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Transactions of the Royal Society of Tropical Medicine and Hygiene (2008) 102, 699704

available at www.sciencedirect.com

journal homepage: www.elsevierhealth.com/journals/trst

Point-of-care testing for malaria outbreak


management
Ratnawati a, Mochammad Hatta b, Henk L. Smits c,
a

Department of Parasitology, Hasanuddin University, Makassar, Indonesia


Department of Medical Microbiology, Molecular Biology and Immunology Laboratory, Faculty of Medicine, Hasanuddin
University, Makassar, Indonesia
c
KIT Biomedical Research, Royal Tropical Institute/Koninklijk Instituut voor de Tropen (KIT), Meibergdreef 39, 1105 AZ
Amsterdam, The Netherlands
b

Received 24 October 2007; received in revised form 10 April 2008; accepted 10 April 2008
Available online 2 June 2008

KEYWORDS
Malaria;
Plasmodium
falciparum;
Plasmodium vivax;
Point of care;
Outbreak
management;
Indonesia

Summary A rapid antigen assay for malaria was performed on blood samples collected during
a simultaneous outbreak of falciparum malaria and vivax malaria on a remote island in the
Indonesian archipelago. During the outbreak, a total of 89 patients (4.3% of the population)
were diagnosed with malaria within a week. Microscopic examination revealed 78 malaria slidepositive cases, of whom 49 (62.8%) were identied as P. falciparum, 7 (9.0%) as P. vivax and
22 (28.2%) as mixed P. falciparum and P. vivax infections. The rapid malaria assay showed
excellent correlation with expert-conrmed routine microscopy for P. falciparum and P. vivax
monoinfections and mixed infections with a parasite density >50 parasites/l. Several slidenegative blood samples collected from febrile patients with clinical malaria tested positive in
the rapid test. The estimated sensitivity calculated for the rapid test (91.0%) was slightly higher
than that of microscopy (87.6%). The result indicates that rapid antigen detection for malaria
could be a useful alternative to microscopy to reduce the workload during emergency outbreak
situations.
2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene.

1. Introduction
Although simple and cheap, microscopic examination of
Giemsa-stained thick and thin lms for conrmation of
malaria parasites in the blood of a patient is time consum-

Corresponding author. Tel.: +31 20 566 5470;


fax: +31 20 697 1841.
E-mail address: h.smits@kit.nl (H.L. Smits)

ing and requires an experienced microscopist as well as a


well maintained and good quality microscope to achieve
good sensitivity. Several different antigen detection devices
for malaria have been developed as an alternative to
microscopy and these rapid tests have been promoted for
use in healthcare centres where microscopy is not available
(Moody, 2002). Several studies have examined the performance of these rapid assays under different epidemiological
conditions and in different countries, with some variation
in results (Murray et al., 2003). The consensus is that the
functioning of these rapid assays is acceptable, with a

0035-9203/$ see front matter 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene.
doi:10.1016/j.trstmh.2008.04.018

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700
sensitivity similar to or slightly lower than routine
microscopy. Microscopy is held to have a detection limit
of approximately 20 parasites/l (Jonkman et al., 1995). A
rapid test could also be very useful in the control of malaria
outbreaks when preparation and microscopic examination
of the increased number of blood lms becomes cumbersome. An outbreak of malaria occurred in March 2006 on
the remote Indonesian island of Sapuka Besar. We carried
out the rapid One-Step Malaria test to analyse blood samples
collected during the outbreak and compared the results with
expert-conrmed routine microscopy to see whether rapid
testing for malaria can provide a rapid and simple alternative to microscopy and thus be benecial during outbreak
situations.

2. Materials and methods


Sapuka Besar is 1 of 29 inhabited small islands of the Liukang
Tangaya archipelago belonging to the Pangkep district of
South Sulawesi Province and is located in the Flores Sea
259 km south of Makassar, the capital of South Sulawesi. The
archipelago is spread across two coral reefs and occupies
nearly 700 km2 . The island measures approximately 1 km2
and has a population of 2068 inhabitants living in 474 households. The Pangkep district includes part of the mainland
of South Sulawesi and the health service for the islands is
organised from there. Only two primary healthcare centres (Puskesmas) are located on the islands, one of them
at Sapuka Besar. At the time of the study, each of the
Puskesmas was staffed by a single nurse. The Puskesmas at
Sapuka Besar has very limited resources, including a microscope and tools for the preparation of Giemsa-stained blood
lms.
A malaria epidemic arose during a visit of a leprosy
research team to the island in March 2006. Assisted by the
research team, blood samples were collected from 89 febrile
patients presenting at the Puskesmas or identied during
home visits, all of whom were diagnosed with malaria. All
patients with 2 days of fever and/or u-like symptoms
were entered into the study. The 89 patients came from 81
households and were diagnosed over a period of 7 days. The
number of patients diagnosed with malaria during the outbreak amounted to 4.3% of the population of Sapuka Besar
and is approximately one-quarter of the total number of
cases recorded in 2006 and approximately one-half of the
number of cases recorded in the year preceding the outbreak. The average duration of fever at the time of diagnosis
was 3.6 days (range 26 days), the male to female ratio
was 0.9 and the average age of the patients was 25.7 years
(range 753 years). Giemsa slide-positive patients as well
as slide-negative patients diagnosed with malaria received
a standard daily dosage of chloroquine for 3 days. The nurse
at the Puskesmas is the only person on the island who has
a stock of antimalarials and none of the patients entered in
the study had been treated for malaria during the 2 months
preceding the outbreak.
Giemsa-stained thick and thin lms were prepared and
examined for the presence of parasites by an experienced
technician of the research team. The lms were labelled
and transported to Makassar were they were re-examined
by an experienced parasitologist. Parasite densities

Ratnawati et al.
were calculated after counting parasites in at least 100
windows as follows: total number of parasites/mm3
blood = 8000/(a b), where a = total number of leukocytes
counted by microscopy and b = total number of parasites
counted, with the assumption that 1 mm3 of blood corresponds to 8000 leukocytes. Blood samples treated with
heparin as anticoagulant were frozen immediately, stored
at 20 C and tested with the rapid One-Step Malaria test
(Arista Biologicals Inc., Allentown, PA, USA) approximately
1 year later. Frozen blood samples collected in March 2007
from 152 healthy individuals living on the island were also
tested. However, the latter samples were not examined by
microscopy as these samples had been collected for other
research purposes and slides had not been prepared.
The rapid One-Step Malaria test employs Plasmodium
falciparum-specic histidine-rich protein-2 (PfHRP-2) antigen for the identication of P. falciparum in the blood of
patients and a pan-malaria antigen, the plasmodium lactate
dehydrogenase (pLDH) antigen, for the detection of other
malaria species. The rapid One-Step Malaria test was performed by spotting 5 l of blood onto the sample pad of
the sample well of the plastic cassette. Next, two drops
of assay buffer were added into the developer well. Test
results were read after 10 min and 20 min and reported following the package insert guidelines as follows: staining of
the control line and the PfHRP-2 line indicates a positive
result for P. falciparum; staining of the control line and the
pLDH line indicates a positive result for P. vivax or other Plasmodium spp.; staining of all three lines indicates a positive
result for P. falciparum and for P. vivax or other Plasmodium spp.; and staining of the control line only indicates a
negative result. However, as P. falciparum expresses the
PfHRP-2 as well as the pLDH antigen, staining of all three
lines also could be interpreted as a positive result for a P.
falciparum monoinfection. The rapid test does not discriminate between any of the malaria species in the case of a test
result indicating a mixed infection and also does not identify malaria species in the case of a test result indicating
a non-falciparum malaria infection (Moody, 2002; Murray et
al., 2003). The package label indicated a residual shelf-life
at 230 C of 1 year and hence storage under hot tropical
conditions may require special care.
Permission for the study was obtained from the leader of
the island, and oral informed consent was obtained from all
patients, their parents or family to take blood for examination for infectious diseases.

3. Results
Microscopy revealed 78 Giemsa lm-positive cases of
malaria, of which 49 (62.8%) were identied as P. falciparum, 7 (9.0%) as P. vivax and 22 (28.2%) as mixed infections
of P. falciparum and P. vivax (Table 1). Plasmodium malariae
and P. ovale were not observed. In addition, 11 patients were
diagnosed with malaria based on clinical signs and symptoms
and response to treatment. The sensitivity of microscopy
was estimated to be 87.6% (95% CI 7989%). Re-examination
by an expert parasitologist conrmed the original ndings. The median parasite density was 346 parasites/l
(range 168765 parasites/l) and was similar for falciparum monoinfections (median 503 parasites/l; range

Author's personal copy

0
9
142

0
3
0
22
1
1
7
0
8
39
0
0
2
6
0
0

Mixed or falciparum only


Non-falciparum
Falciparum
Negative

No. of samples with the following test result in the One-Step Malaria cassette

701
168765 parasites/l), vivax monoinfections (median 427
parasites/l; range 56598 parasites/l) and mixed infections (median 398 parasites/l; range 766780 parasites/
l). Notably, very high parasite densities were not observed
among the vivax malaria monoinfections.
The rapid test gave a positive result for blood samples from 43 (87.8%) of the patients with a P. falciparum
monoinfection, 7 (100%) with a P. vivax monoinfection and
22 (100%) with a mixed infection. Furthermore, the rapid
test showed a positive result for 9 (81.8%) microscopically negative patients diagnosed with malaria. Combined,
the rapid test presented a positive result for 81 (91.0%;
95% CI 8396%) of the total group of Giemsa slide-positive
and -negative malaria patients. All samples collected from
the patients with a monoinfection of P. falciparum that
tested negative in the rapid test had a parasite density
<50 parasites/l. However, several other samples with a
parasite count just above the threshold value tested positive.
The rapid test correctly identied the infecting species
in 39 (90.7%) of the lm-positive samples with a falciparum
monoinfection. In three other falciparum monoinfections
the result of the rapid test indicated a mixed or P.
falciparum-only infection and in a single case the rapid
test result revealed a monoinfection with a non-falciparum
malaria species. The result of the rapid test was consistent
with a mixed infection in all patients with a microscopically
determined mixed infection of P. falciparum and P. vivax,
and the result of the rapid test conrmed infection with
non-falciparum malaria in all cases of P. vivax malaria.
Ten samples (6.6%) from the healthy individuals tested
positive in the rapid test, nine of them with a rapid test
result indicating a falciparum monoinfection and one with a
rapid test result denoting a non-falciparum monoinfection.
Compared with microscopy the rapid test was very easy
to perform without any signicant amount of training; whilst
microscopy required at least 90 min to collect the blood
sample and to prepare, stain and read the lms with approximately 45 min hands-on time in total, the result of the rapid
test could be reported within 25 min with no more than
10 min hands-on time.

Healthy
Not performed (152)

Malaria patients
Negative (11)
Plasmodium falciparum (49; 503, 168765)
Plasmodium vivax (7; 427, 56598)
Mixed P. falciparum/P. vivax (22; 398, 766780)

4. Discussion
Malaria species according to Giemsa-stained lm
(no. of samples; median parasite count, range)

Table 1

Detection and species identication of malaria parasites by a rapid blood test and comparison with microscopy during an outbreak and in healthy individuals

Point-of-care testing for malaria outbreak management

The One-Step Malaria test closely matched microscopy


for lm-positive samples with a parasite density
>50 parasites/l for P. falciparum and P. vivax and correctly
discriminated between almost all P. falciparum and P. vivax
monoinfections and mixed infections. We estimated the
sensitivity of the rapid test to be 91.0%, which is slightly
higher than the 87.6% sensitivity calculated for microscopy
and is consistent with earlier studies generally indicating
a sensitivity of >90% for rapid antigen detection tests at
parasite densities >100500 parasites/l. The observed
lack of reactivity for the samples with a parasite density
<50 parasites/l is consistent with the notion that at low
parasite densities the rapid tests are more likely to fail
(Murray et al., 2003). However, the ability to obtain test
results rapidly and to screen many patients in a relatively
small timespan recommends the rapid test for screening
patients during outbreaks.

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702
Two published studies have eld-investigated a rapid
antigen test for malaria in Indonesia (Fryauff et al., 2000;
Tjitra et al., 1999). In the study by Tjitra et al. (1999) the
immunochromatographic ICT Malaria Pf/Pv test was analysed in a eld study performed in a primary healthcare centre in West Sumba, East Nusa Tenggara Province in Eastern
Indonesia, and in the study by Fryauff et al. (2000) the OptiMAL assay was applied for screening asymptomatic residents
from Armopa on the northeast coast of Irian Jaya. The study
by Tjitra et al. (1999) showed a sensitivity of 96% and a specicity of 90% for the diagnosis of falciparum malaria in the ICT
test and a sensitivity of 75% and a specicity of 95% for the
diagnosis of vivax malaria. The sensitivity of the ICT test was
especially low for vivax malaria parasitaemia with a parasite density <500 parasites/l. A similar result was obtained
in the study by Fryauff et al. (2000). We did not observe
a difference in detection level for the two malaria species
despite the fact that all but one of the P. vivax monoinfections had a parasite density <500 parasites/l. The ICT
test utilises the same antigen as the One-Step Malaria test
to target P. falciparum but employs the aldolase protein as
a pan-specic antigen (Coleman et al., 2002; Singh et al.,
2000). The OptiMAL assay is based on the detection of a P.
falciparum-specic pLDH antigen for the identication of P.
falciparum and, like the One-Step Malaria test, uses a panspecic pLDH antigen for the other malaria species (Forney
et al., 2003; Palmer et al., 1998; Pattanasin et al., 2003).
Such differences in assay design may contribute to a difference in detection level. Despite the lack of sensitivity for
vivax malaria, the authors of these two studies have indicated that these rapid tests are useful tools for diagnosing
malaria in Indonesia but commented that they are relatively
expensive.
Several individuals who participated in our study and
had negative lms tested positive in the rapid test. Whilst
microscopy provides direct evidence for the presence of
the parasite in the blood, the rapid tests provide indirect
evidence and could be detecting residual antigen persisting after treatment of a previous infection or reecting the
presence of gametocytes (Bell et al., 2005; Moody, 2002;
Singh et al., 2005; Tjitra et al., 2001). However, examination of the medical records indicated that these individuals
had not been treated for malaria recently and hence we
assume that they had a current infection at the time of the
outbreak.
Plasmodium falciparum and P. vivax are the most common species in Indonesia but P. malariae and P. ovale have
also been reported occasionally (Anthony et al., 1992; Baird
et al., 1990, 1997; Bangs et al., 1992, 1996; Bragonier et
al., 2002; Gundelnger, 1975; Joesoef and Dennis, 1980;
Maguire et al., 2002; Pribadi et al., 1998; Purnomo et al.,
1999; Syafruddin et al., 2006). However, P. malariae and
P. ovale infections were not observed during the outbreak.
Rapid testing allows correct identication of the parasite
in the case of falciparum malaria but does not discriminate between the infecting species in the case of mixed
infection or non-falciparum malaria (Moody, 2002; Murray et
al., 2003). However, as drug resistance is not a problem in
Indonesia and as in general all uncomplicated malaria cases
receive the same standard treatment, knowledge of the
infecting species is not an absolute requirement (Syafruddin
et al., 2005; Tjaniadi et al., 2003). Microscopy also has the

Ratnawati et al.
advantage of providing accurate estimates of parasite densities, which could be important in identifying and monitoring
cases at risk of severe malaria (Bejon et al., 2007; Idro et
al., 2004, 2006).
The outbreak at Sapuka Besar was characterised by a
high percentage of mixed infections. During other outbreak
investigations in different parts of Indonesia, P. falciparum
was the dominant infection (Maguire et al., 2005; Mueller
et al., 2005). To explain the difference in the epidemiology
of P. falciparum and P. vivax in a native population from the
Amazon, it was postulated that an epidemic pattern of P.
falciparum infection could reect the introduction of a new
strain either by a visitor or by a resident who had picked
up the infection elsewhere, whilst an endemic pattern of
P. vivax may well reect the capability of this species to
relapse (Laserson et al., 1999). Fishermen from the Liukang
Tangaya archipelago occasionally visit other islands in the
Flores Sea or travel to the mainland of Sulawesi to gather
supplies and on such an occasion one of them may well have
become infected. The high percentage of mixed infections
appears unusual and raises the question whether they were
perhaps introduced by a person who had picked up a mixed
infection elsewhere.
The use of a rapid test may help to reduce the work load
and facilitated the management of the malaria outbreak.
However, it should be taken into account that to make effective use of a rapid test the healthcare centre would need to
be well stocked with the test devices. This may be crucial as,
for instance, Sapuka Besar can only be reached by boat and
a one-way trip takes approximately 40 h to reach Makassar,
the nearest place where medical supplies can be obtained.
It may be admitted, however, that the logistic situation in
the Liukang Tangaya archipelago is exceptional and that it
will be easier to keep stock or to call in assistance in other
parts of Indonesia.
We conclude that in Indonesia the One-Step Malaria test,
because of its favourable assay characteristics combined
with its user friendliness, could be highly benecial in outbreak situations. None the less, application of rapid tests for
emergency examination involves complex logistics to keep
sufcient supplies in stock. Other issues that may need to
be addressed before introduction of rapid testing are test
performance in routine clinical practice and cost effectiveness. In most studies evaluating rapid tests, testing was
performed by experienced research staff and results may
be less favourable if performed during routine clinical practice (Jelinek et al., 1999; Wiese et al., 2006). The cost
effectiveness of rapid testing was addressed in a study performed in sub-Saharan Africa (Rolland et al., 2006) but the
costbenet balance is likely to be different for the malaria,
healthcare and economic situation in Indonesia.
Authors contributions: MH and HLS designed the study
protocol; MH carried out the clinical assessment; R and MH
performed the parasite determinations, and analysis and
interpretation of these data; HLS drafted the manuscript.
All authors read and approved the nal manuscript. MH and
HLS are guarantors of the paper.
Acknowledgements: The authors appreciate the donation
of the One-Step Malaria test by Arista Biologicals Inc., PA,

Author's personal copy


Point-of-care testing for malaria outbreak management
USA. They also thank Coosje Tuijn for critical reading of the
manuscript, and Dr H.M. Noor, Head of the Pangkep Health
District Pangkep, for permission and active support. The
dedicated technical support of Mr Saeni and Mr Arif of the
P2M laboratory of Pangkep, and of Mr Romi Usman, Mr Marwani, Mr Syafri, Mrs Asni, Mrs Christina and Mr Mus Jebaru
of the Hasanuddin University, Makassar, Indonesia, is greatly
appreciated. Furthermore, the authors are grateful to Hj.
Rabiah, Head of the Primary Health Centre (Puskesmas)
Liukang Tangaya Pangkep, for hospitality and support during their stay at Sapuka Besar. They also wish to thank all
the inhabitants of the island for their kind co-operation.
Funding: None.
Conicts of interest: None declared.
Ethical approval: Medical Ethical Committee of the
Hasanuddin University, Makassar, Indonesia (ref. no. 21/PenEthic-Clear/2005).

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