ANALYSIS OF PFCRT, PFMDR1, DHFR, AND DHPS MUTATIONS AND DRUG
SENSITIVITIES IN PLASMODIUM FALCIPARUM ISOLATES FROM PATIENTS IN
VIETNAM BEFORE AND AFTER TREATMENT WITH ARTEMISININ
THANH NGO, MANOJ DURAISINGH, MICHAEL REED, DAVID HIPGRAVE, BEVERLEY BIGGS, AND
ALAN F. COWMAN
Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia; University of Melbourne, Parkville; MacFarlane Burnet
Centre for Medical Research, Melbourne, Australia; National Institute of Malariology, Parasitology, and Entomology, Hanoi, Vietnam
Abstract. We have analyzed artemisinin sensitivity in Plasmodium falciparum isolates obtained from patients in
South Vietnam and show that artemisinin sensitivity does not differ before and after drug treatment. There was an
increase in the level of mefloquine resistance in the isolates after drug treatment that was concomitant with a decrease
in chloroquine resistance, suggesting that treatment with artemisinin has selected for increased mefloquine resistance.
Mutations in the pfmdr1 gene, previously shown to be associated with sensitivity to mefloquine, were selected against.
All isolates resistant to chloroquine encoded Thr-76 in the pfcrt gene consistent with an essential role in the mechanism
of chloroquine resistance. Mutations in pfmdr1 also were linked to chloroquine resistance. High levels of mutation in
dhfr and dhps genes, which have previously been associated with Fansidar resistance, also were found, suggesting that
this drug would not be useful for malaria control in this part of Vietnam.
INTRODUCTION
The development and spread of drug resistance in Plasmo-
dium falciparum is a major problem for the treatment and
control of malaria in many endemic countries. In Southeast
Asia, 21.9 million cases of malaria were reported in 1995
alone.
1
In Vietnam, chloroquine resistance was first reported
in 1961 and reached a peak in 1990, ranging in incidence from
60–80% in some regions.
2
Chloroquine resistance has now
spread to most regions of Vietnam where malaria is endemic
3
and has led to the widespread use of alternative antimalarial
drugs (mefloquine, halofantrine, artemisinin derivatives, and
pyrimethamine/sulfadoxine). Use of Fansidar (pyrimeth-
amine + sulfadoxine) has increased rapidly over the last 30
years.
4
As a consequence, reported levels of resistance to the
drug have increased from approximately 20% to over 80%.
5
Since 1991, artemisinin and its derivatives have been used to
treat malarial patients in Vietnam. These drugs have become
increasingly important as antimalarial therapy in this setting
because of their rapid mode of action and efficacy against
multidrug-resistant forms of P. falciparum malaria.
Resistance of P. falciparum to chloroquine has been asso-
ciated with lower drug accumulation.
6
Mutations in the pfcrt
gene have been strongly linked to the mechanism of chloro-
quine resistance.
7
The presence of Tyr-76 residue within the
Pfcrt protein is linked to chloroquine resistance, suggesting
that it plays an important role in the mechanism of resistance
to this antimalarial. Additionally, mutations within the pfmdr
1 gene have been shown to confer increased resistance to
chloroquine, suggesting that they play a role in modulating
higher levels of chloroquine resistance.
8,9
The same mutations
also have been shown to confer quinine resistance and alter
the level of resistance and sensitivity to mefloquine and arte-
misinin.
8
The combination of pyrimethamine and sulfadoxine was
effective when it was introduced in the late 1960s as a single-
dose treatment of acute P. falciparum malaria.
10,11
Over the
years, however, resistance to Fansidar has been reported,
mainly in areas of intense use, particularly areas of chloro-
quine resistance. Variant sequences of P. falciparum dihydro-
folate reductase (DHFR), the target enzyme of pyrimeth-
amine, were first described in 1988.
12,13
Resistance to pyri-
methamine has been shown to result from a mutation in the
DHFR enzyme, changing Ser-108 to Asn-108, and subsequent
mutations can greatly increase the level of resistance to this
drug.
14,15
Ten mutant genotypes for DHFR have been re-
ported from a large number of field samples.
4,16–18
Resistance
to sulfonamide and sulfones has been shown to result from
mutations within dihydropteroate synthetase (DHPS).
19,20–22
The amino acid changes at four positions (Ser-436, Gly-437,
Ala-581, and Ala-613) have been shown to confer resistance
to sulfadoxine and also cross-resistance to sulfones and sul-
fonamides.
21,22
Distribution of mutations in the dhfr and dhps
genes and their association with Fansidar resistance have
been assessed in different geographic areas, and it has been
found that a greater number of mutations in both dhfr and
dhps is a good predictor of likely drug failure.
4,17,18,23
Vietnam has well-developed systems for malaria surveil-
lance, with recent data showing that more than half the popu-
lation lives in forests and mountainous areas where they may
be at risk of malaria infection. Drug-resistant malaria has
been an increasing problem in the last two decades, and al-
though alternative drugs such as artemisinin and its deriva-
tives have become widely used as first-line therapy for ma-
laria, they have been associated with a high frequency of
recrudescence.
24
In this 1998 study, we have further catego-
rized malaria drug resistance in Vietnam by analyzing muta-
tions in the pfcrt, pfmdr1, dhfr, and dhps genes in P. falci-
parum primary and recrudescent isolates collected from pa-
tients in an area of Binh Phuoc Province highly endemic for
malaria.
MATERIALS AND METHODS
Study area and collection of blood samples. The subjects of
the study lived on the Phu Rieng rubber plantation in south-
ern Vietnam. The area is hyperendemic for malaria, which is
aggravated by multidrug-resistant P. falciparum. The peak
seasons of infection are March–June and September–
December (annual main peak of transmission). The annual
parasite rate/slide is 10–30% for both P. falciparum and P.
vivax.
Blood samples were collected from all P. falciparum-
positive cases before administering artemisinin (20 mg/kg on
Am. J. Trop. Med. Hyg., 68(3), 2003, pp. 350–356
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene
350