Frontiers in Cellular and Infection Microbiology (Apr 2022)
Anti-Gametocyte Antigen Humoral Immunity and Gametocytemia During Treatment of Uncomplicated Falciparum Malaria: A Multi-National Study
- Katherine O’Flaherty,
- Jo-Anne Chan,
- Jo-Anne Chan,
- Jo-Anne Chan,
- Julia C. Cutts,
- Julia C. Cutts,
- Sophie G. Zaloumis,
- Elizabeth A. Ashley,
- Elizabeth A. Ashley,
- Aung Pyae Phyo,
- Damien R. Drew,
- Arjen M. Dondorp,
- Arjen M. Dondorp,
- Nicholas P. Day,
- Nicholas P. Day,
- Mehul Dhorda,
- Mehul Dhorda,
- Mehul Dhorda,
- Rick M. Fairhurst,
- Pharath Lim,
- Chanaki Amaratunga,
- Sasithon Pukrittayakamee,
- Tran Tinh Hien,
- Tran Tinh Hien,
- Ye Htut,
- Mayfong Mayxay,
- Mayfong Mayxay,
- Mayfong Mayxay,
- M. Abul Faiz,
- Olugbenga A. Mokuolu,
- Marie A. Onyamboko,
- Caterina Fanello,
- Caterina Fanello,
- Caterina Fanello,
- Eizo Takashima,
- Takafumi Tsuboi,
- Michael Theisen,
- Michael Theisen,
- Francois Nosten,
- Francois Nosten,
- Francois Nosten,
- James G. Beeson,
- James G. Beeson,
- James G. Beeson,
- James G. Beeson,
- Julie A. Simpson,
- Nicholas J. White,
- Nicholas J. White,
- Freya J. I. Fowkes,
- Freya J. I. Fowkes,
- Freya J. I. Fowkes
Affiliations
- Katherine O’Flaherty
- Life Sciences, Burnet Institute, Melbourne, VIC, Australia
- Jo-Anne Chan
- Life Sciences, Burnet Institute, Melbourne, VIC, Australia
- Jo-Anne Chan
- Department of Medicine, The University of Melbourne, Melbourne, VIC, Australia
- Jo-Anne Chan
- Department of Immunology, Monash University, Melbourne, VIC, Australia
- Julia C. Cutts
- Life Sciences, Burnet Institute, Melbourne, VIC, Australia
- Julia C. Cutts
- Department of Medicine, The University of Melbourne, Melbourne, VIC, Australia
- Sophie G. Zaloumis
- Centre for Epidemiology and Biostatistics, School of Population and Global Health, The University of Melbourne, Melbourne, VIC, Australia
- Elizabeth A. Ashley
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Elizabeth A. Ashley
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Aung Pyae Phyo
- Myanmar Oxford Clinical Research Unit, Yangon, Myanmar
- Damien R. Drew
- Life Sciences, Burnet Institute, Melbourne, VIC, Australia
- Arjen M. Dondorp
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Arjen M. Dondorp
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Nicholas P. Day
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Nicholas P. Day
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Mehul Dhorda
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Mehul Dhorda
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Mehul Dhorda
- WorldWide Antimalarial Resistance Network, Asia-Pacific Regional Centre, Bangkok, Thailand
- Rick M. Fairhurst
- Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Pharath Lim
- Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Chanaki Amaratunga
- Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United States
- Sasithon Pukrittayakamee
- 0Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Tran Tinh Hien
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Tran Tinh Hien
- 1Oxford University Clinical Research Unit, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam
- Ye Htut
- 2Department of Medical Research, Ministry of Health and Sports, Yangon, Myanmar
- Mayfong Mayxay
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Mayfong Mayxay
- 3Lao-Oxford-Mahosot Hospital-Wellcome Trust-Research Unit, Mahosot Hospital, Vientiane, Laos
- Mayfong Mayxay
- 4Institute of Research and Education Development, University of Health Sciences, Vientiane, Laos
- M. Abul Faiz
- 5Malaria Research Group and Dev Care Foundation, Chittagong, Bangladesh
- Olugbenga A. Mokuolu
- 6Department of Paediatrics and Child Health, University of Ilorin, Ilorin, Nigeria
- Marie A. Onyamboko
- 7Kinshasa School of Public Health, University of Kinshasa, Kinshasa, Democratic Republic of Congo
- Caterina Fanello
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Caterina Fanello
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Caterina Fanello
- 7Kinshasa School of Public Health, University of Kinshasa, Kinshasa, Democratic Republic of Congo
- Eizo Takashima
- 8Division of Malaria Research, Proteo-Science Center, Ehime University, Matsuyama, Japan
- Takafumi Tsuboi
- 8Division of Malaria Research, Proteo-Science Center, Ehime University, Matsuyama, Japan
- Michael Theisen
- 9Department for Congenital Disorders, Statens Serum Institut, Copenhagen, Denmark
- Michael Theisen
- 0Centre for Medical Parasitology at Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
- Francois Nosten
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Francois Nosten
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Francois Nosten
- 1Shoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand
- James G. Beeson
- Life Sciences, Burnet Institute, Melbourne, VIC, Australia
- James G. Beeson
- Department of Medicine, The University of Melbourne, Melbourne, VIC, Australia
- James G. Beeson
- Department of Immunology, Monash University, Melbourne, VIC, Australia
- James G. Beeson
- 2Department of Microbiology and Central Clinical School, Monash University, Melbourne, VIC, Australia
- Julie A. Simpson
- Centre for Epidemiology and Biostatistics, School of Population and Global Health, The University of Melbourne, Melbourne, VIC, Australia
- Nicholas J. White
- Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
- Nicholas J. White
- Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
- Freya J. I. Fowkes
- Life Sciences, Burnet Institute, Melbourne, VIC, Australia
- Freya J. I. Fowkes
- Centre for Epidemiology and Biostatistics, School of Population and Global Health, The University of Melbourne, Melbourne, VIC, Australia
- Freya J. I. Fowkes
- 3Department of Infectious Diseases and Department of Epidemiology and Preventative Medicine, Monash University, Melbourne, VIC, Australia
- DOI
- https://doi.org/10.3389/fcimb.2022.804470
- Journal volume & issue
-
Vol. 12
Abstract
IntroductionUnderstanding the human immune response to Plasmodium falciparum gametocytes and its association with gametocytemia is essential for understanding the transmission of malaria as well as progressing transmission blocking vaccine candidates.MethodsIn a multi-national clinical efficacy trial of artemisinin therapies (13 sites of varying transmission over South-East Asia and Africa), we measured Immunoglobulin G (IgG) responses to recombinant P. falciparum gametocyte antigens expressed on the gametocyte plasma membrane and leading transmission blocking vaccine candidates Pfs230 (Pfs230c and Pfs230D1M) and Pfs48/45 at enrolment in 1,114 participants with clinical falciparum malaria. Mixed effects linear and logistic regression were used to determine the association between gametocyte measures (gametocytemia and gametocyte density) and antibody outcomes at enrolment.ResultsMicroscopy detectable gametocytemia was observed in 11% (127/1,114) of participants at enrolment, and an additional 9% (95/1,114) over the follow-up period (up to day 42) (total 20% of participants [222/1,114]). IgG levels in response to Pfs230c, Pfs48/45 and Pfs230D1M varied across study sites at enrolment (p < 0.001), as did IgG seroprevalence for anti-Pfs230c and D1M IgG (p < 0.001), but not for anti-Pfs48/45 IgG (p = 0.159). In adjusted analyses, microscopy detectable gametocytemia at enrolment was associated with an increase in the odds of IgG seropositivity to the three gametocyte antigens (Pfs230c OR [95% CI], p: 1.70 [1.10, 2.62], 0.017; Pfs48/45: 1.45 [0.85, 2.46], 0.174; Pfs230D1M: 1.70 [1.03, 2.80], 0.037), as was higher gametocyte density at enrolment (per two-fold change in gametocyte density Pfs230c OR [95% CI], p: 1.09 [1.02, 1.17], 0.008; Pfs48/45: 1.05 [0.98, 1.13], 0.185; Pfs230D1M: 1.07 [0.99, 1.14], 0.071).ConclusionPfs230 and Pfs48/45 antibodies are naturally immunogenic targets associated with patent gametocytemia and increasing gametocyte density across multiple malaria endemic settings, including regions with emerging artemisinin-resistant P. falciparum.
Keywords