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第26巻第3号平成10年9月
内
原

容

著
わが国における輸入マラリアの現況（英文）

一大友

弘士，竹内

勤

一15H56

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高岡 宏行，Odile Bain…………・……一…一…

一15H601991年，1992年の沖縄県の犬における0〃瞬馳吻吻〃z漉sの侵淫状況（英文）一當間 孝子，宮城 一郎，渡久山有子，安里 龍二，
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5亜種Onoo解6Z伽毎hゆ8η廊貝体内に於ける各産地日本住血吸虫セルカリアの発育状況の比較（英文）

一岩永

嚢，李

金木，萢

乗真，辻

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会報・記録
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151

Jpn. J. Tro p. Med. Hyg., Vol. 26, No. 3, 1998, pp. 151 156

STUDIES ON CURRENT TREND OF IMPORTED
MALARIA IN JAPANHIROSHI OHTOMO1 AND TSUTOMU TAKEUCH12
Received May 13, 1998/Accepted June 17, 1998

Abstract: Current epidemiologic and therapeutic aspects of imported malaria in Japan were examined from1980 to 1995 by sending questionnaires every year to more than 1,500 major hospitals. Imported malaria
gradually increased in nurnber from 1980 and became more than 100 from 1990. The number of cases withfalciparum malaria increased in number from around 1993 and becarne comparable to the nurnber of vivax
malaria. As the presumptive place of contraction, Africa has been increasingly important, especially for
falciparum malaria. Recently the nurnber of foreign cases, most often from India, has been becoming rather
high, ranging 24 to 36% of the total cases. We found 7 fatal cases with falciparum malaria, all of whom

seemed to be infected in Africa except for a Japanese female due to domestic transfusion malaria.
Recrudescence and relapse were detected at significant rates, i.e., 2.2 to 9.5% and 5.4 to 17.2% of the caseswith falciparum and vivax malaria analyzed, respectively. Concerning the antimalarial drugs available inJapan, mefloquine has been the drug of choice after the Research Group for Development of Chemother‑apeutic Agents against Tropical Parasitic Diseases supported by the Japanese Ministry of Health andWelfare started its import for clinical trial. Further efforts are still needed to improve the diagnostic andtherapeutic capacity against imported malaria in Japan.

Key words: Imported malaria, Mefloquine, Plasmodium falciparum, Recrudescence, Relapse

INTRODUCTION

mission of malaria parasites was terminated and thepriority of medical research and education has been

Malaria has been increasingly a serious healthhazard in most of the endemic areas, especially in
Africa. At present it is estimated that more than 2placed on such chronic diseases as cancer and vasculardisease. However, as the number of travellers abroadhas been increasing, some tropical parasitic diseases

bil.lion people are at the risk of infection. Approximate‑have been re‑emerging as imported infections. Un‑

ly 300 to 500 million of clinical cases and 1.5 to 2.7
million deaths by malaria occur every year. Morbidity
and mortality due to this infectious disease have notdoubtedly, malaria is one of the serious imported para‑
sitic diseases in developed countries. Thus, measuresfor early diagnosis and effective treatment should beorganized as quickly as possible.

shown any clear trend of decline; rather even somesocial and civil unrests like large‑scale population

As an effort for the chemotherapy of imported

movements have produced new problems on malaria

malaria in Japan, the activity of the Research Group for(Gilles, 1993). In addition, other factors, from theeconomic and agricultural to those concerning priority
setting in the investment in public health have been
apparently affecting the recent epidemiology of malaria

Development of Chemotherapeutic Agents against Trop‑ical Parasitic Diseases has been playing an important(Suzuki, 1997). Thus, current situation of malaria is notcians. Also on the basis of recent efforts by thisascribed to any single cause in the endernic area.

Research Group, some epidemiologic issues of imported
malaria in Japan have been made clear, a part of whichis reported in this communication.

On the other hand, in developed countries, malaria
has beeh of little concern, probably because new trans‑role. It adopted mefloquine for the first time as one ofthe drugs supplied on the request of responsible physi‑

1 Departrnent of Tropical Diseases, Jikei University School of Medicine, Minato‑ku, Tokyo 105‑0003, Japan
2 Department of Tropical Medicine and Parasitology, School of Medicine, Keio University, Shinjuku‑ku, Tokyo 160‑0016, Japan
Address for correspondence to: Tsutomu Takeuchi, Department of T,ropical Medicine and Parasitology, School of Medicine, Keio
University, Shinjuku‑ku, Tokyo 160‑0016, Japan

152

70

MATERIALS AND METHODSThe Research Group for Development of Chemo‑
therapeutic Agents against Tropical Parasitic Diseases
was organized in 1980 by Prof. Hiroshi Tanaka, Insti‑
tute of Medical Sciences, University of Tokyo, on thebasis of support from the Japanese Ministry of Healthand Welfare. This Group has been responsible for thenationwide, comprehensive investigations on

60
50‑H:1‑ p. vivax

40
30

epiderniology of parasitic diseases including imported
malaria in Japan in addition to a variety of other duties.

Every year from 1985, questionnaires concerning
occurrence of malaria have been sent to 1,500‑1,700
major hospitals in Japan. Responses to the question‑
naires have been summarized by the authors. Identifica‑tion of malaria parasites was essentially done by respon‑sible physicians and collaborating laboratories, mostly
parasitology departments in medical schools, and report‑

20‑ ,‑ p. falciparum10

1978 1983 1988 1993

Figure I Annual number of imported falciparum and vivax
malaria cases from 1980 to 1995. The vertical axis
stands for the number of cases with either malaria
each year.

ed to us. When further identification seemed to be1). Although there seemed to be a possibility that thenecessary, e.g., confirmation of the mixed infection, we

number was underestimated, approximately 56% of the
grand total cases were due to Plasmodium vivax, andrequested stained specimens of patients' blood andidentified species of malarial parasites. Informed con‑sent, if needed, was obtained from the cases with import‑
ed malaria.

32% due to Plasmodium falciparum. The cases with
Plasmodium malariae and Plasmodium ovale were muchless and approximately the same in number; about 2% of
the whole cases.

Such a trend of falciparum and vivax malaria is

RESULTS AND DISCUSSION

more clearly illustrated in Figure. l. From 1993, fal‑

The annual number of malaria patients gradually
increased and became more than 100 from 1990 (Table

ciparum and vivax malaria became comparable in thenumber of patients. Of particular importance is that
more than 70% of the Japanese cases were due to fal‑

Table I The number of irnported malaria cases in Japan
from 1980 to 1995 summarized by the ResearchGroup for Development of Chemotherapeutic

ciparum malaria and less than 25% due to vivax malaria
during 1992 to 1995 (data not shown) , which should betaken into consideration for establishing the counter‑

Agents against Tropical Parasitic Diseases

measures against drug resistant and/or complicatedYear P. vivex P, falciparum P. malariae P. ovale Mixed Unknown Total
1980

58

29

l

2

3

94

1981

54

21

2

2

6

86

1982

51

26

5

1

3

87

1983

59

17

4

2

1

5

88

1

malaria.
Concerning the possible place of contraction, morethan 70% of falciparum malaria seemed to be originatedfrom Africa, while 60‑70% of vivax malaria was from
Asian regions (data not shown) . This is generally inagreement with the data on imported malaria in otherdeveloped countries like Canada (Lynk and Gold, 1989) .

1984

54

27

4

O

O

5

90

1985

43

20

2

O

O

4

69

1986

49

25

O

3

2

4

83

1987

41

18

2

4

2

6

73

1988

47

28

1

O

o

78

1989
i990

50

31

2

O

3

7

93

62

40

O

3

5

6

116

Year Total Japanese Cases Foreign Cases

1991

63

43

3

O

3

114

1990

116

88 (75.9%)

28 (24.1%)

1992

70

26

O

3

4

9

112

1991

114

73 (64.0%)

41 (36.0%)

1993

60

40

2

5

3

2

112

1992

112

74 (66.1%)

38 (33.9%)

1994

39

46

3

4

5

7

104

1993

112

85 (75.9%)27 (24.1%)

1995

56

51

1

5

4

o

117

1994

104

76 (73.1%)

28 (26.9%)

856

488

32

37
34 69
1 , 516

1995

117

87 (74.4%)

30 (25.6%)

Table 2 Ratio of Japanese and foreign imported
malaria cases from 1990 to 1995

153

Table 3 Nationalities of foreign cases with im ported
Countries

1990

1991

1992

1993

1994

1995 Total

India

2

11

Sri Lanka

Vietnam

2

2

2

6

7

3

1

2

1

2

Philippines
1

3

6

3

2

6

l

1

Brazil

2

3

1

2

2

2

4

approach, e.g., understanding of different languages and9customs.

11

6

3

1

2

3

1

1

imported malaria prompts medical professionals inJapan to face a novel situation and to employ another

6

3

4

1

6

41

4

1

3

Papua New Guinea

USA

6

2

Indonesia

China
2 . American Region

5

1

ThailandMyanmar

1

8

2

11

2

3

7

3 . European Region

Concerning the clinical aspects, 7 fatal cases due to

falciparum malaria were recorded from 1990 to 1995
(Table 4) . Among them, an attention must be paid to a
70 year old Japanese female, who had never been abroadand died of malaria after platelet transfusion conductedat her own resident city. However, the donor could not
be identified (Kano and Suzuki, 1994). Virtually all ofthese cases died within 7 days after reentering into

Japan, although some of them had administration ofUnited Kingdom

41

4 . African Region
2

7

Nigeria1

Tanzania
Sudan

1
1

1

1

Ghana

2

2

1

2

8

1

1

3

2

1

1

5

l

lvory Coast

Cameroonand Ghana. The number of imported cases from India
appears to be constant from 1990. Such a trend of recent

1 . Asian & Pacific Region
Israelcountries, India has been most prominent in number
followed by Philippines, Brazil, United States, Vietnam

malaria in Japan frorn 1990 to 1995

1

1

3

4

quinine, chloroquine, Fansidar and/or even artemisinin.
Previous literatures also reported that the fatal caseswith imported falciparum malaria had the average
duration of illness from I to 8 days (Philpott andKeystone, 1987) , which stresses the necessity of early
diagnosis and prompt treatment. In accordance with thefact that falciparum malaria has recently been more
serious in Africa, five of the six fatal cases other thanAs one of the characteristics concerning recent

the 70 year old Japanese female seemed to be infected intrend of imported malaria in Japan, it is pointed out thatpatients has been ranging from 24 to 36% of the wholecases since 1990 (Table 2).
Nationalities of the foreign cases with imported

Africa. This also seems consistent with the generaltrend of falciparum malaria in Japan as noted above.
Rates of recrudescence and relapse of falciparumand vivax malaria, respectively, are summarized inTable 5. From 1990 to 95, the number of recrudescentfalciparum malaria was I to 3 cases, corresponding tomalaria were shown in Table 3. Among a variety of

2.2 to 9.5% of the cases analyzed each year. Though therather many foreign cases with malaria have needed
medical care. The rate of imported foreign malaria

Table 4 Fatal cases with imported or domestic falciparum malaria in Japan
from 1990 to 1995
Year Case

Contractiont

Pur pose

PeriodS

Treatment

4 daysQuinineCommerce, 2 months

1 day

Quinine
Chloroquine

Sight‑seeing, 7 days

7 daysChloroquine
QuinineFansidarFansidarArtemisinin

1990

64, M

lvory Coast

Industry, 14 days

1991

70, F

(Platelet transfusion)

1991

28, M

DomesticThailand1992

36, M* Kenya

1994

30, M

Mali

Investigation, 1 month

7 days

1994

30, M

West Africa

Sight‑seeing, 10 days

3 days

1995

50, F

Af rica

Sight‑seeing, 14 days

O day

*UK. A11 other cases were Japaneset Presumptive place of contraction
Purpose of trip with the period of stay
S Period from re‑entering into Japan to the onset of disease

154

Table 5 Recrudescence and relapse of imported falcipar‑
um and vivax malaria, respectively, in Japan
from 1990 to 1995
Falciparum malariaGroup by request; however, a rather high rate of relapse

may be attributed to lack in primaquine administration
because of the mixed infection with P. falciparum at

Vivax malaria

least partially.

Year No. Cases Recrudescence* No. Cases Relapse*
Analyzed

The drugs employed for recrudescent and relapsingmalaria cases were summarized in Table 6. It is evident

Analyzed

1990

37

3

52

7

1991

36

3

44

4

1992

21

2

46

3

1993

36

3

48

6

1994

31

1

29

5

1995

45

1

37

2

that recrudescent falciparum malaria were initiallyadministered with a variety, of drugs; however, 7 out of

the 11 cases were given only chloroquine and/or Fan‑sidar, which might represent recrudescence by chloro‑
quine resistant P. falciparum, although the drug suscepti‑

bility was not examined. Quinine was administered tothree of them. On the other hand, relapse in the caseswith concomitant infection of P. falciparum with P.

* : Number of recrudescent and relapsing cases among the patientswith falciparum and vivax malaria analyzed each year, respec‑tivelyvivax seemed rather common. Analysis of the drugs
rate appeared to decrease from 1994, it should not be given to these cases probably suggests that the coinfec‑
expected that the rate will further decrease as judged tion with P. vivax may have been overlooked. It is alsofrorn the widespread drug resistant falciparum malaria possible that the radical treatment with both schizont‑in the endemic areas. The number of relapsing vivax cides and primaquine was not attempted simply because
malaria was 3 to 7 cases, ranging from 5.4 to 17.2%.
of the lack in knowledge on the chemotherapy of relaps‑

Primaquine has also been supplied by our Research ing malaria.
Table 6 Drugs employed for primary treatment of falciparum malaria and mixed infection with
Plasmodium falciparum and P. vivax or P. ovale which resulted in recrudescence andrelapse, respectively, in Japan

Falciparum malaria

Mixed Infection

Contraction*

Drugs

S pecies

Contraction*

Drugs

Consequence t

Papua New Guinea

Halofantrine

Pf, Pv

VietnamQuininePv

Mef loquine

Minomycin
Thailand

QuininePf, Pv

India

Chloroquine

Pv

Pf, PvIndia

Mef loquine

Pv

Pf, PvThailandFansidarPv

Minomycin
Southeast Asia

Mef loquine

QuinineSolomon Islands

Chloroquine

Primaquine

Mef loquine

Primaquine
India

Tanzania

Chloroquine
QuininePf, PvPf, Pv

Pa puaPv

New Guinea

QuinineFansidarIndonesia

Quinine,Pv

Primaquine

Fansimef
Artemisinin

Myanmar

FansidarPf, PvIndonesia

Mef loquine
Artemisinin

Pv

Myanrnar

Chloroquine

Pf, PoAf rica

Chloroquine

Pv

ThailandFansidarIndonesia

Chloroquine
FansidarCameroon

Fansidar

Pf

Presumptive place of contraction
Species of malaria parasite detected after relapse
P. falciparumPv
Po

P. vivax
P. ovalet

155. The activities of the Research Group for Develop‑
ment of Chemotheriapeutic Agents against Tropical(Table 7) . Mefloquine was occupying only 5.6%, which
was probably based on the personal import. However,Parasitic Diseases has been significant in regard toafter we started official import of mefloquine, it eventu‑

establ, ishing countermeasures against parasitic diseases

ally occupied more than 60% in 1995, virtually all ofwhich were supplied by the Research Group. Moreover,
all of the records on outcome and laboratory data of
mefloquine administration have been maintained by the
Research Group. So far, we have found neither serious
adverse effects nor resistant falciparum malaria con‑cerning mefloquine.
There seems to be no doubt that malaria, mostly as
an imported tropical disease, has been increasingly

in Japan. For these 15 years, this Research Group has
been actively functioning in many aspects of education,
consultation and surveillance on tropical parasitic dis‑eases including imported malaria (Takeuchi, 1993). It
has published a booklet for standard method of chemo‑
therapy of parasitic diseases, which has been distributed

free of charge. One of the most important activities ofthis Research Group is to import appropriate anti‑para‑

informed consent. Before the drugs were supplied, they
were cleared for inspection of the standard for medi‑

important in clinical medicine of Japan as well as otherwestern countries (Miller et al., 1989; Lynk and Gold,1989). It is one of the infectious diseases which should
be reported to the Ministry of Health and Welfare in
Japan. However, this governmental surveillance systemdoes not appear to cover all of the cases with imported
malaria. In 1993, the Ministry reported occurrence of 58

cines by Japanese law. Current drugs which can becases of malaria, whereas the Research Group summar‑

supplied by this Group includes those against amebiasis,ized 109 cases.

sitic drugs, which have not been officially approved inJapan, and to maintain thern under appropriate condi‑
tions as well as supervisions. Based on the request, theResearch Group has been supplying these drugs as theirclinical trial under the responsibility of physicians withgiardiasis, trypanosomiasis, Ieishmaniasis and stron‑

In Japan, currently available clinical measures

gyloidiasis as well as malaria. Among these drugs,
mefloquine has been requested most frequently. We
have imported more than 1,500 tablets of mefloquine

against malaria do not seem entirely sufficient. First of(Lariam tablet, Roche) since 1991.

all, at present, no antimalarial drugs are commerciallyavailable except for Fansidar. Moreover, the number of
personnels as well as laboratories for accurate diagnosis

Concerning the drugs chosen in Japan for chemo‑of malaria is not large enough. Under such circum‑

therapy of imported malaria before we officially started

stances, it is quite important that antimalarial drugs liketo import mefloquine, cornbination of Fansidar andchloroquine seemed to be employed most frequently

mefloquine have been available as orphan drugs throughactivities of such official organs as our Research Group.

As shown earlier in this communication, meflo‑
Table 7 Comparison of drugs employed for chemotherapy
of malaria between 1990 and 1995

quine, which has been supplied by our Research Group,
is now the drug of choice for chemotherapy of imported
malaria, especially of falciparum malaria. It is still of

Fansidar + Chloroquine

22 . 2%

Mef loquine

61 . 5%

Fansidar

19 . 4%

Mef loquine + Fansidar

5 . 1%

significant utility in such a developed country as inJapan despite the occurrence of mefloquine resistant P.
falciparum in the endemic areas (Webster et al., 1985).

Fansidar + Quinine

19 . 4%

Quinine + Fansidar

5.1%

Moroever, there have been many requests for meflo‑

Fansidar + Tetracycline

5 . 6%

Quinine + Tetracycline

5 . 1%

quine for prophylaxis, though it is not acceptable for the

Chloroquine + Fansimef

5.6%

Mef loquine+Quinine

2 . 6%

Research Group. As far as we know, halofantorine,

Mef loquine

5 . 6%

2 . 6%
Mef loquine + Quinine+ Tetracycline

MP Tablet*

2 . 8%

Mefloquine+Artemisinin 2 .6%

Fansidar + Quinine+ Chl oroquine

2 . 8%

Quinine + Halofantrine 2 . 6%

Fansidar + Quinine+ Tetracycline

2.8%

Quinine + Halof antrine 2 . 6 %+ Tetracycline

another antimalarial, as well as mefloquine is underclinical trial in Japan and is expected to appear inmarket soon. Artesunate, which has been employed forthe chemotherapy of severe and complicated malaria

Chloroquine
Chloroquine + Quinine

2 . 8%

Quinine + chloroquine 2 . 6%

2.8%

Quinine + Fansidar 2 . 6%

sessed by the Group.
Such Japanese situations of irnported malaria andChloroquine + Fansimef

2 . 8%

Fansidar + Tetracycline 2 . 6%

the system for its chemotherapy should be evaluated

Chloroquine

through comparison with those of other developed coun‑

1995 (n=39)

1990 (n=36)+ Tetracycline

Fansimef+ Tetracycline

2 . 6%

2 . 8%* : Tablet containing both sulfamonomethoxine and pyrimethaminewith mefloquine (Hien et al., 1996), has also been pos‑tries. At least it is evident that further official commit‑

ment to malaria by the government as well as medical

156

prof essionals must be sought in consideration of its

seriousness as a re‑emerging infectious disease.

Japanese)4) Lynk, A. and Gold. R. (1989): Review of 40 children
with imported malaria. Ped. Infect. Dis. J., 8, 745‑750

5) Miller, K.D., Greenberg, A.E. and Campbell. C.C. (1989) :ACKNOWLEDGEMENT
We thank all of the physicians who kindly respond‑
ed to our questionnaires throughout this study.

REFERENCES
1 ) Gilles, H.M. (1993): Epidemiology of malaria, In Essen‑tial Malariology. 3rd edn. (eds. Gilles, H.M. and War‑rell, D.A.), 124‑163, Edward Arnold, London

Treatment of severe malaria in the United States with acontinuous infusion of quinidine gluconate and exchangetransfusion. N. Eng. J. Med., 321, 65‑70
6) Philpott, J. and Keystone, J.S. (1987) : Severe falcipar‑
um malaria. Can. Med. Assoc. J., 137, 135‑136

7) Suzuki, M. (1997) : Emerging infectious diseases andreemerging infectious diseases ‑ Malaria. Antibio.
Chemother., 13, 191‑197 (in Japanese)
8 ) Takeuchi, T. (1993): Chemotherapy of irnported tropi‑

cal parasitic diseases. Mod. Med., 22, 38‑40 (in2 ) Hien, T.T., Arnold, K., Vinh, H. and Vinh Chau, N.V.
(1996): Treatment of iresistant malaria: From healthJapanese)9 ) Webster, H.K.. Thaithong, S., Pavanand, K., Yongvanit‑

post to university hospital. Abstracts, XIV International

chit. K., Pinswasdi. C. and Boudreau, E.F. (1985):
Cloning and characterization of mefloquine‑resistantCongress for Tropical Medicine and Malaria. p. 139
3 ) Kano, S. and Suzuki, M. (1994): A case of accidental
transmission of Plasmodium falciparum through platelettransfusion. Jpn. J. Trop. Med. Hyg., 22, 193‑198 (inPlasmodium falciparum from Thailand. Am. J. Trop.
Med. Hyg, 34, 1022‑1027

157

Jpn. J. Tro p. Med. Hyg., Vol. 26, No. 3, 1998, pp. 157 160

AN ONCHOCERCA SPECIES FROM CATTLEON KYUSHU ISLAND IS O. SUZUKII,A TRANSFUGE PARASITE FROM

THE JAPANESE ENDEMIC BOVID,CAPRICORNIS CRISPUSSHIGEHIKO UNl*, YOSHITAKA SUZUK12, HIDEYUKI CHIBA3,AKIRA KATSUM14, HIROYUKI TAKAOKA5 AND ODILE BAlN6
Received May 6, 1998/Accepted June 10, 1998

Abstract: In 1988‑1989, microfilariae of an unidentified Onchocerca species were found in the skin of eightof the 16 cattle aged at least 5 years that were examined in Oita, Kyushu, Japan. Adult worms were notfound in cattle, but the microfilariae taken from skin snips, which have coiled posterior parts, were grown
to the infective stage in simuliid. In 1997, both adults and microfilariae of O. suzukii were recovered fromJapanese serows ( Capricornis crispus) in Yamagata, Honshu. Such microfilariae from serows, reported here
for the first time, had coiled posterior parts and measurements { 130‑160 (mean, 140) pm long and 4‑6 (5)pm wide} close to those from cattle. The findings showed that the Olechocerca sp. in cattle in Kyushu is O.

suzukii, a transfuge parasite from the Japanese endemic bovid, C. crispus.
Key words: Filarioidea, Japanese serows, cattle, onchocerciasis

INTRODUCTION

simuliids, and infective Onchocerca larvae were obtainedthat corresponded to one of the three kinds of infective

After the detect‑ion in Oita of a zoonotic onchocer‑
cal nodule from a young girl in 1987, reported by Beaver
et al. (1989) and Hashimoto et al. (1990), a survey oflarvae that have been found in natural infections

Onchocerca species in cattle and of their vectors was1990). If the species from cattle is Cercopithlfilaria, thedone in Kyushu (Takaoka et al., 1989; Takaoka andvector may be ticks. As does the microfilaria, thisBain, 1990; Takaoka, 1990). In skin snips from cattle,
the microfilariae of two ubiquitous species, O. Iienalis

acteristics, including a long, thick body. These findings(Stiles, 1892) and O. gutturosa Neumann, 1910, wereidentified and a third Olechocerca species, unknown
elsewhere, was recovered only in microfilarial form.
The unusual shape of these microfilariae (helicoidal
posterior region and flattened body) suggested that they
belonged to the genus Cercopithlfilaria Eberhard, 1980
(Takaoka and Bain, 1990) .
The microfilariae were injected into the thorax of

1

2
3

4
5

6

(Takaoka, 1990) ; the two others were already identified

as O. Iienalis and O. gutturosa (Takaoka and Bain,

Onchocerca sp. in the infective stage has primitive char‑suggested that the parasite belonged to a primitive
endemic species of Onchocerca.
The geographical isolation and morphological char‑acteristics of the Onchocerca sp. from Oita suggested
that its original host was the relict bovid, Capricornis
crispus, Rupicaprinae, endemic in Japan, with herds in

Mt. Sobo (1,758 m) , Kyushu. Two unnamed Onchocerca
species have been found in Japanese serows by Suzuki etDepartment of Medical Zoology, Osaka City University Medical School, 1‑4‑54 Asahimachi, Abeno‑ku, Osaka 545‑8585, Japan
Laboratory of Veterinary Anatomy, Faculty of Agriculture, Gifu University, Gifu 501‑1193, Japan
Japan Wildlife Research Center, Tokyo 113‑0034, Japan
Animal Husbandry Research Center, Yamagata‑ken Agricultural Co‑op, Yamagata 990‑0894, Japan
Department of Infectious Disease Control, Oita Medical University, Oita 879‑5593, Japan
Biologie Parasitaire, Protistologie, Helminthologie, CNRS URA 114, Mus um National d'Histoire Naturelle, 61 rue Buffon, 75231

Paris, Cedex 05, France
Corres pondence Shigehiko Uni E‑mail: uni@msic.med.osaka‑cu.ac.jp

158

al. (1982). In 1994, one of the Onchocerca species wasreported to be O. skrjabini Rukhlyadev, 1964 ( = O.
tarsicola Bain and Schulz‑Key, 1974), a common para‑of the seven serows examined. The microfilariae were148 and 156 pm long and 5 pm wide, and the posterior
part was coiled. Adult specimens of O. suzukii were
found in this one serow that had dermal microfilariae.

site of deer first found in the Caucasus mountains, andwith a palearctic distribution (Yagi et al., 1994). The
other species, O. suzukii Yagi, Bain and Shoho, 1994, hasposterior parts found from cattle in our earlier studies inbeen found only in C. crispus, and is among the On ‑Oita (Takaoka, 1990) were inspected anew, because

chocerca species with primitive characteristics. Unfortu‑

only illustrations were shown for these microfilariae
from two kinds of specirnens: skin snips and the stom‑
ach of simuliids. Measurements were not given in thenately, none of the female worms recovered had uterine
microf ilariae.

The purpose of this study is to describe microfilar‑

iae of O. suzukii from Japanese serows in the recent
parasitological surveys done in Yamagata, reexamine
our original records on the Onchocerca sp. from cattle in

Oita, Kyushu, examined in 1988‑1989, and compare themicrofilariae of O. suzukii from serows with those fromcattle in Oita.

The original records about microfilariae with coiled

text. Five microfilariae taken from skin snips were156‑181 (169) pm long and 4‑5 (4) pm wide.
The morphological characteristics of O. suzukii
microfilariae seemed to be identical to those of the
microfilariae from cattle, showing that this Onchocerca
sp. was O. suzukii. We therefore concluded that the O.

suzukii discovered in cattle in Oita was a transfuge
parasite from Japanese serows.

MATERIALS AND METHODS

Adult worms of O. suzukii were not detected incattle probably because only the carpal and tarsal

Thirty‑three Japanese serows were killed within athree‑week period in February and March 1997 on Mt.

regions of the cattle slaughtered in Oita were examined;
it is now known that adult worms reside in the subcuta‑

Zao (1,841 m) in Yamagata Prefecture, Japan, in accord‑

neous tissue of the flanks. The survey done at abattoirs
in Oita showed that parasitism of cattle by O. suzukii

ance with the conservation policies of the Agency of

Cultural Affairs, Japan. Serows were immediately
brought to Yamagata City and necropsied by the staff at

the Animal Husbandry Research Center. Subcutaneous

was common: of the 16 animals aged 5 to 10 years, eight
harbored dermal microfilariae of this species. None wasfound in 18 cattle that were 2 years old.

tissues were examined for filarial parasites, and tissues

Another case of transfuge Onchocerca species has

containing filarial parasites were stored in 2% formalinbeen described. The original host of O. skrjabini is red
deer; the species has also been found in reindeer (Bain et

in saline; Iater, microfilariae were removed from theterminal portion of the uterus of O. suzukii females
under a dissection microscope.
Separately, in 22 February 1998 seven Japaneseal., 1979). If O. suzukii has moved in the same way
between serows and cattle, such infection may become
more common in Japanese cattle in the ftiture.

serows were killed in Yamagata and examined for

Is human onchocerciasis possible with this species?

parasites at the same place. Skin snips were taken fromthese serows.

The causative species in the first case of human

RESULTS AND DISCUSSION
Adult worms of O. suzukii (10 intact male speci‑
mens and 16 intact female specimens) were found in
subcutaneous tissues of trunks of 12 (36%) of the 33
serows examined in 1997. At this time, uterine mi‑crofilariae of O. suzukii were detected in only one of the

16 females found. The microfilariae (Figs. 1‑4) were130‑160 (mean of 10 microfilariae, 140) pm long and 4‑

zoonotic onchocerciasis found in Japan resembled O.
gutturosa in its annular cuticular ridges (Beaver et al.,1989) . Another case was reported in Oita in 1996 and thecausative species was identified as O. gutturosa fromfeatures of the annular ridges (Takaoka et al., 1996). In

Oita, O. suzukii is transmitted by a blackfly species,

Simulium bidentatum, which is anthropophilic (Taka‑oka and Bain, 1990). Another kind of human zoonotic
onchocerciasis in which histological sections will notshow annular cuticular ridges (Yagi et al., 1994) may befound in areas inhabited by cattle and serows in Japan.

6 (5) pm wide. The posterior part was coiled andtapered conically. The other Onchocerca species, O.
skrjabini, was found in the carpal and tarsal regions of

ACKNOWLEDGEMENTS

13 (39%) of the serows.
Two microfilariae were found in a skin snip of one

rata, K. Kitaura, and N. Mitani of the Japan Wildlife

We thank Drs. A. Kimura, T. Nakashima, S. Hi‑l 59

Research Center, Tokyo, for their cooperation. We
thank Dr. C. Shoho for his encouragement and sugges=
tions during this study, and Ms. C. Latta for reading themanuscript. We are grateful to the Yamagata City
government far permission to study serows. This study
was supported in part by a grant (l0306020) from the
Ministry of Education, Science, Sports, and Culture,
Japan.

d'Onchocerca tarsicola Bain et Schulz‑Key, 1974 chez lerenne {1). Ann. Parasitol. Hum. Comp., 54, 263‑2652 ) Bain, O. and Schuiz‑Key, H. (1974) : Les onchocerquesde cerf europ6en: Redescription d'O. flexuosa (Wedl,
1856) et description d'O. tubi;cgensis n. sp. et O. tarsicola

n. sp. Tropenmed. Parasitol., 25, 437‑449
3 ) Beaver, P.C., Yoshimura, H., Takayasu, S., Hashimoto,H. and Little, M.D. (1989): Zoonotic Onch.ocerca in a
Japanese child. Am. J. Trop. Med. Ilyg., 40, 298‑300
4 ) Hashimoto, H., Murakami, I., Fujiwara. S., Takayasu,

S., Takaoka, H,, Uga, S., Akao, N., Kondo, K, andYoshimura. H. (1990): A human case of zoonotic on‑

REFEREN CESl ) Bain, O., Rehbinder, C. and Petit, G. (1979): Presenc.e

chocerciasis in Japan. J. Dermatol., 17, 5255sFigures l‑4 Microfilariae of Onchocerca suzukii from a Japanese serow. Arrows show
the coiled posteriar part of the microfilariae. 4, Enlarged area of Fig. 3.
Units of the scale, micrometers.

1605) Suzuki, Y., Sugimura, M., Yagi, K., Ohbayashi, M. andShoho. C. (1982): Onchocerciasis in wild Japaneseserows, Capricornis crispus. Jpn. J. Vet. Sci. 44, 823‑825

6) Takaoka, H. (1990): Development of microfilariae of
two bovine Onchocerca species in blackflies in Japan.
Jpn. J. Trop. Med. Hyg. 18, 183‑188
7) Takaoka, H. and Bain. O. (1990): Infections of black‑flies (Diptera: Simuliidae) with three types of zoonotic

Simuliidae) with larvae of Onchocerca spp., in relation
to a human zoonotic onchocerciasis in Oita, Japan. Jpn.
J. Trop. M d. Hyg., 17, 279‑284
9) Takaoka, H., Bain, O., Tajimi, S., Kashima, K., Naka‑yama, I., Korenaga, M., Aoki, C. and Otsuka, Y. (1996):
Second case of zoonotic Onchocerca infection in a resi‑
dent of Oita in Japan. Parasite, 3, 179‑182
10)Yagi, K., Bain, O. and Shoho, C. (1994): Onchocerca

Onchocerca larvae in Oita, Japan. Jpn. J. Trop. Med.

suzukii n. sp. and O. skrjabini ( = O. tarsicola) from aHyg., 18, 1‑10

relict bovid, Capricornis crispus, in Japan. Parasite, 1,8) Takaoka, H., Baba, M. and Bain, O. (1989): Naturalinfections of Simulium bidentatum (Diptera:349‑356

Jpn. J. Trop. Med. Hyg., Vol. 26, No. 3, 1998, pp. 161‑166

161

PREVALENCE OF CANINE HEART FILARIA,DIR OFILA RIA IMMITIS, I N DOGS I N

OKINAWA PREFECTURE, JAPAN, 1991‑1992
TAKAKO TOMA , ICHIRO MIYAG11, YUKO TOKUYAMA1, RYUJI AsAT02

AND JUN KUDAKA2
Received June 15, 1998/Accepted July 24, 1998

Abstract: From 1991 to 1992, the prevalence of Dirofilaria immitis was clarified in stray dogs from Okinawa,
Kume where the first survey was carried out, Miyako, and Ishigaki Isls. of Okinawa Prefecture, Japan. The
number of dogs examined was 504 in Okinawa, 13 in Kurne, 139 in Miyako and 184 in Ishigaki Isls. In theislands except Miyako Is., about 40% of adult dogs (one year or older) were determined to be infected with
D. immitis; but in Miyako Is., 8.3% of adult dogs were positive. A11 the worms recovered were D. immitis.
In Ishigaki Is., the incidence was higher than that reported by Asato et al. (1985) . However, in Miyako Is.
where young dogs were examined, the incidence was similar to that reported by Asato et al. (1985) . In Kume
Is., the incidence of D. immitis in house dogs was also examined by the presence of the microfilariae, being
25.5% in outdoor dogs reared outside and none in dogs retained indoor.
Key words: Canine filaria, Dirofilaria immitis, epidemiological survey, house dog, Japan, Okinawa, straydog

INTRODUCTION(20 pl) were collected from the heart of the dogs. The
microfilariae abbreviated as mf hereafter were collected

Surveys of dog filaria in Okinawa Prefecture werecarried out by Pennington and Phelps (1969), Suenaga

from the blood using the method of Suenaga et al.

et al. (1976) and Asato et al. (1985). Dirofilaria immitis

drawn underand Dipetalonema

vconditum were found by Pennington

The length of some mf was measured by a digital curvi‑

and Phelps (1969) and Suenaga et al. (1976). The

meter (Uchida). The number of adult worms, male andinfection rate of stray dogs with D. immitis was 0.17%

female, in the internal organs, such as the heart and thein the survey by Pennington and Phelps from 1966 topulmonary arteries of the dogs, was also counted at thesame time. The infection rate for different ages of the1967 and 50.5% in the survey (1981 to 1984) by Asato etal. In the present paper, we report the recent situation(1972) and cotinted, and the outline of the body was

microscope with 100X magnification.

of stray dogs infected with D. immitis in Okinawa,

dogs was determined for 4 islands, Okinawa (1,199
km2), Kume (59 km2), Miyako (158 km2) and Ishigaki

Miyako and Ishigaki Isls., and stray and house dogs in

Isls. (222 km2) ; the last three islands are located approx‑

Kume Is. of Okinawa Prefecture, Japan from 1991 toimately 100 km west, 300 km and 400 km southwest of
Okinawa Is., respectively. The number and age of dogs

1992.

registered in Miyako and Ishigaki Isls. in 1992 were also

MATERIALS AND METHODS
From April 1991 to June 1992, examination wasmade on infection of dog filaria among captured dogs
caged and brought to the Animal Protection Center of
Okinawa Prefecture for mercy killing by carbon diox‑
ide. The sex and age of the dogs were recorded. Bloodexamined by the records kept in the Animal Protection
Center of Okinawa Prefecture (Table 1). In Kume Is.,the infection rate of house dogs with D. immitis was also

examined in May 1991 during the rabies vaccination ofhouse dogs in Okinawa Prefecture. A drop of bloodfrom the earlobe of the dogs was taken and the presenceof mf was determined under a microscope ( x 100). In

1 Laboratory of Medical Zoology, School of Health Science, Faculty of Medicine, University of the Ryukyus, 207 Uehara, Nishihara,

Okinawa 903‑0215, Japan
2 Okinawa Prefectural Institute of Health and Environment, 2085 Ozato, Ozato, Okinawa 901‑1202, Japan162

under three years old (X2=23.3, p=0.001) , and the inci‑

Table I Number of resistered dogs in 1992

Ishigaki

Miyako<2<1317 (53 . 2)

272 (51 . 6)

112 (18 . 8)

83 (15 . 8)

1105 (17 . 6)

99 (18 . 8)

dence in dogs under three‑years old was significantly
10wer than that in three and more than three years old(X2=64.2, p<0.001). In total, 31.6% of 838 stray dogs
exarnined, being 35.9% of the males and 27.7% of thefemales, were infected.
In Ishigaki Is., the percentage of dogs under three2

100 (16 . 8)

90 (17 . 1)

years old was alrnost the same in both the registered and279 (46 . 8)

255 (48 . 4)

examined dogs, being 53.2% and 61.4%, respectively

3

80 (13 . 4)

64 (12 . 1)

4

54 (9 . 1)

65 (12 . 3)

5145 (24 . 3)

126 (23 . 9)

Total

596 (100)

527 (100)in Ishigaki and Miyako Isls.

Age(year)

3

No. (%) of dogs regrstered(Tables 1, 2). On the other hand, in Miyako Is., 51.6%of the registered dogs and 84.2% of the examined dogs
were under three‑years old, and were significantly dif‑ferent (X2=48.0, p<0.001).

Kume Is., 90% of the 70 dogs registered were examinedin 1991. The age of dogs was estimated by the degree ofteeth wearing. Statistical analysis for the difference

2 . Incidence of D. immitis adult worms from the heartand mf from the blood of stray dogs
As shown in Table 3, the incidence of stray dogs
infected with both stages of D. immitis, adult worms andbetween percentages and number of worms were mademf was 54.9% in Okinawa, 50.0% in Kume, 90.0% inby chi‑square and Fisher tests, respectively.

Miyako and 47.8% in Ishigaki Isls., with a total of
54.3%. The percentage of dogs with D. immitis adultworms of both sexes, but without the mf was 15.4% in

RESULTS

Okinawa, 25% in Kume, O% in Miyako and 18.8% in
Ishigaki Isls., with a total of 15.8%. The incidence of

1 . Incidence of stray dogs with D. immitis

As shown in Table 2, the average incidence of
puppies (1ess than one year old) and adults of one year
and older infected with D. immitis in Okinawa Is. wasdogs with mf only was 1.6% in Okinawa and 1.4% in
Ishigaki Isls.

3.6% (2/55) and 40.1% (1801449), respectively. The

3 . Body length of mf from the blood of stray dogs withincidence tended to be higher in older dogs. D. immitis
worms were detected in 36.4% of the 11 dogs in Kume Is.
In Miyako Is., 7.2% of 139 dogs and 37.5% of 184 dogs in
Ishigaki Is. were positive. The difference of incidence
was highly significant between puppies and adult dogs

and without adult worms of D. immitis
There was no significant difference in the length of

mf recovered from stray dogs with D. immitis adultworms and those without adult worms (Table 4). The
length of the mf from the dogs in three different islands,

Table 2 Incidence of D. immitis among stray dogs in 4 islands of the Ryukyu Archipelago(April 1991‑June 1992)
Number of dogs examined and infection rate (%)

Dog age(year)

Okinawa Is. Kume Is

Miyako Is.

Ishigaki Is.

Male

113 (23 . O) 240 (22 . 1)

FemaleTotal

235 (29 . 4)575 (21 . 2)

340 (26 . 2)

5 (o . o)

117 (6 . O)

55 (3 . 6)

1 (O . O)

30 (3 . 3)

12 (O . O)

34 (5 . 9)

64 (1 . 6)

98 (3 . 1)

1

164 (25 . 4)

2 (o . o)

47 (2 . 1)

45 (11 . 1)

98 (19 . 4)

160 (17 . 5)

258 (18 . 2)

2

121 (38 . O)

2 (o . o)

40 (12. 5)

56 (37 . 5) 108 (29 . 6)111(36.0)

219 (32 . 9)

164 (56 . 7)

6 (66 . 7)

22 (13 . 6)71(60.6) 158(57 O)

105 (50 . 5)263 (54 . 4)

3

95 (45 . 3)

2 (50 . O)

12 (8 . 3)

35 (68 . 6) 82 (51 . 2)

62 (43 . 5)

144 (47 . 9)4

46 (71 . 7)

2 (100)8(1Z.5)22 (45 . 5) 47 (61 . 7)

31 (54 . 8)

78 (59 . O)

23 (73 . 9)

2 (50 . O)

2 (50 . O)

41 (68 . 3)

<2
Pup py

<1
Adult

̲>3

Adult

5
Total (1‑ ; 5)Grand total

14 (64 . 3) 29 (65 . 5)

12 (75 . O)

449 (40 . 1)

10 (40 . O)

109 (8 . 3)

172 (40 . 1) 364 (38 . 7)

376 (32 . 2)

740 (35 . 4)504 (36 . 1)ll (36 . 4) 139 (7 . 2)

184(37 5) 398(35.9)440 (27 . 7)

838 (31 . 6)

163

Table 3 Incidence of D. immitis adult worms in the heart and microfilariae in the heart blood of straydogs in 4 islands of Okinawa Prefecture (April, 1991‑June, 1992)
Islands

No. of dogs

examined

Okinawa

Kume

MiyakoIshigaki

Total

504

11

139

184

838

182

4

10

69

265

100 (54 . 9) *2 (50 . o)

9 (90 . o)

33 (47 . 8)

144 (54 . 3)

28 (15 . 4) t

1 (25 . O)o (‑)

13 (18 . 8)

42 (15 . 8)

25 (13 . 7) t

1 (25 . O)O (‑)

8 (11 . 6)

34 (12 . 8)

26 (14 . 3) SO (‑)

1 (10)

14 (20 . 3)

41 (15 . 5)

3(1 .6) ｦ

O (‑)

O (‑)

1 (1 . 4)

4 (1 . 5)

No. of dogs
infected with
D. ilcemitis (A)with adults of
c71, , mf (B)with both sexes ofadults, withoutmf (Owith c t , without,

without mf (D)without c?1 , with,without mf (E)without adult,with mf (F)show the incidence of B, C. D, E and F in infected dogs (A) , respectively.

( )*‑ｦTable 4 Body length of microfilaria from the heart blood of dogs withand without adult worms of D. immitis

Locality Dogs with(Is.) Adult worm mf
Okinawa++
Kume

No. mf examined

Av. Iength (pm) ofmf (min.‑max.)

42

304 . 8 (255 . 8‑355 . O)

10287 . 8 (271 . 3‑300 . 7)23291 . 8 (263 . 5‑320 . 9)10303 . 5 (285 . 2‑325 . 5)+++

Okinawa
Ishigaki

mf: microfilarra

Kurne, Okinawa and Ishigaki Isls., was almost the samemf of D. immitis (Table 5). None of the puppies(Table 4) .

examined were infected. Likewise, all the adult dogs
reared indoor were not infected. Only adult dogs older
than 2 years and reared outdoor were infected with D.
immitis (Table 5) (X2=3.85, p<0.05).

4 . Incidence of indoor and outdoor house dogs with D.
immitis in Kume Is.
In Kume Is., 20.6% of the house dogs were positive

5 . Relationship between the age of stray dogs and the. Table 5

Incidence of house dogs with D. immitis in

Kume Is.
No, of dogs examined and incidence (%) of D. immiti

Dog age(year)

Rearing place

OutdoorIndoor7 (O . O)O (‑)

7 (O . O)

15 (O . O)

O(‑)

15 (O . O)

Puppy

<1

worms increased as the age of the dog increased (Table

6). The average number of worms detected in puppies,
adult dogs under three‑years old, and three and morethan three‑years was significantly different (F= 9.9, p <0.001) , being 2.3 0.6, 4.3i4.0 and 7.7li:7.8, respectively.

Adult
1

Total

number of adult worms of D. immitis
The mean age of 261 stray dogs with adult worms
was 2.9l :1.6 years. In general, the number of adult2

8 (25 . O)O (‑)

8 (25 . O)3

12 (41 . 7)

3 (O . O)

15 (33 . 3)

4

5 (60 . O)

5 (O . O)

10 (30 . O)

; 5

4 (75 . O)

4 (O . O)

8 (37 . 5)

Total (1‑ ; 5)

44 (29 . 5)

12 (O . O)

56 (23 . 2)

Grand total

51 (25 . 5)

12 (O . O)

63 (20 . 6)

The nurnber of the dogs with a single adult worm of D.

immitis was most frequent, 31.8% with one male and28.4% with one female worms (Fig. 1). The average
number of worms recovered from 261 infected dogs was
6.1 6.6; 2.9 male and 3.2 female worms (Table 6) . The

maximum number of adult worms in a dog was 39, 21
male and 18 female worms (Fig. 1).

164

Table 6 Age of stray dogs and number of adult wormsof D. immitis

Dog

No. of emined Average no of adult worms of D wamltls

dogs withage

D. immitis Male Female Total min‑max(year)

<1

70

1.8

2.0

2.3 0.6
4.3 4.0
4.9i4.1
3.8i3.9

141

3.6

4.1

7.7i:7.8

1‑39

3

68

2.6

2.9

45

4.1

4.8

5

28

5.4

5.9

5.5i5.8
8.9 8.5
11.2 9.6

1‑30

4

Total

261

2 . 9 3.2
6 . I

1‑2
1

2

; 3

3

1.0

1.3

117

2.0

2.3

47

2.3

2.7

2‑3
1‑24

1‑14

Okinawa Is., Japan. The incidence of D. reconditum washigh, being 23% of 557 stray dogs' examined in Okinawa,
and microfilariae of both D. reconditum and D. immitis

were also detected in a dog from compouned Kadena
airbase of Okinawa Is. from 1966 to 1967. On the other
hand, Keegan et al. (1967) reported high incidence of D.
immitis; 44.5% in dogs from the wooded foothills outside

1‑39

Kochi City and 12.5% in urban Kochi of Sikoku, Japan.
Also in Nagasaki of western Japan, 29.1% of 690 dogs
had microfilariae of D. immitis (Suenaga et al., 1971).
Subsequently, in Okinawa Is. from 1972 to 1974, Suenaga

1‑32

et al. (1976) conducted a dog filarial survey and report‑

6 . 6 1‑39

ed that the incidence of D. reconditum in stray dogs was

1‑24

6 . Relationship between the number of female worms
in a dog with both sexes of adult worms and microfilar‑

12.1% and in house dogs 2.9%; the incidence of D.
immitis was 0.2% in stray dogs and 1.2% in house dogs.
D. reconditum was predominant in the dogs in Okinawa
at that time. The high incidence of D. reconditum fromial density

1962 to 1974 in Okinawa Is. might be due closely to the

The results are shown in Fig. 2. The number offemale worms in dogs harboring both sexes of D. im ‑mitis showed good correlation with the number of mf

introduction of U.S. army dogs, when Okinawa Prefec‑
ture was under American rule after the World War II.

per 20 pl blood. The line was indicated by Y=

situation of dog filaria in Okinawa Prefecture changed
drastically. An extensive survey carried out from 1981
to 1984 by Asato et al. (1985) showed that 67.2%, 9.1%
and 6.5% of stray adult dogs in Okinawa, Miyako, andIshigaki Isls. respectively were infected with only D.
immitis and that no D. reconditum was detected in 225

38.707X2‑1.054X+527.7 (r=0.52, p<0.001). The num‑
ber of the mf in the dogs iufected with both sexes of D.

immitis worm was increared with increasing of thenumber of female D. immitis worms in dogs.

DISCUSSION
After the World War II, Pennington and Phelps(1969) reported the first record of D. reconditum in

Ten years after the survey by Suenaga et al. (1976) , thedogs examined. After 1972 when Okinawa Prefecture
returned to Japan, many dogs with D. immitis werebrought from mainland Japan to Okinawa Prefecture.
The presence of the vector mosquitoes (Toma et al. ,1978) of D. immitis and reduction of the vector of D.
reconditum might be closely related to the present situa‑30of emalemaletion of high infection rate of D. immitis in Okinawa,
which is similar to those in other prefectures of Japan

20

1:l

:.

11 In

+1

O: tv

y = 527.7 ‑ 1.054x + 38.7X2(r= 0.52, p=0.0001)

o

' ':I

oO 1 5 10 15 20 1 5 10 15 20;*.s 20female and maleoc 9 30

,¥
'

o

o
o
o In
bv

o

r(

10

10

o oooo
o

, do

O

o

'‑1 ':

1 5 10 15 20 25 30 35 40
Number of adult worms of D. jmmftis

Figure 1 Frequency distributions of the number of adultworms of D. immitis detected in stray dogs.

oo 08 o oo

: o1

5 10 15o

8o
20

No. of female worms

Figure 2 Relationship between the number of female wormsof D. immitis in a dog and microfilarial density.

165(Keegan et al., 1967; Suenaga et al., 1971; Tanaka et al.,sewage system. In the house dogs of Hiroshima, reduc‑

1966; Ohshima et al., 1973; Uga et al., 1982).

tion of infection was also reported by Saito et al. (1995) ,The present study reveals high infection of dogs
with D. immitis in Okinawa, Kume and Ishigaki Isls. In

being 45.8% in 1972 and 18.4% in 1992. This was

Ishigaki Is, the incidence of adult dogs with D. immitis

about parasitological diseases of dog and often giving
medicine for prevention or treatment.

was 40.1%, a marked increase over the 6.5% reported
from 1981 to 1984 (Asato et al., 1985). This may bereasonably attributed to the frequent movement of
personnel and transportation of animals and materials

between Ishigaki and Okinawa Isls., and mainland
Japan. The low incidence of dogs with D. immitis in
Miyako Is., 8.3% in the present survey, was similar tothat reported by Asato et al. (1985). The incidence is
expected to be higher if older dogs were examined as theincidence has been demonstrated to increase with age ofthe dogs (Oda et al., 1995). This is the first survey inattributed to the dog owners having good knowledge

Human infection of D. immitis in subcutaneous
tissue of breast was first reported in Japan in 1964
(Nishimura et al., 1964). In Okinawa, infection of D.
repens within a subcutaneous nodule was reported byMaclean et al. (1979) and D. immitis in cheek telasub‑mucosa by Hibino et al. (1981). Up to 1986, one casewith D. repens and 55 cases with D. immitis had beenreported in Japan; 69.6% of the cases involved the lungs(Makiya et al., 1987) . From laboratory and field studies
on vector mosquitoes (Keegan et al., 1967; Intermill andonly D. immitis mf was 3.1% among 96 dogs. In ourFrederick, 1970; Suenaga et al., 1972; Suenaga, 1972a:
Suenaga and Itoh, 1973; Konishi, 1987a,b), Aedes al‑
bopictus. Culex p. pallens. Cx. quinquefasciatus and Cx.
tritaeniorhynchus have been incriminated as importantsurvey, the incidence was 0.7% for 577 dogs which did

vectors in natural infections of D. immitis in Japan. Our

not harbor the adult worms. D. reconditum and D.
repens were not detected in the dogs examined in the

study shows that about 40% of stray dogs in Okinawa
Prefecture were infected with D. immitis. As Okinawa

present survey.

Prefecture is located in the subtropical area, Cx. quin ‑Kume Is. in which a small number of stray dogs was
examined for infection. In Hyogo Prefecture, Uga et al.
(1982) reported that the incidence of stray dogs with

between Okinawa and mainland Japan. The average

quefasciatus as well as Ae. albopictus were abundant
throughout the year (Toma et al., 1978, 1982, 1990;

number of adult worms in a dog was 6.1 (2.9 males andMiyagi et al., 1992), natural transmission of D. immitis

3.2 females) with a maximum number of 39 in our
survey, compared to 18.1 worms (8.7 males and 9.4

the year even in small islands.

The number of worms in a dog was quite different

females) with a maximum number of 178 (77 male and
101 female) in Hyogo Prefecture (Uga et al., 1982).
Likewise, the frequency of 1‑10 worms and more than 10
worms detected in a dog was different between Saitama

and Okinawa. In Okinawa, 83.5% had 1‑10 worms and16.5% had 11‑40 worms, in contrast to 37.5‑51% with

1‑10 worms and 49‑62.5% with 11‑200 worms in
Saitama Prefecture (Tanaka et al., 1966; Oda et al.,1995). The number of mf correlated with that of adultto dogs by these mosquito species will occur throughout

ACKNOWLEDGMENTS
We wish to thank Dr. Yoshio Shingaki and Dr. Eizo
Kinjo, the head and veterinarians of the Animal Protec‑

tion Center of Okinawa Prefecture for cooperation in
our study. Grateful thanks are also due to Professor
Yong Hoi Sen, Department of Zoology, University of
Malaya, for reading the manuscript.

worms of D. immitis in a dog. The number of mf
number of worms detected in this study was also smaller

than those reported by Tanaka et al. (1966). The
difference might be due to the mean age of dogs
examined in this study.
The incidence of house dogs with mf of D. immitis

was also examined in Kume Is. It is noteworthy that
only dogs reared outdoor were infected (25.5%) . Oda etal. (1995) reported that the incidence of the house dogs

with D. immitis had recently decreased in northern andsouthern parts of Nagasaki City, being 46.3% in 1968
and 8.1% in 1994, due to decrease of the breeding placesof Cx. p. pallens as a result of the spread of public

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(1985): Prevalence of helminthic infections in dogs in
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506 (in Japanese with English summary)2 ) Hibino, O., Yokoo. E., Hashimoto, K., Ohnishi, M.,
Shioda, S. and Yamashiro, M. (1981): Dirofilariasis in
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1844‑1850 (in Japanese)3 ) Intermill. R.W. and Frederick, R.M. (1970): A study ofpotential mosquito vectors of Dirofilaria immitis Leidy,
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1664 ) Keegan, H.L., Betchley, W.W., Haberkorn, T.B., Na‑kasone, A.Y., Sugiyama. H. and Warne, R.J. (1967) :Laboratory and field studies of some entomological16) Suenaga, O. (1972a) : Studies on the filarial prevalence

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albopictus (Diptera: Culicidae) as natural vectors ofDirofilaria immitis (Spirurida: Filariidae) in Miki City,

Japan. J. Med. Entomol., 26, 294‑300

among dogs and the mosquito vectors in Nagasaki City,
Western Japan. 2. On the susceptibility of four common17) Suenaga, O. (1972b): Studies on the filarial prevalence
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Western Japan. 3. On the susceptibility of Aedes al ‑6 ) Konishi, E. (1989b) : Susceptibility of Aedes albopictus

bopictus and Culex pipiens molestus to the larvae ofand Culex tritaeniorhynchus (Diptera: Culicidae) col‑Dirofilaria immitis in Nagasaki City. Trop. Med.

lected in Miki City, Japan, to Dirofilaria immitis (Spirur‑(Nagasaki) , 14, 144‑150 (in Japanese with English sum‑ida: Filariidae) . J. Med. Entomol., 26, 420‑424

mary)7 ) Maclean, J.D., Beaver, P.C. and Michalek, H. (1979):
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‑A compiled table‑. J. UOEH., 9, 233‑242 (in Japanesewith English summary)9 ) Miyagi. I., Toma, T. and Mogi, M. (1992): Biologicalcontrol of container‑breeding mosquitoes. Aedes
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Medical and Veterinary Entomology, 6, 290‑300
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infection with a subcutaneous Dirofilaria immitis.
Biken. J., 7, 1‑811) Oda, T., Suenaga, O., Zaitsu, M., Mori, A., Kurokawa,18) Suenaga, O., Itoh, T. and Nishioka, T. (1971): Studies
on the filarial prevalence among dogs and the mosquito

vectors in Nagasaki City, Western Japan. 1. On the
microfilarial prevalence among house dogs in Nagasaki
City. Trop. Med. (Nagasaki), 12, 169‑178 (in Japanesewith English summary)19) Suenaga, O., Kuniyoshi, S., Kishimoto, T., Ura, M. andOhshiro, N. (1976): A survey of canine filariasis on

Okinawa upon return of the island to Japan in 1972.
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on the heartworm and the intestinal helminth parasites
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21) Toma, T. and Miyagi, I. (1990): Seasonal changes in thehatchability of Aedes albopictus (Diptera: Culicidae)

Mine, M. and Kato, K. (1995): Studies on annual

eggs in Okinawajima. Ryukyu Archipelago, Japan. Jpn.

changes in microfilarial prevalence of Dirofilaria im ‑mitis among house dogs for 27 years in Nagasaki City,
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on canine parasites in the Tokyo area. J. Jpn. Vet. Med.
Assoc., 26, 228‑233 (in Japanese with English summary)13) Okamoto, M., Nogami, S., Shibuya, S., Inoue. I. andAsanome, K. (1995): Prevalence of Dirofilaria immitis
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asitol., 44, 325‑327

14) Pennington, N.E. and Phelps, C.A. (1969): Canine filar‑
iasis on Okinawa, Ryukyu Islands. J. Med. Ent., 6, 59‑67
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asitol., 44, 149‑153 (in Japanese with English summary)J. Sani. Zool., 41, 195‑204

22) Torna, T., Miyagi, I., Hoshino, C. and Sakumoto, B.
(1978): Notes on mosquitoes collected by light traps inNaha City. Ryukyu Univ. J. Health Sci. Med., 1, 96‑100(in Japanese with English surnmary)23) Toma, T., Sakarnoto, S. and Miyagi, I. (1982): The
seasonal appearance of Aedes albopictus in Okinawa‑
jima, the Ryukyu Archipelago, Japan. Mosquito News.
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Watanabe, Y., Yamada, T., Onishi, T. and Goto, M.
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Jpn. J. Trop. Med. Hyg., Vol. 26, No. 3, 1998, pp. 167 171

COMPARATIVE STUDIES FOR DEVELOPMENT
OF THREE DIFFERENT GEOGRAPHIC STRAINSOF SCHISTOSOMA JAPONICUM CERCARIAE IN
FIVE SUBSPECIES OF ONCOMELANIA HUPENSISYUZURU IWANAGA , KIM MU LEE2, PlNG CHIN FAN2 AND MORIYASU TsU J13
Received June 10, 1998 /Accepted July 30, 1998

Abstract: Cercarial maturation time, duration of cercarial emergence and number of cercariae released
were studied in five subspecies of laboratory‑reared Oncomelania hupensis ( Oncomelania hupensis nosophor‑a. O. h. hupensis. O. h. formosana. O. h. chiui and O. h. quadrasi) infected with three different geographic
strains of Schistosoma japonicum. O. h. nosophora. O. h. hupensis and O. h. formosana were the most suitable
host snails for the Japanese, Chinese and Taiwanese strains of S. japonicum, respectively. The cercarial
maturation time in the most suitable host snails were 8 weeks for the Taiwanese strain of S. japonicum and

10 weeks for the Japanese and Chinese strains after exposure to 5 miracidia. The duration of cercarial
emergence were 9 weeks for the Taiwanese strain, 17 weeks for the Chinese strain and 16 weeks for theJapanese strain. The duration of cercarial emergence was similar in the remaining subspecies, but thematuration time of cercariae was longer. For numbers of cercariae emergenced from snails, the mostsuitable host snails had a tendency to released more cercariae than the remaining snails.
Key words: Schistosoma japonicum. Oncomelania hupensis. Cercarial development

INTRODUCTION

japonicum and five subspecies of laboratory‑reared
Oncomelania hupensis.

Schistosomiasis japonica is an important disease in

East Asian countries. Diagnosis of the disease, espe=
cially the chronic cases, depends mainly on immuno‑

MATERIALS AND METHODS

serological methods. Therefore, a large amount of

1. Parasites and snails
In this study, the Yamanashi (Japanese) , Shanghai

antigen is needed for immuno‑serological diagnosis ofschistosomiasis japonica. To obtained a large amount(Chinese) and Changhua (Taiwanese) strains of S.

of antigen, it is necessary to establish the life cycle ofjaponicum were used. The Japanese strain was obtained
from the Yamanashi Prefectural Institute of Hygiene
and the other two strains were originated from infectedsnails collected in the endemic areas. These strains
have been maintained in the Department of Immunology

Schistosoma japonicum in the laboratory. In the labora‑
tory maintenance of S. japonicum life cycle, the cercar‑

ial maturation time, duration of cercarial emergenceand the number of cercariae are some of the indicatorsfor its success. There have been few detailed observa‑
tions on these problems and it is well known that differ‑ent geographic strains of S. japonicum show different
degrees of infectivity to Oncomelania hupensis subspecies(Hunter et al.. 1952; DeWitt, 1956; Moose and Williams,
1963; Iwanaga, 1976 a,b; Iwanaga et al.. 1979 a,b; Lo etal.. 1993) . This study was conducted to answer the above
problems using three different geographic strains of S.

1and Parasitology, Hiroshima University School of
Medicine, Japan by passing through most suitable hostsnails and Swiss albino mice.
Five subspecies of laboratory‑reared Oncomelania
hupensis (Iwanaga and Tsuji, 1972; Iwanaga, 1975) were
employed in this study. They were O. h. nosophora frorn
Yamanashi, Japan, O. h. hupensis from Shanghai, China,
O. h. quadrasi from Leyte, Philippines, O. h. formosana

Department of Immunology and Parasitology, Hiroshima University School of Medicine, Kasumi, Minamiku, Hiroshima 734‑0037, Japan.

2 Department of Parasitology, School of Medicine, National Yangming University, Taipei, Taiwan, Republic of China.
3 Department of Tropical Medicine and Parasitology, Kyorin University School of Medicine, Mitaka, Tokyo 181‑0004, Japan.

168

from Changhua, Taiwan and O. h. chiui from Alilao,
Taiwan. The snails used for the study were abult snails.

No * al sn:,ils

No . ofloO. h , nosophora

2. Maturation time of cercariae
For each strain of S. japonicum. 30 snails wereindividually exposed to five miracidia in a small vial for
18 to 20 hours. These snails were kept in inner soil‑filter

circulating tanks (Iwanaga and Tsuji, 1972) for 6 weeks,then maintained in petri dishes with a moistened filter

paper. The emergence of cercariae was determined byshedding for overnight every week for 6 to 25 weeks
after miracidial exposure. The negative snails weredissected and examined for sporocysts and cercariae
two weeks later.

O. h. hupensis

CI
.
$:I
u]

For each strain of S. japonicum, 80 to 100 snails
were individually exposed to one miracidium. Snails

nf
:d"
e

O. h . formosana,CO. h, ehiui

'l9

l :

hL'a'OO , h , qua.drasi

O . h . nosophera

CJr
' gL;

J*'+.'

nf

‑'!
Q

e

O' h' hup'Lnsis

a,I

3. Duration of cercarial emergence and the number of cercariae

sm'l

u]
Q,

lo'

C ,o

:E

U5

O,･ h . chiuiPO ' h ' Oosophora iQl

proven to be positive for mature cercariae were
examined once a week for 20 weeks by cercarial emer‑
gence test for overnight to determine the nurnber and'C ,duration of cercarial production. Snails were dissectedu,O, h ･ hupensisLand examined for sporocysts and cercariae at 24 weeks(1,after the first cercarial emergence.

,:
,U

･"
*

u,

O . h . chiui

(D$
CLl

**

o, h . quadrasi rf:' 'la
RESULTSweeks alter exposure to miracidia

1. Cercarial maturation tinre
Weekly and total numbers of infected O. hupensis

subspecies to different geographic strains of S.
japonicum are shown in Figure 1. With the Taiwanesestrain of S. japonicum, all five subspecies of O. hupensis

were susceptible. But shorter cercarial maturation timeand higher infection rates were observed in O. h. for‑mosana and O. h. chiui, e.g. 90% (18/20) of O. h.
formosana started to shed cercariae between 8 to 11
weeks and 83% (10/12) of O. h. chiui between 11 to 13
weeks.

Figure 1 Weekly and total numbers of infected Oncomelania

hupensis subspecies for different geographic
strains of Schistosoma japonicum* Total numbers of infected Oncomelania hupensis
subspecies at the end of experiments

iae were first detected from O. h. nosophora. O. h.

strain of S. japonicum . Cercariae were detected fromthe remaining snails from 10 to 15 weeks after exposure
to miracidia. 90% (18/20) of the infected snails for O.
h. nosophora was detected 10 to 15 weeks after exposure
to miracidia. O. h. nosophora had a shorter cercarial
maturation time and higher infection rate than those of

hupensis and O. h. chiui at 12, 10 and 15 weeks postex‑

the other snails.

posure, respectively. These O. hupensis released cercar‑
iae up to 20 to 22 weeks postexposure. Especially, 91%(10/11) of the infected snails for O. h. nosophora and

The maturation time of cercariae in the most suit‑able host snails for each strain of S. japonicum were 8

O. h. formosana and O. h. quadrasi were not suscep‑tible to the Chinese strain of S. japonicum. The cercar‑

82% (14/17) of the infected snails for O. h. hupensis
were obtained 12 to 17 weeks and 13 to 17 weeks after
exposure to miracidia, respectively. O. h. hupensis
showed the earliest cercarial maturation time and had
the highest infection rate.

O. h. formosana was not susceptible to the Japaneseweeks for the Taiwanese strain and 10 weeks for the
Chinese and Japanese strains. And the cercariae wereformed at the latest by 14 weeks for the Taiwanesestrain, 21 weeks for the Chinese strain and 20 weeks for
the Japanese strain after the exposure to 5 miracidia.

The Taiwanese strain had a shorter maturation timethan those of the Japanese and Chinese strains.

169

No

to 432. O. h. formosana produced more cercariae thanaf cercariae

No.of cercarlae

the others.

I 8

Taiwanese strain

t2

t

D

Q O,h.ncsopho!zloDoe o,h.hupensis

D O,h,hrmGsena

E9

:

0:
ooD
oo
oD

l O,h,chiuii

The duration of cercarial emergence from O. hupen ‑sis subspecies for the Chinese strain of S. japonicumoA o,h,quadrasi
,,Q,

'CI

a^

ao

E:

,4

[:

JL

e:

A

e

l(

experiment, respectively.
For the Japanese strain of S. japonicum , the dura‑

Chinese strainlranged from 16 to 17 weeks after the first emergence.
Seven weeks after the first emergence, 82‑91% of themean total number of cercariae had emerged from thesnails hosts. The mean total number of cercariae persnail from O. h. nosophora. O. h. hupensis and O. h.
chiui were 340, 585 and 280 cercariae at the end oftion of cercarial emergence from O. h. quadrasi wasslightly shorter than that of other subspecies, in which

the duration were 14 weeks. The mean total numbers ofooI

O. h. hupensis, 327 for O. h. chiui and 258 for O. h.
quadrasi at the end of experiment. Although the mean
total number of cercariae obtained from O. h. quadrasi
was less than those from other subspecies, 95% of themean total cercariae from O. h. quadrasi were detectedby 6 weeks after the first emergence.
All snails were dissected and examined for spor‑

HlJapanese strain
,

l
I

dr

I
I

4a

H

IA
IA
lA
lA
IA
IA
lA

cercariae per snail were 475 for O. h. nosophora, 398 foroeT'ro IA 1'5 l f,‑=weeks alter the first cercarial emer9ence

Figure 2 Weekly and total mean numbers of cercariae
obtained from Oncomelania hupensis subspecies
infected with different geographic strains of Schis ‑tosoma japonicum* Total mean numbers of cercariae obtained from On‑
comelania hupensis subspecies at the end of experi‑ments

2. Duration of cercarial emergence and the number
Weekly and total numbers of cercariae obtained
from O. hupensis subspecies infected with different
geographic strains of S. japonicum are shown in Figure
2. These snails had been infected with one miracidium
and the number of each snail examined was done with 10
infected snails expect O. h. quadrasi exposure to Ta‑
iwanese strain. The number of O. h. quadrasi was donewith one snail.

The emergence of cercariae continued for 7 to 10
weeks after the first emergence in the five subspecies ofO. hupensis for the Taiwanese strain of S. japonicum
and 79‑85% of the mean total number of cercariae persnail had emerged by 4 weeks after the first shedding.
The mean total number of cercariae per snail obtained
from each snail at the end of experiment ranged from 86

ocysts and cercariae 24 weeks after the first cerc'arial

emergence. The presence of both sporocysts and cercar‑
iae were detected in only one specimen of O. h. noso ‑phora and O. h. quadrasi with the Japanese strain (Fig.
3). The remaining subspecies contained only sporocysts(Fig. 4) .

For the duration of emergence and the numbers of
cercariae in the most suitable host snails for each strainof S. japaoicum, the Taiwanese strain produced thecercariae for 9 weeks after the first emergence, butother strains continued to produce for 16 to 17 weeks
after the first emergence. The mean total numbers of
cercariae per snail obtained from each snails at the endof experiment were 432 for the Taiwanese strain, 585 for

the Chinese strain and 475 for the Japanese strain andthey were not significantly different. In order to study
the morphological features of the cercariae, 10 cercariaeof each strain were fixed with 10% hot formalin andexamined under a light microscope. The difference insize of the cercariae was not significant among thedifferent geographic strains. Moreover, there were no
significant difference in morphological features (datanot shown) .

170

Table I Infection rates of Oncomelania hupepesis Sub‑
species to different geographic strains of Schis‑tos()ma japonicum *Strains of Schistosoma jaj;on.icum

Snail subspecies

Japanese Chinese Taiwanese‑ 8{)+

4246

2735(72 . 5)(43 . 7)(30 . 370

O.h. ;eosophor(.l,30 ‑,32

59‑68

23･

(31 . 5)(62 . 2}(30 . 8)O. h. formosana

O O . 8oO,h. chiuiooO . QO(33 . 3)

34‑38

35.57

(36 . 2)(,) :1 . 3)

O, h,. huf)ensis

Figure 3 Sporocyst (included cercariae) found in mid‑gut
region of Oncomelarda hupensis nosaph,0 1?: on 24
weeks after the first cercarial, emergence with theO, h. quadrasi

3S . 1(38, I )

o

3,5:

64‑70
(68 . 4)0‑5
(3 , 7)

Japanese strain of Schislt soma japordcum. Orig:< inalm, agnification: xl6.

* Infection rates as o, btained by exposure to 5 miracidia.

Arrow show sporocyst and arrow‑head, cercaria

The data are extrated from report8. of lwanaga (1976a, b);lwanaga and Tsuji (1982a, b); Iwanaga et al. (19S4) and lwanaga
e't al (1995).

+‑ Range %)Mean(%)
authars. This study revealed that the five sLTbspecies oflaboratoryreared O. hupensis showed different matura‑tion times of cercariae for strains of S. japanicum. In
the most suitable host snails, the maturation time of
cercariae was shorter than, that of the other snails. It issuggest that there is a correlation between infection rate

and the maturation time of cercariae in O. hupensis
subspecies with S. japonicum. Therefore, there arebasic physiologic differences among these snails. In thisFigure. 4

Sporocyst (arrow, non‑included cercariae) foundin midgut region of Opz,comelal ia hupensis for‑mosana on 24 weeks after the first cercarial emer‑
gence with the Ta,iwanese strain of Schistosoma

study, the maturation time of cercariae for the Ta‑
iwanese strain of S. japonicum in O. h, chiui was 9
weeks postexposure ta five miracidia. Our results do
not agree with those of Chiu (1967) who reported 95
days maturation time when exposed to six miracidia.
Ota (1957) and Okamoto (1963) reported that l.3･ and 18
weeks respectively, were required for the cercariae of S.
japo cicum (Japanese strain) to mature in O. h. Itoso ‑.

japo cicum. Original magnification: xl6.

phora, the most suitable host snail, In the present study,

DISCUSSION

the tl,'me was also much shorter.

Infection rates of laboratory‑reared of O. hupensis

In general, the most suitable host snails released

subspecies exposed to different geographic strains of S.

more cercariae than the remaining races. Tomimatsu

j j,o;cicum miracidia have been reported by lwanagaal (1984, 1995) (Table l). The most suitable host snails

and Takano (1949) reported that 29 to 10247 cercariaeof the Japanese strain of S. japonicum were harbored in
O. h. prosophora. In the present study, the number offor the Japanese, Chinese and Tai vanese strains af S.

cercariae harbored per snail after exposure to one

japordcum were O. h. noso/;hor(1. O. h. hupe zsi.

and O.

miracidium were 426 to 504 (meanj 475). Our results areh. formosana, respectively, as reported by the abovequite diffcrent from previous reports. This is perhaps(1976 a,b) , Iwanaga and Tsuii (1982 a,b) and lwanaga etdue to the fact that Tomimatsu and Takano (1949)

171

conducted their study under natural conditions and thenurnber of miracidia given was not known.
The duration of cercarial emergence obtained for
the Taiwanese strain of S. japonicum was found to be
shorter than those of the Japanese and Chinese strains.

On the other hand, the former strain matured more
rapidly to cercariae than the Japanese and Chinese

6 ) Iwanaga, Y. (1976b) : Observation on the susceptibility of

Oncomelania spp. to Schistosoma japonicum, Yamanashi
strain (2). Jpn. J. Parasitol 25, 69‑79

7 ) Iwanaga, Y. and Tsuji, M.(1972): Fundamental studies
on laboratory breeding of Olecomelania hupensis noso ‑phora (1). Med. J. Hiroshima University, 20, 1‑128 ) Iwanaga, Y. and Tsuji. M.(1982a) : Observation on theinfectivity of Oncomelania spp. to Schistosoma

strains. Otori el al (1952) reported that the duration ofjaponicum (5) . Med. J. Hiroshima University, 30, 787‑

cercarial emergence in O. h. nosophora with the790
9 ) Iwanaga, Y. and Tsuji, M.(1982b) : Observation on theJapanese strain was 20 weeks after the first emergence.
However, in the present study, the duration of cercarial

emergence was much shorter.
Chiu (1967), Ota (1957), Okamoto (1963) and Otori
et al (1952) kept snails in simple breeding systems (clayflower‑pot and dish with soiD after exposure to mir‑acidia. Iwanaga (1976 a,b) found that the snails kept in
the inner soil‑filter circulating tank had higher infection
rates than those in the petri dish with filter paper or thepetri dish with agar medium. Therefore, it is likely thatthe maturation times of the cercariae in O. hupensis
subspecies also differ under different breeding condi‑

tions. And it is probably due to a combination ofphysiological and biochemical differences in both snails
and parasites.

ACKNOWLEDGMENTS
We are indebted to Dr. U. Yamashita (University ofOccupational and Environmental Health) for his valu‑
able discussion and encouragements and to Dr. C. T. Lo
for critical review of this manuscript. This work waspartially supported by a grant from the US‑Japan Coo‑perative Medical Science Program.

infectivity of Oncomelania spp. to Schistosoma
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VOL．26NO．3

September1998

CONTENTS
Original Article
Ohtomo，H．and Takeuchi．T．
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