INTRODUCTION
Until the 1970s, many Koreans had intestinal parasitic infections, mostly soil-transmitted helminths such as Ascaris lumbricoides, Trichuris trichiura, hookworms (Ancylostoma duodenale and Necator americanus), and Trichostrongylus orientalis [1,2]. National surveys of these intestinal parasitic infections have been carried out in the Republic of Korea (= Korea) every 5-7 years since 1971 to acquire national level statistical data according to the statistics plan by the National Statistical Office of Korea. The 2nd survey was conducted in 1976, followed by the 3rd in 1981, the 4th in 1986, the 5th in 1992, the 6th in 1997, and the 7th in 2004.
Korea has become a new member of Economic Cooperation and Development (OECD) countries and has shown a remarkable economic growth in the early 21st century [3]. In this respect, the results of the 7th survey conducted 7 years after the 6th are very important since the data can show the transition of intestinal parasitic infections in Korea. At the first survey conducted in 1971, Korea was a traditional agricultural society using human manure and had a poor sanitary and living standard with a variety of conditions that can cause intestinal parasitic infections. The data in 1971 showed an overall helminth egg positive rate of 84.3% and an accumulated egg positive rate of 147.1% indicating that Korean people had at least one or more kinds of intestinal parasitic infections. However, during the subsequent 30 years, Korea showed very high economic growth with a dramatic decrease of the helminth egg positive rate down to 2.4% in 1997. In particular, A. lumbriocoides, a representative intestinal helminth parasite and an index of soil-transmitted helminths, showed a dramatic decrease from 54.9% in the 1st survey in 1971 to 0.06% in the 6th survey in 1997. Other soil-transmitted helminths also showed dramatic decreases in the prevalence; 0.007% for hookworms, 0.04% for T. trichiura, and 0% for T. orientalis in 1997. By comparison, the prevalence of Clonorchis sinensis and heterophyids, mostly Metagonimus yokogawai, were 1.4% and 0.3%, respectively, showing comparatively higher prevalences than soil-transmitted nematodes [4-9]. In addition, about 15 species of trematodes transmitted by fresh- or brackishwater fish, including Heterophyes and Pygidiopsis, have been reported to cause human infections in Korea [10,11].
In the present study, the current status of intestinal helminth infections, i.e., egg positive rate and number of infected people as well as errors of the values, has been estimated using the results of the 7th survey conducted in 2004. Also, a basic statistical analysis was conducted using various characteristics including the region, gender, age, and urban versus rural areas. Then, the results were compared with those of the previous 6 surveys and association analyses were performed among various characteristics. To do this, a contingency table was prepared and an independence test was conducted. Also adapted was a logistic regression model to conduct more in-depth analysis based on analysis of the effect of explanatory variables on response variables to acquire more specific statistical data.
MATERIALS AND METHODS
Survey period
The 7th national survey of the prevalence of intestinal parasitic infections was carried out from June to December, 2004 as a part of Scientific Research Project of National Institute of Health, Republic of Korea (Fig. 1). The statistical analysis of the results was carried out from 30 December 2004 to 29 April 2005.
Survey population
The 10% sample survey data of Population and Housing Census (2000) was used as the survey population which consisted of 23,536 enumeration districts (EDs) excluding those EDs that were used for various other researches such as economically active population, household income, and expenditure surveys. In addition, 153 EDs such as islands, dormitory facilities, social welfare facilities, and rural communities were also excluded because of practically difficult conduction of the survey. Finally we used 23,364 EDs as the population EDs which took up 99.3% of the total EDs of survey population. Also, the number of households and population took up 99.4% and 99.5%, respectively [12].
Sample size and sample allocation
A total of 300 EDs were selected as a sample from 23,364 population EDs which consisted of 8,178 apartment EDs and 15,186 house EDs. In order to allocate samples to strata, we used the compromise of Neyman allocation which is the average of 3 Neyman allocations using 3 variables (C. sinensis, heterophyids, and pinworm infection rate) [12]. Since the infection rates of intestinal parasites were very low, we applied the relative risk and odds ratio instead of ordinary methods such as t-test to study the characteristics in 16 cities and provinces (7 metropolitan cities and 9 megalopolis areas) as in the 6th survey in 1997 [13,14].
Fecal examinations and cello-tape anal swabs
Fecal examinations were performed by the Kato-Katz thick smear and saturated salty water flotation techniques, as these were used in the 3rd, 4th, and 5th surveys [3]. For the Kato-Katz technique, only 1 smear was examined for each person. The results from the 2 examinations were put together. The prevalence of pinworm (Enterobius vermicularis) infections was estimated by the cello-tape anal swab method.
Socio-medical analysis of egg positive rate
This study conducted socio-medical analysis which was started from the third survey along with helminthological examination. Survey questions include 1) type of housing, 2) monthly income, 3) eating habit, 4) education, and 5) occupation and the trend of helminthic egg positive rate was analyzed according to the answers to the questions [15].
Statistical handling of socio-medical analysis
This study used specialized statistical software programs including the Statistical Analysis Software (SAS) and Statistical Package for the Social Sciences (SPSS) to analyze the collected data. It made a contingency table on infection path and an association analysis was conducted. The relative risk and odds ratio were used to analyze the data. Let raw freshwater fish eater's and non-eater's Clonorchis trematode egg positive rate be Π1 and Π2, respectively, at 2 × 2 contingency table. Then, the infection rate γ=Π1/Π2 is the relative risk, and θ=Π2/(1-Π1)/Π2/(1-Π2) is the odds ratio. The large sample 100 (1-α) % confidence interval of the relative risk is as follows. If 1 is not included in the confidence interval of the relative risk, it can be considered that there is a significant difference between the 2 groups.
The large sample 100(1-α)% confidence interval of the odds ratio is calculated using log θ which is the equivalent of θ.
Therefore, the large sample 100(1-α)% confidence interval of the odds ratio θ is as follows [16,17].
Basic statistical analysis
SAS statistical software was used to analyze the data based on the survey results of 2004. The weighted average of estimates of the egg positive rate and the number of egg positive were used. Also, this study used SAS calculation methods for convenience since there were insignificant differences between the correct calculation methods (both primary sampling unit, PSU, and secondary sampling unit, SSU) and SAS calculation method (only PSU) to calculate the error of the estimates [18].
RESULTS
Helminth egg positive rates in 2004 survey
The total helminth egg positive rate was 3.7% and the estimated positive number of infected people was 1,780,000. According to the regional analysis, Gyeongsangnam-do showed the highest prevalence of 16.3%, followed by 13.3% in Daejeon, 10.9% in Chungcheongnam-do, and 8.6% in Jeollanam-do. The estimated number of helminth egg positive cases was the highest in Gyeongsangnam-do as 450,000, and the second highest was observed in Jeollanam-do as 180,000 followed by the third highest in Chungcheongnam-do as 160,000 (Table 1).
Regarding the type of parasites, hookworms, T. orientalis, and tapeworms were not found, and the roundworm, lung fluke, and other parasites revealed very low positive rates. However, C. sinensis and pinworms showed higher egg positive rates in all regions except Jeju-do. The total egg positive rate of T. trichiura was 0.3%, and the number of people infected was estimated to be 130,000. The rate was the highest in Chungcheongnam-do, 2.5%. The average egg positive rate of heterophyids was 0.5% indicating the presence of 220,000 infected people and was the third most prevalent type of parasite following C. sinensis and pinworms. The egg positive rate of heterophyids in Gyeongsangnam-do was 4.6% (120,000 infected people), which was the highest followed by Daejeon of 1.7%. The estimated prevalence of pinworm infection was 0.6% (290,000 infected) and was evenly distributed in all regions except for Daejeon which showed a remarkably higher prevalence of 4.0%. C. sinensis showed the highest prevalence of 2.4% which comprise about 1,170,000 infected people. The regional egg positive rate was the highest in Gyeongsangnam-do with 11.3% followed by Daejeon 6.9%, Chungcheongnam-do 6.8%, and Jeollanam-do 6.2%. The estimated number of infected people was 310,000 in Gyeongsangnam-do, 130,000 in Jeollanam-do, and 110,000 in Busan. It seems that C. sinensis egg positive rates had great effects on the total egg positive rate of each district. The egg positive rate of each parasite, estimated number of infections, and upper and lower confidence limits are in Table 2. Although there were 879 infected cases among 20,370 showing a 4.3% egg positive rate, it was a simple proportion without weights. The estimated egg positive rates calculated by using weights are presented in Table 2.
Comparison according to the year of survey
National surveys of the prevalence of intestinal parasitic infections have been conducted 7 times from the 1st in 1971 until the 7th in 2004 having a 5-7 year gap between surveys. In this section, trends of intestinal parasitic infections were analyzed by comparing the results of all 7 surveys so as to be referred for policy development of the government in the future. According to Table 3, the egg positive rates in the 1st (1971) and the 2nd (1976) surveys were 84.3% and 63.2%, respectively, indicating that most of the people in the country were infected with at least 1 type of parasite. The major parasitic infections at that time were soil-transmitted parasites such as the roundworm, whipworm, and hookworms. However, the egg positive rate decreased dramatically to a 1 digit level from the 5th and 6th surveys conducted in 1992 and 1997, respectively. However, the 7th showed a little bit increased rate (3.7%) than the 6th (2.4%). In the case of snail-transmitted helminths like C. sinensis, they did not contribute much to the total egg positive rate until the 4th survey in 1986. However, in recent surveys, they showed less dramatic decreases in the egg positive rate compared to other types of parasites. Therefore, it became apparent that it would be important to manage snail-transmitted helminths, in particular, C. sinensis.
According to the egg positive rate based on the gender, the egg positive rate of women was higher until the 3rd survey. However, men showed higher prevalences than women after then (Table 4). Females had more infections with soil-transmitted parasites, whereas males had more infections with snail-transmitted helminths like C. sinensis and heterophyids. Especially, the egg positive rate of C. sinensis was much higher in males than in females. The heterophyid egg positive rate also was higher in males than in females. It is considered that the infection by these parasites is directly related to the eating habit of raw freshwater fish.
Until the 6th survey, the age gap was set at 5 year to compare the results according to the subjects' age and the upper age limit was set at 60 year. However, the age gap was set at 10 year from the 7th survey since the difference between age groups became minor, and comparison between each age group seemed less meaningful. Also, the upper age limit was increased from 60 year to 90 year. Since the average life expectancy in Korea has been increasing steadily, and the number and proportion of aged population are also increasing as time goes by, it would be appropriate to subdivide the age group 60 year and over into 4 more age groups (61-70, 71-80, 81-90, and > 90 year) in future analysis. At this time, the data > 60 year of age was used. To compare the age-prevalence data, those collected from the 6 previous surveys were modified after binding them into 10 year intervals.
The overall helminth egg positive rates for the age groups 10s and 20s were much lower, 1.5% and 1.8%, respectively, compared to the total egg positive rate. On the other hand, the egg positive rate was higher for the age groups 40s and over (except the 90s) than the average egg positive rate. Especially, the egg positive rate of the 50s was the highest, 6.9%. Although the egg positive rate of C. sinensis was lower for the age groups of < 40 year compared to the average, over 40 year (except the 90s) showed much higher rates than the average, and the rate was the highest for the 50s at 5.64%. Heterophyids also revealed similar phases with C. sinensis and the highest egg positive rate was shown in the 50s. On the other hand, pinworm infection was higher in the age group 10s, 2.8%, which was much higher than the average value of 0.6% (Table 5).
Through the 6th and 7th surveys, the egg positive rate of helminths has been dramatically decreasing. Especially, except for T. trichiura, C. sinensis, heterophyids, and the pinworm, the egg positive rates were lower than 0.1% which indicated that there were actually almost no infections. Instead, the 4 kinds of parasites should be managed more importantly. The egg positive rate of T. trichuris is dramatically decreasing along with the total positive rate, the rates of the pinworm, C. sinensis, and heterophyids are decreasing rather gradually. In particular, C. sinensis does not show any big difference. Moreover, compared with the 6th survey, the egg positive rate of C. sinensis increased a little whereas it was unchanged for heterophyids.
Association analysis
To observe the correlations among regions (urban and rural areas), genders, types of housing, and education, contingency tables were designed. According to Table 6 that showed the relative risk of parasitic infections by regions, the relative risk of parasites except A. lumbricoides (unfertilized) was higher than 1. The relative risk of A. lumbricoides (fertilized) was the highest (8.3426), followed by T. trichuris (3.0666), heterophyids (2.8334), and C. sinensis (2.4626). The relative risk 2.4626 of C. sinensis means that the infection rate in rural areas was 146% higher than in urban areas. Since 95% confidence interval is between 2.4533 and 2.4719, it is 95% confident to say that the rural area infection rate was between 2.4533 and 2.4719 times that of the urban area infection rate.
On the other hand, C. sinensis odds ratio was 2.5362, which means that C. sinensis infection rate in rural areas is 2.5362 times higher than in urban areas. Since the confidence interval of the odds ratio does not include 1, there were differences in odds ratios of C. sinensis infections between rural and urban areas. Table 7 showed the results of significance test of each parasite infection by gender. The relative risk was higher than 1 except in A. lumbricoides (unfertilized) and T. trichiura. The relative risk of heterophyids was 2.4376 which was the highest followed by C. sinensis of 1.9850. The relative risk of 2.4376 means that the heterophyid infection rate of men was 144% higher than that of women, and it was 95% confident to say that the infection rate of men was between 2.4157 and 2.4597 times higher than that of men. In the meantime, the odds ratio of heterophyids was 2.4472. This means that heterophyid infection rate of males was 2.4472 times higher than that of females. Because the confidence interval of the odds ratio does not include 1, it can be said that there was difference in the odds ratio of heterophyid infection between genders. Since 95% confidence interval of the odds ratio was 2.4252 and 2.4695, heterophyid infection rates in men was at least 143% higher than those of females.
Logistic regression analysis
Among various explanatory variables in C. sinensis data, the explanatory variable that shows the gender was considered to have effects on C. sinensis infection which is the response variable. The gender is a categorical variable that indicates male or female.
The 2-way contingency table of the gender and C. sinensis is shown in Table 8. Among 48,583,806 total Korean people, 1,174,224 (2.4%) were estimated to be infected. Among them, the male infection rate was 66.6% and the female infection rate was 33.3%, indicating that C. sinensis infection rate of males was twice as high as that of females.
DISCUSSION
The national egg positive rate of intestinal helminths and the number of infected people as well as the errors of estimates for each parasite species have been estimated in the present study. The total helminth egg positive rate appeared to be 3.7%, and the estimated total infected number of people among the whole population was 1,780,000. Some results of the present survey were presented in a review paper by Hong et al. [19] who referred the monographic series reports [3]. The overall egg positive rate appeared to have increased a little compared to the 6th survey conducted in 1997 [3]. According to regions, Gyeongsangnam-do showed the highest prevalence, 16.3%, followed by 13.3% of Daejeon, 10.9% of Chungcheongnam-do, and 8.6% of Jeollanam-do. In a survey conducted 28 year previously on 13,373 people living along the 8 large riverside areas in Korea [20], the egg positive rate of any kind of parasites was 58.7% which was remarkably higher than the present figures. Among them, the whipworm (35.2%), roundworm (22.9%), C. sinensis (21.5%), and heterophyids (4.8%) comprised the majority of parasite species involved [20]. Also, the rate of intestinal parasitic infections of the residents in Geum-gang (= river) area, in the middle region of Korea, was reported to be 40.8%, and C. sinensis and heterophyids were the major parasites [9].
In the present survey, C. sinensis revealed the highest prevalence among all parasite species involved. Its nationwide egg positive rate was 2.4% and the estimated number of infected people was at least 1,170,000. According to regions, the egg positive rate was the highest (11.3%) in Gyeongsangnam-do, followed by Daejeon (6.9%), Chungcheongnam-do (6.8%), and Jeollanam-do (6.2%). These figures were comparatively lower than those of a previous report that showed a 16% C. sinensis prevalence in Hamyang, Gyeongsangnam-do in 2002 [4]. The present results of C. sinensis prevalence were also lower than those reported in 4 southern endemic areas; 17.1% in Nakdong-gang, 11.2% in Seomjin-gang, 5.5% in Youngsan-gang, and 4.6% in Geum-gang [21]. However, the results of the present survey were similar to a previous local survey at Geum-gang [5], where the egg positive rate of C. sinensis was 9.3% and that of Metagonimus spp. was 5.5%.
The egg positive rates of C. sinensis and heterophyids appeared to be higher in the present survey than in the 6th survey [3], although it should be considered that the egg positive rate may vary to some extent according to sampling bias of subjected cases. For example, the more riverside people are included in the examination the higher the prevalence would appear to be. Anyhow, in the present study, rural areas compared to urban areas, and males compared to females, had higher total egg positive rates. Since a much higher infection rate was observed in males than females, males should pay more attention to sanitation. Infected men may have difficulties in labor and other social activities, so that the infection could affect the total productivity of the regional society [20]. Regarding the age-dependent prevalence, the age groups of the 10s and 20s had lower egg positive rates than the average rate, and the age group of the 40s and over showed higher egg positive rates than the average. In particular, the age group of the 50s showed the highest egg positive rate of 6.9%. It is suggested that the age group with higher infection rate should have eaten more freshwater fish contaminated with C. sinensis or Metagonimus spp. compared to other age groups [4].
The results of the present survey, together with previous ones, can be used as basic data to claim successful control of soil-transmitted helminths in Korea [19]. Especially, it can be said that Korea achieved one of the standards required by OECD, since the data of soil-transmitted helminths including the roundworm, whipworm, hookworms, and T. orientalis could be used as an index that can evaluate the level of parasitic diseases control, sanitation, and status of economy.
However, the most important focus of this 7th survey was that fishborne parasitic infections, including C. sinensis and heterophyid infections, are steadily prevalent along river side areas. Health education can guide people to be more cautious about eating raw freshwater fish and is in urgent need. It is considered that the present data can be used as a reference by other countries, WHO, and other international health organizations which would like to establish parasite control projects in parasite endemic areas. The present data and files could be used for project analyses and other connected researches in the future.
