Do blood group and sickle cell trait protect against placental malaria?

Authors

  • Arnold Togiwe Luuse University of Health and Allied Sciences, Ho Volta Region, Ghana.

DOI:

https://doi.org/10.4081/jphia.2023.2817

Keywords:

Malaria, PCR, electrophoresis, Placental, gravidae

Abstract

Introduction: Blood group O is reported to confer some degree of protection from severe malaria in endemic setting. This protection is believed to be due to reduced and smaller rosette formation in people of blood group O which can easily be cleared by the host immune system. Also, sickle cell trait (HbAS) is reported to disrupt the adhesion of infected erythrocytes to microvascular endothelial walls, which could protect pregnant women from placental malaria. We determined the association between HbAS and ABO blood group, and placental malaria amongst pregnant women of all parities.

Methods: The study enrolled 221 pregnant women. Peripheral blood samples were taken for malaria smears, ABO blood grouping and haemoglobin (Hb) electrophoresis. A structured questionnaire was used to age, bed net usage, and the number of Sulphadoxine-pyrimethamine (SP) doses taken by a pregnant woman.

Results: Two hundred and twenty-one (221) pregnant women were enrolled and out of this number, 110 (49.8%) were primiparae and 111 (50.2%) multiparae, with a mean age of 23.7±5.2.  Placental malaria (PM) prevalence by PCR detection was 19.4% (43/221). Of those who were malaria positive 58.1% (25/43) were primiparae. Primiparae who are of blood group O were more susceptible to PM (P=0.04, [OR]; 2.85, 95% [Cl], 1.12-9.01). But sickle cell trait did not reduce the prevalence of PM (P=0.84 [OR]; 0.92, 95% [Cl], 0.43-1.99).   

Conclusion. Non-blood group O primiparae women were protected against placental malaria. This could be why some primiparae women are protected from PM, just like multiparae women.

Download data is not yet available.

Author Biography

Arnold Togiwe Luuse, University of Health and Allied Sciences, Ho Volta Region, Ghana.

Department of Medical Laboratory

Assistant Research Fellow

 

References

R. D. Newman et al., ‘Burden of malaria during pregnancy in areas of stable and unstable transmission in Ethiopia during a nonepidemic year’, J. Infect. Dis., vol. 187, no. 11, pp. 1765–1772, Jun. 2003, doi: 10.1086/374878. DOI: https://doi.org/10.1086/374878

C. Menéndez et al., ‘A randomized placebo-controlled trial of intermittent preventive treatment in pregnant women in the context of insecticide treated nets delivered through the antenatal clinic’, PloS One, vol. 3, no. 4, p. e1934, Apr. 2008, doi: 10.1371/journal.pone.0001934. DOI: https://doi.org/10.1371/journal.pone.0001934

C. Luxemburger, ‘Effects of Malaria during Pregnancy on Infant Mortality in an Area of Low Malaria Transmission’, Am. J. Epidemiol., vol. 154, no. 5, pp. 459–465, Sep. 2001, doi: 10.1093/aje/154.5.459. DOI: https://doi.org/10.1093/aje/154.5.459

S. W. Bang and S. S. Lee, ‘The factors affecting pregnancy outcomes in the second trimester pregnant women’, Nutr. Res. Pract., vol. 3, no. 2, p. 134, 2009, doi: 10.4162/nrp.2009.3.2.134. DOI: https://doi.org/10.4162/nrp.2009.3.2.134

C. L. L. Chua, W. Hasang, S. J. Rogerson, and A. Teo, ‘Poor Birth Outcomes in Malaria in Pregnancy: Recent Insights Into Mechanisms and Prevention Approaches’, Front. Immunol., vol. 12, p. 621382, Mar. 2021, doi: 10.3389/fimmu.2021.621382. DOI: https://doi.org/10.3389/fimmu.2021.621382

V. N. Orish, O. S. Onyeabor, J. N. Boampong, R. Aforakwah, E. Nwaefuna, and N. C. Iriemenam, ‘Adolescent pregnancy and the risk of Plasmodium falciparum malaria and anaemia-a pilot study from Sekondi-Takoradi metropolis, Ghana’, Acta Trop., vol. 123, no. 3, pp. 244–248, Sep. 2012, doi: 10.1016/j.actatropica.2012.05.014. DOI: https://doi.org/10.1016/j.actatropica.2012.05.014

B. Brabin, ‘An Assessment of Low Birthweight Risk in Primiparae as an Indicator of Malaria Control in Pregnancy’, Int. J. Epidemiol., vol. 20, no. 1, pp. 276–283, 1991, doi: 10.1093/ije/20.1.276. DOI: https://doi.org/10.1093/ije/20.1.276

S. J. Rogerson, V. Mwapasa, and S. R. Meshnick, ‘Malaria in Pregnancy: Linking Immunity and Pathogenesis to Prevention’, p. 9.

A. Salanti et al., ‘Evidence for the Involvement of VAR2CSA in Pregnancy-associated Malaria’, J. Exp. Med., vol. 200, no. 9, pp. 1197–1203, Nov. 2004, doi: 10.1084/jem.20041579. DOI: https://doi.org/10.1084/jem.20041579

P. E. Duffy and M. Fried, ‘Antibodies That Inhibit Plasmodium falciparum Adhesion to Chondroitin Sulfate A Are Associated with Increased Birth Weight and the Gestational Age of Newborns’, Infect. Immun., vol. 71, no. 11, pp. 6620–6623, Nov. 2003, doi: 10.1128/IAI.71.11.6620-6623.2003. DOI: https://doi.org/10.1128/IAI.71.11.6620-6623.2003

E. Sappenfield, D. J. Jamieson, and A. P. Kourtis, ‘Pregnancy and Susceptibility to Infectious Diseases’, Infect. Dis. Obstet. Gynecol., vol. 2013, pp. 1–8, 2013, doi: 10.1155/2013/752852. DOI: https://doi.org/10.1155/2013/752852

P. R. Walter, Y. Garin, and P. Blot, ‘Placental Pathologic Changes in Malaria: A Histologic and Ultrastructural Study’, Obstet. Gynecol. Surv., vol. 38, no. 8, pp. 469–471, Aug. 1983, doi: 10.1097/00006254-198308000-00008. DOI: https://doi.org/10.1097/00006254-198308000-00008

H. L. Guyatt and R. W. Snow, ‘Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa’, Clin. Microbiol. Rev., vol. 17, no. 4, pp. 760–769, table of contents, Oct. 2004, doi: 10.1128/CMR.17.4.760-769.2004. DOI: https://doi.org/10.1128/CMR.17.4.760-769.2004

S. M. Taylor, C. M. Parobek, and R. M. Fairhurst, ‘Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis’, Lancet Infect. Dis., vol. 12, no. 6, pp. 457–468, Jun. 2012, doi: 10.1016/S1473-3099(12)70055-5. DOI: https://doi.org/10.1016/S1473-3099(12)70055-5

S. M. Taylor, C. Cerami, and R. M. Fairhurst, ‘Hemoglobinopathies: slicing the Gordian knot of Plasmodium falciparum malaria pathogenesis’, PLoS Pathog., vol. 9, no. 5, p. e1003327, 2013, doi: 10.1371/journal.ppat.1003327. DOI: https://doi.org/10.1371/journal.ppat.1003327

T. N. Williams et al., ‘An Immune Basis for Malaria Protection by the Sickle Cell Trait’, PLOS Med., vol. 2, no. 5, p. e128, May 2005, doi: 10.1371/journal.pmed.0020128. DOI: https://doi.org/10.1371/journal.pmed.0020128

O. K. Amodu, S. A. Olaniyan, A. A. Adeyemo, M. Troye-Blomberg, P. E. Olumese, and O. O. Omotade, ‘Association of the sickle cell trait and the ABO blood group with clinical severity of malaria in southwest Nigeria’, Acta Trop., vol. 123, no. 2, pp. 72–77, Aug. 2012, doi: 10.1016/j.actatropica.2012.03.013. DOI: https://doi.org/10.1016/j.actatropica.2012.03.013

N. Amoako, K. P. Asante, G. Adjei, G. A. Awandare, L. Bimi, and S. Owusu-Agyei, ‘Associations between red cell polymorphisms and Plasmodium falciparum infection in the middle belt of Ghana’, PloS One, vol. 9, no. 12, p. e112868, 2014, doi: 10.1371/journal.pone.0112868. DOI: https://doi.org/10.1371/journal.pone.0112868

J. C. Patel et al., ‘Absence of Association between Sickle Trait Hemoglobin and Placental Malaria Outcomes’, Am. J. Trop. Med. Hyg., vol. 94, no. 5, pp. 1002–1007, May 2016, doi: 10.4269/ajtmh.15-0672. DOI: https://doi.org/10.4269/ajtmh.15-0672

R. Afoakwah, E. Aubyn, J. Prah, E. K. Nwaefuna, and J. N. Boampong, ‘Relative Susceptibilities of ABO Blood Groups to Plasmodium falciparum Malaria in Ghana’, Advances in Hematology, 2016. https://www.hindawi.com/journals/ah/2016/5368793/ (accessed Nov. 26, 2019). DOI: https://doi.org/10.1155/2016/5368793

E. Senga et al., ‘ABO blood group phenotypes influence parity specific immunity to Plasmodium falciparum malaria in Malawian women’, Malar. J., vol. 6, p. 102, Aug. 2007, doi: 10.1186/1475-2875-6-102. DOI: https://doi.org/10.1186/1475-2875-6-102

K. T. Wolofsky et al., ‘ABO Blood Groups Influence Macrophage-mediated Phagocytosis of Plasmodium falciparum-infected Erythrocytes’, PLOS Pathog., vol. 8, no. 10, p. e1002942, Oct. 2012, doi: 10.1371/journal.ppat.1002942. DOI: https://doi.org/10.1371/journal.ppat.1002942

H. Tadesse and K. Tadesse, ‘Assessing the association of severe malaria infection and ABO blood groups in northwestern Ethiopia’, J. Vector Borne Dis., vol. 50, no. 4, pp. 292–296, Dec. 2013.

T. Zerihun, A. Degarege, and B. Erko, ‘Association of ABO blood group and Plasmodium falciparum malaria in Dore Bafeno Area, Southern Ethiopia’, Asian Pac. J. Trop. Biomed., vol. 1, no. 4, pp. 289–294, Aug. 2011, doi: 10.1016/S2221-1691(11)60045-2. DOI: https://doi.org/10.1016/S2221-1691(11)60045-2

M. Kweku et al., ‘Prevalenceof malaria and anaemiaamong pregnant women attending Antenatal Care Clinic in the Hohoe Municipality of Ghana’, Int. J. Nurs. Didact., vol. 7, no. 7, Jul. 2017, doi: 10.15520/ijnd.2017.vol7.iss7.240.21-30. DOI: https://doi.org/10.15520/ijnd.2017.vol7.iss7.240.21-30

F. Perandin et al., ‘Development of a Real-Time PCR Assay for Detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for Routine Clinical Diagnosis’, J. Clin. Microbiol., vol. 42, no. 3, pp. 1214–1219, Mar. 2004, doi: 10.1128/JCM.42.3.1214-1219.2004. DOI: https://doi.org/10.1128/JCM.42.3.1214-1219.2004

I. Adam, S. Babiker, A. A. Mohmmed, M. M. Salih, M. H. Prins, and Z. M. Zaki, ‘ABO blood group system and placental malaria in an area of unstable malaria transmission in eastern Sudan’, Malar. J., vol. 6, p. 110, Aug. 2007, doi: 10.1186/1475-2875-6-110. DOI: https://doi.org/10.1186/1475-2875-6-110

M.-P. Loscertales and B. J. Brabin, ‘ABO phenotypes and malaria related outcomes in mothers and babies in The Gambia: a role for histo-blood groups in placental malaria?’, Malar. J., vol. 5, p. 72, Aug. 2006, doi: 10.1186/1475-2875-5-72. DOI: https://doi.org/10.1186/1475-2875-5-72

A. Nasr, M. Eltoum, A. Yassin, and G. ElGhazali, ‘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., vol. 1, no. 1, p. 16, Jan. 2012, doi: 10.4103/2278-0521.94979. DOI: https://doi.org/10.4103/2278-0521.94979

J. A. Rowe et al., ‘Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting’, Proc. Natl. Acad. Sci. U. S. A., vol. 104, no. 44, pp. 17471–17476, Oct. 2007, doi: 10.1073/pnas.0705390104. DOI: https://doi.org/10.1073/pnas.0705390104

I. Vigan-Womas et al., ‘Structural Basis for the ABO Blood-Group Dependence of Plasmodium falciparum Rosetting’, PLOS Pathog., vol. 8, no. 7, p. e1002781, Jul. 2012, doi: 10.1371/journal.ppat.1002781. DOI: https://doi.org/10.1371/journal.ppat.1002781

J. Carmona-Fonseca and E. M. Arango, ‘Asymptomatic plasmodial infection in pregnant women: A global scenario’, J. Vector Borne Dis., vol. 54, no. 3, p. 201, Jul. 2017, doi: 10.4103/0972-9062.217610. DOI: https://doi.org/10.4103/0972-9062.217610

D. Nega, D. Dana, T. Tefera, and T. Eshetu, ‘Prevalence and Predictors of Asymptomatic Malaria Parasitemia among Pregnant Women in the Rural Surroundings of Arbaminch Town, South Ethiopia’, PLoS ONE, vol. 10, no. 4, Apr. 2015, doi: 10.1371/journal.pone.0123630. DOI: https://doi.org/10.1371/journal.pone.0123630

N. Tuikue Ndam et al., ‘Persistent Plasmodium falciparum Infection in Women With an Intent to Become Pregnant as a Risk Factor for Pregnancy-associated Malaria’, Clin. Infect. Dis., May 2018, doi: 10.1093/cid/ciy380. DOI: https://doi.org/10.1093/cid/ciy380

R. Cholera et al., ‘Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin’, Proc. Natl. Acad. Sci. U. S. A., vol. 105, no. 3, pp. 991–996, Jan. 2008, doi: 10.1073/pnas.0711401105. DOI: https://doi.org/10.1073/pnas.0711401105

R. M. Fairhurst, H. Fujioka, K. Hayton, K. F. Collins, and T. E. Wellems, ‘Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state’, Blood, vol. 101, no. 8, pp. 3309–3315, Apr. 2003, doi: 10.1182/blood-2002-10-3105. DOI: https://doi.org/10.1182/blood-2002-10-3105

R. M. Fairhurst et al., ‘Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria’, Nature, vol. 435, no. 7045, pp. 1117–1121, Jun. 2005, doi: 10.1038/nature03631. DOI: https://doi.org/10.1038/nature03631

B. J. Brabin et al., ‘The sick placenta-the role of malaria’, Placenta, vol. 25, no. 5, pp. 359–378, May 2004, doi: 10.1016/j.placenta.2003.10.019. DOI: https://doi.org/10.1016/j.placenta.2003.10.019

S. M. Taylor et al., ‘Molecular Malaria Epidemiology: Mapping and Burden Estimates for the Democratic Republic of the Congo, 2007’, PLoS ONE, vol. 6, no. 1, p. e16420, Jan. 2011, doi: 10.1371/journal.pone.0016420. DOI: https://doi.org/10.1371/journal.pone.0016420

Y. Wang and S. Zhao, Vascular Biology of the Placenta. in Integrated Systems Physiology: from Molecules to Function to Disease. San Rafael (CA): Morgan & Claypool Life Sciences, 2010. Accessed: Nov. 17, 2019. [Online]. Available: http://www.ncbi.nlm.nih.gov/books/NBK53247/

A. Srivastava et al., ‘Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA’, Proc. Natl. Acad. Sci. U. S. A., vol. 107, no. 11, pp. 4884–4889, Mar. 2010, doi: 10.1073/pnas.1000951107. DOI: https://doi.org/10.1073/pnas.1000951107

Downloads

Published

21-12-2023

How to Cite

Luuse, A. T. (2023). Do blood group and sickle cell trait protect against placental malaria?. Journal of Public Health in Africa, 14(12). https://doi.org/10.4081/jphia.2023.2817

Issue

Section

Original Articles