Pro- and anti-inflammatory cytokine profiles in Plasmodium falciparum-infected individuals from Baiyeku, Ikorodu, Lagos, Nigeria
https://dx.doi.org/10.4314/njpar.v43i2.14
Keywords:
Interferon-gamma, Interleukin-12, Tumour necrosis factor-alpha, Cytokine, Plasmodium falciparumAbstract
Available evidence indicates that the various stages of the malaria parasite life cycle elicit specific immune responses of which the relative levels of pro-inflammatory cytokines are key to disease progression, killing the parasite and mediating disease outcomes. This study investigated T-cell response in malaria. Four hundred and sixty-two participants were screened in a community survey of Plasmodium falciparum malaria in Baiyeku, Lagos, Nigeria. P. falciparum parasitaemia was determined by microscopy while the serum levels of IL-10, IFNγ and TNFα were determined by Enzyme-linked immunosorbent assay (ELISA). A total of 70 (15.2 %) participants were microscopically positive for P. falciparum of which 70% were females, 30% were males while children aged 1-17 years were 65.7%. The geometric mean parasite density (GMPD) was significantly (p=0.001) higher among females than males. The GMPD of participants <5 years of age was also significantly (p=0.001) higher than other age groups. About 46.8% of the participants were underweight (Body Mass Index, BMI < 18.5) and also had the highest parasite intensity. The TNFα, IFNγ and IL-10 levels were significantly (p< 0.05) higher in the infected than the uninfected participants. IFN-γ values were significantly (p=0.014) elevated among the symptomatic than the asymptomatic participants while there was no significant difference (P>0.053) in the levels of TNF-α and IL-10 (P>0.093) between the symptomatic and asymptomatic participants. The prevalence of P. falciparum obtained in this study area which is endemic to malaria is 15.2% suggesting a significant reduction of the disease over time due to awareness of the disease in the community. The levels of pro-inflammatory cytokines (IFN-γ and TNF-α) in this study were lower due to the down-regulatory action of the anti-inflammatory cytokines (IL-10). These findings suggest that higher levels of antiinflammatory cytokines, especially IL-10 levels may contribute to the pathogenesis of uncomplicated malaria.
References
Chan, J.A., Fowkes, F. J. and Beeson, J. G. (2014). Surface antigens of Plasmodium falciparum infected erythrocytes as immune targets and malaria vaccine candidates. Cellular & Molecular Life Sciences 71 (19): 3633-3657.
Oelze, B., Elger, K., Schadzek, P., Burmeister, L., Hamm, A., Laggies, S., Seiffart, V., Gross, G. and Hoffmann, A. (2021). The inflammatory signalling mediator TAK1 mediates lymphocyte recruitment to lipopolysaccharide-activated murine mesenchymal stem cells through interleukin-6. Molecular and Cellular Biochemistry 476: 3655 – 3670.https://doi.org/10.1007/s11010-021-04180-
Oyegue-Liabagui, S. L., BouopdaTuedom, A. G., Kouna, L. C., MaghendjiNzondo, S., Nzoughe, H., TchitoulaMakaya, N., Pegha-Moukandja, I. and Lekana-Douki, J. B. (2017). Pro- and antiinflammatory cytokines in children with malaria in Franceville, Gabon. American journal of clinical and experimental immunology 6 (2): 9–20.
Nussenblatt, V., Mukasa, G., Metzger, A., Ndeezi, G., Garrett, E. and Semba, R. D. (2001). Anaemia and interleukin-10, tumour necrosis factor-alpha, and erythropoietin levels among children with acute, uncomplicated Plasmodium falciparum malaria. Clinical and diagnostic laboratory immunology 8 (6): 1164–1170.
Ajibaye, O., Osuntoki, A. A., Ebuehi, A. O., Iwalokun, B. A., Balogun, E. O. and Egbuna, K. N. (2017). Pro-inflammatory Cytokine Response and Genetic Diversity in Merozoite Surface Protein 2 of Plasmodium falciparum Isolates from Nigeria. Advanced biomedical research 11/2017. https://doi.org/10.4103/2277-9175.192631
Winkler, S., Willheim, M., Baier, K. (1998). Reciprocal regulation of Th1- and Th2-cytokine-pro T cells during clearance of parasitemia in Plasmodium falciparum malaria. Infection and Immunity 66 (12):
-4.
Punnath, K., Dayanand, K. K., Chandrashekhar, V. N., Achur, R. N., Kakkilaya, S. B., Ghosh, S. K., Kumari, S. N. and Gowda, D. C. (2019). Association between inflammatory cytokine levels and
anaemia during Plasmodium falciparum and Plasmodium vivax infections in Mangaluru: A Southwestern Coastal Region of India. Tropical parasitology 9 (2): 98–107.
Frimpong, A., Amponsah, J., Adjokatseh, A. S., Agyemang, D., Bentum-Ennin, L., Ofori, E. A., Kyei-Baafour, E., AkyeaMensah, K., Adu, B., Mensah, G. I., Amoah, L. E. and Kusi, K. A. (2020). Asymptomatic Malaria Infection Is Maintained by a Balanced Pro- and Antiinflammatory Response. Frontiers in microbiology 11/2020. https://doi.org/10.3389/fmicb.2020.559255
Gichohi-Wainaina, W. N., MelseBoonstra, A., Feskens, E. J., Demir, A. Y., Veenemans, J., & Verhoef, H. (2015). Tumour necrosis factor allele variants and their association with the occurrence and
severity of malaria in African children: a longitudinal study. Malaria journal 06/2015. https://doi.org/10.1186/s12936- 015-0767-3
Martín-Orozco, E., Norte-Muñoz, M. and Martínez-García, J. (2017). Regulatory T Cells in Allergy and Asthma. Frontiers in pediatrics 05/2017. https://doi.org/10.3389/fped.2017.00117
O’Garra, A., Barrat, F. J., Castro, A. G., Vicari, A. and Hawrylowicz, C. (2008). Strategies for use of IL-10 or its antagonists in human disease. Immunological Reviews 06/2008. https://doi.org/10.1111/j.1600-065X.2008.00635.x
Kumar, R., Ng, S., Engwerda, C. (2019).The Role of IL-10 in Malaria: A DoubleEdged Sword. Frontiers in Microbiology 02/2019.https://doi.org/10.3389/fimmu.201 9.00229
World Health Organization (2019). World malaria report. Geneva, Switzerland: World Health Organization.
World Health Organization (2013). World malaria report. Geneva, Switzerland: World Health Organization.
Konstantinou, G. N. (2017) EnzymeLinked Immunosorbent Assay (ELISA). In Lin J and Alcocer M (eds). Food Allergens. Methods in Molecular Biology. New York, USA: Humana Press, pp. 79–94.
World Health Organization (2022). World malaria report. Geneva, Switzerland: World Health Organization.
Sylvester, B., Gasarasi, D. B., Aboud, S., Tarimo, D., Masawe, S., Mpembeni, R. and Swedberg, G. (2018). Interferon-γ and Interleukin-10 Responses during Clinical Malaria Episodes in Infants Aged 0-2 Years Prenatally Exposed to Plasmodium falciparum: Tanzanian Birth Cohort. Journal of tropical medicine 07/2018. https://doi.org/10.1155/2018/6847498
Aina, O. O., Agomo, C. O., Olukosi, Y. A., Okoh, H. I., Iwalokun, B. A., Egbuna, K. N., Orok, A. B., Ajibaye, O., Enya, V. N., Akindele, S. K., Akinyele, M. O. and Agomo, P. U. (2013). Malariometric survey
of Ibeshe community in Ikorodu, Lagos State: dry season. Malaria research and treatment 05/2013.
https://doi.org/10.1155/2013/487250
Olukosi, A. Y., Agomo, C. O., Aina, O. O., Akindele, S. K., Okoh, H. O., Brai, B. C., Ajibaye, O., Orok, B. A., Iwalokun, B. A., Adeneye, A. K., Adeogun, A., Akinyele, O. M., Oparaugo, C. T., Akintunde, G. A.,
Enya, V. N., Aniedobe, M., Fesobi, O. W., Olakiigbe, A., Awolola, S. (2018). Prevalence of malaria and anaemia during the dry season in north-central and southwestern Nigeria. Journal of
Parasitology and Vector Biology 10 (1): 8-18.
Sam-Wobo, S. O., Adekunle, N. O., Adeleke, M. A., Dedeke, G. A., Oke, O. A., Abimbola, W. A. and Surakat, O. A. (2014). Epidemiological factors in the prevalence of malaria parasites in primary
health facilities attendees, Ogun State, Nigeria. Malaria Control and Elimination 02/2014. doi:10.4172/ 2090-2778.1000111
Animut, A., Negash, Y. (2018). Dry season occurrence of Anopheles mosquitoes and implications in Jabi Tehnan District, West Gojjam Zone, Ethiopia. Malaria Journal 17 (1) :445
Dawaki, S., Al-Mekhlafi, H. M., Ithoi, I., Ibrahim, J., Atroosh, W. M., Abdulsalam, A. M., Sady, H., Elyana, F. N., Adamu, A. U., Yelwa, S. I., Ahmed, A., Al-Areeqi, M. A., Subramaniam, L. R., Nasr, N. A. and Lau, Y. L. (2016). Is Nigeria winning the battle against malaria? Prevalence, risk factors and KAP assessment among Hausa communities in Kano State. Malaria journal 07/2016. https://doi.org/10.1186/s12936- 016-1394-3
Ayanlade, S.,Adeoye, N. O., Babatimehin, O. I. (2013). Intra-annual climate variability and malaria transmission in Nigeria. Bulletin of Geography. Socio-economic Series 08/2013. doi:10.2478/bog-2013-0016
World Health Organization (2013). World malaria report. Geneva, Switzerland: World Health Organization.
Buchwald, A. G., Sorkin, J. D., Sixpence, A., Chimenya, M., Damson, M., Wilson, M. L., Seydel, K., Hochman, S., Mathanga, D., Taylor, T. E. and Laufer, M. K. (2019). Association Between Age and Plasmodium falciparum Infection Dynamics. American journal of epidemiology 188 (1): 169–176.
Moormann, A. M. (2009). How might infant and paediatric immune responses influence malaria vaccine efficacy? Parasite Immunology 31(9): 547-559.
Sumbele, I. U. N., Bopda, O. S. M., Kimbi, H. K. (2015). Nutritional status of children in a malaria meso endemic area: a crosssectional study on prevalence, intensity, predictors, influence on malaria parasitemia and anaemia severity. BMC Public Health 11/2015. https://doi.org/10.1186/s12889-
-2462-2
Gombart, A.F., Pierre, A., Maggini, S. (2020). A Review of Micronutrients and the Immune System–Working in Harmony to Reduce the Risk of Infection. Nutrients 01/2020. https://doi.org/10.3390/nu12010236
Perera, M. K., Herath, N. P., Pathirana, S. L., Phone-Kyaw, M., Alles, H. K., Mendis, K. N., Premawansa, S., & Handunnetti, S. M. (2013).Association of high plasma TNFalpha levels and TNF-alpha/IL-10 ratios with TNF2 allele in severe P. falciparum malaria patients in Sri Lanka. Pathogens and global health 107(1): 21–29.
Leão, L., Puty, B., Dolabela, M. F., Povoa, M. M., Né, Y., Eiró, L. G., Fagundes, N., Maia, L. C. and Lima, R. R. (2020). Association of cerebral malaria and TNF-α levels: a systematic review. BMC infectious diseases 06/2020. https://doi.org/10.1186/s12879-020-05107-2
White, N. J. (2017). Malaria parasite clearance. Malaria Journal 02/2017. https://doi.org/10.1186/s12936-017-1731-1
Depinay, N., Franetich, J. F., Grüner, A. C., Mauduit, M., Chavatte, J. M., Luty, A. J., van Gemert, G. J., Sauerwein, R. W., Siksik, J. M., Hannoun, L., Mazier, D., Snounou, G. and Rénia, L. (2011). Inhibitory effect of TNF-α on malaria preerythrocytic stage development: influence of host hepatocyte/parasite combinations. PloS one 6 (3): e17464.
Fillol, F., Sarr, J. B., Boulanger, D., Cisse, B., Sokhna, C., Riveau, G., Simondon, K. B. and Remoué, F. (2009). Impact of child malnutrition on the specific antiPlasmodium falciparum antibody response.
Malaria journal 06/2009. https://doi.org/10.1186/1475-2875-8-116
Larsson, L., Rymo, L., Berglundh, T. (2010). Sp1 binds to the G allele of the−1087 polymorphism in the IL-10 promoter and promotes IL-10 mRNA transcription and protein production. Genes and Immunity 11 (2): 181-187
Iyer, S.S., Cheng, G. (2012). Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Critical Reviews in Immunology 32(1): 23- 63.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Nigerian Journal of Parasitology
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
