Association of ABO haplotypes with the risk of venous thrombosis: impact on disease risks estimation

Genetic risk score (GRS) analysis is an increasingly popular approach to derive individual risk prediction models for complex diseases. In the context of venous thrombosis (VT), any GRS shall integrate information at the ABO blood group locus, the latter being one of the major susceptibility locus for this disease. However, there is yet no consensus about which single nucleotide polymorphisms (SNPs) must be investigated when one is interested in properly assessing the association of ABO locus with VT risk. Using comprehensive haplotype analyses of ABO blood group tagging SNPs in up to 5,425 cases and 8,445 controls from 6 studies, we demonstrated that using only rs8176719 (tagging O1) to correctly assess the impact of ABO locus on VT risk is suboptimal as 5% of rs8176719-delG carriers are not exposed at higher VT risk. Instead, we recommend to use 4 SNPs, rs2519093 (tagging A1), rs1053878 (A2), rs8176743 (B) and rs41302905 (O2) in any analysis aimed at assessing the impact of ABO locus on VT risk to avoid any risk misestimation. Compared to O1 haplotype that can be inferred from these 4 SNPs, the A2 haplotype is associated with a modest increase in VT risk (odds ratio ~1.2), A1 and B haplotypes are associated with a ~1.8 fold increased risk while O2 tend to be slightly protective (odds ratio ~0.80). In addition, our analyses clearly showed that while the A1 an B blood group are associated with increased vWF and FVIII plasma levels only the A1 blood group is associated wih ICAM plasma levels but in an opposite direction, leaving additional avenues to be explored in order to fully understand the whole spectrum of biological effect of ABO locus on cardiovascular traits.

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The Risk of Venous Thrombosis Related to Increase in Body Mass Index Is Mediated by Factor VIII Induced APC-Resistance.

Blood ◽

10.1182/blood.v114.22.453.453 ◽

2009 ◽

Vol 114 (22) ◽

pp. 453-453 ◽

Cited By ~ 1

Author(s):

Willem M Lijfering ◽

Sverre C Christiansen ◽

Inger-Anne Naess ◽

Jens Hammerstrøm ◽

Astrid van Hylckama Vlieg ◽

...

Keyword(s):

Venous Thrombosis ◽

Blood Group ◽

Odds Ratio ◽

Reference Group ◽

Control Group ◽

Odds Ratios ◽

Apc Resistance ◽

Increased Risk ◽

Fv Leiden ◽

High Bmi

Abstract Abstract 453 Background: The reason why a high BMI predisposes to venous thrombosis is not clarified. People with overweight or obesity tend to be more immobile which may lead to clot formation through stasis. It is also possible that these subjects acquire a prothrombotic state. Factor (F) VIII can be released by adipose tissue through inflammatory cytokines, which consequently might induce APC-resistance. This APC-resistance could be aggravated in case FV Leiden is also present. In addition, presence of high levels of FVIII in non-O blood group subjects could worsen this further. Objective: To determine whether an association exists between BMI and APC-resistance, and whether the combination of both high BMI and APC-resistance increased the risk of venous thrombosis in the Leiden Trombophilia Study (LETS). Whether increasing FVIII levels induced APC-resistance was also studied. In a pooled analysis of LETS and a Norwegian case-cohort study (TROL), we verified if FV Leiden modified the risk of increasing BMI on the occurence of venous thrombosis and whether these risks were further increased by blood group non-O. Methods: Linear regression was used to determine the relation between increasing APC-resistance and BMI, increasing FVIII levels and BMI, increasing APC-resistance and FVIII levels, and between increasing APC-resistance and BMI adjusted for FVIII levels. Cut-off points needed to create tertile categories of APC-resistance were derived from the control-group of the LETS and the TROL population separately. Logistic regression was used to calculate odds ratios and their 95% confidence intervals, adjusted for age and sex. To make the TROL and LETS population more similar for the current analysis, we restricted the analysis in the TROL subjects to those who were younger than 70 and to those who had a DVT only (n=183 cases and n=696 controls). Results: APC-resistance increased linearly with increasing BMI. A same phenomenon was observed for FVIII, i.e. an increase of BMI led to higher FVIII levels. Increased APC-resistance was in its turn associated with an increase of FVIII levels. FVIII explained part of the relation between APC and BMI, as the slope of the regression line of APC-resistance on BMI levels decreased after adjustment for FVIII. To examine the effect of increasing BMI, independent of existing APC-resistance, on the risk of venous thrombosis, we restricted the analysis to subjects from the LETS in whom APC-resistance was not related to other factors such as FV Leiden or oral contraceptive use. In these subjects (n=237 cases and n=369 controls), the risk of venous thrombosis increased 1.4-fold for those with a BMI in the median tertile (odds ratio 1.4; 95% CI, 0.9-2.3) and 2.5-fold for those in the upper tertile (odds ratio 2.5; 95% CI, 1.6-3.9), as compared to subjects in the lowest tertile. Adjustment for APC-resistance or FVIII led to a slight decrease in these relative risk estimates. Non-FV Leiden-carriers with blood group O were only at risk of venous thrombosis when they had a BMI in the upper tertile compared to non-FV Leiden-carriers with blood group O and a BMI in the lowest tertile; (adjusted odds ratio 1.9). This risk was modestly increased when non FV Leiden carriers with non-O blood group were compared with this reference group, with adjusted odds ratios of 1.5, 2.4 and 3.4, respectively, within the BMI tertiles. This risk was strongly increased when FV Leiden carriers with blood group O were compared to the reference group, with adjusted odds ratios of 3.0, 8.3 and 9.7, respectively, within the BMI tertiles. Risk of FV Leiden carriers with non-O blood group showed the highest risk of venous thrombosis compared to the reference group, no longer in a dose-response way, with adjusted odds ratios of 40.6, 23.3 and 25.2, respectively, within the BMI tertiles. Conclusion: The increased risk of venous thrombosis in subjects with high BMI is mediated by FVIII induced APC-resistance. Subjects with FV Leiden and increasing BMI had a higher risk of venous thrombosis compared to non-carriers, and this risks was more than 20 fold increased in carriers of blood group non-O and FV Leiden. Future studies are needed to show if these risks can be downgraded by weight loss. Disclosures: No relevant conflicts of interest to declare.

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Increased risk of venous thrombosis by AB alleles of the ABO blood group and Factor V Leiden in a Brazilian population

Genetics and Molecular Biology ◽

10.1590/s1415-47572009000200010 ◽

2009 ◽

Vol 32 (2) ◽

pp. 264-267 ◽

Cited By ~ 3

Author(s):

Magaly B.P.L.V. Lima ◽

Aldemir Branco de Oliveira-Filho ◽

Júlia F. Campos ◽

Fárida C.B.C. Melo ◽

Washington Batista das Neves ◽

...

Keyword(s):

Venous Thrombosis ◽

Blood Group ◽

Factor V Leiden ◽

Brazilian Population ◽

Abo Blood Group ◽

Factor V ◽

Increased Risk

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ABO blood group, glycosyltransferase activity and risk of Venous Thrombosis

10.1101/2020.03.01.971754 ◽

2020 ◽

Author(s):

Manal Ibrahim Kosta ◽

Pascal Bailly ◽

Monique Silvy ◽

Noemie Saut ◽

Pierre Suchon ◽

...

Keyword(s):

Venous Thrombosis ◽

Blood Group ◽

Plasma Levels ◽

Blood Groups ◽

Abo Blood Group ◽

Abo Blood Groups ◽

Factor Assay ◽

Von Willebrand ◽

First Time ◽

Willebrand Factor

AbstractIntroductionABO blood group influence the risk of venous thrombosis (VT) by modifying A and B glycosyltransferases (AGT and BGT) activities that further modulates Factor VIII (FVIII) and von Willebrand Factor (VWF) plasma levels. The aim of this work was to evaluate the association of plasma GTs activities with VWF/FVIII plasma levels and VT risk in a case-control study.Materials and Methods420 cases were matched with 420 controls for age and ABO blood group. GT activities in plasma were measured using the quantitative transfer of tritiated N-acetylgalactosamine or galactose to the 2’-fucosyl-lactose and expressed in disintegration per minute/30µL of plasma and 2 hours of reaction (dpm/30µL/2H). FVIII and VWF plasma levels were respectively measured using human FVIII-deficient plasma in a 1-stage factor assay and STA LIATEST VWF (Diagnostica Stago).ResultsA and B GT activities were significantly lower in cases than in controls (8119±4027 vs 9682±4177 dpm/30µL/2H, p=2.03 × 10−5, and 4931±2305 vs 5524±2096 dpm/30µL/2H, p=0.043 respectively). This association was observed whatever the ABO blood groups. The ABO A1 blood group was found to explain∼80% of AGT activity. After adjusting for ABO blood groups, AGT activity was not correlated to VWF/FVIII plasma levels. Conversely, there was a moderate correlation (ρ∼0.30) between BGT activity and VWF/ FVIII plasma levels in B blood group carriers.ConclusionThis work showed, for the first time, that GT activities were decreased in VT patients in comparison to controls with the same ABO blood group. The biological mechanisms responsible for this association remained to be determined.

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Is Peripherally Inserted Central Catheter–Related Thrombosis Associated With ABO Blood Group? A Case–Control Pilot Study

Clinical and Applied Thrombosis/Hemostasis ◽

10.1177/1076029618770289 ◽

2018 ◽

Vol 24 (8) ◽

pp. 1297-1300 ◽

Cited By ~ 2

Author(s):

Raad A. Haddad ◽

Yanal Alnimer ◽

Ahmed Abdalla ◽

Carlos F. Ríos-Bedoya ◽

Ghassan Bachuwa

Keyword(s):

Pilot Study ◽

Blood Group ◽

Medical Center ◽

Abo Blood Group ◽

Peripherally Inserted Central Catheter ◽

Central Catheter ◽

Cancer Data ◽

Increased Risk ◽

Group A ◽

Meta Analyses

Peripherally inserted central catheter (PICC) use is associated with many complications including line-related thrombosis. Several studies and meta-analyses confirmed the increased risk to develop venous thromboembolism in non-O blood group individuals. Our pilot study aimed to examine whether PICC-related thrombosis is influenced by ABO blood group. We identified patients admitted to Hurley Medical Center between March 2012 and March 2016 who had PICC placed during their admission, had their ABO blood group identified in their medical record, and had upper extremity venous Doppler ultrasound performed on the same side of PICC. We excluded pregnant women, patients on anticoagulation initiated before PICC insertion, and patients with active cancer. Data of 227 patients who met our criteria were analyzed. Of these patients, 140 (61.7%) patients had PICC-related thrombosis (cases) and 86 (37.9%) patients had O blood group. Controls were patients who had PICC and did not develop PICC-related thrombosis. Multivariate logistic regression revealed no association between PICC-related thrombosis and ABO blood group (adjusted odds ratio: 1.1; 95% confidence interval: 0.6-2.0; P = .733). Therefore, our data suggest that non-O blood group does not increase the odds of having PICC-related thrombosis.

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Musculoskeletal Pain and Impact on Performance in Orchestra Musicians and Actors

Medical Problems of Performing Artists ◽

10.21091/mppa.2004.2009 ◽

2004 ◽

Vol 19 (2) ◽

pp. 55-61

Author(s):

K Engquist ◽

P Ørbaek ◽

K Jakobsson

Keyword(s):

Musculoskeletal Pain ◽

Odds Ratio ◽

Reference Group ◽

Study Groups ◽

Physical Work ◽

Prevalence Odds Ratio ◽

Cross Sectional ◽

Body Regions ◽

Increased Risk ◽

The Impact

We studied the prevalence of musculoskeletal pain and its impact on performance in orchestra musicians and in a reference group of actors, who share the mental stress in a performance situation, but without having the physical work load from an instrument. Swedish musicians (n = 103) from symphony and chamber orchestras and actors (n = 106) participated in a cross-sectional questionnaire study. Musculoskeletal pain was assessed by a further developed Standardized Nordic Questionnaire. The impact of pain on performance (pain affecting playing capacity, decreased playing time, and change of technique) and trouble-related sick leave also was assessed. Pain intensity was assessed by visual analogue scales. Musculoskeletal pain in the neck and shoulders was the most frequently reported problem, with similar prevalence among musicians and actors, around 25% for present pain and 20% for chronic pain (1-year prevalence). Around 10% of the musicians and 5% of the actors reported pain in the hands. Oral pain was reported by 12% of the musicians and 18% of the actors. The number of affected body regions and the intensity of pain were similar in the study groups. The musicians had an increased risk for pain affecting playing capacity. For the neck, the prevalence odds ratio (POR) was 3.0 (95%CI 1.2-7.2; adjusted for age and gender). String instrumentalists had higher risk estimates than nonstring instrumentalists. A gender difference was not observed. Pain in the oral region affecting playing capacity was less common in musicians, with a prevalence odds ratio of 0.4 (95%CI 0.1-0.8). Even though the prevalence of musculoskeletal pain was similar in the two groups of performing artists, the consequences for the work situation were more serious among musicians.

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Association between hydroxocobalamin administration and acute kidney injury after smoke inhalation: a multicenter retrospective study

Critical Care ◽

10.1186/s13054-019-2706-0 ◽

2019 ◽

Vol 23 (1) ◽

Cited By ~ 1

Author(s):

François Dépret ◽

Clément Hoffmann ◽

Laura Daoud ◽

Camille Thieffry ◽

Laure Monplaisir ◽

...

Keyword(s):

Acute Kidney Injury ◽

Retrospective Study ◽

Confidence Interval ◽

Odds Ratio ◽

Adjusted Odds Ratio ◽

Kidney Injury ◽

Smoke Inhalation ◽

Logistic Regression Models ◽

Increased Risk ◽

The Impact

Abstract Background The use of hydroxocobalamin has long been advocated for treating suspected cyanide poisoning after smoke inhalation. Intravenous hydroxocobalamin has however been shown to cause oxalate nephropathy in a single-center study. The impact of hydroxocobalamin on the risk of acute kidney injury (AKI) and survival after smoke inhalation in a multicenter setting remains unexplored. Methods We conducted a multicenter retrospective study in 21 intensive care units (ICUs) in France. We included patients admitted to an ICU for smoke inhalation between January 2011 and December 2017. We excluded patients discharged at home alive within 24 h of admission. We assessed the risk of AKI (primary endpoint), severe AKI, major adverse kidney (MAKE) events, and survival (secondary endpoints) after administration of hydroxocobalamin using logistic regression models. Results Among 854 patients screened, 739 patients were included. Three hundred six and 386 (55.2%) patients received hydroxocobalamin. Mortality in ICU was 32.9% (n = 243). Two hundred eighty-eight (39%) patients developed AKI, including 186 (25.2%) who developed severe AKI during the first week. Patients who received hydroxocobalamin were more severe and had higher mortality (38.1% vs 27.2%, p = 0.0022). The adjusted odds ratio (95% confidence interval) of AKI after intravenous hydroxocobalamin was 1.597 (1.055, 2.419) and 1.772 (1.137, 2.762) for severe AKI; intravenous hydroxocobalamin was not associated with survival or MAKE with an adjusted odds ratio (95% confidence interval) of 1.114 (0.691, 1.797) and 0.784 (0.456, 1.349) respectively. Conclusion Hydroxocobalamin was associated with an increased risk of AKI and severe AKI but was not associated with survival after smoke inhalation. Trial registration ClinicalTrials.gov, NCT03558646

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Prothrombotic State Induced by Middle-Distance Endurance Exercise in Middle-Aged Athletes

Seminars in Thrombosis and Hemostasis ◽

10.1055/s-0038-1667115 ◽

2018 ◽

Vol 44 (08) ◽

pp. 747-755 ◽

Cited By ~ 2

Author(s):

Gian Salvagno ◽

Cantor Tarperi ◽

Matteo Gelati ◽

Martina Montagnana ◽

Elisa Danese ◽

...

Keyword(s):

Blood Coagulation ◽

Blood Group ◽

Thrombin Generation ◽

Area Under The Curve ◽

Abo Blood Group ◽

Middle Aged ◽

Endurance Running ◽

Von Willebrand ◽

The Impact ◽

D Dimer

AbstractSince the impact of possible prothrombotic factors on blood coagulation resulting from exercise remains elusive, this study investigated the acute effects of middle-distance endurance running on blood coagulation parameters in middle-aged athletes. The study population consisted of 33 male endurance runners who were engaged in a 21.1 km run under competitive conditions. Blood samples were collected before the run, immediately after the run, and 3 hours after run completion. Samples were assessed for activated partial thromboplastin time (APTT), prothrombin time (PT), fibrinogen, D-dimer, factor VIII (FVIII), von Willebrand factor antigen (VWF:Ag), endogenous thrombin potential (area under the curve of thrombin generation [TGA-AUC]), and peak thrombin generation (TGA-PK). Post-run variations were expressed as delta (Δ). At baseline, APTT was found to be significantly associated with ABO blood group, VWF:Ag, and FVIII; fibrinogen with age; VWF:Ag with BMI, training regimen, and ABO blood group; APTT with FVIII; FVIII with VWF:Ag and ABO blood group; APTT with VWF:Ag; and TGA-PK with ABO blood group, PT, and TGA-AUC. Immediately after the run, statistically significant increases were observed for PT, D-dimer, VWF:Ag, and FVIII, while statistically significant reductions could be observed for APTT, TGA-AUC, and TGA-PK. Fibrinogen values remained unchanged. Significant correlations were observed between Δ VWF:Ag and Δ FVIII, Δ APTT and Δ VWF:Ag, Δ APTT and Δ FVIII, Δ TGA-AUC and Δ TGA-PK, and between Δ D-dimer and Δ TGA-AUC and Δ TGA-PK. No Δ variation was associated with running time. The results of this study seemingly suggest that middle-distance competitive running may evoke several prothrombotic changes in blood coagulation.

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The influence of ABO blood group on mortality in major trauma

Orthopedic Reviews ◽

10.4081/or.2019.8214 ◽

2019 ◽

Vol 11 (4) ◽

Author(s):

Uwe Hamsen ◽

André Nohl ◽

Andreas Baumann ◽

Rolf Lefering ◽

Laila Boutakmant ◽

...

Keyword(s):

Risk Factor ◽

Injury Severity Score ◽

Blood Group ◽

Severity Score ◽

Injury Severity ◽

Severe Bleeding ◽

Abo Blood Group ◽

Thromboembolic Events ◽

Multiple Injured ◽

The Impact

ABO blood group has a profound influence on hemostasis as it is a major determinant of plasma levels of von Willebrand Factor. In vitro studies suggest that blood group O is a risk factor for increased severe bleeding while blood group non-O is a risk factor for thromboembolic events. Yet, the impact of ABO blood group outcome after multiple trauma is unknown. Retrospective multicenter case-control study from three level-1 trauma centers in Germany from 2012-2015. Inclusion criteria were severe trauma with an Injury severity score ≥9 and admission to an intensive care unit. 1281 patients (69.5% male) were included. Mean Injury Severity Score (ISS) was 21.1±12.4; mean age was 50.2±22.4 years. Distribution of blood groups was: O: 37.4%; A: 44%, B: 12.7 and AB: 5.8%. Hospital mortality depending on blood group was 9.7 (A), 10.4 (B), 6.8 (AB) and 12.7 (O) %. Multivariant logistic regression for mortality revealed an Odds ratio of 0.79 (A), 0.60 (B) and 0.54 (AB) without statistical significance (P=0.35 (A), 0.17 (B), 0.33 (AB)). Thromboembolic events (blood group O vs. others) occurred in 2.8 (O) vs. 3.3 (others) %, P=0.619. In this retrospective study on 1281 multiple injured patients, no relevant influence of ABO blood group on hemorrhage, thromboembolic events and mortality could be found.

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Proton Pump Inhibitors and Dabigatran Therapy: Impact on Gastric Bleeding and Dabigatran Plasma Levels

Seminars in Thrombosis and Hemostasis ◽

10.1055/s-0039-1695735 ◽

2019 ◽

Vol 45 (08) ◽

pp. 846-850 ◽

Cited By ~ 1

Author(s):

Tomáš Bolek ◽

Matej Samoš ◽

Ingrid Škorňová ◽

Peter Galajda ◽

Ján Staško ◽

...

Keyword(s):

Proton Pump Inhibitors ◽

Proton Pump ◽

Plasma Levels ◽

Thrombin Inhibitor ◽

Gi Bleeding ◽

Gastric Bleeding ◽

Increased Risk ◽

The Impact ◽

Dabigatran Therapy

AbstractDabigatran etexilate, a direct thrombin inhibitor, is now frequently used for long-term pharmacological prevention of stroke or systemic embolism in patients with atrial fibrillation. However, such long-term dabigatran therapy (DT) significantly increases the risk of upper gastrointestinal (GI) bleeding. This increased risk of gastric bleeds might be reduced with gastroprotective agents, such as proton pump inhibitors (PPIs). PPIs coadministrated with dabigatran reduce the risk of upper GI bleeding in patients on long-term oral DT. Nevertheless, there is heated discussion regarding interactions between PPI and dabigatran that lead to decreases in dabigatran plasma levels. This article reviews up to date data about the risk of gastric bleeding on dabigatran, the impact of PPI on the reduction of gastric bleeding, and the interaction between PPI and dabigatran leading to decreased dabigatran plasma levels.

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The Impact of NOD2/CARD15, TLR and IL23R Polymorphisms on the Incidence of Infectious Complications in Allo-HSCT Recipients.

Blood ◽

10.1182/blood.v112.11.2201.2201 ◽

2008 ◽

Vol 112 (11) ◽

pp. 2201-2201

Author(s):

Alexandra Maria Holowiecka-Goral ◽

Sebastian Giebel ◽

Jerzy Wojnar ◽

Elzbieta Pietruszka ◽

Agnieszka Karolczyk ◽

...

Keyword(s):

Innate Immunity ◽

Acute Gvhd ◽

Conditioning Regimen ◽

Infectious Complications ◽

Individual Risk ◽

Unrelated Donor ◽

X Rays ◽

Increased Risk ◽

Card15 Gene ◽

The Impact

Abstract BACKGROUND: Infections and graft-vs.-host disease (GvHD) remain the major obstacles for successful allogeneic stem cell transplantation (alloHSCT). As specific immune response is profoundly suppressed during the first months after transplantation, the components of innate immunity are expected to play important role in protection against infections and modulation of GvHD. The goal of this prospective study was to evaluate the impact of NOD2/CARD15 gene, toll-like receptors (TLR), and interleukin-23 receptor (IL-23R) single nucleotide polymorphisms (SNPs), on outcome of alloHSCT, including the incidence of infectious complications and acute GvHD. All these factors were documented to take part in innate immunity. PATIENTS: One-hundred-twenty-five consecutive patients, mainly with hematological malignancies, aged 32 (18–58)y, treated with alloHSCT from HLA-matched related (n=43) or matched unrelated donor (MUD) (n=82) were analyzed. The conditioning regimen was myeloablative, GVHD prophylaxis consisted of cyclosporin, metotrexate, and, in case of MUD-HSCT, pre-transplant anti-thymocyte globulin. METHODS: Donors and recipients were tested for SNP8,12,13 of the NOD2/CARD15 gene, TLR2/753, TLR4/299, TLR4/399, TLR5/C1174T, and TLR9/1635 SNPs, as well as IL23R/11209026 SNP. Study end-points included the incidence of bacterial, fungal and clinically relevant viral infections. Infections were recognized based on clinical symptoms, microbial cultures, chest X-rays for pneumonia confirmation and in case of CMV and EBV- PCR screening. We analyzed separately infections occurring in the early, cytopenic phase and those occurring after engraftment. Additionally, the incidence of acute GvHD and survival was evaluated. RESULTS: Presence of NOD2/CARD15 SNP8 in recipient resulted in higher frequency of neutropenic pneumonia (40% vs. 6%, p=0.045) and bacterial pharyngitis (100% vs. 50%, p=0.06), as well as increased incidence of grade III-IV acute GVHD (40% vs. 7%, p=0.05), which translated into increased non-relapse mortality (60% vs. 14%, p=0.005) and decreased 2-year overall survival (20% vs. 71%, p=0.003). TLR4/299 SNP in recipient tended to increase the risk of neutropenic fever (FUO) (67% vs. 30%, p=0.06) and decrease survival (71% vs. 48%, p=0.09). TLR2/753 SNP in donor was associated with higher incidence of FUO (83% vs. 30%, p-0.01), while TLR5/C1174T SNP in recipient resulted in increased incidence of EBV infection (25% vs. 4%, p-0.05). Presence of IL23R/11209026 SNP in donor tended to increase the incidence of neutropenic pneumonias (29% vs. 6%, p=0.09). CONCLUSIONS: NOD2/CARD15, TLR, and IL23R SNPs appear to influence outcome of alloHSCT contributing to increased incidence of infections, and in case of NOD2/CARD15 SNP8 in recipient to increased risk of severe acute GVHD. The genomic analysis may allow elaboration of adequate preventive strategies based on individual risk assessment. Our results encourage for further, extended studies.

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