Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 
    Users Online: 272
Home Print this page Email this page Small font size Default font size Increase font size


 
 Table of Contents  
EXPERIMENTAL STUDIES
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

Login to access the Email id

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


DOI: 10.4103/2278-0521.94979

Rights and Permissions
  Abstract 

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 2019 Apr 25];1:16-22. Available from: http://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.

Population

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

Click here to view


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

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


Click here to view


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

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

Click here to view
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

Click here to view


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

Click here to view



  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

1.Muentener P, Schlagenhauf P, Steffen R. Imported malaria (1985-95): Trends and perspectives. Bull World Health Organ 1999;77:560-6.  Back to cited text no. 1
[PUBMED]  [FULLTEXT]  
2.Sachs J, Malaney P. The economic and social burden of malaria. Nature 2002;415:680-5.  Back to cited text no. 2
[PUBMED]  [FULLTEXT]  
3.Breman JG, Egan A, Keusch GT. The intolerable burden of malaria: A new look at the numbers. Am J Trop Med Hyg 2001;64(1-2 Suppl): iv-vii.  Back to cited text no. 3
    
4.Cserti CM, Dzik WH. The ABO blood group system and Plasmodium falciparum malaria. Blood 2007;110:2250-8.  Back to cited text no. 4
[PUBMED]  [FULLTEXT]  
5.Uneke CJ. Plasmodium falciparum malaria and ABO blood group: Is there any relationship? Parasitol Res 2007;100:759-65.  Back to cited text no. 5
[PUBMED]  [FULLTEXT]  
6.Fischer PR, Boone P. Short report: Severe malaria associated with blood group. Am J Trop Med Hyg 1998;58:122-3.  Back to cited text no. 6
[PUBMED]  [FULLTEXT]  
7.Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, Greve B, et al. The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis 1999;28:794-9.  Back to cited text no. 7
[PUBMED]  [FULLTEXT]  
8.Pathirana SL, Alles HK, Bandara S, Phone-Kyaw M, Perera MK, Wickremasinghe AR, et al. ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Ann Trop Med Parasitol 2005;99:119-24.  Back to cited text no. 8
[PUBMED]  [FULLTEXT]  
9.Fry AE, Griffiths MJ, Auburn S, Diakite M, Forton JT, Green A, et al. Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet 2008;17:567-76.  Back to cited text no. 9
[PUBMED]  [FULLTEXT]  
10.Rowe JA, Handel IG, Thera MA, Deans AM, Lyke KE, Kone A, et al. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci 2007;104:17471-6.  Back to cited text no. 10
    
11.Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M. Human cerebral malaria: Association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 1990;336:1457-60.  Back to cited text no. 11
[PUBMED]    
12.Ringwald P, Peyron F, Lepers JP, Rabarison P, Rakotomalala C, Razanamparany M, et al. Parasite virulence factors during falciparum malaria: Rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect Immun 1993;61:5198-204.  Back to cited text no. 12
    
13.Thakur A, Verma IC. Malaria and ABO blood groups. Indian J Malariol 1992;29:241-4.  Back to cited text no. 13
[PUBMED]    
14.Kinyanjui SM, Conway DJ, Lanar DE, Marsh K. IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malar J 2007;6:82.  Back to cited text no. 14
[PUBMED]  [FULLTEXT]  
15.WHO: Severe falciparum malaria. World Health Organization, Communicable Diseases Cluster. Trans R Soc Trop Med Hyg 2000; 94 Suppl 1: S1-90.  Back to cited text no. 15
    
16.Nasr A, Iriemenam NC, Troye-Blomberg M, Giha HA, Balogun HA, Osman OF, et al. Fc gamma receptor IIa (CD32) polymorphism and antibody responses to asexual blood-stage antigens of Plasmodium falciparum malaria in Sudanese patients. Scand J Immunol 2007;66:87-96.  Back to cited text no. 16
[PUBMED]  [FULLTEXT]  
17.Nasr A, Iriemenam NC, Giha HA, Balogun HA, Anders RF, Troye-Blomberg M, et al. FcgammaRIIa (CD32) polymorphism and anti-malarial IgG subclass pattern among Fulani and sympatric ethnic groups living in eastern Sudan. Malar J 2009;8:43.  Back to cited text no. 17
[PUBMED]  [FULLTEXT]  
18.Zakeri S, Bereczky S, Naimi P, Pedro Gil J, Djadid ND, Farnert A, et al. Multiple genotypes of the merozoite surface proteins 1 and 2 in Plasmodium falciparum infections in a hypoendemic area in Iran. Trop Med Int Health 2005;10:1060-4.  Back to cited text no. 18
    
19.Ghanchi NK, Martensson A, Ursing J, Jafri S, Bereczky S, Hussain R, et al. Genetic diversity among Plasmodium falciparum field isolates in Pakistan measured with PCR genotyping of the merozoite surface protein 1 and 2. Malar J2010;9:1.  Back to cited text no. 19
    
20.Iriemenam NC, Khirelsied AH, Nasr A, ElGhazali G, Giha HA, Elhassan AE, et al. Antibody responses to a panel of Plasmodium falciparum malaria blood-stage antigens in relation to clinical disease outcome in Sudan. Vaccine 2009;27:62-71.  Back to cited text no. 20
    
21.Perlmann H, Perlmann P, Berzins K, Wahlin B, Troye-Blomberg M, Hagstedt M, et al. Dissection of the human antibody response to the malaria antigen Pf155/RESA into epitope specific components. Immunol Rev 1989;112:115-32.  Back to cited text no. 21
    
22.Barragan A, Kremsner PG, Wahlgren M, Carlson J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun 2000;68:2971-5.  Back to cited text no. 22
[PUBMED]  [FULLTEXT]  
23.Tekeste Z, Petros B. The ABO blood group and Plasmodium falciparum malaria in Awash, Metehara and Ziway areas, Ethiopia. Malar J 2010;9:280.  Back to cited text no. 23
[PUBMED]  [FULLTEXT]  
24.Murphy GS, Oldfield EC 3 rd . Falciparum malaria. Infect Dis Clin North Am 1996;10:747-75.  Back to cited text no. 24
    
25.Kyriacou HM, Steen KE, Raza A, Arman M, Warimwe G, Bull PC, et al. In vitro inhibition of Plasmodium falciparum rosette formation by Curdlan sulfate. Antimicrob Agents Chemother 2007;51:1321-6.  Back to cited text no. 25
[PUBMED]  [FULLTEXT]  
26.Vogt AM, Pettersson F, Moll K, Jonsson C, Normark J, Ribacke U, et al. Release of sequestered malaria parasites upon injection of a glycosaminoglycan. PLoS Pathog 2006;2:e100.  Back to cited text no. 26
[PUBMED]  [FULLTEXT]  
27.(http://hdrstats.undp.org/countries/country_fact_sheets/cty_fs_SDN.html). HDR: The Human Development Index- going beyond income, Sudan. In., 2009;192.  Back to cited text no. 27
    
28.Al-Yaman F, Genton B, Anders RF, Falk M, Triglia T, Lewis D, et al. Relationship between humoral response to Plasmodium falciparum merozoite surface antigen-2 and malaria morbidity in a highly endemic area of Papua New Guinea. Am J Trop Med Hyg 1994;51:593-602.  Back to cited text no. 28
[PUBMED]  [FULLTEXT]  
29.Iriemenam NC, Okafor CM, Balogun HA, Ayede I, Omosun Y, Persson JO, et al. Cytokine profiles and antibody responses to Plasmodium falciparum malaria infection in individuals living in Ibadan, southwest Nigeria. Afr Health Sci 2009;9:66-74.  Back to cited text no. 29
    
30.Metzger WG, Okenu DM, Cavanagh DR, Robinson JV, Bojang KA, Weiss HA, et al. Serum IgG3 to the Plasmodium falciparum merozoite surface protein 2 is strongly associated with a reduced prospective risk of malaria. Parasite Immunol 2003;25:307-12.  Back to cited text no. 30
[PUBMED]  [FULLTEXT]  
31.Sarr JB, Pelleau S, Toly C, Guitard J, Konate L, Deloron P, et al. Impact of red blood cell polymorphisms on the antibody response to Plasmodium falciparum in Senegal. Microbes Infect 2006;8:1260-8.  Back to cited text no. 31
    
32.Baird JK. Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today 1995;11:105-11.  Back to cited text no. 32
[PUBMED]  [FULLTEXT]  
33.Day KP, Marsh K. Naturally acquired immunity to Plasmodium falciparum. Immunol Today 1991;12: A68-71.  Back to cited text no. 33
[PUBMED]    
34.Kanunfre KA, Leoratti FM, Hoffmann EH, Durlacher RR, Ferreira AW, Moraes-Avila SL, et al. Differential recognition of Plasmodium falciparum merozoite surface protein 2 variants by antibodies from malaria patients in Brazil. Clin Diagn Lab Immunol 2003;10:973-6.  Back to cited text no. 34
[PUBMED]  [FULLTEXT]  
35.Shi YP, Sayed U, Qari SH, Roberts JM, Udhayakumar V, Oloo AJ, et al. Natural immune response to the C-terminal 19-kilodalton domain of Plasmodium falciparum merozoite surface 1. Infect Immun 1996;64:2716-23.  Back to cited text no. 35
[PUBMED]  [FULLTEXT]  
36.Courtin D, Oesterholt M, Huismans H, Kusi K, Milet J, Badaut C, et al. The quantity and quality of African children's IgG responses to merozoite surface antigens reflect protection against Plasmodium falciparum malaria. PLoS One 2009;4:e7590.  Back to cited text no. 36
[PUBMED]  [FULLTEXT]  
37.Aribot G, Rogier C, Sarthou JL, Trape JF, Balde AT, Druilhe P, et al. Pattern of immunoglobulin isotype response to Plasmodium falciparum blood-stage antigens in individuals living in a holoendemic area of Senegal (Dielmo, west Africa). Am J Trop Med Hyg 1996;54:449-57.  Back to cited text no. 37
[PUBMED]  [FULLTEXT]  
38.Jafarshad A, Dziegiel MH, Lundquist R, Nielsen LK, Singh S, Druilhe PL. A novel antibody-dependent cellular cytotoxicity mechanism involved in defense against malaria requires costimulation of FcgammaRII and FcgammaRIII. J Immunol 2007;178:3099-106.  Back to cited text no. 38
[PUBMED]  [FULLTEXT]  
39.Tebo AE, Kremsner PG, Luty AJ. Fc gamma receptor-mediated phagocytosis of Plasmodium falciparum-infected erythrocytes in vitro. Clin Exp Immunol 2002;130:300-6.  Back to cited text no. 39
[PUBMED]  [FULLTEXT]  
40.Kay LA, Locke D. Distribution of immunoglobulin G subclasses in anti-A and anti-B sera. J Clin Pathol 1986;39:684-7.  Back to cited text no. 40
[PUBMED]  [FULLTEXT]  
41.Kay LA. Cellular basis of immune response to antigens of ABO blood-group system. Capacity to provide help during response to T-cell-dependent ABO-system antigens is restricted to individuals of blood group O. Lancet 1984;2:1369-71.  Back to cited text no. 41
[PUBMED]  [FULLTEXT]  


    Figures

  [Figure 1]
 
 
    Tables

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


This article has been cited by
1 Antibody responses to P. falciparum Apical Membrane Antigen 1(AMA-1) in relation to haemoglobin S (HbS), HbC, G6PD and ABO blood groups among Fulani and Masaleit living in Western Sudan
Amre Nasr,Ayman M. Saleh,Muna Eltoum,Amir Abushouk,Anhar Hamza,Ahmad Aljada,Mohamed E. El-Toum,Yousif A. Abu-Zeid,Gamal Allam,Gehad ElGhazali
Acta Tropica. 2018; 182: 115
[Pubmed] | [DOI]
2 ABO blood group distribution among endemic Burkitt’s lymphoma patients in Nigeria: Further evidence for the aetiological role of malaria
S. G. Ahmed,M. B. Kagu,U. A. Ibrahim
Journal Africain du Cancer / African Journal of Cancer. 2015; 7(1): 3
[Pubmed] | [DOI]



 

Top
   
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
   Abstract
  Introduction
   Materials and Me...
  Results
  Discussion
  Acknowledgments
   References
   Article Figures
   Article Tables

 Article Access Statistics
    Viewed5068    
    Printed220    
    Emailed1    
    PDF Downloaded587    
    Comments [Add]    
    Cited by others 2    

Recommend this journal