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we examined parasite clearance kinetics and sequenced the parasite k13 gene in a cohort of 78 children with severe malaria ( including 8 children who died ) from the placebo group ( being treated with artesunate alone ) of a randomized , controlled trial conducted at the jinja regional referral hospital , uganda , during july 12 , 2011june 14 , 2013 ( 11 ) .
the median age of patients was 2.0 years ( range 1.08.0 years ) , and 38 ( 49% ) were female .
all patients were treated intravenously with artesunate ( guilin pharmaceutical , shanghai , china ) prequalified by the world health organization and according to the organization s guidelines ( 12 ) .
giemsa - stained peripheral blood smears ( thin and thick ) were assessed for quantitative malaria parasite density by light microscopy at a quality - controlled central research laboratory , the makerere university  johns hopkins university research collaboration core laboratory , which is certified by the college of american pathologists . for each patient , 5 serial parasite densities were measured according to the following sampling schedule : 1 ) admission ; 2 ) 12 hours later ; 3 ) morning of the second day of admission ; 4 ) morning of the third day of admission ; and 5 ) morning of the fourth day of admission . to measure parasite clearance kinetics , we used a standardized tool , the parasite clearance estimator , which expresses parasite clearance as the parasite s half - life ( t1/2 ) , which was calculated by using the slope of the linear portion of the curve of log - transformed parasite densities over time ( 13 ) .
in addition , we computed the parasite clearance time , defined as the interval between the start of treatment and the first of 2 sequential negative peripheral blood films ( 14 ) . to determine molecular markers of resistance , we amplified and sequenced the pf3d7_1343700 gene by using the nested pcr method , as described ( 3 ) , with some modifications .
dna was extracted from cryopreserved erythrocyte fractions by using qiagen columns ( qiagen , valencia , ca , usa ) according to the manufacturer s instructions .
the k13-propeller domain was amplified by using k13 - 1 5-cggagtgaccaaatctggga-3 and 5-k13 - 4 gggaatctggtggtaacagc-3 for the primary pcr and k13 - 2 5-gccaagctgccattcatttg-3 and k13 - 3 5-gccttgttgaaagaagcaga-3 for the nested pcr .
dna sequencing of the 810-bp nested pcr product was performed to determine the amino acid haplotype of residues .
results were aligned to reference pf3d7 kelch protein , putative ( pf13_0238 ) mrna , complete coding sequence ( national center for biotechnology information reference sequence xm_001350122.1 ) .
we identified limited diversity within the k13 gene . for 16 loci tested ( amino acid positions 439 , 441 , 458 , 465 , 467 , 476 , 493 , 522 , 539 , 543 , 557 , 558 , 580 , 617 , 619 , and 637 )
we did not observe any of the most common amino acid substitutions in k13 associated with artemisinin resistance in p. falciparum isolates from cambodia ( c580y , r539 t or y493h ) ( 3 ) , nor the i543 t and n458y mutations most strongly associated with increased clearance t1/2 in another recent study ( 4 ) , nor the m476i mutation selected in vitro under artemisinin pressure ( 3 ) .
similarly , these point mutations were absent in isolates from senegal and uganda and in > 1,100 p. falciparum parasites from 14 sites across sub - saharan africa ( 810 ) . however
, a previously reported point mutation , a578s ( 9,15 ) , was found in 3 ( 3.8% ) of 78 infections .  
the table shows infections with a578s parasites compared with infections caused by wild - type parasites .
parasite clearance time was prolonged in infections with a578s mutant parasites , and a similar trend was observed for clearance t1/2 .
these 2 types of infections showed no differences in prior artemisinin exposure , number of deaths , or recrudescence or reinfection at day 14 from date of admission . * for 7 patients who died , parasite clearance time could not be calculated because of incomplete parasite clearance prior to death .
for these same 7 children , the parasite clearance half - time ( t1/2 ) could not be calculated because of insufficient data points . for 1 child who died , clearance of parasitemia before death
estimates of parasite clearance time and clearance t1/2 are based on the remaining 68 patients .
the role of the a578s amino acid substitution is unclear , but it occurs near the most common k13-propeller mutation ( c580y ) , which has been associated with delayed parasite clearance in southeast asia and with tolerance to artemisinin in vitro ( 3 ) .
computational modeling suggests that a578s should considerably affect the tertiary structure of the k13 protein , thereby destabilizing the domain scaffold and altering its function ( 15 ) .
isolates with a578s exhibited a phenotype of prolonged clearance under artesunate treatment in our study .
delayed clearance of a578s parasites was not observed in previous reports ( 4,9 ) , although the number of isolates in our study and in others was small . because multiple independent mutations in k13 have arisen in geographic regions engaged in intense treatment of malaria with artemisinin derivatives ( 7 ) and because only 2 point mutations were necessary to confer drug tolerance in vitro to a p. falciparum isolate from tanzania ( 3 ) , we are concerned that parasites with the a578s mutation are already causing severe malaria in children in uganda , although with low frequency .
the nonsynonymous snp a578s in the k13-propeller domain may represent another putative marker of delayed response to artesunate , although this indicator occurred infrequently in our cohort of children with severe malaria in uganda .
our study documents an association between a578s and prolonged parasite clearance time , a finding relevant for future monitoring of p. falciparum response to parenteral artesunate in children in africa .
plasmodium falciparum resistance to artemisinin derivatives is emerging in asia . 
 we examined molecular markers of resistance in 78 children in uganda who had severe malaria and were treated with intravenous artesunate . 
 we observed in the k13-propeller domain , a578s , a low - frequency ( 3/78 ) , nonsynonymous , single - nucleotide polymorphism associated with prolonged parasite clearance .