Experimental Parasitology 136 (2014) 63–67

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ABO blood groups of residents and the ABO host choice of malaria vectors in southern Iran Mehdi Anjomruz a, Mohammad A. Oshaghi a,⇑, Mohammad M. Sedaghat a, Ali A. Pourfatollah b, Ahmad Raeisi a, Hassan Vatandoost a, Fatemeh Mohtarami a, Mohammad Yeryan a, Hassan Bakhshi a, Fatemeh Nikpoor a a

Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, P.O. BOX: 14155-6446, Tehran, Iran Department of Immunology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran


h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 ABO blood group of residents in two

malaria endemic areas in southern Iran has been typed.  Ingested blood meal of Anopheline mosquitoes were typed using allelespecific PCR.  O blood group was the most frequently observed group in the regions.  It is the first ABO molecular typing of blood meal in mosquitoes.  ABO typing of arthropod vectors warrant further researches.

a r t i c l e

i n f o

Article history: Received 30 March 2013 Received in revised form 31 October 2013 Accepted 13 November 2013 Available online 23 November 2013 Keywords: ABO blood group Anopheles Malaria Host preference AS-PCR Iran

a b s t r a c t Recent epidemiological evidences revealed the higher prevalence of ‘O’ blood group in the residents of malaria-endemic areas. Also some data indicated preference of mosquitoes to ‘O’ group. The aim of this study was to determine ABO group ratio in the residents as well as ABO group preference of Anopheles in two malaria endemic areas in south of Iran. Agglutination method was used for ABO typing of residents. Field blood fed Anopheles specimens were tested against vertebrate DNA using mtDNA-cytB PCR–RFLP and then the human fed specimens were tested for ABO groups using multiplex allele-specific PCR. A total of 409 human blood samples were identified, of which 150(36.7%) were ‘O’ group followed by 113(27.6%), 109(26.7%), and 37(9.0%) of A, B, and AB groups respectively. Analyzing of 95 blood fed mosquitoes revealed that only four Anopheles stephensi had fed human blood with A(1), B(1), and AB(2) groups. Result of this study revealed high prevalence of O group in south of Iran. To our knowledge, it is the first ABO molecular typing of blood meal in mosquitoes; however, due to low number of human blood fed specimens, ABO host choice of the mosquitoes remains unknown. This study revealed that ABO blood preference of malaria vectors and other arthropod vectors deserves future research. Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction Malaria disease has widespread prevalence in the world which could have great impact on people health and economic cost for communities particularly in developing countries (Murray et al., ⇑ Corresponding author. Fax: +98 21 88951393. E-mail addresses: [email protected], [email protected] (M.A. Oshaghi). 0014-4894/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.exppara.2013.11.005

2012; Sachs and Malaney, 2002). According to the World Malaria Report of WHO, 219 million cases and 660,000 deaths of malaria were reported in 2010 which was more prevalent among aged group less than 5 years (WHO, 2012). In 2011, totally 3239 malaria cases reported in Iran included 1710 indigenous and 1529 imported cases that had relative decreasing trend than 2010 (WHO, 2012). Totally, about 4 million of Iranian people are endangering to risk of malaria, however, currently, Iran has been classified as country in elimination stage of malaria (WHO,


M. Anjomruz et al. / Experimental Parasitology 136 (2014) 63–67

2012). Most of malaria cases were residing in southern parts of the country including Hormozgan, Sistan & Baluchestan and Kerman provinces (Basseri et al., 2005, 2010; Edrissian, 2006; Hanafi-Bojd et al., 2010, 2012). In these regions, there are five malaria vectors including Anopheles stephensi, Anopheles culicifacies s.l., Anopheles superpictus s.l., Anopheles fluviatilis s.l., and Anopheles dthali where A. stephensi and A. culicifacies s.l. regarded as the most important vectors (Manouchehri et al., 1976; Mehravaran et al., 2011a,b, 2012; Naddaf et al., 2012; Oshaghi et al., 2006a,b, 2007, 2008; Vatandoost et al., 2011, 2002). The most important Plasmodium species are Plasmodium vivax (88%) and Plasmodium falciparum (12%) (Edrissian, 2006). Among the vectors, A. stephensi is the main malaria vector in both rural and urban regions, and has shown various anthropophilic indices ranged from 5.4% to 15.8% in Kazeroun and Bander-Abbas (Manouchehri et al., 1992), 11.8% in Jiroft (Mehravaran et al., 2011b), and 0.5% in Kahnouj (Basseri et al., 2005). Literature review suggested an association between ABO blood groups and malaria disease that individuals of blood group O are relatively resistant to severe disease caused by P. falciparum infection. Numerous studies confirmed the low chance of severe malaria for people with O blood group (Adegnika et al., 2011; Deepa et al., 2011; Panda et al., 2011; Wolofsky et al., 2012) which in turn resulted in the high distribution of O blood group in malarious regions of the world. It is suggested that blood type O and the mosquito-transmitted parasite are linked in evolutionary history (Cserti and Dzik, 2007). On the other hand, significant association have been demonstrated between severe falciparum infection and blood group ‘A’ in Gabon (Lell et al., 1999), Ethiopia (Tekeste and Petros, 2010) and Zimbabwe (Fischer and Boone, 1998), blood group ‘AB’ in Sri Lanka (Pathirana et al., 2005), Mali (Rowe et al., 2007), and Ethiopia (Tekeste and Petros, 2010), and blood group ‘B’ in India (Panda et al., 2011). Despite numerous studies in this context, a few studies were conducted to test association of ABO blood groups and malaria in Iran. The main purpose of the present study was to find frequency of ABO blood groups of malaria endemic residents as well as to test whether Anopheline mosquitoes has got any preference to each of ABO groups. 2. Materials and methods 2.1. Study area The study was conducted in the two malaria endemic areas of Minab and Ghale Ganj with a previous history of malaria transmission. Minab located in the Hormozgan province in the southeast of Bandar Abas (capital of Hormozgan province). Its population is 300,000 people including 34% rural and 66% urban residents. Ghale-Ganj district is located in the Kerman province in the south of Iran with a population of approximately 70,000 people. The hot and humid weather of Minab and Ghale-Ganj is an important factor for growth of Anopheles spp. as well as malaria transmission. Malaria seasonal and transmission pattern have two peaks in year from June to July and in October. P. vivax and A. stephensi are the main malaria parasite and vector in this areas, respectively. Implementation of the malaria elimination program leads to the decreasing trend of malaria cases in recent years (Zoghi et al., 2012).

Three drops of the blood specimens were put in three places of glass slide on which a few drops of antisera A, B and D were employed to detect of blood group A and B. Applicator stick was used to mix of blood cell and antigen in each place. Titled slide was applied for agglutination and their results interpreted according to the guideline. 2.3. Anopheline collection Anopheles collections were conducted based on the guideline suggested by WHO (1992). Mosquitoes were collected by hand catch, total catch and shelter pits from outdoor and indoor settings during five months from August to November in 2010 and also March 2011. Female specimens were separated and identified based on the morphological key of Shahgudian (1960). The specimens were conserved into 1.5 ml Eppendorf micro tubes and transferred to the laboratory of School of Public Health, Tehran University of Medical Sciences (SPH-TUMS) and stored at 20 °C until molecular examination. 2.4. Anopheles blood fed identification 2.4.1. DNA extraction Genomic DNA of blood fed mosquitoes was extracted to analyze the blood meal sources, ABO blood groups, as well as the malaria parasite infection in female mosquitoes. DNA extraction was performed using DNeasyÒ Blood & Tissue Kit (Qiagen), according to the manufacturer’s instructions. All of the experiments were carried out with parallel laboratory unfed A. stephensi specimen as negative and the known human ABO blood groups as positive controls. 2.4.2. mtDNA cyt B PCR–RFLP A region of the mtDNA cyt B gene were amplified and digested by HaeIII for host blood meal identification of the blood-fed specimens following the protocol already introduced by Maleki-Ravasan et al. (2009). The primers of UNFOR403 and UNREV1025 (Table 1) were used to amply a 623-basepair region of the cytB gene of vertebrate mtDNA. Following amplification, the PCR products were digested by HaeIII enzyme. Incubation of the mixture was performed based on recommendation of enzyme suppliers. Then, 8 ll of the PCR–RFLP product was loaded onto a 2% agarose gel and subjected to electrophoresis. Electrophoresis was performed using a GeneRuler 100-basepair molecular mass marker (Sinaclone, Iran). Gels were stained with ethidium bromide (2 mg/ml) and the RFLP profiles were observed under ultraviolet light. 2.4.3. Multiplex allele-specific PCR (ASPCR) Following the PCR–RFLP and identification of the mosquitoes fed on human blood, their genomic DNA were also tested for ABO blood groups using the multiplex allele-specific PCR (ASPCR) protocol described by Lee et al. (2009). In this experiments, fourreaction multiplex ASPCR genotyping assays using 10 different primers (Table 1) used to detect specific nucleotide sequence differences between the six ABO alleles A101, A102, B101, O01, O02, and cisAB01. 3. Results

2.2. ABO Blood group determination A total of 409 human blood specimens including 296 peoples from Minab and 113 peoples from Ghaleh-Ganj were randomly collected from the residents to detect their ABO blood groups. ABO blood groups of the people were typed by standard agglutination method using commercial antisera (CinaGen Co., Tehran, Iran).

A total of 409 residents were included for ABO blood group identification, of which 296 individuals belonged to Minab and 113 individuals belonged to Ghale-Ganj. The results of the blood groups in Minab showed 100 (33.8%) – ‘O’ group, 83 (28.0%) – ‘A’ group, 80 (27.0%) – ‘B’ group and 33 (11.2%) – ‘AB’ group (Fig. 1). The results of the blood group typing in Ghale-Ganj showed 52


M. Anjomruz et al. / Experimental Parasitology 136 (2014) 63–67 Table 1 Details of the primers used in this study. Target gene ABO

PCR reaction









Primer names and sequences



Fig. 1. The prevalence of ABO blood groups in two malaria endemic areas of south Iran.

(46.0%) – ‘O’ group, 28 (24.8%) – ‘B’ group, 27 (23.9%) – ‘A’ group and 6 (5.3%) was ‘AB’ group (Fig. 1). Totally, on average O blood group with 37.2% and AB blood group with 9.5% were the most and the least prevalent blood groups, respectively in the study areas. Totally 757 male and female Anopheles specimens were collected from the area study which belonged to five proven malaria vectors and one non vector (Table 2). Totally, 95 adult female Anopheles specimens were fully blood fed and or useful for blood meal identification assays. A. stephensi was the most frequent blood fed species in both Minab and Galeh-Ganj areas. In Minab, except one A. culicifacies specimen, all blood fed specimens belonged to species of A. stephensi (n = 70) whereas in Ghaleh-Ganj, the blood fed specimens belonged to all of the six species captured in the region. A total of 95 blood-fed Anopheles mosquitoes were subjected to PCR amplification of mtDNA CytB gene to find their blood sources. The expected 623 bp band in the PCR reactions using the general vertebrate mtDNA cyt B primers were observed for 37 out of 95 selected samples and positive control. The rest of blood fed specimens did not yield sharp band suitable for PCR–

Fragment size (bp)

Allele/genus/species specificity


A101, A102, B101, cis-AB01


A101, O01, O02


A101, A102, O01, cis-AB01




O01, O02




B101, O02





RFLP analysis. The blood meal sources of the 37 samples included 30 (81.1%) animal blood, four (10.8%) human blood, and three (8.1%) mixed of human and animal bloods (Table 2). ASPCR assays revealed that the four detected human bloods belonged to A (1), B (1), and AB (2) blood groups. According to the Lee et al. (2009) protocol, expected bands of 205, 164, 381, and lack or weak band of 381 bp were observed, respectively in reactions 1, 2, 3, and 4 for A blood group. The expected bands of 205, 381, and lack or weak band of 381, and 164 bp were observed, respectively in reactions 1, 2, 3, and 4 for B blood group. The expected bands of 205, 164/381, 205(weak)/381, and 164 bp were observed respectively in reactions 1, 2, 3, and 4 for AB blood group.

4. Discussion In this study we have found that O blood group was the most prevalent ABO blood group in the study areas. Minab and Gale-Ganj have been considered historically as one of the known malaria endemic areas of the country although the malaria transmission has been reduced to nearly zero in recent years. The high prevalence of O group is in concordance with many epidemiological evidences indicated that O blood group is more frequent in malaria-endemic regions of the world (Carvalho et al., 2010; Cserti and Dzik, 2007; Martin et al., 1979; Saitou and Yamamoto, 1997; Wolofsky et al., 2012). This is shown that high prevalence of O group has been associated with protection against severe malaria and death. Literature has shown that the ABO phenotype modulate malaria severity and outcome of P. falciparum, with blood groups A and B associated with increased disease severity compared to blood group O (Barragan et al., 2000; Chung et al., 2005; Fischer and Boone, 1998; Gupte et al., 2012; Lell et al., 1999; Pathirana et al., 2005; Wolofsky et al., 2012). In a comprehensive study by Wolofsky et al. (2012) it is suggested that both increased

Table 2 Details of fed Anopheles species and their geographical distribution, and vertebrate blood sources in the study areas. Species

A. fluviatilis A. culicifacies A. dthali A. algeriensis A. superpictus A. stephensi Total

Fed blood N (%)

4 (4.2) 6 (6.3) 2 (2.1) 1 (1.05) 1 (1.05) 81 (85.26) 95 (100)


Vertebrate blood sources (N = 37)

Minab (%)

Ghaleh Ganj (%)




0 1 (8.4) 0 0 0 70 (91.6) 71 (100)

4 (16.6) 5 (20.84) 2 (8.33) 1 (4.61) 1 (4.61) 11 (45.83) 24 (100)

– – – – – 4 4

– – – – – 30 30

– – – – – 3 3


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phagocytosis and decreased rosetting of blood group O may contribute functionally to reduced parasite burden, decreased infected erythrocyte adhesion to the endothelium and decreased microvascular obstruction. These events are believed to play important mechanistic roles in the pathophysiology of severe falciparum malaria. In the past, approximately 30–40% of the total mortality of people in the hyper-endemic areas of the country was due to malaria (Edrissian, 2006). In 1991, not very far from present time, the total reported malaria cases in Iran was 96,340 with 45% P. falciparum. It is suggested that presumably due to 1) the influence of fatality and severity of malaria due to P. falciparum in the country and 2) protection role of O group against severe malaria and death, O group has been increased in Iran particularly in endemic areas in southern parts. Along the same line, the frequency of the A, B, and AB phenotype reaches values around 26.9%, 26.4%, and 9.5% within individuals which are similar to the values reported for A (30%), B (24%), and AB (8%) in Iran (Pourfathollah et al., 2004). In regions that are highly endemic for P. falciparum malaria, it is well recognized that a range of red blood cell polymorphisms associated with resistance to severe diseases have undergone positive selection (Min-Oo and Gros, 2005). Moreover, as mentioned before, the blood group O proved to be a protective factor against severe malaria. However, since historically malaria was endemic in most part of Iran, malaria endemicity could be viewed as a selective pressure for maintenance of the observed frequencies of genotypes of the ABO system, which could be very interesting as the focus of a new investigation, including analysis of the genotypes in severe and non-severe malaria patients, as well as in individuals living in non-endemic areas. In addition to malaria, there are clear examples of relationship between blood groups and disease such as dermal cancer, Schistosomiasis, Helicobacter pylori, Escherichia coli, norovirus, Dengue, and cholera which is modulated by regulating the expression of ABO antigens (Anstee, 2010; Blackwell et al., 2002; Frattali and Spitalnik, 1997; Kalayanarooj et al., 2007; Moulds and Moulds, 2000; Ndamba et al., 1997; Tursen et al., 2005). However, available evidence suggests surviving malaria is the most significant selective force affecting the expression of blood groups and has shaped the distribution of ABO blood groups in humans. The ability of P. falciparum to kill children before reproduction stage (normally less than five years old) has given it the capacity to select emerging polymorphisms as rapidly as can be witnessed in evolutionary time (Cserti and Dzik, 2007). To our knowledge, this is the first ABO molecular typing in Anopheles in literature. It is shown that the source of blood meal can be analyzed and indentified to species level in the body of Anopheles 32 h post-ingestion (e.g., Oshaghi et al., 2006c,d). However, ability to ABO typing of the ingested blood meal within abdomen of insects open a new era to better understanding of haematophagous insect or arthropod behavior which are responsible for vector borne diseases. The burden of many of these diseases is borne largely by developing countries. The three mosquito species of Anopheles gambiae, Aedes aegypti, and Culex pipiens are infecting half a billion people each year and transmitting different malaria, dengue fever, and West Nile virus, respectively (Hill et al., 2005). However, there are only two reports indicating preference of A. gambiae (Wood et al., 1974) and Aedes albopictus (Shirai et al., 2004) to O group. If vectors have specific ABO host choice, then the preferred blood group is more prone to vector bites and should be protected than others. Unfortunately in this study, due to lack of significant number of human blood fed mosquitoes, we were not able to recognize the ABO host choice of the mosquitoes, but we strongly suggest further studies to find which blood group/ s are more likely to be bitten by species specific mosquitoes or vectors.

Acknowledgments This work was supported financially by Tehran University of Medical Sciences, I.R. Iran. The authors declare that they have no conflict of interest.

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ABO blood groups of residents and the ABO host choice of malaria vectors in southern Iran.

Recent epidemiological evidences revealed the higher prevalence of 'O' blood group in the residents of malaria-endemic areas. Also some data indicated...
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