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Bivariate and Multivariate Analyses of the Influence of Blood Variables of Patients Submitted to Roux-en-Y Gastric Bypass on the Stability of Erythrocyte Membrane against the Chaotropic Action of Ethanol

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Abstract

The stability of the erythrocyte membrane, which is essential for the maintenance of cell functions, occurs in a critical region of fluidity, which depends largely on its composition and the composition and characteristics of the medium. As the composition of the erythrocyte membrane is influenced by several blood variables, the stability of the erythrocyte membrane must have relations with them. The present study aimed to evaluate, by bivariate and multivariate statistical analyses, the correlations and causal relationships between hematologic and biochemical variables and the stability of the erythrocyte membrane against the chaotropic action of ethanol. The validity of this type of analysis depends on the homogeneity of the population and on the variability of the studied parameters, conditions that can be filled by patients who undergo bariatric surgery by the technique of Roux-en-Y gastric bypass since they will suffer feeding restrictions that have great impact on their blood composition. Pathway analysis revealed that an increase in hemoglobin leads to decreased stability of the cell, probably through a process mediated by an increase in mean corpuscular volume. Furthermore, an increase in the mean corpuscular hemoglobin (MCH) leads to an increase in erythrocyte membrane stability, probably because higher values of MCH are associated with smaller quantities of red blood cells and a larger contact area between the cell membrane and ethanol present in the medium.

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References

  • Aloulou I, Varlet-Marie E, Mercier J, Brun JF (2006) Hemorheological disturbances correlate with the lipid profile but not with the NCEP-ATPIII score of the metabolic syndrome. Clin Hemorheol Microcirc 35:207–212

    CAS  PubMed  Google Scholar 

  • Alves de Rezende CH, Coelho LM, Oliveira LM, Penha-Silva N (2009) Dependence of the geriatric depression scores on age, nutritional status, and haematologic variables in elderly institutionalized patients. J Nutr Health Aging 13:617–621

    Article  CAS  PubMed  Google Scholar 

  • Bernardino Neto M (2011) Analysis of correlations between stability of erythrocyte membrane, serum lipids and hematologic variables. Federal University of Uberlândia, Dissertation

    Google Scholar 

  • Cazzola R, Rondanelli M, Russo-Volpe S, Ferrari E, Cestaro B (2004) Decreased membrane fluidity and altered susceptibility to peroxidation and lipid composition in overweight and obese female erythrocytes. J Lipid Res 45:1846–1851

    Article  CAS  PubMed  Google Scholar 

  • Chi LM, Wu WG (1991) Mechanism of hemolysis of red blood cell mediated by ethanol. Biochim Biophys Acta 1062:46–50

    Article  CAS  PubMed  Google Scholar 

  • Cooper RA (1969) Anemia with spur-cells: a red cell defect acquired in serum and modified in the circulation. J Clin Invest 48:1820–1831

    Article  CAS  PubMed  Google Scholar 

  • Cooper RA (1977) Abnormalities of cell-membrane fluidity in the pathogenesis of disease. N Engl J Med 297:371–377

    Article  CAS  PubMed  Google Scholar 

  • Cooper RA, Diloy-Puray M, Lando P, Greenberg MS (1972) An analysis of lipoproteins, bile acids and red cell membrane associated with target cell and spur-cell in patients with liver disease. J Clin Invest 51:3182–3192

    Article  CAS  PubMed  Google Scholar 

  • Cooper RA, Arner EC, Wiley JS, Shattil SJ (1975) Modification of red cell membrane structure by cholesterol-rich lipid dispersions: a model of primary spur-cell defect. J Clin Invest 55:115–126

    Article  CAS  PubMed  Google Scholar 

  • Cribier S, Morrot G, Zachowski A (1993) Dynamics of the membrane lipid phase. Prostaglandins Leukot Essent Fatty Acids 48:24–32

    Article  Google Scholar 

  • Cunha CC, Arvelos LR, Costa JO, Penha-Silva N (2007) Effects of glycerol on the thermal dependence of the stability of human erythrocytes. J Bioenerg Biomembr 39:341–347

    Article  CAS  PubMed  Google Scholar 

  • Custódio Afonso Rocha V, Ramos de Arvelos L, Pereira Felix G, Prado N, de Souza D, Bernardino Neto M, Santos Resende E, Penha-Silva N (2012) Evolution of nutritional, hematologic and biochemical changes in obese women during 8 weeks after Roux-en-Y gastric bypasss. Nutr Hosp 27:1134–1140

    PubMed  Google Scholar 

  • de Freitas MV, Netto RCM, Huss JCC, De Souza TMT, Costa JO, Firmino CB, Penha-Silva N (2008) Influence of aqueous crude extracts of medicinal plants on the osmotic stability of human erythrocytes. Toxicol In Vitro 22:219–224

    Article  PubMed  Google Scholar 

  • de Freitas MV, Oliveira MR, dos Santos DF, de Cássia Mascarenhas Netto R, Fenelon SB, Penha-Silva N (2010) Influence of the use of statin on the stability of erythrocyte membranes in multiple sclerosis. J Membr Biol 233:127–134

  • Fonseca LC, Arvelos LR, Netto RCM, Lins AB, Garrote-Filho MS, Penha-Silva N (2010) Influence of the albumin concentration and temperature on the lysis of human erythrocytes by sodium dodecyl sulfate. J Bioenerg Biomembr 42:413–418

    Article  CAS  PubMed  Google Scholar 

  • Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    CAS  PubMed  Google Scholar 

  • Garcia JJ, Martínez-Ballarín E, Millán-Plano S, Allué JL, Albendea C, Fuentes L, Escanero JF (2005) Effects of trace elements on membrane fluidity. J Trace Elem Med Biol 19:19–22

    Article  CAS  PubMed  Google Scholar 

  • Hair JF, Black B, Babin B, Anderson RE, Tatham RL (2006) Multivariate data analysis. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

  • Hoefner DM, Hodel SD, O’Brien JF, Branum EL, Sun D, Meissner I, McConnell JP (2001) Development of a rapid, quantitative method for LDL subfractionation with use of the Quantimetrix Lipoprint LDL system. Clin Chem 47:266–274

    CAS  PubMed  Google Scholar 

  • Hubbell WL, McConnell HM (1971) Molecular motion in spin-labeled phospholipids and membranes. J Am Chem Soc 93:314–326

    Article  CAS  PubMed  Google Scholar 

  • Khatri P, Sirota M, Butte AJ (2012) Ten years of pathway analysis: current approaches and outstanding challenges. PLoS Comput Biol 8:1–10

    Article  Google Scholar 

  • Kroes J, Ostwald R, Keith A (1972) Erythocyte membrane: compression of lipid phases by increased cholesterol content. Biochim Biophys Acta 274:71–74

    Article  CAS  PubMed  Google Scholar 

  • Lemmich J, Mortensen K, Ipsen JH, Honger T, Bauer R, Mouritsen OG (1997) The effect of cholesterol in small amounts on lipid bilayer softness in the region on the main phase transition. Eur Biophys J 25:293–304

    Article  CAS  PubMed  Google Scholar 

  • Lemos GSD, Márquez-Bernardes LF, Arvelos LR, Paraiso LF, Penha-Silva N (2011) Influence of glucose concentration on the membrane stability of human erythrocytes. Cell Biochem Biophys 61:531–537

    Article  CAS  PubMed  Google Scholar 

  • Li CC (1975) Path analysis: a primer. Boxwood, Pacific Grove, CA

    Google Scholar 

  • Maeda N, Cicha I, Tateishi N, Suzuki Y (2006) Triglyceride in plasma: prospective effects on microcirculatory functions. Clin Hemorheol Microcirc 34:341–346

    CAS  PubMed  Google Scholar 

  • Malandrino N, Wu WC, Taveira TH, Whitlatch HB, Smith RJ (2012) Association between red blood cell distribution width and macrovascular and microvascular complications in diabetes. Diabetologia 55:226–235

    Article  CAS  PubMed  Google Scholar 

  • Mansur PHG, Cury LKP, Leite JOB, Pereira AA, Penha-Silva N, Andrade AO (2010) The approximate entropy of the electromyographic signals of tremor correlates with the osmotic fragility of human erythrocytes. Biomed Eng Online 9:29

    Article  PubMed  Google Scholar 

  • Martínez M, Vayá A, Martí R, Gil L, Lluch I, Carmena R, Aznar J (1996) Erythrocyte membrane cholesterol/phospholipid changes and haemorheological modifications in familial hypercholesterolemia treated with lovastatin. Thromb Res 83:375–388

    Article  PubMed  Google Scholar 

  • Martínez M, Vayá A, Gil L, Martí R, Dalmau J, Aznar J (1998) The cholesterol/phospholipid ratio of the erythrocyte membrane in children with familial hypercholesterolemia. Its relationship with plasma lipids and red blood cell aggregability. Clin Hemorheol Microcirc 18:259–263

    PubMed  Google Scholar 

  • McNeil PL, Steinhardt RA (1997) Loss, restoration and maintenance of plasma membrane integrity. J Cell Biol 137:1–4

    Article  CAS  PubMed  Google Scholar 

  • Michalska-Malecka K, Slowinska L, Dorecka M, Romaniuk W (2008) Correlations in some pathogenetic factors and values of hemorheological parameters in age-related macular degeneration. Clin Hemorheol Microcirc 38:209–216

    CAS  PubMed  Google Scholar 

  • Murray RK, Granner DK (2012) Membranes: structure, assembly and function. In: Murray RK, Bender DA, Botham KM, Kennelly PJ, Rodwell VW, Weil PA (eds) Harper’s illustrated biochemistry, 29th edn. McGraw-Hill, New York

    Google Scholar 

  • Nikolić M, Stanić D, Baricević I, Jones DR, Nedić O, Niketić V (2007) Efflux of cholesterol and phospholipids derived from the haemoglobin-lipid adduct in human red blood cells into plasma. Clin Biochem 40:305–309

    Article  PubMed  Google Scholar 

  • Nishizaki Y, Yamagami S, Suzuki H, Joki Y, Takahashi S, Sesoko M, Yamashita H, Kuremoto K, Shinozaki T, Daida H (2012) Red blood cell distribution width as an effective tool for detecting fatal heart failure in super-elderly patients. Intern Med 51:2271–2276

    Article  PubMed  Google Scholar 

  • Okada M, Matsuto T, Miida T, Obayashi K, Zhu Y, Fueki Y (2004) Lipid analyses for the management of vascular diseases. J Atheroscler Thromb 11:190–199

    Article  CAS  PubMed  Google Scholar 

  • Ozdemirler G, Küçük S, Orhan Y, Aykaç-Toker G, Uysal M (2001) Lipid and protein oxidation in erythrocyte membranes of hypercholesterolemic subjects. Clin Biochem 34:335–339

    Article  CAS  PubMed  Google Scholar 

  • Patel KV, Semba RD, Ferrucci L, Newman AB, Fried LP, Wallace RB, Bandinelli S, Phillips CS, Yu B, Connelly S, Shlipak MG, Chaves PH, Launer LJ, Ershler WB, Harris TB, Longo DL, Guralnik JM (2010) Red cell distribution width and mortality in older adults: a meta-analysis. J Gerontol A Biol Sci Med Sci 65:258–265

    Article  PubMed  Google Scholar 

  • Penha-Silva N, Firmino CB, De Freitas Reis FG, Huss JCC, De Souza TMT, De Freitas MV, Netto RCM (2007) Influence of age on the stability of human erythrocyte membranes. Mech Ageing Dev 128:444–449

    Article  CAS  PubMed  Google Scholar 

  • Penha-Silva N, Arvelos LR, Cunha CC, Aversi-Ferreira TA, Gouvêa-e-Silva LF, Garrote-Filho MS, Finotti CJ, Bernardino-Neto M, de Freitas Reis FG (2008) Effects of glycerol and sorbitol on the thermal dependence of the lysis of human erythrocytes by ethanol. Bioelectrochemistry 73:23–29

    Article  CAS  PubMed  Google Scholar 

  • Raffy S, Teissié J (1999) Control of lipid membrane stability by cholesterol content. Biophys J 76:2072–2080

    Article  CAS  PubMed  Google Scholar 

  • Schick BP, Schick PK (1985) Cholesterol exchange in platelets, erythrocytes and megakaryocytes. Biochim Biophys Acta 833:281–290

    Article  CAS  PubMed  Google Scholar 

  • Seki K, Sumino H, Nara M, Ishiyama N, Nishino M, Murakami M (2006) Relationships between blood rheology and age, body mass index, blood cell count, fibrinogen, and lipids in healthy subjects. Clin Hemorheol Microcirc 34:401–410

    CAS  PubMed  Google Scholar 

  • Shattil SJ, Cooper RA (1976) Membrane microviscosity and human platelet function. Biochemistry 15:4832–4837

    Article  CAS  PubMed  Google Scholar 

  • Shin S, Ku Y-H, Suh J-S, Singh M (2008) Rheological characteristics of erythrocytes incubated in glucose media. Clin Hemorheol Microcirc 38:153–161

    CAS  PubMed  Google Scholar 

  • Shinitzky M, Inbar M (1976) Microviscosity parameters and protein mobility in biological membranes. Biochim Biophys Acta 433:133–149

    Article  CAS  PubMed  Google Scholar 

  • Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of the cell membranes. Science 175:720–731

    Article  CAS  PubMed  Google Scholar 

  • Spengler MI, Bertoluzzo SM, Catalani G, Rasia ML (2008) Study on membrane fluidity and erythrocyte aggregation in equine, bovine and human species. Clin Hemorheol Microcirc 38:171–176

    CAS  PubMed  Google Scholar 

  • Toh SY, Zarshenas N, Jorgensen J (2009) Prevalence of nutrient deficiencies in bariatric patients. Nutrition 25:1150–1156

    Article  CAS  PubMed  Google Scholar 

  • Tziakas DN, Kaski JC, Chalikias GK, Romero C, Fredericks S, Tentes IK, Kortsaris AX, Hatseras DI, Holt DW (2007) Total cholesterol content of erythrocyte membranes is increased in patients with acute coronary syndrome: a new marker of clinical instability? J Am Coll Cardiol 49:2081–2089

    Article  CAS  PubMed  Google Scholar 

  • Tziakas DN, Chalikias GK, Stakos D, Tentes IK, Chatzikyriakou SV, Mitrousi K, Kortsaris AX, Boudoulas H, Kaski JC (2008) Cholesterol composition of erythrocyte membranes and its association with clinical presentation of coronary artery disease. Coron Artery Dis 19:583–590

    Article  PubMed  Google Scholar 

  • Tziakas DN, Chalikias GK, Stakos D, Tentes IK, Papazoglou D, Thomaidi A, Grapsa A, Gioka G, Kaski JC, Boudoulas H (2011) Independent and additive predictive value of total cholesterol content of erythrocyte membranes with regard to coronary artery disease clinical presentation. Int J Cardiol 150:22–27

    Article  PubMed  Google Scholar 

  • Tziakas D, Chalikias G, Grapsa A, Gioka T, Tentes I, Konstantinides S (2012) Red blood cell distribution width: a strong prognostic marker in cardiovascular disease is associated with cholesterol content of erythrocyte membrane. Clin Hemorheol Microcirc 51:243–254

    CAS  PubMed  Google Scholar 

  • Uydu HA, Yıldırmış S, Orem C, Calapoglu M, Alver A, Kural B, Orem A (2012) The effects of atorvastatin therapy on rheological characteristics of erythrocyte membrane, serum lipid profile and oxidative status in patients with dyslipidemia. J Membr Biol 245:697–705

    Article  CAS  PubMed  Google Scholar 

  • Vanderkooi J, Fischkoff S, Chance B, Cooper RA (1974) Fluorescent probe analysis of the lipid architecture of natural and experimental cholesterol-rich membranes. Biochemistry 13:1589–1595

    Article  CAS  PubMed  Google Scholar 

  • Velcheva I, Antonova N, Dimitrova V, Dimitrov N, Ivanov I (2006) Plasma lipids and blood viscosity in patients with cerebrovascular disease. Clin Hemorheol Microcirc 35:155–157

    CAS  PubMed  Google Scholar 

  • Wright S (1923) The theory of path coefficients—a reply to Nile′s criticism. Genetics 8:239–255

    CAS  PubMed  Google Scholar 

  • Yu MM, Xu Y, Zhang JH, Wang CH, Wang XC, Cheng ZP, Xu BL (2010) Total cholesterol content of erythrocyte membranes levels are associated with the presence of acute coronary syndrome and high sensitivity C-reactive protein. Int J Cardiol 145:57–58

    Article  PubMed  Google Scholar 

  • Zilberman-Kravits D, Harman-Boehm I, Shuster T, Meyerstein N (2006) Increased red cell aggregation is correlated with HbA1C and lipid levels in type 1 but not type 2 diabetes. Clin Hemorheol Microcirc 35:463–471

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported with funds from FAPEMIG (CDS APQ-01862-09, CDS-APQ-02025-10 and PPM-00485-12) and CAPES (PE-PNPD AUX 2718/2011).

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Authors and Affiliations

  1. Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Pará, 1720, Uberlândia, MG, 38400-902, Brazil

    Leticia Ramos de Arvelos, Cleine Chagas da Cunha, Morun Bernardino Neto, Mario da Silva Garrote Filho & Nilson Penha-Silva

  2. Clinical Hospital, Federal University of Uberlândia, Av. Pará, 1720, Uberlândia, MG, 38400-902, Brazil

    Vanessa Custódio Afonso Rocha & Conceição de Fátima Pinheiro

  3. Faculty of Medicine, Federal University of Uberlândia, Av. Pará, 1720, Uberlândia, MG, 38400-902, Brazil

    Gabriela Pereira Felix & Elmiro Santos Resende

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  1. Leticia Ramos de Arvelos
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  2. Vanessa Custódio Afonso Rocha
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Correspondence to Nilson Penha-Silva.

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de Arvelos, L.R., Rocha, V.C.A., Felix, G.P. et al. Bivariate and Multivariate Analyses of the Influence of Blood Variables of Patients Submitted to Roux-en-Y Gastric Bypass on the Stability of Erythrocyte Membrane against the Chaotropic Action of Ethanol. J Membrane Biol 246, 231–242 (2013). https://doi.org/10.1007/s00232-013-9524-0

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