CORRESPONDENCE • CID 2019:69 (15 October) • 1463
suggested, we admit that it is the way sci-
ence perpetuates itself. Given the present
situation and information, we do not see
any justification to reinterpret our data.
We sincerely hope that our responses
reassure the readership of the validity and
robustness of the evidence regarding ar-
temisinin resistance.
Note
Potential conflicts of interest. All authors:
No reported conflicts of interest. All authors
have submitted the ICMJE Form for Disclosure
of Potential Conflicts of Interest. Conflicts that
the editors consider relevant to the content of the
manuscript have been disclosed.
Sabyasachi Das,
1
Bhaskar Saha,
2
Amiya Kumar Hati,
3
and Somenath Roy
1
1
Immunology and Microbiology Laboratory, Department
of Human Physiology with Community Health, Vidyasagar
University, Midnapore, West Bengal,
2
National Centre for
Cell Science, Ganeshkhind, Pune, and
3
Calcutta School of
Tropical Medicine, Kolkata, West Bengal, India
References
1. Das S, Saha B, Hati AK, Roy S. Evidence of arte-
misinin-resistant Plasmodium falciparum malaria
in Eastern India. N Engl J Med 2018; 379:1962–4.
2. Global Malaria Programme. Artemisinin and
artemisinin-based combination therapy resistance.
(WHO) Status report, October 2016. Available
at: https://apps.who.int/iris/bitstream/handle/
10665/250294/WHO-HTM-GMP-2016.11-
eng.pdf;jsessionid=2F5FD02CBA6BDD0D-
55E11F252B58691B?sequence=1
3. WWARN K13 Genotype-Phenotype Study Group.
Association of mutations in the Plasmodium fal-
ciparum Kelch13 gene (Pf3D7_1343700) with
parasite clearance rates after artemisinin-based
treatments a WWARN individual patient data
meta-analysis. BMC Med 2019; 17:1. doi:10.1186/
s12916-018-1207-3
4. World Health Organization. Artemisinin resistance
and artemisinin-based combination therapy effi-
cacy: Status report, August 2018. Geneva: World
Health Organization, 2018. Available at: http://
apps.who.int/iris/bitstream/handle/10665/274362/
WHO-CDS-GMP-2018.18-eng.pdf?ua=1.
5. Das S, Manna S, Saha B, Hati AK, Roy S. Novel
pfkelch13 gene polymorphism associates with arte-
misinin resistance in eastern India. Clin Infect Dis
2018. doi: 10.1093/cid/ciy1038.
6. Phyo AP, Nkhoma S, Stepniewska K, et al.
Emergence of artemisinin-resistant malaria on the
western border of Thailand: a longitudinal study.
Lancet 2012; 379:1960–6.
7. Ahmed A, Lumb V, Das MK, Dev V, Wajihullah,
Sharma YD. Prevalence of mutations associated
with higher levels of sulfadoxine-pyrimethamine
resistance in Plasmodium falciparum isolates from
Car Nicobar Island and Assam, India. Antimicrob
Agents Chemother 2006; 50:3934–8.
8. Das S, Chakraborty SP, Tripathy S, Hati A, Roy S.
Novel quadruple mutations in dihydropteroate
synthase genes of Plasmodium falciparum in
West Bengal, India. Trop Med Int Health 2012;
17:1329–34.
9. Das MK, Lumb V, Mittra P, Singh SS, Dash AP,
Sharma YD. High chloroquine treatment failure
rates and predominance of mutant genotypes as-
sociated with chloroquine and antifolate resistance
among falciparum malaria patients from the island
of Car Nicobar, India. J Antimicrob Chemother
2010; 65:1258–61.
Correspondence: S. Roy, Vidyasagar University, Midnapore,
West Bengal, India (roysomenath@hotmail.com).
Clinical Infectious Diseases
®
2019;69(8):1462–3
© The Author(s) 2019. Published by Oxford University Press for
the Infectious Diseases Society of America. All rights reserved.
For permissions, e-mail: journals.permissions@oup.com.
DOI: 10.1093/cid/ciz167
Ultralow-density Plasmodium
falciparum Infections in African
Settings
To the Editor—As countries accelerate
towards elimination, an increasing pro-
portion of infections may be of low par-
asite densities. In a recent report, Girma
and colleagues [1] deployed ultrasensitive
diagnostics to characterize asymptomatic
infections in Ethiopia. The Plasmodium
falciparum prevalence was 1.3% by mi-
croscopy, 3.6% by conventional rapid
diagnostic tests (RDT), 8.5% by ultrasen-
sitive Alere RDT, 22.2% by loop-medi-
ated isothermal amplification and 21.5%
by ultrasensitive quantitative reverse
transcription-polymerase chain reaction
(qRT-PCR). These findings are in line
with a growing body of evidence demon-
strating the superiority of ultrasensitive
diagnostics in detecting low-density infec-
tions, when compared to microscopy and
standard RDTs [2]. The reported qRT-PCR
prevalence is considerably higher than
prevalence estimates from a meta-analy-
sis tool that relates microscopy and PCR
prevalence data from population sur-
veys [3]. Based on the meta-analysis, one
would expect a P. falciparum PCR preva-
lence in the range of 2.9% to 10.6%. The
higher prevalence in the study by Girma
and colleagues [1] may be explained by
their approach to targeting highly abun-
dant RNA targets instead of DNA targets.
Their finding thus suggests that there may
be a reservoir of infections that is too low
to be detected by conventional diagnostics
or even conventional PCR [4]. Our own
findings, from cross-sectional surveys in
pre-elimination settings of South Africa,
are in line with the findings of Girma and
colleagues [1], in the sense that we also
detected infections with ultralow parasite
densities, below the limit of detection of
conventional PCR. Our study observed
no RDT-positive infections or 18S nest-
ed-PCR–positive infections among 1475
individuals, whilst 3.9% of the study pop-
ulation was positive for P. falciparum par-
asites by sensitive, telomere-associated
repetitive element 2–based quantitative
PCR (qPCR), sometimes with genetically
complex infections (Table 1).
e real challenge of the study by
Girma and colleagues [1], as well as of
our own work, lies in the interpretation
of such parasite survey data in relation
to transmission patterns, particularly in
low-transmission settings. Ethiopia and
South Africa have both set targets for
malaria elimination. It is unclear to what
extent the presence of ultralow-density
infections may challenge these ambi-
tions. e authors correctly point out the
Table 1. Plasmodium falciparum Infection and Multiplicity of Infection Outcomes in South Africa
Local Subjects Migrant Subjects
RDTs (First Response Malaria) 0 (0/933) 0 (0/542)
18S rRNA PCR 0 (0/933) 0 (0/542)
TARE-2 qPCR % (n/N) 2.6% (24/993) 6.1% (33/542)
Mean multiplicity of infections (range) 1.8 (1–3) 2.8 (1–5)
Subjects were recruited in 2 community-wide, cross-sectional surveys among asymptomatic participants in 2014 and 2015.
The 18S rRNA PCR [5], TARE-2 qPCR [6], and multiplicity of infections [7] were based on established protocols, using 4.2 µL
of blood from filter paper bloodspots. Abbreviation: PCR, polymerase chain reaction; RDT, rapid diagnostic tests; rRNA, ribo-
somal RNA; TARE-2 qPCR, telomere-associated repetitive element-2 quantitative PCR.
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