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High Prevalence of Brugia Timori Infection in The Highland of Alor Island, Indonesia
High Prevalence of Brugia Timori Infection in The Highland of Alor Island, Indonesia
560–565
Copyright © 2002 by The American Society of Tropical Medicine and Hygiene
Abstract. To identify areas endemic for Brugia timori infection, a field survey was carried out in 2001 on Alor, East
Nusa Tenggara Timor, Indonesia. Elephantiasis was reported on this island by villagers as a major health problem.
Bancroftian filariasis was detected in four villages in the coastal area, whereas B. timori was identified in four rice-
farming villages. No mixed infections with both species were found. In the highland village Mainang (elevation ⳱ 880
m), 586 individuals were examined for B. timori infection and 157 (27%) microfilaria carriers were detected. The
prevalence of microfilaremic individuals standardized by sex and age was 25%. The geometric mean microfilarial density
of microfilaremic individuals was 138 microfilariae/ml. Among teenagers and adults, males tended to have a higher
microfilarial prevalence than females. Microfilaria prevalence increased with age and a maximum was observed in the
fifth decade of life. In infected individuals, the microfilarial density increased rapidly and high levels were observed in
those individuals 11−20 years old. The highest microfilaria density was found in a 27-year-old woman (6,028 microfi-
lariae/ml). Brugia timori on Alor was nocturnally periodic, but in patients with high parasite loads, a small number of
microfilariae was also detected in the day blood. The disease rate was high and many persons reported a history of acute
filarial attacks. Seventy-seven (13%) individuals showed lymphedema of the leg that occasionally presented severe
elephantiasis. No hydrocele or genital lymphedema were observed. This study showed that B. timori infection is not
restricted to the lowland and indicated that it might have a wider distribution in the lesser Sunda archipelago than
previously assumed.
560
B. TIMORI ON ALOR ISLAND 561
TABLE 1
Identification of villages endemic for lymphatic filariasis by examination of thick smears of capillary night blood for the presence of microfilariae
(mf) on Alor island, Indonesia*
Microfilaria rates. The B. timori-endemic village of Main- Microfilaria densities in microfilaremic individuals reached a
ang in the highlands of Alor was selected for a more detailed peak in both sexes between 10 and 19 years of age (Figure 3).
study. A total of 1,582 individuals lived in Mainang and 37% The highest microfilarial density observed was 6,028 mf/ml in
(586 persons) of the population was examined. No children a 27-year-old women with grade 1 leg lymphedema. Fourteen
less than five years old were included in the study. There was percent of the microfilaremic individuals had microfilarial
no difference in the sex and age distribution of the examined loads of 1−10 mf/ml, 26% had loads of 11−100 mf/ml, 37%
individuals in Mainang. More females were studied than had loads of 101−1,000 mf/ml and 23% had loads greater than
males, and 50% of the eligible females and 27% of the eligible 1,000 mf/ml.
males were included in the study. This was because some men Microfilariae in day blood. When the day blood of mf-
stayed overnight in their fields and could not participate in positive individuals was examined for mf, it was observed that
the survey. Confounding factors due to self-selection were 62% of the individuals had circulating microfilariae. There
possible only in Welai Selatan and Malaipea, but not in was a positive correlation between microfilarial density in
Tominuku where participants were recruited directly from night blood and in day blood (rs⳱ 0.38, FG ⳱ 67, P < 0.002).
their homes. However, there was no significant difference in Among 28 individuals with microfilarial densities greater than
prevalence of microfilaremic individuals and patients with 400 mf/ml in night blood, 27 (96%) also had mf-positive day
clinical signs in three sections of Mainang (Table 2). There- blood. The microfilarial densities in day blood were low: 57%
fore, these three sections were analyzed as a homogeneous of the microfilaremic individuals had 1−10 mf/ml, 39% had
group. 11−100 mf/ml, and 4% had greater than 100 mf/ml. Therefore,
The highest rate of microfilaremic men and women was we briefly examined the periodicity of B. timori on Alor is-
found in those 40−50 years of age (50% for men and 38% for land in a patient with greater than 400 mf/ml in night blood
women) (Figure 2). However, even in those 5−10 years of age, and in another patient with 100 mf/ml in night blood. Between
18% of the children were mf positive. There was no sex dif- 8:00 AM and 4:00 PM, 4.8% and 3.3% of the total number of
ference in prevalence of microfilaremic individuals in this age detected microfilariae were found in the peripheral blood of
group of children (P ⳱ 0.8266). In older children and adults, these two patients, respectively. The peak of microfilarial
a significantly higher percentage of males was mf positive density was observed in one patient between 2:00 AM and 4:00
(35% vs. 23%, P ⳱ 0.0022). The prevalences of microfila- AM and in the other patient between 8:00 PM and 10:00 PM.
remic individuals standardized by sex and age were 25% and
23% if children less than five years old were assumed to be mf
negative. The geometric mean number of microfilariae per
millililter of blood was 118 mf/ml in males and 160 mf/ml in
females. This trend of women having higher microfilarial den-
sities than men was not statistically significant (P ⳱ 0.2380).
TABLE 2
Prevalence of Brugia timori microfilaremic individuals and persons
with lymphedema in the three sections of Mainang village, Alor
island, Indonesia*
DISCUSSION
sities greater than 400 mf/ml of night blood can be identified was achieved by the observation that a single dose of DEC (6
by the filtration of day blood with a sensitivity of 96%. For the mg/kg) has similar effects as the same dose of DEC given
identification of endemic areas with high parasite loads, this daily for two weeks.8,22,23 Community-based treatment using
might be an alternative to the night blood collection. How- a single, annual, or semi-annual dose of DEC is considered to
ever, for areas with low endemicity and low infection density, be more feasible compared with a 10-day or two-week treat-
as well as for the monitoring of intervention programs, the ment course. It is still not known if this single-dose treatment
parasitologic examination of day blood for microfilariae is not strategy is also safe and effective in the control of B. timori
suitable. More sensitive methods, such as the PCR, need to be infection. So far, no animal reservoir for B. timori has been
used for this purpose.17 identified. The distribution of B. timori is restricted to a few
In the opinion of villagers in Mainang, the development of islands and anopheline mosquitoes are the only known vec-
leg edema was due to extensive work in rice fields. In accor- tors. It has already been discussed that filarial parasites trans-
dance with this belief, in rice field-free areas, where Bancrof- mitted by anopheline mosquitoes can be more easily con-
tian filariasis was endemic, almost no edema of the leg was trolled than culicine-transmitted infections.24 For these rea-
observed. It is now well known that external bacterial super- sons, the prospects for the elimination of B. timori filariasis
infections contribute to the pathology of lymphatic filaria- may be more promising compared with the elimination of
sis.18 Therefore, working in irrigated rice fields may be a risk filariasis due to B. malayi and W. bancrofti in many other
factor in the development of elephantiasis of the leg in indi- regions.
viduals infected with B. timori. Although individuals with The present study showed that B. timori filariasis is abun-
open lesions and advanced lymphedema try to avoid contact dant in the highlands of the lesser Sunda archipelago and that
with water because of the pain, they are forced to continue to this infection is still a public health issue of local importance.
work in their rice paddies for economic reasons. Further stud- Further studies are needed to show if B. timori infection can
ies are needed to elucidate the risk factors for the develop- be controlled by the new treatment strategies for the control
ment of lymphedema in individuals living in areas endemic and elimination of lymphatic filariasis proposed by the World
for B. timori. However, the prevalence of lymphedema in Health Organization.
Mainang was in agreement with results of two studies on
Flores, which reported B. timori microfilaremia rates of ap- Acknowledgments: We thank Dr. Paul Manoempil, Sudiman, Dr.
proximately 25% and lymphedema rates ranging between Lani Harijanti, Simone Klüber, and the district health workers for
their help during the field survey. We are grateful to all inhabitants of
11% and 15%.11,12
Mainang and the other villages examined who participated in the
Dennis and others found that elephantiasis due to B. timori study. We also thank Professor Bernhard Fleischer for his encour-
most often developed during the third decade of life.11 This agement and Professor W. Büttner for critically reading the manu-
observation is supported by our results, but we found that script.
lymphedema up to grade 3 was common even in teenagers Financial support: This investigation was supported by the UNDP/
and may lead to serious social and economic consequences at World Bank/WHO Special Program for Research and Training in
an early age. In a sample of 42 previously uninfected immi- Tropical Diseases (TDR). Peter Fischer was supported by the Schol-
arship Program ‘Infectiology’ of the German ‘Bundesministerium für
grants to an area endemic for B. timori, nine individuals were
Forschung und Technologie (BMBF)’.
reported to have developed lymphedema or elephantiasis
within two years following settlement.19 Although the devel- Authors’ addresses: Taniawati Supali, Herry Wibowo, Is S. Ismid,
and Yenny Djuardi, Department of Parasitology, Faculty of Medi-
opment of lymphedema may be faster in individuals who have cine, Salewba 6, University of Indonesia, Jakarta 10430, Indonesia.
not been previously exposed to B. timori, this observation is Paul Rückert, German Agency for Technical Co-operation (GTZ),
in agreement with our data that show that lymphedema due Jalan Wolter Robert Monginsidi II/2, PO Box 1217, Walikota Baru,
to infection with B. timori often affects teenagers and younger Kupang 85000, Indonesia. Kerstin Fischer and Peter Fischer, Bern-
hard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Strasse
adults. The high prevalence of microfilaremic individuals and
74, D-20359 Hamburg, Germany. Purnomo, U.S. Naval Medical Re-
persons with clinical signs such as lymphedema in Mainang search Unit No. 2, Jakarta, Indonesia.
shows that B. timori filariasis is still an important local public
Reprint requests: Peter Fischer, Bernhard Nocht Institute for Tropi-
health problem. cal Medicine, Bernhard-Nocht-Strasse 74, D-20359 Hamburg, Ger-
As of the year 2000, approximately 3.9 million people lived many, E-mail: Pfischer@bni.uni-hamburg.de.
in Nusa Tenggara Timor and approximately 0.75 million
people lived in East Timor.20 These people are at risk of
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