Feng J, Zhang L, Xia ZG, Zhou SS, Xiao N, 2021. Malaria-free certification in China: Achievements and lessons learned from the National Malaria Elimination Programme. Zoonoses 1: 1.
World Health Organization, 2023. World Malaria Report 2023. Available at: https://malariaworld.org/blogs/world-malaria-report-2023. Accessed 20 Dec 2023.
Li Y, Fang Y, Xue J, Yang L, Liu Q, Shi W, Zhang Y, 2021. Surveillance of malaria vectors—18 sites, 12 PLADs, China, 2018–2020. China CDC Wkly 3: 741–745.
Feng X, Feng J, Zhang L, Tu H, Xia Z, 2022. Vector control in China, from malaria endemic to elimination and challenges ahead. Infect Dis Poverty 11: 54.
Zhang L, Feng J, Zhang SS, Xia ZG, Zhou SS, 2018. The progress of national malaria elimination and epidemiological characteristics of malaria in China in 2017. Chin J Parasitol Parasit Dis 36: 201–209.
Zhang L, Feng J, Zhang SS, Xia ZG, Zhou SS, 2019. Epidemiological characteristics of malaria and the progress toward elimination in China in 2018. Chin J Parasitol Parasit Dis 37: 241–247.
Zhang L, Feng J, Xia ZG, Zhou SS, 2020. Epidemiological characteristics of malaria and progress on its elimination in China in 2019. Chin J Parasitol Parasit Dis 38: 133–138.
Zhang L, Feng J, Tu H, Yin JH, Xia ZG, 2021. Malaria epidemiology in China in 2020. Chin J Parasitol Parasit Dis 39: 195–199.
Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, Moonen B, 2012. Malaria resurgence: A systematic review and assessment of its causes. Malar J 11: 122.
Danis K, Lenglet A, Tseroni M, Baka A, Tsiodras S, Bonovas S, 2013. Malaria in Greece: Historical and current reflections on a re-emerging vector borne disease. Travel Med Infect Dis 11: 8–14.
Tanne JH, 2023. CDC reports locally acquired malaria in two US states. BMJ 381: 1484.
Battle KE, Gething PW, Elyazar IRF, Moyes CL, Sinka ME, Howes RE, Guerra CA, Price RN, Baird KJ, Hay SI, 2012. The global public health significance of Plasmodium vivax. Adv Parasitol 80: 1–111.
Xu X, Zhang T, Jiang JJ, Li WD, 2020. Course of malaria control and elimination in Anhui Province. J Trop Dis Parasitol 18: 65–69, 80.
Guo WS et al., 2020. Epidemiological characteristics of malaria in Henan Province from 1950 to 2019. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 33: 62–65.
Xia J et al., 2018. Epidemiological characteristics of malaria from control to elimination in Hubei Province, China, 2005–2016. Malar J 17: 81.
Yang J, Chen L, Zhu LB, Dong XJ, Yao LN, 2021. Epidemiological characteristics of imported cases of malaria in Yiwu from 2009 to 2019. Prev Med 33: 815–817, 821.
Feng J, Zhang L, Tu H, Zhou SS, Xia ZG, 2021. From elimination to post-elimination: Characteristics, challenges and re-transmission preventing strategy of imported malaria in China. China Trop Med 21: 5–10.
WHO, 2021. WHO Malaria Terminology, 2021 Update. Available at: https://www.who.int/publications/i/item/9789240038400. Accessed 20 Dec 2023.
National Health and Family Planning Commission of China, 2015. Diagnostic Criteria for Malaria (WS 259–2015). Available at: http://www.nhc.gov.cn/fzs/s7852d/201511/5a35d124469a4b69884c942c43ae3269.shtml. Accessed 20 Dec 2023.
Yin JH, Xia ZG, 2022. Consolidating the achievements of elimination and preventing re-establishment of transmission: Main challenges and priorities of malaria prevention and control in post-elimination era in China. J Trop Dis Parasitol 20: 241–244.
Bastaki H, Carter J, Marston L, Cassell J, Rait G, 2018. Time delays in the diagnosis and treatment of malaria in non-endemic countries: A systematic review. Travel Med Infect Dis 21: 21–27.
Zhang T et al., 2022. Profile and determinants of delayed care-seeking and diagnosis among patients with imported malaria: A retrospective study in China, 2014–2021. Infect Dis Poverty 11: 125.
Lu GY et al., 2022. Time to initial diagnosis of imported malaria and its influencing factors in Jiangsu Province. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 34: 172–178.
Wang T, Zhou S-S, Feng J, Oo MM, Chen J, Yan C-F, Zhang Y, Tie P, 2019. Monitoring and evaluation of intervals from onset of fever to diagnosis before “1-3-7” approach in malaria elimination: A retrospective study in Shanxi Province, China from 2013 to 2018. Malar J 18: 235.
Rampling T, Sutherland CJ, Whitty CJ, 2019. Imported malaria: Key messages in an era of elimination. Clin Med (Lond) 19: 153–156.
Gitau EN, Newton CRJC, 2005. Review article: Blood-brain barrier in falciparum malaria. Trop Med Int Health 10: 285–292.
Seringe E et al.; French National Reference Center for Imported Malaria Study Group, 2011. Severe imported Plasmodium falciparum malaria, France, 1996–2003. Emerg Infect Dis 17: 807–813.
Kain KC, Harrington MA, Tennyson S, Keystone JS, 1998. Imported malaria: Prospective analysis of problems in diagnosis and management. Clin Infect Dis 27: 142–149.
Checkley AM, Smith A, Smith V, Blaze M, Bradley D, Chiodini PL, Whitty CJM, 2012. Risk factors for mortality from imported falciparum malaria in the United Kingdom over 20 years: An observational study. BMJ 344: e2116.
Christen D, Steffen R, Schlagenhauf P, 2006. Deaths caused by malaria in Switzerland 1988–2002. Am J Trop Med Hyg 75: 1188–1194.
Rabe C, Paar WD, Knopp A, Münch J, Musch A, Rockstroh J, Martin S, Sauerbruch T, Dumoulin FL, 2005. Malaria in the emergency room. Results of the emergency treatment of 137 patients with symptomatic malaria. Dtsch Med Wochenschr 130: 145–149.
Schubert L, Thurnher PMM, Machold PK, Tobudic PS, Winkler PS, 2021. Pandemic-related delay of falciparum malaria diagnosis in a traveller leading to cerebral malaria. J Travel Med 28: taab159.
Wassmer SC, Taylor TE, Rathod PK, Mishra SK, Mohanty S, Arevalo-Herrera M, Duraisingh MT, Smith JD, 2015. Investigating the pathogenesis of severe malaria: A multidisciplinary and cross-geographical approach. Am J Trop Med Hyg 93: 42–56.
Yman V et al., 2019. Persistent transmission of Plasmodium malariae and Plasmodium ovale species in an area of declining Plasmodium falciparum transmission in eastern Tanzania. PLoS Negl Trop Dis 13: e0007414.
Zhang S, Guo S, Feng X, Afelt A, Frutos R, Zhou S, Manguin S, 2017. Anopheles vectors in mainland China while approaching malaria elimination. Trends Parasitol 33: 889–900.
Feng Y, Tang J, Zhu D, Zhang Y, Zhu G, Wang J, 2021. The microbiota of three Anopheles species in China. J Am Mosq Control Assoc 37: 38–40.
Gao XL, Yang K, 2023. Research advances in vectorial capacity of Anopheles sinensis. Chin J Vector Biol Control 34: 440–446.
Adak T, Singh OP, Das MK, Wattal S, Nanda N, 2005. Comparative susceptibility of three important malaria vectors Anopheles stephensi, Anopheles fluviatilis, and Anopheles sundaicus to Plasmodium vivax. J Parasitol 91: 79–82.
Zhu G, Xia H, Zhou H, Li J, Lu F, Liu Y, Cao J, Gao Q, Sattabongkot J, 2013. Susceptibility of Anopheles sinensis to Plasmodium vivax in malarial outbreak areas of central China. Parasit Vectors 6: 176.
White NJ, 2011. Determinants of relapse periodicity in Plasmodium vivax malaria. Malar J 10: 297.
Battle KE et al., 2014. Geographical variation in Plasmodium vivax relapse. Malar J 13: 144.
Lover AA, Coker RJ, 2013. Quantifying effect of geographic location on epidemiology of Plasmodium vivax malaria. Emerg Infect Dis 19: 1058–1065.
Lysenko AJ, Beljaev AE, 1969. An analysis of the geographical distribution of Plasmodium ovale. Bull World Health Organ 40: 383–394.
May J, Mockenhaupt FP, Ademowo OG, Falusi AG, Olumese PE, Bienzle U, Meyer CG, 1999. High rate of mixed and subpatent malarial infections in Southwest Nigeria. Am J Trop Med Hyg 61: 339–343.
Mueller I, Zimmerman PA, Reeder JC, 2007. Plasmodium malariae and Plasmodium ovale – The “bashful” malaria parasites. Trends Parasitol 23: 278–283.
Fuehrer H-P, Noedl H, 2014. Recent advances in detection of Plasmodium ovale: Implications of separation into the two species Plasmodium ovale wallikeri and Plasmodium ovale curtisi. J Clin Microbiol 52: 387–391.
Fernando D, Rodrigo C, Rajapakse S, 2011. Primaquine in vivax malaria: An update and review on management issues. Malar J 10: 351.
World Health Organization, 2023. WHO Guidelines for Malaria. Available at: https://www.who.int/publications/i/item/guidelines-for-malaria. Accessed 20 Dec 2023.
Commons RJ et al., 2018. The effect of chloroquine dose and primaquine on Plasmodium vivax recurrence: A WorldWide Antimalarial Resistance Network systematic review and individual patient pooled meta-analysis. Lancet Infect Dis 18: 1025–1034.
Huber JH, Koepfli C, España G, Nekkab N, White MT, Alex Perkins T, 2021. How radical is radical cure? Site-specific biases in clinical trials underestimate the effect of radical cure on Plasmodium vivax hypnozoites. Malar J 20: 479.
Wångdahl A, Sondén K, Wyss K, Stenström C, Björklund D, Zhang J, Hervius Askling H, Carlander C, Hellgren U, Färnert A, 2022. Relapse of Plasmodium vivax and Plasmodium ovale malaria with and without primaquine treatment in a nonendemic area. Clin Infect Dis 74: 1199–1207.
Nekkab N, Lana R, Lacerda M, Obadia T, Siqueira A, Monteiro W, Villela D, Mueller I, White M, 2021. Estimated impact of tafenoquine for Plasmodium vivax control and elimination in Brazil: A modelling study. PLoS Med 18: e1003535.
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Although China has achieved malaria elimination certification, the risk of malaria transmission reintroduction due to imported malaria remains. We analyzed data on imported malaria cases collected from January 1, 2014 to December 31, 2021, using multivariable logistic regression analysis to identify the factors associated with severe and relapsing malaria. The odds of severe malaria were around 4-fold greater for patients who were initially diagnosed with a nonmalarial illness than for patients initially diagnosed with malaria. The risk of relapse from Plasmodium vivax or Plasmodium ovale varied depending on the regions of Africa where patients resided. Patients residing in western and southern Africa (compared with Central Africa) had a lower relative risk of relapse. In addition, treatment with primaquine provided protection against malaria relapse. Improving the timeliness of treatment of malaria patients could help reduce the severity of illness, and use of primaquine can mitigate the risk of relapse after treatment.
Financial support: The research is supported by a
Disclosures: No specific ethical approval was needed for this study as it represents a secondary analysis of existing data. Individual observations were anonymized prior to analysis. Data were used with the permission of the Centers for Disease Control and Prevention in five provinces.
Current contact information: Chen Gao, Hong-Zheng Lu, and Hong Su, Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, Hefei, China, E-mails: 2345010453@stu.ahmu.edu.cn, luhongzheng0524@163.com, and suhong5151@sina.com. Chris Cotter, University of California, San Francisco, CA, and Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden, E-mail: chris.cotter@ucsf.edu. Tao Zhang, Anhui Provincial Center for Disease Control and Prevention, Hefei, China, E-mail: ahcdczt@126.com. Shen-Ning Lu, Shi-Zhu Li, and Duo-Quan Wang, School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China, E-mails: lusn@nipd.chinacdc.cn, lisz@chinacdc.cn and wangdq@nipd.chinacdc.cn. Shi-Zhu Li and Duo-Quan Wang, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, China. WHO Collaborating Center for Tropical Diseases, Shanghai, China. Key Laboratory of Parasite and Vector Biology, Ministry of Health, Shanghai, China. National Center for International Research on Tropical Diseases, Ministry of Science and Technology, Shanghai, China. E-mails: lisz@chinacdc.cn and wangdq@nipd.chinacdc.cn.
Feng J, Zhang L, Xia ZG, Zhou SS, Xiao N, 2021. Malaria-free certification in China: Achievements and lessons learned from the National Malaria Elimination Programme. Zoonoses 1: 1.
World Health Organization, 2023. World Malaria Report 2023. Available at: https://malariaworld.org/blogs/world-malaria-report-2023. Accessed 20 Dec 2023.
Li Y, Fang Y, Xue J, Yang L, Liu Q, Shi W, Zhang Y, 2021. Surveillance of malaria vectors—18 sites, 12 PLADs, China, 2018–2020. China CDC Wkly 3: 741–745.
Feng X, Feng J, Zhang L, Tu H, Xia Z, 2022. Vector control in China, from malaria endemic to elimination and challenges ahead. Infect Dis Poverty 11: 54.
Zhang L, Feng J, Zhang SS, Xia ZG, Zhou SS, 2018. The progress of national malaria elimination and epidemiological characteristics of malaria in China in 2017. Chin J Parasitol Parasit Dis 36: 201–209.
Zhang L, Feng J, Zhang SS, Xia ZG, Zhou SS, 2019. Epidemiological characteristics of malaria and the progress toward elimination in China in 2018. Chin J Parasitol Parasit Dis 37: 241–247.
Zhang L, Feng J, Xia ZG, Zhou SS, 2020. Epidemiological characteristics of malaria and progress on its elimination in China in 2019. Chin J Parasitol Parasit Dis 38: 133–138.
Zhang L, Feng J, Tu H, Yin JH, Xia ZG, 2021. Malaria epidemiology in China in 2020. Chin J Parasitol Parasit Dis 39: 195–199.
Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, Moonen B, 2012. Malaria resurgence: A systematic review and assessment of its causes. Malar J 11: 122.
Danis K, Lenglet A, Tseroni M, Baka A, Tsiodras S, Bonovas S, 2013. Malaria in Greece: Historical and current reflections on a re-emerging vector borne disease. Travel Med Infect Dis 11: 8–14.
Tanne JH, 2023. CDC reports locally acquired malaria in two US states. BMJ 381: 1484.
Battle KE, Gething PW, Elyazar IRF, Moyes CL, Sinka ME, Howes RE, Guerra CA, Price RN, Baird KJ, Hay SI, 2012. The global public health significance of Plasmodium vivax. Adv Parasitol 80: 1–111.
Xu X, Zhang T, Jiang JJ, Li WD, 2020. Course of malaria control and elimination in Anhui Province. J Trop Dis Parasitol 18: 65–69, 80.
Guo WS et al., 2020. Epidemiological characteristics of malaria in Henan Province from 1950 to 2019. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 33: 62–65.
Xia J et al., 2018. Epidemiological characteristics of malaria from control to elimination in Hubei Province, China, 2005–2016. Malar J 17: 81.
Yang J, Chen L, Zhu LB, Dong XJ, Yao LN, 2021. Epidemiological characteristics of imported cases of malaria in Yiwu from 2009 to 2019. Prev Med 33: 815–817, 821.
Feng J, Zhang L, Tu H, Zhou SS, Xia ZG, 2021. From elimination to post-elimination: Characteristics, challenges and re-transmission preventing strategy of imported malaria in China. China Trop Med 21: 5–10.
WHO, 2021. WHO Malaria Terminology, 2021 Update. Available at: https://www.who.int/publications/i/item/9789240038400. Accessed 20 Dec 2023.
National Health and Family Planning Commission of China, 2015. Diagnostic Criteria for Malaria (WS 259–2015). Available at: http://www.nhc.gov.cn/fzs/s7852d/201511/5a35d124469a4b69884c942c43ae3269.shtml. Accessed 20 Dec 2023.
Yin JH, Xia ZG, 2022. Consolidating the achievements of elimination and preventing re-establishment of transmission: Main challenges and priorities of malaria prevention and control in post-elimination era in China. J Trop Dis Parasitol 20: 241–244.
Bastaki H, Carter J, Marston L, Cassell J, Rait G, 2018. Time delays in the diagnosis and treatment of malaria in non-endemic countries: A systematic review. Travel Med Infect Dis 21: 21–27.
Zhang T et al., 2022. Profile and determinants of delayed care-seeking and diagnosis among patients with imported malaria: A retrospective study in China, 2014–2021. Infect Dis Poverty 11: 125.
Lu GY et al., 2022. Time to initial diagnosis of imported malaria and its influencing factors in Jiangsu Province. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 34: 172–178.
Wang T, Zhou S-S, Feng J, Oo MM, Chen J, Yan C-F, Zhang Y, Tie P, 2019. Monitoring and evaluation of intervals from onset of fever to diagnosis before “1-3-7” approach in malaria elimination: A retrospective study in Shanxi Province, China from 2013 to 2018. Malar J 18: 235.
Rampling T, Sutherland CJ, Whitty CJ, 2019. Imported malaria: Key messages in an era of elimination. Clin Med (Lond) 19: 153–156.
Gitau EN, Newton CRJC, 2005. Review article: Blood-brain barrier in falciparum malaria. Trop Med Int Health 10: 285–292.
Seringe E et al.; French National Reference Center for Imported Malaria Study Group, 2011. Severe imported Plasmodium falciparum malaria, France, 1996–2003. Emerg Infect Dis 17: 807–813.
Kain KC, Harrington MA, Tennyson S, Keystone JS, 1998. Imported malaria: Prospective analysis of problems in diagnosis and management. Clin Infect Dis 27: 142–149.
Checkley AM, Smith A, Smith V, Blaze M, Bradley D, Chiodini PL, Whitty CJM, 2012. Risk factors for mortality from imported falciparum malaria in the United Kingdom over 20 years: An observational study. BMJ 344: e2116.
Christen D, Steffen R, Schlagenhauf P, 2006. Deaths caused by malaria in Switzerland 1988–2002. Am J Trop Med Hyg 75: 1188–1194.
Rabe C, Paar WD, Knopp A, Münch J, Musch A, Rockstroh J, Martin S, Sauerbruch T, Dumoulin FL, 2005. Malaria in the emergency room. Results of the emergency treatment of 137 patients with symptomatic malaria. Dtsch Med Wochenschr 130: 145–149.
Schubert L, Thurnher PMM, Machold PK, Tobudic PS, Winkler PS, 2021. Pandemic-related delay of falciparum malaria diagnosis in a traveller leading to cerebral malaria. J Travel Med 28: taab159.
Wassmer SC, Taylor TE, Rathod PK, Mishra SK, Mohanty S, Arevalo-Herrera M, Duraisingh MT, Smith JD, 2015. Investigating the pathogenesis of severe malaria: A multidisciplinary and cross-geographical approach. Am J Trop Med Hyg 93: 42–56.
Yman V et al., 2019. Persistent transmission of Plasmodium malariae and Plasmodium ovale species in an area of declining Plasmodium falciparum transmission in eastern Tanzania. PLoS Negl Trop Dis 13: e0007414.
Zhang S, Guo S, Feng X, Afelt A, Frutos R, Zhou S, Manguin S, 2017. Anopheles vectors in mainland China while approaching malaria elimination. Trends Parasitol 33: 889–900.
Feng Y, Tang J, Zhu D, Zhang Y, Zhu G, Wang J, 2021. The microbiota of three Anopheles species in China. J Am Mosq Control Assoc 37: 38–40.
Gao XL, Yang K, 2023. Research advances in vectorial capacity of Anopheles sinensis. Chin J Vector Biol Control 34: 440–446.
Adak T, Singh OP, Das MK, Wattal S, Nanda N, 2005. Comparative susceptibility of three important malaria vectors Anopheles stephensi, Anopheles fluviatilis, and Anopheles sundaicus to Plasmodium vivax. J Parasitol 91: 79–82.
Zhu G, Xia H, Zhou H, Li J, Lu F, Liu Y, Cao J, Gao Q, Sattabongkot J, 2013. Susceptibility of Anopheles sinensis to Plasmodium vivax in malarial outbreak areas of central China. Parasit Vectors 6: 176.
White NJ, 2011. Determinants of relapse periodicity in Plasmodium vivax malaria. Malar J 10: 297.
Battle KE et al., 2014. Geographical variation in Plasmodium vivax relapse. Malar J 13: 144.
Lover AA, Coker RJ, 2013. Quantifying effect of geographic location on epidemiology of Plasmodium vivax malaria. Emerg Infect Dis 19: 1058–1065.
Lysenko AJ, Beljaev AE, 1969. An analysis of the geographical distribution of Plasmodium ovale. Bull World Health Organ 40: 383–394.
May J, Mockenhaupt FP, Ademowo OG, Falusi AG, Olumese PE, Bienzle U, Meyer CG, 1999. High rate of mixed and subpatent malarial infections in Southwest Nigeria. Am J Trop Med Hyg 61: 339–343.
Mueller I, Zimmerman PA, Reeder JC, 2007. Plasmodium malariae and Plasmodium ovale – The “bashful” malaria parasites. Trends Parasitol 23: 278–283.
Fuehrer H-P, Noedl H, 2014. Recent advances in detection of Plasmodium ovale: Implications of separation into the two species Plasmodium ovale wallikeri and Plasmodium ovale curtisi. J Clin Microbiol 52: 387–391.
Fernando D, Rodrigo C, Rajapakse S, 2011. Primaquine in vivax malaria: An update and review on management issues. Malar J 10: 351.
World Health Organization, 2023. WHO Guidelines for Malaria. Available at: https://www.who.int/publications/i/item/guidelines-for-malaria. Accessed 20 Dec 2023.
Commons RJ et al., 2018. The effect of chloroquine dose and primaquine on Plasmodium vivax recurrence: A WorldWide Antimalarial Resistance Network systematic review and individual patient pooled meta-analysis. Lancet Infect Dis 18: 1025–1034.
Huber JH, Koepfli C, España G, Nekkab N, White MT, Alex Perkins T, 2021. How radical is radical cure? Site-specific biases in clinical trials underestimate the effect of radical cure on Plasmodium vivax hypnozoites. Malar J 20: 479.
Wångdahl A, Sondén K, Wyss K, Stenström C, Björklund D, Zhang J, Hervius Askling H, Carlander C, Hellgren U, Färnert A, 2022. Relapse of Plasmodium vivax and Plasmodium ovale malaria with and without primaquine treatment in a nonendemic area. Clin Infect Dis 74: 1199–1207.
Nekkab N, Lana R, Lacerda M, Obadia T, Siqueira A, Monteiro W, Villela D, Mueller I, White M, 2021. Estimated impact of tafenoquine for Plasmodium vivax control and elimination in Brazil: A modelling study. PLoS Med 18: e1003535.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1792 | 1792 | 892 |
Full Text Views | 15 | 15 | 7 |
PDF Downloads | 21 | 21 | 7 |