Clinica Chimica Acta 444 (2015) 66–71

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Invited critical review

Evolutionary aspects of ABO blood group in humans Massimo Franchini ⁎, Carlo Bonfanti Department of Hematology and Transfusion Medicine, Azienda Ospedaliera Carlo Poma, Mantova, Italy

a r t i c l e

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a b s t r a c t

Article history: Received 12 January 2015 Received in revised form 4 February 2015 Accepted 5 February 2015 Available online 14 February 2015

The antigens of the ABO blood group system (A, B and H determinants) are complex carbohydrate molecules expressed on red blood cells and on a variety of other cell lines and tissues. Growing evidence is accumulating that ABO antigens, beyond their key role in transfusion medicine, may interplay with the pathogenesis of many human disorders, including infectious, cardiovascular and neoplastic diseases. In this narrative review, after succinct description of the current knowledge on the association between ABO blood groups and the most severe diseases, we aim to elucidate the particularly intriguing issue of the possible role of ABO system in successful aging. In particular, focus will be placed on studies evaluating the ABO phenotype in centenarians, the best human model of longevity. © 2015 Published by Elsevier B.V.

Keywords: ABO blood group Cancers Infections Cardiovascular diseases Longevity

Contents 1. 2.

Introduction . . . . . . . . . . . . ABO blood group and human diseases 2.1. ABO and infectious diseases . . 2.2. ABO and cancers . . . . . . . 2.3. ABO and cardiovascular disease 2.4. Other diseases . . . . . . . . 3. ABO blood group and evolution . . . 4. Conclusions . . . . . . . . . . . . Conflicts of interest . . . . . . . . . . . References . . . . . . . . . . . . . . .

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1. Introduction The ABO blood group system, discovered in 1901 by the Austrian Nobel Prize Karl Landsteiner [1], consists of three main alleles, two co-dominant A and B and one recessive O, and is controlled by a single gene located on the terminal portion of the long arm of chromosome 9 (9q34.2) [2–4]. The A and B alleles encode slightly different glycosyltransferases that act by adding N-acetylgalactosamine and D-galactose to H substance, a joint precursor side chain which is hence ultimately transformed into A- or B-antigen. Owing to a frameshift mutation, the O allele does not encode a functional enzyme. Therefore, OO carriers who lack the active form of these transferase enzymes continue to express the basic and unmodified H structure, with a solitary terminal

⁎ Corresponding author. Tel.: +39 0376201234; fax: +39 0376220144. E-mail address: [email protected] (M. Franchini).

http://dx.doi.org/10.1016/j.cca.2015.02.016 0009-8981/© 2015 Published by Elsevier B.V.

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fucose moiety attached [5]. The variable combinations of the three main alleles generate four major phenotypes, A, B, AB and O, which are characterized by the presence (or absence) of A and B antigens on the surface of red blood cells (RBCs) and by the presence of natural antibodies against the antigen absent at the RBC surface in serum [1]. However, along with their expression on RBCs, ABO antigens are also widely expressed in body fluids and tissues/cell surfaces, including epithelial cells, sensory neurons, platelets and endothelia of blood vessels [6]. The term histo-blood group ABO is often used to reflect the wide distribution of ABO antigens. Recent evidence suggest that the ABO system could extend its clinical importance beyond immunohematology, transfusion and transplantation medicine, thus playing a role in the pathogenesis of cardiovascular, neoplastic and several other human disorders [7–10]. However, despite the fact that ABO antigens have been known for more than a century, their biological significance remains largely elusive. Therefore, the aim of this narrative review is to summarize the current knowledge on the clinical significance of the ABO

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system, providing a tentative interpretation of the available literature data according to an evolutionary perspective. 2. ABO blood group and human diseases Although several investigators tried to authenticate the potential association between ABO blood group and a variety of diseases over the last 60 years, the results were controversial and somehow disappointing [11]. In the following paragraphs and in Table 1, the most striking associations are described. 2.1. ABO and infectious diseases Microbial agents and humans have interacted for several thousands of years, and it is now rather clear that infectious diseases may influence population genetics as well as the evolution of human genome through selection of specific alleles able to modify the pathogenesis [12]. Since infectious agents often use cell-surface glycosylated receptors for their attachment, it can be easily appreciated how ABO determinants play a key role in determining a differential susceptibility among individuals to various infectious disorders by affecting host–pathogen interactions through their different degrees of glycosylation. In support of this close interaction, certain microbial parasites display a strong molecular mimicry and share blood group antigens with their hosts [13]. A number of examples can be found in this setting, the most interesting involving Plasmodium falciparum and gastro-enteric pathogens. The association between malaria and ABO system is known since nearly 50 years [14]. It has recently been suggested that this severe infection may have played an important role in driving the current ABO distribution among populations in endemic areas [15–23]. In a recent review, Cserti and Dzik critically analyzed the literature on the association between the ABO system and P. falciparum malaria, showing that group O subjects tend to exhibit a favorable outcome than group A individuals [18]. In their experimental studies, Fry and colleagues [22] and Rowe and colleagues [21] provided a biological explanation for this clinical finding. Specifically, the authors found that rosettes of P. falciparum, which are formed between parasitized and uninfected RBCs and are responsible of vas occlusion and severe disease through adhesion to vascular endothelium, were consistently reduced in group O Malian children compared with non-O blood groups. The selective survival advantage against malaria conferred by O blood type is hence consistent with the geographic distribution of ABO antigens worldwide. Two genome wide association studies (GWAS) confirmed the suggestive association between non-O haplotypes and severe malaria [22,23]. The association between ABO and gastric ulcer was the first to be identified. In the 1954 Aird and colleagues already described the higher susceptibility of group O individuals to peptic ulcers [24]. It was later recognized that Helicobacter pylori is the causative agent of peptic ulcer, a disease that can be efficaciously treated by eradicating the bacterium with antibiotics and acid secretion inhibitors. In 1993, Boren and colleagues demonstrated that H. pylori binds to blood group

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O Lewis b (Leb) but not A Leb, thus providing a reasonable background for explaining the greater susceptibility of group O secretors to this infectious agent [25]. Although subsequent studies demonstrated that not all strains are specific for O Leb, it can be generally assumed that H. pylori has an approximately 5-fold increased binding affinity for O Leb compared with A Leb [26]. It is now clear that the ABO/Leb blood group antigens represent one of the major functional receptors for H. pylori in the gastric epithelium, and the blood group antigenbinding adhesin (BabA) has been identified as the leading mediator of this binding [27]. The interaction is important not only for H. pylori adhesion to the stomach surface, but also to anchor the bacterial secretion system to the host cell surface, so that bacterial virulence factors, namely the cytotoxin associated gene (CagA), can be effectively injected into the host cell cytosol [27]. Susceptibility to norovirus infection, which is responsible for the vast majority of cases of acute gastroenteritis in humans, is also closely associated with expression of ABH and Le antigens in the gastrointestinal tract [28,29]. The early study published by Hutson and colleagues in 2002 showed that individuals with an O phenotype were more likely to be infected with norovirus (odds ratio [OR]: 11.8; 95% CI: 1.3–103), whereas subjects with a B blood group antigen had a reduced risk of infection (OR: 0.096; 95% CI: 0.016–0.56) and symptomatic disease (OR: 0; 95% CI: 0–0.999) [30]. Further studies have disclosed that norovirus GI-1 (Norwalk virus) binds preferably to O secretor cells, whereas GII-3 and GII-4 strains bind preferably to A secretor cells [31,32], thus suggesting that the association of ABO blood group antigens with susceptibility to norovirus infection could be strain-dependent rather than genogroup-dependent. Association between ABO blood group antigens and other enteric pathogens has also been described. Harris and colleagues showed that the phenotype group O confers a greater likelihood of severe infection from Vibrio cholerae than non-O blood group phenotypes [33]. Accordingly, Glass and colleagues suggested that the low prevalence of group O and the high prevalence of B blood group observed in the Ganges Delta in Bangladesh could be directly related to selective pressure from this infectious disease, which is reportedly endemic in that area [34]. Similarly, in an outbreak of gastrointestinal infections caused by Escherichia coli O157 in Scotland in 1996, 87.5% (14/16) of patients who died were from group O [35]. 2.2. ABO and cancers Another area that has been extensively studied over the last five decades is that of the association between the ABO blood group types and cancer, with and the most consistent relationship being observed for pancreatic and gastric cancers [36]. In the Nurses' Health Study and Health Professionals Follow-up Study, Wolpin and colleagues [37] found that participants with blood groups A, AB or B were more likely to develop pancreatic cancer compared to those with blood group O (adjusted hazard ratio [aHR] 1.44; 95% CI: 1.14–1.82). Further studies confirmed the protective effect of O group and showed that the A1 allele

Table 1 ABO blood groups and diseases: summary of clinical evidences on the association. Category

Disease

ABO association

References

Infectious diseases

– Plasmodium falciparum malaria – Helicobacter pylori-associated peptic ulcer – Norovirus-associated acute gastroenteritis – Vibrio cholerae infection – Escherichia coli infection – Pancreatic cancer – Gastric cancer – VTE – MI, IS and PAD – Parkinson's disease – Incident cognitive impairment

O blood type protects against severe malaria O Leb is associated with H. pylori infection O blood type is associated with norovirus infection O blood type is associated with severe infection O blood type is associated with severe infection O blood type has a protective effect against pancreatic cancer A blood type is associated with an increased risk of gastric cancer Non-O blood type is associated with an increased VTE risk O blood type has a protective effect against MI, IS, and PAD risks B blood group is associated with Parkinson's disease AB blood group is associated with incident cognitive impairment

[14–23] [24–27] [28–32] [33,34] [35] [37,38] [39,40] [50,51,56,57] [53–55] [65] [67]

Cancers Cardiovascular diseases Other diseases

Abbreviations: VTE, venous thromboembolism, MI, myocardial infarction, IS, ischemic stroke, and PAD, peripheral arterial disease.

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(which is responsible for an increased glycosyltransferase activity) confers a greater risk of pancreatic cancer than the A2 allele [38]. As regards gastric cancer, the higher prevalence of blood group A in patients with carcinoma of the stomach historically observed by several studies [36] has been recently confirmed in a large prospective population-based study involving more than one million of Scandinavian blood donors, who were followed for up to 35 years (OR 1.20; 95% CI: 1.02–1.42) [39]. A similar finding emerged also in the recently published Golestan Cohort Study, which analyzed the association between the ABO blood groups, overall and cause-specific mortality in over 50,000 people recruited between the 2004 and 2008 [40]. Although the underlying mechanisms linking the ABO blood group system and cancer are still largely unknown, one plausible hypothesis involves the ABO blood group-driven regulation of circulating levels of several inflammatory adhesion molecules (i.e., soluble E-selectin, P-selectin and intercellular adhesion molecule-1), which may play a key role in the process of tumorigenesis [36]. Moreover, the recent discovery that von Willebrand factor (VWF), which carries the ABO blood group determinants, is an important modulator of angiogenesis and apoptosis offers an alternative, particularly intriguing pathogenetic hypothesis [41]. 2.3. ABO and cardiovascular disease The ABO blood group system exerts a profound influence on hemostasis, particularly on VWF and, consequently, on factor VIII (FVIII) plasma levels, which are both important prothrombotic risk factors [42]. It is well known, indeed, that individuals of non-O blood group status have VWF and FVIII plasma levels that are approximately 25% higher than the O blood group subjects [43]. The molecular basis of this phenomenon is consistent with the presence of ABH antigenic structures on circulating VWF, which are hence capable to modulate VWF activity through different degrees of glycosylation [44]. Indeed, the addition of A and B antigens generated by A and B glycosyltransferase enzymes on the existing VWF H oligosaccharides has been found to positively modulate VWF levels and activity [44]. With this background, it this not surprising that a number of studies were planned to investigate the existence of an association between the ABO blood type and cardiovascular disease over the last 50 years [44,45]. In this chapter, we focus on the contribution of our group to this field. To assess the hypothesis

that ABO subtypes carry different thrombotic risks (see Fig. 1), we first performed three systematic reviews and meta-analysis to analyze the existing literature on the association between the ABO blood group and hemostasis abnormalities [46–48]. In the first meta-analysis, including 38 studies with 10,305 VTE cases of venous thromboembolism (VTE), we concluded that a non-O blood group phenotype carries an approximately twofold increased risk of venous thrombosis (pooled OR: 2.08; 95% CI: 1.83, −2.37; P b 0.00001) [46]. A weaker, but still significant, association was found between the non-O blood type and arterial thrombosis (OR of 1.28 [95% CI: 1.17–1.40; P b 0.001] for myocardial infarction and 1.17 [95% CI: 1.01–1.35; P = 0.03] for ischemic stroke) in another more recent systematic review conducted on 28 studies enrolling 12,231 patients with myocardial infarction or ischemic stroke [47]. The fact that the association between the non-O blood group and the arterial vascular risk seems to lower than that between the non-O blood group and VTE is particularly intriguing, also considering that higher VWF and FVIII levels are predictors of an increased venous, rather than arterial, risk [49]. If these two meta-analyses highlighted the important role of the non-O blood type in the pathogenesis of thrombosis, in another meta-analysis evaluating 22 studies with 9468 bleeding patients, we demonstrated that the O blood group was associated with VWF levels 25–35% lower than the non-O blood groups, as well as with a moderately increased hemorrhagic risk (pooled OR 1.33; 95% CI: 1.25–1.42; P b 0.001) [48]. Following these three meta-analyses, results were validated in our clinical experience. In a case–control study comparing the ABO blood group distribution in 77 consecutive patients with cerebral vein thrombosis (CVT) and 4272 blood donors, we observed a higher prevalence of the non-O blood type in CVT patients (75% versus 55%) [50]. Therefore, carriers of the non-O blood group were found to have a 2.4-fold increase of risk of CVT (OR 2.44; 95% CI: 1.42–4.26; P = 0.0008). Even more impressive results emerged from another study which analyzed the relationship between the ABO blood group and the occurrence of residual vein obstruction (RVO) in 268 patients with a first episode of deep vein thrombosis [51]. Surprisingly, the non-O blood type was independently associated with an almost 4-fold increased risk of RVO persistence (OR 3.71; 95% CI: 1.61–8.56; P b 0.01). Another field of our investigation was that of the association between the ABO blood type and arterial thrombosis, in which the evidence of the literature was less robust than that regarding

Fig. 1. The hypothesis of ABO-related thrombotic risk.

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the non-O blood group and venous thrombosis [52]. In a retrospective case–control study, we observed a statistically significant difference of the prevalence of the O blood group in patients with coronary heart disease versus healthy controls (40.9% versus 44.5%; P = 0.01) [53]. Therefore, the O blood group was found to confer a 10% protective effect against the risk of developing coronary artery disease, which was maintained also in a logistic regression model including possible confounding factors. A similar protective effect for the O group was also observed for the risk of developing peripheral arterial thrombosis in patients with atrial fibrillation [54]. Thanks to our research and that of other investigators [55–57], the ABO blood type has now been included in a number of scores evaluating the thrombotic risk. For instance, Yang and colleagues assessed the association of blood groups with the National Institute of Health Stroke Scale (NIHSS) score in young stroke patients, and identified the AB subtype as a major predictor of stroke severity [58]. In addition, Gong and colleagues investigated the relation of the ABO blood type and the severity of coronary atherosclerosis assessed by Gensini score, and concluded that blood group A was an independent risk factor (OR 1.44; 95% CI: 1.16–1.80; P = 0.001), whereas group O was a protective factor (OR 0.77; 95% CI: 0.65-0.92; P = 0.004) for serious coronary atherosclerosis [59]. Concerning the suggested moderately increased hemorrhagic risk associated with the O blood type [48], another interesting field of research is to investigate whether or not the O group could be implicated in the development of hemorrhagic adverse events in patients with other concomitant bleeding risk factors. To address this issue, we established the relationship existing between the ABO blood group and bleeding risk during treatment with vitamin K antagonists (VKA) by comparing the ABO distribution between VKA patients with (n = 183) and without (n = 166) hemorrhage [60]. Although we could not find an association between the ABO blood group and the risk of developing VKA-related bleeding complications, we observed a higher prevalence, although not statistically significant, of subjects with the O blood group among patients with more severe hemorrhages. This evidence suggests that the O blood group could be involved in the degree of severity of bleeding complications. To further elucidate this hypothesis, we conducted a retrospective cohort study on 676 patients with major hemorrhagic events, 99 of whom were undergoing VKA therapy [61]. Notably, we found a significantly higher prevalence of the O blood type in orally anti-coagulated patients with gastrointestinal hemorrhage than in those with cerebral hemorrhage (60% versus 33%, P = 0.01), thus showing that the O blood group (which has the lowest VWF levels among the ABO blood groups) is an important risk factor for severe mucosal hemorrhage in patients with other concomitant risk factors for bleeding. This finding is not particularly surprising if one considers that the hemostatic role of VWF is particularly critical at mucosal sites. Indeed, patients with congenital von Willebrand disease experience a bleeding diathesis predominantly at mucosal sites, rather than soft tissue bleeding, intracranial hemorrhage and hemarthroses which are, however, more frequent in patients with severe congenital hemophilia [62].

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2.4. Other diseases Among the various areas of research in this setting, there is a particular interest toward the association between the ABO blood type and neurological disorders, also considering that the ABO groups play a key role in neurogenesis [4]. A few studies have addressed this issue, and conflicting results were generated. The most consisting data regard patients with Parkinson's disease. Although no significant difference was found in the ABO blood group distribution in Parkinson's disease patients compared with controls in two studies conducted by Strang [63] and by Chia and Liu [64], in another study published by Kak and Gordon an excess of blood group B was described [65]. No significant association with the ABO blood groups was reported by Renvoize in patients with Alzheimer's disease [66], while in a recent study the blood group AB and higher FVIII were associated with incident cognitive impairment [67]. This latter finding is very interesting, and is seemingly in agreement with previous observations of an involvement of a coagulation system in the pathogenesis of some neurodegenerative disorders [68]. 3. ABO blood group and evolution The ABO blood group polymorphism represents an admirable example of evolutionary adaptation. An effective means to study this phenomenon is that of investigating the association between the ABO and various diseases. Another important issue to be addressed is whether the ABO blood groups may contribute or not to favor individuals' lifeextension by eluding most serious diseases. For instance, the hypothesis that the non-O blood types could confer a survival advantage to early humans by protecting them from hemorrhages is particularly intriguing. A similar argument has been raised for the occurrence of the gainof-function prothrombotic mutations factor V Leiden and prothrombin 20210GA, which emerged approximately 20,000–25,000 years ago and have been significantly associated with a lower bleeding-related risk of death during pregnancy [69,70]. Different approaches have been attempted to elucidate the role of the ABO blood type on successful aging, as summarized in Table 2 [71]. In particular, investigators focused their research on centenarians, who represent a particularly suitable model for studying the possible factors contributing to extreme longevity [72]. A significant increase of the A blood type was observed by Murray in a study conducted more than half a century ago in healthy elderly males from the UK, although very few subjects were over 100 years of age [73]. In a study carried out on a small sample of very long-lived Turkish population, no similar association was found [74]. Likewise, in a more recent study conducted in Sicilian centenarians, the ABO blood groups did not appear to affect longevity [75]. In a survey of 269 Japanese centenarians, B allele was found to be associated with longevity [76]. By contrast, in a further study conducted in the US by Brecher and Hay [77], the authors retrospectively reviewed the blood group distribution in a cohort of patients stratified by a decade of death, and found that the group B patients had

Table 2 Main studies on the association between ABO blood groups and longevity. First author, year

Country

Study population

Main results

Ref.

Murray, 1961 Sturgeon et al., 1969 Shimizu et al., 2004

United Kingdom Turkey Japan

633 persons aged over 64 years/1482 blood donors 50 persons aged 90–140 years/110 controls 269 centenarians/7153 controls

[73] [74] [76]

Vasto et al., 2011 Brecher and Hay, 2011 Mengoli, 2014 Coppola, 2003

Italy USA Italy Italy

38 centenarians/59 controls 772 patients died 28,129 subjects aged 0–103 years 74 centenarians/110 controls

An excess of group A was observed in healthy elderly males No association was found between ABO blood groups and longevity B blood type was more frequent among centenarians than among controls (29.4% versus 21.9%, P = 0.04) No association was found between ABO blood groups and longevity The percentage of patients with group B declined with age (P b 0.01) The percentage of subject with group B declined with age (P b 0.001) No statistical significant difference was found in O blood type distribution between centenarians and controls (43% versus 35%, P = NS).a VWF levels were significantly higher in centenarians than in controls regardless of the ABO blood type

a

Chi square analysis.

[75] [77] [78] [80]

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an overall decreased survival. This latter finding is in keeping with results of another recent study, with a similar design, published by our group. In brief, a negative association between the B blood group and life-expectancy was found in a large cohort (n = 28,129) of Italian subjects [78]. An explanation for this occurrence could be brought as an association between the B blood type and some aging-associated conditions, including degenerative neurological and neoplastic disorders, reported by some investigators [79]. Another interesting result from our study was that seven out of the ten centenarians (70%) subjects were of the O blood type, which, as previously mentioned, has been found to be a protective factor against cardiovascular diseases through its effect on VWF levels in several studies and meta-analyses. This specific issue was analyzed by Coppola and colleagues [80] in a case–control study comparing the VWF levels and ABO blood group distribution in 74 centenarians and 110 controls. Surprisingly, the antigenic and functional (ristocetin cofactor) plasma levels of the VWF were significantly higher in centenarians than in controls without significant difference between the blood group O or non-O, thus suggesting the existence of mechanisms other than those playing a key role in successful aging. Indeed, a series of genome-wide association studies demonstrated that the ABO locus is a main determinant of the serum levels of soluble intercellular adhesion molecule-1 (sICAM-1), P-selectin, S-selectin and interleukin-6 (IL-6) [81–85]. Since these inflammatory biomarkers are involved in several diseases, including cardiovascular disorders, they may hence play a key role in longevity as well. 4. Conclusions There is a growing evidence that the ABO blood groups may be able to influence the individuals' predisposition to several disorders through their capacity of modulating the hemostatic system and the inflammatory response. In particular, the different prevalence of the ABO group genotypes among populations in various geographical areas was found to be driven by some pathogens, most notably P. falciparum and Vibrio cholera. Other consistent data involve an association between the non-O blood type and cardiovascular disease, especially VTE, so that the addition of the ABO phenotype to the current thrombotic risk scores will probably allow the more accurate calculation of the thrombotic risk of each patient, in order to better tailor primary or secondary antithrombotic prophylaxis. The possibility that the ABO gene may be implied in longevity is still a matter of debate. The studies on the ABO phenotype in centenarians, the best example of successful aging, are largely inconclusive. The findings from Brecher and Hay [77] and our [78] studies that the B allele is a marker for earlier death rather than for longevity are particular intriguing, but need to be supported by further evidences from larger studies. In conclusion, the issue of longevity is particularly challenging. According to the current knowledge, the biological explanation is seemingly multifactorial, being the results of several inherited (i.e., polymorphisms in the ABO, HLA [human leukocyte antigen] and inflammatory response regulating genes) and environmental factors (i.e., dietary, physical, mental and social activity, air quality) that interplay to cope with the aging process [86]. Conflicts of interest The authors declare that they have no conflicts of interest regarding this manuscript. References [1] Landsteiner K. Zur kenntnis der antifermentativen, lytischen und agglutinierenden wirkungendes des blutserums und der lymphe. Zentralbl Bakteriol 1900;27:357–63. [2] Storry JR, Olsson ML. The ABO blood group system revisited: a review and update. Immunohematology 2009;25:48–59.

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Evolutionary aspects of ABO blood group in humans.

The antigens of the ABO blood group system (A, B and H determinants) are complex carbohydrate molecules expressed on red blood cells and on a variety ...
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