Contribution of Functional Antimalarial Immunity to Measures of Parasite Clearance in Therapeutic Efficacy Studies of Artemisinin Derivatives.


Journal

The Journal of infectious diseases
ISSN: 1537-6613
Titre abrégé: J Infect Dis
Pays: United States
ID NLM: 0413675

Informations de publication

Date de publication:
30 08 2019
Historique:
received: 21 02 2019
accepted: 09 05 2019
pubmed: 11 5 2019
medline: 28 5 2020
entrez: 11 5 2019
Statut: ppublish

Résumé

Antibodies to the blood stages of malaria parasites enhance parasite clearance and antimalarial efficacy. The antibody subclass and functions that contribute to parasite clearance during antimalarial treatment and their relationship to malaria transmission intensity have not been characterized. Levels of immunoglobulin G (IgG) subclasses and C1q fixation in response to Plasmodium falciparum merozoite antigens (erythrocyte-binding antigen [EBA] 175RIII-V, merozoite surface protein 2 [MSP-2], and MSP-142) and opsonic phagocytosis of merozoites were measured in a multinational trial assessing the efficacy of artesunate therapy across 11 Southeast Asian sites. Regression analyses assessed the effects of antibody seropositivity on the parasite clearance half-life (PC½), having a PC½ of ≥5 hours, and having parasitemia 3 days after treatment. IgG3, followed by IgG1, was the predominant IgG subclass detected (seroprevalence range, 5%-35% for IgG1 and 27%-41% for IgG3), varied across study sites, and was lowest in study sites with the lowest transmission intensity and slowest mean PC½. IgG3, C1q fixation, and opsonic-phagocytosis seropositivity were associated with a faster PC½ (range of the mean reduction in PC½, 0.47-1.16 hours; P range, .001-.03) and a reduced odds of having a PC½ of ≥5 hours and having parasitemia 3 days after treatment. The prevalence of IgG3, complement-fixing antibodies, and merozoite phagocytosis vary according to transmission intensity, are associated with faster parasite clearance, and may be sensitive surrogates of an augmented clearance capacity of infected erythrocytes. Determining the functional immune mechanisms associated with parasite clearance will improve characterization of artemisinin resistance.

Sections du résumé

BACKGROUND
Antibodies to the blood stages of malaria parasites enhance parasite clearance and antimalarial efficacy. The antibody subclass and functions that contribute to parasite clearance during antimalarial treatment and their relationship to malaria transmission intensity have not been characterized.
METHODS
Levels of immunoglobulin G (IgG) subclasses and C1q fixation in response to Plasmodium falciparum merozoite antigens (erythrocyte-binding antigen [EBA] 175RIII-V, merozoite surface protein 2 [MSP-2], and MSP-142) and opsonic phagocytosis of merozoites were measured in a multinational trial assessing the efficacy of artesunate therapy across 11 Southeast Asian sites. Regression analyses assessed the effects of antibody seropositivity on the parasite clearance half-life (PC½), having a PC½ of ≥5 hours, and having parasitemia 3 days after treatment.
RESULTS
IgG3, followed by IgG1, was the predominant IgG subclass detected (seroprevalence range, 5%-35% for IgG1 and 27%-41% for IgG3), varied across study sites, and was lowest in study sites with the lowest transmission intensity and slowest mean PC½. IgG3, C1q fixation, and opsonic-phagocytosis seropositivity were associated with a faster PC½ (range of the mean reduction in PC½, 0.47-1.16 hours; P range, .001-.03) and a reduced odds of having a PC½ of ≥5 hours and having parasitemia 3 days after treatment.
CONCLUSIONS
The prevalence of IgG3, complement-fixing antibodies, and merozoite phagocytosis vary according to transmission intensity, are associated with faster parasite clearance, and may be sensitive surrogates of an augmented clearance capacity of infected erythrocytes. Determining the functional immune mechanisms associated with parasite clearance will improve characterization of artemisinin resistance.

Identifiants

pubmed: 31075171
pii: 5487931
doi: 10.1093/infdis/jiz247
pmc: PMC6735958
doi:

Substances chimiques

Antibodies, Protozoan 0
Antigens, Protozoan 0
Antimalarials 0
Immunoglobulin G 0
Protozoan Proteins 0
Artesunate 60W3249T9M

Types de publication

Journal Article Multicenter Study Randomized Controlled Trial Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1178-1187

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press for the Infectious Diseases Society of America.

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Auteurs

Katherine O'Flaherty (K)

Burnet Institute, Melbourne, Australia.
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Melbourne, Australia.

Ricardo Ataíde (R)

Burnet Institute, Melbourne, Australia.
Department of Immunology, Monash University, Melbourne, Australia.

Sophie G Zaloumis (SG)

Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Melbourne, Australia.

Elizabeth A Ashley (EA)

Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok.
Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.

Rosanna Powell (R)

Burnet Institute, Melbourne, Australia.

Gaoqian Feng (G)

Burnet Institute, Melbourne, Australia.
Department of Medicine, University of Melbourne, Melbourne, Australia.

Linda Reiling (L)

Burnet Institute, Melbourne, Australia.

Arjen M Dondorp (AM)

Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok.
Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.

Nicholas P Day (NP)

Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok.
Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.

Mehul Dhorda (M)

Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok.
Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.
Worldwide Antimalarial Resistance Network, University of Oxford, United Kingdom.
Howard Hughes Medical Institute, Chevy Chase, Baltimore.
Center for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore.

Rick M Fairhurst (RM)

Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.

Pharath Lim (P)

Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.

Chanaki Amaratunga (C)

Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland.

Sasithon Pukrittayakamee (S)

Faculty of Tropical Medicine, Mahidol University, Bangkok.

Tran Tinh Hien (TT)

Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.
Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam.

Ye Htut (Y)

Department of Medical Research, Yangon, Myanmar.

Mayfong Mayxay (M)

Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.
Lao-Oxford-Mahosot Hospital Wellcome Trust Research Unit, Mahosot Hospital, Lao People's Democratic Republic.
Faculty of Postgraduate Studies, University of Health Sciences, Vientiane, Lao People's Democratic Republic.

M Abul Faiz (MA)

Malaria Research Group, Chittagong, Bangladesh.
Dev Care Foundation, Chittagong, Bangladesh.

James G Beeson (JG)

Burnet Institute, Melbourne, Australia.
Department of Microbiology, Monash University, Melbourne, Australia.
Central Clinical School, Monash University, Melbourne, Australia.

Francois Nosten (F)

Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok.
Shoklo Malaria Research Unit, Mae Sot, Thailand.

Julie A Simpson (JA)

Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Melbourne, Australia.

Nicholas J White (NJ)

Mahidol-Oxford Tropical Medicine Research Unit, Mahidol University, Bangkok.
Centre for Tropical Medicine and Global Health, University of Oxford, United Kingdom.

Freya J I Fowkes (FJI)

Burnet Institute, Melbourne, Australia.
Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Melbourne, Australia.
Department of Infectious Diseases, Monash University, Melbourne, Australia.
Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Australia.

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