Association of Parasite Density and Hematological Parameters of Plasmodium vivax- and Plasmodium falciparum-infected Patients Attending Merauke General Hospital, Papua, Indonesia

Roy Bagus Kurniawan; Puspa Wardhani; Heny Arwati; Aryati Aryati; Trieva Verawaty  Butarbutar; Christophorus Oetama  Adiatmaja; Amarensi Milka Betaubun; Nur Chamidah

doi:10.3889/oamjms.2020.4881

Authors

Roy Bagus Kurniawan Medical Doctor Study Programme, Faculty of Medicine, Universitas Airlangga, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Puspa Wardhani Department of Clinical Pathology, Faculty of Medicine, Universitas Airlangga/Dr. Soetomo General Academic Hospital, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Heny Arwati Department of Medical Parasitology, Faculty of Medicine, Universitas Airlangga, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Aryati Aryati Department of Clinical Pathology, Faculty of Medicine, Universitas Airlangga/Dr. Soetomo General Academic Hospital, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Trieva Verawaty Butarbutar Department of Clinical Pathology, Clinical Pathology Specialist Study Programme, Faculty of Medicine, Universitas Airlangga/Dr. Soetomo General Academic Hospital, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Christophorus Oetama Adiatmaja Department of Clinical Pathology, Clinical Pathology Specialist Study Programme, Faculty of Medicine, Universitas Airlangga/Dr. Soetomo General Academic Hospital, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Amarensi Milka Betaubun Department of Clinical Pathology, Clinical Pathology Specialist Study Programme, Faculty of Medicine, Universitas Airlangga/Dr. Soetomo General Academic Hospital, Jl. Prof. Dr. Moestopo No. 47 Surabaya, Indonesia
Nur Chamidah Department of Mathematics, Faculty of Sciences and Technology, Universitas Airlangga, Jl. Mulyorejo Surabaya, Indonesia

DOI:

https://doi.org/10.3889/oamjms.2020.4881

Keywords:

Parasite density, hematology, malaria, Plasmodium vivax, Plasmodium falciparum

Abstract

BACKGROUND: Plasmodium falciparum and Plasmodium vivax are frequent causes of malaria. Although they are blood parasites, their biological characteristics are dissimilar, and their species-related consequences on hematological parameters have not been widely investigated. They might be valuable to distinguish both species infection, notably for an endemic region with limited diagnostic resources.

AIM: This study aimed to know the species-specific effect on hematological parameters and its correlation to the parasite density in P. vivax- and P. falciparum-infected patients attending Merauke General Hospital, Papua, Indonesia.

MATERIALS AND METHODS: Malaria patients confirmed by blood film microscopy from January 1 to July 31, 2019, were recruited, and their hematological parameters were measured using Sysmex XN-1000 instrument. All obtained data were analyzed statistically.

RESULTS: From 100 malaria-positive patients, 87 patients, consisting of 57 P. vivax and 30 P. falciparum patients, met criteria. Anemia and parasite density >50,000 parasites/μL were significantly higher in P. falciparum than P. vivax patients (p < 0.05) though hemoglobin concentration and parasite density were insignificantly different. Interestingly, basophil count was significantly higher in P. falciparum compared to P. vivax patients (p = 0.04). The eosinophil count was significantly higher in P. vivax (p = 0.01) than P. falciparum patients and indicated a significant positive correlation (p = 0.04, r = +0.28) with the parasite density.

CONCLUSION: There were significant differences between basophil and eosinophil count between P. vivax and P. falciparum infections. Eosinophil count showed a significant positive correlation with parasite density.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Plum Analytics Artifact Widget Block

References

World Health Organization. Malaria Report, 2018. Geneva: World Health Organization; 2018.

Kementerian Kesehatan Republik Indonesia. Situasi Terkini Perkembangan Program Pengendalian Malaria di Indonesia Tahun 2018. Jakarta: Kementerian Kesehatan Republik Indonesia; 2018.

Awoke N, Arota A. Profiles of hematological parameters in Plasmodium falciparum and Plasmodium vivax malaria patients attending Tercha general hospital, Dawuro Zone, South Ethiopia. Infect Drug Resist. 2019;12:521-7. https://doi.org/10.2147/idr. s184489 PMid:30881057

Kotepui M, Phunphuech B, Phiwklam N, Chupeerach C, Duangmano S. Effect of malarial infection on hematological parameters in population near Thailand-Myanmar border. Malar J. 2014;13(1):218-24. https://doi.org/10.1186/1475-2875-13-218 PMid:24898891

Kotepui M, Piwkham D, Phunphuech B, Phiwklam N, Chupeerach C, Duangmano S. Effects of malaria parasite density on blood cell parameters. PLoS One. 2015;10(3):e0121057. https://doi.org/10.1371/journal.pone.0121057 PMid:25807235

Arévalo-Herrera M, Lopez-Perez M, Medina L, Moreno A, Gutierrez JB, Herrera S. Clinical profile of Plasmodium falciparum and Plasmodium vivax infections in low and unstable malaria transmission settings of Colombia. Malar J. 2015;14(1):154-64. https://doi.org/10.1186/s12936-015-0678-3

Antwi-Baffour S, Kyeremeh R, Buabeng D, Adjei JK, Aryeh C, Kpentey G, et al. Correlation of malaria parasitemia with peripheral blood monocyte to lymphocyte ratio as indicator of susceptibility to severe malaria in Ghanaian children. Malar J. 2018;17(1):419-27. https://doi.org/10.1186/s12936-018-2569-x PMid:30419923

Garcia LS. Diagnostic Medical Parasitology. 6th ed. Washington, DC: ASM Press; 2016.

Argy N, Kendjo E, Augé-Courtoi C, Cojean S, Clain J, Houzé P. Influence of host factors and parasite biomass on the severity of imported Plasmodium falciparum malaria. PLoS One. 2017;12(4):e0175328. https://doi.org/10.1371/journal. pone.0175328 PMid:28410415

Barber BE, William T, Grigg MJ, Parameswaran U, Piera KA, Price RN, et al. Parasite biomass-related inflammation, endothelial activation, microvascular dysfunction, and disease severity in Vivax malaria. PLoS Pathog. 2015;11(1):e1004558. https://doi.org/10.1371/journal.ppat.1004558 PMid:25569250

Abdallah TM, Abdeen MT, Ahmed IS, Hamdan HZ, Magzoub M, Adam I. Severe Plasmodium falciparum and Plasmodium vivax malaria among adults at Kassala hospital, Eastern Sudan. Malar J. 2013;12(1):148-54. https://doi.org/10.1186/1475-2875-12-148

Tangpukdee N, Duangdee C, Wilairatana P, Krudsood S. Malaria diagnosis: A brief review. Korean J Parasitol. 2009;47(2):93- 102. https://doi.org/10.3347/kjp.2009.47.2.93 PMid:19488414

World Health Organization. Basic Malaria Microscopy, Part 1. 2nd ed. Geneva: World Health Organization; 2010.

Sorontou Y, Asih PB, Wanandi SI, Ramelan W, Syafruddin D. Malaria in Jayapura District, Papua Province, Indonesia, and resistance to sulfadoxine-pyrimethamine. Med J Indones. 2007;16(1):32-8. https://doi.org/10.13181/mji.v16i1.254

David PH, Hommel M, Miller LH, Udeinya IJ, Oligino LD. Parasite sequestration in Plasmodium falciparum malaria: Spleen and antibody modulation of cytoadherence of infected erythrocytes. Proc Natl Acad Sci U S A. 1983;80(16):5075-9. https://doi.org/10.1073/pnas.80.16.5075 PMid:6348780

Safeukui I, Correas JC, Brousse V, Hirt D, Deplaine G, Mulé S, et al. Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood. 2008;112(6):2520-8. https://doi.org/10.1182/ blood-2008-03-146779 PMid:18579796

Evelyn ME, Ezeiruaku FC, Ukaji DC. Experiential relationship between malaria parasite density and some haematological parameters in malaria infected male subjects in port Harcourt, Nigeria. Glob J Health Sci. 2012;4(4):139-48. https://doi. org/10.5539/gjhs.v4n4p139 PMid:22980350

Ademolue TW, Aniweh Y, Kusi KA, Awandare GA. Patterns of inflammatory responses and parasite tolerance vary with malaria transmission intensity. Malar J. 2017;16(1):145-157. https://doi.org/10.1186/s12936-017-1796-x PMid:28399920

Coban C, Lee MS, Ishii KJ. Tissue-specific immunopathology during malaria infection. Nat Rev Immunol. 2018;18(4):266-78. https://doi.org/10.1038/nri.2017.138 PMid:29332936

Day NP, Hien TT, Schollaardt T, Loc PP, Chuong LV, Chau TT, et al. The prognostic and pathophysiologic role of pro-and antiinflammatory cytokines in severe malaria. J Infect. 1999;180(4):1288-97. https://doi.org/10.1086/315016 PMid:10479160

Hearn J, Rayment N, Landon DN, Katz DR, de Souza JB. Immunopathology of cerebral malaria: Morphological evidence of parasite sequestration in murine brain microvasculature. Infect Immun. 2000;68(9):5364-76. https://doi.org/10.1128/ iai.68.9.5364-5376.2000 PMid:10948166

Graham SM, Chen J, Chung DW, Barker KR, Conroy AL, Hawkes MT, et al. Endothelial activation, hemostasis, and thrombosis biomarkers in Ugandan children with severe malaria participating in a clinical trial. Malar J. 2016;15(1):56-64. https:// doi.org/10.1186/s12936-016-1106-z

Waters LS, Taverne J, Tai P, Spry CJ, Targett GA, Playfair JH. Killing of Plasmodium falciparum by eosinophil secretory products. Infect Immun. 1987;55(4):877-81. https://doi. org/10.1128/iai.55.4.877-881.1987 PMid:3549562

Kurtzhals JA, Reimert CM, Tette E, Dunyo SK, Koram KA, Akanmori BD, et al. Increased eosinophil activity in acute Plasmodium falciparum infection-association with cerebral malaria. Clin Exp Immunol. 1998;112(2):303-7. https://doi. org/10.1046/j.1365-2249.1998.00586.x PMid:9649195

Camacho LH, Wilairatana P, Weiss G, Mercader MA, Brittenham GM, Looareesuwan S, et al. The eosinophilic response and haematological recovery after treatment for Plasmodium falciparum malaria. Trop Med Int Health. 1999;4(7):471-5. https://doi.org/10.1046/j.1365-3156.1999.00426.x PMid:10470337

Mecheri S. Contribution of allergic inflammatory response to the pathogenesis of malaria disease. Biochim Biophys Acta Mol Basis Dis. 2012;1822(1):49-56. https://doi.org/10.1016/j. bbadis.2011.02.005

Huang S, Amaladoss A, Liu M, Chen H, Zhang R, Preiser PR, et al. In vivo splenic clearance correlates with in vitro deformability of red blood cells from Plasmodium yoelii-infected mice. Infect Immun. 2014;82(6):2532-41. https://doi. org/10.1128/iai.01525-13 PMid:24686065

Safeukui I, Gomez ND, Adelani AA, Burte F, Afolabi NK, Akondy R, et al. Malaria induces anemia through CD8+ T cell-dependent parasite clearance and erythrocyte removal in the spleen. mBio. 2015;6(1):e02493-14. https://doi.org/10.1128/mbio.02493-14 PMid:25604792

Casals-Pascual C, Kai O, Cheung JO, Williams S, Lowe B, Nyanoti M, et al. Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood. 2006;108(8):2569-77. https://doi.org/10.1182/blood-2006-05-018697 PMid:16804108

Panichakul T, Payuhakrit W, Panburana P, Wongborisuth C, Hongeng S, Udomsangpetch R. Suppression of erythroid development in vitro by Plasmodium vivax. Malar J. 2012;11(1):173-80. https://doi.org/10.1186/1475-2875-11-173

Abbas A, Lichtman A, Pillai S. Cellular, and Molecular Immunology. 9th ed. Philadelphia, PA: Elsevier; 2018.

McKenzie FE, Prudhomme WA, Magill JA, Forney JA, Permpanich B, Lucas C, et al. White blood cell counts and malaria. J Infect. 2005;192(2):323-30. https://doi.org/10.1086/431152 PMid:15962228

Chakravorty SJ, Carret C, Nash GB, Ivens A, Szestak T, Craig AG. Altered phenotype and gene transcription in endothelial cells, induced by Plasmodium falciparum-infected red blood cells: Pathogenic or protective? Int J Parasitol. 2007;37(8-9):975-87. https://doi.org/10.1016/j.ijpara.2007.02.006 PMid:17383656

MacDonald SM, Bhisutthibhan J, Shapiro TA, Rogerson SJ, Taylor TE, Tembo M, et al. Immune mimicry in malaria: Plasmodium falciparum secretes a functional histamine-releasing factor homolog in vitro and in vivo. Proc Natl Acad Sci U S A. 2001;98(19):10829-32. https://doi.org/10.1073/ pnas.201191498 PMid:11535839

Coelho HC, Lopes SC, Pimentel JP, Nogueira PA, Costa FT, Siqueira AM, et al. Thrombocytopenia in Plasmodium vivax malaria is related to platelets phagocytosis. PLoS One. 2013;8(5):e63410. https://doi.org/10.1371/journal. pone.0063410 PMid:23723981

Pelleau S, Diop S, Badiane MD, Vitte J, Beguin P, Nato F, et al. Enhanced basophil reactivities during severe malaria and their relationship with the Plasmodium falciparum histamine-releasing factor translationally controlled tumor protein. Infect Immun. 2012;80(8):2963-70. https://doi.org/10.1128/iai.00072-12 PMid:22753372

Pain A, Ferguson DJ, Kai O, Urban BC, Lowe B, Marsh K, et al. Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci U S A. 2001;98(4):1805-10. https://doi.org/10.1073/pnas.98.4.1805 PMid:11172032

Grau GE, Mackenzie CD, Carr RA, Redard M, Pizzolato G, Allasia C, et al. Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect. 2003;187(3):461-6. https://doi.org/10.1086/367960 PMid:12552430

O’Sullivan JM, Preston RJ, O’Regan N, O’Donnell JS. Emerging roles for hemostatic dysfunction in malaria pathogenesis. Blood. 2016;127(19):2281-8. https://doi.org/10.1182/ blood-2015-11-636464 PMid:26851291