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A First Case of Plasmodium knowlesi Malaria in Phramongkutklao Hospital:- Traipattanakul
J, et al. REPORT 91
CASE
Vol. 31 No. 2
A First Case of Plasmodium knowlesi Malaria in
Phramongkutklao Hospital
Jantima Traipattanakul, M.D., Dhitiwat Changpradub, M.D., Kitti Trakulhun, M.D.,
Danabhand Phiboonbanakit, M.D., Ph.D., Mathirut Mungthin, M.D., Ph.D.
Division of Infectious Disease, Department of Medicine, Phramongkutklao Hospital, Bangkok, Thailand.
ABSTRACT
Plasmodium knowlesi, the latest human malaria parasite, and it was identified a zoonosis. Naturally acquired
human infections are extremely rare in Thailand. We described a 62-year-old woman who presented with
daily fever and shaking chills, after Whipple operation was performed and a packed red cell transfusion was
given. A thin blood smear revealed 0.5% parasitemia with a morphologic appearance suggestive of Plasmodium
malariae infection. Direct nested polymerase chain reaction (PCR) assay enabled detection of Plasmodium
knowlesi from blood sample. She was the first case of probable blood transfusion-transmitted P. knowlesi
malaria in Phramongkutklao Hospital. (J Infect Dis Antimicrob Agents 2014;31:91-100.)
INTRODUCTION
experimentally demonstrated the transmission of
Plasmodium knowlesi, the latest human malaria
the parasite to humans.25 Afterwards, many studies
parasite, was identified a zoonosis. First described,
revealed that the parasite is naturally transmitted to
in 1927, in a long-tailed macaque (crab-eating
humans only by the Anopheles leucosphyrus group
macaque, Macaca fascicularis). 1-5 It primarily
of mosquitoes, all of which essentially are forest
causes chronic harmless infection in the long-
dwellers.2,11,26-31 It feeds on humans and nonhuman
tailed macaques (Macaca fascicularis)2-7, pig-tailed
primates and has the ability to transmit P. knowlesi.
macaques (Macaca nemestrina) and leaf monkeys
In conclusion, humans could be infected when they
(langur, Presbytis melalophos).9,10 These natural
are in the areas where specific vectors and primates
hosts, serve as reservoirs of P. knowlesi, live in the
reside.32
8
Central Thailand, the lower part of the Northeastern
Thailand and the Southern Thailand regions.
In 1965, the first natural infection of P. knowlesi
11-20
in humans was reported in an American military
Nevertheless, P. knowlesi causes fatal infection in
veteran returning from Peninsular Malaysia. 33
Rhesus macaques (Macaca mulatta), first discoverd
Naturally acquired human infect ions were
by laboratory experiment.21,22 Their habitats are the
thought to be extremely rare until a large number
rest of the country.
of human infections were reported in 2000 in
23,24
In 1932, Robert Knowles and Biraj Das Gupta
Kapit Division of Sarawak, Malaysian Borneo.
Keywords: Plasmodium knowlesi, malaria, zoonosis, blood transfusion-transmitted infection, Thailand
Corresponding author: Jantima Traipattankul, M.D., Division of Infectious Disease, Department of Medicine, Phramongkutklao Hospital, Bangkok 10400,
Thailand.
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May-August 2014
Nested PCR assey showed that 120 (57.7%) malaria
rigors, headaches, myalgia/arthralgia, malaise, and
cases were infected with P. knowlesi. They were
poor appetite.47 Cough (48%-56%), abdominal
first misdiagnosed as Plasmodium malariae on blood
pain (31%-52%), and diarrhea (18%- 29%) were
smears.34-38
additional symptoms noted in prospective
In 2004, P. knowlesi malaria was first described
studies of 107 and 130 patients, respectively.48,49
in a Thai patient who lived in a suburb of Bangkok
Gastrointestinal symptoms were predominant
and had visited Prajuab Khiri Khan Province,
features in fatal cases. 35 P. knowlesi can cause
Southern Thailand near the Myanmar border.12
severe infection resulting in fatal complications due
Subsequently, in 2006, 2007, 2008, 2009, 2010 and
to hyperparasitemia. Microcirculatory studies in
2011 incidence rates of malaria infection were 46.25,
Rhesus monkeys22 and post mortem findings for a
49.80, 45.72, 36.61, 40.25 and 33.01 cases per
patient in Sabah50 showed sludging of pigmented
100,000 persons per year, respectively. 39-44 A
parasitized red blood cells in the capillaries of
molecular-base survey during 2006-2007 reported
brain, heart and kidneys. A formerly healthy
10 (0.6%) cases of P. knowlesi from 1,751 malaria
patient who lived in Sabah presented with more
In 2008-2009, molecular-based
than 10% parasitemia, shock and multi-organ
survey of malaria in Thailand had been performed
failure. However, microscopic pathology failed to
again, it still demonstrated low prevalence of P.
demonstrate the possibility of sequestration
knowlesi. There were 23 (0.68%) cases of P. knowlesi
because brain sections were negative for
Recent
intracellular adhesion molecule-1(ICAM-1).35,47,50,51
molecular-based survey in natural hosts showed that
Historically, serial passage of P. knowlesi in
prevalence among maques in Thailand seems to be
humans has resulted in increasingly higher parasite
lower than in Kapit Division of Sarawak. Prevalence
counts, until they reached life-threatening level.52,53
of P. knowlesi among long-tailed and pig-tailed
Most P. knowlesi infections have been identified
macaques were 5.6% and 2.3% in Thailand. On the
as P. malariae infection in routine diagnostic
other hand, the prevalences were 87% and 50% in
laboratories because their trophozoites appear as
Kapit Division of Sarawak, respectively.
“band form”. Careful examination of well-stained
infected patients.
13
from 3,770 malaria infected patients.
14
4,14,17,45
The prepatent (incubation) period in humans
slides shows minor differences in morphology
from experimental infection by sporozoites is
such as early trophozoites of P. knowlesi with
approximately 9-12 days (replicate 24-hours
double-chromat in dots, mult iple infect ion,
Several
and mature schizontes of P. knowlesi containing
experimental studies in human revealed that P.
numerous merozoites. Schizontes of P. knowlesi
knowlesi or the other species of simian malaria
contain 16 merozointes while P. malariae have 6-12
infection were characterized by only a few days or
merozointes. 47,54 P. knowlesi infection usually
weeks of high fever, and clinically mild and low
presents with more than 500 parasitemia/mcL of
parasitemia. Some infected volunteers were self-
blood (0.1%-0.25% of erythrocytes).48
erythrocytic cycle, without hypnozoites).
30
limited.2,32,46 But many natural infections were
P. knowlesi malaria might progress rapidly to
recently reporting typical symptoms similar to other
a severe disease, and all cases need appropriate
types of malaria with quotidian fever pattern, chills,
antimalarial therapy immed iately. Data in
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A First Case of Plasmodium knowlesi Malaria in Phramongkutklao Hospital:- Traipattanakul J, et al.
Malaysia, Thailand, and Singapore reveals
93
physical findings were unremarkable.
that this infection was successfully treated with
Complete blood count demonstrated a hemoglobin
chloroquine.12,19,34,38,47-49,51,55 Fatal cases have been
level of 11.2 g/dL, total white cell blood count of
reported to be associated with parasitemia more
11.2 × 109/L with normal differentiation, and platelet
than 100,000 parasitemia/mcL of blood (2%-5% of
count of 224 × 109/L. Other blood chemistry results
erythrocytes).18,35,56
were within normal ranges. A thin blood smear
Plasmodium falciparum and Plasmodium vivax
are the leading causes of malaria in Thailand.
revealed 0.5% parasitemia with a morphologic
13,14,39-44
appearance suggestive of P. malariae infection
Since 1968, chloroquine-resistance falciparum
(Figure 1-2). The identification of P. knowlesi was
malaria have been discovered widespread throughout
based on the finding of 153 bp small subunit
Thailand.57-59 Practically, because of the difficulty
ribosomal RNA (SSU rRNA) gene (Figure 3). She
in distinguishing between these P. knowlesi
was treated with 10 mg/kg of oral chloroquine
malaria with hyperparasitemia from severe
initially, followed by 5 mg/kg, 6 hours later on day 1,
mixed infection of P. knowlesi and P. falciparum,
and 5 mg/kg/day for the next 2 days. Fever subsided
it should be treated in the same way as P. falciparum
after 3 days of chloroquine administration. The
malaria.49,60,61
patient was hospitalized for 7 days and successfully
Here, we report the first case of probable blood
treated with chloroquine.
transfusion-transmitted P. knowlesi malaria in
Phramongkutklao Hospital.
DISCUSSION
Patient previously lived in non-endemic area of
CASE REPORT
P. knowlesi. Kalasin province located in upper part
In September 2011, a 54-year-old housewife,
of Northeastern Thailand. This area is not known to
from Kalasin province, North-East of Thailand, had
be habitat of reservoir host of P. knowlesi. After
been admitted in Phramongkutklao Hospital because
discharged from the hospital, she relocated into
of daily fever and shaking chills for 5 days. Three
endemic area of P. knowlesi, Kanchanaburi Province.
weeks earlier, she was diagnosed with distal
She lived in the area only for 3 days before she
cholangiocarcinoma with liver metastasis and
developed fever and shaking chills. The fact that
underwent Whipple operation. During admission
prepatent period is 9-12 days, the incubation
she was also given a unit packed red cell transfusion.
period took place during her hospitalization in
She spent two weeks in the hospital without any
Phramongkutklao Hospital, Bangkok where it is not
serious consequence. After that, she lived with her
an endemic area of P. knowlesi. In conclusion, this
daughter in Amphoe Mueang Kanjanaburi and
patient is the first case of probable blood transfusion-
spent most hours indoors and has never been
transmitted P. knowlesi malaria in Phramongkutklao
diagnosed with malaria.
Hospital.
The physical examination on admission revealed
Blood transfusion is a life-saving intervention.
body temperature of 40.3°C, the pulse rate of
Research in blood transfusion began in the 17th
114 beats/minute, blood pressure of 130/80
century and had been successfully established in
mmHg, and respiratory rate of 22/minute. Other
93
1906.62,63 The first case of transfusion-transmitted
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J INFECT DIS ANTIMICROB AGENTS
May-August 2014
..
Figure 1. Microscopic morphology of Plasmodium knowlesi in a May-Grunwald
Giemsa-stained thin blood smear (x1,000 magnification). Infected
erythrocytes were not enlarged with the presence of much hemozoin and
lacked stippling. (A) Early trophozoites (B) Early trophozoites with doublechromatin dots (C) growing trophozoites (band form), (D) growing
trophozoite (compact form) (Courtesy of Mathirut Mungthin, Division of
Parasitology, Phramongkutklao College of Medicine).
malaria from direct blood transfusion was reported
limited data demonstrating viability of malaria in
in 1911.64 During the 1940s, the use of stored blood
stored packed red cells.65,68 Currently, there is only
gradually replaced direct blood transfusion.65 In 1941,
one experimental study of erythrocytic staged P.
the first case of transfusion-transmitted malaria
falciparum in packed red cell which had been stored
from stored blood transfusion was identified.
66
at 4°C and preserved with CPDA-1 solution. There
Of note, usually packed red cells should be kept at
were significant reduction in parasitemia (0.5% VS.
4-6°C with citrate-phosphate-dextrose anticoagulant-
0.12%) after only 1 day in the process. Parasites are
preservative, and the ordinary shelf-life is 21 days.
not able to replicate when cultured in vitro, after
In the present report, the patient recived
storing for more than 14 days. 70 One case of
citrate-phosphate-dextrose-adenine anticoagulant-
transfusion-transmitted P. falciparum malaria from
preservative (CPDA-1) packed red cells, stored up
whole blood, storage after 19 days at 4°C in CPDA-1,
to 12 days from Blood Bank Department of Army
was reported.72 However, viability of P. knowlesi in
Institute of Pathology, Phramongkutklao Medical
stored packed red cells had never been carefully
Center. The ordinary shelf-life is 35 days. There is
investigated.
67
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A First Case of Plasmodium knowlesi Malaria in Phramongkutklao Hospital:- Traipattanakul J, et al.
95
..
Figure 2. Microscopic morphology of Plasmodium knowlesi in a May-Grunwald
Giemsa-stained thin blood smear (x1,000 magnification). (A) mature
trophozoite, (B) early schizont, (C) growing schizont, (D) mature schizont,
(E) gametocyte. (Courtesy of Mathirut Mungthin, Division of Parasitology,
Phramongkutklao College of Medicine)
Incubation period of intravenous inoculation by
packed red cells could extend the incubation
erythrocytic staged parasite is different from
period longer.2,65,72 Only 10 parasite of P. vivax
natural infection in terms of incubation period by
could successfully transmit to humans and cause
sporozoite. Incubation period of blood-induced
illness. 72 This case report, incubation period of
infection depends on the number of parasites
P. knowlesi infection was 15 days.
introduced, susceptibility of recipient, and method
Some parts of Thailand are classified as area of
of inoculation. Mark Frederick Boyd revealed
malaria endemic. The rates of inoculation fluctuate
the incubation period of blood-induced malarial
greatly over seasons and years. Entomological
infection in Table 1.
65,72
Inoculation with stored
inoculation rates (EIR) are usually < 5 per year
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May-August 2014
Figure 3. Species-specific nested polymerase chain reaction amplification
products. Agarose gel electrophoresis Line 1-9, all are only positive
153 bp products of Plamodium knowlesi. Species-specific primers
derived from the small subunit ribosomal RNA gene. (Courtesy of
Mathirut Mungthin, Division of Parasitology, Phramongkutklao College
of Medicine)
Table 1. Dosage of malaria parasites given by intravenous inoculation and the
length of the incubation period.72
Incubation period (fever)
Parasite
No. of parasites
Prepatent period (days
(days)
P. vivax
P. m alariae
106
10.9
11.6
106-108
1.1
3.2
108
1
1
106
23
28
106-108
6.7
13
108
4.5
9.2
and often < 1 per year.73 WHO reported in 2012,
of doners by questionnaires only. This strategy
high transmission population (> 1 case per
focuses on minimizing risk of introducing malaria
1,000 population) was only 8%, low trasnsmission
parasites into blood supplies.75 Restrictions on
population (0-1 case per 1,000 population) 42%
blood donation are illness from malaria within last
and Malaria-free population was 50%.74 Practically,
3 years, receiving blood transfusion within last 1
Thailand National Blood Center suggest screening
year, traveling to an endemic area of malaria within
Vol. 31 No. 2
A First Case of Plasmodium knowlesi Malaria in Phramongkutklao Hospital:- Traipattanakul J, et al.
97
last 1 year (Thai-Myanmar and Thai-Cambodia
Plasmodium knowlesi: the emerging zoonotic
borders e.g. Mae Hong Son, Tak, Kanchanaburi,
malaria parasite. Acta Trop 2013;125:191-201.
Phetchaburi, Prachuap Khiri Khan, Chumphon,
5.
Antinori S, Milazzo L, Corbellino M. Plasmodium
Ranong, Phangnga, Yala, Narathiwat, Chanthaburi,
knowlesi: An Overlooked Italian Discovery? Clin
Trat). 39-44 Complete prevention of transfusion-
Infect Dis 2011;53:849.
transmitted malaria may not be possible.
76
Infected
6.
blood donors may have discrete parasitemia (1-2
Kantele A, Jokiranta TS. Reply to Antinori et al. Clin
Infect Dis 2011 Oct;53(8):849; author reply 849-50.
parasites/mL), which cannot be detected by
7.
ordinary microscopy. Patients may receive
Knowles R. 1935. Monkey malaria. Br Med J
1935;11:1020.
400,000-800,000 parasites per unit of packed
8.
red cell in the worst case scenario. 65
Sinton JA, Mulligan HW. A critical review of the
literature relating to the identification of the malarial
This patient received a packed red cells from
parasites recorded from monkeys of the family
teenager student who trave led to waterfall
Cercopithecidae and Colobidae. Rec Malar Surv India
in national park in Kanchanaburi province
1992;3:381-443.
within last 3 weeks. The donor was noted to have
9.
Eyles DE, Laing ABG, Dobrovolny CG. The malaria
had fever 4-5 days and was diagnosed with
parasites of the pig-tailed macaque, Macaca
dengue fever. He fully recovered without any
nemestrina (Linnaeus), in Malaya. Ind J Malariol
antimicrobial treatment a week before blood
1962;16:285-98.
donation. He previously lived in Bangkok and
10. Eyles DE, Laing ABG, Warren M, Sandosham AA.
never had illness from malaria. Kanchanaburi, is
Malaria parasites of Malayan leaf monkeys of the
Thai-Myanmar border region, located in the West
genus Presbytis. Med J Malaya 1962;17:85-86.
of Thailand. There were 7 P. knowlesi malaria cases
11. Fooden J. Malaria in macaques. Int J Primatol
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during 2006-2009.13,14 Conversely, P. knowlesi
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Kanbara H. Naturally acquired Plasmodium knowlesi
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13. Putaporntip C, Hongsrimuang T, Seethamchai S, et al.
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