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Parasitoses

Recent State of Parasitoses in —Epidemiology for clinicians—

JMAJ 48(3): 148–154, 2005

Yoshiya SATO

Professor, University of the Ryukyus

Abstract: The recent profile of parasitic diseases in Japan has changed dramati- cally from public health problems with high community of classic soil-transmitted parasitoses (, disease, etc) to epidemics of various new types of parasitoses ( migrans, zoonotic parasitoses, imported parasitoses, opportunistic parasitoses, etc). Against this background of change are factors such as the diversification of lifestyles and dietary habits, recent changes in values including the return-to-nature movement and the pet boom, the global- ization of parasitoses due to the development of transportation, and the increase in compromised hosts reflecting the rapid increase in the number of aged citizens. These new types of parasitoses are generally characterized by fragile -parasite relationships, and disruption of these relationships tends to cause the serious manifestation of parasitoses. They also frequently present difficulties in diagnosis and treatment. As a result, we need to shift emphasis from the public health aspects of these diseases that require conventional mass control to respective clinical interventions requiring individualized care for diversified pathogeneses. Key words: Parasitoses; Host-parasite relationship; Parasitic ; Imported parasitoses

Introduction , and whipworms. It was taken for granted that almost everyone in Japan at that Japan was once called a “paradise for para- time had a roundworm . Subsequently, sites” because it was an agricultural country, parasite control associations were organized and the people ate raw . In particular, nation-wide, and their efforts dramatically re- the shortage of directly following World duced these soil-transmitted parasitoses by the War II encouraged the consumption of home latter half of the 1960s. While parasitoses have grown vegetables cultivated using human ex- been a problem in the past for over 30 years, creta, and this resulted in the wide spread of they are now reemerging as a new medical soil-transmitted parasites including roundworms, problem.

This article is a revised English version of a paper originally published in the Journal of the Japan Medical Association (Vol. 131, No. 11, 2004, pages 1715–1720).

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even utilize them for their own survival. In the Host specificity (Host spectrum) case of , for instance, infection Virulence induces strong immune responses in the host to Facultative prevent re-infection. The that invaded Adaptive evolution during initial infection, however, are not elimi- as parasites Host dependence nated by the immune responses elicited, and

Obligate parasitism the defense system only prevents subsequent re-infection that may otherwise increase the

AdvAdvancedanced host-parasitehost-parasite interactionsinteractions burden. Consequently, the defense sys- tem ensures that the host does not suffer heavy Fig. 1 Adaptive evolution of host-parasite interactions infection and may be profitable for the survival and virulence of worms of the initial infection for a period of several years. Similarly, in the case of toxo- plasmosis, the protozoa evade the host’s de- fense responses by forming cysts and fall into a This article introduces the recent state of dormant state. This mechanism is believed to parasitoses in Japan, focusing on new problems prevent the uncontrolled proliferation of the associated with them. parasite and protects host from fatal infection. A similar mechanism is also assumed in Parasites and Parasitism Trichinella infection, in which adult parasites are rapidly eliminated from the digestive tract In considering new problems of recent para- by host immune mechanisms. The early expul- sitoses in Japan, we first need a basic under- sion of adult worms reduces the output of standing of parasitism and the resulting viru- larvae parasitizing in muscle tissues. lence. Parasites are defined as that These observations suggest that host-parasite dwell in other animals (hosts), causing them relationships are maintained over a long period harm. At the same time, parasites cannot under a delicate balance in the presence of the survive without hosts. Interaction between the host’s immune responses. The problems we are parasite and the host (host-parasite relation- facing now are the emergence of new types of ship) has been established in the long process parasitoses (e.g. larval migrans) with poorly of evolution. If a certain type of parasite exerts established host-parasite interaction that are very strong pathogenicity in the host, such a strongly affected by host factors, as is the case host-parasite relationship is eliminated by natu- with opportunistic parasitoses. ral selection in the process of evolution. There- fore, well-established host-parasite relation- Recent Trends in Parasitoses in Japan ships tend to be characterized by relatively low pathogenicity, high host specificity, and strong As mentioned above, soil-transmitted para- host dependency, as shown in Fig. 1. sitoses including ascariasis and hookworm dis- On the other hand, parasitism elicits strong ease comprised the large majority of parasitoses defense responses of host against parasites. in Japan in the past. Because these classic par- However, defense responses, such as inflamma- asitoses generally reveal weak pathogenicity tion and other immune responses, are generally and high host specificity, epidemics were quickly weak in host-parasite relationships that are brought under control through changes in well established through the process of evolu- farming practices and lifestyle, as well as tion. On the other hand, it is believed that some thoroughgoing mass screening and the mass parasites evolve to evade these responses and treatment of infected patients. The only epi-

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Table 1 Parasites from Humans Reported in Okinawa (1981-2003)

Cases of Imported cases domestic origin Japanese Foreigners Protozoa Plasmodium vivax Plasmodium falciparum Entamoeba histolytica Entamoeba coli Endolimax nana Giardia lamblia Toxoplasma gondii Trichomonas vaginalis Isospora belli Acanthamoeba sp. Cryptosporidium parvum Flukes japonicum viverrini buski yokogawai nocens nihonkaiense Diphyllobothrium yonagoense Diplogonoporus grandis Sparganum mansoni Cysticercus cellulosae Raillietina celebensis Dipylidium caninum sp. Enterobius vermicularis colubriformis stercoralis Rhabditis hominis Angiostrongylus cantonensis Dirofilaria immitis Dirofilaria repens (Ͻ10 cases, ˘10 cases)

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Table 2 Types of Parasitoses and Number of Case Reports Presented at the Meetings of the Japanese Society of Clinical Parasitology Since 1990

Parasitosis No. of reports Parasitosis No. of reports Protozoan disease Teniasis (tapeworm infection) Malaria 39 16 Amebiasis 33 mansoni 12 Cryptosporidiosis 8 Hydatidosis 10 Giardiasis 7 Diplogonoporus grandis infection 9 Isosporiasis 6 cellulosae 6 Toxoplasmosis 5 saginata 5 Cyclospora infection 4 Dipylidium caninum infection 3 Acanthamebiasis 3 Nematodiasis ( infection) Leishmaniasis 2 Anisakiasis 49 Chagas disease 1 Trichomoniasis 1 Acariasis 30 Dirofilaria immitis infection 16 Trematodiasis (fluke infection) 10 Schistosomiasis 36 4 Lung fluke disease 23 8 6 Spiruroid infection 7 Fascioliasis 5 callipaeda infection 4 3 4 infection 1 Hookworm disease 2 Heterophyiasis 1 infection 4 Lancet fluke infection 1 Other 4 Each figure represents the number of reports rather than the number of cases reported. Cases of parasitoses discussed in the evaluation of diagnostic methods and treatment efficacy are not included.

demics of classic parasitoses remaining today types of parasitoses. Globalization and the de- are (alveolar hydatid disease) velopment of transportation allow unfamiliar in Hokkaido, in the South- parasitoses to move rapidly across the world. western Islands, Okinawa and Amami, and In addition, medical and social factors, such as among school children in the increase in the number of AIDS patients, urban areas of Japan. the popularization of immunosuppressive ther- Pinworm is normally non-pathogenic and apy and the aging of the population, are dis- does not cause major clinical problems. On the rupting delicately balanced host-parasite rela- other hand, Echinococcus (hydatid) is strongly tionships, resulting in manifestations of dis- pathogenic because the human being is an eases not seen before. Because these new types accidental intermediate host, in which serious of parasitoses often occur unexpectedly, we are manifestations are produced compared with having problems with their diagnosis, treat- the natural intermediate hosts. Strongyloides is ment and prevention. considered to be a parasite in the process of Table 1 shows the parasitoses recognized in parasitic adaptation. The parasites can survive Okinawa since 1981. The number of parasitoses in the environment and frequently cause inter- reported was 44 in total (11 protozoan, 9 fluke, nal autoinfection that leads to fatal infection. 9 tapeworm, and 15 nematode ). Among On the other hand, recent diversification of the 44 parasitoses, as many as 23 were consid- values including eating unusual foods, the pet ered to be imported cases and the boom, and the return-to-nature movement has probably caused in Japan were 33 parasitoses. given rise to epidemics of new, unexpected Table 2 summarizes the numbers of parasitoses

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reported at the annual meetings of the Japa- cians in mainland Japan and also because of the nese Society of Clinical Parasitology since lack of interest in parasitoses, many strongy- 1990. As seen from these data, the problem of loidiasis cases become serious without being parasitoses in Japan has shifted from the high appropriately diagnosed or treated, even though percentage of infected persons to the occur- parasitic infections can easily be diagnosed by rence of a variety of respective parasitoses. In stool examination. this respect, we must recognize that recent Roundworm infection only occurs sporadi- parasitoses in Japan are an old but new prob- cally nowadays. However, it has been pointed lem of medical importance. out that recent cases often involve aberrant migration into the biliary duct, pancreatic duct, 1. Classic parasitoses etc. Diagnosis based on ordinary egg detection Japan has been called as a “paradise of para- in stool is sometimes difficult because solitary sites” due to the large number of epidemics of infection is common in many recent cases. soil-transmitted parasitoses, but these para- sitoses decreased dramatically in and after the 2. Zoonotic parasitoses 1950s. Only remained in As mentioned above, well-established para- Okinawa, as high as 30% until the 1970s, but sitism depends on delicately balanced host- this also fell to approximately zero by the mid- parasite relationships. This notion was formerly 1980s. On the other hand, about 10 cases of understood in a simple way where human para- hydatidosis have been reported every year in sites infect only human beings. However, many Hokkaido. Although the number of cases is not cases of parasite infection in humans a cause for concern, this re- were reported in the 1950s, and the World quires attention because of its strong virulence Health Organization (WHO) and the Food and in human beings. Agriculture Organization (FAO) defined such Strongyloidiasis, which is still endemic in diseases as “parasitic zoonoses” in 1967. The the Okinawa and Amami regions, is currently original list of parasitic zoonoses included as the most remarkable among parasitoses in many as 41 parasitoses (8 protozoan, 12 fluke, Japan because of the large number of infected 10 tapeworm, and 11 nematode infections). persons in these regions. A recent survey in The number has increased since then. Okinawa revealed that prevalence of the infec- Anisakiasis is the most common parasitic tion among middle-aged and elderly inhabit- zoonosis in Japan. Over 2,000 cases are re- ants is estimated to be as high as 10%. This ported yearly associated with the popular habit parasitic disease sometimes develops into seri- of eating raw fish and shellfish. Recently, much ous, often fatal, hyperinfection in an immuno- attention has been paid to infec- compromised system. Therefore, we should tion resulting from eating raw firefly squid consider strongyloidiasis when obstinate diar- (Watasenia scintillans). While the former is rhea of unknown reason is observed in patients characterized by acute abdominal disorder, the receiving prolonged steroid therapy or those latter is mainly manifested by creeping erup- with concurrent HTLV-1 infection. Since the tion. Gnathostomiasis due to infection can persist for a long period, stron- spinigerum and sparganosis mansoni, both gyloidiasis often occurs in mainland Japan, a causing similar creeping eruption and migra- non-endemic area for strongyloidiasis, after tory localized skin swellings, have long been decades of latency among individuals migrat- known to occur due to eating raw snakehead ing from Okinawa and Amami, and World fish, frogs and snakes. A new type of gnatho- War II veterans returning from Southeast Asia. stomiasis due to G. hispidum often occurs due Because this parasite is unfamiliar to physi- to eating live loach imported from .

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Angiostrongyliasis due to Angiostrongylus exposed to parasitic infections. In addition, cantonensis, a parasite of rodents that uses the dietary habits of people have diversified as terrestrial snails (e.g. Achatina fulica) and slugs a result of economic growth, leading to the as the intermediate host, has been reported on emergence of various parasitoses transmitted occasion since 1970. More than 40 cases have from unusual foods and so-called gourmet been reported until now, about 70% of which foods. Examples include the above-mentioned are cases of infection in Okinawa. Physicians spiruroidea infection acquired from firefly squid; in mainland Japan, however, should also be gnathostomiasis, sparganosis mansoni and angio- cautious about this parasitic disease, because strongyliasis from frogs, snakes, snails and slugs the distribution of this parasite is expanding eaten for nutritional supplementation and as in mainland Japan using ordinary slugs and Chinese medicine; from frozen raw snails as intermediate hosts with an increasing bear meat; and lung fluke disease from fresh- number of cases from mainland Japan. Poten- water crab (Potamon dehaani). tial parasitic disease should be considered in For parasitoses caused by foods, we need to cases of eosinophilic encephalitis and menigo- pay great attention to the emergence of new encephalitis of unknown reason. parasitoses from foods that are not normally Toxocariasis, due to infection with the larvae consumed, and contrary to the possibility that of (roundworm of ) and well-known parasitoses may be transmitted T. cati (that of ), has been reported as rare from unexpected foods. cases in Japan. The disease mainly manifests itself through hepatomegaly and uveitis in 4. Imported parasitoses young children. Recently, there has been con- The development of transportation and the cern that the contamination of sandboxes in progress of globalization facilitate the trans- urban parks with infected and feces port of various parasitic infections to Japan may be a source of the infection in infants. from overseas. A typical example is malaria. Parasitoses of animal origin may increase The number of imported malaria cases in Japan further with the progressing pet boom. With is now estimated to be at least 100 cases every the increase in the variety of pet animals, year. Although parasitoses are essentially we may be faced with sudden outbreaks of endemic disease communicable in restricted unknown parasitoses. Many of these zoonotic areas, they will presently be able to move parasitoses are in the category of larva migrans, globally; all types of parasitoses occurring in all and generally have fragile host-parasite rela- countries in the world could potentially be tionships. The infected parasites usually remain imported into Japan. Parasitoses may be im- at the larval stage or stop development before ported in various forms; persons infected in reaching adulthood, but they repeat aberrant foreign countries may carry the disease to migration to various tissues and organs of the Japan, infected animals may also be imported body. The pathogenicity tends to be strong with as pets and cause human infection in Japan, and a strong inflammatory reaction of the host. In imported foods containing the eggs of parasites addition, diagnosis is often difficult because may be the source of infection. In all of these ordinary parasitological testing to detect eggs is cases, particular caution should be taken with not available. imported parasitoses that could take root and cause epidemics in Japan. 3. Food-borne parasitoses Many parasitoses are transmitted orally. In 5. Sexually transmitted parasitoses view of the long-established habit of eating raw The most important example of sexually foods, Japanese people are relatively highly transmitted parasitoses is trichomoniasis of

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the . Recently, a high incidence of Conclusion amoebiasis has been reported among male homosexuals. Other known types of sexually The problems of parasitoses in the past, transmitted parasitoses include cysticercosis which mainly consisted of classic parasitoses, cellulosae, strongyloidiasis, pinworm infection were generally regarded as a public health and giardiasis. issue rather than an individual disease issue because of the large number of infected per- 6. Opportunistic parasitoses sons and the relatively mild pathogenicity of The process of parasitism involves a relation- classic parasitoses. Nowadays, parasitoses are ship in which both the host and the parasite can reemerging in Japan in a completely different survive over time in the presence of a strong mode. We need to face them as diversified indi- immune response of the host. A disruption of vidual diseases that often have serious out- the host’s immunity directly leads to disruption comes. However, the most difficult problem of this relationship. In this sense, all parasitoses lies in diagnosis rather than in treatment. While with highly established relationships are more conventional parasitological tests are not appli- or less opportunistic. In toxoplasmosis, the cable for some recent parasitoses including protozoa form cysts and fall into a dormant larva migrans, the real problem lies in the fact state when the host’s defense system is acti- that many clinicians lack awareness of para- vated. This mechanism to evade uncontrolled sitoses as a current issue. It has often been proliferation of parasites does not work in reported that patients with roundworm infec- patients with AIDS, and the disease progresses tion, in which each adult female produces to an acute infection. Suppression of the host’s hundreds of thousands of eggs every day, immunity is also strongly associated with the moved from one hospital to another as an enhancement of autoinfection in strongyloi- unknown etiology without appropriate diag- diasis, as well the development of crypto- nosis using a simple stool test. As introduced in sporidiosis, isosporiasis and giardiasis into this article, we must renew our awareness of severe and overt conditions. the fact that parasitic infections still exist all In view of the popularized use of immuno- over the country and they are now presenting suppressive therapy and the increasing number many new problems that must be resolved. of aged people in Japan, we need to understand the problems of opportunistic parasitoses.

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