Skip to main content
Top
Published in: Malaria Journal 1/2011

Open Access 01-12-2011 | Research

Association of ABO blood group with severe falciparum malaria in adults: case control study and meta-analysis

Authors: Aditya K Panda, Santosh K Panda, Aditya N Sahu, Rina Tripathy, Balachandran Ravindran, Bidyut K Das

Published in: Malaria Journal | Issue 1/2011

Login to get access

Abstract

Background

Erythrocyte-associated antigenic polymorphisms or their absence have perhaps evolved in the human population to protect against malarial infection. Studies in various populations consistently demonstrate that blood group 'O' confers resistance against severe falciparum infection. In India, Odisha state has one of the highest incidences of Plasmodium falciparum infection and contributes to the highest number of deaths by falciparum malaria. This study aims to evaluate the relationship between ABO blood group and severe malaria in an adult population at the tertiary care centre in Odisha.

Methods

A total of 353 P. falciparum infected subjects and 174 healthy controls were screened for ABO blood group. Falciparum-infected individuals were categorized as severe malaria and uncomplicated malaria. Severe malaria was further clinically phenotyped into cerebral malaria, non-cerebral severe malaria and multi-organ dysfunction. A meta-analysis was performed to assess the role of ABO blood group in severe malaria.

Results

Frequency of blood group 'B' was significantly higher in patients with severe malaria compared to the uncomplicated cases (P < 0.0001; OR = 4.09) and healthy controls (P < 0.0001; OR = 2.79). Irrespective of the level of clinical severity, blood group 'B' was significantly associated with cerebral malaria (P < 0.0001; OR = 5.95), multi-organ dysfunction (P < 0.0001; OR = 4.81) and non-cerebral severe malaria patients (P = 0.001; OR = 3.02) compared to the uncomplicated category. Prevalence of 'O' group in uncomplicated malaria (P < 0.0001; OR = 2.81) and healthy controls (P = 0.0003; OR = 2.16) was significantly high compared to severe malaria. Meta-analysis of previous studies, including the current one, highlighted the protective nature of blood group 'O' to severe malaria (P = 0.01). On the other hand, carriers of blood group 'A' (P = 0.04) and 'AB' (P = 0.04) were susceptible to malaria severity.

Conclusions

Results of the current study indicate that blood group 'O' is associated with reduced and 'B' blood group with increased risk of development of severe malaria in Odisha, India. Meta-analysis also supports the protective nature of blood group 'O' from severe falciparum infection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Tekeste Z, Petros B: The ABO blood group and Plasmodium falciparum malaria in Awash, Metehara and Ziway areas, Ethiopia. Malar J. 2010, 9: 280-10.1186/1475-2875-9-280.PubMedCentralCrossRefPubMed Tekeste Z, Petros B: The ABO blood group and Plasmodium falciparum malaria in Awash, Metehara and Ziway areas, Ethiopia. Malar J. 2010, 9: 280-10.1186/1475-2875-9-280.PubMedCentralCrossRefPubMed
2.
go back to reference Ringwald P, Peyron F, Lepers JP, Rabarison P, Rakotomalala C, Razanamparany M, Rabodonirina M, Roux J, Le Bras J: Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect Immun. 1993, 61: 5198-5204.PubMedCentralPubMed Ringwald P, Peyron F, Lepers JP, Rabarison P, Rakotomalala C, Razanamparany M, Rabodonirina M, Roux J, Le Bras J: Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect Immun. 1993, 61: 5198-5204.PubMedCentralPubMed
3.
go back to reference Uneke CJ: Plasmodium falciparum malaria and ABO blood group: is there any relationship?. Parasitol Res. 2007, 100: 759-765. 10.1007/s00436-006-0342-5.CrossRefPubMed Uneke CJ: Plasmodium falciparum malaria and ABO blood group: is there any relationship?. Parasitol Res. 2007, 100: 759-765. 10.1007/s00436-006-0342-5.CrossRefPubMed
4.
go back to reference Carlson J, Wahlgren M: Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med. 1992, 176: 1311-1317. 10.1084/jem.176.5.1311.CrossRefPubMed Carlson J, Wahlgren M: Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med. 1992, 176: 1311-1317. 10.1084/jem.176.5.1311.CrossRefPubMed
5.
go back to reference Udomsangpetch R, Todd J, Carlson J, Greenwood BM: The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. Am J Trop Med Hyg. 1993, 48: 149-153.PubMed Udomsangpetch R, Todd J, Carlson J, Greenwood BM: The effects of hemoglobin genotype and ABO blood group on the formation of rosettes by Plasmodium falciparum-infected red blood cells. Am J Trop Med Hyg. 1993, 48: 149-153.PubMed
6.
go back to reference Rowe A, Obeiro J, Newbold CI, Marsh K: Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun. 1995, 63: 2323-2326.PubMedCentralPubMed Rowe A, Obeiro J, Newbold CI, Marsh K: Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun. 1995, 63: 2323-2326.PubMedCentralPubMed
7.
go back to reference Barragan A, Kremsner PG, Wahlgren M, Carlson J: Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun. 2000, 68: 2971-2975. 10.1128/IAI.68.5.2971-2975.2000.PubMedCentralCrossRefPubMed Barragan A, Kremsner PG, Wahlgren M, Carlson J: Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun. 2000, 68: 2971-2975. 10.1128/IAI.68.5.2971-2975.2000.PubMedCentralCrossRefPubMed
8.
go back to reference Daniels G: The molecular genetics of blood group polymorphism. Transpl Immunol. 2005, 14: 143-153. 10.1016/j.trim.2005.03.003.CrossRefPubMed Daniels G: The molecular genetics of blood group polymorphism. Transpl Immunol. 2005, 14: 143-153. 10.1016/j.trim.2005.03.003.CrossRefPubMed
9.
go back to reference Fry AE, Griffiths MJ, Auburn S, Diakite M, Forton JT, Green A, Richardson A, Wilson J, Jallow M, Sisay-Joof F, Pinder M, Peshu N, Williams TN, Marsh K, Molyneux ME, Taylor TE, Rockett KA, Kwiatkowski DP: Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet. 2008, 17: 567-576.PubMedCentralCrossRefPubMed Fry AE, Griffiths MJ, Auburn S, Diakite M, Forton JT, Green A, Richardson A, Wilson J, Jallow M, Sisay-Joof F, Pinder M, Peshu N, Williams TN, Marsh K, Molyneux ME, Taylor TE, Rockett KA, Kwiatkowski DP: Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet. 2008, 17: 567-576.PubMedCentralCrossRefPubMed
10.
go back to reference Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, Kivinen K, Bojang KA, Conway DJ, Pinder M, Sirugo G, Sisay-Joof F, Usen S, Auburn S, Bumpstead SJ, Campino S, Coffey A, Dunham A, Fry AE, Green A, Gwilliam R, Hunt SE, Inouye M, Jeffreys AE, Mendy A, Palotie A, Potter S, Ragoussis J, Rogers J, Rowlands K: Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009, 41: 657-665. 10.1038/ng.388.PubMedCentralCrossRefPubMed Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, Kivinen K, Bojang KA, Conway DJ, Pinder M, Sirugo G, Sisay-Joof F, Usen S, Auburn S, Bumpstead SJ, Campino S, Coffey A, Dunham A, Fry AE, Green A, Gwilliam R, Hunt SE, Inouye M, Jeffreys AE, Mendy A, Palotie A, Potter S, Ragoussis J, Rogers J, Rowlands K: Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009, 41: 657-665. 10.1038/ng.388.PubMedCentralCrossRefPubMed
11.
go back to reference Rowe JA, Handel IG, Thera MA, Deans AM, Lyke KE, Kone A, Diallo DA, Raza A, Kai O, Marsh K, Plowe CV, Doumbo OK, Moulds JM: Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci USA. 2007, 104: 17471-17476. 10.1073/pnas.0705390104.PubMedCentralCrossRefPubMed Rowe JA, Handel IG, Thera MA, Deans AM, Lyke KE, Kone A, Diallo DA, Raza A, Kai O, Marsh K, Plowe CV, Doumbo OK, Moulds JM: Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci USA. 2007, 104: 17471-17476. 10.1073/pnas.0705390104.PubMedCentralCrossRefPubMed
12.
go back to reference Pathirana SL, Alles HK, Bandara S, Phone-Kyaw M, Perera MK, Wickremasinghe AR, Mendis KN, Handunnetti SM: ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Ann Trop Med Parasitol. 2005, 99: 119-124. 10.1179/136485905X19946.CrossRefPubMed Pathirana SL, Alles HK, Bandara S, Phone-Kyaw M, Perera MK, Wickremasinghe AR, Mendis KN, Handunnetti SM: ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Ann Trop Med Parasitol. 2005, 99: 119-124. 10.1179/136485905X19946.CrossRefPubMed
13.
go back to reference Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, Greve B, Matousek P, Schmid D, Herbich K, Mockenhaupt FP, Meyer CG, Bienzle U, Kremsner PG: The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis. 1999, 28: 794-799. 10.1086/515193.CrossRefPubMed Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, Greve B, Matousek P, Schmid D, Herbich K, Mockenhaupt FP, Meyer CG, Bienzle U, Kremsner PG: The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis. 1999, 28: 794-799. 10.1086/515193.CrossRefPubMed
14.
go back to reference Fischer PR, Boone P: Severe malaria associated with blood group. Am J Trop Med Hyg. 1998, 58: 122-123.PubMed Fischer PR, Boone P: Severe malaria associated with blood group. Am J Trop Med Hyg. 1998, 58: 122-123.PubMed
15.
go back to reference National Vector Borne Disease Control Programme: Ministry of Health and Family Welfare. Government of India Report. 2004 National Vector Borne Disease Control Programme: Ministry of Health and Family Welfare. Government of India Report. 2004
16.
17.
go back to reference Dhingra N, Jha P, Sharma VP, Cohen AA, Jotkar RM, Rodriguez PS, Bassani DG, Suraweera W, Laxminarayan R, Peto R: Adult and child malaria mortality in India: a nationally representative mortality survey. Lancet. 2010, 376: 1768-1774. 10.1016/S0140-6736(10)60831-8.PubMedCentralCrossRefPubMed Dhingra N, Jha P, Sharma VP, Cohen AA, Jotkar RM, Rodriguez PS, Bassani DG, Suraweera W, Laxminarayan R, Peto R: Adult and child malaria mortality in India: a nationally representative mortality survey. Lancet. 2010, 376: 1768-1774. 10.1016/S0140-6736(10)60831-8.PubMedCentralCrossRefPubMed
18.
go back to reference Sharma SK, Chattopadhyay R, Chakrabarti K, Pati SS, Srivastava VK, Tyagi PK, Mahanty S, Misra SK, Adak T, Das BS, Chitnis CE: Epidemiology of Malaria transmission and development of natural immunity in a malaria-endemic village, San Dulakudar, in Orissa state, India. Am J Trop Med Hyg. 2004, 71: 457-465.PubMed Sharma SK, Chattopadhyay R, Chakrabarti K, Pati SS, Srivastava VK, Tyagi PK, Mahanty S, Misra SK, Adak T, Das BS, Chitnis CE: Epidemiology of Malaria transmission and development of natural immunity in a malaria-endemic village, San Dulakudar, in Orissa state, India. Am J Trop Med Hyg. 2004, 71: 457-465.PubMed
19.
go back to reference World Health Organization, Communicable Diseases Cluster: Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000, 94 (Suppl 1): S1-90.CrossRef World Health Organization, Communicable Diseases Cluster: Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000, 94 (Suppl 1): S1-90.CrossRef
20.
go back to reference Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA: A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999, 60: 687-692.PubMed Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA: A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999, 60: 687-692.PubMed
21.
go back to reference Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN: Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol. 1993, 58: 283-292. 10.1016/0166-6851(93)90050-8.CrossRefPubMed Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN: Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol. 1993, 58: 283-292. 10.1016/0166-6851(93)90050-8.CrossRefPubMed
22.
go back to reference Ranjit MR: The epidemiology of malaria in Orissa. Indian Council of Medical Research Bulletin. 2006, 36: 29-38. Ranjit MR: The epidemiology of malaria in Orissa. Indian Council of Medical Research Bulletin. 2006, 36: 29-38.
23.
go back to reference Duval S, Tweedie R: Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000, 56: 455-463. 10.1111/j.0006-341X.2000.00455.x.CrossRefPubMed Duval S, Tweedie R: Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000, 56: 455-463. 10.1111/j.0006-341X.2000.00455.x.CrossRefPubMed
24.
go back to reference Loscertales MP, Owens S, O'Donnell J, Bunn J, Bosch-Capblanch X, Brabin BJ: ABO blood group phenotypes and Plasmodium falciparum malaria: unlocking a pivotal mechanism. Adv Parasitol. 2007, 65: 1-50.CrossRefPubMed Loscertales MP, Owens S, O'Donnell J, Bunn J, Bosch-Capblanch X, Brabin BJ: ABO blood group phenotypes and Plasmodium falciparum malaria: unlocking a pivotal mechanism. Adv Parasitol. 2007, 65: 1-50.CrossRefPubMed
25.
go back to reference Balgir RS: Genetic heterogeneity of population structure in 15 major scheduled tribes in central-eastern India: A study of immuno-hematological disorders. Indian J Human Gen. 2006, 12: 86-92. 10.4103/0971-6866.27792.CrossRef Balgir RS: Genetic heterogeneity of population structure in 15 major scheduled tribes in central-eastern India: A study of immuno-hematological disorders. Indian J Human Gen. 2006, 12: 86-92. 10.4103/0971-6866.27792.CrossRef
26.
go back to reference Chavhan A, Pawar S, Baig M: Allelic frequency of ABO and Rh D blood group among the Banjara backward caste of Yavatmal District, Maharashtra, India. Nature Precedings. 2010 Chavhan A, Pawar S, Baig M: Allelic frequency of ABO and Rh D blood group among the Banjara backward caste of Yavatmal District, Maharashtra, India. Nature Precedings. 2010
27.
go back to reference Warghat NE, Sharma NR, BAIG MM, Yadav AR, Sharma SH, Pachalore GS: ABO and Rh blood group distribution among Kunbis (Maratha) population of Amravati District, Maharashtra. Nature Precedings. 2010 Warghat NE, Sharma NR, BAIG MM, Yadav AR, Sharma SH, Pachalore GS: ABO and Rh blood group distribution among Kunbis (Maratha) population of Amravati District, Maharashtra. Nature Precedings. 2010
28.
go back to reference Rai V: Genetic analysis of ABO and Rh blood groups in Brahmin population of Uttar Pradesh, India. Nature Precedings. 2011 Rai V: Genetic analysis of ABO and Rh blood groups in Brahmin population of Uttar Pradesh, India. Nature Precedings. 2011
29.
go back to reference Cserti CM, Dzik WH: The ABO blood group system and Plasmodium falciparum malaria. Blood. 2007, 110: 2250-2258. 10.1182/blood-2007-03-077602.CrossRefPubMed Cserti CM, Dzik WH: The ABO blood group system and Plasmodium falciparum malaria. Blood. 2007, 110: 2250-2258. 10.1182/blood-2007-03-077602.CrossRefPubMed
31.
go back to reference Williams TN: Human red blood cell polymorphisms and malaria. Curr Opin Microbiol. 2006, 9: 388-394. 10.1016/j.mib.2006.06.009.CrossRefPubMed Williams TN: Human red blood cell polymorphisms and malaria. Curr Opin Microbiol. 2006, 9: 388-394. 10.1016/j.mib.2006.06.009.CrossRefPubMed
32.
go back to reference Kaeda JS, Chhotray GP, Ranjit MR, Bautista JM, Reddy PH, Stevens D, Naidu JM, Britt RP, Vulliamy TJ, Luzzatto L, Mason PJ: A new glucose-6-phosphate dehydrogenase variant, G6PD Orissa (44 Ala-->Gly), is the major polymorphic variant in tribal populations in India. Am J Hum Genet. 1995, 57: 1335-1341.PubMedCentralPubMed Kaeda JS, Chhotray GP, Ranjit MR, Bautista JM, Reddy PH, Stevens D, Naidu JM, Britt RP, Vulliamy TJ, Luzzatto L, Mason PJ: A new glucose-6-phosphate dehydrogenase variant, G6PD Orissa (44 Ala-->Gly), is the major polymorphic variant in tribal populations in India. Am J Hum Genet. 1995, 57: 1335-1341.PubMedCentralPubMed
33.
go back to reference Balgir RS: Do tribal communities show an inverse relationship between sickle cell disorders and glucose-6-phosphate dehydrogenase deficiency in malaria endemic areas of Central-Eastern India?. Homo. 2006, 57: 163-176. 10.1016/j.jchb.2006.01.003.CrossRefPubMed Balgir RS: Do tribal communities show an inverse relationship between sickle cell disorders and glucose-6-phosphate dehydrogenase deficiency in malaria endemic areas of Central-Eastern India?. Homo. 2006, 57: 163-176. 10.1016/j.jchb.2006.01.003.CrossRefPubMed
34.
go back to reference Al-Yaman F, Genton B, Mokela D, Raiko A, Kati S, Rogerson S, Reeder J, Alpers M: Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans R Soc Trop Med Hyg. 1995, 89: 55-58. 10.1016/0035-9203(95)90658-4.CrossRefPubMed Al-Yaman F, Genton B, Mokela D, Raiko A, Kati S, Rogerson S, Reeder J, Alpers M: Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans R Soc Trop Med Hyg. 1995, 89: 55-58. 10.1016/0035-9203(95)90658-4.CrossRefPubMed
Metadata
Title
Association of ABO blood group with severe falciparum malaria in adults: case control study and meta-analysis
Authors
Aditya K Panda
Santosh K Panda
Aditya N Sahu
Rina Tripathy
Balachandran Ravindran
Bidyut K Das
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2011
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-10-309

Other articles of this Issue 1/2011

Malaria Journal 1/2011 Go to the issue