Infection Status of Hospitalized Diarrheal Patients with Gastrointestinal Protozoa, Bacteria, and Viruses in the Republic of Korea

To understand protozoan, viral, and bacterial infections in diarrheal patients, we analyzed positivity and mixed-infection status with 3 protozoans, 4 viruses, and 10 bacteria in hospitalized diarrheal patients during 2004-2006 in the Republic of Korea. A total of 76,652 stool samples were collected from 96 hospitals across the nation. The positivity for protozoa, viruses, and bacteria was 129, 1,759, and 1,797 per 10,000 persons, respectively. Especially, Cryptosporidium parvum was highly mixed-infected with rotavirus among pediatric diarrheal patients (29.5 per 100 C. parvum positive cases), and Entamoeba histolytica was mixed-infected with Clostridium perfringens (10.3 per 100 E. histolytica positive cases) in protozoan-diarrheal patients. Those infected with rotavirus and C. perfringens constituted relatively high proportions among mixed infection cases from January to April. The positivity for rotavirus among viral infection for those aged ≤ 5 years was significantly higher, while C. perfringens among bacterial infection was higher for ≥ 50 years. The information for association of viral and bacterial infections with enteropathogenic protozoa in diarrheal patients may contribute to improvement of care for diarrhea as well as development of control strategies for diarrheal diseases in Korea.     

Four Cases of Taenia saginata Infection with an Analysis of COX1 Gene

Human taeniases had been not uncommon in the Republic of Korea (=Korea) until the 1980s. The prevalence decreased and a national survey in 2004 revealed no Taenia egg positive cases. However, a subsequent national survey in 2012 showed 0.04% (10 cases) prevalence of Taenia spp. eggs suggesting its resurgence in Korea. We recently encountered 4 cases of Taenia saginata infection who had symptoms of taeniasis that included discharge of proglottids. We obtained several proglottids from each case. Because the morphological features of T. saginata are almost indistinguishable from those of Taenia asiatica, molecular analyses using the PCR-RFLP and DNA sequencing of the cytochrome c oxidase subunit 1 (cox1) were performed to identify the species. The PCR-RFLP patterns of all of the 4 specimens were consistent with T. saginata, and the cox1 gene sequence showed 99.8-100% identity with that of T. saginata reported previously from Korea, Japan, China, and Cambodia. All of the 4 patients had the history of travel abroad but its relation with contracting taeniasis was unclear. Our findings may suggest resurgence of T. saginata infection among people in Korea.     

Echinostome Infections in the Striped-Field Mouse, Apodemus agrarius, and the Ussuri White-Toothed Shrew, Crocidura lasiura, Caught Near the Demilitarized Zone, Gyeonggi-do (Province), Republic of Korea

A total of 1,498 small mammals (rodents and insectivores), including Apodemus agrarius (n = 1,366), Crocidura lasiura (54), Mus musculus (32), Micronytus fortis (28), Eothenomys regulus (9), Micronys minutes (6), and Cricetulus triton (3), were live-trapped in Gyeonggi-do (Province) (Paju-si, Pocheon-gun, and Yeoncheon-gun) near the demilitarized zone (DMZ) from December 2004 to September 2005. A. agrarius was found to be infected with 3 species of echinostomes (Echinostoma hortense, Echinostoma cinetorchis, and Euparyphium murinum), while C. lasiura was infected with 1 species (Echinochasmus japonicas) of echinostome. Other mammals were free from echinostome infections. Total 16 E. hortense were detected in 7 (0.5%) mice, 9 E. cinetorchis from 5 (0.4%), and 3 E. murinum from 2 (0.1%) out of 1.366 A. agrarius examined. E. japonicus was found only in 1 (1.9%; total 3 specimens) C. lasiura. These results demonstrate that A. agrarius and C. lasiura, inhabiting near the DMZ of Gyeonggi-do serve as the natural definitive hosts for several species of echinostomes, although their infection rates are low. This is the first record of natural infections of A. agrarius with E. cinetorchis and C. lasiura with E. japonicus in the Republic of Korea.     

Human Taeniasis in the Republic of Korea: Hidden or Gone?

History and current status of human taeniasis in the Republic of Korea, due to Taenia solium, Taenia asiatica, and Taenia saginata, are briefly reviewed. Until the 1980s, human taeniasis had been quite common in various localities of Korea. A study from 1924 reported 12.0% egg prevalence in fecal examinations. Thereafter, the prevalence of Taenia spp. ranged from 3% to 14% depending on the time and locality. Jeju-do, where pigs were reared in a conventional way, was the highest endemic area of taeniasis. An analysis of internal transcribed spacer 2 and mitochondrial cytochrome c oxidase 1 genes of 68 taeniasis cases reported from 1935 to 2005 in Korea by a research group revealed the relative occurrence of the 3 Taenia spp. as follows: T. solium (4.4%), T. asiatica (75.0%), and T. saginata (20.6%). However, national surveys on intestinal helminths conducted every 5 years on randomly selected people revealed that the Taenia egg prevalence dropped from 1.9% in 1971 to 0.02% in 1997 and finally to 0.0% in 2004. With the exception of 3 egg-positive cases reported in 2008 and 2 worm-proven cases in 2011, no more cases have been officially recorded. Based on these surveys and also on other literature, it can be concluded that taeniasis has virtually disappeared from Korea, although a few sporadic cases may remain hidden. Human cysticercosis is also expected to disappear within a couple of decades in Korea.     

Species Diversity and Seasonal Distribution of Culicoides spp. (Diptera: Ceratopogonidae) in Jeju-do,Republic of Korea

Biting midges belonging to the genus Culicoides (Diptera: Ceratopogonidae) were collected by Mosquito Magnet^® and black light traps at 5 sites on Jeju-do, Republic of Korea (Korea), from May-November 2013 to determine species diversity and seasonal distribution. A total of 4,267 specimens were collected, of which 99.9% were female. The most common species was Culicoides tainanus (91.8%), followed by C. lungchiensis (7.2%) and C. punctatus (0.6%), while the remaining 4 species accounted for <0.5% of all Culicoides spp. that were collected. High numbers of C. tainanus were collected in May, followed by decreasing numbers through August, and then increasing numbers through November when surveillance was terminated. Peak numbers of C. lungchiensis were collected during September, with low numbers collected from May-August and October-November. The presence of C. lungchiensis in Korea was confirmed by morphological and molecular analyses.     

A Cross-Sectional Study on Intestinal Parasitic Infections in Rural Communities,Northeast Thailand

Despite the existence of effective anthelmintics, parasitic infections remain a major public health problem in Southeast Asia, including Thailand. In rural communities, continuing infection is often reinforced by dietary habits that have a strong cultural basis and by poor personal hygiene and sanitation. This study presents a survey of the prevalence of intestinal parasitic infections among the people in rural Thailand. The community-based cross-sectional study was conducted in villages in Khon Kaen Province, northeastern Thailand, from March to August 2013. A total of 253 stool samples from 102 males and 140 females, aged 2-80 years, were prepared using formalin-ethyl acetate concentration methods and examined using light microscopy. Ninety-four individuals (37.2%) were infected with 1 or more parasite species. Presence of parasitic infection was significantly correlated with gender (P=0.001); nearly half of males in this survey (49.0%) were infected. Older people had a higher prevalence than younger members of the population. The most common parasite found was Opisthorchis viverrini (26.9%), followed by Strongyloides stercoralis (9.5%), Taenia spp. (1.6%), echinostomes (0.4%), and hookworms (0.4%). The prevalence of intestinal protozoa was Blastocystis hominis 1.6%, Entamoeba histolytica 0.8%, Entamoeba coli 0.8%, Balantidium coli 0.4%, Iodamoeba bütschlii 0.4%, and Sarcocystis hominis 0.4%. Co-infections of various helminths and protozoa were present in 15.9% of the people. The present results show that the prevalence of parasitic infections in this region is still high. Proactive education about dietary habits, personal hygiene, and sanitation should be provided to the people in this community to reduce the prevalence of intestinal parasite infections. Moreover, development of policies and programs to control parasites is needed.     

Two endemic foci of heterophyids and other intestinal fluke infections in southern and western coastal areas in Korea

Two endemic foci of heterophyid infections were discovered in coastal villages of Puan-gun, Chollabuk-do, and Sachon-gun. Kyongsangnam-do, Korea. Fecal examinations were performed on 153 inhabitants of Puan-gun and 138 of Sachon-gun, using cellophane thick smear and formalin-ether sedimentation technique. The helminth egg and/or protozoan cyst positive rate was 21.5% (33/153) in Puan-gun and 39.1% (54/138) in Sachon-gun. In Puan-gun, the egg positive rate of heterophyids was the highest, 17.6%, and that of other parasites was 0.7-2.6% by parasite species. In Sachon-gun, that of heterophyids was 18.8%, followed by Clonorchis sinensis (12.3%), and other parasites (0.7-5.0%). Twenth-two (Puan-gun) and six (Sachon-gun) heterophyid egg positive cases were treated with praziquantel, and adult flukes were collected from their diarrheic stools. A total of 3,284 adult flukes of Heterophyes nocens was collected from all of the 22 patients treated in Puan-gun (3-778 individually), and other trematodes were also collected from 2-15 patients: Pygidiopsis summa, Stellantchasmus falcalus, Metagonimus yokogawai, M. miyatai, Stictodora fuscata, Heterophyopsis continua, Acanthoparyphium kurogamo, and Gymnophalloides seoi. In Sachon-gun, M. yokogawai (3,007 specimens), H. nocens (120), and S. falcatus (46) were collected from 5 of 6 treated patients, and H. continua and S. lari each from one patient. The present study revealed that heterophyid flukes, especially H. nocens and M. yokogawai, are prevalent in the southern and western coastal areas of Korea where fresh and/or brackish water fishes are popularly eaten raw.     

Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea

Infection status of intestinal flukes was investigated in residents of Muan-gun, Jeollanam-do, the Republic of Korea. Total 1,257 fecal samples of residents were examined by formalin-ether sedimentation technique and Kato-Katz thick smear method. Helminth eggs were detected from 95 (7.6%) residents, and eggs of heterophyid flukes and Clonorchis sinensis were found from 62 (4.9%) and 40 (3.2%) cases, respectively. The larger heterophyid eggs, somewhat dark-brown in color and 37.7 × 21.5 µm in average size, and found in 32 (2.6%) out of 62 egg positive cases of heterophyid flukes. To confirm the adult flukes, we performed worm recovery from 12 cases after praziquantel treatment and purgation with MgSO₄. A total of 1,281 adult flukes, assigned to 7 species, were recovered from 9 cooperative cases. Heterophyes nocens (total 981 specimens) was collected from 9 cases, Stictodora fuscata (80) from 7, Gymnophalloides seoi (75) from 5, Pygidiopsis summa (140) from 3, Stellantchasmus falcatus (3) from 2, and Stictodora lari and Acanthotrema felis (each 1 worm) from 1 case each. The intrauterine eggs of S. fuscata collected from the recovered worm were identical with the larger heterophyid eggs detected in the stool examination. By the present study, it was confirmed that A. felis is a new intestinal fluke infecting humans, and residents in Muan-gun, Jeollanam-do are infected with variable species of intestinal trematodes.     

Trichuris trichiura Infection Diagnosed by Colonoscopy: Case Reports and Review of Literature

Trichuris trichiura, commonly referred to as a whipworm, has a worldwide distribution, particularly among countries with warm, humid climates. In Korea, trichuriasis was a highly prevalent soil-transmitted helminthiasis until the 1970s. However, the nationwide prevalence decreased to 0.02% in 2004 as a result of national control activities and improvement in the socioeconomic status of Koreans. Most infected individuals have no distinct symptoms, if lightly infected. The diagnosis is typically confirmed by detection of T. trichiura eggs on examination of a stool sample; few reports have described detection of the parasite during colonoscopy. Recently, we managed 4 patients with trichuriasis who were diagnosed by detection of the parasite on colonoscopy, and we reviewed the literature on the colonoscopic diagnosis of T. trichiura in Korea. We suggest that colonoscopy might be a useful diagnostic tool, especially when infected by only a few male worms with no eggs in the stool.     

Monthly Occurrence of Vectors and Reservoir Rodents of Scrub Typhus in an Endemic Area of Jeollanam-do, Korea

Monthly surveys were conducted to investigate the occurrence of chigger mites and seroprevalence of scrub typhus among small mammals in Jeollanam-do, the southwestern part of Korea, from November 2006 through October 2007. Fifty-eight small mammals, including 57 Apodemus agrarius (98.3%) and 1 Crocidura lasiura (1.7%), were captured, and a total of 4,675 chigger mites representing 4 genera and 8 species were collected from them. The chigger infestation rate among small mammals was 69.0%. The most predominant species in A. agrarius was Leptotrombidium scutellare (54.0%), followed by Leptotrombidium pallidum (39.4%), Leptotrombidium orientale (4.4%), Leptotrombidium palpale (1.1%), Neotrombicula tamiyai (0.6%), Eushoengastia koreaensis (0.3%), Neotrombicula gardellai (0.3%), and Cheladonta ikaoensis (<0.1%). The chigger index of A. agrarius was the highest in October (740.0), followed by November (242.0), September (134.6), March (98.3), February (38.2), January (35.3), December (34.5), April (30.8), and May (1.7). The average antibody positive rate of scrub typhus in wild rodents was 50.0%. The seropositive rates were high in October (100.0%) and November (83.3%), whereas those in other months were relatively low (28.6-57.1%). The chigger index of L. scutellare rapidly increased in September to form an acuminate peak in October, followed by a gradual decline. These results suggest that the outbreak of scrub typhus in the southwestern part of Korean peninsula is mostly due to L. scutellare.     

Intestinal Helminthic Infections in Striped Field Mice,Apodemus agrarius,from Two Southern Regions of Korea

The present study was performed to know the infection status of intestinal helminths in a most common species of field mice, Apodemus agrarius, from 2 southern regions of Korea. Total 133 and 103 mice were collected by the mouse trap in Hapcheon-gun, Gyeongsangnam-do and Gurye-gun, Jeollanam-do, respectively, from July 2005 to June 2006. The small intestine of each mouse was resected and longitudinally opened with a pair of scissors. The intestinal contents were washed with 0.85% saline until the supernatant became clear. Helminths were collected with naked eyes or under a stereomicroscope from the sediment of the intestinal content. More than 11 species of helminths (4 nematode spp., 5 trematode spp., and 2 cestode spp.) were recovered. Among these, heligmosomoid nematodes (97.5%) was the most highly and heavily infected species. As the members of trematodes, Plagiorchis muris, Brachylaima sp., Echinostoma hortense, Echinostoma cinetorchis, and unidentified echinostome larvae were found in the small intestines of 35 (14.8%), 12 (5.1%), 6 (2.5%), 1 (0.4%), and 1 (0.4%) mice respectively. Two species of tapeworms, Hymenolepis nana and Hymenolepis diminuta were also detected in 79 (33.5%) and 21 (8.9%) mice, respectively. Conclusively, heligmosomoid nematodes were the most prevalent (dominant) species among more than 11 helminth species detected, and Brachylaima sp. fluke is newly added in the list of intestinal trematodes in Korea.     

Sympatric Distribution of Three Human Taenia Tapeworms Collected between 1935 and 2005 in Korea

Taeniasis has been known as one of the prevalent parasitic infections in Korea. Until recently, Taenia saginata had long been considered a dominant, and widely distributed species but epidemiological profiles of human Taenia species in Korea still remain unclear. In order to better understand distribution patterns of human Taenia tapeworms in Korea, partial nucleotide sequences of mitochondrial cox1 and ITS2 (internal transcribed spacer 2) were determined, along with morphological examinations, on 68 Taenia specimens obtained from university museum collections deposited since 1935. Genomic DNA was extracted from formalin-preserved specimens. Phylogenetic relationships among the genotypes (cox1 haplotype) detected in this study were inferred using the neighbor-joining method as a tree building method. Morphological and genetic analyses identified 3 specimens as T. solium, 51 specimens as T. asiatica, and 14 specimens as T. saginata. Our results indicate that all 3 Taenia tapeworms are sympatrically distributed in Korea with T. asiatica dominating over T. saginata and T. solium.     

Strongyloides myopotami (Secernentea: Strongyloididae) from the Intestine of Feral Nutrias (Myocastor coypus) in Korea

Surveys on helminthic fauna of the nutria, Myocastor coypus, have seldom been performed in the Republic of Korea. In the present study, we describe Strongyloides myopotami (Secernentea: Strongyloididae) recovered from the small intestine of feral nutrias. Total 10 adult nutrias were captured in a wetland area in Gimhae-si (City), Gyeongsangnam-do (Province) in April 2013. They were transported to our laboratory, euthanized with ether, and necropsied. About 1,300 nematode specimens were recovered from 10 nutrias, and some of them were morphologically observed by light and scanning electron microscopies. They were 3.7-4.7 (4.0±0.36) mm in length, 0.03-0.04 (0.033) mm in width. The worm dimension and other morphological characters, including prominent lips of the vulva, blunted conical tail, straight type of the ovary, and 8-chambered stoma, were all consistent with S. myopotami. This nematode fauna is reported for the first time in Korea.     

Intestinal Parasitic Infections among Inhabitants of Karaj City, Tehran Province, Iran in 2006-2008

Karaj is an area with large influx of refugee people in Iran. To increase knowledge about parasitic infections, we carried out this research during 2006-2008. We recorded the stool examination results and some of their personal characteristics. A total of 13,915 human stools were examined, and 649 (4.7%) were positive for intestinal parasites. Among them, 13 (0.09%) had worm and 636 (4.6%) had protozoan infections. Maximum infections belonged to Giardia intestinalis, and 534 (3.8%) samples had this infection. Other parasitic infections included Entamoeba coli (0.39%), Entamoeba histolytica (0.021%), Blastocystis hominis (0.08%), Trichomonas hominis (0.1%), Iodamoeba butschlii (0.06%), Chilomastix mesnili (0.007%), Endolimax nana (0.05%), Enterobius spp. eggs (0.028%), Taenia proglottids (0.028%), and Strongyloides stercoralis larvae (0.03%). The maximum numbers of referred people to laboratories were in July and the maximum percentage of infections was in August. There is a point that all 5 Strongyloides stercoralis infections were pertained to 2008. With attention to the rate of parasitic infections (4.7%), it seems that we should take additional educational information to wide spectrum of people living in this city.     

Seasonal Distribution of Ticks in Four Habitats near the Demilitarized Zone,Gyeonggi-do (Province), Republic of Korea

This study describes the seasonal distribution of larvae, nymph, and adult life stages for 3 species of ixodid ticks collected by tick drag and sweep methods from various habitats in the Republic of Korea (ROK). Grasses less than 0.5 m in height, including herbaceous and crawling vegetation, and deciduous, conifer, and mixed forests with abundant leaf/needle litter were surveyed at United States (US) and ROK operated military training sites and privately owned lands near the demilitarized zone from April-October, 2004 and 2005. Haemaphysalis longicornis Neumann adults and nymphs were more frequently collected from April-August, while those of Haemaphysalis flava Neumann and Ixodes nipponensis Kitaoka and Saito were collected more frequently from April-July and again during October. H. longicornis was the most frequently collected tick in grass habitats (98.9%), while H. flava was more frequently collected in deciduous (60.2%) and conifer (57.4%) forest habitats. While more H. flava (54.1%) were collected in mixed forest habitats than H. longicornis (35.2%), the differences were not significant. I. nipponensis was more frequently collected from conifer (mean 8.8) compared to deciduous (3.2) and mixed (2.4) forests.     

Anisakis pegreffii Larvae in Sea Eels (Astroconger myriaster) from the South Sea,Republic of Korea

Anisakis simplex sensu stricto (s.s.), Anisakis pegreffii, Anisakis berlandi (=A. simplex sp. C), and Anisakis typica are the 4 major species of Anisakis type I larvae. In the Republic of Korea (Korea), A. pegreffii, A. berlandi, and A. typica larvae in fish hosts has seldom been documented. In this study, molecular analysis was performed on Anisakis larvae from the sea eels (Astroconger myriaster), the major source of human anisakiasis in Korea, collected from Tongyeong City, a southern coastal area of Korea. All 20 sea eels examined were infected with Anisakis type I larvae (160 larvae; 8 per fish). Their species were analyzed using PCR-RFLP patterns and nucleotide sequences of internal transcribed spacers (ITS1, 5.8 subunit gene, and ITS2) and mitochondrial cytochrome c oxidase 2 (cox2). Most (86.8%; 112/129) of the Anisakis type I larvae were A. pegreffii, and 7.8% (10/129) were A. typica. The remaining 5.4% (7/129) was not identified. Thus, A. pegreffii is the major species of anisakid larvae in sea eels of the southern coast of Korea.     

Morphologic and Genetic Identification of Diphyllobothrium nihonkaiense in Korea

Diphyllobothrium nihonkaiense was first described by Yamane in 1986 but the taxonomical features have been obscure due to lack of critical morphologic criteria in its larval and adult stages. In Korea, this tapeworm had long been known as Diphyllobothrium latum. In this study, we observed 62 specimens collected from Korean residents and analyzed them by morphological features and nucleotide sequences of mitochondrial cox1 gene as well as the ITS1 region. Adult tapeworms were examined after carmine or trichrome stain. Longitudinal sections of the gravid proglottids showed an obtuse angle of about 150 degree between the cirrus sac and seminal vesicle. This angle is known as a major differential point compared with that of D. latum. Nucleotide sequence differences between D. latum and the specimens from Koreans represented 17.3% in mitochondrial DNA cox1 gene. Sequence divergence of ITS1 among 4 Korean isolates was 0.3% and similarity was 99.7% with D. nihonkaiense and D. klebanovskii. All of the Korean specimens analyzed in this study were identified as being D. nihonkaiense (n = 62). We propose its Korean name as "Dong-hae-gin-chon-chung" which means ''long tapeworm of the East Sea'' for this newly analyzed diphyllobothriid tapeworm in Korea.     

Intestinal Nematodes from Small Mammals Captured near the Demilitarized Zone,Gyeonggi Province,Republic of Korea

A total of 1,708 small mammals (1,617 rodents and 91 soricomorphs), including Apodemus agrarius (n = 1,400), Microtus fortis (167), Crocidura lasiura (91), Mus musculus (32), Myodes (= Eothenomys) regulus (9), Micromys minutus (6), and Tscherskia (= Cricetulus) triton (3), were live-trapped at US/Republic of Korea (ROK) military training sites near the demilitarized zone (DMZ) of Paju, Pocheon, and Yeoncheon, Gyeonggi Province from December 2004 to December 2009. Small mammals were examined for their intestinal nematodes by necropsy. A total of 1,617 rodents (100%) and 91 (100%) soricomorphs were infected with at least 1 nematode species, including Nippostrongylus brasiliensis, Heligmosomoides polygyrus, Syphacia obvelata, Heterakis spumosa, Protospirura muris, Capillaria spp., Trichuris muris, Rictularia affinis, and an unidentified species. N. brasiliensis was the most common species infecting small mammals (1,060; 62.1%) followed by H. polygyrus (617; 36.1%), S. obvelata (370; 21.7%), H. spumosa (314; 18.4%), P. muris (123; 7.2%), and Capillaria spp. (59; 3.5%). Low infection rates (0.1-0.8%) were observed for T. muris, R. affinis, and an unidentified species. The number of recovered worms was highest for N. brasiliensis (21,623 worms; mean 20.4 worms/infected specimen) followed by S. obvelata (9,235; 25.0 worms), H. polygyrus (4,122; 6.7 worms), and H. spumosa (1,160; 3.7 worms). A. agrarius demonstrated the highest prevalence for N. brasiliensis (70.9%), followed by M. minutus (50.0%), T. triton (33.3%), M. fortis (28.1%), M. musculus (15.6%), C. lasiura (13.2%), and M. regulus (0%). This is the first report of nematode infections in small mammals captured near the DMZ in ROK.