■■■

王

第27巻第2号平成11年6月
内
原

容

著
Application of Seroepidemiology in the Evaluation of a Community BasedControl Program in Parawan，the Philippines（英文）Pilarita Tongol−Rivera，狩野 繁之，Elena Villacorte，Aldrin Darilag，EdithaMiguelフ鈴木守…………・一…・・…一…………・・一……………

Malaria………

……

一！61−165

バングラデシュの結核対策におけるコミュニティヘルスワーカーの参加とその役割（英文）Mohammed
Sadia

AkramulIslam，中村安秀，Som−Arch

A．Chowdhury，石川Wongkhomthong，

信克・・167−173

フィリピン・ミンドロ島における小学校児童および保虫宿主動物の日本住血吸虫感染状況（英文）松本淳，桐木 雅史，川合・覚，千種 雄一，E．」．Ilagan，B．E．Ducusin，
安羅岡一男，松田
肇一………………・・………一………………………・…一……………・……175−180

ClinicalMalaria

andTreatmentofMultidmg

Resistance

FalciparuminThailand（英文）Srivicha Kmdsood，Watcharee Chokejindachai，Udomsak Silachamroon，Weerapong
Phumratanaprapin，Pampen Viriyavejakul，Valai Bussaratid and Somchai Looareesuwan−181−188
小笠原諸島産オガサワラツノマユブユ（双翔目蜻および成熟幼虫の記載（英文）高岡 宏行，斎藤 一一三1，鈴木
博……

ブユ科）のvem㎜種グループヘの分類と雄成虫，
・189−194

ミクロネシアのパラオにおけるパラオナンヨウブユ（双翔目：ブユ科）の分類および生態に関するノート
成虫の再記載ならびに蜻および成熟幼虫の記載（英文）高岡宏行，Douglas

A．Craig……………・……一

会報・記録
1999年度日本熱帯医学会役員名簿一
日本熱帯医学会雑誌編集委員名簿
投稿規定……一…………・…………
日本医学会だより
日本学術会議のお知らせ…・……・…
著作権複写に関する注意……・・……

・・195−201

一203−204−205
・・206−208−209−210

−211

−212

一■

161

Jpn. J. Tro p. Med. Hyg ., Vol. 27, No. 2, 1999, pp. 161 165

APPLICATION OF SEROEPIDEMIOLOGYIN THE EVALUATION OF A COMMUNITY‑

BASED MALARIA CONTROL PROGRAM
IN PALAWAN, THE PHILIPPINESPILARITA TONGOL‑RIVERAl, SHIGEYUKI KAN02,3, ELENA VILLACORTEl,
ALLDRlN DARILAGl, EDITHA MIGUEL4 AND MAMORU SUZUK12
Received October 27, 1997/Accepted February 24, 1999

Abstract: Seroepidemiology has several proven applications in malaria endemic areas. In this study, it wasused to assess the effectiveness of a community‑based malaria control program in the focus of malariatransmission. The first serological survey was done before the implementation of a c6mmunity‑based
malaria control program (pre‑intervention) , and the second one was done after 5 years of intervention in
the study area. Comparison of the distribution of the indirect fluorescent antibody (IFA) titers showed areduction in the high titer‑responses after the intervention. Moreover, there was a statistically significant

reduction in the geornetric mean reciprocal titer (GMRT) after the intervention. These findings weresuggestive of a reduction in malaria transmission resulting from the intervention. Results of a parallel
parasitologic study revealed the same findings. Therefore, seroepidemiology, when used to complement theparasitologic measurement, is valuable in monitoring the effectiveness of malaria control measures.
Key words: malaria, seroepidemiology, community‑based malaria control

INTRODUCTION
In many endemic communities, malaria control has
been reoriented to better and more efficient use ofresources. Emphasis has been changed from the highlyprescriptive, centralized control programs, to those
programs adapted to local conditions and responding to
10cal needs of the people (WHO, 1992) . The community‑
based approach to malaria control has been adopted inness of a five‑years community‑based malaria control

program in the study community. The findings fromthis study may be of value in monitoring the present

10cal malaria control program and those of otherendemic countries as well.

SUBJECTS, MATERIALS AND METHODS
Study area

the Philippines, especially since the provision of healthThis study is limited to the forest fringe part of theservices has been devolved to the local governments

same study community (Tongol‑Rivera et al.. 1993),(Malaria Control Service, 1996). This type of approach

which was the focus of malaria transmission. An

encourages community participation, people empower‑

already organized group of volunteer health workers(BHWs) was mobilized for the promotion and imple‑
mentation of ongoing malaria control interventions inthis study community. The target population consisted

ment and self‑reliance. Sustainability of malaria con‑trol measures is thus assured on a long term basis. It is

this type of malaria control which was implemented in
the focus of malaria transmission in the study area.

In view of the wide applications of sero‑of 65 families with 344 members. During the five years

study period, the BHWS Were trained and re‑trained.

epidemiology (WHO, 1972; Tharavanij et al.. 1986; Ray

heir activities included the promotion of residual insec‑

et al.. 1988; Ettling et al.. 1989; Kano et al.. 1993), thisticide spraying to cover as many households as possible,

present study attempts to use it to evaluate the effective‑

active and passive case finding by making blood smears

1

Department of Parasitology, College of Public Health, University of the Philippines, Manila

2

Department of Parasitology, Gunma University School of Medicine, Gunma, Japan
Research Institute, International Medical Center of Japan, Tokyo, Japan
Palawan Provincial Hospital, Palawan, the Philippines

3
4

162

and bringing them to the microscopist (both government

isothiocyanate‑conjugated anti‑human lgG (Dako,and non‑government organizations) for parasitologic
diagnosis, administration of Chloroquine and Prima‑quine tablets (Chloroquine Phosphate at 10 mg base/kg
on day I and day 2, and 5 mg base/kg on day 3 for
Plasmodium falciparum; Chloroquine at this dose plus
Primaquine at 15 mg base/kg for 14 days for P. vivax)

Japan) was used as antibody and fluorescence was readwith an incident light illuminating type fluorescent

microscope (model BH‑RFC; Olympus, Tokyo, Japan) .
The highest serum dilution giving a positive reading was
the IFAT titer.

to patients with positive blood smears; and distribution
and monitoring of the use of Permethrin pre‑impregnat‑

Statistical analysis

ed mosquito nets (Japan) . They were also responsiblefor dissemination of information about malaria preven‑tion and control and they actively participated in thethe differences in the geometric mean reciprocal titerparasitologic and serologic surveys.

normally distributed.

The Mann‑Whitney U test was used to determine(GMRT) between the pre and post‑intervention ser‑ologic surveys because the antibody titers were not

The BHWS did passive and active case detection in
the study area during implementation of the project(1992‑1996) . For suspected malaria cases they made thesmears themselves and brought to the microscopists fordiagnosis.

Serologic and Parasitologic Surveys

The results of the serologic and parasitologic sur‑veys which were done at the end of the rainy season, in
December, 1991 were considered as the pre‑intervention

data. At that time, a total of 118 blood samples werecollected by fingerprick in infants and venipuncture in
the older age group (Tongol‑Rivera et al.. 1993). In
February and March, 1997, after five years of commu‑
nity‑based malaria control, repeat surveys were done on
the same study site. These surveys were scheduled at

RESULTSInterviews with the BHWS and the subjects whichwere done simultaneously with the surveys, revealed
that 73.2% have been using the pre‑impregnated mos‑quito nets distributed to them. Those who resided in the
study area after the net distribution (21.5%) have beenusing ordinary mosquito nets. The children, O to 10
years old have been the priority group to use the net
while sleeping. It was also found out that 64.2% of thesubjects' houses have been sprayed with residual insecti‑

cides at least once a year. The general observation of

the BHWS and the subjects was that the frequency ofmalaria in their community has been reduced signifi‑
cantly, considering the lesser nurnber of positive blood

the end of the rainy season which was unusually delayed.

smears and malaria sick residents, even during the rainy

The pre and post‑intervention surveys were both done
after the rainy season, when malaria transmission was
expected to be high. A total of 218 blood specimens

season. Table I shows the yearly number of malaria
cases which were confirmed by peripheral smear anddetected through passive and active case detection by

were collected by fingerprick (Kano et al.. 1989) using

BHWs. Although a trend of increasing number ofblood sampling paper (Nobuto's). The subjects camemalaria cases is observed, the actual counts are stillfrom the following age groups: 0‑9 years of age, 49.5%;
10‑20 years of age, 8.3%; and >20 years of age, 42.2%.

10wer compared to the 99 cases detected by serology(IFAT) during the pre‑intervention survey. Titers ofThey were composed of 67% females and 33% males.
Parallel parasitologic surveys were done at thesame time as the serologic surveys. Thick and thinblood smears were processed. There were 118 smears

examination, it is shown that there are 44 malaria cases

during the pre‑intervention and 219 (this included 1
subject who did not have plasma specimen) during thepost‑intervention.

For the pre‑intervention serologic survey, the in‑direct fluorescent antibody test (IFAT) was used with

1:16‑1:4,096 are considered positive (Table 2) . On closer

detected by IFAT in the post‑intervention survey, as

compared to 39 cases detected by the BHWS throughTable I Malaria cases detected by passive and active casedetection by BHWS and confirmed by peripheral

smear

1992 1993 1994 1995 1996

four‑fold dilutions of serum ranging from 1:4 to 1:4,096

and reacted to both P. falciparum and P. vivax antigens(Tongol‑Rivera et al.. 1993). In the post‑intervention

P. falciparum

5

3

8

P. vivaxo3

1

survey, the IFAT was done with plasma diluted ten‑fold

Mixed

o

1

with phosphate‑buffered saline (PBS). Fluorescein

Total

5

7 10

12 26

6 10

O 3

18 39

163

Table 2 Distribution of indirect fluorescent antibody test (IFAT) titers and parasitemia before and after
community‑based malaria control
Before Community‑based

After Community‑based

Parasitemia
Before Community‑based After Community‑based

Malaria Control

Malaria Control

Malaria Control

IFAT TitersAge(in years)

0‑9

10‑20

> 20

Malaria Control

1:256‑1:4,096

18

1:400‑1:1,000

3

P.f

8

1:16‑1:64

6

1:40‑1:100

7

P. v.

O

< 1:4

10

1:10

10

Mixed

1

O

< 1:1088

Negative

25

108

7

O

O

1:256‑1:4,096

24

1:400‑1:1,000

O

P,f

1:16‑1:64

9

1:40‑1:100

4

P. v.

< 1:4

4

1:10

2

Mixed

o

O

< 1:10

12

Negative

30

18

O

1:256‑1:4,096

38

1:400‑1:1,000

8

P.f

9

o

1:16‑1:64

4

1:40‑1:100

22

P. v.

o

o

< 1:4

5

1:10

28
34

Mixed

o

o

Negative

38

92

118

219

<1:10

218

118

Total

*Values are the number of individuals. P,f =Plasmodium falciparum; P.v, =Plasmodium v ivax.

active and passive cases detection in 1996, which is the

falciparum and P. vivax antigens. A second peak at ayear preceding this survey. These data show that bymeasuring period prevalence, serology is able to mea‑

intervention survey showed a high percentage of nega‑sure the actual estimate of malaria cases. On the othertive titers for both P. falciparum and P. vivax antigens.

hand, detection of parasitemia in malaria smears, mea‑

Table 2 shows a comparison of the specific titers
among the different age groups, and between the pre andpost‑intervention surveys. In the pre‑intervention sur‑vey, 68% (n=118) of the subjects had high titers (1:256‑
1:4,096), 16% had low titers (1:16‑1:64) and only 16%

sures point prevalence and misses low parasitemias,
past and treated infections.

Figure I shows the frequency of antibody titers
when graphically plotted. The distribution profiles ofboth P. falciparum and P. vivax species followed similar

lower titer of 1:16 was also noted. In contrast, the post‑

patterns. Figure I also shows the comparison of the

had negative titers (1:<4). This is in contrast to thepost‑intervention results which showed 80% with nega‑

antibody titer distribution profiles of the pre and post‑

tive titers (1:<10) , 15% with low titers (1:40‑1:100) andintervention serologic surveys in the study community.
In the pre‑intervention survey, a high percentage ofsubjects showed the highest titer (1:4,096) for both P.

only 5% with high titers (1:400‑1:1,000). Moreover, thedifference in the GMRTS Of the two surveys was statisti‑cally significant (p<0.01) .

After E

Before

"I
e
"

80
70

eo

60
SO

50
40

40

% Positive

96 po! ltlve

SO

30
20
10

o

.

:// ¥ ‑, i

1 25 G '1 :4096
fl･4 '1 1 5 '1:64
l F ATTiter
1 ･4'1 : ' o 24

ZO
10

(lP

e‑

l : e' IFeO<1 : 10

'1 :

o

c 1

1 o '1 = 40 '1= I o o '1= 40 o

IFAT Titer

Figure 1 Distribution of the indirect fluorescent antibody test (IFAT) titers before
and after community‑based malaria control.

'1:1000 'l 4000

164

The parallel parasitologic study showed that 25 outof 118 subjects had parasitemia during the pre‑interven‑

falciparum and P. vivax in the post‑intervention survey
against 99 in the pre‑intervention survey. By measuring

tion survey. Of these, 24 had P. falciparum while one
had mixed infection (Table 2) . By the IFAT, there were
99 out of 118 whose titers were 1:16‑1:4,096 and wereconsidered to be malaria cases (Table 2). On the otherperiod prevalence, serology detected cases which occur‑
red in the previous year. The above data may indicate
a significant reduction in malaria prevalence and trans‑mission, although complete interruption of transmission
was not attained.

hand, in the post‑intervention survey, only one out of 219

was positive and this was P. vivax. By the IFAT, morecases were detected, 44 out of 218 whose titers were1:40‑1:1,000. These results show a reduction of malaria

cases during post‑intervention which may suggest a
reduction of the prevalence and transmission of malaria
in the study community.

Comparison of the antibody distribution profiles(Fig. 1) of the two surveys also shows the same trend,

whereas high antibody titers predominate before theimplementation of community‑based malaria control,
10w and even negative titers predominate after the
implementation of control. Both pre and post‑interven‑tion antibody profiles show IFAT titers to both P.

The degree of transmission or prevalence of

falciparum and P. vivax. However, the post‑intervention
profile shows a more significant decrease in P. vivax and
P. falciparum. The reason is that P. falciparum being

malaria is usually measured by either GMRT or thepercentage of the sample population which is sero‑

dominant during the rainy season causes more recent
past infection which are detected by serology in the

logically positive (Kagan, 1973). In the present study,

survey after the rainy season. However, P. vivax

DISCUSSION

both of these measurements consistently showed areduction of malaria transmission and prevalence, which

may have been attributed to the implementation ofcommunity‑based malaria control in this study commu‑
nity. It was shown that there was a statistically signifi‑

increases in frequency during the dry season, so that alesser percentage of P. vivax was detected by the same

serologic survey done after the rainy season. The
paralle parasitologic study (Table 2) shows results
which are consistent with the serologic study. Morecant difference between the GMRTS Of the pre‑interven‑tion and post‑intervention surveys, and which is sugges‑

parasitemic subjects, predominantly P. falciparum weretive of the effectiveness of malaria control. Further‑more, Table 2 shows a high percentage of subjects withhigh antibody titers to both P. falciparum and P. vivax.
and lower percentages of subjects with low and negative
antibody titers before the implementation of community‑

was detected after the intervention. These data further
strengthen the conclusion that malaria prevalence andtransmission are significantly reduced in the study com‑munity.
Seroepidemiology, as shown in the present study isuseful in the assessment of the effectiveness of malaria
control programs. Although, the significant reduction in
malaria prevalence and transmission in the study com‑

based malaria control. The opposite was shown after
the irnplementation, when there was a high percentageof negative and low titers, and very low percentage ofhigh titers. Table I shows the number of malaria cases
per year of the intervention period as determined bydetected before the intervention, while only one P. vivax

post‑intervention parasitologic survey in Table 2, shows

munity may be attributed to the malaria control im‑
plemented, there may be other factors which may havecontributed to this improvement in malaria situation.
These factors which cannot be controlled in the study
include the natural reduction of malaria transmissionthat cases were easily missed by a one‑point par‑which may be due to instability of malaria, environmen‑

asitologic survey. There were more cases detected intal changes and socio‑economic development of thestudy community.

passive and active case detection and confirmed byperipheral smear. Comparison with the results of thethe years during the intervention because case detection

was done throughout the year. The highest number of
39 cases were detected the previous year in 1996. The
post‑intervention parasitologic survey in 1997 detected
only one case. However, serology even if it was done asa one‑point survey detected 44 cases in the post‑inter‑

vention survey in 1997. Comparison with the results ofthe pre‑intervention serologic survey shows a 44%
reduction of cases‑44 showed IFAT titers to both P.

ACKNOWLEDGMENTS
We thank Drs. Jose Socrates and Maridith de Leonof the Palawan Provincial Health Office; Dr. Juanito
Duenas, City Health Officer, Puerto Princesa City;

Malaria Control Service, Palawan; Alayka Palawan,

BHC and BHWS Of Barangay Mangingisda and Sitio

165

Rubber for valuable participation and assistance in this5 ) Malaria Control Service Annual Report (Philippines) ,study. This study was partly supported by WHO TDR

1996
6 ) Ray, K., Upreti, H.B., Yadav. R.N., Sharma, M.C. andMukherjee, A.K. (1988): Evaluation of serology as a

Research Training Grant No. 900729.

1 ) Ettling, M.B., Thimasarn, K., Krachaiklin, S. andtool for malaria surveillance in East Champaran Districtof Bihar, India. Ann. Trop. Med. Parasitol., 82, 225‑228
7 ) Tharavanij, S., Chongsa‑nguan, M., Ketrangsi, S., Patar‑
apotikul, J., Tantivanich, S. and Tapchaisri, P. (1986):

Bualombai. P. (1989): Evaluation of malaria clinics in
Maesot, Thailand: use of serology to assess coverage.
Trans. Roy. Soc. Trop. Med. Hyg., 83, 325‑3302 ) Kagan, I.G. (1973): Parasitic diseases. In: Serological
Epidemiology, 155‑168, Academic Press, London
3 ) Kano, S., E1 Safi, S.H., Omer, F.M., Rivera, P.T., El

Cross‑sectional seroepidemiological survey of malaria
in endemic areas with different activities of malaria
control. Southeast Asian J. Trop. Med. Pub. Hlth., 17,524‑529
8 ) Ton ol‑Rivera, P., Kano, S., Miguel, E., Tongol, P. andSuzuki, M. (1993): Application of seroepidemiology in

Gaddal, A.A. and Suzuki, M. (1993): Antibody fre‑quency distribution curve for risk assessment of aidentification of local foci in a malarious community in

REFERENCES

malaria epidemic in the Sudan. Jpn. J. Trop. Med. Hyg.,21, 207‑211
4 ) Kano, S., Takagi. T., E1 Gaddal, A.A. and Suzuki, M.
(1989): A new method of plasma collection suitable forlarge scale seroepidemiological surveys of malaria in
the tropics. Trans. R. Soc. Trop. Med. Hyg., 83, 304

Palawan, the Philippines. Am. J. Trop. Med. Hyg., 49,
608‑6129 ) WHO (1972): Serological testing in Malaria. Bull.
World Health Organ., 50, 527‑532
10) WHO (1992): Global Malaria Control Strategy, Ministe‑rial Conference on Malaria, Amsterdam

167

Jpn. J. Tro p. Med. Hyg., Vol. 27, No. 2, 1999, pp. 167‑173

INVOLVEMENT OF COMMUNITY HEALTH
WORKERS IN TUBERCULOSISCONTROL IN BANGLADESH

MOHAMMAD AKRAMUL ISLAM , YASUHIDE NAKAMURAl, SOM‑ARCH WONGKHOMTHONGl,
SADIA A. CHOWDHURY2 AND NoBUKATSU ISHIKAWA3
Received October 21, 1998/Accepted March 10, 1999

Abstract: Tuberculosis is a major public health problem in Bangladesh. It is estimated that about 52,000
deaths due to tuberculosis and 300,000 new tuberculosis cases occurred in 1997 in Bangladesh. Bangladesh

Rural Advancement Committee (BRAO , a Bangladeshi non government organization is implementing acommunity based program for tuberculosis since 1984 in collaboration with the national tuberculosis
program. Community health workers are the nucleus of this initiative. A11 of them are female and selectedfrom rural community. They identify suspected persons for sputum test and provide treatment to thepatients in their own community. In the middle of 1998 this program was reviewed, and the achievements
in 1996 and 1997 were analyzed. Treatment outcomes were evaluated through cohort analysis according to
WH0/International Union Against Tuberculosis and Lung Disease (IUATLD) guidelines. Outcome indica‑
tors defined by WH0/IUATLD were used. A total of 7,946 patients were detected in 34 thanas in 1996 and1997. Out of them, 6,163 (77.6%) were new sputum positive patients. Their sputum conversion and cure rates

were about 90% and 86.7% respectively. This program has achieved the WHO target of 85% cure rate.
Community health workers are playing a key role to control tuberculosis in this approach. Thus this model
could reduce burden on health facilities, reduce patient's costs and increase case detection and cure rate.

Key Words: Community Health Workers, Tuberculosis Control, Directly Observed Treatment, Bangladesh,

Bangladesh Rural Advancement Committee (BRAO

INTRODUCTION

Tuberculosis has been a major public health threat
in Bangladesh. According to the recent review by theTuberculosis is one of leading causes of adult deaths

government of Bangladesh and WHO, about 52,000in the world. According to World Health Organization(WHO) , more than 3 million people die of tuberculosis
in the world every year. It is also estimated thatdeaths and 300,000 new cases were estimated in 1997
(Government of Bangladesh, 1997). There were only 13

approximately 30 million people will die from tuberculo‑

sis in the next ten years if the disease continues tospread at the current rate (WHO, 1996). One thirds offor tuberculosis services in Bangladesh until 1980s(Chowdhury et al.. 1991). The national tuberculosis
program had been integrated with general health ser‑the world's population are already infected with tubercu‑

vices basically at thana health complexes as a policy in

10sis bacillus. Twenty million people are currently
suffering from tuberculosis, and 8 million people gettuberculosis disease every year. More than 50 million
people may have been infected with drug resistantstrains of tuberculosis (WHO, 1995). Tuberculosis isearly 1980s. Thana health complex is a primary healththe only disease that the WHO has ever classified as a
global emergency declared in 1993 (WHO, 1994).

identified in those thana health complexes in 1987
(Government of Bangladesh, 1988). Moreover their

hospitals totally with 1,076 beds and 44 clinics available

care center of thana (sub‑district) covering about
250,000 population. However in 1985, only 124 among
460 thana health complexes provided services for tuber‑culosis. Only 560 sputum positive patients were

1 Department of Community Health, The University of Tokyo, Japan
2 Health and Population Division, BRAC, Dhaka, Bangladesh
3 The Research Institute of Tuberculosis, Tokyo, Japan
Correspondence to: Mohammad Akramul Islam, Department of Community Health, School of International Health, The University ofTokyo, 7‑3‑1 Hongo, Bunkyo‑ku, Tokyo 113‑0033, Japan, Fax: 03‑5684‑3198; e‑mail: akram@m.u‑tokyo.ac.jp

168

treatment completion rate was as below as 25% (Islam,1987). The World Bank review in 1990 estimated thatthe overall case detection rate was less than 20% andtreatment completion rate was below 50% (Veen and
Beex‑Bleumink, 1990). In response to these findings,
the national tuberculosis program revised its strategy
with the guidance from WHO and received the financial
assistance from the World Bank and the Government ofNetherlands. Since 1993, the revised program has been
implernented in order to strengthen the integration of
tuberculosis control into the existing primary healthcare system. It focuses largely on collaboration with

non‑government organizations (NGOs) as they havealready developed primary health care program. Until
mid 1997, the national tuberculosis program covered 324

thanas which was about 70% of the whole country. Of
these thanas, the government covered 214 thanas and
NGOS covered 110 thanas (Ali and Colombani, 1997).
The cure rate in thana health complexes under directgovernment supervision was about 71.1%, while that in
the areas supported by NGOS Was about 81.5% (Ali andColombani, 1997). The recent review shows that theoverall case detection rate is about 25% and treatment
success rate is about 80% (Government of Bangladesh,1997) .

Bangladesh Rural Advancement Committee(BRAO, one of the largest NGOS in Bangladesh has

With the successful outcome in Manikganj thana,
this approach was extended to 10 more thanas in 1992
covering a population of approximately 1.8 million to
examine the scope of scaling up. It also showed thetreatment completion rate as high as 80% (Chowdhury
et al., 1997). Following these encouraging results,
BRAC signed a memorandum of understanding with thegovernrnent of Bangladesh in 1994 to extend tuberculo‑
sis control activities to 120 additional thanas. In 1995

BRAC introduced 8 months short course regimen incollaboration with new national program. The program
achieved the WHO target of 85% cure rate (Chowdhury
et al.. 1997). A study showed that the tuberculosis
prevalence rate was reduced in BRAC areas nearly byhalf within four years in compare to non program areas(Chowdhury et al., 1997). This model is currently being

applied in 60 thanas covering a population of approxi‑
mately 13 million. The experience and results of the
project after introducing and extending short course
treatment are summarized in this paper. The detailstrategy and evolution of the program has been publi‑
shed elsewhere (Ishikawa, 1985; Chowdhury et al., 1991;
Chowdhury et al.. 1997).

MATERIALS AND METHODS
Manpower development

been involved in the activities for poverty alleviation

Community health workers, women of 25‑35 years

and empowerment of the poor since 1972. Along withof age, play a key role in tuberculosis control programthe various community development activities i.e. adultand child education, health, income generation, creditby BRAC. Each community health worker covers 150 toand wornen development, BRAC initiated a pilot com‑munity based tuberculosis control project in 1984 in
Manikganj thana. It covered a population of 220,000
through more than 200 community health workers in

200 households. They are mostly illiterate and membersof village organizations. Community health workers are
selected by the members of village organizations. Vil‑lage organizations were formed by women of the poor‑

est section in the community. Community healthcollaboration with national anti tuberculosis association

workers were trained by BRAC staff about tuberculosisof Bangladesh and government of Bangladesh ( Ishi‑

control for 5 days along with other components of healthsuch as nutrition, reproductive health, safe water supply

kawa, 1985; Chowdhury et al.. 1991). The project area

was approximately 50 km north west to Dhaka. The
aim was to make tuberculosis diagnosis and treatment
services available and accessible to the community
people through community health workers, who alreadyexisted in BRAC initiated community program. In thistuberculosis program, the community health workers
were community level service providers in rural villages

for educating the community, identifying of sympto‑
matic persons, providing treatment to patients, andfollowing them up to ensure their compliance. Twelve
months treatment regimen was then used for treating
tuberculosis patients. The treatment completion rate
was about 79% (Chowdhury et al.. 1991).

and sanitation, acute respiratory infection, expanded
program on immunization and so on. One day refresher
training is also conducted every month to share theinformation and discuss their performance and problems
which they encountered during the last month.
In the beginning of this prograrn a basic training
was given to the staff of all levels both in government
and BRAC, including medical doctors, field level man‑agers and supervisors following the national tuberculo‑

sis program training curriculum. Training materials
and logistics were mostly supplied by the national tuber‑culosis program. WHO training modules for districtlevel managers were used to train medical doctors and169

managers. Laboratory technicians were trained cen‑4) and to sign a bond with two witnesses as a guarantee

trally by national tuberculosis program.

of treatment completion. If the patient is too poor toldentificatiou of patients

pay, he/she receives waiver of bond money. In somecases, community people also pay the bond money for

The community is informed about the danger oftuberculosis, signs and symptoms, diagnosis and treat‑ment facilities, treatment schedule and prevention of
tuberculosis through female forums held by community
health workers. In addition, the male seminars, mosque
forums, doctors seminars, teachers and elite seminars

and Bazaar forums are organized by BRAC staff todisseminate the information. Cured patients also play
an important role in disseminating information, identify‑

ing and motivating symptomatic persons for sputum
examination and motivating the patients to continue
treatment until they are cured.

Persons with cough for more than three weeks aremostly identified by community health workers and thenreferred for sputum examination. Each suspected per‑son is given two sputum containers for collecting spu‑
tum samples one at night and the other at early morning,
and also given instruction on how to collect sputum.

Each suspected person is asked to bring two sputum
specimens to the smearing center. Another spot sputum
specimen is collected from each suspected person at thecenter. Sputum collection centers are set up at BRAC
field offices and at village levels in remote areas toincrease the accessibility of community to the diagnostic

facility. Both centers are managed by BRAC staff andcommunity health workers. Sputum smears are prepar‑

patients. From the bond money, Taka 25 is given to thecommunity health worker for each patient identification
and Taka 100 is given on completion of the treatment.
The remaining Taka 75 is refunded to the patient after
completion of treatment. If the patient defaulted fromthe treatment, community health worker is paid propor‑
tionally and the remaining is kept by the organization.
However if the patient dies, community health worker ispaid proportionally and the remaining is returned to theauthorized family member mentioned in the bond.

The eight months short course treatment regimen(i.e. isoniazid, pyrazinamide, ethambutol and rifampicin

daily for two months followed by isoniazid and thioace‑

tazone daily for six months) is given for new smear
positive pulmonary tuberculosis patients as well as forseriously ill smear negative and extra pulmonary
patients. Follow up sputum examination is made at 2nd,

5th and 8th months of the treatment to monitor the
progress of treatment for sputum positive cases.
Drug taking of the patient is directly observed bycommunity health workers. They collect the drugs fromthe BRAC field office monthly during refreshers train‑
ing and store then in their homes. Patients come to thecommunity health worker's home for drug taking during
the intensive phase of the new treatment and for theentire period in case of retreatment. If the patient fails

ed and the slides are sent to the thana level laboratory

to come, the community health worker visits the patient's

for staining and microscopic examination. The resultsof the sputum examination are sent back to the sympto‑
matic persons through the community health workers.
Fifty percent of positive, 5% negative and 5% follow‑up
sputum slides are cross checked by another laboratoryhome and observe the drug taking. In the case ofseriously ill patient, the community health worker visits

technician every month. To ensure quality control,

the patient's home and observe him/her swallow thedrugs until the patient becomes able to come to thecommunity health worker's house. The streptomycin
injections are also administered by community healthrandomly selected slides are also re‑checked periodi‑

workers for retreatment (failure and relapse) patients.

cally by the national tuberculosis program staff.

Patients also collect drugs during ambulatory phase oftreatment once a week from the community health
When two sputum specimens are positive, treatment

workers home. Patients with drug reactions and compli‑
cations are managed at the community level or sent tofor tuberculosis is initiated by community healththe thana health complex or district tuberculosis clinic.

Treatment

workers under the guidance of BRAC field level staff. If

patients are referred to the government health facility

Supervision and monitoring
The program is supervised and monitored by BRAC

i.e. thana health complex or district tuberculosis clinic.

field and regional level staff. A tuberculosis specialist

Sputum negative patients as well as extra pulmonary
patients are given treatrnent after consultation with thefrom central level monitors the activities and provides
technical support to the program. Monitoring from the

district tuberculosis clinic consultant.

head office is also done by the top managers throughsymptoms persist but the sputum is negative, thePatients are asked to deposit Taka 200 (about US $management information system. The research and170

evaluation division of BRAC also evaluate the program
independently. The government staff at thana, district
and central level and WHO staff members also assess
the quality of the program through periodic field visits
and quarterly progress reports.

To monitor the regular treatment in the commu‑
nity, patients are visited by BRAC staff once a weekduring the intensive phase and twice a month during thecontinuation phase. Community health workers also
visit patients at home once a week during the am‑bulatory phase of treatment. Community healthworkers are visited by BRAC staff periodically tomonitor their activities, records and provide necessary
su pport.

Record keeping for laboratory register, thana tuber‑culosis register, along with sputum request forms, treat‑ment cards and referral forms is maintained at the
BRAC field office. A copy of the treatment card alongwith the home visit card is kept at the patient's home.
Monthly performance reports, quarterly reports on casefinding, sputum conversion and treatment outcome areprepared at thana level by BRAC field level staff toevaluate the outcomes.

1994). Treatment cohort analysis was done according

to WH0/IUATLD guidelines. WH0/IUATLD definedindicators (cured, treatment completed, defaulter,
death, failure, transferred/referred) were used for eval‑uation of clinical outcomes (WHO, 1997b). Patients
who complete the treatment full course and become
sputum negative at 5th and 8th months are defined as
cured. Patients who complete the treatment course but
sputum results at 5th and/or 8th months are not avail‑able are defined as treatment completed. Patients whostop treatment for 2 or more months at any time during
treatment are defined as defaulter. Patients who diedduring treatment in any cause are defined as death.
Patients who become sputum positive at 5th months orlater during treatment are designated as failure.
Patients who are referred or transferred to another
district or institute and treatment outcomes are notknown are defined as referred/transferred.

RESULTS
Total number of patients by category in 1996 and1997 is shown in Table 1. In the two years, a total of
7,946 patients were identified in 34 thanas. Of them,Drugs, equipment, reagents and other logistics are

7,023 (88.4%) were sputum positive, 749 (9.4%) were
sputum negative and 174 (2.2%) were extra‑pulmonary

mostly supplied by the government to BRAC throughtuberculosis patients. Among sputum positive patients,

Collaboration and Coordination with Government and othes NGOS

the district civil surgeon on a quarterly basis. Coordina‑a total of 6,163 (87.7%) were new sputum positivetion meetings with the thana health and family planningpatients.

officer, district civil surgeon and project director of thelaboration with WHO. Meetings with other NGOS

Age and sex distribution of new sputum positive
patients is shown in Table 2. Of a total of 6,163 new
sputum positive patients, 4,473 (72.6%) were male andinvolved in tuberculosis control are held quarterly toshare ideas and experience and to improve the quality of

sputum positive patients were between 25‑54 years old.

national tuberculosis program are held monthly in col‑on going activities in collaboration with WHO. A
referral system with the thana health complexes, dis‑
trict tuberculosis clinics and NGOS have been set up to
avoid duplication of patient registration. Monthly andquarterly reports are given to the thana health and

1,690 (27.4%) were female. About two third of newHighest number of patients were between 35‑44 years
old for male and between 25‑34 years old for female.
Proportionally, there were more patients below 35 yearsof age in female than in male.

family planning officer, district civil surgeon and project

director of the national tuberculosis program.

Data collection and analysis
Analysis of program performance was done by theauthors in the middle of 1998. Quarterly case finding
reports, sputum conversion reports, and treatment out‑

comes from January 1996 to December 1997 were col‑lected from BRAC head office. The national reporting

formats recommended by WH0/International Union
Against Tuberculosis and Lung Disease (IUATLD)
were used for data collection (International Union,

Table 1 Tuberculosis patients identified during
1996 and 1997
Category

1996

1997

Sputum Positive Patients

3 158

3 865

7 , 023 (88 . 4%)

2 729

3 434

6 , 163 (87 . 7%)

89

106

195 (2 . 8%)

pletely treated

340

325

665 (9 . 5%)

Sputum Negative
Extra‑pulmonary

217

532

749 (9 . 4%)

53

121

174 (2 . 2%)‑ N ew‑Rela pse

‑Previously Incom‑

Total

3 , 428

Total

4,518 7,946(100%)

171

Table 2 Age and sex distribution of new sputum positive

DISCUSSIONS

tuberculosis patients in 1996 and 1997

Age

Male

Total

Fema le0‑14

32 (0.7%)

45 (2.7%)

77 (1.2%)

15‑24

376 (8.4%)

258 (15 . 3%)

634 (10 . 3%)

25‑34

950 (21 . 2%)532 (31 . 5%)

1 , 482 (24 . O%)

35‑44

1 , 118 (25 . O%)

397 (23 . 5%)

1 , 515 (24 . 6%)45‑54898 (20 . 1%)

273 (16 . 1%)

1 , 171 (19 . O%)

55‑64

722 (16 . 2%)

144 (8.5%)

866 (14 . 1%)

65 +377 (8.4%)

41 (2.4%)

418 (6.8%)

4,473 (100%) 1,690 (100%)

6,163 (100%)<72 . 6%> <27 . 4%><100%>

Total

Table 3 Sputum conversion results at 2nd month of new
sputum positive tuberculosis patients during
1996 and 1997

The concept of using directly observed treatment
for tuberculosis emerged more than three decades ago
as a result of work in Madras and Hong Kong (Bayerand Wilkinson, 1995). WHO recently claimed that
directly observed treatment with short course regimen(DOTS) is the most cost effective strategy for tubercu‑
losis control (WHO, 1997a). However, according to therecent WHO review, only 23% of the worldwide popula‑tion has an access to the DOTS strategy (Raviglione etal.. 1997). And only about 10% of the world's tuberculo‑
sis patients are under this strategy (WHO, 1997a).

One of the crucial elements of DOTS strategy isthat the health provider watches the patient swallow
every single dose of tuberculosis drugs. It can be done
in hospitalized condition, but the long period of hospital

1996

1997

Total

Sputum Negative

2 , 396 (87 . 8%)

3 , 152 (91 . 8%)

5 , 548 (90 . O%)

Sputum Positive

115 (4.2%)

83 (2 . 4%)

198 (3 . 2%)

Nwang et al.. 1993) . It is also very disruptive and costly

Death

124 (4 . 5%)

130 (3.8%)

254 (4. 1%)

Def aulted

45 (1.7%)

37 (1. 1%)

82 (1 .4%)

for the families of patients (Foster, 1990; Saunderson,1995). In many developing countries hospital beds areTransf erred/Ref erred

49 (1 .8%)32, (O . 9%)

81 (1 .3%)

not adequate to admit all infectious tuberculosis

2,729 (100%) 3,434 (100%) 6, 163 (100%)

patients and therefore it is not feasible such as in
Bangladesh and China (Chowdhury et al.. 1991; China,

Total

stay for DOTS increases the burden of hospitals in highepidemic developing countries as seen in Africa (Okot‑

1996) .

Table 4 Treatment outcorne of new sputum positive
tuberculosis patients during 1996 and 1997 (till June)

There are also problems in promoting DOTS at out
patient clinics, since health services are not easily acces‑

1996

Cured
Treatment Completed

Total

till June 1997

2 , 312 (84 . 7%) 1 , 463 (89 . 9%)sible to most of the community people particularly in

3 , 775 (86 . 7%)

rural areas in developing countries (Maher et al.. 1997) .

6 (O. 1%)

Patients either has to come to clinic every day or health

6 (0.2%)

Died

233 (8 .6%)

99 (6 . 1%)

332 (7. 6%)

worker has to go to patient's house.

Failure52 (1 .9%)22 (1 .3%)

74 (1 .7%)

Def aulted

55 (2 . O%)

28 (1. 7%)

83 (1 .9%)

Ref erred/Transf erred

71 (2.6%)

16 (1 .O%)

87 (2.0%)

To ensure DOTS approach, an alternative model ofproviding care for tuberculosis patients needs to be
explored at community level based on community parti‑
cipation. The BRAC initiative for tuberculosis control

Total

2,729 (100%) 1, 628 (100%) 4,357 (100%)

through utilization' of community based voluntary health

Sputum conversion results of new sputum positive
patients at 2nd month are shown in Table 3. Of a totalof 6,163 new sputum positive patients, 5,548 (90.0%)
became sputum negative after initial intensive phase of
the treatment. Deaths during the first two months were254 (4.1%) among new patients.
Treatment outcome after 12‑15 months of diagnosisof new sputum positive patients is shown in Table 4.

Among 4,357 new sputum positive patients, 3,775(86.7%) were cured; 332 (7.6%) d, ied; 74 (1.7%) failed intreatment and 83 (1.9%) patients defaulted.

workers (i.e. community health workers) has proved to
be an example of the alternative approach, achieving
WHO target of curing 85% of diagnosed cases consis‑
tently over few years (Chowdhury et al.. 1997; Kochi,1997). Utilization of available human resources in thecommunity as trained volunteers and community healthworkers achieved high cure and treatment completion
rates in Africa as well (Wilkinson et al.. 1996; Maher etal.. 1997). Supervised chemotherapy on out door basis
by village doctors in China also contributed to achieve
one of the highest cure rate in the world (China, 1996;

WHO, 1997a). Involvement of community healthworkers in the philippines has also increased the curerate (Mantala, 1997).

172

The important features of the BRAC TB programare 1) the community based approach; where commu‑
nity health workers are selected from the poorest sec‑tion of the community; diagnostic and treatment facil‑
ities are available at the door step of people and services

are organized by them, 2) financial bond for treatmentcompletion and incentive scheme for community healthworkers to supervise treatment, 3) training and supervi‑

sion of community health workers by motivated BRAC
staff, 4) effective short course drug regimen, and 5)
collaboration and support from the government.
Community health workers are more trusted by thecommunity because they are selected by them. They are
respected by the villagers in the program and thus they

Furthermore, a cost‑effectiveness analysis of thismodel may determine whether the involvement of com‑munity health workers in national tuberculosis program

can be more cost‑effective approach. In the global
expansion of DOTS strategy, each government needs todevelop a sustainable program. This model of involving
community health workers in tuberculosis control pro‑gram can be an alternative approach to strengthen thenational tuberculosis program by increasing the accessi‑
bility of tuberculosis services, particularly in a remoteareas, where services are inadequate. The partnershipamong government, NGOS and community is essential
for sustainable implementation of DOTS strategy tocontrol tuberculosis.

feel prestige to serve the people (Ishikawa, 1985) . They

could easily find symptomatic patients as they are fromACKNOWLEDGEMENT

same community and know each other. Patients basi‑cally get free treatment in their community except theWe thank all BRAC staff members working for thebond money. Therefore, they can continue their eco‑nomic activities and take care of their families, as
majority (77.9%) patients are from econornically pro‑ductive age group between 15‑54 years old (Table 2).
The system of bond money builds a mutual understand‑ing between patients and community health workers,
which makes each accountable to the other for better
quality of care and makes treatment less expensive(Ishikawa, 1985). The amount of bond money is also
affordable by majority patients, as it was found that83% patients paid full amount of bond money (Osaki,

tuberculosis control program for their efforts and Mr. F.

H. Abed, Executive Director of BRAC for his leadershipin this regard. We are grateful to Dr. A.K.Md. Ahsan
Ali and his colleagues of the national tuberculosis pro‑gram for their assistance. We also thank Dr. Jacob
Kumaresan and WHO staff for their support. BRAC isbeing supported by government of Bangladesh, national
anti tuberculosis association of Bangladesh, the research

institute of tuberculosis‑Japan, WHO, DFID (UK) ,SIDA and UNICEF.

1995) .

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This study shows that the death rate is about 7.6%

by the end of treatment (Table 4). More than half
(4.1%) of them died within the first two months oftreatment initiation (Table 3) . On the other hand, there
is a big gap between the male‑female ratio (73:27) , eventhough BRAC prograrn utilizes female community
health workers (Table 2). These indicate that diagnosis
is still delayed and strong stigma and fear to tuberculo‑
sis exist in the community (Fair et al.. 1997). This gap

between male and female ratio may be caused by poor
women's access to health services due to heavy work‑load, as well as lack of mobility, independence andaccess to cash (Hudelson, 1996). However, proportion‑
ally more females (49.5%) were diagnosed than males(30.3%) below 35 years of age (Table 2). This may due
to feTnales have higher risk to develop disease thanmales in reproductive age (Dolin, 1998). It was also
observed in India that females have 130% higher risk todevelop disease than males between the age of 10 and 44
years (Olakowski, 1973).

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175

Trop. Med. Hyg., Vol. 27, No. 2, 1999, pp. 175 180

PREVALENCE OF SCHISTOSOMIASISJAPONICA AMONG SCHOOLCHILDREN
AND ANIMAL RESERVOIRS IN ORIENTALMINDORO, PHILIPPINESJUN MATSUMOTO , MASASHI KIRlNOK11, SATORU KAWAI , YUICHI CHIGUSA1EUNICE J. ILAGAN2, BENEFICO E. DUCUSIN3, KAZUO YASURAOKA
AND HAJIME MATSUDA
Received February 15, 1999/Accepted March 31, 1999

Abstract: A survey was conducted in Oriental Mindoro, Philippines in 1997 and 1998 for the purpose of
estimating the current situation of schistosomiasis japonica in the area. The prevalence rate in schoolchil

dren determined by enzyme ‑ Iinked immunosorbent assay detecting the parasite egg ‑ specific immuno‑
globulin G revealed that the disease was more highly endemic in Malabo (70.7%) than in the other villages
studied (31.8% in San Pedro and 36.4% in San Narciso), in spite of the fact that all of these villages were
10cated near to each other. The prevalence rates determined by stool examination or necropsy of animalreservoirs in San Pedro, San Narciso and Malabo were as follows; dogs: 9.7%, 7.4% and 19.2%; rats: 10.4%,
8.7% and 26.1%, respectively. Water buffaloes were all negative in all villages. These results showed thatthe prevalences of schistosomiasis japonica in animal reservoirs have intimate correlation with that inschoolchildren. In Malabo, the colonies of intermediate‑host snails were located very close to the resident
area, which might be the major cause of high prevalence of the disease.
Key words: schistosomiasis japonica, Philippines, schoolchildren, animal reservoirs, serological test, stool

examination

INTRODUCTION
Schistosomiasis japonica is one of the most impor‑tant helminthic diseases distributed over Southeast Asia

were carried out on the prevalences of schistosomiasis

japonica in various animals (Pesigan et al.. 1958;
Oshima et al., 1978; Kamiya et al.. 1980; Fernandez etal., 1982; Yasuraoka et al., 1996) . These reports showed

and China. Epidemiological surveys conducted so far inthat several mammals such as dogs, pigs, cows, water

Oriental Mindoro, Philippines (Tubangui and Pasco,

buffaloes and field rats were involved in the transmis‑

1941; Hunter et al.. 1950; Saniel, 1951; Carney et al..
1981; Chigusa et al.. 1997) showed that the disease wassion of the disease. In spite of the fact mentioned above,

highly endemic in the area, especially around Lake

conducted in Mindoro Island. In this survey, we tried toreveal the prevalences among animal reservoirs living in

Nau j an.

no survey on the prevalences in animal reservoirs was

In contrast to the transmission of other schistosome
species, animal reservoirs contribute to the transmission

the given area.

of Schistosoma japonicum in endemic areas. Thus, it isindispensable to estimate the prevalences among mam‑malian hosts to control the disease in the area.
In other islands in the Philippines, investigations

studies on schistosomiasis japonica in Oriental Mindoro,
Philippines to know the current situation of the disease

Since 1994, we have continued epidemiologicaland accumulate the baseline data for future control
campaigns. The purpose of this report is to show the1 Department of Medical Zoology, Dokkyo University School of Medicine, 880 Kitakobayashi, Mibu‑machi, Shimotsuga‑gun, 321‑
0293 Tochigi, Japan
2 Schistosomiasis Control Team, Victoria, Oriental Mindoro, Philippines
3 Schistosomiasis Control Service, Department of Health, Manila, Philippines

Correspondence: Hajime Matsuda, Department of Medical Zoology, Dokkyo University School of Medicine, Mibu, Tochigi
321‑0293, Japan E‑mail: hmatsuda@dokkyomed.ac.jp

176

results of epidemiological studies on the prevalencesamong schoolchildren and animal reservoirs in threeendemic villages (San Pedro, San Narciso and Malabo)
in Oriental Mindoro, Philippines, conducted in 1997 and
1998.

MATERIALS AND METHODS
Study area and period
Mindoro Island is the seventh in size among thePhilippine archipelago and is situated just south ofLuzon (Fig. 1). The island has a big mountain, which
divides the island into two provinces: Oriental Mindoro

and Occidental Mindoro. In the lowland of Oriental
Mindoro lies Lake Naujan, around which exist manyfrom schoolchildren in Minas. This village is locatedabout fifteen kilorneters west of the villages studied, andproved in our previous study to be a non‑endemic areaof schistosomiasis (unpublished data). In addition,
serum samples were obtained from eight Japanese stu‑
dents without any history of schistosome infection.
The parasite specific antibody titer was measured

by enzyme‑1inked immunosorbent assay (ELISA) fol‑lowing the previous report (Matsuda et al.. 1984).
Briefly, the assay was performed in microtiter plates
and plasma samples were used at a dilution of I : 200.
To detect the parasite specific immunoglobulin, horse‑radish peroxidase (HRP) ‑conjugated goat anti‑humanlgG polyclonal antibody (ICN Pharmaceuticals Inc., U.
S.A., cat. No. 674161) was used at a dilution of I : 60,000.

endemic areas of schistosomiasis japonica. As our study
area, we selected three villages in the west side of the

The substrate was 2‑2'‑azino‑di‑ (3‑ethylbenzthiazoline
sulfonic acid) (ABTS, Sigma, St. Louis, U.S.A., cat. No.

lake: San Pedro, San Narciso and Malabo. The climate

A‑1888). S. japonicum‑egg (SjE) antigen was used toof the area is classified as tropical‑wet.

measure the parasite specific antibodies. The prepara‑tion of SjE antigen was previously described (Matsuda

The survey was conducted from 23 July to 20
August in 1997 and from 23 July to 10 August in 1998,
during the period of rainy season in the area.

et al.. 1981). Samples of more than 0.25 of opticaldensity at 415 nm were determined positive, following
the previous report (Matsuda et al.. 1984).

Serological study of schoolchildren

A small amount of blood sample was taken fromschoolchildren of the grade one to six (aged six totwelve years) through finger prick and collected in a
heparinized capillary tube. The number of specimens
collected totaled up to 424: 132 in San Pedro, 118 in San

Narciso and 174 in Malabo. And for the purpose ofcomparing the results, 141 serum samples were collected"'tv"""t""'LvbvblbvbvL'tl"t'Plb'tbvtt bvb't' 'b""'t'tl'v l'vb I"Ibvt vt"'bv vbl'b'b""t"t'L'tlb'bvbvtL't" vbvL 'tv vbvb'tv'vbv""b'bvbvbvt'bvt'b'b""I""L!Lvb 'b ""Ib'b'b'blbvb'LI
lbvL'tvtvL"'LvbvLv'vLvbvtl "Ilbv"Lv" 'tvL,, b

Luzon ls'

'LvblLvb'blb'Lvtvbvblb'LvL'Lvtvb'Lvb'bvt'tlbLlt
tP""'b"vbl"b"'1"tvb'b'bvb'Lv"t 'b""'bILL'bv"b'tvtvL'tv'vbv'vbbvLvtIvt"vtv Iv"'

L'tv v'v'v v'vb't' vbv'l"LvtLv"t'tvt'b'LvLvbvtvtLvt'tvL'bvb ILI"t:blb Ib'bv'l"t'b"""vt'blb"'b'b' vb'b
vb'bvbvbvt'b'blb'b'L'blb"'bl" 'b'L

b"v'v v'vtvtvL't"'ttb'L"'b'L

LvLvLv'vblLvLvLvLv'vt"""'bv'It'Lvb'bvb'b"'b'b"vL
tblL"vbltl""b'b "'b"'bv'v'vv'vtb'b' ""b'b"

vbvtv
vtv'vtvLt"b'blbvblbvtlblltILILlt"
lt

t'blLv"blbvbvbvb'b':"
OSO b'i':"I'vbv'ii''bvb'bvb. /'#;san Narci
v vt"vblbv"b "'San pedr ' ILltlbILN'P"'Plb"'t''b'tvb'bltlL'L'b'bvbvb'b:

L"I"b'b '? 'c't b lltbn :vLvLvltvbvbv,b,,,b,LL,b:/ 'Fecal samples of schoolchildren were brought
together to their own schools. The donors of the fecal
samples were not necessarily identical to those of theblood specimens. We walked along the path collectingstools of dogs and water buffaloes, and covered almost
all resident area. The numbers of stool samples col‑lected from humans and animals in each village areshown in Table 2. All of the fecal specimens were'<<<<<<<<< <<<<<<<<< <<<<<<<<<<<<< .<<<.<< *<..<* ***... *.*....*...
..*....'****.*********************************' *'"'bvLv'lbl'vtvtv'vL"b'P'tb'bv"'It'Llt"""'blbvL'b'tvbvb'Lltv""L'LI'vLvbvbv'vb
vLvb

Stool examination and necropsy'tltvtv'vLvLvL'bv l'v'l

M alabO ":'s' ¥ :Lake Nauian

IL

)

C

[1 ;Mindanaoh I)s

e

II '

Mindoro ISland The Philippine
ISland S

treated by formalin‑detergent technique (Moody, 1986)
and examined for schistosome infection.
In addition, 202 (in San Pedro), 150 (in San Nar‑ciso) and 283 (in Malabo) of field rats (identified as
Rattus rattus mindanensis) were caught by village vol‑unteers (Table 2). These animals were necropsied, andTable I Prevalence of schistosomiasis japonica among
schoolchildren and animal reservoirs in Oriental
Mindoro, Philippines.

Area

No. examined No. positive positive rate (%)

San Pedro132

schoolchildren and animal reservoirs in Oriental
Mindoro, Philippines.

San Narciso

MalaboBrief maps of the Philippine Islands (right) and the

Total

Figure I Prevalence of schistosomiasis japonica among

northeast part of Mindoro Island (1eft) , showing

the location of three villages (San Pedro, San
Narciso and Malabo) where this survey was con‑ducted.

42

31 . 8118

43

36 . 4174

123

70 . 7424

208

49 . 1The prevalence of schistosomiasis japonica among schoolchil‑dren in Oriental Mindoro, Philippines, estimated by enzyme‑
linked immunosorbent assay detecting the parasite‑specific Im‑
munoglobulin G.

177

Table 2 Prevalence of schistosomiasis japonica among

O.D. @ 41 5 nm

schoolchildren and anirnal reservoirs in Orien‑tal Mindro, Philippines.

1 .8

1 .6

.,.

I
,
,
,

...

1 .4

. :.

l
,

1 .2

,
,

0.8
0.6

' Y:
:{:

,p,
,

... J

,
:

'TI

,l
,

. 8 D

,

,

water

,
,

,

buf f aloes

..

t

0.4
0.2

!D

T
.d.
'I

tj " l

dogs

'r

i,,

,

'n
l'u

l

field rats

‑1r
l,, ‑ =‑ ‑ =‑'i'l !
!Id'l,.ij L 5ii li:li D

O‑San San Malabo non‑endemic

Pedro Narciso area

Figure 2 Prevalence of schistosomiasis japonica among
schoolchildren and animal reservoirs in Oriental
Mindoro, Philippines.
The result of serological examination for Schis ‑tosoma japonicum‑infection among schoolchildren

in San Pedro (n=132), San Narciso (n=118),
Malabo (n=174) and Minas (a non‑endemic areaof schistosomiasis, n=141) in Oriental Mindoro,
Philippines. The parasite‑specific immunoglobulin
G was detected by enzyme‑1inked immunosorbent
assay. Open squares and vertical bars represent
mean O.D. and S.D., respectively. And dashed line
indicates cut off limit. The mean O.D. and S.D. of

normal controls of Japanese students were 0.033
and 0.020, respectively.

their mesenteric and portal veins were thoroughly
examined for flukes and foci due to schistosome infec‑
tion microscopically by the press preparation technique22

16 . 7

Total

329

30

9.1

San Pedro
San Narciso

21

9.7
7.4

Malabo

216
148
255

49

1'9 . 2

Total

619

81

13 . 1San Pedro
San Narciso

o

o

o

o

Malabo

86
59
126

o

o

Total

271

o

o

San Pedro
San Narciso

21

10 . 413

8.7

Malabo

202
150
283

74

26 . 1

Total

635

108

17 . O

5

11

The results of stool examination (schoolchildren, dogs andwater buffaloes) or necropsy (field rats) for the detection of
Schistosoma japonicum‑infection in various kinds of final hostsof the parasite in Oriental Mindoro, Philippines.

All of the specimens in Minas, non‑endemic area ofthe disease, were determined to be negative. Normal
controls of Japanese students (n=8) were all negative,

and their mean O.D. and S.D. were 0.033 and 0.020,
res pectively.

Stool examination and necropsy
The results of stool examination or necropsy forschistosome infection are summarized in Table 2. In thestool examination also, schoolchildren in Malabo
showed higher prevalence of the disease than those in
the other two villages studied, although the positive
rates estimated were much lower than in the serologicaltest.

The parasitological examinations showed that theprevalence among animal reservoirs were relativelyof the tissues. 'RESULTS
Serological examination
Seroepidemiological survey of schoolchildren (theresult is shown in Fig. 2 and Table 1) detecting theparasite specific antibody revealed that schistosomiasis
japonica was still endemic in the given area, especiallyin Malabo in which the prevalence of the disease wasrelatively higher (positive rate was 70.7%) than theother villages studied.

3.8
4.5

San Narciso

,

1 .O

3

Malabo130
67
132

schoolchildren San Pedro. tP ',,. .

No,collected , , P o s i t i v e&exarrired No. posrtrve rate (%)

Area

H ost

..

higher in Malabo than those in San Pedro and San
Narciso. The positive rates of schistosome‑infection indogs and field rats were more than twice as high in
Malabo as in the other two villages, but we could not
find any positive case of water buffalo in all the areastudied.

DISCUSSION
This survey undergone in three villages (San Pedro,

178

GRowrHFORESTFOREST"( SECONDFORMERLY'ALABOI LAKE NAUJAN j

SAN NARCISOFOREST

lll l

JL

)

NAU8AGUJAVIER SWAMP
CALAPANCREExl

JLL SEOONO Gnowm

IL JL

r･･.+* :..... ?. ‑. '･･
JL * 'S:.
L $･･

IL

iL I REST

al ll

eol Al,y

8A,,NARa8Q‑ HAIJIISChOOI E:!:'(:,,.;? ; i(:t ;. ; :'r . :6';

CrrRuS FARN

ll

POeLACla, I Il"'̲'r.

Il,i . *""v,5: '1'11̲1

SChoollll

a ciTRUS FARM

l: l

ll

,, '2:':,, ttL S

l aL

Il

J

MALA ARIVERlI Il ll l ll 111 11 ll'll
I I 111l lll

SECOND GROWrH FOREST

r,F1"t "'DANGONGO CfIEEK

lill lpoeLAaal M*'

Il I Illlll I ItIs' I a l

I I

<5"I'c!."l. * :"':aL JLLI ‑';;:':.'.
/ ,̲ ..F*";*(‑*,‑... . !.

TO BRGy.

DuoNGAN

8ARANGAY OF SAN tS,DRO

TO SOCORRO/ NA11ONAL ROAD
Figure 3 Prevalence of schistosomiasis japonica among schoolchildren and anirnal reservoirs inOriental Mindoro, Philippins.
A sketch map of Malabo village, Oriental Mindoro, Philippines. Closed squares indicate
houses and arrow heads colonies of intermediate host snails of Schistosoma japonicum.
As shown in the map, the colonies were located along the central paths in the village.

San Narciso and Malabo) in Oriental Mindoro,
Philippines, showed that schistosomiasis japonica iscurrently endemic in the area.

Seroepidemiological study for schistosome‑infec‑
tion among schoolchildren revealed that the prevalenceof the disease was relatively higher in Malabo than in
the other villages studied. As shown in the sketch map(Fig. 3), we found snail colonies with highly infectedintermediate‑host snails (Oncomelania quadrasi) besidethe paths running through the center of the resident
area. Schoolchildren in this village, we suppose, wererepeatedly exposed to cercarial infection on the way toand from school every time when the paths are flooded.
As indicated by this example, the location of the snailcolonies in relation to the resident areas is one of very
important factors in the transmission of the disease.
Prevalence rate of the disease among schoolchildren

estimated by stool examination was much lower thanthat determined by serological test. In S. japonicum
infection, the daily egg count in feces is relatively low

and irregular compared with those found in other hel‑minthic infections. Although twice or more of fecal
examinations would have improved sensitivity of thetest, we could perform the test only once under limited
condition, with the result that the prevalence rate may
have been underestimated.

On the other hand, serological examinations arehighly sensitive and useful in large‑scale screening,
despite the fact that these kinds of methods cannot befree from following disadvantages, such as possibility offalse positive cases mainly due to cross reaction to otherparasitic infections, inability to discriminate active
infections from very old infections without any living
worms in the subjects. In this study, of 147 donors whooffered both serum and stool samples, egg‑positive
cases was 10.2% (15/147), among which as high as
93.3% (14/15) was determied positive in serodiagnosis
also (data not shown in results) . On the other hand, of

all the donors with the both specimens, 47.6% (70/147)
was positive in serological test, among which only 20.0%

179(14/70) was egg positive in stool examination. These
results strongly confirmed that serological diagnoses
are highly sensitive for the detection of S. japonicum
infection compared with stool examinations. In order tomake up for the defects in each diagnostic method, bothof serological and stool examinations should be em‑from the staff of Schistosomiasis Control Team in
Victoria, Oriental Mindoro, Philippines. We finally
thank village captains and villagers in the study areas
for their cooperation.
This study received financial support from Sasaka‑

wa Memorial Health Foundation.

ployed to estimate the current situation of the disease.

Stool examination of various final hosts indicatedintimate correlation between the prevalence rates of thedisease among schoolchildren and those of various ani‑1 ) Carney, W.P., Banzon, T., Veyra, V., Papasin, M.C. andmal hosts. Among three villages studied, Malabo

Cross, J.H. (1981): Intestinal parasites of man in

showed the highest prevalence rates in animal hosts aswell as in schoolchildren. As humans are suitable final
hosts of S. japonicum and play the major role in trans‑

Oriental Mindoro, Philippines, with emphasis on schis‑mission of the disease due to their behavior, principally2 ) Chigusa, Y., Kirinoki, M., Yokoi, H., Kawai, S.. Ma‑water use practices and indiscriminated defecation in
the field, it is supposed that the high prevalence inhumans has great influence on the prevalences in animalreservoirs in an endemic area. The results of stool
examinations in humans and animal reservoirs support‑

tsuda, H., Bugawan, L.E. and Blas, B.L. (1997) : A survey

REFERENCES

tosomiasis. Southeast Asian J. Trop. Med. Pub. Hlth.,
12, 13‑18

of intestinal parasitic infections in San Narciso, Victo‑

ria, Oriental Mindoro, Philippines. Jpn. J. Trop. Med.
Hyg., 25, 7‑93 ) Fernandez, T.J.J., Petilla, T. and Banez, B. (1982): An

ed this expectation.

epidemiological study on Schistosoma japordcum inPesigan et al. (1958) determined the transmission
index, which express relative transmission potential fordifferent hosts in an endemic area of the disease. In

domestic animals in Leyte, Philippines. Southeast Asiandetermining the index, we have to take four factors into

consideration: population, prevalence and mean daily
egg output of the hosts as well as the hatchability ofeggs excreted. According to their report, in Leyte
Island, dogs showed the highest index rate (14.4%)
among animal reservoirs, following humans (75.7%).
Although the transmission index in Mindoro Island has
not yet determined, we guess that the situation is almost
the sarne. It is our intention to clarify the transmission

dynamics of schistosomiasis japonica in Mindoro Islandby e timating the index rates of final hosts living in the

J. Trop. Med. Pub. Hlth., 13, 575‑579
4 ) Hunter, G.W., Dillahunt. J.A. and Dalton, H.C. (1950):

The epidemiology of schistosomiasis japonica in thePhilippine Islands and Japan. I. Surveys for schis‑tosomiasis japonica on Mindoro, Philippine Islands.
Am. J. Trop. Med. Hyg., 30, 411‑429
5 ) Kamiya, H., Tada, Y., Matsuda, H., Tanaka, H., Blas, B.

L., Nosefias, J.S. and Santos, A.T., Jr. (1980): Annual

fluctuation of Schistosoma japonicum infection in fieldrats, Rattus rattus mindanensis, in Dagami, Leyte,
Philippines. Jpn. J. Exp. Med., 50, 375‑382

6 ) Matsuda, H., Nakao, M., Tanaka, H., Nagata, T. andSantos, A.T., Jr. (1981): A study of ELISA for schis‑area.

tosomiasis japonica using 5‑arninosalicylic acid, a sub‑Due to zoonotic nature of S. japonicum, we cannot
eliminate the disease without controlling the infection

strate of peroxidase‑1abelled antibody. Jpn. J. Par‑among animal reservoirs. Further surveys are .contem‑
plated to monitor the prevalences of the disease among
various animal reservoirs under control operation, such7 ) Matsuda, H., Tanaka, H., Blas, B.L., Nosefias, J.S.,

as treatment of human cases with praziquantel andazoline sulfonic acid) , as the substrate of peroxidase andvegetation removal followed by chemical molluscicid‑

its application to the diagnosis of schistosomiasis. Jpn.

asitol., 30, 363‑372

Tokawa, T. and Ohsawa, S. (1984): Evaluation of
ELISA with ABTS, 2‑2'‑azino‑di‑(3‑ethylbenzthi‑

J. Exp. Med., 54, 131‑138

ing.

ACKNOWLEDGEMENTS
We wish to express our gratitude to Dr. Tatsuo
Yabe of Kanagawa Prefectural Public Health Labora‑8 ) Moody, A.H. (1986): An introduction to selected diag‑nostic methods for parasites available as kits for small

health units. Laboratory in Health Care‑Developing
Country. Proceedings of the 17th Congress of the Inter‑national Association of Medical Laboratory Technolo‑

tories for the identification of the field rats. We would

gists. Doddington: Trop. Hlth Technologic, pp. 28‑29

like to express sincere appreciation to practical support

9 ) Oshima, S.. Yasuraoka, K., Irie, Y., Blas, B.L., Nosehas,

180

J.S. and Santos, A.T., Jr. (1978): Final localization ofAss., 27, 254‑255

Schistosoma japoleicum in the lungs of field rats, Rattus

12) Tubangui, M.A. and Pasco, A.M. (1941): Studies on themindanensis, in Leyte, Philippines. Jpn. J. Exp. Med., 48,

geographical distribution incidence, and control of schis‑503‑509

tosomiasis japonica in the Philippines. Phil. J. Sci., 74,

10) Pesigan, T.P., Farooq, M.. Hariston, N.G., Jauregui, J.J.,

Garcia, E.G.. Santos, A.T., Santos, B.C. and Besa. A.

301‑327
13) Yasuraoka, K., Blas, B.L., Matsuda, H., Irie, Y., Nihei,(1958): Studies on Schistosoma japonicum infection in

N.. Ohmae, H., Yokoi, H., Hambre, R., Pangilinan, R.,

the Philippines.
I. General consideration andepidemiology. Bull. WHO, 18, 345‑455
11) Saniel, V.F. (1951): Survey of Mindoro. J. Phil. Med.

Autentico, C. and Tanaka, H. (1996) : Approaches to theelimination of schistosomiasis on Bohol Island, Philip‑
pines. Jpn. J. Parasitol., 45, 391‑399

181

Jpn．J．Trop．Med．Hyg．，Vo1．27，No．1，1999，pp、181−188

CLINICAL

MALARIA

MULTIDRUG
SRlvlcHAWEERAPONGAND

RESISTANCE
IN

KRuDsooD，WATcHAREE

manifestations

clinicalpresentations

Signs

symptoms

andofmalariaarenonspecificincludefever，headache，muscle

hepatosplenomegaly，jaundice

and

dark

interactions

urine．In

betweenmild

BUssARATIDAND

LooAREEsuwAN

December9，1998／Accepted

complex

SILAcHAMRooN，

VIRIYAvEJAKuL，VALAI

Receivedreflect

OF

FALCIPARUM

THAILAND

CHoKEJINDAcHAI，UDoMsAK

PHuMRATANAPRAPIN，PARNPEN

SoRNCHAI

Abstract：Clinical

TREATMENT

April27，1999

and

the

range

from

host，thepain，abdominal
malaria，these

asymptomatictosevere．The

environment，andtheparasites。

pain，anorexia，nausea，vomiting，

signs

and

symptoms

cannotdifferenti−

ate malaria from common cold，influenza or other systemic diseases．Fever and malaise in malaria are
believed to result from the release of endogenous cytokines［e．g．interleukin1，6and8（IL−1，IL−6，IL−8）
and tumor necrotic factor一α（TNF一α）］in response to parasite antigens．Other signs and symptoms ofmalaria

are also associated with the rupture of parasitized red cells．In severe malaria，the clinicalmanifestations included cerebral malaria，pulmonary edema，renal failure，anaemia，andjaundice、Signs andsymptoms of cerebral malaria are as follow alteration of consciousness，coma，dysconjugated eyeballs andconvulsions．Among fatal cases，80％died within the first48hrs of admission while the rest，death resulted
fromcomplications

such

as

acute

renal

failure，pulmonary

edema，bacterial

infection，and

lacticacidosis

92％of the survivors had completed recovery．Treatment of multidrug resistant falcipamm malaria in
Thailand is complicated．New antimalarial（1rugs have been investigated at the Hospital for Tropical
Diseasesintemisinin

are

also

with

total

dose

a

provedtion

therecentsuccessfully

with

given

plus

Bangkok

Hospitalof600to750mg

produced

cure

the

cure

treatmentofsevererates

improved

a

cure

rate

mefloquineinvarious

over5days

otherwise，the

at

gave

drug

derivatives

the

for

mefloquine

derivatives

years．Artemisinine

testedcombinations

are

such

for

as

artesunate，artemether，arteether，dihydroar−

Tropicalrates

Diseases．Artesunateof80to95％．Artesunate

malaria．The

artemisininto95−100％．Dihydroartemisinin

of90％

At

present，studies

doses

and

durationstill

recommendedforderivatives

when

alone

with

a

the

combination

with

of

treatment

all

adult

and

are

being

patients

artemether

suppositories

been

used

in

combina−

total

dose

of480mgofartemisinin

investigated。Until

suffering

alone

have

from

acute

provenuncom−

plicated falcipamm malaria contracted in multidrug resistant areas．
In severe malaria，the choice of antimalarial chemotherapy depends on the clinical severity，the drug
sensitivity

of

the

parasites，anddrug．Qinghaosu

and

its

falciparum

malaria．Theirhowever，therecrudescenttreatment

are

vital

and

the

antimalarial

drug

is

neededincludescarefulapPropriateKeyavailability

haveeffectiveness
rate

and

is

rather

is

to

aim

been

in

patient

diagnosis

the

fluid

intakegood

nursingandsresistantfalciparum

the

of

in

is

the

drug．Quinine

treating

parasites

life．Prompt

urine

made．Other

available

and

been

extensively

documented，

malaria，earlya（1ministrationofsymptomatic

output，frequent

widelyuncomplicatedhavesevere

is

both

an

and

observations

diagnosis

adequatesevere

and

early

and

effective

supportive

treatmentforcomplications

with

care．

resistance，treatment，Thailand

problem in Thailand． Therapeutic failures with all
available antimalarial drugs arewelldocumented．With

INTRODUCTION
Multi−drugpreparation

successfullyhigh（10−30％）．Intreating

save

once

words：Malaria，drug

and

used

eliminatingof

monitoring

treatmentthederivatives

malariaisaserious

thisdeteriorating

situation，new

drugs

Bangkok Hospital for Tropical Diseases，Faculty of Tropical Medicine，Mahidol University
Address for correspondence：Professor S．Looareesuwan，Dean，Faculty of Tropical Medicine，420／6Rajavithee
10400，Thailand，Fax（662）247−1688E−mail：tmslr＠mucc．mahidoLac、thareurgently

Road，Bangkok

182

needed. The new drugs and drugs in combinations havebeen studied in Bangkok Hospital for Tropical Diseases
since 1988. This paper is an overview of clinical studies

on clinical malaria and treatment of multidrug resis‑
tance falciparum malaria in Thailand.
Clinical Manifestations
Rupture of intraerythrocytic schizonts coincides
with paroxysms of fever and this has led to the tradi‑tional categorization of the different types of humanmalaria. Nowadays, these terms are not recommended,because patterns of fever are variable and some patientsdie from Plasmodium falciparum even though they neverdevelop periodic fever, particularly in nonimmune

explain some reports of patients with cerebral malaria

in whom no parasites were demonstrated on a periph‑eral blood smear. On examination most patients areusually febrile and in unarousable coma. A few patients

who have very severe infection have a subnormal tem‑
perature. Admission temperature usually exceeds 38.0‑
39.0'C in most cases and rises above 39.0'C during thefirst two days of hospitalization. There is no classicalpattern of fever in cerebral malaria. Rigors are rare incomatose patients but a sustained high fever, which is
resistant to antipyretic treatment, is commonly found.

The skin temperature is cool relative to the rectal
temperature in hypoglycemic or shocked patients.
Jaundice is common in adult patients and anemia

patients and during the early stage of illness. Syrhptoms

develops rapidly in severe malaria. The chest is usuallyand signs of malaria are vague including fever, head‑ache, malaise, Iassitude, fatigue, muscle pain and loss ofnormal on clinical examination although aspiration
pneumonia or pulmonary edema may develop. Changes

appetite. These are not specific for malaria and aresimilar to the symptoms of influenza or other viralin respiration can be a warning sign of hypoglycemia,
metabolic acidosis, pneumonia, and pulmonary edema,

infections. It is essential to take blood sarnples for
examination for malaria parasites.

but may occur as a result of high fever alone. Therefore
careful examination and proper investigations should be
performed in all patients.

In severe malaria (Table 1) , alteration of conscious‑

ness is the most prominent manifestation. The patient
usually presents with a history of fever for several days

and loss of consciousness, which may be sudden follow‑

ing one or more grandmal seizures. In approximately
50% of patients over 6 years of age, coma follows a

Hepatosplenomegaly is common. In Thailand, halfof the adults and children over 6 years with cerebral

malaria have a palpable liver or spleen. Massive
splenomegaly is most umusual in severe malaria.
Abdominal pain and tenderness are prominent in someconvulsion. In young children with cerebral malaria, thepatients. In children, the physical signs are similar tohistory may be very short. Vomiting may also occur;

adults except that convulsions are more common, he‑patomegaly may be prominent, and anemia is common;

this is important to know because aspiration pneumonia

could develop before admission to hospital. In many
countries in the tropics, empirical antimalarial or

jaundice is relatively less frequent.

antibacterial treatment and antipyretics have often beenmalaria patients in Thailand. Hemorrhages may occur
anywhere in the retina. Some appear similar to Roth's

given before admission to the hospital. This may
Table 1Retinal hemorrhages occur in 15% of cerebral

Definition of severe malaria and complicated falciparum malaria

Cerebral malaria
2. Severe anemia (Hct< 15%)
3. Renal failure (no urine or urine output <400 ml in 24 hr, or 12 mllkg/24 hr after rehydration, or>3 mg/dl)

4. Pulmonary edema or adult respiratory distress syndrome
5. Hypoglycemia (blood sugar<40 mg/dl)
6. Shock (systolic BP<70 mmHg in adult or <50 mmHg in children age 1‑5 years)
7. Spontaneous bleeding and disseminated intravascular coagulation

8. Repeated convulsions
9. Acidosis (arterial pH<7.25 or plasma HCO* <15)
10.
11.
12.
13.

Macroscopic hemoglobinuria
Hyperparasitemia (>5% parasitemia in non‑immunes)
Hepatic dysfunction
Hyperpyrexia (persistence of rectal T>40'O

serum creatinine

183

spots, which are associated with endocarditis. Exudates
are unusual and papilledema is rare (1ess than 1%) . The

than 5%) ･ Abnormal eye movements such as divergenceof the eyes or nystagmus are seen occasionally. Pupi‑
1lary responses to light, and the oculocephalic andoculovestibular reflexes are always normal. Corneal
reflexes are usually present. There may be passive

hernorrhages resolve rapidly in survivors and do notinterfere with vision after recovery of consciousness.
Systemic bleeding due to disseminated intravascular
coagulopathy (DIO is present in a few patients (lessTable 2

resistance to head flexion but other signs of meningeal

Clinical trials of oral antimalarial drug either alone or in combination with other anti‑malarial drugs

in Bangkok Hospital for Tropical Diseases

Duration

No.

Cure rate(d)of patients

(%)

5

40

88

5

39

100

Looareesuwan et al., 1993
300
Artesunate
follow by mefloquine 15 mglkg divided into 2 doses

2.5

50

90

Looareesuwan et al., 1994
Artesunateplus doxycycline 200 mg/dx 7 d

2.5

55

80

Ref erence and drug

Total dose(mg)

Looareesuwan et al., 1992
600
Artesunate
600
Artesunate
followed by mefloquine 25 mg/kg divided into 2 doses

300

Looareesuwan et al., 1997

Artemether
Artemether
Artemether

40

74

750

7

58

98

600

1

53

98

500

follow by mefloquine 25 mg/kg divided into 2 doses
Looareesuwan et al., 1996a
Dihydroartemisinin

480

7

53

90

Looareesuwan et al., 1999
CGP 56697

Artemether 320

2

126

69

and
benf lumetol
1,920

Looareesuwan et al., 1996c

Atovaquone
Atovaquone

9,000

1

25

72

12,000

3

24

100

5,000

5

24

100

1,200

3

69

63

1,800

5

32

88

Dapsone 200

3

10

10

3

14

29

plus proguanil 4,800 mg

Atovaquone
plus proguanil 2.000 mg

Looareesuwan et al., 1996b
Pyronaridine
Pyronaridine
Wilairatana et al., 1997

Biguanide‑dapsone

plus proguanil
400

Biguanide‑da psone

Dapsone 200 plus
Chlorproguanil
70

184

irritation are absent. Ankle clonus is present in one
third of patients. The abdominal reflexes are almost
absent. There is no other clinical evidence of autonomic

dysfunction in cerebral malaria. The duration of coma
is 48‑72 hrs in most adult patients in Thailand. After
treatment most (92%) of the survivors have complete
recovery.

Treatment

Table 3

Causes of shock in severe falciparum malaria

Dehydration (hypovolemia)
2. Septicemia
3. Endotoxemia (TNF)
4. Hypoglycemia
5. Lactic acidosis
6. Hemorrhage (DIC, (jl bleeding, drugs, ruptured spleen)
7. Myocardial failure or cardiac arrhythmias

1 ) Uncomplicated falciparum malaria
With the emergence of multidrug resistant falcipar‑
urn malaria in Thailand, new drugs and drugs in combi‑
nation are urgently needed. The artemisinin derivatives

when used in combinations with mefloquine irnproved
cure rates to 95‑100% (Looareesuwan et al., 1993).
Dihydroartemisinin alone with a total dose of 480 mg
given over 5 days gave a cure rate of 90% (Looarees‑

required. Persistent parasitemia after a loading dose ofquinine is not uncommon. It is believed that the MIC ofquinine must be maintained for seven days of effectcomplete cure of P. falciparum infections. Therefore,quinine must be given for at least seven days or longer.

In quinine‑resistant areas, a second drug such as

uwan et al., 1996; Wilairatana et al., 1998). Combina‑

tetracycline or doxycycline has been added to increasecure rates, which approached 100% in 1986 but declinedtion of artemether with benflumetol proved safe andto 90% in 1991. For children, in whom tetracycline iseffective (cure rate over 90%) in the treatment of acutecontraindicated, increasing the dose of quinine to 15 mgl

uncomplicated falciparum malaria (Looareesuwan et

kg in the second half of the treatrnent period irnprovesal., 1999) . Other combinations (artemisinin derivatives

the cure rate.

combined with doxycycline, mefloquine combined withtetracycline or doxycycline) have also been evaluatedwith the improvement in cure rates (Table 2) (Looar‑

In severe malaria, if the patient has not received
quinine or mefloquine in the previous 24 hrs, then an
initial loading dose of 20 mg/kg of quinine dihydrochlor‑ide salt should be infused over 4 hrs followed by mainte‑
nance doses of 10 mglkg at 8 hrs intervals until thepatient can take oral medication, fot a total treatment

eesuwan et al., 1994).

2 ) Severe malaria
Management of severe malaria bases on the early
diagnosis and early treatment with a potent antimalar‑ial drug. Early detection and treatment of complica‑
tions (convulsions, acute renal failure, pulmonary

edema, acidosis, hypoglycaemia, hyperthermia) areessential. The aim of management is to save thepatient's life. The choice of antimalarial chemotherapy
depends on the clinical severity, the drug sensitivity ofthe parasites, and the availability and preparation of thedrug.

course of 7 days. The initial doses should never be
reduced, the maintenance doses should be reduced by
one‑third if by the third day of treatment there has been
no clinical improvement, or if there is established acuterenal failure. Hypoglycemia is the most serious andfrequent adverse effect of cinchona alkaloids.
Quin id ine

Quinidine, the diastereomer of quinine, has a lower
MIC for P. falciparum in Thailand. It is as effective asor perhaps more effective than quinine for the treatmentof falciparum malaria, as shown in open trials of oral

QuinineQuinine is the most commonly used and available

quinidine sulfate and parenteral quinidine gluconate in

drug in treating falciparum malaria. Recently, its effec‑

both acute uncomplicated and severe falciparum

tiveness has declined when used alone. Quinine resis‑
Tanzania, Vietnam, and Thailand; however, most of themalaria in Thailand. Quinidine bisulfate and quinidine
slow‑release formula was tested in uncomplicated fal‑ciparum malaria in Thailand in 1983‑1984. They proved

resistance is at the RI Ievel. Minimal inhibitory concen‑

effective (with the cure rate of 100%) , were well tolerat‑

trations (MIO of quinine for P. falciparum parasites
have risen above 10 mglJ in some areas. In this situa‑tion, and in severe malaria, a loading dose of 20 mg ofquinine dihydrochloride per kg body weight, and mainte‑

ed and had few side effects. They should be consideredas alternative antimalarial drugs in the treatment of
uncomplicated falciparum malaria.
In places where quinine is not available, such asnance doses of 10 mg per kg given every 8 hrs, areJapan, America or Europe, quinidine may be used intance is appearing in several parts of the world including

185

place of quinine. It is 4 times more effective but also 4

over 90% of parasitemias within 24 hrs (Wilairatana ettimes more cardiotoxic than quinine. The electrocardio‑
gram shows consistent dose‑related prolongation of the
QTC interval. In severe malaria, an initial loading doseof 15 mg base/kg is given over 4 hrs, followed by 7.5 mgal., 1997). However, recrudescence rates are high,ranging from 10 to 30% depending upon the dose andduration of initial treatment. A recent study inbase/kg given over 4 hrs at 8 hrs intervals. Quinine
should be substituted when, it becornes available tocomplete a 7 days treatrnent course. Hypotension is aof 600 mg given over 5 days had a cure rate of 88%(Looareesuwan et al., 1992). However the efficacy
increased to 100%, in both acute uncomplicated andserious side effect particularly when it is given over a
period of less than 4 hrs.

recrudescent falciparum malaria infections, when meflo‑
quine 1,250 mg (divided in 2 doses 6 hrs apart) was given

Thailand has shown that oral artesunate at a total dose

following artesunate treatment. If a half dose of
Combination of quinip e, quinidine and cinchonidine
In vitro testing against fresh isolates of P. falcipar‑

um suggested that a combination‑containing equal part
(1 : I : 1) of the three drugs was more potent than theartesunate (300 mg) was given over 2.5 days, followed

by 750 mg mefloquine, the cure rate reduced to 90%(Looareesuwan et al., 1993, Looareesuwan et al., 1997) .

individual drugs. In clinical trials, this combination wasBoth oral and parenteral preparations of artesunate
have been licensed for use in Thailand. In order tostudied in uncomplicated falciparum malaria in

reduce the high recrudescence rate, the optimum dose ofThailand. The combination drug was given every 8 hrs
in a dose of 11.4 mg base/kg for 7 days. The results
revealed that neither the oral nor the intravenous prepa‑
rations of the three drugs are toxic and that it is effec‑
tive in the treatment of chloroquine‑resistant falcipar‑

um malaria. However, the drug is not generally avail‑able.

artesunate in combination with other drugs such as
mefloquine or tetracycline or doxycycline is currently
being investigated in Thailand.
A rtemether

Artemether (60 mg ampoule), manufactured byKunming Pharmaceutical Factory, Kunming, China, isformulated in peanut oil for intramuscular injection and

Qinghaosu (artemisinin) derivatives

licensed for use in Thailand. Oral arternether (50 mg

Qinghaosu is sesquiterpene lactone peroxidetablet or capsule) is undergoing clinical trials. As withextracted from the qinghao plant (Artemisia annua L.) .
It has been used in Chinese traditional medicine for over2000 years, to treat the chills and fever associated withartesunate, the parasiticidal effect is rapid, with clear‑malaria. The active constituent, artemisinin, was iso‑lated in 1972. Qinghaosu derivatives are highly effective

in killing parasites; however, recrudescence rates areance of over 90% of parasitemias within 24 hrs. Unfor‑
tunately, recrudescence rates are also high. Optimum
dose of artemether combined with other drugs such as
mefloquine, tetracycline or doxycycline is being understudied in Myanmar and Thailand.

high. Attempts have been made to reduce the highrecrudescence rates by increasing the dosage, or length‑

ening the period of drug administration, or using drug
combinations.
Two derivatives, (artemether andartesunate) are now widely used and have been regis‑
tered in Thailand. Other qinghaosu derivatives includ‑ing arteether and artelinic acid, are under development.
A rtesunate

Artesunate is formulated either as tablets (50 mg
tablet) or as a dry powder of artesunic acid for injection

Symptomatic treatment
Supportive and symptomatic treatment of malaria
are equally important to antimalarial drugs since mostpatients have headache, nausea, vomiting, diarrhea, highfever and inability to take any food while they are ill.

Therefore, rehydration and the use of antipyretic andantiemetic drugs may be necessary. Antipyretics andantiemetics drugs should be administered a few hours
before antimalarials are given, in order to reduce thechance of vomiting and to comfort the patients. After(supplied in 60 mg vial with an ampoule of I m/ 5%

antimalarial drug administration, it is advisable to keep

sodium bicarbonate) . The powder is dissolved in the 1
ml sodium bicarbonate and then further diluted in I ml
of normal saline and use immediately as intravenous or
intramuscular injection. Artesunate is manufactured by
Guilin No. 2 Pharmaceutical Factory, Guangxi, China.
It has rapid antimalarial activity with the clearance of

patients under observation for an hour or let the patientslie down, to make sure that they have completed thedose and do not vomit. If they vomit within I hr, thedose should be repeated.
In severe malaria, especially in cerebral malaria,
intensive care of the unconscious patient and treatment

186

of life‑threatening complications such as pulmonary

Hepatic dysfunction

edema, metabolic acidosis, renal failure, hypoglycemia,This is manifested by jaundice, raised serum

bacterial septicemia, and aspiration pneumonia areessential (WHO, 1990). Cerebral malaria is an emer‑
gency condition, which requires intensive care during

enzymes, prolonged prothrombin time, decreased serum
albumin and lactic acidosis. Bilirubinemia is predomi‑
nantly of the unconjugated type but some patients show

the first 48 hrs of admission (Warell, 1997). It has been

an increase in conjugated bilirubin, indicating hepatocel‑

calculated that nearly 80% of patients die during thisperiod. Other complications or manifestations should be

lular damage. Saline enema in these patients is recom‑
mended (Wilairatana et al., 1994).

treated as follows:

Cerebral malaria patients usually deteriorate while

Hypoglycemia
Hypoglycemia should be reversed by intravenous
dextrose and plasma glucose maintained between 80‑120

they have high fever. Temperatures above 38.5'C are

mg/dl Frequent monitoring is essential. This condition

associated with an increased incidence of convulsions,especially in children. Temperatures between 39.5'C and
40'C is associated with delirium, and above 42.0'C withshould be suspected in any patient whose consciousness
is deteriorating, who develops convulsions or who haschanged respiratory patterns.

coma. High body temperatures may cause permanent
severe neurological damage. In pregnant women with

Shock ( "algid malaria")

Hyperthermia

malaria, high fever is associated with fetal distress. In

the severely ill patient, cooling blankets, fanning, andThis is most commonly the result of hypovolemia orcomplicating septicernia.

tepid sponging are necessary. In the tropics, clinicians

often accept the risk of agranulocytosis and use par‑enteral antipyretics such as dipyrone.

Severe anemia
Anemia develops very rapidly in cerebral malaria
and blood transfusion is often required. Anemia results

Acute pulmonary edema
Although pulmonary edema may develop at any

from a combination of bone marrow suppression andstage of the acute illness, it tends to occur later than theunparasitized red cells. Blood should be crossmatchedon admission and transfused to maintain the hematocrit

other acute manifestations of malaria. Central venous
pressure is a useful measure of hydration. A permeabil‑

ity ederna associated with normal pulmonary wedge
pressure measurements may develop at any time in thefirst few days of treatment and is difficult to treat.
There is no specific therapy and management should be
the same as that for adult respiratory distress syndrome

accelerated red cell destruction of both parasitized andover 21%. Fresh blood is preferable as throm‑
bocytopenia and clotting factor depletion may coexist
with anemia. Transfusion rates should be slow to avoid

volume overload, and it may be necessary to give apotent diuretic such as furosemide intravenously at thesame time.

occurring in other conditions. Malaria in pregnancy
usually has a high risk of pulmonary edema, particularly

Metabolic acidosis

after delivery.

This condition is serious and rapidly fatal. Lactic
acidosis and renal impairment both contribute to hydro‑

Acute renal failure

gen ion retention. Lactic acidosis results from theThis results from acute tubular necrosis. Someparasite, increased anaerobic glycolysis and a failure of

impairment of renal function is common in adults withcerebral malaria and is also associated with classicalblackwater fever but only a minority of patients go on
to develop established renal failure. Hypercatabolic
acute renal failure should be managed by dialysis orconservative treatment if dialysis is not available.

hepatic gluconeogenesis. Sodium bicarbonate provides
temporary correction of acidosis. Dichloroacetate has

Hemodialysis treatment in acute renal failure frommalaria does not shorten the course of acute tubular
necrosis, which is usually last for I ‑ 3 weeks.

cerebral malaria patients.

Hemodialysis requires 5‑10 times during the 1‑3 weeks
of anuria. Fluid balance should be strictly monitored.

In nonimmune patients with severe falciparum
malaria, mortality increases with the degree of para‑

proved to be safe and to decrease the degree of acidosis.

However, it did not reduce the mortality rate in arandomised controlled study in adult patients sufferingfrom other diseases. The drug should be tested inHyperparasitemia

187

sitemia. Exchange transfusion may reduce the burdenof parasitemia more rapidly than chemotherapy alone
and might also remove harmful toxic products e.g.
toxins and cytokines (Looareesuwan et al., 1998; Udom‑

Chemoprophylaxis
1 General Principles
A practical approach to any prophylaxis regimen

sangpetch et al., 1997; Wenisch et al., 1998). This tech‑includes the following concepts:
o Drugs should begin at least I week before entering anique replaces blood, plasma, platelets, clotting factors

malarious area. The drugs must be taken regularly

and correct other abnormalities e.g. fluid, electrolytes

and acid‑base imbalance. Exchange transfusion should

and, for most regimens, continued for at least 4 weeks
after leaving the endemic area.

be considered in nonimmune patients who have moreo No antimalarial regimen is completely effective, eventhan 10% parasitemia and who have deteriorated on theconventional chemotherapy and have at least two com‑plications of severe falciparum malaria e.g. cerebral
malaria, renal failure, jaundice or acute pulmonary
edema. In areas where total exchange transfusion is notwith absolute compliance. Antimalarial chemopro‑
phylactic regimens do not prevent infection: they

possible, partial exchange transfusion with 4‑6 units ofsuppress the infection sufficiently in most cases sothat clinical signs and symptoms do not appear. In
areas of increasing drug resistance, 'breakthrough'infections will occur more frequently.

fresh blood performed manually, alternately venesecting

e Chemoprophylaxis should always be combined withand transfusing the patient is still useful. Monitoring of

personal protective measures such as the use of insec‑

central venous pressure, vital signs and blood pressuremust be done frequently during exchange transfusion.

ticide impregnated bed nets for sleeping, avoiding
peak mosquito biting times, using insect repellents on

exposed surfaces, and wearing clothes that minimize
Bacterial infections

Gram‑negative septicemia, aspiration pneumonia,
and urinary tract infections may complicate cerebral
malaria and should be treated with appropriate antibio‑

tics. Any patient who develops shock at any stage
should be investigated because ups to 40% of such cases
have been found to have positive blood cultures.

exposure.

Antimalarial prophylaxis by people living inmalaria endernic areas remains controversial. Pregnant

women are at increased risk for severe malaria andshould take antimalarial prophylaxis. Antimalarial
prophylaxis in children living in endemic areas has beenshown to reduce mortality, but some issues remain
unsettled.

Coagul o pathy

Using sensitive measures, activation of the coagula‑tion cascade be detected in all patients with acute symp‑

tomatic malaria, but significant disseminated intravas‑
cular coagulopathy occurs in less than 5% of patientswith severe disease. Replacement therapy (not heparin)

Recommendations for malaria chemoprophylaxis intravelers are complicated by cornpliance issues andadverse effects. In areas where the risk of infection is
low or there are brief exposures in intermediate or hightransmission areas, travelers may carry a treatment
course of antimalarial drugs ('standby drugs') instead ofis essential, and in the tropics fresh blood is preferable.

taking prophylaxis. If they become ill, especially in

Prognosis

areas without medical facilities, the treatment is self‑
administered.

Poor prognostic indicators in severe falciparum
malaria include deep coma, repeated convulsions withsigns of decerebration, high parasitetnia ( > 5% in
nonimmunes) , peripheral schizontemia, clinical jaundiceor more than three‑fold elevated serum enzyme concen‑
trations, uremia (creatinine more than 3.0 mg/dl andblood urea nitrogen more than 60 mg/dl after rehydra‑tion) , metabolic acidosis (elevated plasma and /or cere‑

brospinal fluid lactate, or arterial blood gas <7.2),

leucocytosis (>15,000/pl), retinal hemorrhages andhypoglycemia (clinical hypoglycemia or blood glu‑
cose <40 mg/dJ) .

2 Current Prophylactic Drugs
Increasing drug resistance in many parts of theworld, especially Southeast Asia and South America, isslowly diminishing the effectiveness of many prophylac‑
tic regimens. Knowing the drug resistance patterns of
P. falciparum in different geographic locations is essen‑tial for choosing an appropriate regimen.

The major chemoprophylactic drugs for falciparum
malaria include doxycyline, mefloquine.

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189

Jpn. J. Tro p. Med. Hyg., Vol. 27, No. 2, 1999, pp. 189 194

SIMULIUM ( NE VERMANNIA ) BONNINENSEFROM THE OGASAWARA (BONIN) ISLANDS,JAPAN (DIPTERA= SIMULIIDAE) =TAXONOMIC ASSIGNMENT TO
THE VERNUM‑GROUP AND DESCRIPTIONS
OF MALE, PUPA AND MATURE LARVAHIROYUKI TAKAOKA , KATSUMI SAIT02 AND HIROSHI SUZUK13
Received March 10, 1999/Accepted April 27, 1999

Abstract: Descriptions and illustrations of male, pupa and mature larva of a black‑fly species, Simulium(Nevermannia) bonninense (Shiraki, 1935), from the Ogasawara (Bonin) Islands in Japan are given for the
first time; the female adult is also redescribed. Within the subgenus Nevermannia, this species is assigned
to the vernum‑group by the combination of the following characters: male genitalia with a lamellate ventral
plate without median keel, an elongate style with a large, broad, inwardly‑twisted apex, a single parameral
hook per side, and an inverted Y‑shaped median sclerite; pupal gill with four slender filaments per side; andlarval mandible with supernumerary serrations. Interestingly, this species has the katepisternum haired inboth sexes of adults, female genital fork with a prominent projection directed forwards on each arm, andpupal frons with two trichomes on each side, all of which are rare in this species‑group. Brief notes on adultblood‑feeding, and larval habitats of S. (N.) bonninense are given.

Key words: Simuliidae, Simulium, black fly, Ogasawara Islands, bonrdnense

Shiraki (1935) described Simulium (Nevermannia)
bonninense (then, under the genus Eusimulium) from a

History Museum, London, UK (BMNH). This species

single female adult specimen collected in the Ogasawara

is assigned to the vernum‑group within the subgenus
Nevermannia, as provisionally treated by Takaoka and(Bonin) Islands, ca. 1,000 km south‑southeast from

Davies (1995).

Tokyo, in the Pacific Ocean. Stone (1964) gave excel‑
lent illustrations as well as a brief description of the

Simulium (Nevermannia) bonninense (Shiraki, 1935)

female of this species based on 13 females collected in

Eusimulium bonninense Shiraki, 1935: 21‑23.

1958 frorn Hahajima Is., while reporting three otherspecies of Simuliidae from Micronesia. The immature

Simulium (Eusimulium) bonninense: Tokunaga, 1943:

stages of this species were found for the first time by
Saito et al. (1974). However, no descriptions have ever

Simulium (Nevermannia) bonninense: Takaoka andbeen made.
The present paper gives the redescription of thefemale, and descriptions of the male, pupa and maturelarva, of S. (N.) bonninense, based on reared or light‑
trapped adults, and immature stages recently collectedby one of us (HS) , as well as those examined by Saito
et al. (1974), and one female loaned from the Natural

943; Stone, 1964: 634‑635; Crosskey, 1989: 223.

Okazawa, 1988: 98; Takaoka and Davies, 1995: 163;
Crosskey and Howard, 1997: 49.

DESCRIPTION. Female. Body length 2.7‑3.0 mm.
Head. Narrower than thorax. Frons and clypeus
brownish black, not shiny, white‑pruinose, moderately
covered with whitish yellow fine simple hairs, intersper‑

sed with brown longer and stouter hairs. Frontal ratiol Department of Infectious Disease Control, Oita Medical University, Hasama, Oita 879‑5593 Japan
2 Department of Parasitology, School of Medicine, Yokohama City University, Kanazawa‑ku, Yokohama City, Kanagawa 236‑
O004, Japan
3 Information and Reference Center of Tropical Medicine, Institute of Tropical Medicine, Nagasaki University, Sakamoto,Nagasaki City, Nagasaki 852‑8523, Japan

190

1.6:1.0:1.6. Frons‑head ratio 1.0:4.9. Fronto‑ocular area

tized; internal setae absent.

(Fig. 1) well developed. Antenna composed of 2+9
segrnents, dark brown to brownish black. Maxillary

Male. Body length 2.5 mm. Head. As wide as, or

palp consisting of 5 segments, brownish black, propor‑

slightly wider than, thorax. Holoptic; upper eye consist‑tional lengths of 3rd, 4th and 5th segments 1.0:1.0:1.7; 3rd

ing of large facets in 19 vertical columns and 20 horizon‑

segment (Fig. 2) somewhat enlarged, with sensory vesi‑
cle elongate, ca. 2.0X as long as wide, and ca. 0.3x as
long as 3rd segment. Maxillary lacinia with 14 inner
teeth and 15 or 16 outer ones. Mandible with 26‑28 inner
teeth and 11‑15 outer ones. Cibarium smooth. Thorax.

tal rows. Clypeus dark brown, gray‑pruinose, moderate‑

Scutum brownish black, white‑pruinose, densely cov‑
ered with whitish yellow recumbent fine hairs, and withseveral brown upright hairs on prescutellar area.
Scutellum brownish black, with many brown uprightly covered with dark simple hairs. Antenna composedof 2 + 9 segments, dark brown; Ist flagellar segment
somewhat elongate, ca. 1.9x as long as 2nd flagellar
segment. Maxillary palp brown, composed of 5 seg‑ments, proportional lengths of 3rd, 4th and 5th segments
1.0:1.0:2.3; sensory vesicle small, ellipsoidal. Thorax.
Scutum brownish black, not shiny, densely covered withyellow recumbent fine hairs, and with several brownhairs as well as whitish yellow recumbent fine hairs.
Postscutellum brownish black, bare. Pleural mernbranebare. Katepisternum longer than deep, with several fine

upright hairs on prescutellar area. Scutellum brownish
black, with many brown upright hairs as well as palehairs near upper margin on each side. Legs. Dark

membrane bare. Katepisternum longer than deep, withbrown to brownish black, except hind trochantef dark

several fine hairs near upper margin on each side. Legs.

yellow to light brown, base of hind tibia yellow, basal
3/5 of hind basitarsus and basal 1/2 of 2nd hind tarsal

Dark brown to brownish black except basal 2/5 of hindbasitarsus and basal 1/2 of 2nd hind tarsal segment

segment whitish yellow. Fore basitarsus slender, ca.
7.2x as long as wide. Hind basitarsus (Fig. 3) nearly

whitish yellow. Fore basitarsus slender, ca. 7.9>< as longfine hairs. Postscutellum brownish black, bare. Pleuralas wide. Hind basitarsus (Fig. 4) enlarged, 3.2x as longparallel‑sided, 5.6 x as long as wide, and much narrower

as its greatest width, slightly wider than hind tibia butthan hind tibia. Calcipala and pedisulcus (Fig. 3) welldeveloped. Claws (Fig. 5) each with large basal tooth.

slightly narrower than hind femur. Calcipala and pedi‑

Wing. Length 2.0‑2.3 mm. Costa with 2 parallel rows

except subcosta bare or with a few hairs; Iength 2.0 mm.

of short spines as well as hairs. Subcosta haired except
apical 1/4 bara (in I female, apical 1/2 bare). Hair tuft

Abdomen. Basal scale brownish black, with fringe ofpale long hairs. Dorsal surface of abdominal segments
dark brown to brownish black, not shiny, with shorton stem vein brown. Basal portion of radius fully
haired. Basal cell absent. Abdomen. Basal scale
brownish black, with fringe of pale long hairs. Dorsal
surface of abdominal segments dark brown to brownish

black, not shiny, with short dark hairs; terga 3‑6
medium, nearly quadrate, subequal in size to one
another, tergum 7 nearly 2.0 X as wide as terga 3‑6, but
still confined to dorsal surface, while terga 8 and 9 very

wide, extending laterally. Genitalia (Figs. 6‑8). Ster‑sulcus (Fig. 4) well developed. Wing. As in female

dark hairs. Genitalia (Figs. 9‑15). Coxite subquadratemuch longer than wide. Style slightly shorter thancoxite, broadly truncate apically, twisted, then apicalpart bent inwards, and with a subapical spine directed
inward and forward. Ventral plate larnellate, shorter
than wide, with a srnall medial notch on anterior border,

and a deep medial concavity on posterior border, andmoderately covered with fine short setae on ventral

nal plate of 7th abdominal segment well developed,
nearly triangular. Sternum 8 wide, bare medially but

surface; arms short, stout, and bent inwardly and dorsal‑

furnished with ca. 12 stout hairs on each side. Anterior

hook. Median sclerite slender, forked apically. Dorsal
plate of various forms, much broader than median scle‑

gonapophysis thin, mernbraneous, triangular, densely
covered with microsetae and several short setae; innerly. Parameres of normal form, each with a distinct

rite. Aedeagal membrane with spinous microsetae.

margin narrowly sclerotized; posteromedian corner

Cercus small, spherical in lateral view, with several

rounded. Genital fork with well sclerotized stem andwide arms; each arm with a wide round lobe directed
medioposteriorly and a prominent projection directed
forward. Paraproct sornewhat protruding ventrally.
Cercus rounded posteriorly in lateral view. Spermathe‑
ca ovoid or pear ‑ shaped, strongly sclerotized except

hairs.

nal sheath also sparsely covered with groups of many

tube and small area of tubal base bare or weakly sclero‑cone‑shaped tubercles; face with I simple (or occasion‑

Pupa. Body length ca. 2.5 mm. Head. Integument
yellowish brown, sparsely or moderately covered withcone‑shaped tubercles of various sizes (Fig. 16); anten‑

191

ally bifid) , stout trichome on each side (Fig. 17) , while

yellow to yellowish brown on posterior 3/5, with poste‑

frons with 2 slenderer trichomes, of which I is much
shorter, on each side (Fig. 18). Thorax. Integument
yellowish brown, moderately covered with cone‑shapedrior margin somewhat darkened, and with distinct posi‑tive head spots. Cervical sclerite composed of 2 smallrod‑1ike pieces, not fused to occiput, widely separated

tubercles of various sizes, with 3 Iong, stout trichomes
mediodorsally (Fig. 19), 2 (1 Iong, stout, and I medium,
slender) trichomes mediolaterally (Fig. 20), I medium,

medially from each other. Antenna consisting of 3
segments and apical sensillum, Ionger than stem ofstout trichome posterolaterally (Fig. 21), and 3 (2labral fan; proportional lengths of Ist, 2nd and 3rd
segments 1.0:1.1:0.7‑0.8. Labral fan with 34‑36 main

medium, stout and I short, slender) trichomes

rays. Mandible (Fig. 25) with a few supernumerary

ventrolaterally (Fig. 22), all simple (or occasionallybifid on tip) . Gill (Fig. 23) with 4 slender filaments

serrations, as well as 2 usual mandibular serrations;comb‑teeth composed of 3 teeth, of which Ist tooth isarranged in pairs, each pair with very short stalk,arising from very short basal common stalk; all fila‑

largest, 2nd is srnallest and 3rd is intermediate. Hypos‑

dorsal pair slightly shorter than those of ventrolateral

tomium (Fig. 26) with a row of 9 apical teeth, of whichmedian and corner teeth are moderately developed, and3 intermediate teeth on each side are small and subequalin size to one another; Iateral serrations moderatelypair) , and 2 filaments of dorsal pair slightly thicker thandeveloped; 5 or 6 hypostomal bristles lying slightly

those of ventrolateral pair, at least near base; cuticulardivergent posteriorly from lateral margin on each side.

surface with distinct annular ridges and furrows, andPostgenal cleft (Fig. 27) medium, miter‑shaped, with

densely covered with minute tubercles. Abdomeu.

apex pointed or occasionally rounded, variable in length,

Terga I and 2 yellowish brown, moderately tuberculate;

1.0‑1.8x as long as postgenal bridge. Thoracic cuticle
bare. Abdominal cuticle bare except last segment cov‑
ered with colorless short setae on each side of anal

ments yellowish brown to dark brown, subequal inlength to one another (1.7‑2.0 mm) (or 2 filaments oftergum I with I medium, slender seta on each side;
tergum 2 with I medium, slender seta and 5 short,spinous setae (1 or 2 occasionally much stouter thanothers). Terga 3‑8 each with yellowish brown area ofvarying sizes anteriorly; terga 3 and 4 each with 4 hooks

sclerite. Rectal papilla of 3 simple lobes, without secon‑

dary lobules. Anal sclerite of usual X‑form, with poste‑rior arms ca. 1.4x as long as anterior ones; basal

and a few spinous setae on each side; tergum 5 bare;portion of arms and anterior arms widely sclerotized.

terga 6‑9 each with many groups of minute spines
directed backward on each side; tergum 6 with 0‑3

Accessory sclerite absent. Ventral papillae small, Iater‑

spine‑combs, which are, if present, much smaller thanally placed, then, often indiscernible when the larva isviewed laterally. Posterior circlet with ca. 90 rows of up

those on tergum 8; tergum 7 with 0‑8 spine‑combs;

to 15 hooklets per row.

tergum 8 with 7 or more spine‑combs in transverse row
on each side; tergum 9 yellowish brown, with a pair of

SPECIMENS EXAMlNED. HAHAJIMA IS. (E142'07'‑

distinct, cone‑shaped terminal hooks (Fig. 24) . Sternum

E142"I1', N26'36'‑N26'43'), OGASAWARA (BONlN)

4 with I simple or bifid hook submedially, which is

ISLANDS, JAPAN: I female (genitalia dissected andsubequal in size to those on sterna 5‑7, and a few slender

mounted on glass slide) , pinned, probably light‑trapped,

setae (1 of which is often somewhat longer and stouter)

26.IV‑9.VI.1958, F.M. Snyder (BMNH); 3 females, 3

on each side; sternum 5 with a pair of bifid hooks

males, all reared from pupae (all dissected and mounted
on glass slides) , 14 pupae, 10 pupal exuviae, 5 maturelarvae, 3.VII.1973, K. Saito; 2 pupal exuviae, Kitamura,
20.IV.1996, H. Suzuki; 2 females, Iight‑trapped, lO.V.
1996, M. Yoshihara; 5 females, 27.V.1996, M. Yoshihara;
6 females (1 blood‑engorged) , Iight‑trapped, 17.VI.1996,

submedially and a few slender setae on each side; sterna
6 and 7 each with I bifid hook submedially and I simple

hook laterally, and a few slender setae, on each side.

Cocoon. Wall‑pocket‑shaped, usually with narrowanteroventral connection, compactly woven without
open spaces in web, with anterior margin thickly woven,and only slightly extending ventrolaterally; 2.8‑3.0 mm

M. Yoshihara; 3 females, 17.VII.1996, M. Yoshihara; 310ng x 1.2‑1.4 mm wide.

VII.1997, K. Takehara. CHICHIJIMA IS. (E142"I1'‑E142'

Mature larva. Body length 5.0‑5.3 mm. Body grayish

ISLANDS: 2 females, Iight‑trapped, Sakaiura, 15.IV.
1996, H. Suzuki; 3 pupae, 2 pupal exuviae, 9 mature

females, 12.Vlll.1996, M. Yoshihara; I female, netted, 10.

14', N27'02'‑N27'06'), OGASAWARA (BONlN)
dorsally, mottled to varying extents with dark violet
brown color on each thoracic and abdominal segment.
Cephalic apotome (Photo. 1) pale on anterior 2/5, darklarvae, Sakaiura, 17.IV.1996, H. Suzuki; 5 females (allblood‑engorged) , 2 males, Iight‑trapped, 16.IV.1996, H.

192

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Figures 1‑15. Female and male adult characters of Simulium (Nevermannia) bonninense. 1, fronto‑oculararea of fernale; 2, 3rd segment with sensory vesicle of female maxillary palp; 3 and 4, basitarsus and 2ndtarsal segment of hind leg, showing calcipala and pedisulcus (3, female; 4, male) ; 5, tarsal claw of female

foreleg; 6, female genitalia (ventral view, female loaned from BMNH), showing 8th sternite, anterior
gonapophyses, genital fork, spermatheca with weakly sclerotized tubal base and right paraproct and cercus;
7, right paraproct and cercus (lateral view) ; 8, spermatheca with pale tubal base (female reared from pupa) ;9, male genitalia (ventral view) , showing coxite, style of right side, ventral plate, parameres, aedeagal
membrane and median sclerite; 10, ventral plate (1ateral view) ; 11, style (ventromedial view) ; 12‑14, dorsal
plates in different shapes; 15, male 10th abdominal segment (lateral view) showing small hairy round cercus.

1

193

Suzuki; 3 females, I male, all reared from pupae, 9

uncertain as to whether this species feeds on man,pupae, 2 pupal exuviae, 17 mature larvae, Shigure‑dam,
16.IV.1996, H. Suzuki; 4 mature larvae, Ohgiura, 18.IV.
1996, H. Suzuki.

although villagers often claimed so.

Immature stages of S. (N.) bonninense were foundin small, swift‑flowing streams partially shaded byshrubbery. Stream beds were mostly rocky and widths

BIOLOGICAL NOTES. Female and male adults of S.

were about 50 cm or less. The pupae and larvae(N.) bonninense were captured by light trap from April
to August, and some of the females were fully blood‑fed,

attached to grasses trailing in the water from the banks.

indicating that its life cycle is multivoltine, and its
ovarian development is anautogenous. Host animals are

The larvae collected comprised a final instar and manyother earlier instars including a first instar. No othersimuliid species was found in all the streams sampled.

unknown. One female adult was netted while flying
around the knee of man during day‑time. It remains

DISTRIBUTION. Chichijima Is. and Hahajima Is. inll//....̲ / .̲..... "' f¥

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Figures 16‑27. Pupal and larval characters of Simulium (Nevermannia) bonninense. 16‑24, pupa; 25‑27,
larva. 16, tubercles on frons (oblique view) ; 17, facial trichomes (1eft, of usual simple form; right, ofoccasional bifid form) ; 18, frontal trichomes; 19, mediodorsal thoracic trichome; 20, mediolateral thoracic
trichomes; 21, posterolateral thoracic trichome; 22, ventrolateral thoracic trichomes; 23, gill filaments(1ateral view) ; 24, terminal hook (1ateral view) ; 25, apical part of mandible; 26, hypostomium (ventralview) ; 27, head capsule (ventral view) showing postgenal cleft. Scale bars: 0.02 mm for Fig. 16; 0.04 mm
for Figs. 17 and 18, and Figs. 19‑22.

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l 94

ACKNOWLEDGEMENTS
We thank Dr. D.M. Davies, professor emeritus,
McMaster University, Ontario, and. Dr. D.A. Craig,
professor emeritus, University af Alberta, EdiTlonton,
Canada, for their kindn,ess in reading tht:;. manuscript,

and giving valuable suggestions. Dr. D.A. Craing alsr=)

kindly took a picture of the larval head of S. (N'.)
bonnine ts= e (Photo, l) for this poper. Thanks, are als̲odue ta Dr. A. Shelley, Ms. C. Lowry, and /liss T.

Howard, Department of Entomology, BMNH, London,
UK, for their kind arrangement of the loan. We are
grateful to Mr, . M. Yoshihara, and Prof. S. Kitaoka, whosPhoto. I Larval head (dorsal view) of Simidium (Never‑gave us their adult fly samples caught by light trap.
This study was supported in part by the Grant‑in Aid ofmannia) hoplnieeerlse. Scale bar O 2 mm

I linistry of Education, Science and Culture, Japan (no.

ll670246) to H.T.

the Ogasawara (Bonin) lslands, Japan.
REFEREN Cr‑*.S

PRMARKS. Within the subgenus Simulium (Nevermal ‑rda). S. (N.) bonpsinense is assigned to the vernum‑l ) Cros skey, R.W. (1969): A reclassification of thegroup (ronTlerly latipes‑group, as defined by Cro, sskey in

Simuliidae (Diptera) of Africa and its islands. Bull. Br.
Mus. Natur. Hist. (Entomol.) suppl., 14, 195p.

1969), by the combination of the fallowing characters:
male genitaliavith a simple, Iamellate ventral plate, an2 ) Okazawa, T. (1984): A new species of Simidium(Eus7:midium) (Diptera, Simuliidae) from Hokkaido,
Japan. Kontyu, 52, 213221

elongate style with a large, inwardly‑twisted apex, asingle parameral hook per side, and an inverted Y‑
shaped median sclerite; pupal gill with faur slenderfilaments per side; and larval mandible with, supernu‑
merary serrations.

3 ) Ono, H. (1978); Description of the two new species of
the genus Cnetha from Japan (Diptera, Simuliidae) .
4

Res. Bull. Obihir,o Univ., lO, 893909
Saito, K., Hori, E. and Ogata, K. {1974): ShTluliidae of

It is worthwhile to note that S. (iV.) bon;einense has

Ogasawara Islands. Jpn. J. Sanit. Zool., 24, 33,. 8

the katepisternum haired in both sexes of adults, fcmale(Japanese abstract oTnly)
5 ) Shirakl', T. (19?>5 : Simuliidae of the Japanese Empire.

genital fork with a prominent projection directed for‑wards on each arm, and pupal frons with two trichomeson each side, all of which are rare in the vernum‑group.
There are five other known species belonging to thevernum‑group in Japan: S. (N̲) acmeria (Ono), S. (N.)

boldstemta (Ono) (Ono, 1978). S. (N.) Iarvipilosum
Okazawa (Okaza va, 1984). S. (N.) subcoslatum (Taka‑hasi) and S. (N.) uchidai (Takahasi) (Takaoka, 1976).
The first two species resemble S. (N.) bonnipzense byhaving the forwardly‑directed projection on each anr of
the female genital fork and two pairs of trichomes on
the pupal frons, although there are great differences inmany other characters inciuding the shape of the ventral
plate and the coloration of the hind legs.

lvlem. Fac. Sci. & Agr. Taihaku Imp. Univ., 16, 1‑90

6 ) Stone, A. (1964) : Diptera: Silnuliidae. Insects ofMicronesia, 12, 629 635

7 ) Takaaka, H. (1976): Studies on black flies of the
Nansei Islands, Japan (Simuliidae; Diptera) I. On six
species of the subgenus Eusi 7s;idium Roubaud, w ith thedescriptions of Simulium (E. ) satsumense sp. nov. and S.
(E.) subcostatum koshikieeese ssp. nov. Jpn. J. Sanit,
Zool., 27, 163l80

8 ) Takaoka. H, and Davies, D.M. (1995): The black flies(Diptera; Simuliidae) of 'est Malaysia. Kyushu Uni‑
versity Press. Fukuoka, viii+ 175p.

J pn. J. Tro p.

195

Med. Hyg Vol 27 No 1 1999, pp. 195‑201

TAXONOMIC AND ECOLOGICAL NOTESON SIMULIUM ( GOMPHOSTILBIA)PALA UENSE (DIPTERA= SIMULIIDAE)
FROM PALAU, MICRONESIA, WITH

REDESCRIPTIONS OF ADULTS AND
DESCRIPTIONS OF THE PUPA AND

MATURE LARVAHIROYUKI TAKAOKAI AND DOUGLAS A. CRAIG2
Received March 23, 1999/Accepted April 27, 1999

Abstract: Redescriptions for the female and male, and descriptions for the pupa and mature larva, ofSimulium ( Gomphostilbia) palauense Stone are given based on reared adults and immature stages recently
collected from Palau, Micronesia. S. palauense has several remarkable pupal and larval characters, whichhave not (or very rarely) been found in any other species of the subgenus Gomphostilbia, such as, in the pupa,
the reduced number (i.e., four) of the gill filaments and the absence of spine‑combs on the abdomen; in thelarva, the presence of serrations on the lateral margins of the hypostomium, supernumerary mandibular
serrations, and accessory sclerites, and the absence of a postgenal cleft. Ecological notes on immature stages
are also given.

Key words: black fly, Simulium. Simuliidae. Palau. Micronesia

Stone (1964) described three species of Simuliidae

species. Ecological notes on immature stages are also

from Micronesia. He described Simulium (Gomphostil‑bia) palauense (then, under the subgenus Eusimulium)from five female and 12 male adult specimens from
Palau. This species was transferred to the subgenus
Inseliellum by Crosskey (1989), but has been recently

given.

assigned in the subgenus Gomphostilbia after one of its

Simulium (Gomphostilbia) palauense: Takaoka andparatype males preserved in The Natural History

Davies, 1995: 161; Crosskey and Howard, 1997: 34.

Simulium ( Gomphostilbia) palaueuse Stone
Simulium (Eusimulium) palauense Stone, 1964: 633.
Simulium (Inseliellum) palauelese: Crosskey, 1989: 224.

Museum, London (BMNH), was examined (Takaoka
and Davies, 1995). The other two species viere fromGuam, and Chuuk (Truk) State, Federated States ofMicronesia.
Larvae of S. palauense were collected for the firsttime by P. S. Cranston at Ngardmau Falls, Babeldoab,
Palau in 1997. More larvae and pupae, for the first time,
were collected from the same locality by us (D.A. Craig
and R.E.G. Craig) in 1998 and adults successfully reared

from pupae. In this paper we redescribe the adultfemale and male, describe the pupa and mature larva

Female. Body length 1.8 mm. Head. Slightly narrower
than thorax. Frons black, shiny, densely covered withwhitish recumbent pubescence, interspersed with several
brown hairs, except median longitudinal portion narrow‑ly bare; frontal ratio (i.e., greatest width at vertex:
narrowest width near antennal base: height) 1.7‑1.9:1.0:

1.8‑2.4. Frons‑head ratio (greatest width of frons:
greatest width of head) 1.0:4.0‑4.6. Fronto‑ocular area

(Fig. 1) deep, rounded apically. Clypeus black, shiny,

from these new specimens, and note briefly on several

densely covered with whitish recumbent pubescence,
interspersed with brown hairs. Antenna composed of

unusual pupal and larval characters found in this2 +9 segments, brownish black except scape, pedicel and

1

2

Department of I･nfectious Disease Control, Oita Medical University, Hasama, Oita 879‑5593, Japan
Department of Biological Sciences, University of Alberta, Edmonton, T6G 2E9, Canada

196base of Ist flagellar segment yellow. Maxillary palp
composed of 5 segments, dark brown to brownish black,
proportional lengths of 3rd, 4th and 5th segments 1.0:1.1:
2.3; sensory vesicle (Fig. 2) small, ellipsoidal, ca. 0.25x

as long as 3rd segment. Maxillary lacinia with 8‑11
inner teeth and 10‑12 outer teeth. Mandible (Fig. 4)
with ca. 20 small inner teeth and no outer teeth thoughouter margin is very weakly erose. Cibarium (Fig. 5)
medially forming a thinly sclerotized plate folded for‑ward frorn posterior margin, and with Y‑shaped, heavily

sclerotized medial projection. Thorax. Scutum brown‑
ish black, shiny, densely covered with brown recumbent
pubescence, intermixed laterally and posteriorly withwhitish yellow one. Scutellum brownish black, withbrown recumbent pubescence and with brown uprighthairs near posterior margin. Postscutellum brownish
brown, shiny, bare. Pleural membrane bare. Katepister‑num dark brown to brownish black, Ionger than deep,
shiny, with many brown hairs. Legs. Brownish black
except fore coxa dark yellow, base of mid tibia white ofyellowish white, hind trochanter yellow, basal 2/5 orhind tibia white or yellowish white, basal 2/3 of hindbasitarsus and basal 1/2 of 2nd hind basitarsus white;
mid and hind tibiae covered with whitish hairs brightly

somewhat produced ventrally beyond ventral margin of
cercus, covered with 17‑23 hairs on outer and ventral
surface. Cercus semicircular, with dark hairs. Sper‑matheca ellipsoidal, well sclerotized except small area
at tubal juncture and tube unsclerotized, without inter‑
nal setae.

Male. Body length 1.6 mm. Head. Much wider thanthorax. Upper eye consisting of 12 vertical columns and13 horizontal rows of large facets. Face black, white‑pruinose. Clypeus black, shiny, white‑pruinose, moder‑ately covered with dark hairs, intermixed with whitish
yellow scale‑1ike pubescence laterally except median
10ngitudinal portion somewhat widely bare on lower 3/5
of clypeus. Antenna composed of 2+9 segments, yellow
except apical 5 or 6 flagellar segments grayish brown;
Ist flagellar segment somewhat elongate, ca. 1.5x as
10ng as 2nd flagellar segment. Maxillary palp composedof 5 segments, grayish brown, proportional lengths of3rd, 4th and 5th segments 1.0:1.2:2.3; sensory vesicle(Fig. 3) small, ellipsoidal, ca. 0.2x as long as 3rd seg‑

ment. Thorax. As in female. Legs. Light brown tobrownish black except fore coxa dark yellow, base of
mid tibia white, hind trochanter yellow, basal 1/3 of hindshiny in light on basal 1/3 and basal 3/5 of posterior andtibia yellow, basal 2/3 and a little more of hind basitar‑outer surface, respectively. Fore basitarsus somewhat
dilated, ca. 5.0X as long as its greatest width. Hind

sus and basal 1/2 of 2nd hind tarsal segment white; midbasitarsus (Fig. 6) slender, parallel‑sided, ca. 6.6x as

10ng as wide, and much narrower than hind femur andtibia, of which greatest breadths are ca. 2.3 x and 1.7x

as wide as basitarsus, respectively. Calcipala and pedi‑

sulcus (Fig. 6) well developed. All femora and tibiae
densely covered with scale‑1ike hairs (Fig. 8) on outersurface. Claws (Fig. 9) each with large basal tooth.
Wing. Length 1.5 mm. Costa with spinules and hairs.
Subcosta fully haired. Hair tuft on stem vein brown.
Basal portion of radial vein fully haired. Basal cellabsent. Abdomen. Basal scale brownish black, with afringe of pale long hairs; segment 2 dark yellow to lightbrown except narrow portion near posterior margin
brownish black, with light brown tergal plate, white‑pruinose and shiny when illuminated, other segments

and hind tibiae covered with whitish hairs, which arebrightly shiny in light on basal 1/3 and basal 1/2 or alittle more of posterior and outer surface, respectively.
Fore basitarsus somewhat dilated, ca. 5.1 x as long as its
greatest width. Hind basitarsus (Fig. 7) slender, paral‑

lel‑sided, ca. 5.6x as long as wide, and much narrower
than hind femur and tibia, of which greatest breadths
are ca. 2.3x and 1.9x as wide as basitarsus, respective‑
ly. Calcipala and pedisulcus (Fig. 7) well developed. A11

femora and tibiae densely covered with scale‑1ike hairson outer surface. Wing. As in female except length 1.3mm, and subcosta with a few hairs. Abdomen. Basal
scale brownish black, with a fringe of light brown long
hairs. Dorsal surface of abdominal segments black, withbrown short hairs; segment 2 with a pair of light brown,bare medially, and with 16‑18 dark stout hairs on eachlarge, dorsolateral patches, which are silvery shining
when illuminated; segments 5, 6 and 7 each with a pairof shiny, Iarge, dorsolateral patches. Genitalia (Figs.
12‑15). Coxite large, ca. 1.9>< as long as wide. Styleside. Anterior gonapophysis triangular, thin, mem‑much shorter than coxite, gradually tapered towardbrownish black to black, with dark short hairs; ferga 6,
7 and 8 shiny. Genitalia (Figs. 10 and 11). Sternite 8

braneous, densely covered with microsetae, with a few

apex, with single apical spine. Ventral plate transverse,

short setae; inner margin well sclerotized and darkened.
Genital fork of usual inverted‑Y form, with arms curved

medially with distinct projection directed forward; basemuch shorter than wide, remarkably produced ventrally,
densely covered with microsetae on ventral and poste‑rior surface; basal arms directed outward, then forward.

of arms broad with narrow notch inbetween. Paraproct

Parameres narrow, each with 2 Iong parameral hooks

197

and several shorter ones. Median sclerite broad, nearlyparallel‑sided, and with apex rounded. Aedeagal mem‑brane uniformly covered with microsetae. Dorsal plate
wide, thin, iveakly sclerotized, covering aedeagal mem‑brane.

Pupa. Body length ca. 2.0 mm. Head and Thorax.
Integument light to dark brown, moderately or some‑what sparsely covered with round tubercles; antennal
sheath bare. Head with I facial and 3 frontal pairs of
10ng, simple trichomes (Fig. 16). Thorax with 11 simple
trichomes on each side (Fig. 17): 3 Iong mediodorsal
trichomes, 2 dorsolateral ones (1 Iong and I medium)situated anteriorly, I medium dorsolateral one situatedposteriorly, 2 short anterolateral ones just below gillbase, and 3 mediolateral ones (1 Iong and 2 short). Gill
(Figs. 18 and 19) with 4 simple, slender filaments oneach side, arranged in pairs, arising from short basal

a pair of bifid or trifid submedial hook and bifid or
simple lateral hook, and 2 short simple setae, on eachside; sternum 8 usually darkened to some extent, with 1
short simple seta on each side; sterna 6‑8 each with

comb‑1ike groups of very minute spines; sternum 9
darkened, bare; segment 9 with 3 grapnel‑shaped hook‑lets laterally on each side (Fig. 22). Cocoon. Simple,

wall‑pocket‑shaped (or slipper,‑shaped) , somewhat
roughly woven, with several small open spaces in webs,
with anterior margin not thickly woven, and not extend‑
ing ventrolaterally (though I of 12 cocoons examined
extends slightly) ; floor woven on posterior 1/2; individ‑

ual threads distinct; 2.3‑2.5 mm long X 1.0‑1.3 mm wide.

Mature larva. Body length 3.8‑4.3 mm. Body color
grayish green, often mottled with violet brown markings
on posterior abdominal segments, in most of larvae, orcommon stalk; ventral pair of filaments with shortyellowish or yellowish brown in some. Cephalicapotome (Photo. 1) pale except narrow area alongstalk, and distinctly longer and thicker than dorsal pairposterior margin somewhat darkened, with distinct

of filaments which are sessile; inner filament in eachpositive head spots; ventral and lateral surfaces dark‑
ened except eye spot areas. Cervical sclerites (Photo.

pair is slightly longer and thicker than outer one; fila‑

ments somewhat variable in length by individual pupae,
with longest filament (i.e., inner filament of ventralpair) 1.1‑1.6 mm, and shortest one (i.e., outer filamentof dorsal pair) 0.7‑1.2 mm; basal portion of inner fila‑
ment of ventral pair subequal in thickness to interspi‑
racular trunk; all filaments light to dark brown, gradu‑
ally tapered toward apex, furnished with annular ridges
and furrows, and densely covered with minute tubercles

1) , which are absent in earlier instars, rod‑1ike, Iateradand not fused to occiput in last instar. Antenna com‑posed of 3 segments and apical sensillum, much longer
than stem of labral fan; proportional lengths of Ist, 2nd

and 3rd segments 1.0:0.6:1.1. Labral fan with stem
slightly flattened, posterobasal corner notched, with 36‑

40 rays, 0.86 mm in length, medium brown, width ofmedial rays 0.012 mm, microtrichia of similar length,

on outer surface. Abdomen. Terga 1, 2 and 9 grayish
brown, well sclerotized, other terga also sclerotized(and also dark‑colored) to varying extent. Tergum 1

pattern of longer microtrichia with 3‑4 slightly smallerwith I medium, simple seta on each side; tergum 2 with
1 medium, sirnple seta and 5 short, simple setae on eachside; terga 3 and 4 each with 4 hooked spines directed
forward and 2 short, simple setae on each side; tergum
5 with several short simple setae near posterior marginand comb‑1ike groups of very minute spines anterolater‑

composed of 1 Iarge and I small teeth; supernumerary
serrations present. Hypostomium (Fig. 24 and Photo. 2)

ally on each side; terga 6‑8 each with I short, simple setanear posterior margin and comb‑1ike groups of very
minute spines transversely near anterior margin; tergum
9 with a pair of distinct, simple, terminal hooks (Figs. 20

and 21) somewhat bent anterodorsally, and with apex
rounded, and comb‑1ike groups of very minute spinestransversely near anterior margin; terga 5‑9 without
spine‑combs. Sternum 3 with a few short simple setaeon each side; sternum 4 with I simple hook and 3 short
simple setae (1 of them somewhat longer and stouter)on each side; sternum 5 with a pair of bifid or trifid
hooks submedially on each side; sterna 6 and 7 each withones between. Mandible (Fig. 23) with comb‑teeth
decreasing in size from Ist to 3rd; mandibular serrations

with a row of 9 apical teeth, of which median and corner
teeth are largest, subequal in length to each other, and3rd and 7th teeth are smallest; Iateral serrations welldeveloped; hypostomal bristles 5 or 6 in row, diverging
posteriorly from lateral margin on each side. Postgenal
cleft (Photo. 2) absent. Thoracic and abdominal cuticle

almost bare except small areas on both sides of analsclerite covered with pale short setae. Rectal papillacompound, each of 3 Iobes with 0‑2 (mostly 1) finger‑
like secondary lobules ventrally. Anal sclerite (Fig. 25)

X‑shaped, posterior arms longer than anterior ones;
accessory sclerites present, extending ventrally andcontinuous to each other (in earlier stages, accessory
sclerites are present likewise but they are usually dis‑continuous at the ventral midline) . Ventral papillae
present ventrolaterally. Posterior circlet of hooks with

198

ca. 104 rows of up to 13 hooks per row.

SPECIMENS EXAMlNED Immature larvae, collected
at Ngardmau Falls, NW Babeldoab Is., Palau, 14.Vll.

1997, P.S. Cranston. Reared adults (7 females and 1male) , all associated with their pupal exuviae andcocoons, 25 pupae, and 10 mature larvae, many othermature and immature larvae collected from first rapid.':;i' ::'*1:*: j:=; ;*,' ,'･:,. ,. !:/}:! =i

x

=*

7tl+.

: &*,r f.:

3

2

5

{ ;oO.

f

io

1

l' l

1 ,

l,
J,
,t]
f

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.‑,,"'...b #:

bC

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,,; ;L! ?; l , " ‑*},:i : :iik', , ,, ftX iL *1 tl.

'V,:"p'!/^'
L '!" i ":.i' "**.= .} i:. i*'.i:=.*.*:=;

Ti :L: ::': ;:': ")If;:il : "J""{;1 :1 'F ' '= *:**= 'i"' " 'Is:;h̲;'l" ･/' { ';'j ' I f'{iR:1!{{}{1 {..,; ,t: : ･':' *"i :'t ; *:* 'i*'i i ;i' *‑ ';;;'‑"':!"TF '::;!!':iji;; ;';'' rrrl"'1 't;1"ItPl;'rl ltrl'**'};=1:'1
lr Inl" r'r"{11{1 t"""'1' !t' /f If
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ll '

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^ "F*' "i{¥¥*" $ *:1=' 1j!{';:" ':* 1,:"̲ii'l
1 11L ;1 l}'lLllt :' ' '11 l¥11¥Li:;t :L':;il t' '; '1 : '/*f '*{: 't" i Y*}'*' '*/')"Js
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' L '

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Figs. 1‑15 Characters of the female and male of Simulium (Gomphostilbia) palauense. 1, fronto‑ocular areaof female; 2 and 3, 3rd segments of maxillary palp showing sensory vesicle (2, female and 3, male) ;4, apex of female mandible; 5, cibarium of female; 6 and 7, basitarsi and 2nd tarsal segments of hindlegs (6, female and 7, male) ; 8, scale‑1ike setae of femora and tibiae of female; 9, female claw; 10,
female genitalia in situ (ventral view) showing 8th sternite, anterior gonapophyses, genital fork,
paraproct and cercus; 11, paraproct and cercus (lateral view) ; 12, male genitalia in situ (ventralview) showing left coxite and style, and ventral plate; 13, ventral plate (end view) ; 14, paramere(dorsal view); 15, median sclerite.

199

on the main tributary (Photo. 3) of the Diongradid
River, near Ngardmau Falls, NW Babeldoab Is., Palau,reard adults, together with their pupal exuviae andcocoons, 5 pupae, and many other mature and immature

4.XII.1998, D.A. Craig and R.E.G. Craig.

larvae (D.A. Craig, Univ. Alberta) . All these specimens

are preserved in 80% ethanol.

DEPOSITION OF MATERIAL. 4 reared adults (3females, I male) , together with their pupal exuviae and

ECOLOGICAL NOTES. The locality, known generally

cocoons, 5 pupae, 5 mature larvae (Bernice P. Bishop
Museum, Hoholulu) , 2 female reared adults, together
with their pupal exuviae and cocoons, and 5 pupae, 5mature larvae (H. Takaoka, Oita Med. Univ.) , 2 female

as Ngardmau Falls is a major tourist attraction in
Palau. Since road travel is impossible if it has beenraining, the falls are best reached by boat, from Koror,

up the westernside of Babeldoab, a one‑hour voyage to

r‑‑‑‑
ll'
l

1' , L I, f ,,tl I r'o

II1111 ¥. .11 1 'LII Y':" I' I.,

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1 , ;1rl i
lr ' e e ;'.,1'iIl oi ':e eb

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̲‑s Q'eeo+ 't

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'

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111,,
̲/*¥
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pl i

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,

̲̲̲̲ /

Figs. 16‑25 Characters of the pupa and mature larva of Simulium (Gomphostilbia) palauense. 16‑22, pupa;
23‑25, mature larva. 16, frons and part of face (1eft half only) ; 17, thoracic integument (1ateral view)

showing arrangement of 11 trichomes; 18, gill filaments (1ateral view) ; 19, basal portion of gill
filaments (dorsal view) ; 20 and 21, terminal hooks (20, end view and 21, Iateral view) ; 22, grapnel‑
shaped hooklets; 23, apex of mandible; 24, anterior half of hypostomium; 25, anal sclerite with a welldeveloped accessory sclerite.

200

Particulate material in the water was 1.30‑1.90 mg/1.

" . ..! . ' ; i;*< **: "il ･ *

‑

;

" i

; .

,

･/!!!fr,.?･"‑

̲.*.. ;･.

Larvae and pupae were found in large numbers on
the rock in full flow and also on leaves that weretrapped in shallow water which flows over them. The
leaves appeared to be the preferred habitat. Larvae of
S. palaue ase do not twist their bodies longitudinally,

similar. to larvae of the madicolousflow inhabitingfin.<... ""

: ;""i"' , ･ . ･.,･;'; : .

{*;,,*=.

Tahitian S. (Ipilselidlum) cataractarum (Craig, 1997).
From the same rapid, collected was a single in'nTlaturelarva of the other simuliid s.pecies. This second species
lacks a postgenal cleft like S. p(llauense, but has well‑‑developed ventral papillae placed ventrally, no supernu‑

merary serration on the mandible, and no accessory
sclerite around the posterior circlet of hooks. No otherinvertebrates were taken except a few Chiranomidae
larvae and aquatic pyralid lepidopteran larvae.
Since this is the only locality sampled for immature

stages of s̲imuliids in Palau, and S. palauense larvae
appear specialized for fast flow, it is possible that smal‑ler streams, yet unsampled, will have theecond or others pecies.

2

REIVIARKS. Female and male adults reared from pupae
collected by un (D.A.C. and R.E.G.C.) are conspecifl.'c tothose of S. palauense described by Stone (1964) , accord‑

ing to the comparison of the genitalia, and the shape andcoloring of the body and legs. This result confirms thatthe association of both sexes of adults of S. palauense

made by Stone was correct. The morphological charac‑ters of the present adult specimens agree with the.
original descriptions and illustrations given by Stone(1964) except a few characters. In the original, terga 8

and 9 of the female abdomen were stated to be shiny, but
in fact terga 6, 7 and 8 (and also 9) are all shirLy; in

Photos. 13 1 and ? , head capsule of mature larva ofaddition, gray‑pruinose areas were mentioned to be

Simidium ( Gomphostilbia) palauense ( l, dorsal view; 2,ventral view; scale bars=0.2 mm) ; 3, habitat of S. (G.)
palauense larvae: first rapid, main tributary of the Dion‑

present at least on sides of tergum 2 of the male abdo‑

gradid River, near Ngardmau Falls, NW Babeldoab Is.,
Palau.

men, but these are found on terga 2, 5, 6 and 7; thefemale calcipala is large but not reaching the apex of
the second tarsal segment, though noted so in the origi‑
nal description.

the Ucherael jetty and then by= vehicle past Ngetbang

It is noteworthy that S, palauense has several

Village. A anehour walk up the Diongradid River

remarkable pupal an, d larval characters which are not(or very rarely) possessed by any other species of thepasses the Medallaiechad waterfall, which is the main
attraction, and shortly thereafter reaches a major rapid

at N7"35'267"; E134 35 304" The n er here Is at 10 m
altitude, 8 m wide, between l7 cm depth and flowing
extremely rapidly, with velocities of 125300 cm/s. Air

temperature was 31.5'C and water temperature 27.0'C
under overcast conditions. Since the substrate wassubgenus GomphostiJbia. In the pupa, the absence ofspine‑combs on the abdon. Ien has not been recorded
previously in this subyenus, though this is one of the key

characters of the subgenus Wallacellum (Takaoka,1983); the reduced number (i.e., four) of the gill fila‑

black basalt, water temperatures are likely to be muchments has been known only in a fe v species of the
ceylordcumgroup collected from Sulawesi and Flores,

higher in full sunshine. Canductivity was 40,lS and pH 8.0.

Indonesia (Takaoka, unpublished data) and in one

201

species from the Solomon and Bougainville Islands

which remains very obvious, and is connected dorsally(Takaoka, 1994, 1995). In the larva, three characters,i.e., the absence of a postgenal cleft, the presence ofserrations on the lateral margins of hypostomium, andthe presence of supernumerary mandibular serrations,have not been found; in addition, this species has acces‑with the anal sclerite proper. However, the extension isoften discontinuous at the ventral midline. In S. palauen ‑sory sc, Ierites on the last abdorninal segment, a charac‑

ter being reported only in a few Gomphostilbia species
collected from Papua New Guinea (Smart and Clifford,1965) and lrian Jaya (Takaoka, unpublished data) .

se this sclerite is constructed differently and is notconnected to the anal sclerite proper, but is continued
strongly cornpletely around the circlet. The only evi‑
dence of the accessory sclerite, as known in other sub‑genera, is a paler dorsolateral area (Fig. 25).

ACKNOWLEDGEMEN T

Although having such unusual characters, S.
palauense belongs in the subgenus Gomphostilbia byThis study was supported in part by the Grant‑in‑having the following combinations of characters: adultAid of Ministry of Education, Science and Culture,

thorax with the bare pleural membrane and haired

Japan (no. 11670246) to H.T. Financial support for D.A.

katepisternum, wing with the basal portion of radialvein fully haired, male genitalia with a ventral plate
hairy on its ventral and posterior surface, and with

C. was from the Natural Sciences and Engineering
Council of Canada, grant # OG5753.

several parameral hooks, pupal head with three pairs offrontal trichomes, pupal abdomen with grapnel‑shaped
hooklets on the sides of the last segment, and larval
abdomen with ventral papillae. This species is further
assigned in the batoense‑group, defined by Takaoka andDavies (1996) , by having the antenna of both adult sexes

11‑segmented, the female tarsal claw with a large basal

tooth, and the male hind basitarsus parallel‑sided,
though the pupal gill filaments of this species are four inplace of eight.

REFEREN CES .
1 ) Craig. D.A. (1997): A taxonornic revision of the black
fly subgenus Inseliellum (Diptera: Simuliidae) . Can. J.
Zool., 75, 855‑904

2 ) Craig, D.A. and Currie, D.C. (1999): Phylogeny of theCentral‑Western Pacific subgenus Inseliellum (Diptera:
Simuliidae). Can. J. Zool. (in press)

3 ) Crosskey, R.W. (1989): Family Simuliidae. In: N.L.
Evenhuis ed. "Catalog of the Diptera of the Australasianand Oceanian Regions". Bishop Mus. Spec. Pub. 86,

Larvae of S. palauense show considerable mor‑
phological convergence with the madicolous‑flow in‑

1155p. Bishop Mus. Press, Honolulu.
4 ) Smart, J. and Clifford, E.A. (1965): Simuliidae (Dipte‑

habiting larvae of S. cataractarum of Tahiti (Craig,ra) of the territory of Papua and New Guinea. Pac.

1997) . While there is not the same reduction in numberof labral fan rays, the fan stem is similarly slightly
flattened and possesses a posterobasal notch. Craig andCurrie (1999) suggest that this fan‑stem shape is used tomanipulate madicolous flow into the fans. The post‑
genal cleft in S. cataractarum while present, is reduced.

Body shape is also similar, in that both have amphora‑shaped posterior abdomens, expanded rapidly at the 5th
abdominal segment and smoothly decreased posteriorly;
probably an adaptation for fast flow.
Both species possess a sclerite that is continuous
around the circlet of hooks. In S. cataractarum, thisappears to be an extension of the accessory sclerite,

Insects, 7, 505‑619

5 ) Stone, A. (1964): Diptera: Simuliidae. Insects of Mi‑
cronesia, 12, 629‑635

6 ) Takaoka, H. (1994): A new blackfly species ofSimulium ( Gomphostilbia) from Solomon Islands, South
Pacific (Diptera: Simuliidae) . Jpn. J. Trop. Med. Hyg.,22, 103‑108

7 ) Takaoka, H. (1995): The Simuliidae (Diptera) from the
Bougainville Island, Papua New Guinea. Jpn. J. Trop.
Med. Hyg., 23, 253‑266
8 ) Takaoka, H. and Davies, D.M. (1995): The black flies(Diptera: Simuliidae) of West Malaysia. Kyushu Uni‑
versity Press, Fukuoka, viil + 175p.

VOL、27NO．2
JUNE1999
CONTENTS

Original

articleTongol−Rivera，P．，Kano，S．，Villacorte，E．，Darilag，A．，Migue1，E．and

Suzuki，M．

Application of Seroepidemiology intheEvaluationofaCommunity BasedMalariaControl
Programin

Parawan，thePhilippines・………・……………………・……………・・…………………・161−165

Islam，M．A．，Nakamura，Y．，Wongkhomthong S．A．，Chowdhury，S．A．，and Ishikawa，N．
Involvement of Community Health Workers in Tuberculosis Control in Bangladesh・・

一167−173

Matsumoto，」．，Kirinoki，M．，Kawai，S．，Chigusa，Y．，Ilagan，E．」．，Ducusin，B．E．，Yasuraoka，K．

andMatsuda，H．

Prevalence of Schistosomiasis Japonica among Schoolchildren and Animal Reservoirs inOriental MindoroンPhilippines………・……・…………・・…………・一…・…一……………・・………・175−180

Krudsood，S．，Chokejindachai，W．，Silachamroon，U．，Phumratanaprapin，W．，Viriyavejakul，
P．，Bussaratid，V．and

ClinicalMalaria

andLooareesuwan．，S．

TreatmentofMultidrug

Resistance

FalciparuminThailand…………181−188

Takaoka，H．，Saito，K．and Suzuki，H．
S物％枷彫（飽泥 ％n％勿）60朋蜘s召fromtheQgasawara（Bonin）Island，Japan（Diptera：S㎞uliidae）：
Taxonomic Assignment to the％7捌吻一group and Descriptions of Male，Pupa andMature Larva一………・……一…一……………………・…・……………・・…………・・……・…………189−194

Takaoka，H．and Craig，D．A．
Taxonomic and Ecological Notes onξ魏％1伽卿（（30卿ρhos痂伽）勿伽8％s8（Diptera：Simuliidae）

from

Palau，Micronesia，with

Larva……・…………・…・…・…………・…・………・……・………』…・……・………………一・…………・195−201

RedescriptionsofAdultsandDescriptionsofthePupaandMature