IgM antibody responses against Plasmodium antigens in neotropical primates in the Brazilian Atlantic Forest

Front Cell Infect Microbiol. 2023 Sep 27:13:1169552. doi: 10.3389/fcimb.2023.1169552. eCollection 2023.

Abstract

Introduction: Zoonotic transmission is a challenge for the control and elimination of malaria. It has been recorded in the Atlantic Forest, outside the Amazon which is the endemic region in Brazil. However, only very few studies have assessed the antibody response, especially of IgM antibodies, in Neotropical primates (NP). Therefore, in order to contribute to a better understanding of the immune response in different hosts and facilitate the identification of potential reservoirs, in this study, naturally acquired IgM antibody responses against Plasmodium antigens were evaluated, for the first time, in NP from the Atlantic Forest.

Methods: The study was carried out using 154 NP samples from three different areas of the Atlantic Forest. IgM antibodies against peptides of the circumsporozoite protein (CSP) from different Plasmodium species and different erythrocytic stage antigens were detected by ELISA.

Results: Fifty-nine percent of NP had IgM antibodies against at least one CSP peptide and 87% against at least one Plasmodium vivax erythrocytic stage antigen. Levels of antibodies against PvAMA-1 were the highest compared to the other antigens. All families of NP showed IgM antibodies against CSP peptides, and, most strikingly, against erythrocytic stage antigens. Generalized linear models demonstrated that IgM positivity against PvCSP and PvAMA-1 was associated with PCR-detectable blood-stage malaria infection and the host being free-living. Interestingly, animals with IgM against both PvCSP and PvAMA-1 were 4.7 times more likely to be PCR positive than animals that did not have IgM for these two antigens simultaneously.

Discussion: IgM antibodies against different Plasmodium spp. antigens are present in NP from the Atlantic Forest. High seroprevalence and antibody levels against blood-stage antigens were observed, which had a significant association with molecular evidence of infection. IgM antibodies against CSP and AMA-1 may be used as a potential marker for the identification of NP infected with Plasmodium, which are reservoirs of malaria in the Brazilian Atlantic Forest.

Keywords: Atlantic forest; IgM antibodies; Plasmodium; erythrocytic stage antigens; malaria; neotropical primates; pre-erythrocytic stage antigen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Protozoan
  • Antibody Formation
  • Antigens, Protozoan
  • Brazil / epidemiology
  • Forests
  • Immunoglobulin M
  • Malaria* / veterinary
  • Peptides
  • Plasmodium vivax
  • Plasmodium*
  • Primates
  • Protozoan Proteins
  • Seroepidemiologic Studies

Substances

  • Protozoan Proteins
  • Immunoglobulin M
  • Antigens, Protozoan
  • Antibodies, Protozoan
  • Peptides

Grants and funding

This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológia (CNPq - Grant nos. 457274/2014-0, 310477/2017-4), Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG – Grant no. CBB-APQ-02620-15), Fiocruz Inova Grant for innovative products (VPPIS-004-FIO-18-16), and the Secretary for Health Surveillance of the Brazilian Ministry of Health (IOC-017-FIO-17 and IOC-028-FIO-18). This study was partially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001. GA was supported by a scholarship from CAPES. CB, LC, CD-R, TS, and IS are supported by a Productivity in Research fellowship from CNPq. CD-R is also supported by Faperj as a “Cientistas do nosso Estado”.