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Published in: Malaria Journal 1/2010

Open Access 01-12-2010 | Research

Alterations in early cytokine-mediated immune responses to Plasmodium falciparum infection in Tanzanian children with mineral element deficiencies: a cross-sectional survey

Authors: Erasto V Mbugi, Marjolein Meijerink, Jacobien Veenemans, Prescilla V Jeurink, Matthew McCall, Raimos M Olomi, John F Shao, Hans Verhoef, Huub FJ Savelkoul

Published in: Malaria Journal | Issue 1/2010

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Abstract

Background

Deficiencies in vitamins and mineral elements are important causes of morbidity in developing countries, possibly because they lead to defective immune responses to infection. The aim of the study was to assess the effects of mineral element deficiencies on early innate cytokine responses to Plasmodium falciparum malaria.

Methods

Peripheral blood mononuclear cells from 304 Tanzanian children aged 6-72 months were stimulated with P. falciparum-parasitized erythrocytes obtained from in vitro cultures.

Results

The results showed a significant increase by 74% in geometric mean of TNF production in malaria-infected individuals with zinc deficiency (11% to 240%; 95% CI). Iron deficiency anaemia was associated with increased TNF production in infected individuals and overall with increased IL-10 production, while magnesium deficiency induced increased production of IL-10 by 46% (13% to 144%) in uninfected donors. All donors showed a response towards IL-1β production, drawing special attention for its possible protective role in early innate immune responses to malaria.

Conclusions

In view of these results, the findings show plasticity in cytokine profiles of mononuclear cells reacting to malaria infection under conditions of different micronutrient deficiencies. These findings lay the foundations for future inclusion of a combination of precisely selected set of micronutrients rather than single nutrients as part of malaria vaccine intervention programmes in endemic countries.
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Literature
2.
go back to reference Wellinghausen N, Kirchner H, Rink L: The immunobiology of zinc. Immunol Today. 1997, 11: 519-521.CrossRef Wellinghausen N, Kirchner H, Rink L: The immunobiology of zinc. Immunol Today. 1997, 11: 519-521.CrossRef
3.
go back to reference Wieringa FT, Dijkhuizen MA, West CE, Ven-Jongekrijg van der J, Muhilal , Meer van der JWM: Reduced production of immunoregulatory cytokines in vitamin A- and zinc-deficient Indonesian infants. Eur J Clin Nutr. 2004, 58: 1498-1504.CrossRefPubMed Wieringa FT, Dijkhuizen MA, West CE, Ven-Jongekrijg van der J, Muhilal , Meer van der JWM: Reduced production of immunoregulatory cytokines in vitamin A- and zinc-deficient Indonesian infants. Eur J Clin Nutr. 2004, 58: 1498-1504.CrossRefPubMed
4.
go back to reference Black RE: Therapeutic and preventive effects of zinc on serious childhood infectious diseases in developing countries. Am J Clin Nutr. 1998, 68: 476S-479S.PubMed Black RE: Therapeutic and preventive effects of zinc on serious childhood infectious diseases in developing countries. Am J Clin Nutr. 1998, 68: 476S-479S.PubMed
5.
go back to reference Muller O, Becher H, van Zweeden AB, Ye Y, Diallo DA, Konate AT, Gbangou A, Kouyate B, Garenne M: Effect of zinc supplementation on malaria and other causes of morbidity in west African children: randomised double blind placebo controlled trial. BMJ. 2001, 322: 1567-PubMedCentralCrossRefPubMed Muller O, Becher H, van Zweeden AB, Ye Y, Diallo DA, Konate AT, Gbangou A, Kouyate B, Garenne M: Effect of zinc supplementation on malaria and other causes of morbidity in west African children: randomised double blind placebo controlled trial. BMJ. 2001, 322: 1567-PubMedCentralCrossRefPubMed
6.
go back to reference Shankar AH, Genton B, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Bannon D, Tielsch JM, Alpers MP, West KP: The influence of zinc supplementation on morbidity due to Plasmodium falciparum: a randomized trial in preschool children in Papua New Guinea. Am J Trop Med Hyg. 2000, 62: 663-669.PubMed Shankar AH, Genton B, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Bannon D, Tielsch JM, Alpers MP, West KP: The influence of zinc supplementation on morbidity due to Plasmodium falciparum: a randomized trial in preschool children in Papua New Guinea. Am J Trop Med Hyg. 2000, 62: 663-669.PubMed
7.
go back to reference Shankar AH, Prasad AS: Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr. 1998, 68: 447S-463S.PubMed Shankar AH, Prasad AS: Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr. 1998, 68: 447S-463S.PubMed
8.
go back to reference Percival SS: Neutropenia caused by copper deficiency: possible mechanisms of action. Nutr Rev. 1995, 53: 59-66.CrossRefPubMed Percival SS: Neutropenia caused by copper deficiency: possible mechanisms of action. Nutr Rev. 1995, 53: 59-66.CrossRefPubMed
9.
go back to reference Erickson KL, Medina EA, Hubbard NE: Micronutrients and Innate Immunity. J Infect Dis. 2000, 182: S5-S10.CrossRefPubMed Erickson KL, Medina EA, Hubbard NE: Micronutrients and Innate Immunity. J Infect Dis. 2000, 182: S5-S10.CrossRefPubMed
10.
go back to reference Walther M, Woodruff J, Edele F, Jeffries D, Tongren JE, King E, Andrews L, Bejon P, Gilbert SC, De Souza JB, Sinden R, Hill AV, Riley EM: Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J Immunol. 2006, 177: 5736-5745.CrossRefPubMed Walther M, Woodruff J, Edele F, Jeffries D, Tongren JE, King E, Andrews L, Bejon P, Gilbert SC, De Souza JB, Sinden R, Hill AV, Riley EM: Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J Immunol. 2006, 177: 5736-5745.CrossRefPubMed
11.
12.
go back to reference Walker CF, Black RE: Zinc and the risk for infectious disease. Ann Rev Nutr. 2004, 24: 255-275.CrossRef Walker CF, Black RE: Zinc and the risk for infectious disease. Ann Rev Nutr. 2004, 24: 255-275.CrossRef
13.
go back to reference Ibs K-H, Rink L: Zinc-Altered Immune Function. J Nutr. 2003, 133: 1452S-1456S.PubMed Ibs K-H, Rink L: Zinc-Altered Immune Function. J Nutr. 2003, 133: 1452S-1456S.PubMed
14.
15.
17.
go back to reference Pallauf J, Rimbach G: Nutritional significance of phytic acid and phytase. Arch Animal Nutr. 1997, 50: 301-319. Pallauf J, Rimbach G: Nutritional significance of phytic acid and phytase. Arch Animal Nutr. 1997, 50: 301-319.
18.
go back to reference Veenemans J, Andang'o PEA, Mbugi EV, Kraaijenhagen RJ, Mwaniki DL, Mockenhaupt FP, Roewer S, Olomi RM, Shao JF, Meer van der JWM, Savelkoul HFJ, Verhoef H: α+-Thalassemia protects against anemia associated with asymptomatic malaria: evidence from community-based surveys in Tanzania and Kenya. J Infect Dis. 2008, 198: 401-408.CrossRefPubMed Veenemans J, Andang'o PEA, Mbugi EV, Kraaijenhagen RJ, Mwaniki DL, Mockenhaupt FP, Roewer S, Olomi RM, Shao JF, Meer van der JWM, Savelkoul HFJ, Verhoef H: α+-Thalassemia protects against anemia associated with asymptomatic malaria: evidence from community-based surveys in Tanzania and Kenya. J Infect Dis. 2008, 198: 401-408.CrossRefPubMed
20.
go back to reference Piper R, Lebras J, Wentworth L, Hunt-Cooke A, Houzé S, Chiodini P, Makler M: Immunocapture diagnostic assays for malaria using Plasmodium lactate dehydrogenase (pLDH). Am J Trop Med Hyg. 1999, 60: 109-18.PubMed Piper R, Lebras J, Wentworth L, Hunt-Cooke A, Houzé S, Chiodini P, Makler M: Immunocapture diagnostic assays for malaria using Plasmodium lactate dehydrogenase (pLDH). Am J Trop Med Hyg. 1999, 60: 109-18.PubMed
21.
go back to reference Ryan A: Analysis of blood serum on the Liberty Series II ICP-AES with the axially-viewed plasma. ICP-24: Varian Inc. 1998, 1-9. Ryan A: Analysis of blood serum on the Liberty Series II ICP-AES with the axially-viewed plasma. ICP-24: Varian Inc. 1998, 1-9.
22.
go back to reference Jeurink PV, Vissers YM, Rappard B, Savelkoul HFJ: T cell responses in fresh and cryopreserved peripheral blood mononuclear cells: Kinetics of cell viability, cellular subsets, proliferation, and cytokine production. Cryobiol. 2008, 57: 91-103.CrossRef Jeurink PV, Vissers YM, Rappard B, Savelkoul HFJ: T cell responses in fresh and cryopreserved peripheral blood mononuclear cells: Kinetics of cell viability, cellular subsets, proliferation, and cytokine production. Cryobiol. 2008, 57: 91-103.CrossRef
23.
go back to reference Hartgers FC, Obeng BB, Kruize YCM, Dijkhuis A, McCall M, Sauerwein RW, Luty AJF, Boakye DA, Yazdanbakhsh M: Responses to malarial antigens are altered in helminth-infected children. J Inf Dis. 2009, 199: 1528-1535.CrossRef Hartgers FC, Obeng BB, Kruize YCM, Dijkhuis A, McCall M, Sauerwein RW, Luty AJF, Boakye DA, Yazdanbakhsh M: Responses to malarial antigens are altered in helminth-infected children. J Inf Dis. 2009, 199: 1528-1535.CrossRef
24.
go back to reference McCall MBB, Netea MG, Hermsen CC, Jansen T, Jacobs L, Golenbock D, Ven van der AJAM, Sauerwein RW: Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J Immunol. 2007, 179: 162-171.CrossRefPubMed McCall MBB, Netea MG, Hermsen CC, Jansen T, Jacobs L, Golenbock D, Ven van der AJAM, Sauerwein RW: Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J Immunol. 2007, 179: 162-171.CrossRefPubMed
25.
go back to reference Rivadeneira EM, Wasserman M, Espinal CT: Separation and concentration of schizonts of Plasmodium falciparum by Percoll gradients. J Eukary Microbiol. 1983, 30: 367-370. Rivadeneira EM, Wasserman M, Espinal CT: Separation and concentration of schizonts of Plasmodium falciparum by Percoll gradients. J Eukary Microbiol. 1983, 30: 367-370.
26.
go back to reference Artavanis-Tsakonas K, Riley EM: Innate immune response to malaria: rapid induction of IFN-γ from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol. 2002, 169: 2956-2963.CrossRefPubMed Artavanis-Tsakonas K, Riley EM: Innate immune response to malaria: rapid induction of IFN-γ from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol. 2002, 169: 2956-2963.CrossRefPubMed
27.
go back to reference Yssel H, De Vries JE, Koken M, Van Blitterswijk W, Spits H: Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. J Immunol Methods. 1984, 72: 219-227.CrossRefPubMed Yssel H, De Vries JE, Koken M, Van Blitterswijk W, Spits H: Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. J Immunol Methods. 1984, 72: 219-227.CrossRefPubMed
28.
go back to reference Imada M, Simons FE, Jay FT, HayGlass KT: Antigen mediated and polyclonal stimulation of human cytokine production elicit qualitatively different patterns of cytokine gene expression. Int Immunol. 1995, 7: 229-237.CrossRefPubMed Imada M, Simons FE, Jay FT, HayGlass KT: Antigen mediated and polyclonal stimulation of human cytokine production elicit qualitatively different patterns of cytokine gene expression. Int Immunol. 1995, 7: 229-237.CrossRefPubMed
29.
go back to reference Lichodziejewska MDB, Kos MDJ, Rezler MDJ, Grudzka MDK, Duzzniewska MDM, Budaj MDA, Ceremuzynski MDPL: Clinical symptoms of mitral valve prolapse are related to hypomagnesemia and attenuated by magnesium supplementation. Am J Cardiol. 1997, 79: 768-772.CrossRefPubMed Lichodziejewska MDB, Kos MDJ, Rezler MDJ, Grudzka MDK, Duzzniewska MDM, Budaj MDA, Ceremuzynski MDPL: Clinical symptoms of mitral valve prolapse are related to hypomagnesemia and attenuated by magnesium supplementation. Am J Cardiol. 1997, 79: 768-772.CrossRefPubMed
30.
go back to reference Naderi ASA, Reilly RF: Hereditary etiologies of hypomagnesemia. Nat Clin Pract Neph. 2008, 4: 80-89.CrossRef Naderi ASA, Reilly RF: Hereditary etiologies of hypomagnesemia. Nat Clin Pract Neph. 2008, 4: 80-89.CrossRef
31.
go back to reference Perkins DJ, Weinberg JB, Kremsner PG: Reduced interleukin-12 and Transforming Growth Factor-beta in severe childhood malaria: relationship of cytokine balance with disease severity. J Infect Dis. 2000, 182: 988-992.CrossRefPubMed Perkins DJ, Weinberg JB, Kremsner PG: Reduced interleukin-12 and Transforming Growth Factor-beta in severe childhood malaria: relationship of cytokine balance with disease severity. J Infect Dis. 2000, 182: 988-992.CrossRefPubMed
32.
go back to reference Ramharter M, Willheim M, Winkler H, Wahl K, Lagler H, Graninger W, Winkler S: Cytokine profile of Plasmodium falciparum-specific T cells in non-immune malaria patients. Parasite Immunol. 2003, 25: 211-219.CrossRefPubMed Ramharter M, Willheim M, Winkler H, Wahl K, Lagler H, Graninger W, Winkler S: Cytokine profile of Plasmodium falciparum-specific T cells in non-immune malaria patients. Parasite Immunol. 2003, 25: 211-219.CrossRefPubMed
33.
go back to reference Wintergerst ES, Maggini S, Hornig DH: Contribution of selected vitamins and trace elements to immune function. Ann Nutr Metab. 2007, 51: 301-323.CrossRefPubMed Wintergerst ES, Maggini S, Hornig DH: Contribution of selected vitamins and trace elements to immune function. Ann Nutr Metab. 2007, 51: 301-323.CrossRefPubMed
34.
go back to reference Artavanis-Tsakonas K, Tongren JE, Riley EM: The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol. 2003, 133: 145-152.PubMedCentralCrossRefPubMed Artavanis-Tsakonas K, Tongren JE, Riley EM: The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol. 2003, 133: 145-152.PubMedCentralCrossRefPubMed
35.
go back to reference Prasad A: Zinc: mechanisms of host defense. J Nutrition. 2007, 137: 1345-1349. Prasad A: Zinc: mechanisms of host defense. J Nutrition. 2007, 137: 1345-1349.
36.
go back to reference Loharungsikul S, Troye-Blomberg M, Amoudruz P, Pichyangkul S, Yongvanitchit K, Looareesuwan S, Mahakunkijcharoen Y, Sarntivijai S, Khusmith S: Expression of Toll-like receptors on antigen-presenting cells in patients with falciparum malaria. Acta Trop. 2008, 105: 10-15.CrossRefPubMed Loharungsikul S, Troye-Blomberg M, Amoudruz P, Pichyangkul S, Yongvanitchit K, Looareesuwan S, Mahakunkijcharoen Y, Sarntivijai S, Khusmith S: Expression of Toll-like receptors on antigen-presenting cells in patients with falciparum malaria. Acta Trop. 2008, 105: 10-15.CrossRefPubMed
37.
go back to reference Krishnegowda G, Hajjar AM, Zhu J, Douglass EJ, Uematsu S, Akira S, Woods AS, Gowda DC: Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem. 2005, 280: 8606-8616.CrossRefPubMed Krishnegowda G, Hajjar AM, Zhu J, Douglass EJ, Uematsu S, Akira S, Woods AS, Gowda DC: Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem. 2005, 280: 8606-8616.CrossRefPubMed
38.
go back to reference Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, Halmen KA, Lamphier M, Olivier M, Bartholomeu DC, Gazzinelli RT, Golenbock DT: Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Nat Acad Sci USA. 2007, 104: 1919-1924.PubMedCentralCrossRefPubMed Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, Halmen KA, Lamphier M, Olivier M, Bartholomeu DC, Gazzinelli RT, Golenbock DT: Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Nat Acad Sci USA. 2007, 104: 1919-1924.PubMedCentralCrossRefPubMed
39.
go back to reference Hartgers FC, Obeng BB, Voskamp A, Larbi IA, Amoah AS, Luty AJF, Boakye D, Yazdanbakhsh M: Enhanced Toll-Like Receptor responsiveness associated with mitogen-activated protein kinase activation in Plasmodium falciparum-infected children. Infect Immun. 2008, 76: 5149-5157.PubMedCentralCrossRefPubMed Hartgers FC, Obeng BB, Voskamp A, Larbi IA, Amoah AS, Luty AJF, Boakye D, Yazdanbakhsh M: Enhanced Toll-Like Receptor responsiveness associated with mitogen-activated protein kinase activation in Plasmodium falciparum-infected children. Infect Immun. 2008, 76: 5149-5157.PubMedCentralCrossRefPubMed
40.
go back to reference Rivera MT, De Souza AP, Araujo-Jorge TC, De Castro SL, Vanderpas J: Trace elements, innate immune response and parasites. Clin Chem Lab Med. 2003, 41: 1020-1025.CrossRefPubMed Rivera MT, De Souza AP, Araujo-Jorge TC, De Castro SL, Vanderpas J: Trace elements, innate immune response and parasites. Clin Chem Lab Med. 2003, 41: 1020-1025.CrossRefPubMed
41.
go back to reference Overbeck S, Rink L, Haase H: Modulating the immune response by oral zinc supplementation: a single approach for multiple diseases. Arch Immunol Ther Exp. 2008, 56: 15-30.CrossRef Overbeck S, Rink L, Haase H: Modulating the immune response by oral zinc supplementation: a single approach for multiple diseases. Arch Immunol Ther Exp. 2008, 56: 15-30.CrossRef
42.
go back to reference Haase H, Rink L: Signal transduction in monocytes: the role of zinc ions. BioMetals. 2007, 20: 579-585.CrossRefPubMed Haase H, Rink L: Signal transduction in monocytes: the role of zinc ions. BioMetals. 2007, 20: 579-585.CrossRefPubMed
43.
go back to reference Prasad AS, Bao B, Beck FWJ, Kucuk O, Sarkar FH: Antioxidant effect of zinc in humans. Free Radic Biol Med. 2004, 37: 1182-1190.CrossRefPubMed Prasad AS, Bao B, Beck FWJ, Kucuk O, Sarkar FH: Antioxidant effect of zinc in humans. Free Radic Biol Med. 2004, 37: 1182-1190.CrossRefPubMed
44.
go back to reference Wellinghausen N, Martin M, Rink L: Zinc inhibits interleukin-1-dependent T cell stimulation. Eur J Immunol. 1997, 27: 2529-2535.CrossRefPubMed Wellinghausen N, Martin M, Rink L: Zinc inhibits interleukin-1-dependent T cell stimulation. Eur J Immunol. 1997, 27: 2529-2535.CrossRefPubMed
45.
go back to reference von Bulow V, Dubben S, Engelhardt G, Hebel S, Plumakers B, Heine H, Rink L, Haase H: Zinc-dependent suppression of TNF-alpha production is mediated by protein kinase A-induced inhibition of Raf-1, I kappa B kinase beta, and NF-kappa B. J Immunol. 2007, 179: 4180-4186.CrossRefPubMed von Bulow V, Dubben S, Engelhardt G, Hebel S, Plumakers B, Heine H, Rink L, Haase H: Zinc-dependent suppression of TNF-alpha production is mediated by protein kinase A-induced inhibition of Raf-1, I kappa B kinase beta, and NF-kappa B. J Immunol. 2007, 179: 4180-4186.CrossRefPubMed
46.
go back to reference von Bulow V, Rink L, Haase H: Zinc-mediated inhibition of cyclic nucleotide phosphodiesterase activity and expression suppresses TNF-alpha and IL-1beta production in monocytes by elevation of guanosine 3',5'-cyclic monophosphate. J Immunol. 2005, 175: 4697-4705.CrossRefPubMed von Bulow V, Rink L, Haase H: Zinc-mediated inhibition of cyclic nucleotide phosphodiesterase activity and expression suppresses TNF-alpha and IL-1beta production in monocytes by elevation of guanosine 3',5'-cyclic monophosphate. J Immunol. 2005, 175: 4697-4705.CrossRefPubMed
47.
go back to reference Keller CC, Yamo O, Ouma C, Ong'echa JM, Ounah D, Hittner JB, Vulule JM, Perkins DJ: Acquisition of hemozoin by monocytes down-regulates interleukin-12 p40 (IL-12p40) transcripts and circulating IL-12p70 through an IL-10-dependent mechanism: in vivo and in vitro findings in severe malarial anemia. Infect Immun. 2006, 74: 5249-5260.PubMedCentralCrossRefPubMed Keller CC, Yamo O, Ouma C, Ong'echa JM, Ounah D, Hittner JB, Vulule JM, Perkins DJ: Acquisition of hemozoin by monocytes down-regulates interleukin-12 p40 (IL-12p40) transcripts and circulating IL-12p70 through an IL-10-dependent mechanism: in vivo and in vitro findings in severe malarial anemia. Infect Immun. 2006, 74: 5249-5260.PubMedCentralCrossRefPubMed
48.
go back to reference Uh HW, Hartgers FC, Yazdanbakhsh M, Houwing-Duistermaat JJ: Evaluation of regression methods when immunological measurements are constrained by detection limits. BMC Immunol. 2008, 9: 59-PubMedCentralCrossRefPubMed Uh HW, Hartgers FC, Yazdanbakhsh M, Houwing-Duistermaat JJ: Evaluation of regression methods when immunological measurements are constrained by detection limits. BMC Immunol. 2008, 9: 59-PubMedCentralCrossRefPubMed
49.
go back to reference Scragg IG, Hensmann M, Bate CAW, Kwiatkowski D: Early cytokine induction by Plasmodium falciparum is not a classical endotoxin-like process. Eur J Immunol. 1999, 29: 2636-2644.CrossRefPubMed Scragg IG, Hensmann M, Bate CAW, Kwiatkowski D: Early cytokine induction by Plasmodium falciparum is not a classical endotoxin-like process. Eur J Immunol. 1999, 29: 2636-2644.CrossRefPubMed
50.
go back to reference Prasad AS: Effects of zinc deficiency on Th1 and Th2 cytokine shifts. J Inf Dis. 2000, 182: S62-68.CrossRef Prasad AS: Effects of zinc deficiency on Th1 and Th2 cytokine shifts. J Inf Dis. 2000, 182: S62-68.CrossRef
51.
go back to reference Omer FM, Kurtzhals JAL, Riley EM: Maintaining the immunological balance in parasitic infections: a role for TGF-β?. Parasitol Today. 2000, 16: 18-23.CrossRefPubMed Omer FM, Kurtzhals JAL, Riley EM: Maintaining the immunological balance in parasitic infections: a role for TGF-β?. Parasitol Today. 2000, 16: 18-23.CrossRefPubMed
52.
go back to reference Torre D, Speranza F, Martegani R: Role of proinflammatory and anti-inflammatory cytokines in the immune response to Plasmodium falciparum malaria. Lancet Infect Dis. 2002, 2: 719-720.CrossRefPubMed Torre D, Speranza F, Martegani R: Role of proinflammatory and anti-inflammatory cytokines in the immune response to Plasmodium falciparum malaria. Lancet Infect Dis. 2002, 2: 719-720.CrossRefPubMed
53.
go back to reference Clark IA, Rockett KA: The cytokine theory of human cerebral malaria. Parasitol Today. 1994, 10: 410-412.CrossRefPubMed Clark IA, Rockett KA: The cytokine theory of human cerebral malaria. Parasitol Today. 1994, 10: 410-412.CrossRefPubMed
54.
go back to reference Perlmann P, Troye-Blomberg M: Malaria and the immune system in humans. Chem Immunol. 2002, 80: 229-242.CrossRefPubMed Perlmann P, Troye-Blomberg M: Malaria and the immune system in humans. Chem Immunol. 2002, 80: 229-242.CrossRefPubMed
Metadata
Title
Alterations in early cytokine-mediated immune responses to Plasmodium falciparum infection in Tanzanian children with mineral element deficiencies: a cross-sectional survey
Authors
Erasto V Mbugi
Marjolein Meijerink
Jacobien Veenemans
Prescilla V Jeurink
Matthew McCall
Raimos M Olomi
John F Shao
Hans Verhoef
Huub FJ Savelkoul
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2010
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-9-130

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