PARASITOLOGICAL STUDIES IN THE EAR EAST VI. AN EPIDEMIOLOGIG SURVEY ON KYUSHU ISLAND, JAPAN1)

L. S. RITCHIE, G. W. HUNTER III ), C. PAN, M. YOKOGAWA3 ) AND J. T. SZEWCZAK*

(Received: Feb. 29th, 1952)

INTRODUCTION

A parasitological survey was made on Kyushu, southernmost island of , during the months of May and June, 1948. The island is comprised of seven prefectures, five of which were surveyed : Saga, Fu- kuoka, , Kagoshima and Oita. Actually only four distinct centers were investigated, as the contiguous portions of Saga and Fuku- oka, comprising the schistosomiasis center, were considered as one area. Others centers were located near the cities of Kumamoto, Kagoshima and Beppu. The entire island of Kyushu was considered the geographical survey unit, as was , whereas a single prefecture served this role in previous surveys of this series. In addition to the primary objective of determining the incidence of intestinal helminths and protozoa, special attention was given to the status of schistosomiasis. The distribution of the intermediate host, Oncome- lania nosophora, and its incidence of infection in both snails and man were investigated, Blood specimens were collected at two places ; subse- quently these were examined for microfilariae.

METHODS

Single stool specimens were collected from 2073 individuals, all of which were examined by both the AMS III and 406th MGL concentration

1) From the Department of Medical Zoology, 406th Medical General Labora- tory, APO 500, U.S. Army, and the Japanese National Institute of Health, , Japan. 2) Colonel, Medical Service Corps, Chief of Department. 3) National Institute of Health, Tokyo, Japan. * With the technical assistance of S. Asakura, Y. Hishinuma, M. Shimizu and F. Verre.

299 300 RITCHIE et al technics. Pen-anal swabs, by means of the Graham Scotch Tape Technic, were made on 412 children. Knott's modified survey method for detecting microfilariae was used. Details of the technics and procedures are des- cribed elsewhere (1, 2).

PHYSICAL AND CLIMATOLOGIC DATA

Description of Kyushu and Areas Surveyed.-Kyushu Island constitutes about one-tenth of the land area of Japan proper. It lies between 31•‹ and 34•‹ North Latitude, corresponding to Southern California or Georgia.

The terrain is no less mountainous than other parts of Japan, tillable areas being largely limited to the coast ; considerable coal is mined ; and heavy industries are located in the northern part. Four rural communities were studied in the Saga- area. In the survey included Kumamoto City and two rural areas. Blood specimens were drawn for the possible recovery of micro- filariae in one of the latter-the mountain village of Yamanishi-where Japanese health officials suspected the presence of filariasis. Near the southern tip of Kyushu, Kagoshima City and the rural communities of Ishiki and Kiire (Sesekushi) were investigated. At the latter only blood specimens were obtained. At Beppu (Oita Prefecture) which is located on the northeastern coast, both suburban and business districts were sur- veyed. Climatologic Data.-Rainfall is highest during the warm months, yearly precipitation ranging from about 1650 mm, in the north to 2250 mm. in the south. Mean temperatures are relatively uniform throughout the island, those of winter being only a few degrees higher in the south. Mean minimum temperatures rarely go below freezing. Winters are cloudy in the north but there is maximum sunshine in the south. Mean relative humidity is high, ranging from about 72% in the winter to 84% in summer3).

DISCUSSION OF DATA

Previous Reports by the Japanese of Intestinal Parasites in Kyushu.- These data have already been summarized in tabular form1). Japanese Government Reports (1922-1927) gave for Saga, Fukuoka, Kumamoto, Ka- goshima and Oita, respectively, the following findings : ascaris 68%, 76%, 74%, 75% and 64%; whipworm 24%, 40%, 14%, 9% and 23%; hookworm PARASITOLOGICAL STUDIES IN THE FAR EAST 301

38 0, 50%, 31%, 11% and 20%; Trichostrongylus sp. was negligible ;

Clonorchis sinensis was less than 1.0% in all cases ; Metagonimus yoko- gawai 0.3 0, 1.4 3.0 0, 0.0 o and 4.6 0 ; Paragonimus sp, was less than 1.0%, although 373 cases were reported for Kumamoto ; Schistosoma japonicum was reported as 2.2% in . Reports with authorship were based on much smaller numbers of cases, and a lower incidence of specific parasites was obtained. Information on the occurrence of intestinal protozoa is very limited. Hirayama4) reported protozoa in

225 individuals from Fukuoka as follows : Endamoeba histolytica 6.7 .

E. coli 18.7 0, Endolimax nana 36.9 o and Iodamoeba bð¹tschill 6.7%,

Takahashi et al5) reporting on 594 students and residents of Kumamoto

Prefecture, found the above organisms to occur with the following in- cidence : 0.0% , 18.4% , 13.1% and 4.5, respectively. Results of the Current Survey.-Some of these data have been previously reported6). One or more species of intestinal parasites were found in 94.2% of all persons examined. Helminths alone accounted for an in- cidence of parasitism of 92.6 0, while only 33.2% were infected with pro- tozoa (Table I). A total of 5036 separate parasitic infections were identi- fied for 2073 individuals, an average of 2.43 per person. The corresponding figures for helminths alone were 4084 infections, or 1.97 per person. In the case of the protozoa there was a total of 950 infections, an average of 0.46. The above figures are in sharp contrast to those for 7, 8) which were approximately twice the above. All parasitic infections were less common in Kyushu, especially Trichostrongylus sp. and whipworm. Ascaris lumbricoides was the helminth most commonly encountered, occurring in 74.6% of the people examined. The incidence was 92.3% for the Kagoshima area in contrast to 70.7% for Saga-Fukuoka ; 75.3% for Oita and 65.6% at Kumamoto. These figures are similar to those given above by the Japanese. The overall incidence of Trichuris trichiura was 30.4%, varying as follows for the several prefectural areas Oita 44.3%, Kagoshima 36.3%, Kumamoto 25.0% and Saga-Fukuoka 22.6%. The incidence of hookworm was 50.2%. For the several prefectural are- as, it was Saga-Fukuoka 36.9% Oita 47.8 Kumamoto 55.4% and Kagoshima 69.4% Current findings for whipworm and hookworm are well above those reported previously, except for Saga and Fukuoka. Al- though warmer temperatures and greater rainfall prevail in . Kyushu, the 302 RITCHIE et al PARASITOLOGICAL STUDIES IN THE FAR EAST 303

occurrence of hookworm was much less than in Yamanashi Prefecture7) . The incidence of Trichostrongylus sp. was only 3.2 0, which contrasted sharply with other areas in Japan where as many as 40% of those ex- amined were infected. By means of a scotch tape swab, 25.7% of 412 children were found to be positive for pinworm. The incidence of this parasite varied in the several prefectures from 21.2% in the Saga-Fuku- oka area to 35.5% at Kumamoto. In general, Metagonimus yokogawai was encountered with slightly greater frequency than C. sinensis, 4.9% and 3.3%, respectively. For the communities svrveyed in Kumamoto and Oita prefectures, this dif- ference was considerable ; the incidence of M. yokogawai being 8.2% and 7.0% and of C. sinensis, 3.1% and 2.3%, respectively. This predominance of M. yokogawai was evident from Japanese public health records listed previously, but the figures were only about one-half those reported here. Other findings included three cases of Hymenolepis nana, two of H. diminuta, five of Strongyloides stercoralis, one of Taenia sp., one of P. westermani, four of Echinochasmus peyfoliatus and three of Capillaria hepatica. Several species of heterophyid-like eggs were recovered from 42 individuals. Many of these were apparently spurious infections due to the ingestion of uneviscerated fish. Larvae of Rhabd i ti s hominis were re- covered from 25 persons.

Among the intestinal protozoa there was an overall incidence of only

5.3% for E. histolytica. The corresponding figures for other protozoa

were ,E. coli 19.9%, Endolimax nana 12.1%, lodamoeba bð¹tschlii 1.7 0,

Giardia lamblia 6.0% and Chilomastix mesnili 1.3 The highest in-

cidence for E. histolytica (11.1%) occurred in ; while

in the Saga-Fukuoka area only 1.8 % of those examined were infected.

Other protozoa were also correspondingly low in the latter area. Comparison of Parasitism by Community.-The incidence of parasitism, for the 11 population centers surveyed, ranged from 87% to 100% For helminths, exclusive of protozoa, these same figures were essentially applicable. In the case of the protozoa, only 16.8 0 of the people of Na- gatoishi were found to harbor one or more species, while at Kagoshima City, 49.3% were infected (Table II). Ascaris occurred in 95 0 or more of the people examined at Kiyama and Ishiki, while the figure was about 60% for Nagatoishi and Oshima. For whipworm there was a range from 11.7% to 65.0%. Hookworm 304 RITCHIE et al PARASITOLOGICAL STUDIES IN THE FAR EAST 305 306 RITCHIE et al

varied from 30.4% to 76.7%, exceeding 60% in two communities of and one in the northern part . Temperature apparently was not a critical factor for hookworm anywhere in Kyushu , since in Yamanashi Prefecture, where somewhat lower temperatures prevail , the incidence was higher ). Since the annual rainfall ranged from 1653 to 2244 mm., it seems unlikely that this was a determining factor . Like- wise, soil differences were not commensurate with differences of incidence; fluctuations of hookworm are most likely linked with the type of crop as well as with variations in methods of utilizing night soil . At Nagatoishi, where a baffled mull-chambered toilet receptacle was in use , the incidence was lowest. The baffled receptacle made it possible to remove well- processed night soil, exclusive of fresh accumulation ; processing by storage is known to be destructive to all eggs and cysts . At Oshima, M. yokogawai occurred in 15.5% of the people examined and is one of the highest figures obtained in Japan , being well above the overall survey figure of 4.9% for Kyushu. The incidence of E, histolytica ranged from 0.5% at Nagatoishi to 14.8% at Kagoshima City. As at Nagatoishi, all communities in the Saga- Fukuoka area had a relatively low incidence of E . histolytica and other protozoa. The construction of most of the wells in this region was un- usually good, as they were well sealed by a base and apron of cement ; also, in some cases, there was a tight cover with pump . General con- ditions of sanitation and the fly population did not afford an explanation for the lower rates of protozoan infections, as these factors were relatively uniform throughout Kyushu. Furthermore, there is reason to question whether night soil used as fertilizer is a basic factor in the transmission of protozoa in Japan ; in spite of its universal use , the occurrence of intestinal protozoa among the Japanese is in general moderate . This supports recent investigations which suggest that night soil applied to vegetables may not play an important role in the transmission of protozoa . The observations of Beaver and Deschamps9), and Rudolfs et al10) indicate that cysts of E. histolytica probably do not remain viable in the soil for more than one week. Parasitic Diseases of Special Interest.- Schistosoniasis.-This infection is limited to the vicinity of Kurume City in contiguous portions of Saga and Fukuoka prefectures. For the several communities surveyeded in this endemic center the incidence was PARASITOLOGICAL STUDIES IN THE FAR EAST 307

THE SEVERITY OF HELMINTH INFECTIONS BY PREFECTURES ON KYUSHU

* For method of determination see Tigertt , Hunter and Ritchie1). 308 RITCHIE et al

47.1%. At Nagatoishi an incidence of 72.9 % was found for Schi stosoma japonicum. This figure exceeded any obtained in Yamanashi Prefecture7) where the highest incidence by community was 65.9 At Tosu, in- cluding the settlements of Anrakuji and Takata, 60.2% were infected, and at Asahi, 29.4 At Kiyama, near the edge of the endemic area, only one of a hundred individuals was found to have schistosomiasis. The distribution of Oncomelania nosophora, snail intermediate host of S. japonicum, was intensively studied as well as the incidence of schisto- somiasis in man and these results will be published subsequently. Filariasis.-Summarizing the status of filariasis in Japan, Ishii11) referred to Kagoshima, Kumamoto, Nagasaki and Miyazaki prefectures (Kyushu) as heavily infected areas. The infection is known to be prevalent on certain small islands adjacent to the coast of Kyushu. Since these data were included in prefectural reports from Kyushu the high incidence of the parasites there may have resulted in a false impression of the extent of the disease in of the various prefectures. Nevertheless, filariasis has been reported in various communities on Kyushu for over fifty years. Nagato12) reported two cases among 81 students from Kagoshima who were in attendence at the Japanese Navy School. The communities of Yamanishi, near Kumamoto City, and Kiire (Sesekushi) near Kagoshima City, were selected as likely endemic centers of filariasis. At Yamanishi 103 persons were all negative, while at Kiire microfilariae of Wucher eria bancrofti were recovered from 21 (19.4%) of 108 individuals. Clinical manifestations suggest even a greater incidence of infection since lymphadenopathy occurred in 76.9%, in contrast to 12.5% for other areas of Kyushu furthermore, microfilariae were not recovered from the five individuals who had elephantiasis. The Severity of Heiminth Infections.-The parasite density index of ascaris for the entire survey was 158 (Table III), the maximum figure being 204 far Kagoshima Prefecture ; areas of Japan with higher ascaris indices were limited to Island13). It has been calculated that about 11% of all the ascaris cases in Kyushu were severe. The index for whipworm was 56, the range, by village, being limited between 50 and 63. On the basis of our equivalent of the Stoll Dilution Egg Count, and the estimate of Burrows14) that 120 eggs per gram of feces can be used as the unit number per worm, it has been calculated that only about 10% of those infected had more than ten whipworms. PARASITOLOGICAL STUDIES IN THE FAR EAST 309

For all areas surveyed in Kyushu the hookworm density index was

51, ranging from 39 at Saga-Fukuoka , to 64 at Kagoshima. On the basis of a correlation between hookworm egg counts and the ability of the body to compensate for blood less-Cort et al15) and Hunter et al17)-it can be safely assumed that few, if any, of the hookworm cases encountered in Kyushu were severe. The parasite density index for S. japonicum was 28, the corresponding figure in Yamanashi Prefecture being 20 7). The highest figure by village in Kyushu was 38 (Nagatoishi) in contract to 27 for Yamanashi (Sancho).

SUMMARY

An epidemiologic survey of intestinal and blood parasites was made on Kyushu, southernmost island of Japan , including areas of Saga, Fuku- oka, Kumamoto, Kagoshima and Oita prefectures . Intestinal parasites occurred in 94.2% of 2073 persons ; 92.6% harbored helminths and 33.2% had protozoa. Specific helminths included : A . lumbricoides 74.6 T. trichiura 30.4%, hookworm 50.2%, Trichostrongylus sp . 3.2%, E. vermi- cularis (by scotch tape swab) 25.7% , M. yokogawai 4.9% and C. sinensis 3.3%.

The incidence of specific protozoa was E . histolytica 5.3%, E. coli

19.9 0, E. nana 12.1%, I . bð¹tschlii 1.7%, G, lamblia 6.0% and C. mesnili

1.3%, E, histolytica ranged from 0 .5% at Nagatoishi to 14.8% at Kago- shima City.

In the endemic area of Saga and Fukuoka prefectures 47.1% of those examined were positive for Schistosoma japonicum . In Nagatoishi (Kuru- me) 72.9% were positive. Microfilariae of W. bancrofti were recovered from 19.4% of the people in a village near Kagoshima City, at the southern end of Kyushu .

REFERENCES

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4) Hirayama, S.: Statistical observations of intestinal protozoa, and their morphological and biological features. Fukuoka Ikadaigaku Zasshi. 27(4): 719-832. 1934. 5) Takahashi, S., Ueno, N. and Ishii, K.: Amebic dysentery carriers in Ku- mamoto and its vicinity. Tokyo I j i Shinshi 54 (2666) : 4-6. 1930. 6) Ritchie, L. S., Hunter, G. W. III, Pan, C., Yokogawa, M. and Szewczak, J. T.: Parasitological studies in the Far East. VI. An epidemiological survey of Kyushu Island, Japan. J. Parasit. 35 (Suppl.) : 41 (Abstract). 1949. 7) Hunter, G. W. III, Ritchie, L. S., Kaufman, E. H., Jr., Pan. C., Szewczak, J. T., Yokogawa, M. and Ishii, N.: Parasitological studies in the Far East. IV. An epidemiologic survey in Yamanashi Prefecture, , Japan. Jap. Med. Jour. 4 (2) : 113-124. 1951. 8) Hunter, G. W. III, Ritchie, L. S., Kaufman, E. H. Jr., Pan, C., Szewczak, J. T., Yokogawa, N. and Ishii, N.: Parasitological studies in the Far East. IV. An epidemiologic survey in Yamanashi Prefecture. Honshu, Japan. J. Parasit. 34 (Suppl.) : 35. (Abstract). 1948. 9) Beaver, P. C. and Deschamps, G.: The viability of E. histolytica cysts in soil. Am. J. Trop. Med. 29 (2) : 189-191. 1949. 10) Rudolfs, W., Falk, L. L. and Ragotzkie, R. A.: Contamination of vegetables grown in polluted soil. II. Field and laboratory studies on Endamoeba cysts. Sewage and Indust. Wastes 23 (4) : 478-485. 1951. 11) Ishii, N.: In : Modern Tropical Medicine, by Y. Miyagawa. Nanzando Book Co., Ltd. 977 pp. 1946. 12) Nagato, H.: Survey of microfilariae at The Navy School. Kaigun Gunikai Zasshi. 28 (10) : 726. 1939. 13) Hunter, G. W. III, Pan, C., Yokogawa, M., Ritchie, L. S. and Altamirano, M.: Parasitological studies in the Far East. IX. An epidemiologic survey on Shikoku Island, Japan. MS. 14) Burrows, R. B.: On the estimation of Trichuris worm burdens in patients. J. Parasit. 36 (3) : 227-231. 1950. 15) Cort, W. W., Stoll, N. R. and Grant, J. B.: Researches on hookworm in China. I. Problems and methods of attack. Am. J. Hyg. Mono. Series No. 7 : 1-32. 1926.