Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life
Abstract Background Factors driving inter-individual differences in immune responses upon different types of prenatal malaria exposure (PME) and subsequent risk of malaria in infancy remain poorly understood. In this study, we examined the impact of four types of PME (i.e., maternal peripheral infec...
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| Format: | Article |
| Language: | English |
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BMC
2018-11-01
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| Series: | BMC Medicine |
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| Online Access: | http://link.springer.com/article/10.1186/s12916-018-1187-3 |
| _version_ | 1818441514219470848 |
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| author | Hamtandi Magloire Natama Gemma Moncunill Eduard Rovira-Vallbona Héctor Sanz Hermann Sorgho Ruth Aguilar Maminata Coulibaly-Traoré M. Athanase Somé Susana Scott Innocent Valéa Petra F. Mens Henk D. F. H. Schallig Luc Kestens Halidou Tinto Carlota Dobaño Anna Rosanas-Urgell |
| author_facet | Hamtandi Magloire Natama Gemma Moncunill Eduard Rovira-Vallbona Héctor Sanz Hermann Sorgho Ruth Aguilar Maminata Coulibaly-Traoré M. Athanase Somé Susana Scott Innocent Valéa Petra F. Mens Henk D. F. H. Schallig Luc Kestens Halidou Tinto Carlota Dobaño Anna Rosanas-Urgell |
| author_sort | Hamtandi Magloire Natama |
| collection | DOAJ |
| description | Abstract Background Factors driving inter-individual differences in immune responses upon different types of prenatal malaria exposure (PME) and subsequent risk of malaria in infancy remain poorly understood. In this study, we examined the impact of four types of PME (i.e., maternal peripheral infection and placental acute, chronic, and past infections) on both spontaneous and toll-like receptors (TLRs)-mediated cytokine production in cord blood and how these innate immune responses modulate the risk of malaria during the first year of life. Methods We conducted a birth cohort study of 313 mother-child pairs nested within the COSMIC clinical trial (NCT01941264), which was assessing malaria preventive interventions during pregnancy in Burkina Faso. Malaria infections during pregnancy and infants’ clinical malaria episodes detected during the first year of life were recorded. Supernatant concentrations of 30 cytokines, chemokines, and growth factors induced by stimulation of cord blood with agonists of TLRs 3, 7/8, and 9 were measured by quantitative suspension array technology. Crude concentrations and ratios of TLR-mediated cytokine responses relative to background control were analyzed. Results Spontaneous production of innate immune biomarkers was significantly reduced in cord blood of infants exposed to malaria, with variation among PME groups, as compared to those from the non-exposed control group. However, following TLR7/8 stimulation, which showed higher induction of cytokines/chemokines/growth factors than TLRs 3 and 9, cord blood cells of infants with evidence of past placental malaria were hyper-responsive in comparison to those of infants not-exposed. In addition, certain biomarkers, which levels were significantly modified depending on the PME category, were independent predictors of either malaria risk (GM-CSF TLR7/8 crude) or protection (IL-12 TLR7/8 ratio and IP-10 TLR3 crude, IL-1RA TLR7/8 ratio) during the first year of life. Conclusions These findings indicate that past placental malaria has a profound effect on fetal immune system and that the differential alterations of innate immune responses by PME categories might drive heterogeneity between individuals to clinical malaria susceptibility during the first year of life. |
| first_indexed | 2024-12-14T18:29:27Z |
| format | Article |
| id | doaj.art-a25207b8eca44804979d5600ca93d1d3 |
| institution | Directory Open Access Journal |
| issn | 1741-7015 |
| language | English |
| last_indexed | 2024-12-14T18:29:27Z |
| publishDate | 2018-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Medicine |
| spelling | doaj.art-a25207b8eca44804979d5600ca93d1d32022-12-21T22:51:50ZengBMCBMC Medicine1741-70152018-11-0116111510.1186/s12916-018-1187-3Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of lifeHamtandi Magloire Natama0Gemma Moncunill1Eduard Rovira-Vallbona2Héctor Sanz3Hermann Sorgho4Ruth Aguilar5Maminata Coulibaly-Traoré6M. Athanase Somé7Susana Scott8Innocent Valéa9Petra F. Mens10Henk D. F. H. Schallig11Luc Kestens12Halidou Tinto13Carlota Dobaño14Anna Rosanas-Urgell15Department of Biomedical Sciences, Institute of Tropical MedicineBarcelona Institute for Global Health (ISGlobal), Hospital Clinic – Universitat de BarcelonaDepartment of Biomedical Sciences, Institute of Tropical MedicineBarcelona Institute for Global Health (ISGlobal), Hospital Clinic – Universitat de BarcelonaUnité de Recherche Clinique de Nanoro, Institut de Recherche en Sciences de la SantéBarcelona Institute for Global Health (ISGlobal), Hospital Clinic – Universitat de BarcelonaUnité de Recherche Clinique de Nanoro, Institut de Recherche en Sciences de la SantéUnité de Recherche Clinique de Nanoro, Institut de Recherche en Sciences de la SantéDepartment of Epidemiology and Population Health, London School of Hygiene and Tropical MedicineUnité de Recherche Clinique de Nanoro, Institut de Recherche en Sciences de la SantéDepartment of Medical Microbiology - Parasitology Unit, Academic Medical CentreDepartment of Medical Microbiology - Parasitology Unit, Academic Medical CentreDepartment of Biomedical Sciences, Institute of Tropical MedicineUnité de Recherche Clinique de Nanoro, Institut de Recherche en Sciences de la SantéBarcelona Institute for Global Health (ISGlobal), Hospital Clinic – Universitat de BarcelonaDepartment of Biomedical Sciences, Institute of Tropical MedicineAbstract Background Factors driving inter-individual differences in immune responses upon different types of prenatal malaria exposure (PME) and subsequent risk of malaria in infancy remain poorly understood. In this study, we examined the impact of four types of PME (i.e., maternal peripheral infection and placental acute, chronic, and past infections) on both spontaneous and toll-like receptors (TLRs)-mediated cytokine production in cord blood and how these innate immune responses modulate the risk of malaria during the first year of life. Methods We conducted a birth cohort study of 313 mother-child pairs nested within the COSMIC clinical trial (NCT01941264), which was assessing malaria preventive interventions during pregnancy in Burkina Faso. Malaria infections during pregnancy and infants’ clinical malaria episodes detected during the first year of life were recorded. Supernatant concentrations of 30 cytokines, chemokines, and growth factors induced by stimulation of cord blood with agonists of TLRs 3, 7/8, and 9 were measured by quantitative suspension array technology. Crude concentrations and ratios of TLR-mediated cytokine responses relative to background control were analyzed. Results Spontaneous production of innate immune biomarkers was significantly reduced in cord blood of infants exposed to malaria, with variation among PME groups, as compared to those from the non-exposed control group. However, following TLR7/8 stimulation, which showed higher induction of cytokines/chemokines/growth factors than TLRs 3 and 9, cord blood cells of infants with evidence of past placental malaria were hyper-responsive in comparison to those of infants not-exposed. In addition, certain biomarkers, which levels were significantly modified depending on the PME category, were independent predictors of either malaria risk (GM-CSF TLR7/8 crude) or protection (IL-12 TLR7/8 ratio and IP-10 TLR3 crude, IL-1RA TLR7/8 ratio) during the first year of life. Conclusions These findings indicate that past placental malaria has a profound effect on fetal immune system and that the differential alterations of innate immune responses by PME categories might drive heterogeneity between individuals to clinical malaria susceptibility during the first year of life.http://link.springer.com/article/10.1186/s12916-018-1187-3Malaria in pregnancyPrenatal malaria exposureInnate immunityCytokinesToll-like receptorMalaria in infancy |
| spellingShingle | Hamtandi Magloire Natama Gemma Moncunill Eduard Rovira-Vallbona Héctor Sanz Hermann Sorgho Ruth Aguilar Maminata Coulibaly-Traoré M. Athanase Somé Susana Scott Innocent Valéa Petra F. Mens Henk D. F. H. Schallig Luc Kestens Halidou Tinto Carlota Dobaño Anna Rosanas-Urgell Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life BMC Medicine Malaria in pregnancy Prenatal malaria exposure Innate immunity Cytokines Toll-like receptor Malaria in infancy |
| title | Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life |
| title_full | Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life |
| title_fullStr | Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life |
| title_full_unstemmed | Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life |
| title_short | Modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life |
| title_sort | modulation of innate immune responses at birth by prenatal malaria exposure and association with malaria risk during the first year of life |
| topic | Malaria in pregnancy Prenatal malaria exposure Innate immunity Cytokines Toll-like receptor Malaria in infancy |
| url | http://link.springer.com/article/10.1186/s12916-018-1187-3 |
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