Parasites, Hosts and Diseases

"Anisakis"

Brief Communication

Anisakid Larvae from Anchovies in the South Coast of Korea: Taehee Chang, Bong-Kwang Jung, Sooji Hong, Hyejoo Shin, Jeonggyu Lee, Laddawan Patarwut, Jong-Yil Chai; Korean J Parasitol 2019;57(6):699-704.
Published online December 31, 2019; DOI: https://doi.org/10.3347/kjp.2019.57.6.699

Abstract
PDF

Anisakiasis (anisakidosis) refers to a foodborne zoonosis caused by ingesting raw or undercooked marine fish or cephalopods infected with anisakid larvae. The present study was performed to investigate the prevalence of anisakid larvae in anchovies (Engraulis japonica) purchased from 2 local markets in Gyeongsangnam-do, the Republic of Korea (=Korea), during 2018-2019. Anchovies were transported to our laboratory and examined by pepsin-HCl artificial digestion technique followed by microscopic observations and molecular analyses. The overall prevalence of anisakid larvae was 19.5% (39/200), from which a total of 51 larvae (av. 1.3 larvae/infected anchovy) were recovered. Sequencing of the larvae targeting the ITS region, including ITS1, 5.8S rRNA, and ITS2 genes confirmed the species of larvae as Anisakis pegreffii (54.9%; 28/51), Hysterothylacium sinense (23.5%; 12/51), and Hysterothylacium aduncum (21.5%; 11/51). The results suggested that anchovies could be a potential source of human anisakiasis in Korea.

Citations

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Case Report

Anisakiasis: Report of 15 Gastric Cases Caused by Anisakis Type I Larvae and a Brief Review of Korean Anisakiasis Cases: Woon-Mok Sohn, Byoung-Kuk Na, Tae Hyo Kim, Tae-Joon Park; Korean J Parasitol 2015;53(4):465-470.
Published online August 25, 2015; DOI: https://doi.org/10.3347/kjp.2015.53.4.465

Abstract
PDF

The present study was performed to report 15 anisakiasis cases in Korea and to review the Korean cases reported in the literature. Total 32 Anisakis type I larvae were detected in the stomach of 15 patients by the endoscopy. Single worm was detected from 12 cases, and even 9 larvae were found from 2 cases. Epigastric pain was most commonly manifested in almost all cases, and hemoptysis and hematemesis were seen in 1 case each. Symptom manifestations began at 10-12 hr after eating fish in 73.3% cases. Endoscopy was performed 1-2 days after the symptom onset in most cases. The common conger, Conger myriaster, was the probable infection source in 7 cases. In the review of Korean anisakiasis cases, thus far, total 645 cases have been reported in 64 articles. Anisakis type I larva was the most frequently detected (81.3%). The favorable infection site of larvae was the stomach (82.4%). The common conger was the most probable source of human infections (38.6%). Among the total 404 cases which revealed the age and sex of patients, 185 (45.8%) were males, and the remaining 219 (54.2%) were female patients. The age prevalence was the highest in forties (34.7%). The seasonal prevalence was highest in winter (38.8%). By the present study, 15 cases of gastric anisakiasis are added as Korean cases, and some epidemiological characteristics of Korean anisakiasis were clarified.

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Brief Communication

Anisakis pegreffii Larvae in Sea Eels (Astroconger myriaster) from the South Sea, Republic of Korea: Jaeeun Cho, Hyemi Lim, Bong-Kwang Jung, Eun-Hee Shin, Jong-Yil Chai; Korean J Parasitol 2015;53(3):349-353.
Published online June 30, 2015; DOI: https://doi.org/10.3347/kjp.2015.53.3.349

Abstract
PDF

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.

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Molecular Identification of Anisakis Larvae Extracted by Gastrointestinal Endoscopy from Health Check-up Patients in Korea
Hyemi Song, Bong-Kwang Jung, Jaeeun Cho, Taehee Chang, Sun Huh, Jong-Yil Chai
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Anisakid Larvae from Anchovies in the South Coast of Korea
Taehee Chang, Bong-Kwang Jung, Sooji Hong, Hyejoo Shin, Jeonggyu Lee, Laddawan Patarwut, Jong-Yil Chai
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Original Articles

Molecular Analysis of Anisakis Type I Larvae in Marine Fish from Three Different Sea Areas in Korea: Woon-Mok Sohn, Jung-Mi Kang, Byoung-Kuk Na; Korean J Parasitol 2014;52(4):383-389.
Published online August 29, 2014; DOI: https://doi.org/10.3347/kjp.2014.52.4.383

Abstract
PDF

Anisakiasis, a human infection of Anisakis L3 larvae, is one of the common foodborne parasitic diseases in Korea. Studies on the identification of anisakid larvae have been performed in the country, but most of them have been focused on morphological identification of the larvae. In this study, we analyzed the molecular characteristics of 174 Anisakis type I larvae collected from 10 species of fish caught in 3 different sea areas in Korea. PCR-RFLP and sequence analyses of rDNA ITS and mtDNA cox1 revealed that the larvae showed interesting distribution patterns depending on fish species and geographical locations. Anisakis pegreffii was predominant in fish from the Yellow Sea and the South Sea. Meanwhile, both A. pegreffii and A. simplex sensu stricto (A. simplex s.str.) larvae were identified in fish from the East Sea, depending on fish species infected. These results suggested that A. pegreffii was primarily distributed in a diverse species of fish in 3 sea areas around Korea, but A. simplex s.str. was dominantly identified in Oncorhynchus spp. in the East Sea.

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Genetic analyses of Anisakis pegreffii (Nematoda: Anisakidae) from the East Asian finless porpoise Neophocaena asiaeorientalis sunameri (Cetacea: Phocoenidae) in Korean waters
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Occurrence and Molecular Identification of Anisakis Dujardin, 1845 from Marine Fish in Southern Makassar Strait, Indonesia: Hilal Anshary, Sriwulan, Mark A. Freeman, Kazuo Ogawa; Korean J Parasitol 2014;52(1):9-19.
Published online February 19, 2014; DOI: https://doi.org/10.3347/kjp.2014.52.1.9

Abstract
PDF

Anisakis spp. (Nematoda: Anisakidae) parasitize a wide range of marine animals, mammals serving as the definitive host and different fish species as intermediate or paratenic hosts. In this study, 18 fish species were investigated for Anisakis infection. Katsuwonus pelamis, Euthynnus affinis, Caranx sp., and Auxis thazard were infected with high prevalence of Anisakis type I, while Cephalopholis cyanostigma and Rastrelliger kanagurta revealed low prevalence. The mean intensity of Anisakis larvae in K. pelamis and A. thazard was 49.7 and 5.6, respectively. A total of 73 Anisakis type I larvae collected from K. pelamis and A. thazard were all identified as Anisakis typica by PCR-RFLP analysis. Five specimens of Anisakis from K. pelamis and 15 specimens from A. thazard were sequenced using ITS1-5.8S-ITS2 region and 6 specimens from A. thazard and 4 specimens from K. pelamis were sequenced in mtDNA cox2 region. Alignments of the samples in the ITS region showed 2 patterns of nucleotides. The first pattern (genotype) of Anisakis from A. thazard had 100% similarity with adult A. typica from dolphins from USA, whereas the second genotype from A. thazard and K. pelamis had 4 base pairs different in ITS1 region with adult A. typica from USA. In the mtDNA cox2 regions, Anisakis type I specimens from A. thazard and K. pelamis showed similarity range from 94% to 99% with A. typica AB517571/DQ116427. The difference of 4 bp nucleotides in ITS1 regions and divergence into 2 subgroups in mtDNA cox2 indicating the existence of A. typica sibling species in the Makassar Strait.

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Larval Anisakid Infections in Marine Fish from Three Sea Areas of the Republic of Korea: Shin-Hyeong Cho, Sang-Eun Lee, Ok-Hee Park, Byoung-Kuk Na, Woon-Mok Sohn; Korean J Parasitol 2012;50(4):295-299.
Published online November 26, 2012; DOI: https://doi.org/10.3347/kjp.2012.50.4.295

Abstract
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The present study was performed to determine the infection status of anisakid larvae in marine fish collected from 3 sea areas of the Republic of Korea. Total 86 marine fish (8 species) collected from the East Sea (Goseong-gun, Gangwon-do), 171 fish (10 species) from the South Sea (Sacheon-si, Gyeongsangnam-do), and 92 fish (7 species) from the Yellow Sea (Incheon Metropolitan City) were examined by both naked eyes and artificial digestion method. Among the total of 349 fish examined, 213 (61.0%) were infected with 8 species of anisakid larvae, i.e., Anisakis simplex, 6 types of Contracaecum spp., and Raphidascaris sp., and the mean larval density was 13.8 per infected fish. Anisakid larvae were detected in 45 fish (52.3%) from the East Sea, 131 fish (76.6%) from the South Sea, and 37 fish (40.2%) from the Yellow Sea. The average numbers of larvae detected were 4.0, 16.6, and 15.9, respectively. Anisakis simplex larvae were detected in 149 fish (42.7%), and the mean larval density was 9.0 per infected fish. They were found in 26 fish (30.2%) collected from the East Sea, 96 fish (56.1%) from the South Sea, and 27 fish (29.3%) from the Yellow Sea. The average numbers of larvae detected were 2.9, 10.3, and 10.5, respectively. Conclusively, the present study suggests that the infection rate and density of anisakid larvae are more or less higher in the fish from the South Sea than those from the East Sea or the Yellow Sea.

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Brief Communication

Expression and Characterization of α-Methylacyl CoA Racemase from Anisakis simplex Larvae: Bong Jin Kim, Sun Mi Kim, Min Kyung Cho, Hak Sun Yu, Yong Seok Lee, Hee Jae Cha, Meesun Ock; Korean J Parasitol 2012;50(2):165-171.
Published online May 24, 2012; DOI: https://doi.org/10.3347/kjp.2012.50.2.165

Abstract
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Larval excretory-secretory products of Anisakis simplex are known to cause allergic reactions in humans. A cDNA library of A. simplex 3rd-stage larvae (L3) was immunoscreened with polyclonal rabbit serum raised against A. simplex L3 excretory-secretory products to identify an antigen that elicits the immune response. One cDNA clone, designated as α-methylacyl CoA racemase (Amacr) contained a 1,412 bp cDNA transcript with a single open reading frame that encoded 418 amino acids. A. simplex Amacr showed a high degree of homology compared to Amacr orthologs from other species. Amacr mRNA was highly and constitutively expressed regardless of temperature (10-40℃) and time (24-48 hr). Immunohistochemical analysis revealed that Amacr was expressed mainly in the ventriculus of A. simplex larvae. The Amacr protein produced in large quantities from the ventriculus is probably responsible for many functions in the development and growth of A. simplex larvae.

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Original Articles

A 24 kDa Excretory-Secretory Protein of Anisakis simplex Larvae Could Elicit Allergic Airway Inflammation in Mice: Hye-Kyung Park, Min Kyoung Cho, Mi Kyung Park, Shin Ae Kang, Yun Seong Kim, Ki Uk Kim, Min Ki Lee, Mee Sun Ock, Hee Jae Cha, Hak Sun Yu; Korean J Parasitol 2011;49(4):373-380.
Published online December 16, 2011; DOI: https://doi.org/10.3347/kjp.2011.49.4.373

Abstract
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We have reported that a 24 kDa protein (22U homologous; As22U) of Anisakis simplex larvae could elicit several Th2-related chemokine gene expressions in the intestinal epithelial cell line which means that As22U may play a role as an allergen. In order to determine the contribution of As22U to allergic reactions, we treated mice with 6 times intra-nasal application of recombinant As22U (rAs22U). In the group challenged with rAs22U and ovalbumin (OVA), the number of eosinophils in the bronchial alveolar lavage fluid (BALF) was significantly increased, as compared to the group receiving only OVA. In addition, mice treated with rAs22U and OVA showed significantly increased airway hyperresponsiveness. Thus, severe inflammation around the airway and immune cell recruitment was observed in mice treated with rAs22U plus OVA. The levels of IL-4, IL-5, and IL-13 cytokines in the BALF increased significantly after treatment with rAs22U and OVA. Similarly, the levels of anti-OVA specific IgE and IgG1 increased in mice treated with rAs22U and OVA, compared to those treated only with OVA. The Gro-α (CXCL1) gene expression in mouse lung epithelial cells increased instantly after treatment with rAs22U, and allergy-specific chemokines eotaxin (CCL11) and thymus-and-activation-regulated-chemokine (CCL17) gene expressions significantly increased at 6 hr after treatment. In conclusion, rAs22U may induce airway allergic inflammation, as the result of enhanced Th2 and Th17 responses.

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Seroprevalence of Antibodies against Anisakis simplex Larvae among Health-Examined Residents in Three Hospitals of Southern Parts of Korea: Jung Kim, Jin Ok Jo, Seon Hee Choi, Min Kyoung Cho, Hak Sun Yu, Hee Jae Cha, Meesun Ock; Korean J Parasitol 2011;49(2):139-144.
Published online June 14, 2011; DOI: https://doi.org/10.3347/kjp.2011.49.2.139

Abstract
PDF

The present study was performed to estimate the seroprevalence of larval Anisakis simplex infection among the residents health-examined in 3 hospitals in southern parts of Korea. A total of 498 serum samples (1 serum per person) were collected in 3 hospitals in Busan Metropolitan city, Masan city, and Geoje city in Gyeongsangnam-do (Province) and were examined by IgE-ELISA and IgE-western blotting with larval A. simplex crude extract and excretory-secretory products (ESP). The prevalence of antibody positivity was 5.0% and 6.6% with ELISA against crude extracts and ESP, respectively. It was also revealed that infection occurred throughout all age groups and higher in females than in males. A specific protein band of 130 kDa was detected from 10 patients with western blot analysis against crude extract and ESP among those who showed positive results by ELISA. Our study showed for the first time the seroprevalence of anisakiasis in Korea. The allergen of 130 kDa can be a candidate for serologic diagnosis of anisakiasis.

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Anisakis simplex Larvae: Infection Status in Marine Fish and Cephalopods Purchased from the Cooperative Fish Market in Busan, Korea: Seon Hee Choi, Jung Kim, Jin Ok Jo, Min Kyung Cho, Hak Sun Yu, Hee Jae Cha, Mee Sun Ock; Korean J Parasitol 2011;49(1):39-44.
Published online March 18, 2011; DOI: https://doi.org/10.3347/kjp.2011.49.1.39

Abstract
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The infection status of marine fish and cephalopods with Anisakis simplex third stage larva (L3) was studied over a period of 1 year. A total of 2,537 specimens, which consisted of 40 species of fish and 3 species of cephalopods, were purchased from the Cooperative Fish Market in Busan, Korea, from August 2006 to July 2007. They were examined for A. simplex L3 from the whole body cavity, viscera, and muscles. A. simplex L3 were confirmed by light microscopy. The overall infection rate reached 34.3%, and average 17.1 larvae were parasitized per infected fish. Fish that recorded the highest infection rate was Lophiomus setigerus (100%), followed by Liparis tessellates (90%), Pleurogrammus azonus (90%), and Scomber japonicus (88.7%). The intensity of infection was the highest in Gadus macrocephalus (117.7 larvae per fish), followed by S. japonicus (103.9 larvae) and L. setigerus (54.2 larvae). Although abundance of A. simplex L3 was not seasonal in most of the fish species, 10 of the 16 selected species showed the highest abundance in February and April. A positive correlation between the intensity of L3 infection and the fish length was obvious in S. japonicus and G. macrocephalus. It was likely that A. simplex L3 are more frequently infected during the spring season in some species of fish. Our study revealed that eating raw or undercooked fish or cephalopods could still be a source of human infection with A. simplex L3 in Korea.

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Mini Review

Immune reactions and allergy in experimental anisakiasis: Sung-Weon Cho, Haneul Nari Lee; Korean J Parasitol 2006;44(4):271-283.
Published online December 20, 2006; DOI: https://doi.org/10.3347/kjp.2006.44.4.271

Abstract
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The third-stage larvae (L3) of the parasitic nematode, Anisakis simplex, have been implicated in the induction of hyperimmune allergic reactions in orally infected humans. In this work, we have conducted a review of an investigation into immune reactions occurring in animals experimentally infected with A. simplex L3. The patterns of serum antibody productions in the experimental animals against excretory-secretory products (ESP) of A. simplex L3 contributed to our current knowledge regarding specific humoral immune reactions in humans. In our review, we were able to determine that L3 infection of experimental animals may constitute a good model system for further exploration of immune mechanisms and allergy in anisakiasis of humans.

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Case Reports

Four cases of gastric submucosal mass suspected as anisakiasis: Seoung-Gu Kim, Yun-Ju Jo, Young-Sook Park, Sung-Hwan Kim, Moon-Hee Song, Han-Hyo Lee, Jeong-Seon Kim, Ji-Won Ryou, Jong-Eun Joo, Dong-Hoon Kim; Korean J Parasitol 2006;44(1):81-86.
Published online March 20, 2006; DOI: https://doi.org/10.3347/kjp.2006.44.1.81

Abstract
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Anisakiasis is a parasitic disease caused by ingestion of raw fish infected with anisakid larvae. Endoscopic changing patterns of submucosal lesions in chronic gastric anisakiasis have not been known yet. Here we report 4 cases of suspected gastric anisakiasis which were improved during follow-up periods without surgical treatment. The patients presented with abdominal pain, nausea and vomiting after consuming raw marine fish, and visited our gastroenterology outpatient department. Their endoscopic findings showed firm and yellowish submucosal masses accompanied with eccentric erosions. Histologic findings showed severe eosinophilic infiltrations. In blood tests, peripheral eosinophil counts and total IgE levels were elevated. We believed that all cases were caused by larval anisakid infections. The submucosal mass lesions disappeared during the follow-up periods of 2 to 4 mo.

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Anisakis simplexLarvae: Infection Status in Marine Fish and Cephalopods Purchased from the Cooperative Fish Market in Busan, Korea
Seon Hee Choi, Jung Kim, Jin Ok Jo, Min Kyung Cho, Hak Sun Yu, Hee Jae Cha, Mee Sun Ock
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A case of acute gastric anisakiasis provoking severe clinical problems by multiple infection: Ji Hun Noh, Bong-Jin Kim, Sun Mee Kim, Mee-Sun Ock, Moo In Park, Ja Young Goo; Korean J Parasitol 2003;41(2):97-100.
Published online June 20, 2003; DOI: https://doi.org/10.3347/kjp.2003.41.2.97

Abstract
PDF

Acute gastric anisakiasis with multiple anisakid larvae infection is reported. A 68-year-old woman residing in Busan, Korea, had epigastric pain with severe vomiting about 5 hours after eating raw anchovies. Four nematode larvae penetrating the gastric mucosae in the great curvature of the middle body and fundus were found and removed during gasteroendoscopic examination. Another one thread-like moving larva was found in the great curvature of upper body on the following day. On the basis of their morphology, the worms were identified as the 3rd stage larvae of Anisakis simplex. This case is acute gastric anisakiasis provoking severe clinical problems by the multiple infection and the greatest number of anisakid larvae found in a patient in Korea.

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Hyemi Song, Bong-Kwang Jung, Jaeeun Cho, Taehee Chang, Sun Huh, Jong-Yil Chai
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Hilal Anshary, Sriwulan, Mark A. Freeman, Kazuo Ogawa
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Anisakis simplexLarvae: Infection Status in Marine Fish and Cephalopods Purchased from the Cooperative Fish Market in Busan, Korea
Seon Hee Choi, Jung Kim, Jin Ok Jo, Min Kyung Cho, Hak Sun Yu, Hee Jae Cha, Mee Sun Ock
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A case of gastric pseudoterranoviasis in a 43-year-old man in Korea: Moon-Soo Koh, Sun Huh, Woon-Mok Sohn; Korean J Parasitol 1999;37(1):47-49.
Published online March 31, 1999; DOI: https://doi.org/10.3347/kjp.1999.37.1.47

Abstract
PDF

A case of Pseudoterranova decipiens infection was found in a 43-year-old man by gastroendoscopic examination on August 20, 1996. On August 6, 1996, he visited a local clinic, complaining of epigastric pain two days after eating raw marine fishes. Although the symptoms were relieved soon, endoscopic examination was done for differential diagnosis. A white, live nematode larva was removed from the fundus of the stomach. The larva was 38. 3×1.0 mm in size and had a cecum reaching to the mid-level of the ventriculus. A lot of transverse striations were regularly arranged on the cuticle of its body surface, but the boring tooth and mucron were not observed at both ends of the worm. The worm was identified as the 4th stage larva of P. decipiens.

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Kurt Buchmann, Foojan Mehrdana
Food and Waterborne Parasitology.2016; 4: 13. CrossRef
Mitochondrial genomes of Anisakis simplex and Contracaecum osculatum (sensu stricto) – Comparisons with selected nematodes
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Infection, Genetics and Evolution.2014; 21: 452. CrossRef
A human case of gastric infection by Pseudoterranova decipiens larva
Jae-Ran Yu, Min Seo, Young-Wook Kim, Mee-Hee Oh, Woon-Mok Sohn
The Korean Journal of Parasitology.2001; 39(2): 193. CrossRef

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Brief Communication

Intestinal Helminthic Infections Diagnosed by Colonoscopy in a Regional Hospital during 2001-2008: Do, Kyong Rock , Cho, Young Seok , Kim, Hyung Keun , Hwang, Byung Hee , Shin, Eun Jung , Jeong, Hae Bin , Kim, Sung Soo , Chae, Hiun Suk , Choi, Myung Gyu; Korean J Parasitol 2010;48(1):75-78.; DOI: https://doi.org/10.3347/kjp.2010.48.1.75

Abstract
PDF

The present study investigated characteristics of 24 parasite infection cases detected during colonoscopy in a regional hospital from January 2001 to December 2008. Sixteen patients were confirmed with Trichuris trichiura infection, 6 patients were with Ascaris lumbricoides infection, 1 patient with Enterobius vermicularis infection, and 1 patient with Anisakis infection. Among them, 7 patients (43.8%) were asymptomatic. Colonoscopy findings were normal in 18 patients (75.0%). Among the patients with T. trichiura infection, colonoscopy showed several erosions in 2 patients (8.3%) and non-specific inflammation of the affected segment of the colon in 3 patients (12.5%). In 1 patient with anisakiasis, colonoscopy revealed a markedly swollen colonic wall. Stool examinations were performed before treatment in 7 patients (29.2%) and were all negative for parasite eggs or worms. These results suggest that colonoscopy is a useful diagnostic approach for parasitic infections even for asymptomatic patients and for patients with negative stool examinations.

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