The Association between Serum Oxidative Stress Indexes and Pathogenesis of Parkinson's Disease in the Northwest of Iran
-
Haleh BARMAKI
,
Ali MOROVATI
,
Zainab EYDIVANDI
,
Fatemeh JAFARI NALESHKENANI
,
Samira SAEDI
,
Hadis MUSAVI
,
Mojtaba ABBASI
,
Mohsen HEMMATI-DINARVAND
Abstract
Background: Parkinson's disease (PD) is a prevalent neurodegenerative disorder. Oxidative stress is a main modulator in the advancement of PD. This investigation aimed to evaluate the relations between serum trace elements, vitamin C, ferritin, transferrin, Nitrite Oxide (NOx) and Peroxynitrite (PrN) concentrations and clinical parameters in patients with PD.
Methods: Serum concentrations of variables were measured in 75 PD patients and 75 healthy subjects from Imam Reza Hospital, Tabriz University of Medical Sciences, Tabriz, Iran between Feb 2016 and Sep 2018. Receiver Operating Characteristic (ROC) analysis was performed to examine incremental diagnostic value of vitamin C, NOx, and PrN in the study groups.
Results: Mean serum NOx (35.81±5.16 vs. 11.27±3.59 mol/L, P<0.001) and PrN (15.78±4.23 vs. 9.62±4.57 mol/L, P= 0.004) were markedly higher in patient group versus healthy individuals. Significant differences were also observed in the serum levels of vitamin C (P<0.001), copper (Cu) (P<0.001), Iron (Fe) (P=0.003), and Zinc (Zn) (P<0.001) between patients with PD and healthy subjects. Nevertheless, the serum levels of Se (P=0.515), ferritin (P=0.103), and transferrin (P=0.372) were not statistically significant between the study groups. ROC analysis has revealed a diagnostic ability of serum vitamin C levels for PD with an area under ROC curve of ≥0.7 (P<0.05) and relatively high sensitivity and specificity.
Conclusion: Serum levels of NOx and PrN are significantly higher in patients with PD. In additions, serum vitamin C levels have a diagnostic value as a biomarker. Further studies are required with larger sample size to provide more detailed information about the cognitive profile of participants and the outcome measures.
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2. Kouti L, Noroozian M, Akhondzadeh S, et al (2013). Nitric oxide and peroxynitrite serum levels in Parkinson’s disease: correlation of oxidative stress and the severity of the disease. Eur Rev Med Pharmacol Sci, 17(7):964-70.
3. Wang N, Jin X, Guo D, Tong G, Zhu X (2017). Iron chelation nanoparticles with delayed saturation as an effective therapy for Parkinson Disease. Biomacromolecules, 18(2):461-474.
4. Prasad S, Gupta SC, Tyagi AK (2017). Reactive oxygen species (ROS) and cancer: Role of antioxidative nutraceuticals. Cancer Lett, 387:95-105.
5. Zang X, Geng X, Wang F, et al (2017). Overexpression of wheat ferritin gene TaFER-5B enhances tolerance to heat stress and other abiotic stresses associated with the ROS scavenging. BMC Plant Biol, 17:14.
6. Pino J, da Luz MH, Antunes HK, et al (2017). Iron-restricted diet affects brain ferritin levels, dopamine metabolism and cellular prion protein in a region-specific manner. Front Mol Neurosci, 10:145.
7. Quintana C, Gutiérrez L (2010). Could a dysfunction of ferritin be a determinant factor in the aetiology of some neurodegenerative diseases? Biochim Biophys Acta, 1800(8):770-82.
8. Mariani S, Ventriglia M, Simonelli I, et al (2013). Fe and Cu do not differ in Parkinson's disease: a replication study plus meta-analysis. Neurobiol Aging, 34(2):632-3.
9. Zuo L-J, Yu S-Y, Hu Y, et al (2016). Serotonergic dysfunctions and abnormal iron metabolism: Relevant to mental fatigue of Parkinson disease. Sci Rep, 6:19.
10. Si Q-Q, Yuan Y-S, Zhi Y, et al (2018). Plasma transferrin level correlates with the tremor-dominant phenotype of Parkinson’s disease. Neurosci Lett, 684:42-46.
11. Zhao H-W, Lin J, Wang X-B, et al (2013). Assessing plasma levels of selenium, copper, iron and zinc in patients of Parkinson’s disease. PLoS One, 8(12):e83060.
12. Ellwanger JH, Franke SI, Bordin DL, Pra D, Henriques JA (2016). Biological functions of selenium and its potential influence on Parkinson's disease. An Acad Bras Cienc, 88(3):1655-1674.
13. Shahar A, Patel KV, Semba RD, et al (2010). Plasma selenium is positively related to performance in neurological tasks assessing coordination and motor speed. Mov Disord, 25(12):1909-15.
14. Dexter DT, Jenner P, Schapira AH, Marsden CD (1991). Alterations in levels of iron, ferritin, and other trace metals in neurodegenerative diseases affecting the basal ganglia. Brain, 114:1953-75.
15. Younes-Mhenni S, Aissi M, Mokni N, et al (2013). Serum copper, zinc and selenium levels in Tunisian patients with Parkinson’s disease. Tunis Med, 91(6):402-5.
16. Jomova K, Vondrakova D, Lawson M, Valko M (2010). Metals, oxidative stress and neurodegenerative disorders. Mol Cell Biochem, 345(1-2):91-104.
17. Evans RM, Currie L, Campbell A (1982). The distribution of ascorbic acid between various cellular components of blood, in normal individuals, and its relation to the plasma concentration. Br J Nutr, 47(3):473-482.
18. Ide K, Yamada H, Umegaki K, et al (2015). Lymphocyte vitamin C levels as potential biomarker for progression of Parkinson's disease. Nutrition, 31(2):406-8.
19. Hughes AJ, Ben-Shlomo Y, Daniel SE, Lees AJ (1992). What features improve the accuracy of clinical diagnosis in Parkinson's disease A clinicopathologic study. Neurology, 42(6):1142-6.
20. Setsukinai K-i, Urano Y, Kakinuma K, et al (2003). Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J Biol Chem, 278(5):3170-5.
21. Huang J-C, Li D-J, Diao J-C, et al (2007). A novel fluorescent method for determination of peroxynitrite using folic acid as a probe. Talanta, 72(4):1283-7.
22. Jacques‐Silva MC, Nogueira CW, Broch LC, et al (2001). Diphenyl diselenide and ascorbic acid changes deposition of selenium and ascorbic acid in liver and brain of mice. Pharmacol Toxicol, 88(3):119-25.
23. Wang X-L, Xing G-H, Hong B, et al (2014). Gastrodin prevents motor deficits and oxidative stress in the MPTP mouse model of Parkinson's disease: Involvement of ERK1/2–Nrf2 signaling pathway. Life Sci, 114(2):77-85.
24. Lv E, Deng J, Yu Y, et al (2015). Nrf2-ARE signals mediated the anti-oxidative action of electroacupuncture in an MPTP mouse model of Parkinson's disease. Free Radic Res, 49(11):1296-307.
25. González-Estecha M, Palazón-Bru I, Bodas-Pinedo A, et al (2017). Relationship between serum selenium, sociodemographic variables, other trace elements and lipid profile in an adult Spanish population. J Trace Elem Med Biol, 43:93-105.
26. Gellein K, Syversen T, Steinnes E, et al (2008). Trace elements in serum from patients with Parkinson's disease—a prospective case-control study: The Nord-Trøndelag Health Study (HUNT). Brain Res, 1219:111-5.
27. Forte G, Bocca B, Senofonte O, et al (2004). Trace and major elements in whole blood, serum, cerebrospinal fluid and urine of patients with Parkinson’s disease. J Neural Transm (Vienna), 111(8):1031-40.
28. Sayre LM, Perry G, Smith MA (1999). Redox metals and neu rodegenerative disease. Curr Opin Chem Biol, 3(2):220-5.
29. Miao L, Clair DKS (2009). Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med, 47(4):344-56.
30. Jentzsch AM, Bachmann H, Fürst P, Biesalski HK (1996). Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med, 20(2):251-6.
31. Medeiros MS, Schumacher-Schuh A, Cardoso AM, et al (2016). Iron and oxidative stress in Parkinson’s disease: an observational study of injury biomarkers. PLoS One, 11(1):e0146129.
32. Costa-Mallen P, Gatenby C, Friend S, et al (2017). Brain iron concentrations in regions of interest and relation with serum iron levels in Parkinson disease. J Neurol Sci, 378:38-44.
33. Bowman GL, Dodge H, Frei B, et al (2009). Ascorbic acid and rates of cognitive decline in Alzheimer's disease. J Alzheimers Dis, 16(1):93-8.
34. Shukla R, Rajani M, Srivastava N, et al (2006). Nitrite and malondialdehyde content in cerebrospinal fluid of patients with Parkinson’s disease. Int J Neurosci, 116(12):1391-402.
35. Chen H-M, Lin C-Y, Wang V (2011). Amyloid P component as a plasma marker for Parkinson's disease identified by a proteomic approach. Clin Biochem, 44(5-6):377-85.
36. Costa-Mallen P, Zabetian CP, Hu S-C, et al (2016). Smoking and haptoglobin phenotype modulate serum ferritin and haptoglobin levels in Parkinson disease. J Neural Transm (Vienna), 123(11):1319-1330.
2. Kouti L, Noroozian M, Akhondzadeh S, et al (2013). Nitric oxide and peroxynitrite serum levels in Parkinson’s disease: correlation of oxidative stress and the severity of the disease. Eur Rev Med Pharmacol Sci, 17(7):964-70.
3. Wang N, Jin X, Guo D, Tong G, Zhu X (2017). Iron chelation nanoparticles with delayed saturation as an effective therapy for Parkinson Disease. Biomacromolecules, 18(2):461-474.
4. Prasad S, Gupta SC, Tyagi AK (2017). Reactive oxygen species (ROS) and cancer: Role of antioxidative nutraceuticals. Cancer Lett, 387:95-105.
5. Zang X, Geng X, Wang F, et al (2017). Overexpression of wheat ferritin gene TaFER-5B enhances tolerance to heat stress and other abiotic stresses associated with the ROS scavenging. BMC Plant Biol, 17:14.
6. Pino J, da Luz MH, Antunes HK, et al (2017). Iron-restricted diet affects brain ferritin levels, dopamine metabolism and cellular prion protein in a region-specific manner. Front Mol Neurosci, 10:145.
7. Quintana C, Gutiérrez L (2010). Could a dysfunction of ferritin be a determinant factor in the aetiology of some neurodegenerative diseases? Biochim Biophys Acta, 1800(8):770-82.
8. Mariani S, Ventriglia M, Simonelli I, et al (2013). Fe and Cu do not differ in Parkinson's disease: a replication study plus meta-analysis. Neurobiol Aging, 34(2):632-3.
9. Zuo L-J, Yu S-Y, Hu Y, et al (2016). Serotonergic dysfunctions and abnormal iron metabolism: Relevant to mental fatigue of Parkinson disease. Sci Rep, 6:19.
10. Si Q-Q, Yuan Y-S, Zhi Y, et al (2018). Plasma transferrin level correlates with the tremor-dominant phenotype of Parkinson’s disease. Neurosci Lett, 684:42-46.
11. Zhao H-W, Lin J, Wang X-B, et al (2013). Assessing plasma levels of selenium, copper, iron and zinc in patients of Parkinson’s disease. PLoS One, 8(12):e83060.
12. Ellwanger JH, Franke SI, Bordin DL, Pra D, Henriques JA (2016). Biological functions of selenium and its potential influence on Parkinson's disease. An Acad Bras Cienc, 88(3):1655-1674.
13. Shahar A, Patel KV, Semba RD, et al (2010). Plasma selenium is positively related to performance in neurological tasks assessing coordination and motor speed. Mov Disord, 25(12):1909-15.
14. Dexter DT, Jenner P, Schapira AH, Marsden CD (1991). Alterations in levels of iron, ferritin, and other trace metals in neurodegenerative diseases affecting the basal ganglia. Brain, 114:1953-75.
15. Younes-Mhenni S, Aissi M, Mokni N, et al (2013). Serum copper, zinc and selenium levels in Tunisian patients with Parkinson’s disease. Tunis Med, 91(6):402-5.
16. Jomova K, Vondrakova D, Lawson M, Valko M (2010). Metals, oxidative stress and neurodegenerative disorders. Mol Cell Biochem, 345(1-2):91-104.
17. Evans RM, Currie L, Campbell A (1982). The distribution of ascorbic acid between various cellular components of blood, in normal individuals, and its relation to the plasma concentration. Br J Nutr, 47(3):473-482.
18. Ide K, Yamada H, Umegaki K, et al (2015). Lymphocyte vitamin C levels as potential biomarker for progression of Parkinson's disease. Nutrition, 31(2):406-8.
19. Hughes AJ, Ben-Shlomo Y, Daniel SE, Lees AJ (1992). What features improve the accuracy of clinical diagnosis in Parkinson's disease A clinicopathologic study. Neurology, 42(6):1142-6.
20. Setsukinai K-i, Urano Y, Kakinuma K, et al (2003). Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J Biol Chem, 278(5):3170-5.
21. Huang J-C, Li D-J, Diao J-C, et al (2007). A novel fluorescent method for determination of peroxynitrite using folic acid as a probe. Talanta, 72(4):1283-7.
22. Jacques‐Silva MC, Nogueira CW, Broch LC, et al (2001). Diphenyl diselenide and ascorbic acid changes deposition of selenium and ascorbic acid in liver and brain of mice. Pharmacol Toxicol, 88(3):119-25.
23. Wang X-L, Xing G-H, Hong B, et al (2014). Gastrodin prevents motor deficits and oxidative stress in the MPTP mouse model of Parkinson's disease: Involvement of ERK1/2–Nrf2 signaling pathway. Life Sci, 114(2):77-85.
24. Lv E, Deng J, Yu Y, et al (2015). Nrf2-ARE signals mediated the anti-oxidative action of electroacupuncture in an MPTP mouse model of Parkinson's disease. Free Radic Res, 49(11):1296-307.
25. González-Estecha M, Palazón-Bru I, Bodas-Pinedo A, et al (2017). Relationship between serum selenium, sociodemographic variables, other trace elements and lipid profile in an adult Spanish population. J Trace Elem Med Biol, 43:93-105.
26. Gellein K, Syversen T, Steinnes E, et al (2008). Trace elements in serum from patients with Parkinson's disease—a prospective case-control study: The Nord-Trøndelag Health Study (HUNT). Brain Res, 1219:111-5.
27. Forte G, Bocca B, Senofonte O, et al (2004). Trace and major elements in whole blood, serum, cerebrospinal fluid and urine of patients with Parkinson’s disease. J Neural Transm (Vienna), 111(8):1031-40.
28. Sayre LM, Perry G, Smith MA (1999). Redox metals and neu rodegenerative disease. Curr Opin Chem Biol, 3(2):220-5.
29. Miao L, Clair DKS (2009). Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med, 47(4):344-56.
30. Jentzsch AM, Bachmann H, Fürst P, Biesalski HK (1996). Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med, 20(2):251-6.
31. Medeiros MS, Schumacher-Schuh A, Cardoso AM, et al (2016). Iron and oxidative stress in Parkinson’s disease: an observational study of injury biomarkers. PLoS One, 11(1):e0146129.
32. Costa-Mallen P, Gatenby C, Friend S, et al (2017). Brain iron concentrations in regions of interest and relation with serum iron levels in Parkinson disease. J Neurol Sci, 378:38-44.
33. Bowman GL, Dodge H, Frei B, et al (2009). Ascorbic acid and rates of cognitive decline in Alzheimer's disease. J Alzheimers Dis, 16(1):93-8.
34. Shukla R, Rajani M, Srivastava N, et al (2006). Nitrite and malondialdehyde content in cerebrospinal fluid of patients with Parkinson’s disease. Int J Neurosci, 116(12):1391-402.
35. Chen H-M, Lin C-Y, Wang V (2011). Amyloid P component as a plasma marker for Parkinson's disease identified by a proteomic approach. Clin Biochem, 44(5-6):377-85.
36. Costa-Mallen P, Zabetian CP, Hu S-C, et al (2016). Smoking and haptoglobin phenotype modulate serum ferritin and haptoglobin levels in Parkinson disease. J Neural Transm (Vienna), 123(11):1319-1330.
| Files | ||
| Issue | Vol 50 No 3 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v50i3.5621 | |
| Keywords | ||
| Parkinson diseases Trace elements Oxidative stress Ferritin Nitric oxide | ||
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How to Cite
1.
BARMAKI H, MOROVATI A, EYDIVANDI Z, JAFARI NALESHKENANI F, SAEDI S, MUSAVI H, ABBASI M, HEMMATI-DINARVAND M. The Association between Serum Oxidative Stress Indexes and Pathogenesis of Parkinson’s Disease in the Northwest of Iran. Iran J Public Health. 2021;50(3):606-615.
