The ABO Blood Group System and *Plasmodium falciparum* (*Pf* ) Infection in Three Ethnic Groups Living in the Stable and Seasonal Malaria Transmission Areas of Burkina Faso (BF)

*Edith Christiane Bougouma, Alphonse Ouedraogo and Sodiomon Bienvenu Sirima*

## **Abstract**

Genetic factors, including red blood cell polymorphisms, influence the severity of disease due to infection with *Plasmodium falciparum (Pf)*. Studies show that these genetic factors associated with malaria susceptibility or resistance vary geographically, ethnically, and racially. We performed cross-sectional surveys in population living in rural villages from three ethnic groups. The blood group (BG) was determined genetically using two polymorphisms (rs8176719 and rs8176746). Out of 548 participants, 29.7% were Mossi, 38.2% were Fulani, and 32.1% were Rimaibe. The distribution of BG was, respectively, A: 25.5%, B: 26.6%, AB: 7.3%, and O: 40.5%. BG O was not only the common blood type overall, but was higher in Fulani (52.6%) than others. Fulani was associated with a reduced risk of infection and lower parasite densities than sympatric populations. The subjects with non-O blood were less susceptible to malaria infection. An association between ethnicity and malaria infection during the high transmission season as well as an association between the non-O blood group and malaria infections according to ethnicity was found. This was also true when ethnic groups were considered separately. Our results have demonstrated that the Fulani are not only less susceptible to *Pf* malaria infection, but when infected have lower parasite densities. Individuals with non-O blood are at lower risk of infection.

**Keywords:** ABO blood group system, malaria, *Plasmodium falciparum*, ethnic groups, Burkina Faso

#### **1. Introduction**

Malaria is one of the prevalent infectious diseases globally. In malaria-endemic areas, a significant proportion of children harbor parasites without presenting signs of clinical malaria and are considered asymptomatic cases [1]. Moreover, in communities where children are repeatedly infected with malaria, one can question why some children die while others do not. Variant-specific immunity may help explain chronic low-grade malaria infection without clinical symptoms [2]. A better knowledge of the polymorphic host genes associated with resistance to clinical malaria and/ or with high parasite densities might provide new insights into disease mechanisms, and suggest new approaches for prophylactic or therapeutic interventions [3, 4].

*Plasmodium falciparum* (*Pf*) has been called "the strongest known force for evolutionary selection in the recent history of the human genome [5, 6]. Indeed, the high mortality associated with *Pf* has given it the capacity to select emerging polymorphisms as rapidly as can be witnessed in evolutionary time [7, 8]. Several human genetic factors including red blood cell polymorphisms influence the severity of disease due to infection with *Pf*. To date, there is a paucity of information concerning the role of these host genetic factors (ABO blood group, sickle-cell trait, G6PD deficiency) in asymptomatic malaria, characterized by low-grade *Pf* infection and absence of fever/overt symptoms.

The ABO blood groups consist of A, B, and H carbohydrate antigens which can regulate protein activities during infection and antibodies against these antigens [9–11]. Several studies did try to establish an association between severe malaria and the ABO-blood group type [11–13], with some reporting significant associations on infection status and a particular ABO blood group [11, 13].

The relationship between ABO and malaria was first suggested more than 40 years ago [14]. Few studies have corroborated this hypothesis [8, 11, 14, 15], but some studies showed a weak association [2]. In India, for example, a significantly lower frequency of *Pf* infection was observed among individuals with blood groups A and O [9]. Thus, the selection pressures defining the ABO distributions remain uncertain with contrasting results between studies.

This study aimed to investigate the association between the ABO blood group and malaria susceptibility among Fulani compared to other sympatric ethnic groups living in Burkina Faso.

We offer four perspectives in support of this investigation:


#### **2. Brief review of malaria infection ABO blood groups**

For a long time ago, the ABO blood group system has been suggested to be associated with infectious diseases including malaria. ABO blood groups appear to protect against malaria, through loss of function due to a defective allele: the O phenotype of the ABO system seems to confer protection against *Pf* infection (see **Table 1**).

The human ABO gene consists of seven exons that are more than 18 kb in length and genomic analysis has found over 70 alleles at this locus, suggesting that it is one of the polymorphic genes in humans [1]. The three main antigenic classes (A, B, and O) are all comprised of numerous alleles in both coding and non-coding sequences [1].

The O alleles share a one-nucleotide deletion in codon 87 of exon 6 resulting in a frameshift mutation and premature termination of the polypeptide [2, 3]. O alleles are the most common of the three allelic classes (about 0.6 worldwide) and have frequencies between 0.3 and 0.7 in most populations. The A alleles generally have



frequencies between 0.2 and 0.3, and the B alleles have frequencies between 0.1 and 0.2 [4]. There is substantial evidence supporting the importance of allele O for protecting against malaria, based primarily on the consistency between the worldwide distributions of ABO variants and the historical presence of malaria. Uneke (2007) showed that the O allele, which is more frequent in malaria-endemic regions, is associated with greater resistance to malaria, in contrast to the A and B genotypes, which are less resistant [5]. Fry et al. [6] corroborated this finding through a study in three African populations showing a strong association of O individuals with resistance to severe malaria and a recessive effect in AO and BO individuals. Consequently, AO and BO would have the same susceptibility or sensitivity to malaria as AA and BB individuals; with AB genotype individuals being the most sensitive. The O allele is thought to protect against severe malaria through a mechanism of reduced reinitiation (*i.e.,* spontaneous binding of infected erythrocytes to uninfected erythrocytes) [7].

However, although the major O alleles share a one-nucleotide deletion, they differ in the number of nucleotide substitutions in both exons and introns. The O human alleles, although different from the O chimpanzee allele [8], are much older [1]. The most common O alleles, O01 and O02, are the result of separate mutations and are 1.15 and 2.5 million years old, respectively. In other words, assuming that the O allele protects from malaria, this protection may be a result of selection originally favoring O alleles for some other reason.

### **3. Method**

#### **3.1 Study area**

The study was conducted in four shrub-savanna villages located northeast (Barkoumbilen and Barkoundouba) and east (Bassy and Zanga) of Ouagadougou, the capital city of Burkina Faso (see **Figure 1**).

In the northeast zone, the Mossi and Rimaibè communities inhabit the village of Barkoumbilen, while the Fulani and Rimaibè inhabit the village of Barkoundouba. The Fulani and Rimaibe are present in both villages, so the Rimaibe represent an optimal internal control for the study. The two villages are 5 km apart. In the eastern zone, Mossi and Fulani communities independently inhabit two villages, Zanga and Bassy, about 1(one) km apart.

Malaria transmission in the study areas is hyperendemic and seasonal, with a rainy season from June to October. The entomological inoculation rate (EIR) is estimated to be around 200–300 infecting bites per person per year and is comparable between villages [6]. The main malaria vectors are *Anopheles gambiae* ss, *An. arabiensis* and *An. funestus*. *Plasmodium falciparum* (*Pf*) is responsible for more than 90% of malaria infections.

#### **3.2 Study participants and study period**

The population of the study area is predominantly of the Mossi ethnic group, followed by the widespread Fulani, who are generally closely associated with the Rimaibe (a hybrid of the two in terms of customs and even genetics). All three populations live in similar houses. However, the Fulani group, while adopting the habits of the sedentary Mossi populations, has retained their pastoral activities so that their habitat is characterized by the presence of cattle herds.

The total population of the four villages was obtained from a general census and enrolled in a demographic monitoring process. Except for children under 6 months

*The ABO Blood Group System and* Plasmodium falciparum *(*Pf*) Infection... DOI: http://dx.doi.org/10.5772/intechopen.102475*

#### **Figure 1.**

*Study site in Burkina. The study was carried out in four rural villages of shrubby savannah areas of Burkina Faso: northeast (Nioniokodogo and Barkoundouba), and east (Bassy and Zanga) of the capital town Ouagadougou. Compounds of the various ethnic groups are represented as capital letters. Inset/smaller map represents the study site relative to the whole country.*

of age, the entire population was eligible for the study and was characterized/ designated into two groups: participants aged 0.6 to 17 years and participants aged 18 years and older.

The study was conducted for two consecutive years and consisted of five crosssectional surveys (see **Table 2**).

i. Four surveys during the high malaria transmission seasons: in the middle of August 2007 and 2008; and in the middle of November/December 2007 and 2008.

ii.One survey in the middle of the low transmission/dry season: March 2008.

#### **3.3 Data collection**

Community sensitization meetings were held during which information or explanations about the context of the study, its objectives, its methodological approach, and the associated ethical issues were provided. The signing of written informed consent was a requirement for all study participants, including the guardians of minor children.

Following consent, a clinical team of physicians and nurses examined all participants for clinical signs of malaria, measured weight, and axillary body temperature. Suspected malaria cases (T ≥ 37.5°C) were treated with artemether and lumefantrine.

During the first cross-sectional survey, a two (2) ml venous blood sample was collected from all participants in EDTA tubes.

Thick and thin blood smears were prepared and the hemoglobin level was measured by the HemoCue technique.


#### **Table 2.**

*Population demographic.*

## **3.4 Laboratory methods**

### *3.4.1 Sample collection*

For each subject in this study, physical examination and capillary blood samples on slides and filter papers were collected. Slides were used for the diagnosis of malaria infection and the venous sampling was for the blood group characterization.

## *3.4.2 Blood slides*

Blood slides were stained with Giemsa for microscope identification of the *Plasmodium* species and determination of parasite density.

## *3.4.3 Malaria parasite diagnosis by microscopy*

Blood films were air-dried, the thin films fixed with methanol, and the slide stained with Giemsa. The slides were read by highly experienced laboratory technicians according to the site SOPs. Briefly, 100 high power fields were examined, and the number of malaria parasites/each species and stage was recorded. The number of parasites per microliter of blood was calculated assuming 200 white blood cells per high power field and a fixed white blood cell count of 8000/μL. A slide was considered negative if no parasites were found after the 100 HPF examination. Two independent microscopists read each slide and in case of discrepancy between the two readers, in terms of species, presence or absence of malaria parasites, or if the parasite densities differed by more than 30%, the slide was re-examined by a third laboratory technician. The arithmetic mean of the two closest readings was used as the final value of the parasite density. If there was no agreement after the third reading, the arithmetic mean of the three parasite densities was used.

## *3.4.4 DNA samples*

DNA extraction from the buffy coat (about 1.5 ml in volume) was performed using Nucleon BACC2 Kits. Successful DNA extraction was checked on a 1% agarose gel stained with ethidium bromide. A total of 2235 DNA samples (about 50 μl in

*The ABO Blood Group System and* Plasmodium falciparum *(*Pf*) Infection... DOI: http://dx.doi.org/10.5772/intechopen.102475*

volume) were collected: 825 from Mossi, 877 from Fulani, and 533 from Rimaibè individuals. Samples were stored in screw cap tubes labeled with the study code. Samples were kept at −20°C in cryo boxes. The DNA samples were shipped to the WTCHG in Oxford, UK, in May 2008. The DNA samples of study participants were genotyped at the WTCHG in Oxford, UK.

#### **3.5 Data management**

Demographic variables collected during the census of the four villages include for each person; age, gender, father and mother ethnicity, village, compound, family members and sequential number within the family, and census code. Assignment of ethnicity has been performed with the assistance of local guides.

The census data file was anonymized (name identification has been removed for privacy protection) according to the study protocol which was approved by the ethical committee of Burkina Faso. Clinical data were matched to the census data with study enrolment codes. Case report forms (CRF) for cross-sectional surveys were verified by the supervisor of the clinical study before data entry. Similarly, parasitological data were verified by the lab supervisor before data entry. Data entry was conducted by a team of computer engineers at Ouagadougou, Burkina Faso, and data files were validated by the database manager.

#### **3.6 Statistical analysis**

Data were entered into Microsoft Access. A Chi-square test was used to assess the difference between frequencies/associations between blood groups and *Pf* cases. ANOVA was used to test the difference between mean parasitemia.

Two-sided *p* values were reported, with differences considered significant at *p* ≤ 0.05. All analyses were carried out with the statistical software R 2.10.

#### **3.7 Clearance from National Ethics Committee**

The National Ethics Committee of the Ministry of Health (in Burkina Faso) granted ethical clearance. The study was conducted in compliance with the International Conference on Harmonization, Good Clinical Practices, the Declaration of Helsinki, and applicable Burkina Faso regulatory requirements. Individual written informed consent was obtained from each participant, participant's parents, or legally acceptable representative.

### **4. Results**

This study aimed to investigate *Pf* infection in Burkina Faso in the different ethnic groups: Fulani, Rimaibe, and Mossi according to the ABO group.

#### **4.1 Characteristics of the study participants**

A total of 548 subjects (380 children and 178 adults) were included in this study: Mossi, n = 163 (29.7%), Fulani, n = 209 (38.2%), and Rimaibe, n = 176 (32.1%). **Table 2** shows baseline demographic characteristics according to ethnicity. We did not find any significant difference among the three ethnic groups. The ABO blood group analysis in all children revealed that O antigen: 40.5% (222/548) was the most predominant, followed by A: 25.5% (140/548), B: 26.6% (146/548), and AB: 7.3% (40/548) antigens.

Blood group O was not only the commonest blood type overall, but was higher in the Fulani (n = 110 (52.6%)) than Mossi (n = 48 (29.4%)) and Rimaibe (n = 64 (36.4%)).

## **4.2 Malaria infection**

The malariometric indices for each cross-sectional survey are summarized in **Table 3**. The prevalence of *Pf* infection decreased from 51.6% during the high transmission season to 18.4% in the low season; the prevalence of clinical malaria also decreased significantly from 9.5% to 0.7%. The geometric mean parasite density according to the season (high transmission season and low transmission season) was represented in **Table 3**.

## **4.3 Malaria infection and ethnicity**

The study showed that during the period of high transmission, there was an association between ethnicity and malaria infection (*p* = 0.039). Subjects from the Fulani ethnic group were associated with a reduced risk of *Pf* infection (0.0001 and *p* = 0.02 for Fulani vs. Mossi/Rimaibe respectively during the start and end of the high transmission season). As a result, the Fulani ethnic group had lower parasite densities than the sympatric populations during the high transmission season: The mean density by ethnicity was 374 (251–557), respectively; 865 (598–1252); 483 (331–708) parasites/μl for Fulani, Mossi & Rimaibe (**Table 4**).


*The ABO Blood Group System and* Plasmodium falciparum *(*Pf*) Infection... DOI: http://dx.doi.org/10.5772/intechopen.102475*


#### *\*Survey number.*

*1: First survey, the middle of high malaria transmission season (August 2008).*

*2: Second survey, the end of high malaria transmission season (Nov 2008).*

*3: Third survey, the middle of the dry low transmission season (March 2008).*

*4: The fourth survey, the start of the high transmission season (July 2008).*

*5: Fifth survey, the end of the high transmission season (November/December 2008).*

#### **Table 3.**

*Malariometric indices according to the ethnicity group/survey.*



#### **Table 4.**

*Malariometric indices according to the ethnicity and blood group/season.*

## **4.4 Malaria infection and ABO blood groups**

The subjects with Non-O blood (i.e. A, B, or AB) were less susceptible to malaria infection (*p* = 0.011). We found also a significant difference when Non-O groups were considered separately (O versus A, *p* = 0.028; O versus B, *p* = 0.04; O versus AB, *p* = 0.0067). **Table 5** shows malaria infection according to the blood group. Parasitological data did not differ when comparing subjects with and without blood group O, the most prevalent blood group in the population sample.

## **4.5 Malaria infection, ABO blood groups, and ethnicity**

There was an association between the Non-O blood group of all ethnicities and malaria infections during high transmission. However, this association disappeared when the ethnic groups were considered separately (all ethnicities *p* = 0.011; Mossi: *p* = 0.56; Fulani: *p* = 0.59; Rimaibe: *p* = 0.49) (**Table 5**). Likewise, in the low transmission season, the difference in malaria infection between subjects with and without blood group O was not statistically significant (all ethnicities *p* = 0.86 Mossi: *p* = 0.72, Fulani: *p* = 0.94, Rimaibe: *p* = 0.91 On the other hand, a weak association between the Fulani and the Mossi with the


#### **Table 5.**

*The p values for the frequency of O and non-O blood group types between the three ethnic groups according to malaria infection and parasite density.*

antigen of blood group O and the prevalence of asymptomatic malaria was found (61.7% with the Mossi against 45.5% with the Fulani; *p* = 0.05). Considering the subjects of blood group B, the study showed an association between Fulani versus Mossi/Rimaibe, *p* = 0.001; Fulani versus Mossi, P *p* = 0.02 and Fulani versus Rimaibe, *p* = 0.003.

## **5. Discussion**

This study revealed that blood group O represented the most observed phenotype among participants (40.5%), followed by blood group B (26.6%), then blood group A (25.5%), and finally the AB blood group, which is rarer (7.3%). These results are consistent with those of previous studies that reported a high frequency of group O phenotypes in areas endemic to malaria [5, 9–13].

Other studies have corroborated this evidence by the inverse relationship: they have reported a high prevalence of blood group A and a low prevalence of phenotypes of blood group O in colder regions where malaria is an exotic disease [5, 10, 14].

These results would confirm the hypothesis of a selective evolutionary advantage (survival) of *Pf* infection on blood group O cells compared to other blood groups (A, B, or AB) in malaria-endemic areas [4].

The results of this study according to ethnicity also showed that Fulani were less infected with malaria despite their way of life and living in the same conditions of hyperendemic transmission. These were comparable to observations in previous studies in Burkina Faso and West Africa [15, 16].

Like the study carried out in Gabon by Monbo et al. [17], this study showed a high prevalence of malaria infection in participants with blood group O compared to participants with blood groups A, B, or AB; and is in contrast to previous studies that suggested individuals of blood groups A, B, and AB is more susceptible to *Pf* infection than group O [6, 18].

Lower parasite densities in subjects of blood group O compared to non-O subjects were observed, but the differences were not statistically significant. These observations are in line with the conclusions of previous studies which have shown that patients with blood group O were associated with increased protection against parasitemia [18–23].

These results would suggest a protective effect of the O antigen against clinical malaria. However, other explanations, such as the anti-rosette formation effect associated with blood group antigens, should also be considered [24].

In any case, this study made it possible to establish the involvement of Fulani groups against malaria infection and parasitemia. It also revealed that for all ethnicities combined, there would be a statistically significant difference in susceptibility to malaria between participants of blood groups O and participants of other blood groups (A, B, and AB).

The absence of any statistically significant difference in susceptibility to malaria in an intra-ethnic blood group analysis could be due to a sample size effect. Hence, the need for in-depth and broader epigenetic studies to accurately capture the effects of ABO blood groups in susceptibility to Pf malaria is highlighted.

### **6. Conclusion**

The study confirmed that the Fulani group is less susceptible to *Pf* clinical malaria and when infected had generally lower parasite densities. The study also *The ABO Blood Group System and* Plasmodium falciparum *(*Pf*) Infection... DOI: http://dx.doi.org/10.5772/intechopen.102475*

found that despite infectivity being more frequent in blood group O, individuals of this blood group are at less risk of clinical malaria and have low parasitaemias compared to individuals of other blood groups (A, B, or AB).

Evidence of correlations between ethnicity and blood group at risk of malaria infection would support the idea that the presumed association between blood group and malaria infection depends on the demographic distribution and characteristics of the population studied. As a result, each region of the world has a characteristic ABO phenotypic distribution, making it urgent to fully understand the biology of malaria infection through detailed studies of the interactions between the ABO blood grouping system: A critical condition for saving lives in malaria-endemic regions.

## **Authorship contributions**

BEC wrote the manuscript and agree to be accountable for all aspects of the work.

AO and SBS read and approved the final manuscript and agree to be accountable for all aspects of the work.

## **Conflicts of interest**

The authors have declared no conflict of interest.

## **Ethics approval**

The study received approval from the ethical committees of the Ministry of Health of Burkina Faso.

## **Acronyms and abbreviations**


*Blood Groups - More than Inheritance of Antigenic Substances*

## **Author details**

Edith Christiane Bougouma\*, Alphonse Ouedraogo and Sodiomon Bienvenu Sirima Groupe de Recherche Action en Santé (GRAS), Ouagadougou, Burkina Faso

\*Address all correspondence to: bougouma.cedith@gmail.bf

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*The ABO Blood Group System and* Plasmodium falciparum *(*Pf*) Infection... DOI: http://dx.doi.org/10.5772/intechopen.102475*

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## **Chapter 9**
