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Published in: Malaria Journal 1/2023

Open Access 01-12-2023 | Plasmodium Ovale | Research

Analysis of the relapse of imported Plasmodium vivax and Plasmodium ovale in five provinces of China

Authors: Hui Yan, Shujiao Wei, Yuan Sui, Shenning Lu, Weiwei Zhang, Xiangyang Feng, Ying Liu, Tao Zhang, Wei Ruan, Jing Xia, Wen Lin, Benedikt Ley, Sarah Auburn, Shizhu Li, Jun Li, Duoquan Wang

Published in: Malaria Journal | Issue 1/2023

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Abstract

Background

The global battle against malaria is facing formidable challenges, particularly in controlling Plasmodium vivax and Plasmodium ovale, whose cases have not been reduced as effectively as Plasmodium falciparum because of their relapse. This study investigates the current situation and underlying factors contributing to relapse or recrudescence of imported cases of P. vivax and P. ovale, and seeks to provide a reference for reducing relapse or recrudescence in malaria-free areas and offers a scientific basis for designing strategies to prevent imported re-transmission.

Methods

This study analysed imported P. vivax and P. ovale in Anhui, Zhejiang, Henan, Hubei, and Guangxi provinces during 2014–2021 by retrospective analysis. A case–control study was conducted on patients who experienced relapse or recrudescence.

Results

From 2014 to 2021, 306 cases of P.vivax and 896 cases of P.ovale were included in the study, while 75 cases had relapse or recrudescence, including 49 cases of P. ovale (65.33%) and 26 cases of P. vivax (34.67%). Within less than 5 weeks after returning to the country, 122 cases of P. vivax (39.87%, 122/306) and 265 cases of P. ovale (29.58%, 265/896) occurred. Within less than 53 weeks, the ratio of P. vivax was 94.77% (290/306), and that of P. ovale was 89.96% (806/896). Among the cases experiencing relapse or recrudescence, only 1 case of P. vivax (1/26 3.85%) and 3 cases of P. ovale (3/49 6.12%) occurred within less than 5 weeks after the first onset, whereas 21 cases of P. vivax (21/26 80.77%) and 42 cases of P. ovale (42/49 85.71%) occurred within less than 53 weeks after the first onset. The difference in relapse or recrudescence due to different drugs and medication regimens and medical activities at various levels of medical institutions was statistically significant.

Conclusion

In areas where malaria has been eliminated, routine health screening in a scientific time frame for people returning from at-risk areas can effectively improve the efficiency of preventing re-transmission, thereby reducing prevention costs and disease burden. Preventing patients from self-treating and strengthening medication regulations in health facilities are key measures to reduce relapse or recrudescence.
Literature
1.
go back to reference WHO. World malaria report 2021. Geneva: World Health Organization; 2021. WHO. World malaria report 2021. Geneva: World Health Organization; 2021.
2.
go back to reference Yman V, Wandell G, Mutemi DD, Miglar A, Asghar M, Hammar U, et al. Persistent transmission of Plasmodium malariae and Plasmodium ovale species in an area of declining Plasmodium falciparum transmission in eastern Tanzania. PLoS Negl Trop Dis. 2019;13: e0007414.PubMedPubMedCentralCrossRef Yman V, Wandell G, Mutemi DD, Miglar A, Asghar M, Hammar U, et al. Persistent transmission of Plasmodium malariae and Plasmodium ovale species in an area of declining Plasmodium falciparum transmission in eastern Tanzania. PLoS Negl Trop Dis. 2019;13: e0007414.PubMedPubMedCentralCrossRef
3.
go back to reference Battle KE, Lucas TCD, Nguyen M, Howes RE, Nandi AK, Twohig KA, et al. Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000–17: a spatial and temporal modelling study. Lancet. 2019;394:332–43.PubMedPubMedCentralCrossRef Battle KE, Lucas TCD, Nguyen M, Howes RE, Nandi AK, Twohig KA, et al. Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000–17: a spatial and temporal modelling study. Lancet. 2019;394:332–43.PubMedPubMedCentralCrossRef
4.
go back to reference Baird JK. African Plasmodium vivax malaria improbably rare or benign. Trends Parasitol. 2022;38:683–96.PubMedCrossRef Baird JK. African Plasmodium vivax malaria improbably rare or benign. Trends Parasitol. 2022;38:683–96.PubMedCrossRef
5.
go back to reference Okafor CN, Finnigan NA. Plasmodium ovale malaria. In: StatPearls. Treasure Island: StatPearls Publishing; 2022. Okafor CN, Finnigan NA. Plasmodium ovale malaria. In: StatPearls. Treasure Island: StatPearls Publishing; 2022.
6.
go back to reference Hawadak J, Dongang Nana RR, Singh V. Epidemiological, physiological and diagnostic comparison of Plasmodium ovale curtisi and Plasmodium ovale wallikeri. Diagnostics (Basel). 2021;11:1900.PubMedCrossRef Hawadak J, Dongang Nana RR, Singh V. Epidemiological, physiological and diagnostic comparison of Plasmodium ovale curtisi and Plasmodium ovale wallikeri. Diagnostics (Basel). 2021;11:1900.PubMedCrossRef
7.
go back to reference Dayananda KK, Achur RN, Gowda DC. Epidemiology, drug resistance, and pathophysiology of Plasmodium vivax malaria. J Vector Borne Dis. 2018;55:1–8.PubMedCrossRef Dayananda KK, Achur RN, Gowda DC. Epidemiology, drug resistance, and pathophysiology of Plasmodium vivax malaria. J Vector Borne Dis. 2018;55:1–8.PubMedCrossRef
9.
go back to reference Taylor AR, Watson JA, Chu CS, Puaprasert K, Duanguppama J, Day NPJ, et al. Resolving the cause of recurrent Plasmodium vivax malaria probabilistically. Nat Commun. 2019;10:5595.PubMedPubMedCentralCrossRef Taylor AR, Watson JA, Chu CS, Puaprasert K, Duanguppama J, Day NPJ, et al. Resolving the cause of recurrent Plasmodium vivax malaria probabilistically. Nat Commun. 2019;10:5595.PubMedPubMedCentralCrossRef
10.
go back to reference National Malaria Elimination Surveillance Programme. 2015. (in Chinese). National Malaria Elimination Surveillance Programme. 2015. (in Chinese).
13.
go back to reference Feng X, Feng J, Zhang L, Tu H, Xia Z. Vector control in China, from malaria endemic to elimination and challenges ahead. Infect Dis Poverty. 2022;11:54.PubMedPubMedCentralCrossRef Feng X, Feng J, Zhang L, Tu H, Xia Z. Vector control in China, from malaria endemic to elimination and challenges ahead. Infect Dis Poverty. 2022;11:54.PubMedPubMedCentralCrossRef
14.
go back to reference Richter J, Franken G, Mehlhorn H, Labisch A, Häussinger D. What is the evidence for the existence of Plasmodium ovale hypnozoites? Parasitol Res. 2010;107:1285–90.PubMedCrossRef Richter J, Franken G, Mehlhorn H, Labisch A, Häussinger D. What is the evidence for the existence of Plasmodium ovale hypnozoites? Parasitol Res. 2010;107:1285–90.PubMedCrossRef
15.
go back to reference Das R, Dhiman RC, Savargaonkar D, Anvikar AR, Valecha N. Genotyping of Plasmodium vivax by minisatellite marker and its application in differentiating relapse and new infection. Malar J. 2016;15:115.PubMedPubMedCentralCrossRef Das R, Dhiman RC, Savargaonkar D, Anvikar AR, Valecha N. Genotyping of Plasmodium vivax by minisatellite marker and its application in differentiating relapse and new infection. Malar J. 2016;15:115.PubMedPubMedCentralCrossRef
16.
go back to reference Smoak BL, DeFraites RF, Magill AJ, Kain KC, Wellde BT. Plasmodium vivax infections in U.S. Army troops: failure of primaquine to prevent relapse in studies from Somalia. Am J Trop Med Hyg. 1997;56:231–4.PubMedCrossRef Smoak BL, DeFraites RF, Magill AJ, Kain KC, Wellde BT. Plasmodium vivax infections in U.S. Army troops: failure of primaquine to prevent relapse in studies from Somalia. Am J Trop Med Hyg. 1997;56:231–4.PubMedCrossRef
17.
go back to reference He X, Pan M, Zeng W, Zou C, Pi L, Qin Y, et al. Multiple relapses of Plasmodium vivax malaria acquired from West Africa and association with poor metabolizer CYP2D6 variant: a case report. BMC Infect Dis. 2019;19:704.PubMedPubMedCentralCrossRef He X, Pan M, Zeng W, Zou C, Pi L, Qin Y, et al. Multiple relapses of Plasmodium vivax malaria acquired from West Africa and association with poor metabolizer CYP2D6 variant: a case report. BMC Infect Dis. 2019;19:704.PubMedPubMedCentralCrossRef
18.
go back to reference Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, Nandy A, et al. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis. 2007;195:927–33.PubMedCrossRef Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, Nandy A, et al. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis. 2007;195:927–33.PubMedCrossRef
19.
go back to reference Imwong M, Boel ME, Pagornrat W, Pimanpanarak M, McGready R, Day NPJ, et al. The first Plasmodium vivax relapses of life are usually genetically homologous. J Infect Dis. 2012;205:680–3.PubMedCrossRef Imwong M, Boel ME, Pagornrat W, Pimanpanarak M, McGready R, Day NPJ, et al. The first Plasmodium vivax relapses of life are usually genetically homologous. J Infect Dis. 2012;205:680–3.PubMedCrossRef
20.
go back to reference Groger M, Fischer HS, Veletzky L, Lalremruata A, Ramharter M. A systematic review of the clinical presentation, treatment and relapse characteristics of human plasmodium ovale malaria. Malar J. 2017;16:112.PubMedPubMedCentralCrossRef Groger M, Fischer HS, Veletzky L, Lalremruata A, Ramharter M. A systematic review of the clinical presentation, treatment and relapse characteristics of human plasmodium ovale malaria. Malar J. 2017;16:112.PubMedPubMedCentralCrossRef
21.
go back to reference Cui Y, Zhang L, Xia Z, Zhou H, Huang F. Epidemiological characterization of imported recurrent Plasmodium vivax and Plasmodium ovale in China, 2013–2020. Infect Dis Poverty. 2021;10:113.PubMedPubMedCentralCrossRef Cui Y, Zhang L, Xia Z, Zhou H, Huang F. Epidemiological characterization of imported recurrent Plasmodium vivax and Plasmodium ovale in China, 2013–2020. Infect Dis Poverty. 2021;10:113.PubMedPubMedCentralCrossRef
22.
go back to reference China NHC. Diagnosis of malaria (WS259-2015). Health industry standards of the People’s Republic of China; 2015. (in Chinese). China NHC. Diagnosis of malaria (WS259-2015). Health industry standards of the People’s Republic of China; 2015. (in Chinese).
23.
go back to reference China NHC. Technical regulations for application of antimalarials. Beijing: National Health Commission of the People’s Republic China; 2015. (in Chinese). China NHC. Technical regulations for application of antimalarials. Beijing: National Health Commission of the People’s Republic China; 2015. (in Chinese).
24.
go back to reference Lee YC, Tang CS, Ang LW, Han HK, James L, Goh KT. Epidemiological characteristics of imported and locally-acquired malaria in Singapore. Ann Acad Med Singap. 2009;38:840–9.PubMedCrossRef Lee YC, Tang CS, Ang LW, Han HK, James L, Goh KT. Epidemiological characteristics of imported and locally-acquired malaria in Singapore. Ann Acad Med Singap. 2009;38:840–9.PubMedCrossRef
25.
go back to reference Karunasena VM, Marasinghe M, Koo C, Amarasinghe S, Senaratne AS, Hasantha R, et al. The first introduced malaria case reported from Sri Lanka after elimination: implications for preventing the re-introduction of malaria in recently eliminated countries. Malar J. 2019;18:210.PubMedPubMedCentralCrossRef Karunasena VM, Marasinghe M, Koo C, Amarasinghe S, Senaratne AS, Hasantha R, et al. The first introduced malaria case reported from Sri Lanka after elimination: implications for preventing the re-introduction of malaria in recently eliminated countries. Malar J. 2019;18:210.PubMedPubMedCentralCrossRef
26.
go back to reference Brook JH, Genese CA, Bloland PB, Zucker JR, Spitalny KC. Brief report: malaria probably locally acquired in New Jersey. N Engl J Med. 1994;331:22–3.PubMedCrossRef Brook JH, Genese CA, Bloland PB, Zucker JR, Spitalny KC. Brief report: malaria probably locally acquired in New Jersey. N Engl J Med. 1994;331:22–3.PubMedCrossRef
27.
go back to reference Layton M, Parise ME, Campbell CC, Advani R, Sexton JD, Bosler EM, et al. Mosquito-transmitted malaria in New York City, 1993. Lancet. 1995;346:729–31.PubMedCrossRef Layton M, Parise ME, Campbell CC, Advani R, Sexton JD, Bosler EM, et al. Mosquito-transmitted malaria in New York City, 1993. Lancet. 1995;346:729–31.PubMedCrossRef
28.
go back to reference Simões LR, Alves ER Jr, Ribatski-Silva D, Gomes LT, Nery AF, Fontes CJ. Factors associated with recurrent Plasmodium vivax malaria in Porto Velho, Rondônia State, Brazil, 2009. Cad Saude Publica. 2014;30:1403–17.PubMedCrossRef Simões LR, Alves ER Jr, Ribatski-Silva D, Gomes LT, Nery AF, Fontes CJ. Factors associated with recurrent Plasmodium vivax malaria in Porto Velho, Rondônia State, Brazil, 2009. Cad Saude Publica. 2014;30:1403–17.PubMedCrossRef
29.
go back to reference Yeshiwondim AK, Tekle AH, Dengela DO, Yohannes AM, Teklehaimanot A. Therapeutic efficacy of chloroquine and chloroquine plus primaquine for the treatment of Plasmodium vivax in Ethiopia. Acta Trop. 2010;113:105–13.PubMedCrossRef Yeshiwondim AK, Tekle AH, Dengela DO, Yohannes AM, Teklehaimanot A. Therapeutic efficacy of chloroquine and chloroquine plus primaquine for the treatment of Plasmodium vivax in Ethiopia. Acta Trop. 2010;113:105–13.PubMedCrossRef
30.
go back to reference Golassa L, White MT. Population-level estimates of the proportion of Plasmodium vivax blood-stage infections attributable to relapses among febrile patients attending Adama Malaria Diagnostic Centre, East Shoa Zone, Oromia, Ethiopia. Malar J. 2017;16:301.PubMedPubMedCentralCrossRef Golassa L, White MT. Population-level estimates of the proportion of Plasmodium vivax blood-stage infections attributable to relapses among febrile patients attending Adama Malaria Diagnostic Centre, East Shoa Zone, Oromia, Ethiopia. Malar J. 2017;16:301.PubMedPubMedCentralCrossRef
31.
go back to reference Lawpoolsri S, Sattabongkot J, Sirichaisinthop J, Cui L, Kiattibutr K, Rachaphaew N, et al. Epidemiological profiles of recurrent malaria episodes in an endemic area along the Thailand-Myanmar border: a prospective cohort study. Malar J. 2019;18:124.PubMedPubMedCentralCrossRef Lawpoolsri S, Sattabongkot J, Sirichaisinthop J, Cui L, Kiattibutr K, Rachaphaew N, et al. Epidemiological profiles of recurrent malaria episodes in an endemic area along the Thailand-Myanmar border: a prospective cohort study. Malar J. 2019;18:124.PubMedPubMedCentralCrossRef
32.
go back to reference James SP, Nicol WD, Shute PG. Clinical and parasitological observations on induced malaria. Proc R Soc Med. 1936;29:27–42. James SP, Nicol WD, Shute PG. Clinical and parasitological observations on induced malaria. Proc R Soc Med. 1936;29:27–42.
33.
go back to reference James SP, Shute PG. Report on the first results of laboratory work on malaria in England. In: League of Nations. Health Organization. Volume 57. Geneva. C. H. Malaria; 1926:30. James SP, Shute PG. Report on the first results of laboratory work on malaria in England. In: League of Nations. Health Organization. Volume 57. Geneva. C. H. Malaria; 1926:30.
34.
go back to reference Schuffner WAC, Kortweg PC, Swellengrebel NH. Pathology—experimental malaria with protracted incubation. Proc R Acad Sci Amsterdam. 1929;32:903–11. Schuffner WAC, Kortweg PC, Swellengrebel NH. Pathology—experimental malaria with protracted incubation. Proc R Acad Sci Amsterdam. 1929;32:903–11.
35.
go back to reference Nikolaiev BP. Subspecies of the parasite of tertian malaria (Plasmodium vivax). Dokl Akad Navk USSR. 1949;67:201–10. Nikolaiev BP. Subspecies of the parasite of tertian malaria (Plasmodium vivax). Dokl Akad Navk USSR. 1949;67:201–10.
36.
go back to reference Boyd MF. The influence of sporozoite dosage in vivax malaria. Am J Trop Med. 1940;20:279–86.CrossRef Boyd MF. The influence of sporozoite dosage in vivax malaria. Am J Trop Med. 1940;20:279–86.CrossRef
38.
go back to reference Daher A, Silva JCAL, Stevens A, Marchesini P, Fontes CJ, Ter Kuile FO, et al. Evaluation of Plasmodium vivax malaria recurrence in Brazil. Malar J. 2019;18:18.PubMedPubMedCentralCrossRef Daher A, Silva JCAL, Stevens A, Marchesini P, Fontes CJ, Ter Kuile FO, et al. Evaluation of Plasmodium vivax malaria recurrence in Brazil. Malar J. 2019;18:18.PubMedPubMedCentralCrossRef
40.
go back to reference Teklehaimanot A, Teklehaimanot H, Girmay A, Woyessa A. Primaquine failure for radical cure of Plasmodium vivax malaria in Gambella, Ethiopia. Am J Trop Med Hyg. 2020;103:415–20.PubMedPubMedCentralCrossRef Teklehaimanot A, Teklehaimanot H, Girmay A, Woyessa A. Primaquine failure for radical cure of Plasmodium vivax malaria in Gambella, Ethiopia. Am J Trop Med Hyg. 2020;103:415–20.PubMedPubMedCentralCrossRef
41.
go back to reference Ariffin NM, Islahudin F, Kumolosasi E, Makmor-Bakry M. Effects of MAO-A and CYP450 on primaquine metabolism in healthy volunteers. Parasitol Res. 2019;118:1011–8.PubMedCrossRef Ariffin NM, Islahudin F, Kumolosasi E, Makmor-Bakry M. Effects of MAO-A and CYP450 on primaquine metabolism in healthy volunteers. Parasitol Res. 2019;118:1011–8.PubMedCrossRef
42.
go back to reference Zhou Y, Ingelman-Sundberg M, Lauschke VM. Worldwide distribution of cytochrome P450 alleles: a meta-analysis of population-scale sequencing projects. Clin Pharmacol Ther. 2017;102:688–700.PubMedPubMedCentralCrossRef Zhou Y, Ingelman-Sundberg M, Lauschke VM. Worldwide distribution of cytochrome P450 alleles: a meta-analysis of population-scale sequencing projects. Clin Pharmacol Ther. 2017;102:688–700.PubMedPubMedCentralCrossRef
43.
go back to reference Baird JK, Louisa M, Noviyanti R, Ekawati L, Elyazar I, Subekti D, et al. Association of impaired cytochrome P450 2D6 activity genotype and phenotype with therapeutic efficacy of primaquine treatment for latent Plasmodium vivax malaria. JAMA Netw Open. 2018;1:e181449.PubMedPubMedCentralCrossRef Baird JK, Louisa M, Noviyanti R, Ekawati L, Elyazar I, Subekti D, et al. Association of impaired cytochrome P450 2D6 activity genotype and phenotype with therapeutic efficacy of primaquine treatment for latent Plasmodium vivax malaria. JAMA Netw Open. 2018;1:e181449.PubMedPubMedCentralCrossRef
44.
go back to reference Zhang T, Wang D, Qian Y, Ruan W, Liu Y, Xia J. Profile and determinants of delayed care-seeking and diagnosis among patients with imported malaria: a retrospective study in China, 2014–2021. Infect Dis Poverty. 2022;11:125.PubMedPubMedCentralCrossRef Zhang T, Wang D, Qian Y, Ruan W, Liu Y, Xia J. Profile and determinants of delayed care-seeking and diagnosis among patients with imported malaria: a retrospective study in China, 2014–2021. Infect Dis Poverty. 2022;11:125.PubMedPubMedCentralCrossRef
45.
go back to reference Newman RD, Parise ME, Barber AM, Steketee RW, et al. Malaria-related deaths among US travelers, 1963–2001. Ann Intern Med. 2004;141:547–55.PubMedCrossRef Newman RD, Parise ME, Barber AM, Steketee RW, et al. Malaria-related deaths among US travelers, 1963–2001. Ann Intern Med. 2004;141:547–55.PubMedCrossRef
Metadata
Title
Analysis of the relapse of imported Plasmodium vivax and Plasmodium ovale in five provinces of China
Authors
Hui Yan
Shujiao Wei
Yuan Sui
Shenning Lu
Weiwei Zhang
Xiangyang Feng
Ying Liu
Tao Zhang
Wei Ruan
Jing Xia
Wen Lin
Benedikt Ley
Sarah Auburn
Shizhu Li
Jun Li
Duoquan Wang
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2023
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-023-04642-y

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