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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Research

Hospital-derived antibody profiles of malaria patients in Southwest India

Authors: Apoorva Venkatesh, Aarti Jain, Huw Davies, Ligia Periera, Jennifer N. Maki, Edwin Gomes, Philip L. Felgner, Sanjeeva Srivastava, Swati Patankar, Pradipsinh K. Rathod

Published in: Malaria Journal | Issue 1/2019

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Abstract

Background

Naturally acquired immunity to malaria across the globe varies in intensity and protective powers. Many of the studies on immunity are from hyperendemic regions of Africa. In Asia, particularly in India, there are unique opportunities for exploring and understanding malaria immunity relative to host age, co-occurrence of Plasmodium falciparum and Plasmodium vivax infections, varying travel history, and varying disease severity. Variation in immunity in hospital settings is particularly understudied.

Methods

A US NIH ICEMR (South Asia) team examined the level of immunity in an Indian malaria patient population visiting or admitted to Goa Medical College and Hospital in Goa, India. Sera from 200 patients of different ages, in different seasons, infected with P. falciparum or P. vivax or both species, and with different clinical severity were applied to an established protein array system with over 1000 P. falciparum and P. vivax antigens. Differential binding of patient IgG to different antigens was measured.

Results

Even though Goa itself has much more P. vivax than P. falciparum, IgG reactivity towards P. falciparum antigens was very strong and comparable to that seen in regions of the world with high P. falciparum endemicity. Of 248 seropositive P. falciparum antigens, the strongest were VAR, MSP10, HSP70, PTP5, AP2, AMA1, and SYN6. In P. vivax patients, ETRAMPs, MSPs, and ApiAP2, sexual stage antigen s16, RON3 were the strongest IgG binders. Both P. falciparum and P. vivax patients also revealed strong binding to new antigens with unknown functions. Seropositives showed antigens unique to the young (HSP40, ACS6, GCVH) or to non-severe malaria (MSP3.8 and PHIST).

Conclusion

Seroreactivity at a major hospital in Southwest India reveals antibody responses to P. falciparum and P. vivax in a low malaria transmission region with much migration. In addition to markers of transmission, the data points to specific leads for possible protective immunity against severe disease. Several, but not all, key antigens overlap with work from different settings around the globe and from other parts of India. Together, these studies confidently help define antigens with the greatest potential chance of universal application for surveillance and possibly for disease protection, in many different parts of India and the world.
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Literature
2.
go back to reference Das MK, Prajapati BK, Tiendrebeogo RW, Ranjan K, Adu B, Srivastava A, et al. Malaria epidemiology in an area of stable transmission in tribal population of Jharkhand, India. Malar J. 2017;16:181.CrossRef Das MK, Prajapati BK, Tiendrebeogo RW, Ranjan K, Adu B, Srivastava A, et al. Malaria epidemiology in an area of stable transmission in tribal population of Jharkhand, India. Malar J. 2017;16:181.CrossRef
3.
go back to reference Mannan BA, Patel K, Malhotra I, Ravindran B, Sharma S. How specific is the immune response to malaria in adults living in endemic areas? J Vector Borne Dis. 2003;40:84–91.PubMed Mannan BA, Patel K, Malhotra I, Ravindran B, Sharma S. How specific is the immune response to malaria in adults living in endemic areas? J Vector Borne Dis. 2003;40:84–91.PubMed
4.
go back to reference Sharma SK, Chattopadhyay R, Chakrabarti K, Pati SS, Srivastava VK, Tyagi PK, et al. Epidemiology of malaria transmission and development of natural immunity in a malaria-endemic village, San Dulakudar, in Orissa state, India. Am J Trop Med Hyg. 2004;71:457–65.CrossRef Sharma SK, Chattopadhyay R, Chakrabarti K, Pati SS, Srivastava VK, Tyagi PK, et al. Epidemiology of malaria transmission and development of natural immunity in a malaria-endemic village, San Dulakudar, in Orissa state, India. Am J Trop Med Hyg. 2004;71:457–65.CrossRef
5.
go back to reference Baird JK, Andersen EM, Bangs MJ, Sorensen K, Gunawan S, Marwoto H, et al. Review of studies of naturally acquired immunity to malaria in Irian Jaya. Indonesian Bull Health Res. 1991;19:1–14. Baird JK, Andersen EM, Bangs MJ, Sorensen K, Gunawan S, Marwoto H, et al. Review of studies of naturally acquired immunity to malaria in Irian Jaya. Indonesian Bull Health Res. 1991;19:1–14.
6.
go back to reference Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–7.CrossRef Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–7.CrossRef
7.
go back to reference Muellenbeck MF, Ueberheide B, Amulic B, Epp A, Fenyo D, Busse CE, et al. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. J Exp Med. 2013;210:389–99.CrossRef Muellenbeck MF, Ueberheide B, Amulic B, Epp A, Fenyo D, Busse CE, et al. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. J Exp Med. 2013;210:389–99.CrossRef
8.
go back to reference Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, Chantavanich P, et al. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg. 1991;45:297–308.CrossRef Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, Chantavanich P, et al. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg. 1991;45:297–308.CrossRef
9.
go back to reference Weiss GE, Clark EH, Li S, Traore B, Kayentao K, Ongoiba A, et al. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS ONE. 2011;6:e15983.CrossRef Weiss GE, Clark EH, Li S, Traore B, Kayentao K, Ongoiba A, et al. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS ONE. 2011;6:e15983.CrossRef
10.
go back to reference Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA. 2010;107:6958–63.CrossRef Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, et al. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA. 2010;107:6958–63.CrossRef
11.
go back to reference Doolan DL, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C, et al. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics. 2008;8:4680–94.CrossRef Doolan DL, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C, et al. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics. 2008;8:4680–94.CrossRef
12.
go back to reference Arévalo-Herrera M, Lopez-Perez M, Dotsey E, Jain A, Rubiano K, Felgner PL, et al. Antibody profiling in naïve and semi-immune individuals experimentally challenged with Plasmodium vivax sporozoites. PLoS Negl Trop Dis. 2016;10:e0004563.CrossRef Arévalo-Herrera M, Lopez-Perez M, Dotsey E, Jain A, Rubiano K, Felgner PL, et al. Antibody profiling in naïve and semi-immune individuals experimentally challenged with Plasmodium vivax sporozoites. PLoS Negl Trop Dis. 2016;10:e0004563.CrossRef
13.
go back to reference Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRef Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRef
14.
go back to reference Chen J-H, Chen S-B, Wang Y, Ju C, Zhang T, Xu B, et al. An immunomics approach for the analysis of natural antibody responses to Plasmodium vivax infection. Mol BioSyst. 2015;11:2354–63.CrossRef Chen J-H, Chen S-B, Wang Y, Ju C, Zhang T, Xu B, et al. An immunomics approach for the analysis of natural antibody responses to Plasmodium vivax infection. Mol BioSyst. 2015;11:2354–63.CrossRef
15.
go back to reference Felgner PL, Roestenberg M, Liang L, Hung C, Jain A, Pablo J, et al. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci Rep. 2013;3:3549.CrossRef Felgner PL, Roestenberg M, Liang L, Hung C, Jain A, Pablo J, et al. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci Rep. 2013;3:3549.CrossRef
16.
go back to reference King CL, Davies DH, Felgner P, Baum E, Jain A, Randall A, et al. Biosignatures of exposure/transmission and immunity. Am J Trop Med Hyg. 2015;93(3 Suppl):16–27.CrossRef King CL, Davies DH, Felgner P, Baum E, Jain A, Randall A, et al. Biosignatures of exposure/transmission and immunity. Am J Trop Med Hyg. 2015;93(3 Suppl):16–27.CrossRef
17.
go back to reference Liu EW, Skinner J, Tran TM, Kumar K, Narum DL, Jain A, et al. Protein-specific features associated with variability in human antibody responses to Plasmodium falciparum malaria antigens. Am J Trop Med Hyg. 2018;98:57–66.CrossRef Liu EW, Skinner J, Tran TM, Kumar K, Narum DL, Jain A, et al. Protein-specific features associated with variability in human antibody responses to Plasmodium falciparum malaria antigens. Am J Trop Med Hyg. 2018;98:57–66.CrossRef
18.
go back to reference Stone WJR, Campo JJ, Ouédraogo AL, Meerstein-Kessel L, Morlais I, Da D, et al. Unravelling the immune signature of Plasmodium falciparum transmission-reducing immunity. Nat Commun. 2018;9:558.CrossRef Stone WJR, Campo JJ, Ouédraogo AL, Meerstein-Kessel L, Morlais I, Da D, et al. Unravelling the immune signature of Plasmodium falciparum transmission-reducing immunity. Nat Commun. 2018;9:558.CrossRef
19.
go back to reference Uplekar S, Rao PN, Ramanathapuram L, Awasthi V, Verma K, Sutton P, et al. Characterizing antibody responses to Plasmodium vivax and Plasmodium falciparum antigens in India using genome-scale protein microarrays. PLoS Negl Trop Dis. 2017;11:e0005323.CrossRef Uplekar S, Rao PN, Ramanathapuram L, Awasthi V, Verma K, Sutton P, et al. Characterizing antibody responses to Plasmodium vivax and Plasmodium falciparum antigens in India using genome-scale protein microarrays. PLoS Negl Trop Dis. 2017;11:e0005323.CrossRef
20.
go back to reference Chery L, Maki JN, Mascarenhas A, Walke JT, Gawas P, Almeida A, et al. Demographic and clinical profiles of Plasmodium falciparum and Plasmodium vivax patients at a tertiary care centre in Southwestern India. Malar J. 2016;15:569.CrossRef Chery L, Maki JN, Mascarenhas A, Walke JT, Gawas P, Almeida A, et al. Demographic and clinical profiles of Plasmodium falciparum and Plasmodium vivax patients at a tertiary care centre in Southwestern India. Malar J. 2016;15:569.CrossRef
21.
go back to reference Pathak S, Rege M, Gogtay NJ, Aigal U, Sharma SK, Valecha N, et al. Age-dependent sex bias in clinical malarial disease in hypoendemic regions. PLoS ONE. 2012;7:35592.CrossRef Pathak S, Rege M, Gogtay NJ, Aigal U, Sharma SK, Valecha N, et al. Age-dependent sex bias in clinical malarial disease in hypoendemic regions. PLoS ONE. 2012;7:35592.CrossRef
22.
go back to reference Doolan DL, Dobaño C, Baird JK. Acquired immunity to malaria. Clin Microbiol Rev. 2009;22:13–36.CrossRef Doolan DL, Dobaño C, Baird JK. Acquired immunity to malaria. Clin Microbiol Rev. 2009;22:13–36.CrossRef
23.
go back to reference Ghani AC, Sutherland CJ, Riley EM, Drakeley CJ, Griffin JT, Gosling RD, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS ONE. 2009;4:e4383.CrossRef Ghani AC, Sutherland CJ, Riley EM, Drakeley CJ, Griffin JT, Gosling RD, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS ONE. 2009;4:e4383.CrossRef
24.
go back to reference Aponte JJ, Menendez C, Schellenberg D, Kahigwa E, Mshinda H, Vountasou P, et al. Age interactions in the development of naturally acquired immunity to Plasmodium falciparum and its clinical presentation. PLoS Med. 2007;4:e242.CrossRef Aponte JJ, Menendez C, Schellenberg D, Kahigwa E, Mshinda H, Vountasou P, et al. Age interactions in the development of naturally acquired immunity to Plasmodium falciparum and its clinical presentation. PLoS Med. 2007;4:e242.CrossRef
25.
go back to reference Hay SI, Okiro EA, Gething PW, Patil AP, Tatem AJ, Guerra CA, et al. Estimating the global clinical burden of Plasmodium falciparum malaria in 2007. PLoS Med. 2010;7:e1000290.CrossRef Hay SI, Okiro EA, Gething PW, Patil AP, Tatem AJ, Guerra CA, et al. Estimating the global clinical burden of Plasmodium falciparum malaria in 2007. PLoS Med. 2010;7:e1000290.CrossRef
26.
go back to reference Das A, Anvikar AR, Cator LJ, Dhiman RC, Eapen A, Mishra N, et al. Malaria in India: the center for the study of complex malaria in India. Acta Trop. 2012;121:267–73.CrossRef Das A, Anvikar AR, Cator LJ, Dhiman RC, Eapen A, Mishra N, et al. Malaria in India: the center for the study of complex malaria in India. Acta Trop. 2012;121:267–73.CrossRef
27.
go back to reference Dehal N, Krishan K, Kanchan T, Unnikrishnan B, Singh J. Integrated disease surveillance in India—progress and pitfalls. Perspect Public Health. 2015;135:290.CrossRef Dehal N, Krishan K, Kanchan T, Unnikrishnan B, Singh J. Integrated disease surveillance in India—progress and pitfalls. Perspect Public Health. 2015;135:290.CrossRef
28.
go back to reference Baum E, Badu K, Molina DM, Liang X, Felgner PL, Yan G. Protein microarray analysis of antibody responses to Plasmodium falciparum in western Kenyan highland sites with differing transmission levels. PLoS ONE. 2013;8:e82246.CrossRef Baum E, Badu K, Molina DM, Liang X, Felgner PL, Yan G. Protein microarray analysis of antibody responses to Plasmodium falciparum in western Kenyan highland sites with differing transmission levels. PLoS ONE. 2013;8:e82246.CrossRef
29.
go back to reference Trieu A, Kayala MA, Burk C, Molina DM, Freilich DA, Richie TL, et al. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol Cell Proteomics. 2011;10:M111.007948.CrossRef Trieu A, Kayala MA, Burk C, Molina DM, Freilich DA, Richie TL, et al. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol Cell Proteomics. 2011;10:M111.007948.CrossRef
30.
go back to reference Lobo CA, Kar SK, Ravindran B, Kabilan L, Sharma S. Novel proteins of Plasmodium falciparum identified by differential immunoscreening using immune and patient sera. Infect Immun. 1994;62:651–6.PubMedPubMedCentral Lobo CA, Kar SK, Ravindran B, Kabilan L, Sharma S. Novel proteins of Plasmodium falciparum identified by differential immunoscreening using immune and patient sera. Infect Immun. 1994;62:651–6.PubMedPubMedCentral
31.
go back to reference Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, et al. Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008;7:195.CrossRef Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, et al. Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008;7:195.CrossRef
Metadata
Title
Hospital-derived antibody profiles of malaria patients in Southwest India
Authors
Apoorva Venkatesh
Aarti Jain
Huw Davies
Ligia Periera
Jennifer N. Maki
Edwin Gomes
Philip L. Felgner
Sanjeeva Srivastava
Swati Patankar
Pradipsinh K. Rathod
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2771-5

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