Abstract
In endemic areas of Taenia tapeworms in Korea, most of the reports showed that T. saginata was dominant over T. solium, but eating pigs is the dominant habit over eating cattle. Why do they have more T. saginata despite lower consumption of beef? This problem actually has long been recognized but until recently there has been no intensive trial to give a scientific explanation on this epidemiological enigma. By summing up the data published between the years 1963 and 1999, the ratio of armed versus unarmed tapeworms in humans was estimated at approximately 1:5. The ratio of pig-eaters versus cattle-eaters, however, was approximately 5:1. This inconsistency could be explained with the recently described T. asiatica, which infects humans through the eating of pig's viscera. We re-evaluate the importance of the consumption of visceral organ of pigs, leading us to an improved epidemiological understanding of the T. asiatica infection together with co-existing T. saginata and T. solium in Korea.
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Key words: Taenia asiatica, T. saginata, T. solium, tapeworm, taeniasis, Asian tapeworm, epidemiological inconsistency
INTRODUCTION
Taenia tapeworm, according to the definition of the World Health Organization, is 'cyclo-zoonotic parasite' transmissable between vertebrates and humans. Sprent (
1969) defined this group as 'anthropozoonotic helminths' due to the fact that humans spread the parasites as a final host. Garnham (
1958) considered it euzoonosis, because humans are indispensable in the life cycle of
Taenia tapeworms. Human taeniasis is distributed worldwide, and the beef tapeworm
T. saginata is regarded as dominant over
T. solium (
Refuerzo and Albis, 1947;
Arambulo, 1967,
1971).
Korea is also known to be
T. saginata dominant country, even though there is an apparent epidemiological inconsistency between the species ratio and the eating habits of intermediate hosts (
Eom, 1991). In areas of
Taenia tapeworm endemicity, most of the reports show that
T. saginata is dominant over
T. solium, but consumption of pigs dominates over that of cattle. Yet, why do they have more
T. saginata despite the lower consumption of cattle? Many Korean researchers recognized this inconsistency long ago (
Park and Chyu, 1963;
Kang et al., 1965a;
Lee et al., 1966;
Cho et al., 1967;
Han, 1969;
Kim, 1980,
1982;
Joo et al., 1985;
Soh et al., 1988). And the most peculiar example of all the areas with this problem was Sorokdo Island, located in the southernmost peninsula of Korea in which no cattle are reared (
Hong et al., 1983).
We approached this question with available references, covering prevalence and species distribution of Taenia tapeworms, and the eating habit of raw foods since 1915 in the most important endemic areas within Korea, to clarify the picture of inconsistency.
Recently there was a description of a third human tapeworm,
Taenia asiatica Eom et Rim 1993, a species whose possible existence had been noted since 1935 in Taiwan. This parasite was found to be infective as a larval form in the liver of Korean domestic pigs, and as adult form in the intestines of humans. With the eggs from a volunteer, pigs were infected in the visceral organs with living metacestodes, but only calcified ones were found in the liver of cattle (
Eom et al., 1992). Fan et al. (
1995) redescribed it as
T. saginata asiatica on the basis of morphological similarity to
T. saginata, and on which arguments are continuing. Unfortunately, even recent molecular biological studies show conflicting results and do not support the insistence for either species or subspecies. Some researchers argue for species level, while others for subspecies. Recently, however, support for recognition at species level is gaining, however more time is needed to accumulate further data for definitive answers.
The life cycle of the Asian tapeworm (
T. asiatica), is reported to have a striking difference in having viscerotropism instead of musculotropism (
Eom et al., 1992;
Eom and Rim, 1993).
T. asiatica is thought to be transmissable only through the liver and visceral organs, and not through the muscle of intermediate hosts; while
T. solium and
T. saginata are transmissible through pork and beef, respectively. This Asian tapeworm is thought to be distributed in many Asian countries, and it may even occur on other continents too. However, isolates of
T. asiatica from many countries require careful evaluation especially on genetic variations.
T. asiatica thus can be a clue to solve the epidemiological inconsistency between the species ratio of tapeworms and the eating habit of intermediate hosts in Korea. This problem actually has long been recognized and addressed by researchers far before T. asiatica was recognized. However, until recently there has been no attempt to give a scientific explanation for this epidemiological enigma with the use of T. asiatica.
We believe this approach could be successfully applied to address epidemiological problem, and may also be applied to other countries having the same kind of epidemiological questions about Taenia tapeworms.
EPIDEMIOLOGICAL INCONSISTENCY OF TAENIA TAPEWORM INFECTIONS IN KOREA
The epidemiological inconsistency of
Taenia tapeworm infections among Korean people could be recognized by calculating the species ratio of adult
Taenia tapeworms, and the habit of eating raw foods of the intermediate hosts. An example observed in Sorokdo Island of Southern Korea clearly showed this kind of inconsistency (
Hong et al., 1983).
Prevalences of human taeniasis since 1915 in Korea are summarized in
Table 1. There are other records not summarized in this table because of insufficient detail of description. In a report of Inoba (
1924), prevalences of
Taenia tapeworms among Koreans were quoted as 16% from author Handa, 7-8% from Mine, without description of locality or date. Probably they were small sized surveys done before 1924. Somewhat detailed prevalence data of
Taenia tapeworms among Koreans were accumulated until 1929, so it was not difficult to understand about the tapeworm status of those days. In 1930s, research almost ceased, except focal surveys started again from 1945. It was, however, not until the 1960s that more substantial surveys for parasites began. Most of the data collected in the 1960s were from local surveys, although those by Soh et al. (
1961) and Lee et al. (
1966)' were relatively large scale. In 1969, Seo et al. conducted the first nationwide parasitological survey, including most of the provinces, and thus it could be regarded as one of the most important reports after the Second World War. It was revealed that 0.7% of Koreans were positive for taeniid eggs. Carefully prepared is this survey, dealing with total 40,581 individuals including adequate sample sizes for male/female comparisons, as well as with military soldiers. The only limitation of this survey is that there was a serious bias for the 5-29 year-old age group, comprising 96% of all subjects, making it difficult to call it a real nationwide survey representing all age groups of Koreans (
Table 1). Thereafter nationwide surveys were conducted every five years, revealing taeniid egg positives of between 0.02 and 1.9%, with fluctuation varying greatly, causing difficulties in figuring out trends (
Table 1).
Morphological similarity between taeniid eggs makes it difficult to determine the species ratio between
T. solium and
T. saginata. Gravid proglottids spread eggs irregularly through the proctostoma (
Mazzotti, 1947;
Rijpstra et al., 1961), and distribute them unevenly into stools, causing a lower detection rate than real cases (
Lee, 1970;
Rim, 1980). Possible ways to make differential diagnosis are observing the number of main uterine branches, and the motility of gravid proglottids, as well as observing the hooklets on the scolex. Kang et al. (
1965a) reported that
T. saginata is more common than
T. solium, with as much as 86.9% out of 327 adult tapeworms collected from Cheju inhabitants after treatment with bithionol (
Table 2). Lee et al. (
1966) observed
T. saginata comprised 73.1% of adults among 26 taeniasis patients in Chollabuk-do; Cho et al. (
1967), 86.7% of 105; Rim et al. (
1980), 55.8% of 199 in Seoul. Chungchongbuk-do, Kyongsangnam-do and Cheju-do; Joo et al. (
1985), 73.8% of 84 in Seoul and Cheju-do; and Hong et al. (
1983), 100% of 26 of Sorokdo (Island, a leprosarium), Chollanam-do. Summarizing the data during the past 25 years makes it clear that
T. saginata is dominant by an average of 79.4% (53.3-100.0%) over
T. solium (15.4%) among Korean people, which makes the approximate ratio of 1 : 5 for
T. solium and
T. saginata (
Table 2).
Most of the reports on the metacestode surveys in intermediate hosts for
Taenia tapeworms are on the Cysticercus cellulosae in pigs in Korea (
Inoba, 1924;
Kim, 1984a,
1984b;
Kim, 1985;
Jang and Kang, 1989). On the other hand, only limited reports are available for C. bovis, the larval tapeworm of
T. saginata, from cattle. Inoba (
1924) reported prevalences of 17.8-21.3% among 731 cattle in Seoul and Kongju. Nakanishi (
1926) reported 37.6% of C. bovis positive cases in 408 Korean native calves from all over the country. Additionally, prevalences of 37.1% (56/151) were reported in Kyongju, 61.1% (22/36) in Masan, 14.6% (3/22) in Kimhae, 40.1% (8/20) in Ulsan, 40.0% (4/10) in Milyang, 0% (0/2) in Chongju, 42.9% (3/7) in Sariwon, 28.6% (2/7) in Chongdo, 100.00% (3/3) in Taegu, 40.0% (2/5) in Namhae 50.0% (2/4) in Tongnae, 0% (0/1) in Kojedo, and 34.8% (48/138) of C. bovis from areas of southern Korea. Most of the calves (62.1%), in the report, revealed light infections with under 10 metacestodes per calf; however, more than 100 were also found in some calves (2.6%), with a maximum infection of 10,462 in one calf. Infective organs were the heart, striated muscle, tongue, masseter muscle, diaphragm, lung, sub-cutaneous tissue, omentum, serosa, scrotum and stomach wall as well as a few cases from lymph nodes, esophagus, liver, kidney, pancreas, bladder, thymus, intestinal wall, testicles, epididymis, spleen, breast, uterus, ovary, spinal cord and eyes. Another paper by Isshiki (
1960) reported retrospectively 30.9% of metacestodes from cattle back to 1936, and 5.1% back to 1943 in Cheju-do. Most recently, there was at least one local episode of measled cattle in Kongkun-myon, Hoengsong-Gun, Kangwon-do in November, 1975. The inhabitant who found the measled beef could not eat it, and should have discarded it (personal communication with Dr. Seung-Yull Cho in 1990).
All these data reveal that larval T. saginata tapeworms in cattle was common in Korea.
Eating habits reveal an inconsistency with the species ratio of tapeworms
Since the 1960s, substantial epidemiological studies on
Taenia tapeworm infections were performed in Cheju-do, Chollabuk-do or other provinces; and for more than 30 years thereafter, most of the researchers repeatedly felt that the textbooks do not coincide well with the tapeworm life cycles in Korea. Most of the epidemiological studies on consumption of foods showed continual inconsistency with the species ratio of
Taenia tapeworms. Especially on the occasions of special ceremonies like weddings, funerals and meetings, the residents in rural villages used to slaughter the pigs by themselves; which is known as 'Churyum'. Eating the raw liver is the most favorite (96.7%) habit, and other organs, like the apex of the spleen, lungs, kidneys, pancreas and tongue are eaten preferably raw. In those villages, however, eating the raw beef is rare (
Park and Chyu, 1963). Cho et al. (
1967) suggested that
T. saginata infected people more frequently even though they ate the raw pork (25.6%) or the raw liver of pigs (37.2%) more frequently than eating the raw beef (15.7%) or raw liver of cattle (11.4%) among 2,104 subjects in Cheju. Kim (
1980) reported that most of the rural people with taeniasis in Cheju-do ate raw liver of pigs and cattle. Kim (
1982), in a survey on the habit of eating raw foods and parasite infections, found the majority of people (32.6%) ate the raw liver of pigs.
Summing up the ratio of pork-eaters versus beef-eaters, it was approximately 1:1 (7.1% : 6.1%) out of 12,477 individuals subjected to questionnaire surveys. Additionally, those who consume pig viscera may reach as high as 25.0% of the population in Korea. Therefore the data can be analysed as pig-eaters versus cattle-eaters, in other words, pork plus viscera eaters of pigs versus beef-eaters, (7.1 + 25.0) : 6.1 = 32.1 : 6.1 (approximately 5:1), as seen in
Table 3.
A more specific breakdown of Korean eating habits for the visceral organ of pigs, among 7,357 respondents, were: liver 24.0%, intestine 5.4%, lung 0.8% and spleen 0.7%. Of these, average 10.2% (10.1-11.4) were also liver-eaters of cattle (
Kang et al., 1965a;
Cho et al., 1967).
Between 1992 and 1995, a survey on the eating of the raw liver of pigs and cattle, covering eight provinces in South Korea, revealed that an average of 18.7% (1,349/7,211) of Koreans had experiences of eating raw liver of pigs; and 19.8% (1,425/7,211) for eating cattle liver. The report also determined that Cheju inhabitants (27.2%) eat more raw pig liver than those of any other province (
Fig. 1). Some of the pig's livers were obtained from neighbors, pubs or meat shops, but most (80%) were obtained by slaughtering pigs on their own. Twenty-two percent of subjects had experienced eating raw pig liver more than 11 times. Most of the cattle's livers, in contrast, were purchased from meat shops (42%) as well as from pubs, neighbors or department stores. The percentage of people who had experienced eating raw liver of cattle more than 11 times was 25% (
Eom, 1995).
These collective data give us a clear understanding on the inconsistency between food consumption patterns and the prevalence of T. saginata. The still unchanged habits for eating the raw liver of pigs and cattle in the 1990s Korea is noteworthy.
Enigmatic Sorokdo Island showing clear inconsistency
Obviously the most distinct puzzle, recognized by Hong et al, (
1983), was in Sorokdo Island, at a leprosarium, where there were no cattle, although many
T. saginata-like tapeworm occured among inhabitants; and only pigs were reared. Considering that the small island is isolated from the peninsula, it is difficult to understand what led the authors to speculate that the worms might be transfered from other provinces, or from land.
TAENIA ASIATICA, A CLUE TO EPIDEMIOLOGICAL UNDERSTANDING
What is Taenia asiatica?
Historically, Huang et al. (
1966) first refused to refer to the Taiwan
Taenia as
T. saginata because it didn't seem to come to human through beef, as most textbooks indicate. Consequently, Chao et al. (
1979) observed that the eggs of Taiwan
Taenia could infect the liver of pigs, but not the muscle of cattle. Consequently Chung et al. (
1987) found that wild boars and Lanyu pigs were intermediate hosts in Taiwan. Eom and Rim (
1992a,
1992b) in Korea also observed that this special tapeworm caused human taeniasis through the eating of the raw pig liver. The natural infection rate was revealed to be 1.01% in Korean domestic pigs (
Eom and Rim, 1992a). Further more, Eom et al. (
1992) observed that the Asian
Taenia metacestodes caused viscero-tropic cysticercosis experimentally in new internal organs of pigs, such as the omentum, lung and serosa, as well as in an organ already known to be infected, the liver. Eom and Rim (
1993) proposed a new species for this worm.
Taenia asiatica, with the following taxonomic evidence:
T. asiatica has a rostellum without hooklets, and this feature discriminates it from the classical
T. saginata, along with some other morphological characteristics, such as the large number of uterine twigs, and the posterior protuberance of gravid proglottids.
T. asiatica metacestodes (Cysticercus viscerotropica) also differ morphologically from
T. saginata metacestodes (C. bovis) in having wart-like formations on the external surface of the bladder wall (
Eom and Rim, 1993).
Traditionally the armed T. solium Linnaeus (1758) and the unarmed T. saginata Goeze (1782) were classified on the basis of the presence or absence of the hooklets (arm) and the rostellum on the scolex. The armed tapeworm, T. solium, has both of these structures. T. asiatica, on the other hand, looks phenotypically similar to classical T. saginata, which provoked debates on the taxonomic status at the level of species or subspecies.
Taxonomic disagreement on this tapeworm induced a redescription of Fan et al. (
1995), where it was considered as a subspecies,
T. saginata asiatica, on the basis of morphological similarities. Molecular methodologies were applied to this debate by comparing nucleotide sequences of the mitochondrial cytochrome C oxidase I (COI) and 5' 28S rDNA, and exhibited an intimate relationship of the
Taenia species or subspecies, which supported the insistence of subspecies (
Bowles and McManus, 1994;
Fan and Chung, 1998).
Classical
T. saginata infects humans through beef, and
T. solium through pork, but
T. asiatica through the viscera of pigs; in other words, the life cycles are different (
Fig. 2).
The natural infection status of
T. asiatica metacestodes (C. viscerotropica) was reported by Eom and Rim (
1992a) from the liver of pigs inspected in Chongju, Chungchongbuk-do, Korea. All pigs were six months old cross-bred pigs of Yorkshire, Landrace, Duroc or Hampshire breeds. Live metacestodes were found in only 0.01% (3/25,358) of the examined livers, and were distributed randomly in lobes of livers (
Fig. 3). The liver Livers were infected with one to ninety-six metacestodes. Most of the metacestodes, however, were either calcified (87.1%) or highly degenerated (12.9%). When metacestodes were alive, host tissue capsules were transparent. The capsule with degenerated metacestodes contained pus cells or mucopurulent fluid in the space between the thick yellowish host tissue capsule and the non-motile bladder worm.
If we postulate that Asian tapeworm metacestodes develop from eggs in 1 month, the metacestodes recognized in the liver had been infected for 1 to 5 months. In this short period of infection, all but a very few died. This is not a common feature in metacestodes of either T. solium or T. saginata, which live in the muscle of pigs or cattle for longer than a year. Even if very few T. asiatica metacestodes are alive in the liver, and the liver can still be a source of human infection. Chances of human infection should be very low, if any. This fact of rapid death of T. asiatica metacestodes in the livers of the pigs raises the question that there may be other tissues where T. asiatica metacestodes maintain patent infection for a longer period.
Experimental infections in a human volunteer, pigs and cattle
The infectivity of metacestodes of
T. asiatica in human hosts was confirmed in a volunteer (
Eom and Rim, 1992b). The metacestodes used in the experimental infection were collected from the livers of naturally infected domestic pigs at an abattoir in Chongju City (
Eom and Rim, 1992a). The scolex, recovered after treatment, was found to be unarmed. The number of main uterine branches, varying from 16 to 21, was similar to that of
T. saginata. With the eggs of
T. asiatica from the experimentally infected Korean volunteer, the authors infected and observed the infection sites of the metacestodes in the visceral organs of pigs and cattle.
In the experimental study in pigs,
T. asiatica eggs infected both of the hepatic and extrahepatic organs of pigs. Viscerotropic cysticercosis was observed in the pigs, with a majority of the non-calcified metacestodes in the livers (hepatic) and a minority in other organs (extrahepatic) such as the omentum, the lung and the serosa. Living metacestodes were observed both in hepatic and extrahepatic infection (
Fig. 4).
In the experimental study using cattle,
T. asiatica eggs infected calves in their livers but all were found to be calcified, measuring diameter less than 1.5 mm.
T. saginata eggs infected calves in the muscle only (
Fig. 4).
There is no doubt that Korea is one of the endemic areas for T. saginata, recalling the reports on C. bovis between the years 1924 and 1943 from calves in Cheju and many other provinces, with infection rates revealed to be 5.1-37.6% in cattle. The most recent observation appears to be in the measled cattle which was discarded by villagers in Kongkun-myon, Hoengsong-gun, Kangwon-do in 1975; this anecdote was reported to a Korean parasitologist. Considering all of the previous evidence, as well as the Korean habit of eating raw beef, and that no parasitologists living today had ever seen larval tapeworms in cattle by themselves, it is not difficult to speculate that Korea has had classical T. saginata in the past. But the recent researches by morphological or molecular biological methods after 1993 reveal that most of the tapeworms found are T. asiatica, and not T. saginata.
This situation leads to curiosity about the presence of T. saginata in recent times. Even if it is possible to find T. asiatica among the old slide specimens, labeled as T. saginata, preserved in many parasitology laboratories in universities and institutes scattered in Korea, the differential diagnosis is not easy, due to the morphological similarities between T. asiatica and T. saginata. An alternative method of identification, with the use of recently developed molecular biological methods, also has limited application due to DNA damage by long-term preservation of the worms in formalin.
More recently, Eom et al. (
2000) reported a
T. saginata case collected from a local hospital in Pusan. The
Taenia worm from the case was transfered to and analysed in the Department of Parasitology, Chungbuk National University School of Medicine. The two terminal proglottids transfered did not show posterior protuberances, which are one of the differential diagnostic characters. One of them was 9 by 4 mm and the other was 11 by 4 mm, in measurements of terminal proglottids. The numbers of uterine main branches were not countable, because most of the eggs were discharged out of the uterus. Random amplified polymorphic DNA-polymerase chain reaction was done on isolated genomic DNA, which showed main bands in 1.95, 1.59, 1.00, 0.80 and 0.66 kb with a primer, oligonucleotides A-08 5'-GTG ACG TAG G-3'; and multiple bands of 2.07, 1.82, 1.59, 1.13 and 0.86 kb with another primer, A-20 5'-GTT GCG ATC C-3'. These bands were identical with
T. saginata from Poland and Belgium but were different from
T. solium originating from Honduras and China, as well as from
T. asiatica from many countries.
This subject, a Korean woman aged 46-years, had no experience of eating raw liver of pigs, but prefered raw beef without any experience of traveling to other countries a few years before and after observing the expulsion of terminal proglottids by herself. With overall consideration of these data, T. saginata thus is distributed sympatrically with T. asiatica in Korea.
UNRAVELING THE EPIDEMIOLOGICAL INCONSISTENCY WITH REFERENCE TO T. ASIATICA
Hypothesis 1 with reference to pig's viscera
Natural infection of
T. asiatica metacestodes in Korean domestic pigs was reported in 1992 by Eom and Rim. The infectivity of those metacestodes was also confirmed in a human volunteer (
Eom and Rim, 1992). If we assume the visceral organ of pigs as a source of
Taenia tapeworm infection, we can now explain the epidemiological inconsistency as follows. The species ratio of 'armed tapeworm versus unarmed tapeworm = 15.4 : 79.4 = 16 : 84' and fits well to 'the food-consuming ratio of pork versus pig's viscera plus beef = 7.1 : (25.0 + 6.1) = 7.1 : 31.1 = 19 : 81' (
Table 2 &
3;
Fig. 5). Or being more simple, armed tapeworm versus unarmed tapeworm is 16 : 84 = (approximately) 1:5. And pork versus pig's viscera versus beef is 7.1 : 25.0 : 6.1 = (approximately) 1 : 4 : 1. In other words, pork : (pig's viscera + beef) is 1 : (4 + 1) = 1 : 5. Conversely, the 5 : 1 ratio of pig-eaters versus cattle-eaters can be explained as follows. Pig-eaters consist of pork-eaters and viscera-eaters, and cattle-eaters consist only of beef-eaters, which makes (1 + 4) : 1 = 5 : 1. This figuring can be shown with simple numbers in brackets in
Fig. 5. Again, the pig's viscera plays an important role in the transmission of
T. asiatica, with a relative ratio value, 4, which unravels the inconsistency between 1 : 5 and 5 : 1. Here we can now understand that pigs play their role both as an infective source of
T. solium with pork, and
T. asiatica with visceral organs. This hypothesis gives a definite role of the pig's viscera in the tapeworm epidemiology in Korea (
Table 3).
Still no natural evidence of live C. viscerotropica In the liver of cattle is available. It needs further evaluation yet, but 10.2% (10.1-11.4) of people eat raw liver of cattle (
Kang et al., 1965a;
Cho et al., 1967) and this may receive due consideration for its importance in
T. asiatica epidemiology in future, because human infection is possible with live metacestodes recovered from the liver of experimental cattle in Taiwan (
Chao et al., 1988). This hypothesis gives a good fit between the species ratio of armed tapeworm versus unarmed tapeworm, at 16 : 84, and the eating habits, i.e., pork : pig's viscera plus cattle's liver plus beef was 7.1 : (25.0 + 10.2 + 6.1) = 7.1 : 41.3 = 15 : 85, theoretically though, if we assume that transmission rates to humans are equal for the three different species.
Taenia tapeworm infections among humans correspond closely to the eating habits of intermediate hosts in each country. In Korea, we can count the eating habits of 'Churyum' and 'Semmai' those rationalize our hypothesis 1 and 2. 'Churyum' is one of Korean habits of eating widely spread among rural people in Cheju or other provinces where they eat raw liver of pigs while they are still warm right after slaughtering during village ceremonies. The other term, 'Semmai' is also called 'Senmai' which means [Senezi (n) n. Fat around the intestines: epiploon, fatty skin around the intestine of animals, fat of the epiploon: thin layer of fatty tissue on the cud pouch or rumen, semeze = semezi (provided by Prof. Won-Kll Park, Academic Society of Korea and Mongolia)]. The terms implicate the possible source of T. asiatica infection by eating 'Semmai', the fat, contaminated with extrahepatic metacestodes that could be introduced to human and cause tapeworm infections. In other words, this Mongolian term has been used in Korea, especially in Cheju-do, since the 13th century when Mongolian soldiers temporarily ruled. The habit of eating raw Semmai alone or attached to the stomach, spleen or any other visceral organs may cause the infection with T. asiatica. The omentum and fat tissue around the stomach, spleen and intestine harbor sometimes many hidden, hardly recognizable, transparent metacestodes. Eating the raw spleen itself may have no meaning but eating the omentum or fat tissues around the organs together with fat may induce the tapeworm infection. We can say the same is true for the other visceral organs such as the stomach, intestine, kidney and pancreas.
Of the three tapeworms in Korea, the distribution ratio is uncertain now, but it may be possible to speculate a ratio of T. solium : T. asiatica : T. saginata is about 7.1 : 25.0 : 6.1 = 19 : 65 : 16 (approximately 1 : 4 : 1) according to hypothesis-1; or 7.1 : (25.0 + 10.2) : 6.1 = 15 : 73 : 13 (approximately 1:5:1) according to hypothesis-2.
Evaluating the application of these hypotheses, we can get a clear understanding about the epidemiologicalal enigma, which was addressed continuously since the 1960s in Korea, by simply acknowledging the existence of T. asiatica.
Comparative epidemiologicalal patterns in Korea and other Asian countries
The custom of eating raw viscera is not new in other Asian countries also, like Taiwan and Thailand where Asian tapeworm is endemic (
Cross et al., 1991;
Fan et al., 1989b). Usually the small intestine and the flesh of wild or domestic animals are eaten raw in these countries, and most Asian countries are believed to have a similar kind of Asian tapeworm phenomenon as in Korea.
An isolated island Sorokdo (a leprosarium) is a small place showing the most simple pattern of
Taenia epidemiology in Korea, and possibly, in the world. This unique place of leprosy patients' residence has a single kind of
Taenia tapeworm with a single kind of intermediate host, pig. So distinct was this epidemiological pattern with unarmed
Taenia tapeworm, the pig was suspected to be an intermediate host of this tapeworm, and
T. asiatica was identified later, without difficulty in retrospective, though; this place is considered to be the most simple place in this study (
Fig. 6A).
The most similar Taiwanese place to Korean Sorokdo Island is Lanyu Island, of 30 square miles. As is known to western hemisphere with a familiar name, Orchid Island is a land of the Yami tribe, who moved to this small island two hundred years ago from South-East Asia, via the Philippines. Since 1960 when Hsieh first reported a beef tapeworm, it was known as one of the endemic areas of
T. saginata. Quite recently, however, it was recognized as Asian
Taenia, which was transfered to humans through Lanyu native pigs, a confirmed intermediate host (
Chung et al., 1987). It is a simpler place, with wild animals and native goats, than mainland Taiwan; but it shows a rather more complicated epidemiological pattern than Korean Sorokdo Island, because it has cattle, the intermediate host of beef tapeworm (
Fig. 6B).
In contrast, the mainland Taiwan is an island far bigger than either Sorokdo Island or Orchid Island, with many intermediate hosts as well as with complicated eating habits of raw foods. In Taiwan,
Taenia tapeworms are prevalent as high as 17% and all of the tapeworms are unarmed, and thus
T. solium is not available (
Liu et al., 1981;
Chan et al., 1987;
Chung et al., 1987;
Chung et al., 1988;
Lin et al., 1988;
Fan et al., 1989a,
1989b). It shows a more complicated epidemiological pattern than on Lanyu Island, in having many kinds of possible intermediate hosts as well as with complicated eating habits of raw foods; but there is no
T. solium (
Fig. 6C).
It is strongly considered that the pork tapeworms and the beef tapeworms occur together in Korea where the pigs and cattle are also distributed, and as well, both of them are eaten raw. Considering this epidemiologicalal complexity, it must have been difficult for parasitologists to determine what kinds of tapeworms are transfered through what kinds of intermediate hosts. As for the reason for more beef tapeworm infections, the suggestion that raw beef was consumed more frequently was not persuasive at all, because of the rarity of T. saginata metacestodes in intermediate hosts. Evidently, this erroneous speculation was closely related to the presence of T. asiatica that shares the pigs as intermediate hosts with T. solium; Cheju-do Island had been a very complex place to understand.
We can rearrange from the simplest to the hardest aspect of environmental complexity in understanding
Taenia epidemiology as follows: Sorokdo Island < Lanyu Island < Mainland Taiwan < Cheju-do Island (
Fig. 6A, B, C & D). It may sound paradoxical, but Cheju-do is one of the best places to study because it is separated from the land, has a small area, but has all complex factors on
Taenia epidemiology just as in other Asian countries which have a similar infection pattern to Korea.
Thus the explanation for the epidemiological inconsistency, which may possibly occur in other Asian countries also, is likely to depend on recognition of the unarmed tapeworm, T. asiatica.
Notes
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This study was supported in part by a research grant for basic medical sciences, Ministry of Education (1992-1993 and 1993-1994), Republic of Korea.
ACKNOWLEDGMENTS
The authors are grateful to Dr. Young-Chul Rim of Chung-Ang Animal Clinic for his kind help to arrange experimental animals, and to Dr. Young-Chul Seo and Dr. Kyung-Jae Park, Veterinary Service Laboratory for their kind help in observation of visceral organs of domestic animals. We thank Professor Seung-Yull Cho, Department of Molecular Parasitology, College of Medicine, Sungkyunkwan University for his valuable discussions on the etymology of the term semmai as well as for many useful suggestions at the beginning of the research. We also record the great help of Dr. Young-Gun Lee, Dr. Dae-Eui Hong and Dr. Jung-Tae Kim, former students in the College of Medicine, Chungbuk National University. Great thanks are also due to Mr. K. D. Kim, for his deep understanding about the importance of basic medical sciences and providing the private grant for this study without making any conditions. Dr. Craig Hayward, for his critical reading and corrections for the text, and Mr. Hyung-Kyu Jeon and Kyu-Heon Kim, for their help in preparing this manuscript should be mentioned with the authors appreciation.
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Fig. 1Eating habit of raw liver of pigs (•) or cattle (○) by interview in eight surveyed provinces in Korea (1992-1995). The overall positive cases eating raw liver of pigs or cattle out of 7,211 subjects were 18.7% and 19.8%, respectively. Open or closed circles represent 1% each.
Fig. 2Life cycles of three human Taenia tapeworms showing different organotropism, viscerotropism for T. asiatica and musculotropism for T. saginata or T, solium, in intermediate hosts.
Fig. 3Natural infection status of
Taenia asiatica metacestodes, living or dead, in the livers of 25,358 pigs slaughtered at an abattoir in Chongju, Korea (
Eom and Rim, 1992a).
Fig. 4Hepatic or extrahepatic distributions of Cysticercus viscerotropica in pigs and calves experimentally infected with the Taenia asiatica eggs collected from an experimentally infected human volunteer. Viscerotropic cysticerci do not affect muscles, but affect visceral organs of intermediate hosts.
Fig. 5Comparison of ratios between species and food consumed. Approximate numbers are shown in the brackets. In this hypothesis, pig's viscera plays an important role in the transmission of
T. asiatica, with a relative ratio of 4, which unravels the inconsistency between 1 : 5 and 5 : 1.
a)Data obtained from the egg positives based on the
Table 1 by averaging prevalences during 1990-1999.
b)Proportion of species was based on the ratio summarized in
Table 2.
c)Viscera consumed consists of the liver, intestine, lung and spleen with the proportion obtained from data summarized in
Tables 3.
Fig. 6Comparative epidemiologic patterns of Taenia tapeworms in Korea and Taiwan with host ranges. Complexity of Taenia epidemiology can be rearranged as Sorokdo Island < Lanyu Island < Mainland Taiwan < Cheju Island.
Table 1.Prevalence of human taeniasis by coprological examinations in Korea surveyed between the years 1915 and 1997
Table 1.
|
Authors |
Years |
Localities and subjects |
Number of cases
|
Prevalence (%) |
|
Examined |
Positives |
|
Matsumoto |
1915 |
Taegu |
351 |
13 |
3.7 |
|
Kobayashi & Kwona)
|
1917 |
Kyongsong Hospitalb)
|
323 |
29 |
9.0 |
|
Provincial officea)
|
1922 |
Hamkyongnam-do |
600 |
10 |
1.7 |
|
Yabe et al.a)
|
1923 |
Taegub)
|
323 |
6 |
1.9 |
|
Inobaa)
|
1923 |
Huichon-gunc)
|
102 |
3 |
2.9 |
|
1924 |
Namhaed)
|
100 |
6 |
6.0 |
|
Hara & Yoshino |
1924 |
Kyongsangnam-do |
1,141 |
24 |
2.1 |
|
Government generala)
|
1925 |
Chollabuk-doe)
|
1,592 |
16 |
1.0 |
|
Choia)
|
1927 |
Kyongsong |
4,000 |
12 |
0.3 |
|
Koyamaa)
|
1927 |
Kyongsangnam-do |
192 |
7 |
3.6 |
|
Millsa)
|
1927 |
Kyonggi-do |
7,000 |
201 |
2.9 |
|
Oda |
1929 |
Chonjuf)
|
442 |
14 |
3.2 |
|
Miwa |
1935a |
Kanggyec)
|
596 |
4 |
0.7 |
|
Miwa |
1935b |
Mokpog)
|
862 |
3 |
0.3 |
|
Nishimura |
1943 |
Taeguh)
|
341 |
2 |
0.6 |
|
Hunter et al. |
1949 |
Seoul, inhabitants |
169 |
2 |
1.2 |
|
Choi et al. |
1949 |
Chollanam-doi)
|
150 |
2 |
1.3 |
|
Brooke et al. |
1956 |
South Korea |
919 |
16 |
1.7 |
|
Lee et al. |
1960 |
Taeguj)
|
384 |
3 |
0.8 |
|
Soh et al. |
1961 |
Seoulb)
|
14,682 |
73 |
0.5 |
|
Rim |
1963 |
Wonju, Kangwon-dok)
|
1,963 |
39 |
2.0 |
|
Jeong |
1964 |
Namwonb), f)
|
250 |
7 |
2.8 |
|
Lee et al. |
1966 |
Okkuf), i)
|
803 |
32 |
4.0 |
|
|
Sunchangf), i)
|
542 |
33 |
6.1 |
|
Lee & Ryang |
1967 |
Taeguk)
|
239 |
5 |
2.1 |
|
Yun et al. |
1968 |
Taegui), l)
|
1,370 |
15 |
1.1 |
|
Park et al. |
1969 |
Wonju, Kangwon-dok)
|
1,012 |
15 |
1.5 |
|
Seo et al. |
1969 |
South Korea |
40,581 |
284 |
0.7 |
|
Kim et al. |
1970 |
Koreans in Vietnamk)
|
433 |
5 |
1.2 |
|
|
South Koreak)
|
114 |
1 |
0.9 |
|
Choi et al. |
1971 |
Kyongsangbuk-dob)
|
5,288 |
33 |
0.6 |
|
Cho et al. |
1969 |
South Korea |
1,843 |
27 |
1.5 |
|
Kim et al. |
1971 |
South Korea |
2,250 |
7 |
0.3 |
|
KAPEs)
|
1971 |
1st National surveyu)
|
24,887 |
461 |
1.9 |
|
Im et al. |
1972 |
Taeguk), m)
|
2,073 |
12 |
0.6 |
|
Seo et al. |
1972 |
Cheju-do |
3,169 |
402 |
12.7 |
|
Lee |
1973 |
South Korea |
3,822 |
61 |
1.6 |
|
Choi et al. |
1974 |
Military zonek)
|
17,775 |
75 |
0.4 |
|
Lim et al. |
1975 |
Koesan-guni), n)
|
608 |
5 |
0.8 |
|
KAPE |
1976 |
2nd National surveyu)
|
27,178 |
197 |
0.7 |
|
Seo et al. |
1977 |
Pochon-guno)
|
141 |
1 |
0.7 |
|
|
Chinyang-gund)
|
147 |
0 |
0 |
|
Choi et al. |
1979 |
Kyongsangbuk-do |
1,066 |
4 |
0.4 |
|
Joo |
1979 |
South Koreak), m)
|
3,330 |
23 |
0.7 |
|
Kim |
1980 |
Provincesf), n), p)
|
790 |
26 |
3.3 |
|
Rim et al. |
1980 |
Seoul, Provincesd), n)
|
1,946 |
40 |
2.1 |
|
KAPE |
1981 |
3rd National surveyu)
|
35,018 |
389 |
1.1 |
|
Seo et al. |
1981 |
South Korea |
13,373 |
67 |
0.5 |
|
Chai et al. |
1982 |
Kyonggi-do, Taeguk)
|
411 |
3 |
0.7 |
|
Rhee et al. |
1983 |
Mankyonggang basinf)
|
1,266 |
27 |
2.1 |
|
Bae et al. |
1983 |
Namgang basind)
|
5,291 |
28 |
0.5 |
|
Hong et al. |
1983 |
Sorokdog), i), q)
|
2,026 |
69 |
3.4 |
|
Rhee et al. |
1984 |
Tongjingang basin |
923 |
48 |
5.2 |
|
Joo |
1984 |
Taegui)
|
1,697 |
n |
0.6 |
|
Choi et al. |
1984 |
Masan, Kong]ur)
|
329 |
2 |
0.6 |
|
Joo et al. |
1985 |
Seouli), l)
|
4,256 |
4 |
0.1 |
|
|
Cheju-doi), l)
|
1,280 |
50 |
3.9 |
|
Min et al. |
1986 |
Hanyang Universityb)
|
5,251 |
0 |
0 |
|
KAHt)
|
1986 |
4th National surveyu)
|
43,590 |
119 |
0.3 |
|
Hong |
1986 |
Taegu, Seoulk)
|
2,643 |
8 |
0.3 |
|
Goo et al. |
1988 |
Yochon-gung), i)
|
1,011 |
59 |
5.8 |
|
KAH |
1992 |
5th National surveyu)
|
46,912 |
26 |
0.06 |
|
KAH |
1997 |
6th National surveyu)
|
45,832 |
11 |
0.02 |
Table 2.Collective data on species ratios of Taenia solium and T. saginata from different areas in Korea with differential diagnosis by identification of scoleces or by counting the uterine branches in the gravid proglottids (1965-1988)
Table 2.
|
Authors |
Years |
Localities |
No. of exam. |
T. solium No. (%) |
T. saginata No. (%) |
Unidentifleda) No. (%) |
|
Kang et al. |
1965 |
Cheju-do |
376 |
27 (7.1) |
327 (86.9) |
22 (6.0) |
|
Lee et al. |
1966 |
Chollabuk-do |
26 |
7 (26.9) |
19 (73.1) |
0 (0) |
|
Cho et al. |
1967 |
Cheju-do |
105 |
11 (10.5) |
91 (86.7) |
3 (2.9) |
|
Rim et al. |
1980 |
Seoul |
151 |
59 (39.1) |
82 (54.3) |
10 (6.6) |
|
|
Chungchongbuk-do |
10 |
0 (0) |
7 (70.0) |
3 (0.0) |
|
|
Kyongsangnam-do |
30 |
12 (40.0) |
16 (53.3) |
2 (6.7) |
|
|
Cheju-do |
8 |
2 (25.0) |
6 (75.0) |
0 (0) |
|
Hong et al. |
1983 |
Sorokdo Island |
26 |
0 (0) |
26 (100.0) |
0 (0) |
|
Joo et al. |
1985 |
Seoul |
13 |
4 (30.8) |
9 (69.2) |
0 (0) |
|
|
Cheju-do |
71 |
13 (18.3) |
53 (74.6) |
5 (7.0) |
|
Soh et al. |
1988 |
Cheju-do |
58 |
0 (0) |
58 (100.0) |
0 (0) |
|
Total |
|
|
874 |
135 (15.4) |
694 (79.4) |
45 (5.1) |
Table 3.Interviews on the habit of eating raw pork, pig's viscera and raw beef of inhabitants in Cheju-do (1963-1982)
Table 3.
|
|
Pigs
|
Cattle
|
|
Authors |
Years |
Intrva)
|
Pork |
% |
Intrv |
Viscera |
% |
Intrv |
Beef |
% |
|
Park and Chyu |
1963 |
463 |
97 |
21.0 |
463 |
242 |
52.3 |
NDb)
|
ND |
ND |
|
Kang et al. |
1965a |
8,161 |
353 |
4.3 |
5,286 |
1,017 |
19.2 |
8,223 |
266 |
3.2 |
|
Cho et al. |
1967 |
473 |
121 |
25.6 |
473 |
176 |
37.2 |
473 |
74 |
15.7 |
|
Kim |
1977 |
1,010 |
165 |
16.3 |
ND |
ND |
ND |
1,010 |
204 |
20.2 |
|
Kim |
1980 |
1,304 |
122 |
9.4 |
652 |
209 |
32.1 |
1,304 |
153 |
11,7 |
|
Kim |
1982 |
1,066 |
32 |
3.0 |
956 |
310 |
32.4 |
1,066 |
39 |
4.0 |
|
Total |
|
12,477 |
890 |
7.1 |
7,830 |
1,954 |
25.0 |
12,076 |
736 |
6.1 |
