Jpn. J. Infect. Dis., 57, 2004

Laboratory and Epidemiology Communications

Changing Epidemiology of Angiostrongyliasis Cantonensis
in Okinawa Prefecture, JapanRyuji Asato*, Katsuya Taira, Masaji Nakamura, Jun Kudaka, Kiyomasa Itokazu and Masanori Kawanaka11

Okinawa Prefectural Institute of Health and Environment, Okinawa 901-1202 andDepartment of Parasitology, National Institute of Infectious Diseases, Tokyo 162-8640
Communicated by Tetsutaro Sata
(Accepted July 16, 2004)

Okinawa Prefecture experienced an outbreak of angiostrongyliasis in January of 2000 (1). The origin of the infection’soutbreak could not be identified. We examined the past recordsof Angiostrongylus cantonensis (Ac) infection outbreaks andinvestigated the current distribution of Ac’s intermediate andparatenic hosts with infective third-stage larvae in Okinawa.
In order to find the infective larvae of Ac in the giant Africansnail, Achatina fulica, the pallial organ (lung) of the snail
was compressed between two glass plates and examined
under a microscope (2) (Figs. 1A, 1B). In other host animals,
the whole body was digested in artificial gastric juice (1%pepsin/1% HCl), and the digested material was allowed tosediment; the sediment thus formed was then examined
microscopically. In particular, albino rats were given larvae
from Platydemus manokwari (Fig. 2) and Parmarion martensi(Fig. 3) orally with the specimen, and identification was madebased on the morphology of the adult Ac recovered at 59 days
post-inoculation.
As shown in Table 1, the Ac epidemic showed different
features before and after 1990. Before 1990, 17 in 21 (80%)
of the infections were traced to their infection sources, while
after 1990 only 2 in 14 could be traced to its source. The infection was more frequent (15/21) in April - November before
1990, although it was more frequent (11/14) in December -1A1B23Fig. 1A. Achatina fulica (the giant African snail), the pallial organ (lung)is shown. Scale: 1 cm.
Fig. 1B. I nfective third-stage larvae of Ac in the tissue. Scale: 100 μm.
Fig. 2. Platydemus manokwari; newly discovered paratenic host of Ac
in Okinawa. Scale: 1 cm.
Fig. 3. Parmarion martensi; newly discovered intermediate host of Ac
in Okinawa. Scale: 1 cm.

*Corresponding author: Mailing address: Okinawa Prefectural
Institute of Health and Environment, Ozato 2085, Ozato-son,
Okinawa 901-1202, Japan. Fax: +81-98-945-9366, E-mail:asatoryj@pref.okinawa.jp
184Jpn. J. Infect. Dis., 57, 2004
March after 1990.
Table 2 shows the Ac-positives among the intermediate andparatenic hosts collected in the present and in past field surveys.
In the 2000s, among six intermediate host species that werepositive in the 1970s, Satuma mercatoria, Acusta despecta,
and Bradybaena circulus became negative, and the positive

rate of A. fulica, the prevailing host, that was 39% in the 1970s
decreased to 10% in the 2000s. Meanwhile, P. martensi whose
presence was not recognized in the 1970s became prevalent
in the 2000s, particularly in the northern part of the mainlandof Okinawa, and its infection rate was as high as 20.3%. P.
manokwari, whose presence in Okinawa was noticed recently

Table 1. Epidemiologic characteristics of angiostrongyliasis cantonensis in Okinawa,
1969 - 1989 and 1990 - 2000
Characteristics

1969 - 1989 (20 years)

1990 - 2000 (10 years)

2114

Age range (mean) (y)1 - 68 (32.4)

11 - 62 (26.0)

Ratio, Male to Female

1:1.25

1:1.8

Suspected place of infection (%)
Okinawa Island
Miyako Island
Unknown

14 (66.7)
6 (28.6)
1 ( 4.8)

14 (100)0 (0.0)0 (0.0)

Suspected source of infection (%)
Eating host with the infective larva
Achatina fulica
Veronicella alte
Bufo asiaticus
Handling of Achatina fulica
Crushing with the bare hand
Handling with the bare hand
Swallowing by the play
Ingestion of a fresh vegetable
Unknown

12 (57.1)
6 (28.6)
3 (14.3)
3 (14.3)
5 (23.8)
1 ( 4.8)
3 (14.3)
1 ( 4.8)0 ( 0.0)
4 (19.0)0 ( 0.0)0 ( 0.0)0 ( 0.0)0 ( 0.0)
1 ( 0.7)
1 ( 0.7)0 ( 0.0)0 ( 0.0)
1 ( 0.7)
12 (85.7)

Occurrence time (%)
Apr.–Nov. (Active period of A. fulica)
Dec.–Mar. (Non-active period of A. fulica)
Unknown

15 (71.4)
3 (14.3)
3 (14.3)

3 (21.4)
11 (78.6)0 ( 0.0)

Human cases(Ref. 6)

Table 2. Surveys of the host animals of Angiostrongylus cantonensis infective
larvae in Okinawa, the 1970s and the 2000s
SpeciesIntermediate hosts
Terrestrial snails
Achatina fulica
Satsuma mercatoria
Acusta despecta
Bradybaena circulus
Cyclophorus turgidus
Parmarion martensi
Aquatic snail
Ampullarium sp.
Slugs
Veronicella alte
Limax valentianus
Meghimatinum confusum
Paratenic hosts
Land planarian
Platydemus manokwari
Amphibians
Bufo asiaticus
Bufo marinus
Rana catesbeiana
Rhacophorus leucomystax
Rana limnocharis

The 1970s1)
Infected/Examined (%)

The 2000s
Infected/Examined (%)

1,049/2,683 (39.1)
36/240 (15.0)
3/427 ( 0.7)
3/448 ( 0.7)**

222/2,189 (10.1)
0/139 ( 0.0)
0/904 ( 0.0)
0/53 ( 0.0)
0/529 ( 0.0)
153/753 (20.3)**

0/3,764 ( 0.0)76/347 (21.9)
9/50 (18.0)
0/24 ( 0.0)

108/783 (13.8)
3/78 ( 3.8)
0/95 ( 0.0)**

227/1,613 (14.1)

37/108 (34.0)
0/37 ( 0.0)
7/44 (15.9)
1/4 (25.0)
1/8 (12.5)

1/18 ( 5.6)
0/6 ( 0.0)****: Not examined, **: Not discovered from the field.
1): Based on references 7, 8.

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Jpn. J. Infect. Dis., 57, 2004
The present case communicated in Japanese appeared inInfectious Agents Surveillance Report (IASR), vol. 24, p.120121, 2004.

in 1993 (3), also showed a high infection rate of 14.1%.
Ac infection is mediated not only by ingestion of the Accarrier intermediate or paratenic hosts but also through theingestion of vegetables, drinking water, and by contact withfingers that are contaminated by the infective larvae of Ac(4).
In the outbreak in January 2000 in Okinawa that involved
seven patients, the clinical symptoms and immunologicalreactions were too weak for typical angiostrongyliasis andwere somewhat similar to those of infection by low dosesof Ac larvae. In the epidemic, larvae-contaminated fresh
vegetables such as lettuce and cabbage were suspected as thesource of infection. The first Ac infection case via a fresh
vegetable salad had been reported for a patient who developed symptoms 7 days after a short trip to Okinawa inDecember 1999 (5). Among the 52 Ac cases reported so farin Japan, 35 were from Okinawa Prefecture (6).
As already indicated, the peak season of infection wasdisplaced from April - November to December - March, andtracing the infection to its source has become more difficultin recent years. The displacement of the outbreak season
coincided with the decline in the infection rate in A. fulicathat is more active in April - November and the appearance of
new hosts P. martensi that is more active in the winter season,
while P. manokwari is active throughout the year. In relation
to the displacement of the outbreak season, it should be notedthat the harvest season for lettuce is November-May and thatfor cabbage is November-July.
Ac-infected P. martensi and Veronicella alte were examined histologically. Ac larvae were present in the muscularlayer just beneath the body surface of these snails. However,the former species appeared to be more easily infected
because of the less dense muscular layer and tended to containa greater number of larvae. P. manokwari is frequently
observed adhering to the lower side of cabbage leaves. It isquite possible that the larvae are released from the hosts whensliced together with the cabbage leaves in the preparation offresh salad.

REFERENCES
1. Toma, H. and Sato, Y. (2000): A mini-outbreak ofangiostrongyliasis in Okinawa. Clin. Parasitol., 11, 4043 (in Japanese).
2. Kishimoto, T. (1972): A survey of Angiostrongylus
cantonensis in Okinawa. 1. Method for determination ofA. cantonensis larvae in Achatina fulica. Rep. Okinawa
Pref. Inst. Pub. Health, 6, 117-118 (in Japanese).
3. Kawakatsu, M., Oki, I., Tamura, S., Ito, H., Nagai, Y.,
Ogura, K., Shimabukuro, S., Ichinohe, F., Katsumata, H.
and Kaneda, M. (1993): An extensive occurrence of a land
planarian, Platydemus monokwari DE BEAUCHAMP,1962, in the Ryukyu Island, Japan (Turbellaria, Tricladida,Terricola). Biol. Inl. Water, no. 8, 5-14.
4. Alicata, J. E. and Jindrak, K. (1970): Angiostrogylosis in
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6. Asato, R., Taira, K., Nakamura, M., Kudaka, J. andItokazu, K., (2002): Emerging and re-emerging infection investigation report in Okinawa: Epidemiologicalstudies on Angiostrongylus cantonebsis (1). Okinawa
Prefectural Institute of Health and Environment. p. 12(in Japanese).
7. Asato, R. and Kishimoto, T. (1976): A survey ofAngiostrongylus cantonensis in Okinawa. 6. Distribution
and positive rate of A. cantonensis in mollusks andfrogas. Rep. Okinawa Pref. Inst. Pub. Health, 9, 50-55( in Japanese).
8. Asato, R., Sato, Y. and Otsuru, M. (1978): The occurrenceof Angiostrongylus cantonensis in toads and froga in
Okinawa prefecture, Japan. Jpn. J. Parasitol., 27, 1-8.

The authors thank Prof. H. Yoshikura, Emeritus Memberof the National Institute of Infectious Diseases, for advice inpreparing this manuscript.

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