Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Ashley EA et al. Tracking Resistance to Artemisinin Collaboration (TRAC), 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371: 411–423.
-
2.
Fairhurst RM, Dondorp AM, 2016. Artemisinin-resistant Plasmodium falciparum malaria. Microbiol Spectr 4: EI10-0013-2016.
-
3.
Dondorp AM et al. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361: 455–467.
-
4.
Muwanguzi J, Henriques G, Sawa P, Bousema T, Sutherland CJ, 2016. Lack of K13 mutations in Plasmodium falciparum persisting after artemisinin combination therapy treatment of Kenyan children. Malar J 15: 36.
-
5.
Escobar C, Pateira S, Lobo E, Lobo L, Teodosio R, Dias F, Fernandes N, Arez AP, Varandas L, Nogueira F, 2015. Polymorphisms in Plasmodium falciparum K13-propeller in Angola and Mozambique after the introduction of the ACTs. PLoS One 10: e0119215.
-
6.
Isozumi R, Uemura H, Kimata I, Ichinose Y, Logedi J, Omar AH, Kaneko A, 2015. Novel mutations in K13 propeller gene of artemisinin-resistant Plasmodium falciparum. Emerg Infect Dis 21: 490–492.
-
7.
Kamau E et al. 2015. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis 211: 1352–1355.
-
8.
Taylor SM et al. 2015. Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: a molecular epidemiologic study. J Infect Dis 211: 680–688.
-
9.
Borrmann S et al. 2011. Declining responsiveness of Plasmodium falciparum infections to artemisinin-based combination treatments on the Kenyan Coast. PLoS One 6: e26005.
-
10.
Gadalla NB et al. 2011. Increased pfmdr1 copy number and sequence polymorphisms in Plasmodium falciparum isolates from Sudanese malaria patients treated with artemether-lumefantrine. Antimicrob Agents Chemother 55: 5408–5411.
-
11.
Chang HH et al. 2016. Persistence of Plasmodium falciparum parasitemia after artemisinin combination therapy: evidence from a randomized trial in Uganda. Sci Rep 6: 26330.
-
12.
Betson M, Sousa-Figueiredo JC, Atuhaire A, Arinaitwe M, Adriko M, Mwesigwa G, Nabonge J, Kabatereine NB, Sutherland CJ, Stothard JR, 2014. Detection of persistent Plasmodium spp. infections in Ugandan children after artemether-lumefantrine treatment. Parasitology 141: 1880–1890.
-
13.
Beshir KB et al. 2013. Residual Plasmodium falciparum parasitemia in kenyan children after artemisinin-combination therapy is associated with increased transmission to mosquitoes and parasite recurrence. J Infect Dis 208: 2017–2024.
-
14.
Duparc S, Borghini-fuhrer I, Craft JC, Arbe-barnes S, Miller RM, Shin C, Fleckenstein L, 2013. Safety and efficacy of pyronaridine-artesunate in uncomplicated acute malaria: an integrated analysis of individual patient data from six randomized clinical trials. Malar J 12: 70.
-
15.
Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH, 2007. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg 77: 119–127.
-
16.
Moody A, 2002. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 15: 66–78.
-
17.
Murray CK, Gasser RA, Magill AJ, Miller RS, 2008. Update on rapid diagnostic testing for malaria. Clin Microbiol Rev 21: 97–110.
-
18.
Omar SA, Mens PF, Schoone GJ, Yusuf A, Mwangi J, Kaniaru S, Omer GAA, Schallig HDFH, 2005. Plasmodium falciparum: evaluation of a quantitative nucleic acid sequence-based amplification assay to predict the outcome of sulfadoxine–pyrimethamine treatment of uncomplicated malaria. Exp Parasitol 110: 73–79.
-
19.
Vasoo S, Pritt BS, 2013. Molecular diagnostics and parasitic disease. Clin Lab Med 33: 461–503.
-
20.
Mens P et al. 2012. Direct blood PCR in combination with nucleic acid lateral flow immunoassay for detection of Plasmodium species in settings where malaria is endemic. J Clin Microbiol 50: 3520–3525.
-
21.
Roth JM, de Bes L, Sawa P, Omweri G, Osoti V, Oberheitmann B, Schallig HDFH, Mens PF, 2018. Plasmodium detection and differentiation by direct-on-blood PCR nucleic acid lateral flow immunoassay. J Mol Diagn 20: 78–86.
-
22.
World Health Organization, 2009. Methods for Surveillance of Antimalarial Drug Efficacy. Geneva, Switzerland: WHO. Available at: http://www.who.int/malaria/publications/atoz/9789241597531/en/. Accessed December 19, 2017.
-
23.
World Health Organization, 2010. Basic Malaria Microscopy—Part I: Learner’s Guide, 2nd edition. Geneva, Switzerland: WHO.
-
24.
Snounou G, 2002. Genotyping of Plasmodium spp. nested PCR. Methods Mol Med 72: 103–116.
-
25.
World Health Organization, 2007. Methods and Techniques for Clinical Trials on Antimalarial Drug Efficacy: Genotyping to Identify Parasite Populations. Geneva, Switzerland: WHO. Available at: http://www.who.int/malaria/publications/atoz/9789241596305/en/. Accessed December 19, 2017.
-
26.
Kattenberg JH, Tahita CM, Versteeg IAJ, Tinto H, Traore-Coulibaly M, Schallig HDFH, Mens PF, 2012. Antigen persistence of rapid diagnostic tests in pregnant women in Nanoro, Burkina Faso, and the implications for the diagnosis of malaria in pregnancy. Trop Med Int Health 17: 550–557.
-
27.
Hermsen CC, Telgt DSC, Linders EHP, Van De Locht LATF, Eling WMC, Mensink EJBM, Sauerwein RW, 2001. Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol 118: 247–251.
-
28.
Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, Lavstsen T, 2009. The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int 58: 478–480.
-
29.
Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, Eling W, Sauerwein R, 2004. Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol 137: 35–41.
-
30.
White NJ, 1997. Assessment of the pharmacodynamic properties of antimalarial drugs in vivo. Antimicrob Agents Chemother 41: 1413–1422.
-
31.
Beshir KB, Hallett RL, Eziefula AC, Bailey R, Watson J, Wright SG, Chiodini PL, Polley SD, Sutherland CJ, 2010. Measuring the efficacy of anti-malarial drugs in vivo: quantitative PCR measurement of parasite clearance. Malar J 9: 312.
-
32.
Tshefu AK, Gaye O, Kayentao K, Thompson R, Bhatt KM, Sesay SSS, Bustos DG, Tjitra E, 2010. Efficacy and safety of a fixed-dose oral combination of pyronaridine-artesunate compared with artemether-lumefantrine in children and adults with uncomplicated Plasmodium falciparum malaria: a randomised non-inferiority trial. Lancet 375: 1457–1467.
-
33.
Kayentao K et al. 2012. Pyronaridine-artesunate granules versus artemether-lumefantrine crushed tablets in children with Plasmodium falciparum malaria: a randomized controlled trial. Malar J 11: 364.
-
34.
Méndez F, Muñoz Á, Carrasquilla G, Jurado D, Arévalo-Herrera M, Cortese JF, Plowe CV, 2002. Determinants of treatment response to sulfadoxine-pyrimethamine and subsequent transmission potential in falciparum malaria. Am J Epidemiol 156: 230–238.
-
35.
Carrara VI et al. 2009. Changes in the treatment responses to artesunate-mefloquine on the northwestern border of Thailand during 13 years of continuous deployment. PLoS One 4: e4551.
-
36.
Das D, Price RN, Bethell D, Guerin PJ, Stepniewska K, 2013. Early parasitological response following artemisinin-containing regimens: a critical review of the literature. Malar J 12: 125.
-
37.
Stepniewska K et al. 2010. In vivo parasitological measures of artemisinin susceptibility. J Infect Dis 201: 570–579.
-
38.
Vijaykadga S, Alker AP, Satimai W, MacArthur JR, Meshnick SR, Wongsrichanalai C, 2012. Delayed Plasmodium falciparum clearance following artesunate-mefloquine combination therapy in Thailand, 1997–2007. Malar J 11: 296.
-
39.
Greenhouse B, Dokomajilar C, Hubbard A, Rosenthal PJ, Dorsey G, 2007. Impact of transmission intensity on the accuracy of genotyping to distinguish recrudescence from new infection in antimalarial clinical trials. Antimicrob Agents Chemother 51: 3096–3103.
-
40.
Lo E, Nguyen J, Oo W, Hemming-Schroeder E, Zhou G, Yang Z, Cui L, Yan G, 2016. Examining Plasmodium falciparum and P. vivax clearance subsequent to antimalarial drug treatment in the Myanmar-China border area based on quantitative real-time polymerase chain reaction. BMC Infect Dis 16: 154.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1174 | 934 | 92 |
| Full Text Views | 692 | 20 | 1 |
| PDF Downloads | 249 | 17 | 0 |
Molecular Detection of Residual Parasitemia after Pyronaridine–Artesunate or Artemether–Lumefantrine Treatment of Uncomplicated Plasmodium falciparum Malaria in Kenyan Children
Johanna M. Roth
Johanna M. Roth
Department of Medical Microbiology, Academic Medical Center, Amsterdam, The Netherlands;
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Patrick Sawa
Patrick Sawa
Human Health Division, International Centre of Insect Physiology and Ecology, Mbita Point, Kenya
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George Omweri
George Omweri
Human Health Division, International Centre of Insect Physiology and Ecology, Mbita Point, Kenya
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Nicodemus Makio
Nicodemus Makio
Human Health Division, International Centre of Insect Physiology and Ecology, Mbita Point, Kenya
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Victor Osoti
Victor Osoti
Human Health Division, International Centre of Insect Physiology and Ecology, Mbita Point, Kenya
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Menno D. de Jong
Menno D. de Jong
Department of Medical Microbiology, Academic Medical Center, Amsterdam, The Netherlands;
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Henk D. F. H. Schallig
Henk D. F. H. Schallig
Department of Medical Microbiology, Academic Medical Center, Amsterdam, The Netherlands;
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Pètra F. Mens
Pètra F. Mens
Department of Medical Microbiology, Academic Medical Center, Amsterdam, The Netherlands;
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Artemisinin resistance is rapidly rising in Southeast Asia and may spread to African countries, where efficacy estimates are currently still excellent. Extensive monitoring of parasite clearance dynamics after treatment is needed to determine whether responsiveness to artemisinin-based combination therapies (ACT) is changing in Africa. In this study, Kenyan children with uncomplicated falciparum malaria were randomly assigned to pyronaridine–artesunate (PA) or artemether–lumefantrine (AL) treatment. Parasite clearance was evaluated over 7 days following the start of treatment by quantitative polymerase chain reaction (qPCR) and direct-on-blood PCR nucleic acid lateral flow immunoassay (db-PCR-NALFIA), a simplified molecular malaria diagnostic. Residual parasitemia at day 7 was detected by qPCR in 37.1% (26/70) of AL-treated children and in 46.1% (35/76) of PA-treated participants (P = 0.275). Direct-on-blood PCR nucleic acid lateral flow immunoassay detected residual parasites at day 7 in 33.3% (23/69) and 30.3% (23/76) of AL and PA-treated participants, respectively (P = 0.692). qPCR-determined parasitemia at day 7 was associated with increased prevalence and density of gametocytes at baseline (P = 0.014 and P = 0.003, for prevalence and density, respectively) and during follow-up (P = 0.007 and P = 0.011, respectively, at day 7). A positive db-PCR-NALFIA outcome at day 7 was associated with treatment failure (odds ratio [OR]: 3.410, 95% confidence interval [CI]: 1.513–7.689, P = 0.003), but this association was not found for qPCR (OR: 0.701, 95% CI: 0.312–1.578, P = 0.391). Both qPCR and db-PCR-NALFIA detected substantial residual submicroscopic parasitemia after microscopically successful PA and AL treatment and can be useful tools to monitor parasite clearance. To predict treatment outcome, db-PCR-NALFIA may be more suitable than qPCR.
Author Notes
Financial support: This work was supported by the EU FP7-Health-2013.0-1 project “Translation of the direct-on-blood PCR-NALFIA system into an innovative near point-of-care diagnostic for malaria” (DIAGMAL) (grant number 601714).
Disclosures: Shin Poong Pharmaceutical Company (Seoul, South-Korea) provided pyronaridine-artesunate tablets and granules, but had no further role in study design, data collection, data analysis and writing of the report.
Authors’ addresses: Johanna M. Roth, Menno D. de Jong, Henk D. F. H. Schallig, and Pètra F. Mens, Academic Medical Center, Amsterdam, The Netherlands, E-mails: j.m.roth@amc.uva.nl, m.d.dejong@amc.uva.nl, h.d.schallig@amc.uva.nl, and p.f.mens@amc.uva.nl. Patrick Sawa, George Omweri, and Nicodemus Makio, International Centre of Insect Physiology and Ecology, Mbita Point, Kenya, E-mails: psawa@icipe.org, gomweri@icipe.org, and nmakio@icipe.org. Victor Osoti, KEMRI-Wellcome Trust Research Programme, Kilifi, Kenya, E-mail: vosoti@kemri-wellcome.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Ashley EA et al. Tracking Resistance to Artemisinin Collaboration (TRAC), 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371: 411–423.
-
2.
Fairhurst RM, Dondorp AM, 2016. Artemisinin-resistant Plasmodium falciparum malaria. Microbiol Spectr 4: EI10-0013-2016.
-
3.
Dondorp AM et al. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361: 455–467.
-
4.
Muwanguzi J, Henriques G, Sawa P, Bousema T, Sutherland CJ, 2016. Lack of K13 mutations in Plasmodium falciparum persisting after artemisinin combination therapy treatment of Kenyan children. Malar J 15: 36.
-
5.
Escobar C, Pateira S, Lobo E, Lobo L, Teodosio R, Dias F, Fernandes N, Arez AP, Varandas L, Nogueira F, 2015. Polymorphisms in Plasmodium falciparum K13-propeller in Angola and Mozambique after the introduction of the ACTs. PLoS One 10: e0119215.
-
6.
Isozumi R, Uemura H, Kimata I, Ichinose Y, Logedi J, Omar AH, Kaneko A, 2015. Novel mutations in K13 propeller gene of artemisinin-resistant Plasmodium falciparum. Emerg Infect Dis 21: 490–492.
-
7.
Kamau E et al. 2015. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. J Infect Dis 211: 1352–1355.
-
8.
Taylor SM et al. 2015. Absence of putative artemisinin resistance mutations among Plasmodium falciparum in sub-Saharan Africa: a molecular epidemiologic study. J Infect Dis 211: 680–688.
-
9.
Borrmann S et al. 2011. Declining responsiveness of Plasmodium falciparum infections to artemisinin-based combination treatments on the Kenyan Coast. PLoS One 6: e26005.
-
10.
Gadalla NB et al. 2011. Increased pfmdr1 copy number and sequence polymorphisms in Plasmodium falciparum isolates from Sudanese malaria patients treated with artemether-lumefantrine. Antimicrob Agents Chemother 55: 5408–5411.
-
11.
Chang HH et al. 2016. Persistence of Plasmodium falciparum parasitemia after artemisinin combination therapy: evidence from a randomized trial in Uganda. Sci Rep 6: 26330.
-
12.
Betson M, Sousa-Figueiredo JC, Atuhaire A, Arinaitwe M, Adriko M, Mwesigwa G, Nabonge J, Kabatereine NB, Sutherland CJ, Stothard JR, 2014. Detection of persistent Plasmodium spp. infections in Ugandan children after artemether-lumefantrine treatment. Parasitology 141: 1880–1890.
-
13.
Beshir KB et al. 2013. Residual Plasmodium falciparum parasitemia in kenyan children after artemisinin-combination therapy is associated with increased transmission to mosquitoes and parasite recurrence. J Infect Dis 208: 2017–2024.
-
14.
Duparc S, Borghini-fuhrer I, Craft JC, Arbe-barnes S, Miller RM, Shin C, Fleckenstein L, 2013. Safety and efficacy of pyronaridine-artesunate in uncomplicated acute malaria: an integrated analysis of individual patient data from six randomized clinical trials. Malar J 12: 70.
-
15.
Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH, 2007. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg 77: 119–127.
-
16.
Moody A, 2002. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 15: 66–78.
-
17.
Murray CK, Gasser RA, Magill AJ, Miller RS, 2008. Update on rapid diagnostic testing for malaria. Clin Microbiol Rev 21: 97–110.
-
18.
Omar SA, Mens PF, Schoone GJ, Yusuf A, Mwangi J, Kaniaru S, Omer GAA, Schallig HDFH, 2005. Plasmodium falciparum: evaluation of a quantitative nucleic acid sequence-based amplification assay to predict the outcome of sulfadoxine–pyrimethamine treatment of uncomplicated malaria. Exp Parasitol 110: 73–79.
-
19.
Vasoo S, Pritt BS, 2013. Molecular diagnostics and parasitic disease. Clin Lab Med 33: 461–503.
-
20.
Mens P et al. 2012. Direct blood PCR in combination with nucleic acid lateral flow immunoassay for detection of Plasmodium species in settings where malaria is endemic. J Clin Microbiol 50: 3520–3525.
-
21.
Roth JM, de Bes L, Sawa P, Omweri G, Osoti V, Oberheitmann B, Schallig HDFH, Mens PF, 2018. Plasmodium detection and differentiation by direct-on-blood PCR nucleic acid lateral flow immunoassay. J Mol Diagn 20: 78–86.
-
22.
World Health Organization, 2009. Methods for Surveillance of Antimalarial Drug Efficacy. Geneva, Switzerland: WHO. Available at: http://www.who.int/malaria/publications/atoz/9789241597531/en/. Accessed December 19, 2017.
-
23.
World Health Organization, 2010. Basic Malaria Microscopy—Part I: Learner’s Guide, 2nd edition. Geneva, Switzerland: WHO.
-
24.
Snounou G, 2002. Genotyping of Plasmodium spp. nested PCR. Methods Mol Med 72: 103–116.
-
25.
World Health Organization, 2007. Methods and Techniques for Clinical Trials on Antimalarial Drug Efficacy: Genotyping to Identify Parasite Populations. Geneva, Switzerland: WHO. Available at: http://www.who.int/malaria/publications/atoz/9789241596305/en/. Accessed December 19, 2017.
-
26.
Kattenberg JH, Tahita CM, Versteeg IAJ, Tinto H, Traore-Coulibaly M, Schallig HDFH, Mens PF, 2012. Antigen persistence of rapid diagnostic tests in pregnant women in Nanoro, Burkina Faso, and the implications for the diagnosis of malaria in pregnancy. Trop Med Int Health 17: 550–557.
-
27.
Hermsen CC, Telgt DSC, Linders EHP, Van De Locht LATF, Eling WMC, Mensink EJBM, Sauerwein RW, 2001. Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol 118: 247–251.
-
28.
Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, Lavstsen T, 2009. The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int 58: 478–480.
-
29.
Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, Eling W, Sauerwein R, 2004. Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol 137: 35–41.
-
30.
White NJ, 1997. Assessment of the pharmacodynamic properties of antimalarial drugs in vivo. Antimicrob Agents Chemother 41: 1413–1422.
-
31.
Beshir KB, Hallett RL, Eziefula AC, Bailey R, Watson J, Wright SG, Chiodini PL, Polley SD, Sutherland CJ, 2010. Measuring the efficacy of anti-malarial drugs in vivo: quantitative PCR measurement of parasite clearance. Malar J 9: 312.
-
32.
Tshefu AK, Gaye O, Kayentao K, Thompson R, Bhatt KM, Sesay SSS, Bustos DG, Tjitra E, 2010. Efficacy and safety of a fixed-dose oral combination of pyronaridine-artesunate compared with artemether-lumefantrine in children and adults with uncomplicated Plasmodium falciparum malaria: a randomised non-inferiority trial. Lancet 375: 1457–1467.
-
33.
Kayentao K et al. 2012. Pyronaridine-artesunate granules versus artemether-lumefantrine crushed tablets in children with Plasmodium falciparum malaria: a randomized controlled trial. Malar J 11: 364.
-
34.
Méndez F, Muñoz Á, Carrasquilla G, Jurado D, Arévalo-Herrera M, Cortese JF, Plowe CV, 2002. Determinants of treatment response to sulfadoxine-pyrimethamine and subsequent transmission potential in falciparum malaria. Am J Epidemiol 156: 230–238.
-
35.
Carrara VI et al. 2009. Changes in the treatment responses to artesunate-mefloquine on the northwestern border of Thailand during 13 years of continuous deployment. PLoS One 4: e4551.
-
36.
Das D, Price RN, Bethell D, Guerin PJ, Stepniewska K, 2013. Early parasitological response following artemisinin-containing regimens: a critical review of the literature. Malar J 12: 125.
-
37.
Stepniewska K et al. 2010. In vivo parasitological measures of artemisinin susceptibility. J Infect Dis 201: 570–579.
-
38.
Vijaykadga S, Alker AP, Satimai W, MacArthur JR, Meshnick SR, Wongsrichanalai C, 2012. Delayed Plasmodium falciparum clearance following artesunate-mefloquine combination therapy in Thailand, 1997–2007. Malar J 11: 296.
-
39.
Greenhouse B, Dokomajilar C, Hubbard A, Rosenthal PJ, Dorsey G, 2007. Impact of transmission intensity on the accuracy of genotyping to distinguish recrudescence from new infection in antimalarial clinical trials. Antimicrob Agents Chemother 51: 3096–3103.
-
40.
Lo E, Nguyen J, Oo W, Hemming-Schroeder E, Zhou G, Yang Z, Cui L, Yan G, 2016. Examining Plasmodium falciparum and P. vivax clearance subsequent to antimalarial drug treatment in the Myanmar-China border area based on quantitative real-time polymerase chain reaction. BMC Infect Dis 16: 154.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1174 | 934 | 92 |
| Full Text Views | 692 | 20 | 1 |
| PDF Downloads | 249 | 17 | 0 |