PHWR Public Health Weekly Report

In the Republic of Korea, most foodborne parasitic infections occur because people living near rivers have a habit of eating raw freshwater fish infected with Clonorchis sinensis or Heterophyid flukes metacercaria. For this reason, the five major river watersheds in the Republic of Korea (Seomjingang [River], Nakdonggang [River], Yeongsangang [River], Geumgang [River], and Hangang [River]) have become epidemic areas for liver flukes and intestinal flukes. Since 2005, the Korea Disease Control and Prevention Agency (KDCA)’s Division of Vectors and Parasitic Diseases has been conducting a surveillance project for intestinal parasite infections including liver flukes, targeting areas where foodborne parasites are prevalent. Additionally, the infection status of Enterobius vermicularis, a statutory intestinal parasite but distinct from liver flukes in terms of specimen acquisition methods and targets for testing, was further investigated. This study presents the results of the 2023 intestinal parasite surveillance in endemic areas and the E. vermicularis infection survey conducted among preschool children, analyzing the infection rates by parasite type and region.

The intestinal parasite surveillance project including liver flukes enlisted 200 to 2,000 volunteers in the region from the following 36 regions: Chungcheongbuk-do (Goesan-gun, Yeongdong-gun, and Okcheon-gun), Chungcheongnam-do (Gongju-si and Geumsan-gun), Jeollabuk-do (Namwon-si, Jinan-gun, Sunchang-gun, and Imsil-gun), Jeollanam-do (Gurye-gun, Suncheon-si, Naju-si, Gwangyang-si, Damyang-gun, Gokseong-gun, Boseong-gun, Hwasun-gun, Gangjin-gun, Haenam-gun, and Hampyeong-gun), Gyeongsangbuk-do (Pohang-si, Andong-si, Sangju-si, Cheongsong-gun, Yeongcheon-si, and Yecheon-gun), Gyeongsangnam-do (Jinju-si, Miryang-si, Uiryeong-gun, Haman-gun, Changnyeong-gun, Hadong-gun, Sancheong-gun, Hamyang-gun, Geochang-gun, and Hapcheon-gun). The KDCA conducted treatment verification, including planning and management. Community health centers collected specimens, offered education on case management and infection prevention, and provided treatment support for individuals who tested positive. The Korea Association of Health Promotion conducted parasite infection tests. A total of 26,258 specimens collected were subjected to testing for 10 species of intestinal parasites including C. sinensis, Heterophyid flukes, Trichuris trichiura, Ascaris lumbricoides, Paragonimus westermani, Taenia spp., Diphyllobothrium latum, Gymnophalloides seoi, Hookworm, Echinostoma hortense.

The eggs from these intestinal parasites were isolated using the ParaEgg kit (no. 10-2561898), a simple pretreatment kit developed by the KDCA based on the established water-ether precipitation method. The ParaEgg kit consists of a 15-ml tube with distilled water, a filter insert, and a sample collection spoon. Approximately 0.5 g of specimen was scooped out using the spoon, placed into the tube with the filter insert, blended to completely loosened the specimen, and centrifuged. The filter insert was removed from the tube and discarded. After adding 3 ml of ether and closing the lid, the mixture was blended again, centrifuged to collect the precipitate, and examined under a microscope to identify the presence of parasite eggs.

To investigate the national prevalence of E. vermicularis infection, 34,993 infants and young children across the nation’s 12 metropolitan cities and provinces (comprising 53 cities and guns) underwent screening. The testing locations were determined based on the number of participants: 1,691 individuals in Seoul, 2,398 in Gyeonggi, 1,049 in Incheon, 3,571 in Busan, 2,036 in Gangwon-do, 689 in Chungcheongbuk-do, 1,473 in Chungcheongnam-do, 282 in Jeollabuk-do, 8,040 in Jeollanam-do, 2,779 in Gyeongsangbuk-do, 4,116 in Gyeongsangnam-do, and 6,869 in Jeju-do. The specimens were obtained using the cello tape perianal swab method tape and examined under a microscope to determine the presence of parasite eggs.

In 2023, a survey on the status of intestinal parasite infections was conducted among 26,258 residents in endemic areas, the results revealed that the rates of intestinal parasites infection decreased a 1.6% in the previous year. A total of 3.7% (980 individuals). The highest infection rates of intestinal parasites was observed for C. sinensis (1.9%, 512 individuals), followed by Heterophyids flukes (1.6%, 417 individuals), T. trichiura (0.2%, 40 individuals), and G. seoi (0.1%, 11 individuals) (Table 1). By sex, the proportion of males (5.8%) with intestinal parasites infection was more than twice higher than that of females (2.6%), showing a similar pattern to that reported in the previous year. By age, the highest infection rate was observed among individuals in their 60s (5.2%), followed by 4.9% among those in their 50s, 3.7% among those in their 40s, and 3.4% among those in their 70s. Meanwhile, intestinal parasite infection was not reported among individuals in their 20s or younger (Figure 1). By region, Jeollanam-do exhibited the highest intestinal parasite infection rate (4.4%), followed by Gyeongsangbuk-do (4.2%), Gyeongsangnam-do (3.3%), Chungcheongbuk-do (1.9%), Jeollabuk-do (1.7%), and Chungcheongnam-do (0.4%). By city and gun, Gwangyang-si recorded the highest rate (12.3%). The positive rates in Gwangyang-si showed a gradually increase from 2019 to 2022 but decreased in 2023, with a slight change of 0.6%. By city and gun, nine regions experienced an increase in positivity rates from 2022 to 2023, while others experienced a decrease in rates. Specifically, increases were observed in Yeongdong-gun in Chungcheongbuk-do; Namwon-si in Jeollabuk-do; Gurye-gun in Jeollanam-do; and Cheongsong-gun, Yeongcheon-si, Yecheon-gun, Milyang-si, Changnyeong-gun, and Hadong-gun in Gyeongsangbuk-do. The increase ranged modestly from 0.2% to 1.2%, while the decrease was substantial, ranging from 0.2% to 9.1% (Table 2). The positivity rate of parasite eggs in 2022 and 2023 was significant (Table 3).

Figure 1. Comparision intestinal parasites infection by age and sex

Table 1 Egg positive rate of intestinal parasites

Investigation	Egg positive rates of intestinal parasites (%)
	Total	Clonorchis sinensis	Heterophyid flukes	Trichuris trichiura	Gymnophalloides seoi
26,258	980 (3.7)	512 (1.9)	417 (1.6)	40 (0.2)	11 (0.1)

Unit: n (%)..

Table 2 The egg positive rates of intestinal parasites by survey areas

Location	Positive rate (%)	Survey area	2022 year				2023 year			Change of positive rate (%p)
			Investigation	No. of egg positive case	Egg positive rate (%)		Investigation	No. of egg positive case	Egg positive rate (%)
Chungcheongbuk-do	1.9	Goesan-gun	311	9	2.9		296	8	2.7	–0.2
		Yeongdong-gun	1,541	53	3.4		372	15	4.0	0.6
		Okcheon-gun	1,010	15	1.5		996	9	0.9	–0.6
		Gongju-si	569	3	0.5		538	2	0.4	–0.2
		Geumsan-gun	503	14	2.8		520	3	0.6	–2.2
Jeollabuk-do	1.7	Namwon-si	498	8	1.6		500	13	2.6	1.0
		Jinan-gun	541	7	1.3		535	2	0.4	–0.9
		Sunchang-gun	507	12	2.4		574	10	1.7	–0.6
		Imsil-gun	956	37	3.9		799	21	2.6	–1.2
Jeollanam-do	4.4	Gurye-gun	1,068	69	6.5		1,215	81	6.7	0.2
		Suncheon-si	532	52	9.8		502	34	6.8	–3.0
		Naju-si	532	13	2.4		576	6	1.0	–1.4
		Gwangyang-si	1,017	131	12.9		1,018	125	12.3	–0.6
		Damyang-gun	582	25	4.3		562	14	2.5	–1.8
		Gokseong-gun	1,025	88	8.6		1,528	72	4.7	–3.9
		Boseong-gun	503	11	2.2		557	8	1.4	–0.8
		Hwasun-gun	525	44	8.4		545	18	3.3	–5.1
		Gangjin-gun	505	9	1.8		512	6	1.2	–0.6
		Haenam-gun	760	31	4.1		1,215	20	1.6	–2.4
		Hampyeong-gun	511	17	3.3		511	13	2.5	–0.8
Gyeongsangbuk-do	4.2	Pohang-si	500	36	7.2		501	25	5.0	–2.2
		Andong-si	2,014	204	10.1		1,117	11	1.0	–9.1
		Sangju-si	499	9	1.8		502	6	1.2	–0.6
		Cheongsong-gun	1,012	45	4.4		828	40	4.8	0.4
		Yeongcheon-si	1,039	44	4.2		1,131	61	5.4	1.2
		Yecheon-gun	503	9	1.8		552	10	1.8	-
Gyeongsangnam-do	3.3	Jinju-si	851	42	4.9		836	41	4.9	-
		Miryang-si	800	22	2.8		658	25	3.8	1.0
		Uiryeong-gun	500	19	3.8		514	11	2.1	–1.7
		Haman-gun	1,051	31	2.9		666	18	2.7	–0.2
		Changnyeong-gun	641	21	3.3		500	30	6.0	2.7
		Hadong-gun	2,231	194	8.7		1,104	99	9.0	0.3
		Sancheong-gun	840	51	6.1		817	45	5.5	–0.6
		Hamyang-gun	897	52	5.8		1,111	42	3.8	–2.0
		Geochang-gun	917	52	5.7		893	19	2.1	–3.5
		Hapcheon-gun	627	49	7.8		657	17	2.6	–5.2
Total			28,918	1,528	5.3		26,258	980	3.7	–1.6

Table 3 Analysis of statistical significance and change in egg positive rates

Year	Investigation	No. of egg positive case	Egg positive rate (%)	COR (95% CI)	p-value
2022	28,918	1,528	5.3	5.28 (5.0, 5.6)	0.0001
2023	26,258	980	3.7	3.7 (3.5, 4.0)

COR=correlation; CI=confidence interval..

The infection rates of the E. vermicularis was 0.20% (67 individuals) (Table 4). By region, Jeollanam-do had the highest positivity rate (0.37%), followed by Jeju (0.17%, 12 individuals), Chungcheongnam-do (0.68%, 10 individuals), Gyeongsangnam-do (0.22%, 9 individuals), and Gyeongsangbuk-do (0.07%, 2 individuals). Gangwon-do, Seoul, Jeollabuk-do, and Chungcheongbuk-do each reported one infection case, while Busan, Incheon, and Gyeonggi had no infection cases. In the analysis of 67 individuals with E. vermicularis infection, 36 boys and 31 girls were infected. The peak incidence occurred at age 7 years for boys (16 cases) and at age 6 years for girls (17 cases) (Figure 2).

Figure 2. Comparision Enterobius vermicularis infection by age and sex

Table 4 Infection of Enterobius vermicularis in regions

Investigation and infection rates (%) in region
Region	Total	Seoul	Gyeonggi	Incheon	Busan	Kangwon	Chungbuk	Chungnam	Jeonbuk	Jeonnam	Gyeongbuk	Gyeongnam	Jeju
Investigation	34,993	1,691	2,398	1,049	3,571	2,036	689	1,473	282	8,040	2,779	4,116	6,869
No. of infection (rates, %)	67 (0.20)	1 (0.06)	0 (0.00)	0 (0.00)	0 (0.00)	1 (0.05)	1 (0.15)	10 (0.68)	1 (0.35)	30 (0.37)	2 (0.07)	9 (0.22)	12 (0.17)

The survey project for intestinal parasites was initiated in 2005, targeting eight regions with an intestinal parasite infection rate of 11.0%. In 2022, the survey was conducted in 36 regions where the infection rate decreased to 5.3%; the infection rate has remained at 5% since 2015 [1]. However, the current survey reported a 3.7% infection rate, a reduction of 1.6% from that observed in 2022 [2]. In this survey, the KDCA’s ParaEgg kit was used instead of the traditional water-ether precipitation method for the pretreatment of fecal samples to reduce the fecal pretreatment time and improve the testing environment, enhancing work efficiency. In the validity test, the ParaEgg kit detected parasite eggs in 3 out of 20 samples that yielded a negative result on the conventional water-ether precipitation method, demonstrating its higher sensitivity. However, as this was the first application in the field, further analysis is needed to determine if testing using the ParaEgg kit is associated with a reduction in infection rates. Age-based analyses showed that individuals in their 50s living near the Seomjingang River or Nakdonggang River still frequently consume raw fish [3]. Liver flukes, which had the highest rate of C. sinensis infections, accounted for 52.2% of all cases, while Heterophid flukes accounted for 42.5%. This finding indicates that foodborne parasites accounted for 94.7% of intestinal parasite infections. Of the 36 cities and guns, Gwangyang-si had the highest overall infection rate for intestinal parasites, consistent with that reported in the previous year, while Pohang-si had the highest infection rate for liver flukes (5.0%). Last year, Andong-si had a significantly higher infection rate. However, this year, Andong-si experienced the largest decrease among the regions, with the infection rate dropping from 10.1% in 2022 to 1.0% in 2023. This decline may be attributed to the exclusion of Gilan-myeon and Imha-myeon, which had high positivity rates, from the 2023 survey area. To reduce the current infection rate of intestinal parasites in the Republic of Korea, detailed surveillance and analysis of areas with high liver fluke infection by eup, myeon, and dong are necessary. Additionally, ongoing investigation of new regions is essential. E. vermicularis is primarily transmitted through the oral-fecal route by unclean hands, consumption of contaminated food, or contact with contaminated objects such as toys. Thus, infants and young children who do not wash their hands regularly and fail to understand the concept that the hands in contact with their anus may harbor contamination tend to experience high infection rates [4]. The national survey of preschool children reported a low prevalence of E. vermicularis infection. A 5-year survey was conducted in Yeosu-si in Jeollanam-do. The results showed an average positivity rate of 3.6%, which decreased from 5.0% at the beginning of the project to 1.0% after 5 years of continuous field survey [5]. From 2008 to 2019, E. vermicularis testing by province and metropolitan city showed positivity rates ranging from 0.6% to 3.9% depending on the region [6]. In our study, the positivity rate for E. vermicularis was notably low at 0.2%. This decrease may be attributed to heightened personal hygiene practices, especially among children, since the emergence of the coronavirus disease 2019 pandemic. The Division of Vectors and Parasitic Diseases in the KDCA will continue to conduct testing and treatment support projects in endemic areas to reduce the prevalence of intestinal parasite infections. Additionally, they will continue to collaborate with relevant departments and local governments to promote awareness and alter the local consumption patterns of wild freshwater fish to prevent infection.

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

Conflict of Interest: The authors have no conflicts of interest to declare.

Author Contributions: Conceptualization: HIL. Data curation: JWJ. Methodology: SOB. Visualization: ESL. Investigation: YJL. Writing – original draft: MRL. Writing – review & editing: MRL.