Xii. an Epidemiologic Survey in Shizuoka Prefecture, Honshu, Japan

Home , Kano River, Numazu, Shizuoka Prefecture

Jap. J. M. Sc.& Biol., 9, 165-177, 1956

PARASITOLOGICAL STUDIES IN THE FAR EAST

XII. AN EPIDEMIOLOGIC SURVEY IN SHIZUOKA PREFECTURE, HONSHU, JAPAN

LAWRENCE S. RITCHIE, GEORGE W. HUNTER III1), ROBERT E. FREYTAG, CHIATUNG PAN, MUNEO YOKOGAWA2) AND SUNG SHENG LIN With the Technical Assistance of MITSUAKI SHIMIZU, YOSHIMASA HISHINUMA, SOICHI ASAKURA

AND CARROL B. KNOX

Department of Medical Zoology, 406th Medical General

Laboratory APO 343, San Francisco, California

and

The National Institute of Health, Tokyo, Japan

(Received: July 16th, 1956)

A parasitologic survey of human parasitic infections was made in Shizuoka Prefecture, Japan, during August and September, 1950 (Ritchie et al., 1951a). The objectives included a determination of (i) the incidence of infections, (ii) helminth densities,(iii) factors predisposing infections,(iv) the status of schistosomiasis,(v) status of paragonimiasis and filariasis, and (vi) the efficiency of the intradermal test for the diagnosis of paragonimiasis.

METHODS

Single-stool examinations were made on 2278 persons in 22 communities of Shizu- oka Prefecture. Survey centers were selected independently of knowledge regarding the status of parasitic infections, with the exception of schistosomiasis, paragonimiasis and filariasis. For these three, localized occurrence necessitated making selections on the basis of a priori knowledge of distribution. All specimens were examined by means of both the 406th MGL (formalin-ether) and the AMS III concentration technics, the latter being especially effective for eggs of Schistosoma japonicum and Paragonimus westermani. Further information on occurrence of schistosomiasis was obtained by intradermal tests on 470 additional persons. Sputum concentrates were examined for a group with a history of paragonimiasis. Scotch tape swabs were taken on 427 children included in the survey to detect pinworm infections. Blood specimens from 350 persons in a suspected filaria-

1) Col., USA (Ret .). Present address: 109 Bryker Drive, San Antonio, Texas 2) Present address: Institute of Para ,sitology, Chiba University, Chiba, Japan

165 166 RITCHIE et at Vol. 9 1956 PARASITOLOGICAL STUDIES, XII 167 sis area were examined by the Knott concentration method for microfilariae. Details of these technics and procedures have been reported previously (Tigertt et al., 1952).

PHYSICAL AND BIOLOGIC CONDITIONS

Description of localities surveyed: Shizuoka Prefecture is located on the Pacific Coast of Central Honshu, about 100 miles southwest of Tokyo. It is bounded on the north by Yamanashi Prefecture, where one of our surveys was made, and on the south by Suruga Bay. Sparcely populated mountainous areas (including part of Mt. Fuji) predominate, but coastal areas and several broad inland valleys support dense populations. One of the major paragonimiasis centers of Japan is located to the east of Numazu along the Kano River. The principal schistosomiasis center is a mile-wide rectangular area extending westward from Numazu for a distance of about 10 miles. It is bounded on the south by the shoreline Tokaido highway and railroad, and to the north by a parallel country road. A suspected filariasis center is located in a valley extending inland from Yoshiwara at the western end of the schistosomiasis area (See Fig. 1). Most of the population centers selected were rural, but some were at the perimeter of urban centers and consequently included other than farmers; one was a fishing center (Ganyudo) and another a business section of Numazu (Ote Machi). Conditions of living : Though typical of Japan, living conditions reflected an above-average economic status. This was linked with industrial pursuits, and the fruit and tea crops for which Shizuoka is noted. Rural dwellings, which were concentrated in villages, included the thatch- or tile-roofed house, stable, compost shed and storage structures, all arranged around a central dooryard. Houses were commonly neat and clean, although some were untidy and had a sour smell with uneaten food and dirty dishes in evidence. Kitchens usually had a dirt floor while the rest of the house had typical straw mats placed over wooden floors. Pumps were in general use, being associated about equally with driven and dug wells ; the latter were commonly sealed. Springs supplied household re- servoirs at Hita and Kanaoka, and tap water was in common usage in Izumi, Harada and Numazu. Where accessible, flowing streams were used for washing clothes, vegetables and sometimes dishes. Crops and livestock : Extent of rice culture varied from 30 to 90% in different areas. Tea and vegetables predominated in the foot hills. Except in strictly urban sections, most homes had dooryard gardens fertilized by night soil. There was an average of one cow or horse per dwelling, actual numbers varying according to available grass on untilled foothills or river levees. Two villages reported a considerable number of pigs, which were penned, and most families kept a few chickens. Fertilizers : Livestock was sufficient to furnish considerable manure, which 168 RITCHIE et at Vol. 9

with refuse and straw was composted. Commonly, a portion of available night soil was added to the compost piles. Chemical fertilizers were used in varying amounts in different villages. About 60 families were interrogated regarding the processing and use of night soil. The amount processed by composting varied from 0 to 80% by family and the extent of this practice varied consider- ably in different communities. Otherwise the liquid night soil was stored for a varying time, rarely exceeding one month, in open cement tanks constructed in the ground. Composted materials were applied on dry fields, paddy fields, and gardens. Liquid night soil was limited to dry fields and gardens, being used only occasionally for wet rice culture. Night soil was not utilized in any form for cultivation of tea or sweet potatoes, thus excluding two likely avenues of hookworm transmission. Whereas farmers were said to apply some chemical fertilizer on vegetables, dooryard gardens of non-farming families were usually fertilized directly from household toilets. Only about one-third of the , farm families interrogated reported direct applications of toilet receptacle contents to gardens. There was no consistent design in the processing and use of night soil that suggested a deliberate plan to suppress transmission of helminths; rather, the practices appeared to be agricultural expediencies.

RESULTS AND DISCUSSION

Occurrence of intestinal parasites for the entire survey (Table 1): One or more parasites were diagnosed for 93.6% of all persons examined; 91.8% harbored helminths and 33.5% were found to be infected with one or more intestinal protozoa. Total numbers of helminth and protozoan infections identified constituted an average of 1.9 and 0.45 infections, respectively, for each person examined. This is quite in contrast to adjoining Yamanashi Prefecture where corresponding averages were 3.4 and 0.85 (Hunter et al., 1951a). There were four examinees who harbored seven different parasites ; 31 had six species, 93 had five and 274 had four. Ascaris lumbricoides was the most common parasite, for which the overall prevalent rate was 79.9 %. The prevalent rate of other common helminths was Trichuris trichiura 58.3%, hookworm 27.4%, Trichostrongylus sp. 8.7% and . Enterobius vermicularis 56.4% (by Scotch tape swabs on children). No infections of Strong yloides stercoralis were encountered; this parasite is encountered only infrequently in Japan. For the entire survey the prevalent rate of S. japonicum and P. westermani was 1.8 and 1.9 % respectively, and Clonorchis sinensis and Metagonimus yokogawai each occurred to the extent of about 1 %. Only four tapeworm infections were found, two each of Hymenolepis nana and H. diminuta. Echinostome eggs were recovered from two persons and Fasciola hepatica from one. Heterophyid-like eggs were noted in 36 persons (1.6%). In general the helminthic infections were lower than for the Kof u Valley in. 1956 PARASITOLOGICAL STUDIES, XII 169 adjacent Yamanashi Prefecture (Hunter et al., 1951a). Endamoeba histolytica was found in only 4.4% of the persons examined. For the other protozoa the figures were E. coli 22.6%, Endolimax nana 13.6%, Iodamoeba butschlii 0.6%, Giardia lamblia 4.1% and Chilomastix mesnili 0.2%.

Table 1. Summary of intestinal parasites in Shizuoka Prefecture

* No. positive/No. examined by scotch tape swab

Frequency of the intestinal protozoa was only about one-half that for Yamanashi Prefecture. Comparison of parasitism in the various communities surveyed (Table 2): Parasitosis by community ranged from 87 to 99%. Considering only the helminths, the corresponding figures were 83 and 99 %. The occurrence of one or more protozoa ranged from 20 to 48%. The ascaris infection rate varied from 61 to 93%; whipworm from 34 to 85% and hookworm from 4 to 55%. In one community no infections of Trichostrongylus infections were found, in contrast to 26% which occurred in the largest urban center (Numazu). On the basis of small numbers of cases, the infection rate of pinworm was as high 170 RITCHIE et al Vol. 9

Table 2. Prevalent rate of intestinal parasites by community

* No . positive/No. examined by scotch tape swab

Table 2 (Continued).

* No . positive/No. examined by scotch tape swab 1956 PARASITOLOGICAL STUDIES, XII 171

Table 2 (Continued).

* No . positive/No. examined by scotch tape swab

Table 2 (Continued).

* No. positive/No. examined by scotch tape swab 172 RITCHIE et al Vol. 9 as 89 %. Maximum rates of M. yokogawai and C. sinensis were 8 and 5% respectively. E. histolytica was limited to 1 % in three communities and 5 % or less in 14 of the 22 population centers surveyed. The highest prevalent rate encountered was 9%, which occurred in two villages. Endamoeba coli varied from 11 to 32%, E. nana from 3 to 30% and Giardia did not exceed 9%. Kitaema was the

Table 3. Parasite density index (PDI) by community for ascaris, whipworm and hookworm

* Parasite Density Index is based only on positive cases.•¬

High factor due to one of the four cases. community with lowest protozoan infections : E. histolytica 0.8%, E. coli 12.7%, E. nana 3.2%, G. lamblia 6.3%, I. butschlii 0.0% and C. mesnili 0.0%. Severity of helminthic infections (Table 3): The parasite density indices were calculated on the basis of egg counts obtained with the concentration technics (Tigertt et al., 1952). Numerical indices, based on eggs per microscopic prepa- ration, were established by community for the more prevalent helminths. For comparison of such groups this procedure is deemed indicative of infection in- tensities (Hunter et al., 1951b). The ascaris density index for the entire survey was 190, which is relatively high when compared with our other surveys in 1956 PARASITOLOGICAL STUDIES, XII 173

Japan. This figure varied from 60 (Takaoka) to 261 (Hita). Such a contrast is believed to indicate that epidemiologic factors were fundamentally different in these two villages. Of all the ascaris infections, it was calculated that 13% may have constituted heavy infections (50 or more worms). The density index of 73 for whipworm was also relatively high as compared with other areas of Japan. It was calculated that 19% of the infections may have involved ten or more worms, but that only 3 % had as many as 30 worms. For hookworm, the density index was 68, and of the 625 infections, 47 or 8% had egg counts of the 4 and 5 plus categories. Severe infections were obviously rare and pro- bably non-existent, while infections accounting for any break in body compensation of blood loss constituted a low percentage. Status of schistosomiasis in Shizuoka Prefecture (Tables 2 and 4): Wright et al.(1947) described the endemic center of schistosomiasis in the Numazu area of Shizuoka Prefecture as follows :"... a low-lying section comprising about 10 square miles and extending from a mile to the east of the town of Numazu westward as far as Yoshiwara. It is bounded on the north by the back road between these two towns and on the south by the main road (Tokaido Highway) and the railroad (Tokaido Main Line) which follows the shore line of Suruga Bay." These authors examined children 11-13 years old in one

Table 4. Results of intradermal tests for schistosomiasis correlated with age and sex

* Exclusive of Yoshiwara village (Sudo) and their survey of snails was also limited to this village. They found 14 of 155 children to be positive, a positive rate of 9.0%, as compared to 5.0 % for our survey of the general population at Sudo. Among a collection of 315 snails they found 2, or 0.63%, infected. In the current investigation stool examinations were made in 14 communities of the above described schistosomiasis area ; 470 individuals were skin tested with a saline-extracted adult worm antigen ; and a systematic search for snails was made over a large portion of the area. Infections of S. japonicum were found by stool examination in six communities with the following prevalent rate : 174 RITCHIE et al Vol. 9

Katahama and Hara, 1%; Motoyoshiwara, 3.8%; Sudo, 5%; Ukishima, 3%; and Kanaoka, 26.0% (Table 2). In sections of the latter three villages, skin tests were made on additional persons with the following frequency of positive reaction : Sudo, 55%; Ukishima, 43%; and Kanaoka, 33%. In a fourth village (Ashitaka), where no stooj positives were found, 14% were positive by skin test (Table 4). Although stool and skin tests were not made on the same persons, proximity of the various village sections to each other and to the snail habitat warrants the conjecture that occurrence of infection was, in general, consider- ably higher than revealed by a single-stool examination. In an area of low endemicity, such as Shizuoka, a single-stool examination might be expected to be relatively less effective than skin tests, due to light and infrequent exposure, combined with probable persistence of a skin reaction after eggs cease to be discharged. Correlation of infection with age, as based on skin test, gave an infection rate of 12% for the age groups of 1-15 years, 34% for the 16-30 year group and 60% for all persons over 30 years of age. This is in contrast to highly endemic centers where children of 10-15 years are as frequently infected as adults. In addition to the fact of low endemicity in the Shizuoka area, the dwellings were primarily located outside the limits of the snail habitat, which would tend to delay exposure for children. Indeed the low prevalent rate among the children may reflect a recent decline in the exposure hazard for the Shizuoka center, as was suggested by Wright et al.(1947). Correlation of infection with sex showed that the prevalent rate for males was twice that of females. A careful six-day search for Oncomelania nosophora by a team of five members revealed only two snail foci, one near each end of the endemic area at Kanaoka and Sudo (Fig. 1). The entire collection included a total of 594 snails, of which none were infected. At Sudo they were limited to a few colonies in marshy areas at some distance from dwellings, while at Kanaoka they were found in irrigation ditches, some of which were near dwellings. The snails were limited to a few ditches at Kanaoka and did not extend into the northern perimeter of Numazu City, where they were reported to have occurred in years past. Accumulated data (Tables 2 and 4 ; and Fig. 1) indicate that Numazu City approximates the eastern limit of the schisto,somiasis area. The western limit appears to be in the vicinity of Sudo and Motoyoshiwara, possibly delineated by the Akabuchi River. No snails were found west of this line, and human infections were not recognized by stool examination ; furthermore no positive skin reactions were obtained among 121 school children in an additional survey center selected on the adjacent (eastern) edge of Yoshiwara. Apparently the endemic area terminates short of Yoshiwara by several miles. Schistosomiasis in Shizuoka appears to have decreased as a result of swamp reclamation with snails reduced to the two small foci at Sudo and Kanaoka. This is in contrast to endemic areas of Kofu Valley and Kyushu where snails have survived under tillage by inhabiting irrigation channels, but is similar to the 1956 PARASITOLOGICAL STUDIES, XII 175 situation along the Tone River (Ritchie et al., 1953). Although the occurrence of infections in Shizuoka, as revealed by skin test, is still high, particularly in age groups over 15 years, egg passers are apparently infrequent. It is possible that within a period of a generation schistosomiasis may essentially disappear in this endemic center. Status of paragonimiasis in Shizuoka : Three villages were selected for survey in the known endemic center of paragonimiasis along the Kano River. Stool examinations were made by means of the AMS III technic, which has been shown to give results comparable to sodium hydroxide sputum concentrates (Komiya and Yokogawa, 1953). The prevalent rate of paragonimiasis at Tsuka- moto, Hita and Kitaema was 12.5, 16.3 and 4.0% respectively. These results are similar to the findings of Komiya, Yokogawa et al.(1952) who carried out a more comprehensive epidemiologic study of paragonimiasis in the Kano area. For village,s outside the Kano endemic center, infections were mostly limited to the villages of Sudo (5%) and Ukishima (3%), which are adjacent and may constitute a minor endemic point. An evaluation of the intradermal test for the diagnosis of P. westermani was made using a saline-extracted adult worm antigen. The results have been reported in abstract (Ritchie et al., 1951b) and a detailed report will appear separately. Status o f filariasis in Shizuoka Prefecture : Although the Japanese literature (Ishii, 1946) contains comments on the existence of filariasis in the general area of Yoshiwara, where collections from 6 communities were made, no microfilariae were found among blood specimens from 350 people. Histories and physical examinations were slightly suggestive that filariasis might exist in certain of the communities surveyed. Reportedly, manifestations of the disease were greater in years past. If filariasis does exist where specimens were taken, the endemicity is presently of a very low level, and certainly is of no public health concern.

SUMMARY

A survey of parasitic infections was made in 22 population centers of Shizu- oka Prefecture, Japan, with special attention given to the status of paragonimiasis, schistosomiasis and filariasis. Single-stool examinations were made for 2278 persons, of which 93.6% had intestinal parasites; 91.8% harbored helminths and 33.5% had protozoa. Common helminths included: A. lumbricoides 79.9%, T. trichiura 58.3%, hookworm 27.4%, Trichostrongylus sp. 8.7% and E. vermicularis (by Scotch tape) 56.4% of 427 children. The prevalent rate of Clonorchis sinensis and Metagonimus yokogawai was about 1%, but in one village 7.7% were infected with M. yokogawai. Intestinal protozoa occurred as follows: E. histolytica 4.4%, E. coli 22.6%, E. nana 13.6%, Giardia 4.1% and I. butschlii 0.6%. The highest prevalent rate 176 RITCHIE et al Vol. 9 of E. histolytica by community was 9%, while it was only 1% in three rural centers and 5% or less in 14 of 22 places. Helminth density indices, based on stool concentrate egg-counts, were deter- mined for comparison with other surveys in Japan. For ascaris and whipworm, the density indices were relatively high. Severe hookworm infections were rare, and cases with blood loss in excess of body compensation were infrequent. The occurrence of schistosomiasis exceeded 5% in only one village (Kanaoka), where 26% of the people were positive by the AMS III stool examination. Intradermal tests revealed that much larger portions of the general population had experienced this infection at sometime; as high as 55% gave a positive reaction in one population center. Maximum infection occurred in the age group of 30 years and over, and males were about twice as frequently infected as females. These two observations are in contrast to findings for highly endemic centers. The overall prevalent rate of paragonimiasis by stool examination was only 1.9%, but figures of 12.5 and 16.3% were found in two villages. One of the major endemic centers of this disease in Japan occurs to the east of Numazu City, along the Kano River. No microfilariae were recovered from 350 blood specimens examined by the Knott concentration technic in a reported endemic center of filariasis.

REFERENCES

Hunter, G. W. III, Ritchie, L. S., Kaufman, E. H., Pan, C., Yokogawa, M., Ishii, N., and Szewczak, J. T.(1951a): Parasitological studies in the Far East. IV. An epidemiologic survey in Yamanashi Prefecture, Honshu, Japan. Jap. M. J., 4, 113-124. Hunter, G. W. III, Ritchie, L. S., Pan, C. and Lin, S.(1951b): Parasitological studies in the Far East. XI. An epidemiologic survey of Okinawa, Ryukyu Islands. Japan Logistical Command Bull. No. 3, pp. 29.

Ishii, N.(1946): In •gModern Tropical Medicine•h by Y. Miyagawa, pp. 977, Nanzando

Book Co., Ltd, Tokyo. Komiya, Y. and Yokogawa, M.(1953): The recovering of Paragonimus eggs from stools of paragonimiasis patients by AMS III centrifuging technic. Jap. J. M. Sc. & Biol., 6, 207-211. Komiya, Y., Yokogawa, M., Chichijo, K., Nishimiya, H., Suguro, T. and Yamaoka, K. (1952): Studies on paragonimiasis in Shizuoka Prefecture I. An epidemiologic survey of Paragonimus westermani along the banks of the Kano River. Jap. J. M. Sc. & Biol., 5, 341-350. Ritchie, L. S., Hunter, G. W. III, Freytag, R. E., Pan, C. and Yokogawa, M.(1951a): An epidemiologic survey of Shizuoka Prefecture, Japan. J. Parasiotol. (Suppl.), 37, 17-18. Ritchie, L. S., Hunter, G. W. III, Nagano, K., and Pan, C.(1953): The distribution of the snail Oncomelania nosophora, intermediate host of Sehistosoma japonicum, along the Tone River, Japan. Am. J. Trop. Med. & Hyg., 2, 915-925. Ritchie, L. S., Hunter, G. W. III, Pan, C. and Yokogawa, M.(1951b): Skin-tests for paragonimiasis with antigen from adult worms of Paragonimus westermani. J. Parasitol. (Suppl.), 37, 28. 1956 PARASITOLOGICAL STUDIES, XII 177

Tigertt, W. D., Hunter, G. W. III and Ritchie, L. S. (1952): Parasitological studies in the Far East. I. Methods and review of Japanese literature. Jap. J. M. Sc. & Biol., 5, 357-385. Wright, W. H., McMullen, D. B., Bennett, H. J., Bauman, P. M. and Ingalls, J. W., Jr. (1947): The epidemiology of schistosomiasis japonica in the Philippine Islands and Japan. III. Surveys of endemic areas of schistosomiasis japonica in Japan. Am. J. Trop. Med., 27, 417-447.