factors and association of body composition components for lumbar disc herniation in Northwest, Mexico. Sci. Rep., 2020, 10(1), 18479.
[http://dx.doi.org/10.1038/s41598-020-75540-5] [PMID: 33116248]
[62]
Lener, S.; Wipplinger, C.; Hartmann, S.; Thomé, C.; Tschugg, A. The impact of obesity and smoking on young individuals suffering from lumbar disc herniation: A retrospective analysis of 97 cases. Neurosurg. Rev., 2020, 43(5), 1297-1303.
[http://dx.doi.org/10.1007/s10143-019-01151-y] [PMID: 31414196]
[63]
Chen, C.M.; Sun, L.W.; Tseng, C.; Chen, Y.C.; Wang, G.C. Surgical outcomes of full endoscopic spinal surgery for lumbar disc herniation over a 10-year period: A retrospective study. PLoS One, 2020, 15(11), e0241494.
[http://dx.doi.org/10.1371/journal.pone.0241494] [PMID: 33152001]
[64]
Kaviarasan, K.; Jithu, M.; Arif Mulla, M.; Sharma, T.; Sivasankar, S.; Das, U.N.; Angayarkanni, N. Low blood and vitreal BDNF, LXA4 and altered Th1/Th2 cytokine balance are potential risk factors for diabetic retinopathy. Metabolism, 2015, 64(9), 958-966.
[http://dx.doi.org/10.1016/j.metabol.2015.04.005] [PMID: 26004392]
[65]
Selvaraju, V.; Babu, J.R.; Geetha, T. Salivary neurotrophins brain-derived neurotrophic factor and nerve growth factor associated with childhood obesity: A multiplex magnetic luminescence analysis. Diagnostics, 2022, 12(5), 1130.
[http://dx.doi.org/10.3390/diagnostics12051130] [PMID: 35626286]
[66]
Duan, W.; Guo, Z.; Jiang, H.; Ware, M.; Mattson, M.P. Reversal of behavioral and metabolic abnormalities, and insulin resistance syndrome, by dietary restriction in mice deficient in brain-derived neurotrophic factor. Endocrinology, 2003, 144(6), 2446-2453.
[http://dx.doi.org/10.1210/en.2002-0113] [PMID: 12746306]
[67]
Yamanaka, M.; Itakura, Y.; Inoue, T.; Tsuchida, A.; Nakagawa, T.; Noguchi, H.; Taiji, M. Protective effect of brain-derived neurotrophic factor on pancreatic islets in obese diabetic mice. Metabolism, 2006, 55(10), 1286-1292.
[http://dx.doi.org/10.1016/j.metabol.2006.04.017] [PMID: 16979397]
[68]
Pillai, A.; Bruno, D.; Sarreal, A.S.; Hernando, R.T.; Saint-Louis, L.A.; Nierenberg, J.; Ginsberg, S.D.; Pomara, N.; Mehta, P.D.; Zetterberg, H.; Blennow, K.; Buckley, P.F. Plasma BDNF levels vary in relation to body weight in females. PLoS One, 2012, 7(7), e39358.
[http://dx.doi.org/10.1371/journal.pone.0039358] [PMID: 22768299]
[69]
Xu, B.; Xie, X. Neurotrophic factor control of satiety and body weight. Nat. Rev. Neurosci., 2016, 17(5), 282-292.
[http://dx.doi.org/10.1038/nrn.2016.24] [PMID: 27052383]
[70]
Cannata, F.; Vadalà, G.; Ambrosio, L.; Fallucca, S.; Napoli, N.; Papalia, R.; Pozzilli, P.; Denaro, V. Intervertebral disc degeneration: A focus on obesity and type 2 diabetes. Diabetes Metab. Res. Rev., 2020, 36(1), e3224.
[http://dx.doi.org/10.1002/dmrr.3224] [PMID: 31646738]
[71]
Zhang, X.Y.; Tan, Y.L.; Chen, D.C.; Tan, S.P.; Yang, F.D.; Zunta-Soares, G.B.; Soares, J.C. Effects of cigarette smoking and alcohol use on neurocognition and BDNF levels in a Chinese population. Psychopharmacology (Berl.), 2016, 233(3), 435-445.
[http://dx.doi.org/10.1007/s00213-015-4124-6] [PMID: 26518023]
[72]
Heberlein, A.; Muschler, M.; Wilhelm, J.; Frieling, H.; Lenz, B.; Gröschl, M.; Kornhuber, J.; Bleich, S.; Hillemacher, T. BDNF and GDNF serum levels in alcohol-dependent patients during withdrawal. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2010, 34(6), 1060-1064.
[http://dx.doi.org/10.1016/j.pnpbp.2010.05.025] [PMID: 20553781]
[73]
Schmidt, R.E.; Spencer, S.A.; Coleman, B.D.; Roth, K.A. Immunohistochemical localization of GAP-43 in rat and human sympathetic nervous system — effects of aging and diabetes. Brain Res., 1991, 552(2), 190-197.
[http://dx.doi.org/10.1016/0006-8993(91)90083-8] [PMID: 1833035]
[74]
Casoli, T.; Di Stefano, G.; Gracciotti, N.; Fattoretti, P.; Solazzi, M.; Bertoni-Freddari, C. Age-related effects of moderate alcohol consumption on GAP-43 levels in rat hippocampus. Mech. Ageing Dev., 2001, 122(15), 1723-1738.
[http://dx.doi.org/10.1016/S0047-6374(01)00295-0] [PMID: 11557276]