Plasmodium vivax malaria serological exposure markers: Assessing the degree and implications of cross-reactivity with P. knowlesi

Rhea J Longley, Matthew J Grigg, Kael Schoffer, Thomas Obadia, Stephanie Hyslop, Kim A Piera, Narimane Nekkab, Ramin Mazhari, Eizo Takashima, Takafumi Tsuboi, Matthias Harbers, Kevin Tetteh, Chris Drakeley, Chetan E Chitnis, Julie Healer, Wai-Hong Tham, Jetsumon Sattabongkot, Michael T White, Daniel J Cooper, Giri S Rajahram, Bridget E Barber, Timothy William, Nicholas M Anstey, Ivo Mueller, Rhea J Longley, Matthew J Grigg, Kael Schoffer, Thomas Obadia, Stephanie Hyslop, Kim A Piera, Narimane Nekkab, Ramin Mazhari, Eizo Takashima, Takafumi Tsuboi, Matthias Harbers, Kevin Tetteh, Chris Drakeley, Chetan E Chitnis, Julie Healer, Wai-Hong Tham, Jetsumon Sattabongkot, Michael T White, Daniel J Cooper, Giri S Rajahram, Bridget E Barber, Timothy William, Nicholas M Anstey, Ivo Mueller

Abstract

Serological markers are a promising tool for surveillance and targeted interventions for Plasmodium vivax malaria. P. vivax is closely related to the zoonotic parasite P. knowlesi, which also infects humans. P. vivax and P. knowlesi are co-endemic across much of South East Asia, making it important to design serological markers that minimize cross-reactivity in this region. To determine the degree of IgG cross-reactivity against a panel of P. vivax serological markers, we assayed samples from human patients with P. knowlesi malaria. IgG antibody reactivity is high against P. vivax proteins with high sequence identity with their P. knowlesi ortholog. IgG reactivity peaks at 7 days post-P. knowlesi infection and is short-lived, with minimal responses 1 year post-infection. We designed a panel of eight P. vivax proteins with low levels of cross-reactivity with P. knowlesi. This panel can accurately classify recent P. vivax infections while reducing misclassification of recent P. knowlesi infections.

Trial registration: ClinicalTrials.gov NCT01708876 NCT03056391.

Keywords: Plasmodium knowlesi; Plasmodium vivax; antibodies; antibody cross-reactivity; malaria; malaria elimination; serological exposure markers; serosurveillance; species cross-reactivity.

Conflict of interest statement

Declaration of interests R.L., M.W., T.T., and and I.M. are inventors on filed patent PCT/US17/67926 on a system, method, apparatus, and diagnostic test for P. vivax. M.H. was an employee of the company CellFree Sciences Co., Ltd.

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Figures

Graphical abstract
Graphical abstract
Figure 1
Figure 1
IgG antibody levels against 21 P. vivax proteins in patients with clinical P. knowlesi infections IgG levels were measured against the 21 P. vivax proteins using a multiplexed antibody assay. Individual patients (n = 99) had longitudinal samples obtained and run at the time of diagnosis of P. knowlesi infection (day 0), and days 7 and 28 following enrollment (ACTKNOW cohort). Day 0 has data from 98 samples. Results are expressed as relative antibody units (RAU). All samples were run in singlicate. Proteins are ordered by highest level of median IgG at day 7 compared with the seropositivity cut-off. Dashed lines indicate the malaria-naive negative-control samples (n = 369, MSP3b n = 213): orange, average of the negative control samples; blue, seropositivity cut-off (average plus 2× standard deviation). The box plots indicate the median, 25th, and 75th percentiles with the whiskers showing the 2.5 and 97.5 percentiles. Dots are outliers.
Figure 2
Figure 2
IgG antibody levels against 21 P. vivax proteins in patients up to 1 year post-clinical P. knowlesi infections IgG levels were measured against the 21 P. vivax proteins using a multiplexed antibody assay. Samples were obtained and run at the time of P. knowlesi infection (day 0) (n = 41), days 4–9 (n = 35), days 10–15 (n = 15), days 27–30 (n = 33), and days 339–444 (n = 42) following enrollment (PACKNOW cohort). Results are expressed as RAU. All samples were run in singlicate. Proteins are ordered as per Figure 1. Dashed lines indicate the malaria-naive negative-control samples (n = 369, MSP3b n = 213): orange, average of the negative control samples; blue, seropositivity cut-off (average plus 2× standard deviation). The box plots indicate the median, 25th and 75th percentiles with the whiskers showing the 2.5 and 97.5 percentiles. Dots are outliers.
Figure 3
Figure 3
Correlation between the peak anti-P. vivax IgG level at day 7 and the percent sequence identity of the P. vivax and P. knowlesi orthologs (A–C) The median IgG level at day 7 (the peak of the response) was divided by the seropositivity cut-off to generate the fold change at the peak compared with the background. The percentage sequence identity was calculated for the protein construct sequence using NCBI BlastP, or the PlasmoDB method when required (see Table 1). A Spearman’s correlation was performed to determine the relationship of the fold change with the sequence identity using data from all 21 P. vivax proteins, for the (A) ACTKNOW r = 0.63, p = 0.0023, (B) PACKNOW cohorts r = 0.56, p = 0.0083, and (C) ACTKNOW and PACKNOW combined (median antibody level of n = 134 P. knowlesi patients at day 7 divided by the seropositivity cut-off) r = 0.69, p = 0.0006.

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