Cytokine profiles amongst Sudanese patients with visceral leishmaniasis and malaria co-infections

BMC Immunology

Volumn 15, Issue 1, 2014, Pages

  Van den Bogaart, Erika ^a   Talha, Al Badawi A ^b   Straetemans, Masja ^a   Mens, Pètra F ^a   Adams, Emily R ^d   Grobusch, Martin P ^c   Nour, Bakri Y M ^b   Schallig, Henk D F H ^a  

^a ROYAL TROPICAL INSTITUTE   (Netherlands)

^b UNIVERSITY OF GEZIRA   (Sudan)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

Co infection; Cytokines; Malaria; Sudan; Visceral leishmaniasis

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; TUMOR NECROSIS FACTOR;

ADOLESCENT; ADULT; ARTICLE; CHILD; COMPARATIVE STUDY; CONCURRENT INFECTION; CONTROLLED STUDY; FEMALE; HUMAN; IMMUNE RESPONSE; LEISHMANIA DONOVANI; MAJOR CLINICAL STUDY; MALARIA; MALARIA FALCIPARUM; MALE; MIXED INFECTION; NONHUMAN; PARASITEMIA; PLASMODIUM FALCIPARUM; RECEPTOR UPREGULATION; VISCERAL LEISHMANIASIS;

ADOLESCENT; ADULT; CHILD; COINFECTION; CYTOKINES; FEMALE; HUMANS; LEISHMANIASIS, VISCERAL; MALARIA; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; SUDAN; YOUNG ADULT;

EID: 84900860039     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-15-16     Document Type: Article

References (68)

1. Cattadori IM, Boag B, Hudson PJ. Parasite co-infection and interaction as drivers of host heterogeneity. Int J Parasitol 2008, 38(3-4):371-380.
2. Cattadori IM, Albert R, Boag B. Variation in host susceptibility and infectiousness generated by co-infection: the myxoma-Trichostrongylus retortaeformis case in wild rabbits. J R Soc Interface 2007, 4(16):831-840. 10.1098/rsif.2007.1075, 2386892, 17580288.
3. Ezenwa VO, Jolles AE. From host immunity to pathogen invasion: the effects of helminth coinfection on the dynamics of microparasites. Integr Comp Biol 2011, 51(4):540-551. 10.1093/icb/icr058, 21727178.
4. Cox FEG. Concomitant infections, parasites and immune responses. Parasitology 2001, 122(Suppl 122):S23-S38.
5. Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MM, Wammes LJ, van Lieshout L, Luty AJ, Sartono E, Yazdanbakhsh M. Polyparasitism and its impact on the immune system. Int J Parasitol 2010, 40(10):1171-1176. 10.1016/j.ijpara.2010.05.003, 20580905.
6. Graham AL, Cattadori IM, Lloyd-Smith JO, Ferrari MJ, Bjørnstad ON. Transmission consequences of coinfection: cytokines writ large?. Trends Parasitol 2007, 23(6):284-291. 10.1016/j.pt.2007.04.005, 17466597.
7. Page KR, Scott AL, Manabe YC. The expanding realm of heterologous immunity: friend or foe?. Cell Microbiol 2006, 8(2):185-196. 10.1111/j.1462-5822.2005.00653.x, 16441430.
8. Kourilsky P, Truffa-Bachi P. Cytokine fields and the polarization of the immune response. Trends Immunol 2001, 22(9):502-509. 10.1016/S1471-4906(01)02012-9, 11525941.
9. van den Bogaart E, Berkhout MM, Adams ER, Mens PF, Sentongo E, Mbulamberi DB, Straetemans M, Schallig HD, Chappuis F. Prevalence, features and risk factors of malaria co-infections among visceral leishmaniasis patients from Amudat Hospital. Uganda PLoS Negl Trop Dis 2012, 6(4):e1617.
10. van den Bogaart E, Berkhout MM, Nour AB, Mens PF, Talha AB, Adams ER, Ahmed HB, Abdelrahman SH, Ritmeijer K, Nour BY, Schallig HD. Concomitant malaria among visceral leishmaniasis in-patients from Gedarif and Sennar States, Sudan: a retrospective case-control study. BMC Public Health 2013, 13:332. 10.1186/1471-2458-13-332, 3659061, 23577673.
11. Stäger S, Joshi T, Bankoti R. Immune evasive mechanisms contributing to persistent Leishmania donovani infection. Immunol Res 2010, 47(1-3):14-24.
12. Olivier M, Gregory DJ, Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 2005, 18(2):293-305. 10.1128/CMR.18.2.293-305.2005, 1082797, 15831826.
13. Bacellar O, Brodskyn C, Carvalho EM, Barral-Netto M, Costa CH, Coffman RL, Johnson WD, Carvalho EM. Interleukin-12 restores interferon-γ production and cytotoxic responses in visceral leishmaniasis. J Infect Dis 1996, 173(6):1515-1518. 10.1093/infdis/173.6.1515, 8648233.
14. Hailu A, van Baarle D, Knol GJ, Berhe N, Miedema F, Kager PA. T cell subset and cytokine profiles in human visceral leishmaniasis during active and asymptomatic or sub-clinical infection with Leishmania donovani. Clin Immunol 2005, 117(2):182-191. 10.1016/j.clim.2005.06.015, 16125466.
15. Karp CL, El-Safi SH, Wynn TA, Satti MM, Kordofani AM, Hashim FA, Hag-Ali M, Neva FA, Nutman TB, Sacks DL. In vivo cytokine profiles in patients with kala-azar: marked elevation of both interleukin-10 and interferon-gamma. J Clin Invest 1993, 91(4):1644-1648. 10.1172/JCI116372, 288142, 8097208.
16. Nylén S, Maurya R, Eidsmo L, Manandhar KD, Sundar S, Sacks D. Splenic accumulation of IL-10 mRNA in T cells distinct from CD4 + CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J Exp Med 2007, 204(4):805-817. 10.1084/jem.20061141, 2118563, 17389235.
17. Ansari NA, Saluja S, Salotra P. Elevated levels of interferon-γ, interleukin-10, and interleukin-6 during active disease in Indian kala azar. Clin Immunol 2006, 119(3):339-345. 10.1016/j.clim.2006.01.017, 16540374.
18. Nylén S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol 2007, 28(9):378-384. 10.1016/j.it.2007.07.004, 17689290.
19. McGuirk P, Mills KHG. Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends in Immunol 2002, 23(9):450-455.
20. Ghalib HW, Piuvezam MR, Skeiky YAW, Siddig M, Hashim FA, El-Hassan AM, Russo DM, Reed SG. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 1993, 92(1):324-329. 10.1172/JCI116570, 293600, 8326000.
21. Walther M, Tongren JE, Andrews L, Korbel D, King E, Fletcher H, Andersen RF, Bejon P, Thompson F, Dunachie SJ, Edele F, de Souza JB, Sinden RE, Gilbert SC, Riley EM, Hill AV. Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 2005, 23(3):287-296. 10.1016/j.immuni.2005.08.006, 16169501.
22. Todryk SM, Bejon P, Mwangi T, Plebanski M, Urban B, Marsh K, Hill AV, Flanagan KL. Correlation of memory T cell responses against TRAP with protection from clinical malaria, and CD4 CD25 high T cells with susceptibility in Kenyans. PLoS ONE 2008, 3:e2027. 10.1371/journal.pone.0002027, 2323567, 18446217.
23. Torcia MG, Santarlasci V, Cosmi L, Clemente A, Maggi L, Mangano VD, Verra F, Bancone G, Nebie I, Sirima BS, Liotta F, Frosali F, Angeli R, Severini C, Sannella AR, Bonini P, Lucibello M, Maggi E, Garaci E, Coluzzi M, Cozzolino F, Annunziato F, Romagnani S, Modiano D. Functional deficit of T regulatory cells in Fulani, an ethnic group with low susceptibility to Plasmodium falciparum malaria. Proc Natl Acad Sci U S A 2008, 105(2):646-651. 10.1073/pnas.0709969105, 2206590, 18174328.
24. Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, Deininger S, Lawrence E, Ngwa-Amambua A, Jayasooriya S, Cheeseman IH, Gomez-Escobar N, Okebe J, Conway DJ, Riley EM. Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog 2009, 5(4):e1000364. 10.1371/journal.ppat.1000364, 2658808, 19343213.
25. Minigo G, Woodberry T, Piera KA, Salwati E, Tjitra E, Kenangalem E, Price RN, Engwerda CR, Anstey NM, Plebanski M. Parasite-dependent expansion of TNF receptor II-positive regulatory T cells with enhanced suppressive activity in adults with severe malaria. PLoS Pathog 2009, 5(4):e1000402. 10.1371/journal.ppat.1000402, 2668192, 19390618.
26. Ferreira A, Schofield L, Enea V, Schellekens H, Van der Meide P, Collins WE, Nussenzweig RS, Nussenzweig V. Inhibition of development of exoerythrocytic forms of malaria parasites by gamma-interferon. Science 1986, 232(4752):881. 10.1126/science.3085218, 3085218.
27. Ferreira A, Enea V, Morimoto T, Nussenzweig V. Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro. J Immunol 1987, 139(6):2020-2025.
28. McCall MB, Sauerwein RW. Interferon-γ-central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J Leukoc Biol 2010, 88(6):1131-1143. 10.1189/jlb.0310137, 20610802.
29. Lumsden JM, Schwenk RJ, Rein LE. Protective immunity induced with the RTS, S/AS vaccine is associated with IL-2 and TNF-alpha producing effector and central memory CD4 T cells. PLoS ONE 2011, 6(7):e20775. 10.1371/journal.pone.0020775, 3136919, 21779319.
30. Nussler A, Pied S, Goma J, Renia L, Miltgen F, Grau GE, Mazier D. TNF inhibits malaria hepatic stages in vitro via synthesis of IL-6. Int Immunol 1991, 3(4):317-321. 10.1093/intimm/3.4.317, 1878339.
31. Sun P, Schwenk R, White K, Stoute JA, Cohen J, Ballou WR, Voss G, Kester KE, Heppner DG, Krzych U. Protective immunity induced with malaria vaccine, RTS, S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J Immunol 2003, 171(12):6961-6967. 10.4049/jimmunol.171.12.6961, 14662904.
32. Cabantous S, Poudiougou B, Traore A, Keita M, Cisse MB, Doumbo O, Dessein AJ, Marquet S. Evidence that interferon-gamma plays a protective role during cerebral malaria. J Infect Dis 2005, 192(5):854-860. 10.1086/432484, 16088835.
33. D'Ombrain MC, Robinson LJ, Stanisic DI, Taraika J, Bernard N, Michon P, Mueller I, Schofield L. Association of early interferon-gamma production with immunity to clinical malaria: a longitudinal study among Papua New Guinean children. Clin Infect Dis 2008, 47(11):1380-1387. 10.1086/592971, 18947328.
34. Robinson LJ, D'Ombrain MC, Stanisic DI, Taraika J, Bernard N, Richards JS, Beeson JG, Tavul L, Michon P, Mueller I, Schofield L. Cellular tumor necrosis factor, gamma interferon, and interleukin-6 responses as correlates of immunity and risk of clinical Plasmodium falciparum malaria in children from Papua New Guinea. Infect Immun 2009, 77(7):3033-3043. 10.1128/IAI.00211-09, 2708537, 19380468.
35. Luty AJ, Lell B, Schmidt-Ott R, Luckner D, Greve B, Matousek P, Herbich K, Schmid D, Migot-Nabias F, Deloron P, Nussenzweig RS, Kremsner PG. Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis 1999, 179(4):980-988. 10.1086/314689, 10068595.
36. Roestenberg M, McCall M, Hopman J, Wiersma J, Luty AJ, van Gemert GJ, van de Vegte-Bolmer M, van Schaijk B, Teelen K, Arens T, Spaarman L, de Mast Q, Roeffen W, Snounou G, Rénia L, van der Ven A, Hermsen CC, Sauerwein R. Protection against a malaria challenge by sporozoite inoculation. N Engl J Med 2009, 361(5):468-477. 10.1056/NEJMoa0805832, 19641203.
37. Doolan DL, Hoffman SL. The complexity of protective immunity against liver-stage malaria. J Immunol 2000, 165(3):1453-1462. 10.4049/jimmunol.165.3.1453, 10903750.
38. Perlaza BL, Sauzet JP, Brahimi K, BenMohamed L, Druilhe P. Interferon-gamma, a valuable surrogate marker of Plasmodium falciparum pre-erythrocytic stages protective immunity. Malar J 2011, 10(1):27. 10.1186/1475-2875-10-27, 3046914, 21303495.
39. Artavanis-Tsakonas K, Riley EM. Innate immune response to malaria: rapid induction of INF-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 2002, 169(6):2956-2963. 10.4049/jimmunol.169.6.2956, 12218109.
40. Teirlinck AC, McCall MBB, Roestenberg M, Scholzen A, Woestenenk R, de Mast Q, van der Ven AJ, Hermsen CC, Luty AJ, Sauerwein RW. Longevity and composition of cellular immune responses following experimental Plasmodium falciparum malaria infection in humans. PLoS Pathog 2011, 7(12):e1002389. 10.1371/journal.ppat.1002389, 3228790, 22144890.
41. Hensmann M, Kwiatkowski D. Cellular basis of early cytokine response to Plasmodium falciparum. Infect Immun 2001, 69(4):2364-2371. 10.1128/IAI.69.4.2364-2371.2001, 98166, 11254594.
42. Biemba G, Gordeuk VR, Thuma P, Weiss G. Markers of inflammation in children with several malarial anaemia. Trop Med Int Health 2000, 5(4):256-262.
43. Rovira-Vallbona E, Moncunill G, Bassat Q, Aguilar R, Machevo S, Puyol L, Quintó L, Menéndez C, Chitnis CE, Alonso PL, Dobaño C, Mayor A. Low antibodies against Plasmodium falciparum and imbalanced pro-inflammatory cytokines are associated with severe malaria in Mozambican children: a case-control study. Malar J 2012, 11:181. 10.1186/1475-2875-11-181, 3464173, 22646809.
44. Perkins DJ, Weinberg JB, Kremsner PG. Reduced interleukin-12 and transforming growth factor-beta1 in severe childhood malaria: relationship of cytokine balance with disease severity. J Infect Dis 2000, 182(3):988-992. 10.1086/315762, 10950804.
45. Hunt NH, Grau GE. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 2003, 24(9):491-499. 10.1016/S1471-4906(03)00229-1, 12967673.
46. Marques CS, Rolão N, Centeno-Lima S, Lousada H, Maia C, Campino L, do Rosário VE, Silveira H. Studies in a co-infection murine model of Plasmodium chabaudi chabaudi and Leishmania infantum: interferon-gamma and interleukin-4 mRNA expression. Mem Inst Oswaldo Cruz 2005, 100(8):889-892. 10.1590/S0074-02762005000800011, 16444421.
47. Coleman RE, Edman JD, Semprevivo LH. Leishmania mexicana: effect of concomitant malaria on cutaneous leishmaniasis. Development of lesions in a Leishmania-susceptible (BALB/c) strain of mouse. Exp Parasitol 1988, 65(2):269-276. 10.1016/0014-4894(88)90131-2, 3350106.
48. Coleman RE, Edman JD, Semprevivo LH. Interactions between Plasmodium yoelii and Leishmania mexicana amazonensis in Leishmania resistant C57B1/6 mice. Am J Trop Med Hyg 1988, 39(6):540-544.
49. Adler S. The behaviour of Plasmodium berghei in the golden hamster Mesocricetus auratus infected with visceral leishmaniasis. Trans R Soc Trop Med Hyg 1954, 48(5):431-440. 10.1016/0035-9203(54)90145-5, 13216948.
50. Center for Disease Control and Prevention Guidelines for the Use of Antiretroviral Agents in Pediatric HIV Infection 1998, Atlanta: MMWR 47(No. RR-4), Center for Disease Control and Prevention.
51. Comans-Bitter WM, de Groot R, van den Beemd R, Neijens HJ, Hop WC, Groeneveld K, Hooijkaas H, van Dongen JJ. Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations. J Pediatr 1997, 130(3):388-393. 10.1016/S0022-3476(97)70200-2, 9063413.
52. Warhurst DC, Williams JE. Laboratory diagnosis of malaria. J Clin Pathol 1996, 49(7):533-538. 10.1136/jcp.49.7.533, 500564, 8813948.
53. Harith AE, Kolk AH, Kager PA, Leeuwenburg J, Muigai R, Kiugu S, Laarman JJ. A simple and economical direct agglutination test for serodiagnosis and seroepidemiological studies of visceral leishmaniasis. Trans R Soc Trop Med Hyg 1986, 80(4):583-587. 10.1016/0035-9203(86)90149-5, 3101241.
54. World Health Organization Expert Committee Control of the Leishmaniases 1990, Geneva: WHO Technical Report Series No. 793, World Health Organization Expert Committee.
55. O'Connor W, Zenewicz LA, Flavell RA. The dual nature of T (H) 17 cells: shifting the focus to function. Nat Immunol 2010, 11(6):471-476. 10.1038/ni.1882, 20485275.
56. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006, 203(10):2271-2279. 10.1084/jem.20061308, 2118116, 16982811.
57. Pitta MGR, Romano A, Cabantous S, Henri S, Hammad A, Kouriba B, Argiro L, el Kheir M, Bucheton B, Mary C, El-Safi SH, Dessein A. IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J Clin Invest 2009, 119(8):2379-2387. 2719936, 19620772.
58. Ghosh K, Sharma G, Saha A, Kar S, Das PK, Ukil A. Successful therapy of visceral leishmaniasis with curdlan involves T-helper 17 cytokines. J Infect Dis 2013, 207(6):1016-1025. 10.1093/infdis/jis771, 23255562.
59. Bueno LL, Morais CG, Lacerda MV, Fujiwara RT, Braga T. Interleukin-17 producing T helper cells are increased during natural Plasmodium vivax infection. Acta Trop 2012, 123(1):53-57. 10.1016/j.actatropica.2012.02.071, 22476130.
60. Ishida H, Imai T, Suzue K, Hirai M, Taniguchi T, Yoshimura A, Iwakura Y, Okada H, Suzuki T, Shimokawa C, Hisaeda H. IL-23 protection against Plasmodium berghei infection in mice is partially dependent on IL-17 from macrophages. Eur J Immunol 2013, 43(10):2696-2706. 10.1002/eji.201343493, 23843079.
61. Mastelic B, Do Rosario AP, Veldhoen M, Renauld JC, Jarra W, Spoonas AM, Roetynck S, Stockinger B, Langhorne J. IL-22 protects against liver pathology and lethality of an experimental blood-stage malaria infection. Front Immunol 2012, 3:85. 3342387, 22566965.
62. Ryan-Payseur B, Ali Z, Huang D, Chen CY, Yan L, Wang RC, Collins WE, Wang Y, Chen ZW. Virus infection stages and distinct Th1 or Th17/Th22 T-cell responses in malaria/SHIV coinfection correlate with different outcomes of disease. J Infect Dis 2011, 204(9):1450-1462. 10.1093/infdis/jir549, 3218650, 21921207.
63. Hu WC. Human immune responses to Plasmodium falciparum infection: molecular evidence for a suboptimal THalphabeta and TH17 bias over ideal and effective traditional TH1 immune response. Malar J 2013, 12(1):392. 10.1186/1475-2875-12-392, 3928643, 24188121.
64. Griffiths MJ, Shafi MJ, Popper SJ, Hemingway CA, Kortok MM, Wathen A, Rockett KA, Mott R, Levin M, Newton CR, Marsh K, Relman DA, Kwiatkowski DP. Genomewide analysis of the host response to malaria in Kenyan children. J Infect Dis 2005, 191(10):1599-1611. 10.1086/429297, 15838786.
65. Doolan DL, Martinez-Alier N. Immune response to pre-erythocytic stages of malaria parasites. Cur Mol Med 2006, 6(2):169-185.
66. Puri SK, Maheshwari RK, Dutta GP, Friedman RM, Dhar MM. Human interferon-gamma protects rhesus monkeys against sporozoite-induced Plasmodium cynomolgi malaria infection. J Interferon Res 1988, 8(2):201-206. 10.1089/jir.1988.8.201, 3132512.
67. Donovan MJ, Messmore AS, Scrafford DA, Sacks DL, Kamhawi S, Kamhawi S, McDowell MA. Uninfected mosquito bites confer protection against infection with malaria parasites. Infect Immun 2007, 75(5):2523-2530. 10.1128/IAI.01928-06, 1865743, 17339356.
68. De Oliveira CI, Teixeira MJ, Gomes R, Barral A, Brodskyn C. Animal models for infectious diseases caused by parasites: Leishmaniasis. Drug Dis Today: Dis Mod 2004, 1(1):81-86.