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Published in: BMC Infectious Diseases 1/2020

Open Access 01-12-2020 | Yersinia Pestis | Technical advance

Short- and long-term humoral immune response against Yersinia pestis in plague patients, Madagascar

Authors: Voahangy Andrianaivoarimanana, Alice Lantoniaina Iharisoa, Lila Rahalison, Marie Laurette Ralimanantsoa, Maherisoa Ratsitorahina, Rado J. L. Rakotonanahary, Elisabeth Carniel, Christian Demeure, Minoarisoa Rajerison

Published in: BMC Infectious Diseases | Issue 1/2020

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Abstract

Background

Plague, a fatal disease caused by the bacillus, Yersinia pestis, still affects resources-limited countries. Information on antibody response to plague infection in human is scarce. Anti-F1 Ig G are among the known protective antibodies against Y. pestis infection. As a vaccine preventable disease, knowledge on antibody response is valuable for the development of an effective vaccine to reduce infection rate among exposed population in plague-endemic regions. In this study, we aim to describe short and long-term humoral immune responses against Y. pestis in plague-confirmed patients from Madagascar, the most affected country in the world.

Methods

Bubonic (BP) and pneumonic plague (PP) patients were recruited from plague- endemic foci in the central highlands of Madagascar between 2005 and 2017. For short-term follow-up, 6 suspected patients were enrolled and prospectively investigated for kinetics of the anti-F1 IgG response, whereas the persistence of antibodies was retrospectively studied in 71 confirmed convalescent patients, using an ELISA which was validated for the detection of plague in human blood samples in Madagascar.

Results

Similarly to previous findings, anti-F1 IgG rose quickly during the first week after disease onset and increased up to day 30. In the long-term study, 56% of confirmed cases remained seropositive, amongst which 60 and 40% could be considered as high- and low-antibody responders, respectively. Antibodies persisted for several years and up to 14.8 years for one individual. Antibody titers decreased over time but there was no correlation between titer and time elapsed between the disease onset and serum sampling. In addition, the seroprevalence rate was not significantly different between gender (P = 0.65) nor age (P = 0.096).

Conclusion

Our study highlighted that the circulating antibody response to F1 antigen, which is specific to Y. pestis, may be attributable to individual immune responsiveness. The finding that a circulating anti-F1 antibody titer could persist for more than a decade in both BP and PP recovered patients, suggests its probable involvement in patients’ protection. However, complementary studies including analyses of the cellular immune response to Y. pestis are required for the better understanding of long-lasting protection and development of a potential vaccine against plague.
Literature
1.
go back to reference Brygoo ER. Epidemiologie de la peste à Madagascar. Arch Inst Pasteur Madagascar. 1966;35:9–147. Brygoo ER. Epidemiologie de la peste à Madagascar. Arch Inst Pasteur Madagascar. 1966;35:9–147.
2.
go back to reference World Health Organization. Plague around the world. Wkly Epidemiol Rec. 2019;94:289–92. World Health Organization. Plague around the world. Wkly Epidemiol Rec. 2019;94:289–92.
3.
go back to reference Randremanana R, Andrianaivoarimanana V, Nikolay B, Ramasindrazana B, Paireau J, Ten Bosch QA, et al. Epidemiological characteristics of an urban plague epidemic in Madagascar, august-November, 2017: an outbreak report. Lancet Infect Dis. 2019;19(5):537–45.CrossRef Randremanana R, Andrianaivoarimanana V, Nikolay B, Ramasindrazana B, Paireau J, Ten Bosch QA, et al. Epidemiological characteristics of an urban plague epidemic in Madagascar, august-November, 2017: an outbreak report. Lancet Infect Dis. 2019;19(5):537–45.CrossRef
4.
go back to reference Galimand M, Carniel E, Courvalin P. Resistance of Yersinia pestis to antimicrobial agents. Antimicrob Agents Chemother. 2006;50(10):3233–6.CrossRef Galimand M, Carniel E, Courvalin P. Resistance of Yersinia pestis to antimicrobial agents. Antimicrob Agents Chemother. 2006;50(10):3233–6.CrossRef
5.
go back to reference Perry RD, Fetherston JD. Yersinia pestis--etiologic agent of plague. Clin Microbiol Rev. 1997;10(1):35–66.CrossRef Perry RD, Fetherston JD. Yersinia pestis--etiologic agent of plague. Clin Microbiol Rev. 1997;10(1):35–66.CrossRef
6.
go back to reference Du Y, Rosqvist R, Forsberg A. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun. 2002;70(3):1453–60.CrossRef Du Y, Rosqvist R, Forsberg A. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun. 2002;70(3):1453–60.CrossRef
7.
go back to reference Meyer KF. Serological tests for the confirmation of plague infections: a preliminary communication. Bull World Health Organ. 1964;30:750–1.PubMedPubMedCentral Meyer KF. Serological tests for the confirmation of plague infections: a preliminary communication. Bull World Health Organ. 1964;30:750–1.PubMedPubMedCentral
8.
go back to reference Marshall JD Jr, Cavanaugh DC, Bartelloni PJ, Meyer K. F. Plague immunization. III. Serologic response to multiple inoculations of vaccine. J Infect Dis. 1974;129(Suppl):S26–9.CrossRef Marshall JD Jr, Cavanaugh DC, Bartelloni PJ, Meyer K. F. Plague immunization. III. Serologic response to multiple inoculations of vaccine. J Infect Dis. 1974;129(Suppl):S26–9.CrossRef
9.
go back to reference Rasoamanana B, Leroy F, Boisier P, Rasolomaharo M, Buchy P, Carniel E, et al. Field evaluation of an immunoglobulin G anti-F1 enzyme-linked immunosorbent assay for serodiagnosis of human plague in Madagascar. Clin Diagn Lab Immunol. 1997;4(5):587–91.CrossRef Rasoamanana B, Leroy F, Boisier P, Rasolomaharo M, Buchy P, Carniel E, et al. Field evaluation of an immunoglobulin G anti-F1 enzyme-linked immunosorbent assay for serodiagnosis of human plague in Madagascar. Clin Diagn Lab Immunol. 1997;4(5):587–91.CrossRef
10.
go back to reference Williamson ED, Oyston PC. Protecting against plague: towards a next-generation vaccine. Clin Exp Immunol. 2013;172(1):1–8.CrossRef Williamson ED, Oyston PC. Protecting against plague: towards a next-generation vaccine. Clin Exp Immunol. 2013;172(1):1–8.CrossRef
11.
go back to reference Li B, Du C, Zhou L, Bi Y, Wang X, Wen L, et al. Humoral and cellular immune responses to Yersinia pestis infection in long-term recovered plague patients. Clin Vaccine Immunol. 2012;19(2):228–34.CrossRef Li B, Du C, Zhou L, Bi Y, Wang X, Wen L, et al. Humoral and cellular immune responses to Yersinia pestis infection in long-term recovered plague patients. Clin Vaccine Immunol. 2012;19(2):228–34.CrossRef
12.
go back to reference Chanteau S, Rahalison L, Ralafiarisoa L, Foulon J, Ratsitorahina M, Ratsifasoamanana L, et al. Development and testing of a rapid diagnostic test for bubonic and pneumonic plague. Lancet. 2003;361(9353):211–6.CrossRef Chanteau S, Rahalison L, Ralafiarisoa L, Foulon J, Ratsitorahina M, Ratsifasoamanana L, et al. Development and testing of a rapid diagnostic test for bubonic and pneumonic plague. Lancet. 2003;361(9353):211–6.CrossRef
13.
go back to reference Rasoamanana B, Rahalison L, Raharimanana C, Chanteau S. Comparison of Yersinia CIN agar and mouse inoculation assay for the diagnosis of plague. Trans R Soc Trop Med Hyg. 1996;90(6):651.CrossRef Rasoamanana B, Rahalison L, Raharimanana C, Chanteau S. Comparison of Yersinia CIN agar and mouse inoculation assay for the diagnosis of plague. Trans R Soc Trop Med Hyg. 1996;90(6):651.CrossRef
14.
15.
go back to reference World Health Organization. International meeting on preventing and controlling plague: the old calamity still has a future. Wkly Epidemiol Rec. 2006;81:278–84. World Health Organization. International meeting on preventing and controlling plague: the old calamity still has a future. Wkly Epidemiol Rec. 2006;81:278–84.
16.
go back to reference Migliani R, Chanteau S, Rahalison L, Ratsitorahina M, Boutin JP, Ratsifasoamanana L, et al. Epidemiological trends for human plague in Madagascar during the second half of the 20th century: a survey of 20,900 notified cases. Tropical Med Int Health. 2006;11(8):1228–37.CrossRef Migliani R, Chanteau S, Rahalison L, Ratsitorahina M, Boutin JP, Ratsifasoamanana L, et al. Epidemiological trends for human plague in Madagascar during the second half of the 20th century: a survey of 20,900 notified cases. Tropical Med Int Health. 2006;11(8):1228–37.CrossRef
17.
go back to reference Andrianaivoarimanana V, Piola P, Wagner DM, Rakotomanana F, Maheriniaina V, Andrianalimanana S, et al. Trends of human plague, Madagascar, 1998-2016. Emerg Infect Dis. 2019;25(2):220–8.CrossRef Andrianaivoarimanana V, Piola P, Wagner DM, Rakotomanana F, Maheriniaina V, Andrianalimanana S, et al. Trends of human plague, Madagascar, 1998-2016. Emerg Infect Dis. 2019;25(2):220–8.CrossRef
18.
go back to reference Andrianaivoarimanana V, Bertherat E, Rajaonarison R, Rakotondramaro T, Rogier C, Rajerison M. Mixed pneumonic plague and nosocomial MDR-bacterial infection of lung: a rare case report. BMC Pulm Med. 2018;18(1):92.CrossRef Andrianaivoarimanana V, Bertherat E, Rajaonarison R, Rakotondramaro T, Rogier C, Rajerison M. Mixed pneumonic plague and nosocomial MDR-bacterial infection of lung: a rare case report. BMC Pulm Med. 2018;18(1):92.CrossRef
19.
go back to reference Richard V, Riehm JM, Herindrainy P, Soanandrasana R, Ratsitoharina M, Rakotomanana F, et al. Pneumonic plague outbreak, northern Madagascar, 2011. Emerg Infect Dis. 2015;21(1):8–15.CrossRef Richard V, Riehm JM, Herindrainy P, Soanandrasana R, Ratsitoharina M, Rakotomanana F, et al. Pneumonic plague outbreak, northern Madagascar, 2011. Emerg Infect Dis. 2015;21(1):8–15.CrossRef
20.
go back to reference Ramasindrazana B, Andrianaivoarimanana V, Rakotondramanga JM, Birdsell DN, Ratsitorahina M, Rajerison M. Pneumonic plague transmission, Moramanga, Madagascar, 2015. Emerg Infect Dis. 2017;23(3):521–4.CrossRef Ramasindrazana B, Andrianaivoarimanana V, Rakotondramanga JM, Birdsell DN, Ratsitorahina M, Rajerison M. Pneumonic plague transmission, Moramanga, Madagascar, 2015. Emerg Infect Dis. 2017;23(3):521–4.CrossRef
21.
go back to reference Ratsitorahina M, Chanteau S, Rahalison L, Ratsifasoamanana L, Boisier P. Epidemiological and diagnostic aspects of the outbreak of pneumonic plague in Madagascar. Lancet. 2000;355(9198):111–3.CrossRef Ratsitorahina M, Chanteau S, Rahalison L, Ratsifasoamanana L, Boisier P. Epidemiological and diagnostic aspects of the outbreak of pneumonic plague in Madagascar. Lancet. 2000;355(9198):111–3.CrossRef
22.
go back to reference Bertherat E, Thullier P, Shako JC, England K, Koné ML, Arntzen L, et al. Lessons learned about pneumonic plague diagnosis from two outbreaks, Democratic Republic of the Congo. Emerg Infect Dis. 2011;17(5):778–84.CrossRef Bertherat E, Thullier P, Shako JC, England K, Koné ML, Arntzen L, et al. Lessons learned about pneumonic plague diagnosis from two outbreaks, Democratic Republic of the Congo. Emerg Infect Dis. 2011;17(5):778–84.CrossRef
Metadata
Title
Short- and long-term humoral immune response against Yersinia pestis in plague patients, Madagascar
Authors
Voahangy Andrianaivoarimanana
Alice Lantoniaina Iharisoa
Lila Rahalison
Marie Laurette Ralimanantsoa
Maherisoa Ratsitorahina
Rado J. L. Rakotonanahary
Elisabeth Carniel
Christian Demeure
Minoarisoa Rajerison
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2020
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-020-05565-8

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