Biochemical and Biophysical Properties of Red Blood Cells in Disease

A special issue of Biomolecules (ISSN 2218-273X). This special issue belongs to the section "Molecular Biology".

Deadline for manuscript submissions: closed (20 March 2022) | Viewed by 29958

Special Issue Editor

Special Issue Information

Dear Colleagues,

Red blood cells (RBCs, erythrocytes) are highly specialized cells devoted to the transport of respiratory gases. In blood circulation, RBCs are subjected to blood flow-induced shear stress and oxidative stress. To withstand these conditions, RBCs have unique biochemical and biophysical properties, which define their functionality. In a mature state in a healthy person, these cells live in the circulation for 100 to 120 days. However, in numerous pathological conditions (e.g., diabetes, cardiovascular, hemoglobinopathies, malaria) and under aging (in vivo and during storage), the biochemical and biophysical features of RBCs can be drastically altered.

The nature of the membrane of erythrocytes, as well as proteins of the cytoskeleton, their molecular interactions, and the lipid composition of this membrane, the content of ions and water, membrane permeability, and the regulation of signaling pathways through specific receptors are different aspects that determine the unique properties of red blood cells.

RBC research is very dynamic, experiencing interdisciplinary, multifaceted approaches. This journal issue will gather articles addressing biochemical, biophysical, and physiological aspects of RBCs in different pathological states.

Dr. Gregory Barshtein
Guest Editor

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Keywords

  • Pathologies of red blood cells
  • Erythrocytes life cycle
  • RBC membrane
  • Oxygen transport in red blood cells
  • Erythrocyte metabolism

Published Papers (10 papers)

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Editorial

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4 pages, 193 KiB  
Editorial
Biochemical and Biophysical Properties of Red Blood Cells in Disease
by Gregory Barshtein
Biomolecules 2022, 12(7), 923; https://doi.org/10.3390/biom12070923 - 01 Jul 2022
Cited by 4 | Viewed by 1116
Abstract
Red blood cells (RBCs, erythrocytes) are highly specialized cells devoted to the transport of respiratory gases [...] Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)

Research

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19 pages, 21057 KiB  
Article
Filterability of Erythrocytes in Patients with COVID-19
by Dmitry S. Prudinnik, Elena I. Sinauridze, Soslan S. Shakhidzhanov, Elizaveta A. Bovt, Denis N. Protsenko, Alexander G. Rumyantsev and Fazoil I. Ataullakhanov
Biomolecules 2022, 12(6), 782; https://doi.org/10.3390/biom12060782 - 03 Jun 2022
Cited by 2 | Viewed by 1837
Abstract
For the first time, the influence of COVID-19 on blood microrheology was studied. For this, the method of filtering erythrocytes through filters with pores of 3.5 μm was used. Filterability was shown to significantly decrease with the increasing severity of the patient’s condition, [...] Read more.
For the first time, the influence of COVID-19 on blood microrheology was studied. For this, the method of filtering erythrocytes through filters with pores of 3.5 μm was used. Filterability was shown to significantly decrease with the increasing severity of the patient’s condition, as well as with a decrease in the ratio of hemoglobin oxygen saturation to the oxygen fraction in the inhaled air (SpO2/FiO2). The filterability of ≤ 0.65, or its fast decrease during treatment, were indicators of a poor prognosis. Filterability increased significantly with an increase in erythrocyte count, hematocrit and blood concentrations of hemoglobin, albumin, and total protein. The effect of these parameters on the erythrocyte filterability is directly opposite to their effect on blood macrorheology, where they all increase blood viscosity, worsening the erythrocyte deformability. The erythrocyte filterability decreased with increasing oxygen supply rate, especially in patients on mechanical ventilation, apparently not due to the oxygen supplied, but to the deterioration of the patients’ condition. Filterability significantly correlates with the C-reactive protein, which indicates that inflammation affects the blood microrheology in the capillaries. Thus, the filterability of erythrocytes is a good tool for studying the severity of the patient’s condition and his prognosis in COVID-19. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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16 pages, 2483 KiB  
Article
A Potential Citrate Shunt in Erythrocytes of PKAN Patients Caused by Mutations in Pantothenate Kinase 2
by Maike Werning, Verena Dobretzberger, Martin Brenner, Ernst W. Müllner, Georg Mlynek, Kristina Djinovic-Carugo, David M. Baron, Lena Fragner, Almut T. Bischoff, Boriana Büchner, Thomas Klopstock, Wolfram Weckwerth and Ulrich Salzer
Biomolecules 2022, 12(2), 325; https://doi.org/10.3390/biom12020325 - 18 Feb 2022
Cited by 2 | Viewed by 2307
Abstract
Pantothenate kinase-associated neurodegeneration (PKAN) is a progressive neurodegenerative disease caused by mutations in the pantothenate kinase 2 (PANK2) gene and associated with iron deposition in basal ganglia. Pantothenate kinase isoforms catalyze the first step in coenzyme A (CoA) biosynthesis. Since PANK2 is the [...] Read more.
Pantothenate kinase-associated neurodegeneration (PKAN) is a progressive neurodegenerative disease caused by mutations in the pantothenate kinase 2 (PANK2) gene and associated with iron deposition in basal ganglia. Pantothenate kinase isoforms catalyze the first step in coenzyme A (CoA) biosynthesis. Since PANK2 is the only isoform in erythrocytes, these cells are an excellent ex vivo model to study the effect of PANK2 point mutations on expression/stability and activity of the protein as well as on the downstream molecular consequences. PKAN erythrocytes containing the T528M PANK2 mutant had residual enzyme activities but variable PANK2 abundances indicating an impaired regulation of the protein. Patients with G521R/G521R, G521R/G262R, and R264N/L275fs PANK2 mutants had no residual enzyme activity and strongly reduced PANK2 abundance. G521R inactivates the catalytic activity of the enzyme, whereas G262R and the R264N point mutations impair the switch from the inactive to the active conformation of the PANK2 dimer. Metabolites in cytosolic extracts were analyzed by gas chromatography–mass spectrometry and multivariate analytic methods revealing changes in the carboxylate metabolism of erythrocytes from PKAN patients as compared to that of the carrier and healthy control. Assuming low/absent CoA levels in PKAN erythrocytes, changes are consistent with a model of altered citrate channeling where citrate is preferentially converted to α-ketoglutarate and α-hydroxyglutarate instead of being used for de novo acetyl-CoA generation. This finding hints at the importance of carboxylate metabolism in PKAN pathology with potential links to reduced cytoplasmic acetyl-CoA levels in neurons and to aberrant brain iron regulation. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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15 pages, 16388 KiB  
Article
Comparison of Two Alternative Procedures to Obtain Packed Red Blood Cells for β-Thalassemia Major Transfusion Therapy
by Davide Schiroli, Lucia Merolle, Eleonora Quartieri, Roberta Chicchi, Tommaso Fasano, Tiziana De Luca, Giuseppe Molinari, Stefano Pulcini, Thelma A. Pertinhez, Erminia Di Bartolomeo, Rino Biguzzi, Roberto Baricchi and Chiara Marraccini
Biomolecules 2021, 11(11), 1638; https://doi.org/10.3390/biom11111638 - 04 Nov 2021
Cited by 5 | Viewed by 2089
Abstract
β-thalassemia major (βTM) patients require frequent blood transfusions, with consequences that span from allogenic reactions to iron overload. To minimize these effects, βTM patients periodically receive leucodepleted packed red blood cells (P-RBCs) stored for maximum 14 days. The aim of this study was [...] Read more.
β-thalassemia major (βTM) patients require frequent blood transfusions, with consequences that span from allogenic reactions to iron overload. To minimize these effects, βTM patients periodically receive leucodepleted packed red blood cells (P-RBCs) stored for maximum 14 days. The aim of this study was to compare two alternative routine procedures to prepare the optimal P-RBCs product, in order to identify differences in their content that may somehow affect patients’ health and quality of life (QoL). In method 1, blood was leucodepleted and then separated to obtain P-RBCs, while in method 2 blood was separated and leucodepleted after removal of plasma and buffycoat. Forty blood donors were enrolled in two independent centers; couples of phenotypically matched whole blood units were pooled, divided in two identical bags and processed in parallel following the two methods. Biochemical properties, electrolytes and metabolic composition were tested after 2, 7 and 14 days of storage. Units prepared with both methods were confirmed to have all the requirements necessary for βTM transfusion therapy. Nevertheless, RBCs count and Hb content were found to be higher in method-1, while P-RBCs obtained with method 2 contained less K+, iron and storage lesions markers. Based on these results, both methods should be tested in a clinical perspective study to determine a possible reduction of transfusion-related complications, improving the QoL of βTM patients, which often need transfusions for the entire lifespan. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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13 pages, 3886 KiB  
Article
Red Blood Cells’ Thermodynamic Behavior in Neurodegenerative Pathologies and Aging
by Svetla Todinova, Sashka Krumova, Desislava Bogdanova, Avgustina Danailova, Elena Zlatareva, Nikolay Kalaydzhiev, Ariana Langari, Ivan Milanov and Stefka G. Taneva
Biomolecules 2021, 11(10), 1500; https://doi.org/10.3390/biom11101500 - 12 Oct 2021
Cited by 6 | Viewed by 1779
Abstract
The main trend of current research in neurodegenerative diseases (NDDs) is directed towards the discovery of novel biomarkers for disease diagnostics and progression. The pathological features of NDDs suggest that diagnostic markers can be found in peripheral fluids and cells. Herein, we investigated [...] Read more.
The main trend of current research in neurodegenerative diseases (NDDs) is directed towards the discovery of novel biomarkers for disease diagnostics and progression. The pathological features of NDDs suggest that diagnostic markers can be found in peripheral fluids and cells. Herein, we investigated the thermodynamic behavior of the peripheral red blood cells (RBCs) derived from patients diagnosed with three common NDDs—Parkinson’s disease (PD), Alzheimer’s disease (AD), and amyotrophic lateral sclerosis (ALS) and compared it with that of healthy individuals, evaluating both fresh and aged RBCs. We established that NDDs can be differentiated from the normal healthy state on the basis of the variation in the thermodynamic parameters of the unfolding of major RBCs proteins—the cytoplasmic hemoglobin (Hb) and the membrane Band 3 (B3) protein. A common feature of NDDs is the higher thermal stability of both Hb and B3 proteins along the RBCs aging, while the calorimetric enthalpy can distinguish PD from ALS and AD. Our data provide insights into the RBCs thermodynamic behavior in two complex and tightly related phenomena—neurodegenerative pathologies and aging, and it suggests that the determined thermodynamic parameters are fingerprints of the altered conformation of Hb and B3 protein and modified RBCs’ aging in the studied NDDs. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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17 pages, 1968 KiB  
Article
Coagulation Abnormalities in Renal Pathology of Chronic Kidney Disease: The Interplay between Blood Cells and Soluble Factors
by Efthimia G. Pavlou, Hara T. Georgatzakou, Sotirios P. Fortis, Konstantina A. Tsante, Andreas G. Tsantes, Efrosyni G. Nomikou, Athanasia I. Kapota, Dimitrios I. Petras, Maria S. Venetikou, Effie G. Papageorgiou, Marianna H. Antonelou and Anastasios G. Kriebardis
Biomolecules 2021, 11(9), 1309; https://doi.org/10.3390/biom11091309 - 04 Sep 2021
Cited by 14 | Viewed by 6319
Abstract
Coagulation abnormalities in renal pathology are associated with a high thrombotic and hemorrhagic risk. This study aims to investigate the hemostatic abnormalities that are related to the interaction between soluble coagulation factors and blood cells, and the effects of hemodialysis (HD) on it, [...] Read more.
Coagulation abnormalities in renal pathology are associated with a high thrombotic and hemorrhagic risk. This study aims to investigate the hemostatic abnormalities that are related to the interaction between soluble coagulation factors and blood cells, and the effects of hemodialysis (HD) on it, in end stage renal disease (ESRD) patients. Thirty-two ESRD patients under HD treatment and fifteen healthy controls were included in the study. Whole blood samples from the healthy and ESRD subjects were collected before and after the HD session. Evaluation of coagulation included primary and secondary hemostasis screening tests, proteins of coagulation, fibrinolytic and inhibitory system, and ADAMTS-13 activity. Phosphatidylserine (PS) exposure and intracellular reactive oxygen species (iROS) levels were also examined in red blood cells and platelets, in addition to the platelet activation marker CD62P. Platelet function analysis showed pathological values in ESRD patients despite the increased levels of activation markers (PS, CD62P, iROS). Activities of most coagulation, fibrinolytic, and inhibitory system proteins were within the normal range, but HD triggered an increase in half of them. Additionally, the increased baseline levels of ADAMTS-13 inhibitor were further augmented by the dialysis session. Finally, pathological levels of PS and iROS were measured in red blood cells in close correlation with variations in several coagulation factors and platelet characteristics. This study provides evidence for a complex coagulation phenotype in ESRD. Signs of increased bleeding risk coexisted with prothrombotic features of soluble factors and blood cells in a general hyperfibrinolytic state. Hemodialysis seems to augment the prothrombotic potential, while the persisted platelet dysfunction might counteract the increased predisposition to thrombotic events post-dialysis. The interaction of red blood cells with platelets, the thrombus, the endothelium, the soluble components of the coagulation pathways, and the contribution of extracellular vesicles on hemostasis as well as the identification of the unknown origin ADAMTS-13 inhibitor deserve further investigation in uremia. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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16 pages, 2089 KiB  
Article
Ex Vivo Activation of Red Blood Cell Senescence by Plasma from Sickle-Cell Disease Patients: Correlation between Markers and Adhesion Consequences during Acute Disease Events
by Philippe Chadebech, Gwellaouen Bodivit, Gaétana Di Liberto, Alicia Jouard, Corinne Vasseur, France Pirenne and Pablo Bartolucci
Biomolecules 2021, 11(7), 963; https://doi.org/10.3390/biom11070963 - 30 Jun 2021
Cited by 4 | Viewed by 2463
Abstract
BACKGROUND: Blood transfusion remains a key treatment for managing occlusive episodes and painful crises in sickle-cell disease (SCD). In that clinical context, red blood cells (RBCs) from donors and transfused to patients, may be affected by plasma components in the recipients’ blood. Senescence [...] Read more.
BACKGROUND: Blood transfusion remains a key treatment for managing occlusive episodes and painful crises in sickle-cell disease (SCD). In that clinical context, red blood cells (RBCs) from donors and transfused to patients, may be affected by plasma components in the recipients’ blood. Senescence lesion markers appear on the red cells after transfusion, shortening the RBC lifespan in circulation. In the specific context of SCD, senescence signals can also trigger the occlusive painful events, typical of the disease. This work follows through our previous data that described a RBC senescence process, rapidly detected after challenge with SCD pathological plasmas. In this clinical context, we wanted here to further explore the characteristics and physiologic consequences of AA RBC lesions associated with senescence, as lesions caused by RBCs after transfusion may have adverse consequences for SCD patients. METHODS: Plasma samples from SCD patients, with acute symptoms (n = 20) or steady-state disease (n = 34) were co-incubated with donor AA RBCs from blood units for 24 to 48 h. Specific markers signing RBC senescence were quantified after the incubation with SCD plasma samples. The physiologic in-flow adhesion was investigated on senescent RBCs, an in vitro technic into biochips that mimic adherence of RBCs during the occlusive events of SCD. RESULTS: Senescence markers on AA RBCs, together with their in-flow adhesion to the plasma-bridging protein thrombospondin, were associated with the clinical status of the SCD patients from whom plasma was obtained. In these experiments, the highest values were obtained for SCD acute plasma samples. Adhesion of senescent RBCs into biochips, which is not reversed by a pre-treatment with recombinant Annexin V, can be reproduced with the use of chemical agents acting on RBC membrane channels that regulate either Ca2+ entry or modulating RBC hydration. CONCLUSION: We found that markers on red cells are correlated, and that the senescence induced by SCD plasma provokes the adhesion of RBCs to the vessel wall protein thrombospondin. In-flow adhesion of senescent red cells after plasma co-incubations can be reproduced with the use of modulators of RBC membrane channels; activating the Piezo1 Ca2+ mechanosensitive channel provokes RBC adhesion of normal (non-senescent) RBCs, while blocking the Ca2+-dependent K+ Gardos channel, can reverse it. Clinically modulating the RBC adhesion to vascular wall proteins might be a promising avenue for the treatment of painful occlusive events in SCD. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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14 pages, 5635 KiB  
Article
The Erythrocyte Sedimentation Rate and Its Relation to Cell Shape and Rigidity of Red Blood Cells from Chorea-Acanthocytosis Patients in an Off-Label Treatment with Dasatinib
by Antonia Rabe, Alexander Kihm, Alexis Darras, Kevin Peikert, Greta Simionato, Anil Kumar Dasanna, Hannes Glaß, Jürgen Geisel, Stephan Quint, Adrian Danek, Christian Wagner, Dmitry A. Fedosov, Andreas Hermann and Lars Kaestner
Biomolecules 2021, 11(5), 727; https://doi.org/10.3390/biom11050727 - 12 May 2021
Cited by 16 | Viewed by 3870
Abstract
Background: Chorea-acanthocytosis (ChAc) is a rare hereditary neurodegenerative disease with deformed red blood cells (RBCs), so-called acanthocytes, as a typical marker of the disease. Erythrocyte sedimentation rate (ESR) was recently proposed as a diagnostic biomarker. To date, there is no treatment option for [...] Read more.
Background: Chorea-acanthocytosis (ChAc) is a rare hereditary neurodegenerative disease with deformed red blood cells (RBCs), so-called acanthocytes, as a typical marker of the disease. Erythrocyte sedimentation rate (ESR) was recently proposed as a diagnostic biomarker. To date, there is no treatment option for affected patients, but promising therapy candidates, such as dasatinib, a Lyn-kinase inhibitor, have been identified. Methods: RBCs of two ChAc patients during and after dasatinib treatment were characterized by the ESR, clinical hematology parameters and the 3D shape classification in stasis based on an artificial neural network. Furthermore, mathematical modeling was performed to understand the contribution of cell morphology and cell rigidity to the ESR. Microfluidic measurements were used to compare the RBC rigidity between ChAc patients and healthy controls. Results: The mechano-morphological characterization of RBCs from two ChAc patients in an off-label treatment with dasatinib revealed differences in the ESR and the acanthocyte count during and after the treatment period, which could not directly be related to each other. Clinical hematology parameters were in the normal range. Mathematical modeling indicated that RBC rigidity is more important for delayed ESR than cell shape. Microfluidic experiments confirmed a higher rigidity in the normocytes of ChAc patients compared to healthy controls. Conclusions: The results increase our understanding of the role of acanthocytes and their associated properties in the ESR, but the data are too sparse to answer the question of whether the ESR is a suitable biomarker for treatment success, whereas a correlation between hematological and neuronal phenotype is still subject to verification. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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19 pages, 2814 KiB  
Article
Assessment of Fibrinogen Macromolecules Interaction with Red Blood Cells Membrane by Means of Laser Aggregometry, Flow Cytometry, and Optical Tweezers Combined with Microfluidics
by Alexey N. Semenov, Andrei E. Lugovtsov, Evgeny A. Shirshin, Boris P. Yakimov, Petr B. Ermolinskiy, Polina Y. Bikmulina, Denis S. Kudryavtsev, Peter S. Timashev, Alexei V. Muravyov, Christian Wagner, Sehyun Shin and Alexander V. Priezzhev
Biomolecules 2020, 10(10), 1448; https://doi.org/10.3390/biom10101448 - 15 Oct 2020
Cited by 16 | Viewed by 3500
Abstract
An elevated concentration of fibrinogen in blood is a significant risk factor during many pathological diseases, as it leads to an increase in red blood cells (RBC) aggregation, resulting in hemorheological disorders. Despite the biomedical importance, the mechanisms of fibrinogen-induced RBC aggregation are [...] Read more.
An elevated concentration of fibrinogen in blood is a significant risk factor during many pathological diseases, as it leads to an increase in red blood cells (RBC) aggregation, resulting in hemorheological disorders. Despite the biomedical importance, the mechanisms of fibrinogen-induced RBC aggregation are still debatable. One of the discussed models is the non-specific adsorption of fibrinogen macromolecules onto the RBC membrane, leading to the cells bridging in aggregates. However, recent works point to the specific character of the interaction between fibrinogen and the RBC membrane. Fibrinogen is the major physiological ligand of glycoproteins receptors IIbIIIa (GPIIbIIIa or αIIββ3 or CD41/CD61). Inhibitors of GPIIbIIIa are widely used in clinics for the treatment of various cardiovascular diseases as antiplatelets agents preventing the platelets’ aggregation. However, the effects of GPIIbIIIa inhibition on RBC aggregation are not sufficiently well studied. The objective of the present work was the complex multimodal in vitro study of the interaction between fibrinogen and the RBC membrane, revealing the role of GPIIbIIIa in the specificity of binding of fibrinogen by the RBC membrane and its involvement in the cells’ aggregation process. We demonstrate that GPIIbIIIa inhibition leads to a significant decrease in the adsorption of fibrinogen macromolecules onto the membrane, resulting in the reduction of RBC aggregation. We show that the mechanisms underlying these effects are governed by a decrease in the bridging components of RBC aggregation forces. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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Other

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24 pages, 536 KiB  
Opinion
Do We Store Packed Red Blood Cells under “Quasi-Diabetic” Conditions?
by Leonid Livshits, Gregory Barshtein, Dan Arbell, Alexander Gural, Carina Levin and Hélène Guizouarn
Biomolecules 2021, 11(7), 992; https://doi.org/10.3390/biom11070992 - 05 Jul 2021
Cited by 7 | Viewed by 2694
Abstract
Red blood cell (RBC) transfusion is one of the most common therapeutic procedures in modern medicine. Although frequently lifesaving, it often has deleterious side effects. RBC quality is one of the critical factors for transfusion efficacy and safety. The role of various factors [...] Read more.
Red blood cell (RBC) transfusion is one of the most common therapeutic procedures in modern medicine. Although frequently lifesaving, it often has deleterious side effects. RBC quality is one of the critical factors for transfusion efficacy and safety. The role of various factors in the cells’ ability to maintain their functionality during storage is widely discussed in professional literature. Thus, the extra- and intracellular factors inducing an accelerated RBC aging need to be identified and therapeutically modified. Despite the extensively studied in vivo effect of chronic hyperglycemia on RBC hemodynamic and metabolic properties, as well as on their lifespan, only limited attention has been directed at the high sugar concentration in RBCs storage media, a possible cause of damage to red blood cells. This mini-review aims to compare the biophysical and biochemical changes observed in the red blood cells during cold storage and in patients with non-insulin-dependent diabetes mellitus (NIDDM). Given the well-described corresponding RBC alterations in NIDDM and during cold storage, we may regard the stored (especially long-stored) RBCs as “quasi-diabetic”. Keeping in mind that these RBC modifications may be crucial for the initial steps of microvascular pathogenesis, suitable preventive care for the transfused patients should be considered. We hope that our hypothesis will stimulate targeted experimental research to establish a relationship between a high sugar concentration in a storage medium and a deterioration in cells’ functional properties during storage. Full article
(This article belongs to the Special Issue Biochemical and Biophysical Properties of Red Blood Cells in Disease)
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