Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Characteristics of Imported Malaria and Species of Plasmodium Involved in Shandong Province, China (2012-2014)

  • Xu, Chao (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Wei, Qing-Kuan (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Li, Jin (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Xiao, Ting (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Yin, Kun (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Zhao, Chang-Lei (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Wang, Yong-Bin (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Kong, Xiang-Li (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Zhao, Gui-Hua (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Sun, Hui (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Liu, Xin (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis) ;
  • Huang, Bing-Cheng (Shandong Academy of Medical Sciences, Shandong Institute of Parasitic Diseases, Shandong Provincial Reference Laboratory for Malaria Diagnosis)
  • Received : 2015.12.16
  • Accepted : 2016.05.24
  • Published : 2016.08.31
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Abstract

Malaria remains a serious public health problem in Shandong Province, China; therefore, it is important to explore the characteristics of the current malaria prevalence situation in the province. In this study, data of malaria cases reported in Shandong during 2012-2014 were analyzed, and Plasmodium species were confirmed by smear microscopy and nested-PCR. A total of 374 malaria cases were reported, 80.8% of which were reported from 6 prefectures. Of all cases, P. falciparum was dominant (81.3%), followed by P. vivax (11.8%); P. ovale and P. malariae together accounted for 6.4% of cases. Notably, for the first time since 2012, no indigenous case had been reported in Shandong Province, a situation that continued through 2014. Total 95.2% of cases were imported from Africa. The ratio of male/female was 92.5:1, and 96.8% of cases occurred in people 20-54 years of age. Farmers or laborers represented 77.5% of cases. No significant trends of monthly pattern were found in the reported cases. All patients were in good condition after treatment, except for 3 who died. These results indicate that imported malaria has increased significantly since 2012 in Shandong Province, especially for P. falciparum, and there is an emergence of species diversity.

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References

  1. Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RG. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet 2013; 382: 900-911. https://doi.org/10.1016/S0140-6736(13)60310-4
  2. World Health Organization. World Malaria Report, 2011. Geneva, Switzerland. World Health Organization. 2011.
  3. World Health Organization. World Malaria Report, 2013. Geneva, Switzerland. World Health Organization. 2013.
  4. Zhang Q, Lai S, Zheng C, Zhang H, Zhou S, Hu W, Clements AC, Zhou XN, Yang W, Hay SI, Yu H, Li Z. The epidemiology of Plasmodium vivax and Plasmodium falciparum malaria in China, 2004-2012: from intensified control to elimination. Malar J 2014; 13: 419. https://doi.org/10.1186/1475-2875-13-419
  5. Tang L. Progress in malaria control in China. Chin Med J (Engl) 2000; 113: 89-92.
  6. Bu XQ, Wang YB, Zhao CL, Chen XX, Kong XL, Zhang BG. Effects of integrated malaria control measures in Shandong Province, 2010. Chin J Parasitol Parasit Dis 2012; 24: 116-118 (in Chinese).
  7. Feng J, Xia ZG, Vong S, Yang WZ, Zhou SS, Xiao N. Preparedness for malaria resurgence in China: case study on imported cases in 2000-2012. Adv Parasitol 2014; 86: 231-265.
  8. Tang LH. Diagnosis, Treatment and Management of Imported Malaria Cases. Shanghai, China. Shanghai Scientific and Technical Publishers. 2010, pp 25-29.
  9. World Health Organization. Basic Malaria Microscopy. Part 1. Learner's Guide. 2nd ed. Geneva, Switzerland. WHO Press. 2010.
  10. Ashraf S, Kao A, Hugo C, Christophel EM, Fatunmbi B, Luchavez J, Lilley K, Bell D. Developing standards for malaria microscopy: external competency assessment for malaria microscopists in the Asia-Pacific. Malar J 2012; 11: 352. https://doi.org/10.1186/1475-2875-11-352
  11. Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 1993; 61: 315-320. https://doi.org/10.1016/0166-6851(93)90077-B
  12. Johnston SP, Pieniazek NJ, Xayavong MV, Slemenda SB, Wilkins PP, da Silva AJ. PCR as a confirmatory technique for laboratory diagnosis of malaria. J Clin Microbiol 2006; 44: 1087-1089. https://doi.org/10.1128/JCM.44.3.1087-1089.2006
  13. The Chinese Center for Disease Control and Prevention of the People's Republic of China. Technology Solutions for Eliminating Malaria (edition 2011). Available at: http://www.chinacdc.cn/tzgg/201109/t20110906_52137.htm (accessed September 06, 2011).
  14. The Ministry of Health of the People's Republic of China. The National Malaria Control Programme (2006-2015). Available at: http://www.moh.gov.cn/mohbgt/pw10603/200804/27565.shtml (accessed February 22, 2006).
  15. Liu Y, Hsiang MS, Zhou H, Wang W, Cao Y, Gosling RD, Cao J, Gao Q. Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu Province, 2001-2011. Malar J 2014; 13: 29. https://doi.org/10.1186/1475-2875-13-29
  16. Feng J, Yan H, Feng XY, Zhang L, Li M, Xia ZG, Xiao N. Imported malaria in China, 2012. Emerg Infect Dis 2014; 20: 1778-1780.
  17. Xia ZG, Wang RB, Wang DQ, Feng J, Zheng Q, Deng CS, Abdulla S, Guan YY, Ding W, Yao JW, Qian YJ, Bosman A, Newman RD, Ernest T, O'leary M, Xiao N. China-Africa cooperation initiatives in malaria control and elimination. Adv Parasitol 2014; 86: 319-337.
  18. Makler MT, Palmer CJ, Ager AL. A review of practical techniques for the diagnosis of malaria. Ann Trop Med Parasitol 1998; 92: 419-433. https://doi.org/10.1080/00034989859401
  19. Moody A. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 2002; 15: 66-78. https://doi.org/10.1128/CMR.15.1.66-78.2002
  20. Ohrt C, Purnomo, Sutamihardja MA, Tang D, Kain KC. Impact of microscopy error on estimates of protective efficacy in malaria-prevention trials. J Infect Dis 2002; 186: 540-546. https://doi.org/10.1086/341938
  21. Collins WE, Jeffery GM. Plasmodium ovale: parasite and disease. Clin Microbiol Rev 2005; 18: 570-581. https://doi.org/10.1128/CMR.18.3.570-581.2005
  22. Coleman RE, Sattabongkot J, Promstaporm S, Maneechai N, Tippayachai B, Kengluecha A, Rachapaew N, Zollner G, Miller RS, Vaughan JA, Thimasarn K, Khuntirat B. Comparison of PCR and microscopy for the detection of asymptomatic malaria in a Plasmodium falciparum/vivax endemic area in Thailand. Malar J 2006; 5: 121. https://doi.org/10.1186/1475-2875-5-121
  23. Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol 1993; 58: 283-292. https://doi.org/10.1016/0166-6851(93)90050-8
  24. Barker RH Jr, Banchongaksorn T, Courval JM, Suwonkerd W, Rimwungtragoon K, Wirth DF. A simple method to detect Plasmodium falciparum directly from blood samples using the polymerase chain reaction. Am J Trop Med Hyg 1992; 46: 416-426. https://doi.org/10.4269/ajtmh.1992.46.416
  25. Gonzalez JM, Hurtado S, Arevalo-Herrera M, Herrera S. Variants of the Plasmodium vivax circumsporozoite protein (VK210 and VK247) in Colombian isolates. Mem Inst Oswaldo Cruz 2001; 96: 709-712. https://doi.org/10.1590/S0074-02762001000500023
  26. del Portillo HA, Longacre S, Khouri E, David PH. Primary structure of the merozoite surface antigen 1 of Plasmodium vivax reveals sequences conserved between different Plasmodium species. Proc Natl Acad Sci USA 1991; 88: 4030-4034. https://doi.org/10.1073/pnas.88.9.4030
  27. Zakeri S, Barjesteh H, Djadid ND. Merozoite surface protein-$3{\alpha}$ is a reliable marker for population genetic analysis of Plasmodium vivax. Malar J 2006; 5: 53. https://doi.org/10.1186/1475-2875-5-53
  28. Xu C, Xu XL, Huang BC. Research progress on polymorphism in the merozoite surface protein-$3{\alpha}$ gene of Plasmodium vivax. Chin J Parasitol Parasit Dis 2013; 31: 473-476 (in Chinese).
  29. Borre MB, Dziegiel M, Hogh B, Petersen E, Rieneck K, Riley E, Meis JF, Aikawa M, Nakamura K, Harada M. Primary structure and localization of a conserved immunogenic Plasmodium falciparum glutamate rich protein (GLURP) expressed in both the preerythrocytic and erythrocytic stages of the vertebrate life cycle. Mol Biochem Parasitol 1991; 49: 119-131. https://doi.org/10.1016/0166-6851(91)90135-S
  30. Kho WG, Chung JY, Sim EJ, Kim DW, Chung WC. Analysis of polymorphic regions of Plasmodium vivax Duffy binding protein of Korean isolates. Korean J Parasitol 2001; 39: 143-150. https://doi.org/10.3347/kjp.2001.39.2.143
  31. Imwong M, Sudimack D, Pukrittayakamee S, Osorio L, Carlton JM, Day NP, White NJ, Anderson TJ. Microsatellite variation, repeat array length, and population history of Plasmodium vivax. Mol Biol Evol 2006; 23: 1016-1018. https://doi.org/10.1093/molbev/msj116
  32. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naude B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems TE. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 2000; 6: 861-871. https://doi.org/10.1016/S1097-2765(05)00077-8
  33. Sidhu AB, Verdier-Pinard D, Fidock DA. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 2002; 298: 210-213. https://doi.org/10.1126/science.1074045
  34. Sidhu AB, Valderramos SG, Fidock DA. pfmdr1 mutations contribute to quinine resistance and enhance mefloquine and artemisinin sensitivity in Plasmodium falciparum. Mol Microbiol 2005; 57: 913-926. https://doi.org/10.1111/j.1365-2958.2005.04729.x
  35. Sanchez CP, Rotmann A, Stein WD, Lanzer M. Polymorphisms within PfMDR1 alter the substrate specificity for anti-malarial drugs in Plasmodium falciparum. Mol Microbiol 2008; 70: 786-798.
  36. Jelinek T, Proll S, Hess F, Kabagambe G, von Sonnenburg F, Loscher T, Kilian AH. Geographic differences in the sensitivity of a polymerase chain reaction for the detection of Plasmodium falciparum infection. Am J Trop Med Hyg 1996; 55: 647-651. https://doi.org/10.4269/ajtmh.1996.55.647
  37. Yin JH, Yan H, Huang F, Li M, Xiao HH, Zhou SS, Xia ZG. Establishing a China malaria diagnosis reference laboratory network for malaria elimination. Malar J 2015; 14: 40. https://doi.org/10.1186/s12936-015-0556-z
  38. Cao J, Sturrock HJ, Cotter C, Zhou S, Zhou H, Liu Y, Tang L, Gosling RD, Feachem RG, Gao Q. Communicating and monitoring surveillance and response activities for malaria elimination: China's "1-3-7" strategy. PLoS Med 2014; 11: e1001642. https://doi.org/10.1371/journal.pmed.1001642
  39. The Ministry of Health of the People's Republic of China. Action Plan of China Malaria Elimination (2010-2020). Available at: http://www.moh.gov.cn/mohbgt/s10788/201005/47529.shtml (accessed May 19, 2010).

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