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 Table of Contents  
Year : 2012  |  Volume : 1  |  Issue : 1  |  Page : 16-22  

Blood group O protects against complicated Plasmodium falciparum malaria by the mechanism of inducing high levels of anti-malarial IgG antibodies

1 Department of Microbiology, College of Medicine and Medical Science, Taif University, Taif, Saudi Arabia; Faculty of Science and Technology, Al Neelain University, Khartoum, Sudan
2 Department of Haematology, Faculty of Medical Laboratory Science, University of Medical Science and Technology, Khartoum, Sudan
3 Department of ENT, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
4 Department of Biochemistry, Faculty of Medicine, Malaria Research Centre (MalRC), University of Khartoum, Khartoum, Sudan; Department of Clinical Immunology, Faculty of Medicine, King Fahad Medical City, Riyadh, Saudi Arabia

Date of Web Publication13-Apr-2012

Correspondence Address:
Amre Nasr
Department of Microbiology, College of Medicine and Medical Science, Taif University, P.O. Box: 888, Taif, Saudi Arabia

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Source of Support: Ministry of Higher Education and Research, Sudan (MHER.SD. 2009.4771)., Conflict of Interest: None

DOI: 10.4103/2278-0521.94979

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In a prospective clinical study in North Kordofan (Western Sudan), the possible association between blood groups and anti-malarial antibody responses with clinical outcome of Plasmodium falciparum malaria among Sudanese patients was investigated. A total of 184 individuals were consecutively enrolled from an outpatient clinic. Sixty six (35.9%) patients were classified as complicated malaria (CM), 53 (28.8%) with uncomplicated malaria (UM) and 65 (35.3%) were malaria free controls (MFC). Phenotypes of ABO blood groups were typed using commercial anti-sera. The antibody responses to MSP2 malaria antigens were assessed by an enzyme-linked immunosorbent assay (ELISA). The frequency of O blood group was significantly lower in those with CM when compared with MFC and UM patients (P value < 0.001 and 0.002 respectively). The levels of IgG1, IgG2 and IgG3 antibodies were statistically significantly higher in UM and MFC compared with CM patients. Statistical analysis indicated that higher levels of total IgG, IgG1, IgG2, and IgG3 specific to the MSP2 (both antigen forms, 3D7 and FC27) were associated with a reduced risk of complicated CM in O blood type carriers than in non-O blood type carriers, P value <0.001. Taken together, the current study indicates that blood group O is associated with a reduction in the risk of developing complicated malaria in western Sudan. Our results also revealed that the natural acquisition of immunity against clinical malaria appeared to be more associated with IgG1 and IgG3 antibodies, signifying their roles in parasite-neutralizing immune mechanisms.

Keywords: Antimalarial antibodies, blood group, IgG subclass and Sudan, Plasmodium falciparum

How to cite this article:
Nasr A, Eltoum M, Yassin A, ElGhazali G. Blood group O protects against complicated Plasmodium falciparum malaria by the mechanism of inducing high levels of anti-malarial IgG antibodies. Saudi J Health Sci 2012;1:16-22

How to cite this URL:
Nasr A, Eltoum M, Yassin A, ElGhazali G. Blood group O protects against complicated Plasmodium falciparum malaria by the mechanism of inducing high levels of anti-malarial IgG antibodies. Saudi J Health Sci [serial online] 2012 [cited 2022 Jan 24];1:16-22. Available from: https://www.saudijhealthsci.org/text.asp?2012/1/1/16/94979

  Introduction Top

Malaria remains a devastating global health problem. Worldwide, an estimated 300-500 million people contract malaria each year, resulting in 1.5-2.7 million deaths annually. [1],[2] Malaria has a broad distribution in both the subtropics and tropics, with many areas of the tropics endemic for the disease. [3]

ABO and malaria have both been studied for over 100 years, and there are numerous papers on the effects of ABO blood group on various forms of malaria from multiple countries, many coming to contradictory conclusions (covered in some recent reviews) [4],[5] Remarkably, and until recently, there has been no clear answer to the crucial and obvious question: Does ABO blood group affect susceptibility to life-threatening malaria? Preliminary evidence suggested that blood group A might be detrimental [6],[7] and group O protective; [8] however, a definitive case-control study taking into account other potentially confounding malaria risk factors such as hemoglobin variants was lacking. This need has now been met by two recent studies agreeing in their conclusions that blood group O confers resistance to severe malaria. [9],[10]

The virulence of Plasmodium falciparum has been associated with the capacity of the infected RBCs to adhere to uninfected RBCs, leading to rosetting of cells. [11],[12] Previous studies have implicated the ABO blood group type in resetting. [13]

There is accumulating evidence for a role of IgG antibodies in protection against malarial infection and susceptibility to disease. Kinyanjui et al.[14] described long term antibody responses to malaria in Kenyan children. These responses were very brief. The brevity of the response has been traditionally attributed to a skew in the response towards IgG3. Human IgG3 antibodies have a half-life of 8 days, whereas the half-lives of IgG1, IgG2, and IgG4 are up to 23 days.

The present study is aimed to show whether blood group types are associated with the risk of P. falciparum malaria infection. This is in association to the influence of blood group types on the IgG subclass patterns of antibodies to malaria vaccine candidate, antigens was analyzed in symptomatic patients living in western Sudan malaria endemic localities.

  Materials and Methods Top

Study area

This study was conducted at the National Health Insurance Funds Hospital (NHIF) in (Obied) North Kordofan (Western Sudan) state during April and May 2010. North Kordofan is a region that falls between latitude 12°43΄-13°42΄N and longitude 30°14΄-31°55΄E. It is characterized by a dry, hot climate, typically tropical continental with a relatively short raininy season.


Obied (North Kordofan) is an interesting region that combines Afro-Arab, Arabs and non-Arabs ethnic groups. The major inhabitant groups are Arabs which include Kababish, Kawahla, Hamr, Hawawir and the Maganin tribes. The sedentary groups, which are mainly Arabs, include Dar Hamid, Danagla, Gawamaa and Bedaireia. A few sedentary tribes are non-Arabs; they are mainly of Hausa and Fulani origin from West Africa. North Kordofan is an agricultural area (most foods are millet, sorghum, groundnuts and sesame), and pastoral activities (cattle and goats) characterize the way of life of the people in the region.

Selection and description of participants

A prospective clinical study was carried out over one successive malarial transmission season during 2009-2010 in the outpatient clinics at (NHIFH) where patients suspected of having malarial infection were treated by clinicians. Patients, who presented with severe symptoms were admitted to the hospital if they fulfilled the WHO criteria for severe malaria. [15] Full details of the study design, malaria definition, malaria diagnosis and characterization of patient enrolment (clinical findings) was adopted from Nasr et al. 2007. [16] In our study area, the baseline hemoglobin levels are relatively high and symptoms of severe disease occur at relatively low parasite densities (2,500 parasite/ml). Those co-infected with P. falciparum and other infections were excluded from the study.

A total of 184 individuals, who were consecutively enrolled in the study were classified into three groups. Group I: 65 individuals (35.3%) who had negative blood smears for P. falciparum and did not show any clinical symptoms of malaria. These were confirmed by polymerase chain reaction (PCR) and classified as malaria-free control. Group II: 53 individuals (28.8%) comprised of patients with uncomplicated-malaria with positive malaria-parasite film confirmed by PCR, without any symptoms of severe malarial disease (these occur [15] at relatively low parasite densities). Group III: 66 individuals (35.9%), who were diagnosed as complicated (severe) malaria according to WHO criteria for severe malaria, [15] with positive blood film for malaria-parasite and confirmed by PCR. Patients with uncomplicated malaria received standard pyrimethamine/sulfadoxine tablets treatment of 25 mg/kg in divided doses, quinine tablets 10 mg/kg every 8 h for 10 days. On the other hand, patients with severe malaria were admitted to the main hospital and treated with intravenous quinine at a dose of 10 mg/kg ever 8 h, changed to oral treatment as appropriate for a total of 10 days.

The blood samples were collected in the malarial transmission season during 2009-2010, from 184 individuals (age range 4-75 years, median age 31.0 years, 39.7% males). No patients had any known history of hemoglobinopathies such as Sickle cell anemia, Thalassemia, G6PD, Asthma, Hypersensitivity or Diabetes.

Blood collection

Three millilitres of peripheral blood was collected from the individuals into vacuum EDTA tubes. The collected blood samples were centrifuged for 15 min at 250 Xg. The layers of white cells on top of the red blood cells were collected into sterile cryotubes and stored frozen at −20°C for DNA extraction for MSP2 (FC27 and 3D7) genotyping. The plasma was transferred into cryotubes stored at −20°C, until use for antibody detection.

DNA purification

Genomic DNA was purified from the buffy coat cells using a similar version of the Chelex-100 method and then stored at −20°C was described elsewhere. [17]

Genotyping of the msp2 gene

The initial amplification was followed by individual nested PCR reactions using family specific primers for msp2 (FC27 and 3D7), respectively, based on previously described standard protocols. [18],[19] Positive and negative controls were systematically incorporated in each PCR run. The msp2 PCR products were loaded on 2% agarose gels, stained with ethidium bromide, separated by electrophoresis and visualized under UV trans-illumination (GelDoc® , Biorad, Hercules, USA).

Determination of antibodies

The levels of serum antibodies (IgG total and subclasses) to four malaria antigens MSP 2 two alleles (3D7 and FC27) were measured using enzyme-linked immunosorbent assays (ELISA), mainly as previously described. [17],[20],[21] The antibody concentrations were deduced from the log-log correlative coefficient of each IgG subclass standard curve (six dilutions of myeloma proteins of IgG1-4 subclasses), ranging from 0.01 to 3 mg/ml for IgG1, 0.01 to 0.3 mg/ml for IgG2, 0.001 to 0.1 mg/ml for IgG3 and 0.01 to 1 mg/ml for IgG4 according to the manufacturer's recommendation (Biogenesis, Poole, England).

Blood group determination

ABO blood groups were typed by agglutination using commercial anti-sera (Biotech laboratories Ltd, Ipswich, Suffolk, UK). [22],[23] Two drops of whole blood were placed in two different places of a grease-free clean glass slide on which a few drops of anti-sera for blood group A and B was applied. The blood cells and the antigen were mixed with applicator stick. The slide was then tilted to detect for agglutination and the result recorded accordingly. [22],[23]

Statistical analysis

ABO blood group types and antibody levels were analyzed using SPSS version 10.0 (SPSS, Inc, Chicago, IL, USA). Logistic regression analysis was performed with age, sex and antibodies modelled as binary dummy variables (ranked into third distribution using the first third as the reference indicator). Associations were quantified using odds ratios [OR] with 95% confidence intervals [CI] that do not cross 1.00 with P value <0.05, defined as statistically significant.

Ethical clearance

The study protocol was reviewed and approved by the Ethical Review Committee at Faculty of Medical Laboratory Science, University of Medical Science and Technology and national clearance from the Sudanese Ministry of Health. Written informed consent was obtained from all study participants and mothers/caretakers of children under 18 who participated in the study, after explaining the purpose and objective of the study.

  Results Top

This study included 119 individuals with defined clinical malaria manifestations complicated malaria (CM) with median of age=33; range (11-73) years, and uncomplicated malaria patients (UM) with median of age=28; range (4-75) years and 65 malaria free controls {median of age=32; range (11-75) years. The three groups showed similar proportions of risk of complicated malaria in different age groups [Table 1].
Table 1: The risk of complicated malaria in different age groups range 4– 75 years

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Distribution of the ABO blood group types in the study categories

The overall blood group frequencies showed statistically significant difference between the studied categories (P<0.001). No significant differences in ABO blood groups were seen between uncomplicated malaria patients and the malaria-free controls [Table 2] and [Table 3]. This was in contrast to what was seen, when comparing the patients with complicated malaria and those with uncomplicated and malaria-free controls [Table 3]. Logistic regression analysis showed that, blood group O was statistically significant and associated with a reduced risk of complicated malaria when compared with uncomplicated malaria (13.6% versus 47.2%; Odds ratio [OR]=0.13, 95% Confidence interval [CI] [0.4-0.46] and P value=0.002) and when compared with malaria-free control (13.6% versus 49.2%; OR=0.06, 95%CI [0.01-0.26]; and P value <0.001) [Table 3]. Difference was also seen when comparing malaria patients (complicated and uncomplicated malaria) with malaria-free control, where O blood group was at a statistically significantly higher frequency in malaria-free control [28.6% versus 49.2%; OR=0.17, 95% CI [0.05-0.62] and P value=0.008] [Table 3]. With regards to non-O blood group types, no statistical significant differences were found between the study categories [Table 3].
Table 2: Distribution of the ABO blood group types in the study categories

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Table 3: Logistic regression analysis of ABO blood groups types in study categories using AB blood group as
reference value

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Patterns of antibody isotypes in relation to relative risk of malaria infection and complication P. falciparum-specific IgG subclasses antibodies

[Table 4] and [Table 5] show the median ELISA units, 95% CI and P value from logistic regression analyses against a recombinant MSP2 (3D7 and FC27) antigens, respectively. Malarial complication was the dependent variable in the statistical analyses. The levels of both, the 3D7 and FC27 forms of anti-malarial MSP2 antibodies of the different immunoglobulin isotypes differed between the study groups. This was higher in individuals with mild malaria than in those with severe malaria. The CM patients showed lower anti-malarial IgG subclasses antibody levels when compared to the uncomplicated patients [Table 4] and [Table 5]. While, the UM showed higher levels of IgG subclasses antibody when compared to complicated/malaria-free control [Figure 1]a-b and [Table 4] and [Table 5]. The malaria-free controls had the lowest levels of anti-malarial IgG/IgG subclasses antibodies, while UM had higher, although statistically significant, levels of IgG subclasses [Figure 1]a-b, [Table 4] and [Table 5]. No differences in levels of antibodies of the different IgG subclasses were seen among the different ethnicities and age groups within the studies categories (P value = 0.164 and 0.208 respectively).
Table 4: Logistic regression analysis of IgG/IgG- (MSP2-3D7) subclass levels between study categories

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Table 5: Logistic regression analysis of IgG/IgG-(MSP2-FC27) subclass levels between study categories

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Figure 1 (a and b): Comparison of IgG/IgG subclasses antibody levels in study categories. The values were deduced from the log– log correlative coefficient of each of the respective antibody standard curve. The boxes illustrate the total observations corresponding to the 25% and 75% quartile, and the median is represented by the horizontal line. The whiskers illustrate the 10% and 90% quartile, excluding outliers

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The relation of the ABO blood groups and P. falciparum-specific IgG subclass distribution

The relation to ABO blood groups and IgG antibody subclasses were analyzed, using 3D7 and FC27 forms of malarial MSP2 antigens. The result showed that, the IgG/IgG subclasses specific to the MSP2 both antigen forms (3D7 and FC27) were associated with a reduced risk of complicated malaria in O blood type carriers than in non-O blood types carriers, P value <0.001 [Table 6]. In contrast, no correlation between IgG4 MSP2 FC27 antibody levels and carriage of O blood type was found in complicated malaria patients [Table 6].
Table 6: Descriptive statistics of antibody non-parametric tests in relation to ABO blood groups types compared in clinical outcomes

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  Discussion Top

This study provides strong evidence that complicated malaria is reduced in blood group O compared with non-O blood groups (A, B, and AB). Blood group O was statistically significantly associated with reduced risk of complicated malaria, where O blood group was at a statistically significantly higher frequency in malaria-free control. Taken together, the study by Rowe et al., [10] with its focus on pathogenic mechanisms, and that by Fry et al., [9] with its focus on genetic mechanisms, along with the report of Pathirana et al.[24] from Sri Lanka; the finding of greater infant length, placental weight and low placental parasite count among blood group O mothers compared with non-O group in the Gambia, also supports the hypothesis that group O individuals may have survival advantage in severe falciparum malaria infection. Furthermore, according to a study made in Zimbabwe, coma following severe malarial infections was three times more common among A blood group individuals compared with non-A blood group. [23]

The data obtained also supports the hypothesis that malaria parasite rosetting plays a direct role in the pathogenesis of complicated malaria and provides extra impetus for research exploring the potential for rosette disrupting drugs [25],[26] or vaccines [27] as interventions against life-threatening malaria. [10] It also supports previous studies that rosetting is reduced in blood group O erythrocytes compared with the non-O blood groups in P. falciparum laboratory strains and field isolates. [27] Blood group antigens A and B are trisaccharides attached to a variety of glycoprotein's and glycolipids on the surface of erythrocytes, and these trisaccharides are thought to act as receptors for rosetting on uninfected erythrocytes and bind to parasite rosetting legends. [10],[23] However, blood group antigens A and B are not expressed in blood group O individuals. As a result, rosettes formed by blood group O are suggested to be smaller and easily disrupted than rosettes formed by blood group A, B or AB erythrocytes. [27]

This study also assesses the associations between parasite-specific antibody activity and protection from malaria, the levels of both the 3D7 and FC27 forms of anti-malarial MSP2 antibodies of the different immunoglobulin isotypes differed between the study groups; being higher in individuals with mild malaria than in those with complicated malaria. The malaria-free controls had the lowest levels of anti-malarial IgG/IgG subclasses antibodies. The study will agree with other studies that have shown associations between anti-malarial protection and IgG responses directed to MSP2. [28],[29],[30],[31] The slow development of protective immunity is one of the characteristics of the naturally acquired immune response to malaria. The factors that contribute to this slow development have not been fully characterized, but it seems likely that exposure to multiple antigenic variants of malaria parasites [32],[33] plays an important role. There are several antigens associated with the merozoite surface of P. falciparum; that display repetitive amino acid sequences. [34] Insertion and deletion of repeat units, resulting from either mitotic or meiotic recombination, generate new antigenic variants that may be positively evading host's immunity. Thus, high mutation rates coupled with natural selection may accelerate the evaluation of repetitive antigens with clear implications for MSP2 antibodies (3D7 and FC27) forms. [34] The specificity of antibodies to malaria antigens may play an important role in the protective immune response. in vivo protective immunity to malaria correlates with in vitro inhibition of parasite growth by immune IgG, in the presence of blood monocytes, [27] specific IgG are proposed to have either direct [35] or indirect effect [36] on parasite growth inhibition. Among the IgG subclasses, IgG1 and IgG3 are thought to play a key role in the protection. [36],[37] The subclasses can neutralize parasites directly by inhibiting parasite invasion or growth in erythrocytes, or indirectly by a mechanism involving cooperation between parasite-opsonising antibody and monocyte. This mechanism is through binding of the fc gamma receptor IIA (FcγRIIA), leading to secretion of soluble parasite growth-inhibitory factors, such as nitric oxide or tumor necrosis factor-alpha, [36],[38],[39] so the individual may not be protected, until there are sufficient levels of antibodies of the correct specificity and appropriate subclass.

In previous studies, it has been suggested that carriers of blood group O produce a wider range of responses and a greater strength of activation within each IgG subclass. [40] Although, only a few subjects in this study produced strong reactions within IgG1 and IgG3. [40] The Fc proteins of IgG1 and IgG3 induce the macrophage for phagocytosis, via antibody-dependent cellular cytotoxicity (ADCC). In another study, it has been suggested that, subjects of blood group O are able to produce IgG antibodies to non-self ABO system antigens more readily than those of group A or B because there is a greater antigenic disparity between blood group O and groups A/B than that between blood groups A and B. This was postulated to allow a greater ability to provide T cell help during the response to T dependent forms of ABO system antigens in subjects of group O. [41] T-helper cell is known to allow responding B cells to change from IgM production to IgG, giving a less restricted response.

It is not possible to say for sure, that the ABO blood groups affected the specific IgG subclass levels. However, the data obtained using 3D7 and FC27 forms of malarial MSP2 antigens, proved the association between the ABO blood groups and the level of IgG antibody subclasses. In this study, the IgG/IgG subclasses specific to the MSP2, both antigen forms (3D7 and FC27) were increased in blood group O types (non complicated malaria patients) than non group O types (complicated malaria patients). As such, this has proven that there is a strong association between the ABO and specific IgG/IgG subclasses and reduced risk of complicated malaria. To consolidate these results; more studies are required to further establish the association between the ABO blood types and the severity of malarial infection.

  Acknowledgments Top

The authors would like to thank the donors, their families and the staff at NHIF in North Kordofan, for their participation in this study. They, thank Doctors Najm El-Deen Ghanm, Osman Mohamed and Mr. Mohamed Basher at NHIFH, in Obied. We, also thank the staff at Immunology Laboratory at Tropical Medicine Institute, Khartoum, Sudan. Professor Robin Anders is acknowledged, for the supply of MSP-2 FC27 and 3D7 antigens. The authors also thank Hayder Giha and Dr. Nnaemeka C. Iriemenam for assistance with statistical analyses, useful discussion and comments. The Department of hematology, Faculty of Medical Laboratory Science, University of Medical Science and Technology, Khartoum-Sudan for the fruitful discussion, comments and technical support. This work was supported by grants from the Ministry of Higher Education and Research, Sudan (MHER-SD- 2009-4771). All authors read and approved the final version of the manuscript and the authors declare no conflict of interest.

  References Top

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]

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