The effect of maternal helminth infection on maternal and neonatal immune function and immunity to tuberculosis

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Gebreegziabiher, Dawit ^a,b,c   Desta, Kassu ^b   Desalegn, Girmay ^a,b   Howe, Rawleigh ^a   Abebe, Markos ^a  

^a ARMAUER HANSEN RESEARCH INSTITUTE   (Ethiopia)

^b ADDIS ABABA UNIVERSITY   (Ethiopia)

^c MEKELLE UNIVERSITY   (Ethiopia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERLEUKIN 4; BACTERIUM ANTIBODY; HELMINTH ANTIBODY; IFNG PROTEIN, HUMAN; IL4 PROTEIN, HUMAN;

ADULT; AMEBIASIS; ARTICLE; ASCARIASIS; BACTERIAL IMMUNITY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CYTOKINE RESPONSE; ELISA KIT; ELISA READER; ELISPOT KIT; ELISPOT READER; ENTEROBIASIS; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GIARDIASIS; HELMINTHIASIS; HUMAN; HUMAN CELL; HYMENOLEPIASIS; IMMUNOLOGY TEST KIT; LATENT TUBERCULOSIS; MAJOR CLINICAL STUDY; MICROPLATE READER; MIXED INFECTION; MONONUCLEAR CELL; MYCOBACTERIUM TUBERCULOSIS TEST KIT; NEWBORN; PARASITE PREVALENCE; PLACENTAL TRANSFER; SCHISTOSOMIASIS MANSONI; TRICHURIASIS; UMBILICAL CORD BLOOD; ANIMAL; BLOOD; CLINICAL TRIAL; ETHIOPIA; FETOMATERNAL TRANSFUSION; FETUS BLOOD; IMMUNOLOGY; MALE; MYCOBACTERIUM BOVIS; PREGNANCY; PREGNANCY COMPLICATION; SCHISTOSOMA MANSONI; TUBERCULOSIS;

ADULT; ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, HELMINTH; CROSS-SECTIONAL STUDIES; ETHIOPIA; FEMALE; FETAL BLOOD; HUMANS; INFANT, NEWBORN; INTERFERON-GAMMA; INTERLEUKIN-4; LEUKOCYTES, MONONUCLEAR; MALE; MATERNAL-FETAL EXCHANGE; MYCOBACTERIUM BOVIS; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TUBERCULOSIS;

EID: 84899462904     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093429     Document Type: Article

References (52)

1. Bentwich Z, Horner R, Borkow G (2010) De-Worming in Developing Countries as a Feasible and Affordable Means to Fight Co-Endemic Infectious Diseases. Open Biology Journal 3:97-103.
2. Bourke C, Maizels R, Mutapi F (2011) Acquired immune heterogeneity and its sources in human helminth infection. Parasitology 138(02):139-159.
3. Sheriff FG, Manji KP, Manji MP, Chagani MM, Mpembeni RM, et al. (2010) Latent tuberculosis among pregnant mothers in a resource poor setting in Northern Tanzania: a cross-sectional study. BMC Infect Dis; 10(1):52.
4. Banfield S, Pascoe E, Thambiran A, Siafarikas A, Burgner D (2012) Factors associated with the performance of a blood-based interferon-γ release assay in diagnosing tuberculosis. PloS one 7(6):e38556.
5. Loto OM, Awowole I (2012) Tuberculosis in Pregnancy. A Review: Journal of Pregnancy.
6. Hassan G, Qureshi W, Kadri S (1994) Congenital tuberculosis. tuberculosis 13:73-741.
7. Latorre I, Martínez-Lacasa X, Font R, Lacoma A, Puig J, et al. (2010) IFN-γ response on T-cell based assays in HIV-infected patients for detection of tuberculosis infection. BMC Infect Dis; 10(348):1471-2334.
8. Kariminia A, Sharifnia Z, Aghakhani A, Banifazl M, Eslamifar A, et al. (2009) Comparison of QuantiFERON TB-G-test to TST for detecting latent tuberculosis infection in a high-incidence area containing BCG-vaccinated population. J Eval Clin Pract; 15(1):148-151.
9. Hassan G, Waseem Q, SM K (October-December 2006) Congenital T uberculosis. JK Science 8(4).
10. Chen A, Shih SL (2004) Congenital tuberculosis in two infants. Am J Roentgenol; 182(1):253-256. (Pubitemid 38017750)
11. Laartz BW, Nar varte HJ, Holt D, Larkin JA, Pomputius WF (2002) Congenital tuberculosis and management of exposures in neonatal intensive care unit. Infect Control Hosp Epidemiol; 23(10):573-579.
12. Elias D, Britton S, Aseffa A, Engers H, Akuffo H (2008) Poor immunogenicity of BCG in helminth infected population is associated with increasedin vitroTGF-β production. Vaccine 26:3897-3902.
13. Kozakiewicz L, Phuah J, Flynn J, Chan J (2013) The Role of B Cells and Humoral Immunity in Mycobacterium tuberculosis Infection. The New Paradigm of Immunity to Tuberculosis : Springer 2013:225-250.
14. Manivannan S, Narayan RV, Ramanathan VD (2012) Role of complement activation and antibody in the interaction between Mycobacterium tuberculosis and human macrophages. Indian J Exp Biol; 50:542-550.
15. Elliott AM, Kizza M, Quigley MA, Ndibazza J, Nampijja M, et al. (2007) The impact of helminths on the response to immunization and on the incidence of infection and disease in childhood in Uganda: design of a randomized, double-blind, placebo-controlled, factorial trial of deworming interventions delivered in pregnancy and early childhood [ISRCTN32849447]. Clinical Trials 4(1):42-57.
16. Malhotra I, Ouma JH, Wamachi A, Kioko J, Mungai P, et al. (2003) Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun; 71(9):5231-5237. (Pubitemid 37070769)
17. Elliott AM, Namujju PB, Mawa PA, Quigley MA, Nampijja M, et al. (2005) A randomised controlled trial of the effects of albendazole in pregnancy on maternal responses to mycobacterial antigens and infant responses to Bacille Calmette-Guerin (BCG) immunisation [ISRCTN32849447]. BMC Infect Dis; 5(1):115.
18. Woodburn PW, Muhangi L, Hillier S, Ndibazza J, Namujju PB, et al. (2009) Risk factors for helminth, malaria, and HIV infection in pregnancy in Entebbe, Uganda. PLoS Negl Trop Dis 3(6):e473.
19. Malhotra I, Ouma J, Wamachi A, Kioko J, Mungai P, et al. (1997) In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J Clin Invest; 99(7):1759.
20. Christian P, Khatry SK, West KP (2004) Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. The Lancet 364(9438):981-983. (Pubitemid 39208460)
21. LaBeaud AD, Malhotra I, King MJ, King CL, King CH (2009) Do antenatal parasite infections devalue childhood vaccination? PLoS Negl Trop Dis 3(5):e442.
22. Baidoo S, Tay S, Obiri-Danso K, Abruquah H (2010) Intestinal helminth infection and anaemia during pregnancy: A community based study in Ghana. J Bacteriol Res 2(2):9-13.
23. MacDonald AS, Araujo MI, Pearce EJ (2002) Immunology of parasitic helminth infections. Infect Immun; 70(2):427-433. (Pubitemid 34083798)
24. Maizels R, Yazdanbakhsh M (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat rev immunol 3(9):733-744. (Pubitemid 41070814)
25. Cooper PJ, Chico ME, Guadalupe I, Sandoval CA, Mitre E, et al. (2011) Impact of early life exposures to geohelminth infections on the development of vaccine immunity, allergic sensitization, and allergic inflammatory diseases in children living in tropical Ecuador: the ECUAVIDA birth cohort study. BMC Infect Dis; 11(184):1471-2334.
26. Elias D, Wolday D, Akuffo H, Petros B, Bronner U, et al. (2001) Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after Bacille Calmette-GueÂrin (BCG) vaccination. Clin Exp Immunol; 123:219-225. (Pubitemid 32174772)
27. Liu Z, Liu Q, Pesce J, Whitmire J, Ekkens MJ, et al. (2002) Nippostrongylus brasiliensis can induce B7-independent antigen-specific development of IL-4-producing T cells from naive CD4 T cells in vivo. J Immunol 169(12):6959.
28. Seydel LS, Petelski A, van Dam GJ, van der Kleij D, Kruize-Hoeksma YCM, et al. (2012) Association of In Utero Sensitization to Schistosoma haematobium with Enhanced Cord Blood IgE and Increased Frequencies of CD5-B Cells in African Newborns. Am J Trop Med Hyg; 86(4):613-619.
29. McMichael AJ, Rowland-Jones SL (2001) Cellular immune responses to HIV. Nature 410(6831):980-987. (Pubitemid 32335849)
30. Elias D, AkuffoH, Pawlowski A, Haile M, SchonT, et al. (2005) Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine 23:1326-1334. (Pubitemid 40127324)
31. Gallagher M, Malhotra I, Mungai PL, Wamachi AN, Kioko JM, et al. (2005) The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS 19(16):1849.
32. Pit D, Polderman A, Schulz-Key H, Soboslay P (2000) Prenatal immune priming with helminth infections: parasite specific cellular reactivity and Th1 and Th2 cytokine responses in neonates. Allergy 55(8):732-739. (Pubitemid 30619490)
33. Soboslay P, Geiger S, Drabner B, Banla M, Batchassi E, et al. (1999) Prenatal immune priming in onchocerciasis-Onchocerca volvulus-specific cellular responsiveness and cytokine production ils newborns from infected mothers. Clin Exp Immunol; 117:130-137. (Pubitemid 29292788)
34. Elias D, Akuffo H, Thors C, Pawlowski A, Britton S (2005) Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin Exp Immunol; 139(3):398-404. (Pubitemid 40333250)
35. Malhotra I, Mungai PL, Wamachi AN, Tisch D, Kioko JM, et al. (2006) Prenatal T cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. J Infect Dis; 193(7):1005-1013.
36. Pearce E (2005) Priming of the immune response by schistosome eggs. Parasite Immunol; 27(7-8):265-270.
37. Faheem S, Karim M, Mohamed M, Mohamedsuhel C, Rose M, et al. Latent tuberculosis among pregnant mothers in a resource poor setting in Northern Tanzania: a cross-sectional study. BMC infectious diseases 10.
38. Raja A (2004) Immunology of tuberculosis. Indian J Med Res 120:213-232.
39. NALA Foundation Report (2009/2010) Deworming program in Mekelle. Bringing Hope to Africa.
40. Legesse M, Ameni G, Mamo G, Medhin G, Bjune G, et al. (2011) Community-based cross-sectional survey of latent tuberculosis infection in Afar pastoralists, Ethiopia, using QuantiFERON-TB Gold In-Tube and tuberculin skin test. BMC Infect Dis; 11(1):89.
41. Legesse M, Ameni G, Mamo G, Medhin G, Bjune G, et al. (2010) Performance of QuantiFERON-TB Gold In-Tube (QFTGIT) for the diagnosis of Mycobacterium tuberculosis (Mtb) infection in Afar Pastoralists, Ethiopia. BMC Infect Dis; 10(1):354.
42. Dagnew AF, Hussein J, Abebe M, Zewdie M, Mihret A, et al. (2012) Diagnosis of latent tuberculosis infection in healthy young adults in a country with high tuberculosis burden and BCG vaccination at birth. BMC Research Notes 5(1):415.
43. Reinharda G, Arno Nolla A, Schlebuschb H, Peter Mallmannc P, Rueckera AV (2002) Shifts in the TH1/TH2 Balance during Human Pregnancy Correlate with Apoptotic Changes. Biomedical and biophysical communications 245(3):933-938.
44. King CL, Malhotra I, Mungai P, Wamachi A, Kioko J, et al. (1998) B cell sensitization to helminthic infection develops in utero in humans. J Immunol 160(7):3578-3584. (Pubitemid 28164754)
45. Bentwich Z, Kalinkovich A, Weisman Z, Borkow G, Beyers N, et al. (1999) Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunol Today 20(11):485-487. (Pubitemid 29507090)
46. Demissie A, Abebe M, Aseffa A, Rook G, Fletcher H, et al. (2004) Healthy individuals that control a latent infection with Mycobacterium tuberculosis express high levels of Th1 cytokines and the IL-4 antagonist IL-4d2. J Immunol 172(11):6938.
47. Potian JA, Rafi W, Bhatt K, McBride A, Gause WC, et al. (2011) Preexisting helminth infection induces inhibition of innate pulmonary anti-tuberculosis defense by engaging the IL-4 receptor pathway. J Exp Med 208(9):1863-1874.
48. Stewart G, Boussinesq M, Coulson T, Elson L, Nutman T, et al. (1999) Onchocerciasis modulates the immune response to mycobacterial antigens. Clin Exp Immunol; 117(3):517.
49. Leng Q, Bentwich Z, Borkow G (2006) Increased TGF-beta, Cbl-b and CTLA-4 levels and immunosuppression in association with chronic immune activation. Int Immunol 18:637-644. (Pubitemid 43779053)
50. McElroy MD, Elrefaei M, Jones N, Ssali F, Mugyenyi P, et al. (1996) High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. JID (173):769-773.
51. Doetze A, Satoguina J, Burchard G, Rau T, Loliger C, et al. (2000) Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int Immunol 12:623-630. (Pubitemid 30248895)
52. Elston DM (2006) The hygiene hypothesis and atopy: Bring back the parasites? J Am Acad Dermatol; 54(1):172-178.