Cited by 74Antioxidant Activity and Oxidative StressCancer and biochemical researchCancer, Lipids, and Metabolism

Oxidative stress in lung cancer patients is associated with altered serum markers of lipid metabolism

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Zabłocka-Słowińska, Katarzyna, Płaczkowska, Sylwia, Skórska, Katarzyna, Prescha, Anna, Pawełczyk, Konrad, Porębska, Irena, Kosacka, Monika, Grajeta, Halina·2019·PLOS ONE

Abstract

In lung cancer (LC), alterations in redox balance are extensively observed and are a consequence of disease as well as co-occurrent with smoking. We previously demonstrated that metabolic disturbances such as trace element status and carbohydrate metabolism alterations are linked with redox status. The aim of this study was to evaluate relationships between the serum parameters of lipid metabolism and redox balance in LC patients. Serum parameters of lipid metabolism, i.e. total cholesterol (T-C), HDL cholesterol (HDL-C), LDL cholesterol (LDL-C), triglycerides (TG), T-C:HDL-C ratio, non-HDL-C, apolipoprotein A1 (Apo-A1), apolipoprotein B (Apo-B) and Apo-B:Apo-A1 ratio, as well as systemic redox status, i.e. total antioxidant status (TAS), total oxidant status (TOS), oxidative stress index (OSI), vitamin E (VE), vitamin C (VC), malonyldialdehyde (MDA), conjugated dienes (CD), and 4-hydroxynonenal (4-HNE) were determined in 92 LC patients and 82 control subjects (CS). LC women had significantly lower T-C and LDL-C, and higher TG, while HDL-C, Apo-A1 and Apo-B were significantly decreased in LC patients regardless of sex, when compared to CS. LC men had alterations in the systemic total redox balance such as lower TAS and higher OSI than CS men. LC women had lower VC, but VE was decreased in LC patients, regardless of sex. We observed higher lipid peroxidation in LC patients expressed via higher 4-HNE and CD. Systemic redox disturbances were associated with serum lipid alterations: TOS and OSI were positively correlated with T-C:HDL-C ratio and Apo-B:Apo-A1 ratio and negatively with HDL-C. The parameters of lipid peroxidation CD and MDA were significantly associated with variables reflecting lipid disturbances. The observed correlations were strengthened by general overweight/obesity, abdominal obesity, hypertriglyceridemia and non-smoking status. In conclusion, parameters related to lipid alterations are associated with oxidative stress in LC patients. The largest contribution from lipid parameters was revealed for T-C:HDL-C ratio, HDL-C and Apo-B:Apo-A1 ratio, while the largest contribution from redox status was revealed for OSI and VE. Overweight, obesity, hypertriglyceridemia and non-smoking status intensified these relationships.

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  • MDA concentrations are unchanged between lung cancer patients and control individuals at advanced age.

    “In combination with lower MDA levels in elderly male and female AD and PD patients compared to healthy subjects as well as unchanged concentrations between lung cancer patients and control individuals at advanced age [151,183], this suggests that MDA is no suitable marker for human aging and age-related diseases.”

    From Protein oxidation - Formation mechanisms, detection and relevance as biomarkers in human diseases (2021) · cites this paper as [183]

    The Discussion reports no significant difference in serum MDA between lung cancer patients and controls. However, Table 1 (Materials and methods; page unavailable) shows that male controls had a median age of 49.5 years, versus 62 years for male patients, so the comparison was not entirely between people of advanced age. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Serum 4-HNE levels are higher in male and female lung cancer patients (n = 92) than in control subjects (n = 40), as measured by ELISA.

    “| Lung cancer | Serum | Control subjects (n = 40) vs. lung cancer patients (n = 92) | ELISA | Higher levels of 4-HNE in male and female lung cancer patients | [183] |”

    From Protein oxidation - Formation mechanisms, detection and relevance as biomarkers in human diseases (2021) · cites this paper as [183]

    The Results report higher serum 4-HNE in lung cancer patients, and the Discussion says the increase occurred regardless of sex. The Methods specify an ELISA assay. The sample sizes are misstated: the study included 92 lung cancer patients and 82 controls; 40 was the number of male controls, not all controls (Methods and Results, Table 2; page numbers unavailable). (LLM, conf=0.91)

    Experimental — accuracy not yet measured
  • Serum MDA levels do not differ between lung cancer patients (n = 92) and control subjects (n = 40), as measured by TBARS assay.

    “| Lung cancer | Serum | Control subjects (n = 40) vs. lung cancer patients (n = 92) | TBARS assay | No differences in MDA levels between the groups | [183] |”

    From Protein oxidation - Formation mechanisms, detection and relevance as biomarkers in human diseases (2021) · cites this paper as [183]

    The Results state that serum MDA concentrations were comparable between lung cancer patients and controls, and Methods describe a thiobarbituric-acid-based serum assay. But Methods report 92 patients and 82 controls enrolled, not 40 controls; the Results table lists 40 male controls, with MDA measurements available for 39 of them. Thus the cited group sizes do not describe the overall MDA comparison. (LLM, conf=0.90)

    Experimental — accuracy not yet measured
  • Zablocka-Slowinska et al. found no differences in MDA between healthy subjects and lung cancer patients.

    “Except of Zablocka-Slowinska and colleagues, showing no differences between healthy subjects and patients with lung cancer [183], all clinical investigations using the TBARS assay consistently found elevated MDA levels in diverse human metabolic disease, as shown in Table 6.”
  • All clinical investigations using the TBARS assay except Zablocka-Slowinska et al. found elevated MDA levels in diverse human metabolic diseases.

    “Except of Zablocka-Slowinska and colleagues, showing no differences between healthy subjects and patients with lung cancer [183], all clinical investigations using the TBARS assay consistently found elevated MDA levels in diverse human metabolic disease, as shown in Table 6.”

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Research works printed but not linked: 58

  1. [1]Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: How are they linked? Free Radic Biol Med. Elsevier Inc.; 2010; 49: 1603– 1616. 10.1016/j.freeradbiomed.2010.09.006 20840865 PMC2990475 · DOI · Paper page
  2. [2]Lee G, Walser TC, Dubinett SM. Chronic inflammation, chronic obstructive pulmonary disease, and lung cancer. Curr Opin Pulm Med. 2009; 15: 303– 307. 10.1097/MCP.0b013e32832c975a 19417670 · DOI
  3. [3]Zabłocka-Słowińska K, Płaczkowska S, Prescha A, Pawełczyk K, Kosacka M, Porębska I, et al Systemic redox status in lung cancer patients is related to altered glucose metabolism. PLoS One. 2018; 13: e0204173 10.1371/journal.pone.0204173 30235348 PMC6147499 · DOI
  4. [4]Jaruga P, Zastawny TH, Skokowski J, Dizdaroglu M, Olinski R. Oxidative DNA base damage and antioxidant enzyme activities in human lung cancer. FEBS Lett. 1994; 341: 59– 64. Available: http://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=emed3&NEWS=N&AN=1994087244 8137923
  5. [5]Lin KF, Wu HF, Huang WC, Tang PL, Wu MT, Wu FZ. Propensity score analysis of lung cancer risk in a population with high prevalence of non-smoking related lung cancer. BMC Pulm Med. BMC Pulmonary Medicine; 2017; 17: 1– 8. 10.1186/s12890-016-0353-7 28874145 PMC5585962 · DOI
  6. [6]Zabłocka-Słowińska K, Płaczkowska S, Prescha A, Pawełczyk K, Porębska I, Kosacka M, et al Serum and whole blood Zn, Cu and Mn profiles and their relation to redox status in lung cancer patients. J Trace Elem Med Biol. 2018; 45: 78– 84. 10.1016/j.jtemb.2017.09.024 29173487 · DOI
  7. [7]Lin X, Lu L, Liu L, Wei S, He Y, Chang J, et al Blood lipids profile and lung cancer risk in a meta-analysis of prospective cohort studies. J Clin Lipidol. Elsevier Inc; 2017; 11: 1073– 1081. 10.1016/j.jacl.2017.05.004 28669687 · DOI
  8. [8]Chi P-D, Liu W, Chen H, Zhang J-P, Lin Y, Zheng X, et al High-Density Lipoprotein Cholesterol Is a Favorable Prognostic Factor and Negatively Correlated with C-Reactive Protein Level in Non-Small Cell Lung Carcinoma. PLoS One. 2014; 9: e91080 10.1371/journal.pone.0091080 24625581 PMC3953329 · DOI
  9. [9]Kucharska-Newton AM, Rosamond WD, Schroeder JC, McNeill AM, Coresh J, Folsom AR. HDL-cholesterol and the incidence of lung cancer in the Atherosclerosis Risk in Communities (ARIC) study. Lung Cancer. 2008; 61: 292– 300. 10.1016/j.lungcan.2008.01.015 18342390 PMC2580072 · DOI
  10. [10]Zhou T, Zhan J, Fang W, Zhao Y, Yang Y, Hou X, et al Serum low-density lipoprotein and low-density lipoprotein expression level at diagnosis are favorable prognostic factors in patients with small-cell lung cancer (SCLC). BMC Cancer. 2017; 17: 1– 10. 10.1186/s12885-016-3022-6 28410578 PMC5391547 · DOI
  11. [11]Karabacak M, Varol E, Kahraman F, Ozaydin M, Türkdogan AK, Ersoy IH. Low high-density lipoprotein cholesterol is characterized by elevated oxidative stress. Angiology. 2014; 65: 927– 931. 10.1177/0003319713512173 24280265 · DOI
  12. [12]Jurek A, Turyna B, Kubit P, Klein A. LDL susceptibility to oxidation and HDL antioxidant capacity in patients with renal failure. Clin Biochem. 2006; 39: 19– 27. 10.1016/j.clinbiochem.2005.08.009 16309663 · DOI
  13. [13]Rodríguez-Carrio J, Alperi-López M, López P, López-Mejías R, Alonso-Castro S, Abal F, et al High triglycerides and low high-density lipoprotein cholesterol lipid profile in rheumatoid arthritis: A potential link among inflammation, oxidative status, and dysfunctional high-density lipoprotein. J Clin Lipidol. 2017; 11: 1043– 1054.e2. 10.1016/j.jacl.2017.05.009 28662934 · DOI
  14. [15]Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005; 38: 1103– 1111. 10.1016/j.clinbiochem.2005.08.008 16214125 · DOI
  15. [16]Motor S, Ozturk S, Ozcan O, Gurpinar AB, Can Y, Yuksel R, et al Evaluation of total antioxidant status, total oxidant status and oxidative stress index in patients with alopecia areata. Int J Clin Exp Med. 2014; 7: 1089– 1093. 24955187 PMC4057866
  16. [17]Recknagel RO, Glende EA. Spectrophotometric detection of lipid conjugated dienes. Methods Enzymol. 1984; 105: 331– 7. Available: http://www.ncbi.nlm.nih.gov/pubmed/6727673 6727673
  17. [18]Huang X, Alonso A, Guo X, David M, Lichtenstein ML, Ballantyne CM, et al Statins, plasma cholesterol, and risk of Parkinson’s disease: a prospective study. Mov Disord. 2016; 30: 552– 559. 10.1002/mds.26152.Statins PMC4390443 25639598 · DOI
  18. [19]Martinez-Outschoorn UE, Peiris-Pagés M, Pestell RG, Sotgia F, Lisanti MP. Cancer metabolism: a therapeutic perspective. Nat Rev Clin Oncol. 2017; 14: 11– 31. 10.1038/nrclinonc.2016.60 27141887 · DOI · Paper page
  19. [20]Hamanaka RB, Chandel NS. Warburg Effect and Redox Balance. Science. 2011; 334: 1219– 1220. 10.1126/science.1215637 22144609 · DOI
  20. [21]Vaziri ND. Role of dyslipidemia in impairment of energy metabolism, oxidative stress, inflammation and cardiovascular disease in chronic kidney disease. Clin Exp Nephrol. 2014; 18: 265– 268. 10.1007/s10157-013-0847-z 23974528 · DOI
  21. [22]Yang R-L, Shi Y-H, Hao G, Li W, Le G-W. Increasing oxidative stress with progressive hyperlipidemia in human: relation between malondialdehyde and atherogenic index. J Clin Biochem Nutr. 2008; 43: 154– 158. 10.3164/jcbn.2008044 19015749 PMC2581765 · DOI
  22. [23]Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes. 2015; 6: 456 10.4239/wjd.v6.i3.456 25897356 PMC4398902 · DOI
  23. [24]Santos CR, Schulze A. Lipid metabolism in cancer. FEBS J. 2012; 279: 2610– 2623. 10.1111/j.1742-4658.2012.08644.x 22621751 · DOI
  24. [25]Merino Salvador M, Gómez de Cedrón M, Merino Rubio J, Falagán Martínez S, Sánchez Martínez R, Casado E, et al Lipid metabolism and lung cancer. Crit Rev Oncol Hematol. Elsevier Ireland Ltd; 2017; 112: 31– 40. 10.1016/j.critrevonc.2017.02.001 28325263 · DOI
  25. [26]Shah F, Shukla S, Shah P, Patel H, Patel P. Significance of alterations in plasma lipid profile levels in breast cancer. Integr Cancer Ther. 2008; 7: 33– 41. 10.1177/1534735407313883 18292593 · DOI
  26. [27]Patel PS, Shah MH, Jha FP, Raval GN, Rawal RM, Patel MM, et al Alterations in plasma lipid profile patterns in head and neck cancer and oral precancerous conditions. Indian J Cancer. 2004; 41: 25– 31. Available: http://www.ncbi.nlm.nih.gov/pubmed/15105576 15105576
  27. [28]Siemianowicz K, Gminski J, Stajszczyk M, Wojakowski W, Goss M, Machalski M, et al Serum total cholesterol and triglycerides levels in patients with lung cancer. Int J Mol Med. 2000; 5: 201– 205. 10639602
  28. [29]Borgquist S, Butt T, Almgren P, Shiffman D, Stocks T, Orho-Melander M, et al Apolipoproteins, lipids and risk of cancer. Int J Cancer. 2016; 138: 2648– 2656. 10.1002/ijc.30013 26804063 · DOI
  29. [30]Sniderman AD, St-Pierre AC, Cantin B, Dagenais GR, Després JP, Lamarche B. Concordance/discordance between plasma apolipoprotein B levels and the cholesterol indexes of atherosclerotic risk. Am J Cardiol. 2003; 91: 1173– 1177. 10.1016/S0002-9149(03)00262-5 12745098 · DOI · Paper page
  30. [31]Manzato E, Romanato G. Lipid metabolism in cachexia In: Mantovani G, Anker SD, Inui A, Morley JE, Rossi Fanelli F, Scevola D, et al, editors. Cachexia and wasting: a modern approach. Springer; 2006 pp. 191– 194.
  31. [32]Yang JJ, Yu D, Takata Y, Smith-Warner SA, Blot W, White E, et al Dietary fat intake & lung cancer risk: A pooled analysis. J Clin Oncol. 2017; 35: 3055– 3064. 10.1200/JCO.2017.73.3329 28742456 PMC5590804 · DOI
  32. [33]Sørensen J. Lung cancer cachexia: Can molecular understanding guide clinical management? Integr Cancer Ther. 2018; 17: 1000– 1008. 10.1177/1534735418781743 29896984 PMC6142092 · DOI
  33. [34]Kapancik S. The relationship of agmatine deficiency with the lung cancer. Int J Hematol Oncol. 2016; 26: 103– 109. 10.4999/uhod.160971 · DOI
  34. [35]Vassalle C, Sciarrino R, Bianchi S, Battaglia D, Mercuri A, Maffei S. Sex-related differences in association of oxidative stress status with coronary artery disease. Fertil Steril. Elsevier Inc.; 2012; 97: 414– 419.e2. 10.1016/j.fertnstert.2011.11.045 22196713 · DOI
  35. [36]Bellanti F, Matteo M, Rollo T, De Rosario F, Greco P, Vendemiale G, et al Sex hormones modulate circulating antioxidant enzymes: Impact of estrogen therapy. Redox Biol. Elsevier; 2013; 1: 340– 346. 10.1016/j.redox.2013.05.003 24024169 PMC3757703 · DOI
  36. [37]Eckl PM, Bresgen N. Genotoxicity of lipid oxidation compounds. Free Radic Biol Med. Elsevier B.V.; 2017; 111: 244– 252. 10.1016/j.freeradbiomed.2017.02.002 28167130 · DOI
  37. [38]Hussain SP, Harris CC. Inflammation and cancer: An ancient link with novel potentials. Int J Cancer. 2007; 121: 2373– 2380. 10.1002/ijc.23173 17893866 · DOI
  38. [39]Cobanoglu U, Demir H, Cebi A, Sayir F, Alp HH, Akan Z, et al Lipid peroxidation, DNA damage and coenzyme Q10 in lung cancer patients—markers for risk assessment? Asian Pac J Cancer Prev. 2011; 12: 1399– 1403. 22126471
  39. [40]Gönenç A, Özkan Y, Torun M, Şmşek B. Plasma malondialdehyde (MDA) levels in breast and lung cancer patients. J Clin Pharm Ther. 2001; 26: 141– 144. 10.1046/j.1365-2710.2001.00334.x 11350537 · DOI
  40. [41]Ma Y, Zhang L, Rong S, Qu H, Zhang Y, Chang D, et al Relation between Gastric Cancer and Protein Oxidation, DNA Damage, and Lipid Peroxidation. Oxid Med Cell Longev. 2013; 2013: 1– 6. 10.1155/2013/543760 24454985 PMC3886607 · DOI
  41. [42]Gęgotek A, Nikliński J, Žarković N, Žarković K, Waeg G, Łuczaj W, et al Lipid mediators involved in the oxidative stress and antioxidant defence of human lung cancer cells. Redox Biol. 2016; 9: 210– 219. 10.1016/j.redox.2016.08.010 27567474 PMC5007445 · DOI
  42. [43]Chen ZH, Niki E. 4-Hydroxynonenal (4-HNE) has been widely accepted as an inducer of oxidative stress. Is this the whole truth about it or can 4-HNE also exert protective effects? IUBMB Life. 2006; 58: 372– 373. 10.1080/15216540600686896 16754333 · DOI
  43. [44]Zhong H, Yin H. Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: Focusing on mitochondria. Redox Biol. Elsevier; 2015; 4: 193– 199. 10.1016/j.redox.2014.12.011 25598486 PMC4803793 · DOI
  44. [45]Csala M, Kardon T, Legeza B, Lizák B, Mandl J, Margittai É, et al On the role of 4-hydroxynonenal in health and disease. Biochim Biophys Acta—Mol Basis Dis. Elsevier B.V.; 2015; 1852: 826– 838. 10.1016/j.bbadis.2015.01.015 25643868 · DOI
  45. [46]Crohns M, Saarelainen S, Kankaanranta H, Moilanen E, Alho H, Kellokumpu-Lehtinen P. Local and systemic oxidant/antioxidant status before and during lung cancer radiotherapy. Free Radic Res. 2009; 43: 646– 657. 10.1080/10715760902942824 19444690 PMC2691182 · DOI
  46. [47]Manju V, Sailaja JK, Nalini N. Circulating lipid peroxidation and antioxidant status in cervical cancer patients: A case-control study. Clin Biochem. 2002; 35: 621– 625. 10.1016/S0009-9120(02)00376-4 12498996 · DOI
  47. [48]Senthil K, Aranganathan S, Nalini N. Evidence of oxidative stress in the circulation of ovarian cancer patients. Clin Chim Acta. 2004; 339: 27– 32. 10.1016/j.cccn.2003.08.017 14687890 · DOI
  48. [49]Zieba M, Nowak D, Suwalski M, Piasecka G, Grzelewska-Rzymowska I, Tymińska K, et al Enhanced lipid peroxidation in cancer tissue homogenates in non-small cell lung cancer. Monaldi Arch chest Dis = Arch Monaldi per le Mal del torace. 2001; 56: 110– 4. 11499296
  49. [50]Niki E, Noguchi N. Dynamics of antioxidant action of vitamin E. Acc Chem Res. 2004; 37: 45– 51. 10.1021/ar030069m 14730993 · DOI
  50. [51]Gackowski D, Kowalewski J, Siomek A, Olinski R. Oxidative DNA damage and antioxidant vitamin level: Comparison among lung cancer patients, healthy smokers and nonsmokers. Int J Cancer. 2005; 114: 153– 156. 10.1002/ijc.20700 15523686 · DOI
  51. [52]Abiaka C, Al-Awadi F, Al-Sayer H, Gulshan S, Behbehani A, Farghally M, et al Serum antioxidant and cholesterol levels in patients with different types of cancer. J Clin Lab Anal. 2001; 15: 324– 330. 10.1002/jcla.1045 11793433 PMC6807942 · DOI
  52. [53]Vieira Da Costa VA, Vianna LM. Effect of α-tocopherol supplementation on blood pressure and lipidic profile in streptozotocin-induced diabetes mellitus in spontaneously hypertensive rats. Clin Chim Acta. 2005; 351: 101– 104. 10.1016/j.cccn.2004.08.007 15563877 · DOI
  53. [54]Barzegar-Amini M, Ghazizadeh H, Seyedi SM reza, Sadeghnia HR, Mohammadi A, Hassanzade-Daloee M, et al Serum vitamin E as a significant prognostic factor in patients with dyslipidemia disorders. Diabetes Metab Syndr Clin Res Rev. Elsevier Ltd; 2019; 13: 666– 671. 10.1016/j.dsx.2018.11.034 30641786 · DOI
  54. [55]Hasselwander O, McEneny J, McMaster D, Fogarty DG, Nicholls DP, Maxwell AP, et al HDL composition and HDL antioxidant capacity in patients on regular haemodialysis. Atherosclerosis. 1999; 143: 125– 133. 10.1016/S0021-9150(98)00286-X 10208487 · DOI
  55. [56]Moradi H, Pahl M V., Elahimehr R, Vaziri ND. Impaired antioxidant activity of high-density lipoprotein in chronic kidney disease. Transl Res. Mosby, Inc.; 2009; 153: 77– 85. 10.1016/j.trsl.2008.11.007 19138652 · DOI
  56. [57]Matsuda M, Shimomura I. Increased oxidative stress in obesity: Implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obes Res Clin Pract. Asia Oceania Assoc. for the Study of Obesity; 2013; 7: e330– e341. 10.1016/j.orcp.2013.05.004 24455761 · DOI
  57. [58]Cardona F, Tunez I, Tasset I, Murri M, Tinahones FJ. Similar increase in oxidative stress after fat overload in persons with baseline hypertriglyceridemia with or without the metabolic syndrome. Clin Biochem. 2008; 41: 701– 705. 10.1016/j.clinbiochem.2008.03.001 18371305 · DOI
  58. [59]Cardona F, Túnez I, Tasset I, Garrido-Sánchez L, Collantes E, Tinahones FJ. Circulating antioxidant defences are decreased in healthy people after a high-fat meal. Br J Nutr. 2008; 100: 312– 316. 10.1017/S0007114507894347 18184452 · DOI

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Authors
Zabłocka-Słowińska, K., Płaczkowska, S., Skórska, K., Prescha, A., Pawełczyk, K., Porębska, I., Kosacka, M., & Grajeta, H.
Affiliations
  • Wroclaw Medical University (PL)
  • University of Wrocław (PL)
Corresponding author
  • Zabłocka-Słowińska, Katarzyna
  • Płaczkowska, Sylwia
  • Skórska, Katarzyna
  • Prescha, Anna
  • Pawełczyk, Konrad
  • Porębska, Irena
  • Kosacka, Monika
  • Grajeta, Halina
Venue
PLOS ONE
Published
2019-04-11
Volume
14
Issue
4
Pages
e0215246
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2939249800
Cited by
74
References
0
Citations by year
2026: 7 · 2025: 10 · 2024: 14 · 2023: 11 · 2022: 8 · 2021: 15 · 2020: 4 · 2019: 5
FWCI
4.80
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Uniwersytet Medyczny im. Piastów Slaskich we Wroclawiu (grant no ST-758)
Topics
  • Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer and biochemical research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
Keywords
lung cancer, oxidative stress, lipid metabolism, serum lipids, HDL cholesterol, apolipoprotein B, apolipoprotein A-I, lipid peroxidation, 4-hydroxynonenal, malondialdehyde, conjugated dienes, total antioxidant status, total oxidant status, oxidative stress index, vitamin E, vitamin C, sex differences, obesity, hypertriglyceridemia, smoking
MeSH terms
Aged, Cholesterol, Female, Humans, Cholesterol, HDL, Cholesterol, LDL, Lung Neoplasms, Male, Middle Aged, Oxidation-Reduction, Triglycerides, Biomarkers, Case-Control Studies, Apolipoprotein A-I, Oxidative Stress, Lipid Metabolism, Apolipoprotein B-100

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