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Anisakidosis in humans and animals and detection of anisakid larvae in fish and cephalopods in Korea: a literature review (1971-2022)

Review article

Chai JY, Sohn WM, Jung BK. Anisakidosis in humans and animals and detection of anisakid larvae in fish and cephalopods in Korea: a literature review (1971-2022). Ann Clin Microbiol 2024;27:93-130.

Annals of Clinical Microbiology (Ann Clin Microbiol) 2024 June, Volume 27, Issue 2, pages 93-130. https://doi.org/10.5145/ACM.2024.27.2.6

Received on 3 April 2024, Revised on 23 April 2024, Accepted on 29 April 2024, Published on 20 June 2024.

Anisakidosis in humans and animals and detection of anisakid larvae in fish and cephalopods in Korea: a literature review (1971-2022)

1Department of Tropical Medicine and Parasitology, Seoul National University College of Medicine, Seoul2Department of Parasitology and Tropical Medicine, Gyeongsang National University College of Medicine, Jinju;3MediCheck Research Institute, Korea Association of Health Promotion, Seoul, Korea

Corresponding author: Jong-Yil Chai, E-mail: cjy@snu.ac.kr

Abstract

Human anisakiasis (or anisakidosis) is a disease caused by the ingestion of marine fish or cephalopods infected with anisakid nematode larvae of the genera Anisakis, Pseudoterranova, Contracaecum, and Hysterothylacium. Anisakiasis is a clinically important disease that often manifests as an acute abdominal syndrome requiring emergency medical attention and care. In Korea, at least several thousand clinical cases have been diagnosed to date; however, only a small proportion of them have been reported in the literature (1971-2022). The most common etiological agents were Anisakis pegreffii (reported as Anisakis sp., Anisakis type I, or erroneously Anisakis simplex), followed by Pseudoterranova decipiens, Contracaecum sp., and Anisakis simplex sensu stricto (s.s.). Most cases involved the stomach and small or large intestine, with a few involving the oral cavity (oral mucosa, pharynx, and tonsils), esophagus, omentum, and mesocolic lymph nodes. Anisakis allergies and host immune responses have been studied in humans and experimental animals. Marine fish and cephalopods, including sea eel (Astroconger myriaster), squid (Todarodes pacificus), yellow corvina (Pseudosciaena manchurica), Japanese flounder (Paralichthys olivaceus), codfish (Gadus macrocephalus), yellowtail (Seriola quinquaradiata), and rockfish (Sebastes spp.), are the most common infection sources. Surveys were performed on anisakid nematode larvae in marine fish and cephalopods caught in the western, eastern, and southern seas of Korea. The larvae recovered from fish or cephalopods caught from the western and southern seas were predominantly A. pegreffii larvae; however, the larvae from the eastern sea were either A. pegreffii larvae (in the chub mackerel, Japanese flounder, and rockfish) or A. simplex s.s. (in the salmon and pollock; these fish migrate through the northern North Pacific Ocean and Bering Sea and come to Korea). Health education to avoid eating raw or improperly cooked marine fish and cephalopods (particularly the viscera) is crucial for preventing human anisakidosis in Korea.

Keywords

Anisakis pegreffii, Anisakis simplex, Pseudoterranova decipiens, anisakidosis, Korea

Introduction

Anisakiasis, or more broadly anisakidosis (infection with anisakid nematode larvae; Anisakidae and Raphidascarididae), is a typical example of fishborne parasitic zoonoses in localities where marine fish or cephalopods are consumed raw or improperly cooked [1]. The etiological agents include species of Anisakis (A. pegreffii, A. simplex s.s., and A. physeteris), Pseudoterranova (P. decipiens s.s., P. azarasi, and P. cattani), Contracaecum (C. osculatum), and Hysterothylacium (H. aduncum) [2,3]. However, 4 species, A. pegreffii, A. simplex, P. decipiens, and P. azarasi, are most frequently involved in highly endemic countries, especially Korea and Japan [3,4]. Natural definitive hosts include dolphins, porpoises, whales, seals, and rarely, large marine fish [2]. Animal or human (accidental host) infection is caused by third-stage larvae found in the viscera or muscles of various fish and cephalopod (mollusks) species [1].

The concept of this zoonotic disease (initially called ‘herring worm disease’ or ‘codworm disease’) was f irst introduced in 1960 by van Thiel et al. [5], who reported 11 patients complaining of acute abdominal syndrome in the Netherlands, followed by Ashby et al. [6] in England in 1964, who reported 2 such patients and reviewed 89 cases possibly due to this disease. However, the diagnosis of the causative worms at this time was erroneously Eustoma rotundatum [5,6]. In 1965, Asami et al. [7] and Yokogawa and Yoshimura [8] reported similar human infections in Japan and assigned the causative worms to Anisakis-like larvae. Since then, human anisakidosis has been reported in various locations worldwide, including Japan, Korea, the Netherlands, Spain, France, Italy, Germany, England, and the USA [1,2]. To date, at least 50,000 clinical cases have been reported in these countries [1,2]. However, this is a significant underestimation of the actual situation. For example, in Japan, an average annual incidence of 19,737 anisakidosis cases was estimated from 2018 to 2019 [4], and in Spain, an annual incidence of 7,700-8,320 anisakidosis cases was estimated [9].

The most common site of anisakidosis in humans is the stomach, followed by the intestines (small and large intestines), and rarely the oral cavity, pharynx, tonsils, and esophagus [1,2]. Extra-gastrointestinal infections may also occur in rare instances, in the peritoneum, liver, lymph nodes, omentum, mesentery, pancreas, ovaries, and lungs [2]. In gastrointestinal anisakiasis, acute abdomen, nausea, vomiting, and mucosal bleeding are the most common clinical manifestations, although some cases reveal no special clinical problems, and the larvae can be incidentally found during surgery or endoscopy [2]. Diagnosis is mainly based on the recovery of anisakid larvae from the affected lesions through gastrointestinal endoscopy or surgery. In some cases, the diagnosis is made based on sectional morphologies of the larvae in histopathological specimens [2]. Serology to detect serum antibodies, for example, enzyme-linked immunosorbent assay (ELISA), and radiography, are other diagnostic methods used to diagnose acute and/or chronic anisakidosis [2]. No anthelmintic drugs have been proven to be effective in anisakidosis patients.

In Korea, human anisakidosis is common because Koreans generally prefer to eat the raw or undercooked f lesh of marine fish or cephalopods (cuttlefish, squid, and octopus). Since the first case was reported in 1971 [10], over a hundred articles have been published on clinical anisakidosis cases until 2022. The status was briefly reviewed by Sohn et al. [11] in 2015, in which 64 articles were analyzed concerning the number of cases, locality of patient occurrence, gender characteristics, source of infection (fish or cephalopods), morphological types of larvae, and predilection sites. However, since then, there has been no further review of the anisakidosis status in Korea.

Besides clinical case reports, there have been reports on the detection of anisakid larvae from marine fish and cephalopods, the occurrence of animal anisakidosis, and immunologic studies on experimental anisakidosis in animals. Thus, the present study focused on reviewing the Korean literature on human and animal anisakidosis (occurrence of clinical cases, clinicopathologic characteristics, immunity, diagnosis, and natural and experimental animal infections), as well as the status of anisakid larval infections in fish and cephalopods, larval morphology, molecular analyses, and resistance of anisakid larvae to physicochemical agents.

Literature analyzed

We searched and analyzed Korean literature on Anisakis, Pseudoterranova, anisakiasis, and anisakidosis from sources, including Google Scholar, PubMed Central, and KoreaMed. International literature to refer was also obtained from the same data sources.

Reported cases of human anisakidosis in Korea

In Korea, human anisakidosis was first reported in 1971 [10] in a patient living in Seoul complaining of a foreign body sensation and dull pain in the palatine tonsil. It was evident that these symptoms were due to infection with a larva of Anisakis sp. penetrating the palatine tonsil, which was extracted using forceps. The second case was reported in 1980 by Cho et al. [12] in a patient living in Seoul with an acute abdomen due to duodenal ulcer perforation. An anisakid larva section was incidentally found in the ileum of this patient.

By the end of 2022, at least 108 articles (including several abstracts) had been published on human anisakidosis cases in Korea (Tables 1-4) [3,10-116]. The total number of cases reported was 851, including 131 cases during 1971-1990, 225 cases during 1991-2000, 229 cases during 2001-2010, and 268 cases during 2011-2022, which demonstrated a chronologically increasing trend (Fig. 1). Seropositive cases were excluded if anisakid larvae were not parasitologically confirmed [117-120]. In addition, an increasing number of anisakiasis cases were reported from 2011 to 2018 in Korea based on big data analysis of Health Insurance Review Assessment claims [121]. According to this article, the annual number of anisakiasis cases registered in the Korean Health Insurance Database (2011-2018) was 333-818, including 409 cases in 2011, 333 cases in 2012, 359 cases in 2013, 409 cases in 2014, 450 cases in 2015, 491 cases in 2016, 685 cases in 2017, and 818 cases in 2018, totaling 3,954 cases during the 8 years (avg. 494 cases/year) [121]. Therefore, at least 800 cases of human anisakidosis occur annually in the Korean population. However, most of these cases were not officially reported in scientific publications (it is also uncertain whether these cases were parasitologically proven) and thus were not included in the clinical case analyses of this review.

Table 1. Case reports of anisakidosis from 1971 to 1990 in Korea

Study (yr)No. of casesOrgan (s) involvedLarva identifiedLocality of case (s)
Kim et al. (1971) [10]1Platine tonsilAnisakis sp.Seoul
Cho et al. (1980) [12]1IleumAnisakis sp.Seoul
Lee et al. (1981) [13]5StomachAnisakis sp.Busan
Chung et al. (1983) [14]27StomachAnisakis sp.Busan
Paik et al. (1984) [15]1IleumAnisakis sp.Seoul
Seo et al. (1984) [16]1IleumTerranova type AIncheon
Jeong and Suk (1984) [17]1StomachAnisakis sp.Busan
Lee et al. (1985) [18]1StomachTerranova type AIncheon
Lee et al. (1986) [19]4StomachAnisakis sp.Daegu
Yun and Whang (1987) [20]1IleumAnisakis sp.Daegu
Kim et al. (1987) [21]7StomachAnisakis sp.Daegu
Chi et al. (1988) [22]*3?Anisakis sp.?
Yang et al. (1988) [23]3StomachAnisakis sp.Gwangju
Ko et al. (1988) [24]3Ileum (2), colon (1)Anisakis sp.Jinju
Han et al. (1988) [25]6Stomach (2), ileum (4)Anisakis sp.Pohang
Ahn et al. (1988) [26]1StomachAnisakis sp.?
Jang et al. (1989) [27]12StomachAnisakis sp.Pohang
Jin et al. (1989) [28]1StomachAnisakis sp.Wonju
Lee HS et al. (1989) [29]3StomachAnisakis sp.Chuncheon
Lee MS et al. (1989) [30]1IleumAnisakis sp.Seoul
Choi et al. (1989) [31]5StomachAnisakis sp.Seoul
Jung et al. (1990) [32]1IleumAnisakis sp.Pohang
Park et al. (1990) [33]1IleumAnisakis sp.Suwon
Im et al. (1990) [34]39StomachAnisakis type I (13)
Terranova type A (1)
Contracaecum sp. (2)
Unknown (23)
Jeju
Subtotal129Stomach (111),
intestine (14),
tonsil (1),
unknown (3)
Anisakis sp. (88),
Anisakis type I (13),
Terranova type A (3),
Contracaecum sp. (2),
Unknown (23)
Jeju (39), Busan (33),
Pohang (19), Daegu (12),
Seoul (9), Gwangju (3),
Chuncheon (3), inju (3),
Incheon (2), Wonju (1),
Suwon (1), Unknown (4)

Only scientific reports (including abstracts) dealing with anisakidosis cases were included. Diagnosis based only on serological tests were excluded. *They reported 4 anisakiasis cases but 1 of them was previously reported by Cho et al. [12].

Table 2. Case reports of anisakidosis from 1991 to 2000 in Korea

Study (yr)No. of casesOrgan (s) involvedLarva identifiedLocality of case (s)
Im and Shin (1991) [35]3StomachTerranova type AJeju (2), Seoul (1)
Kim SE et al. (1991) [36]9StomachAnisakis sp.Seoul
Kim LS et al. (1991) [37]1JejunumAnisakis sp.Seoul
Sohn et al. (1991) [38]2StomachAnisakis type IBusan
Shin et al. (1992) [39]1IleumAnisakis sp.Seoul
Lee SH et al. (1993) [40]1StomachAnisakis sp.Busan
Lee HS et al. (1993) [41]1StomachAnisakis sp.Daejeon
Kim et al. (1994) [42]1Greater omentum?Gwangju
Sohn and Seol (1994a) [43]1StomachPseudoterranova decipiensBusan
Sohn and Seol (1994b) [44]1DuodenumAnisakis type IBusan
Seol et al. (1994) [45]20StomachAnisakis type IBusan
Im et al. (1995) [46]107StomachAnisakis simplex (82),
Anisakis type II (5),
Pseudoterranova decipiens (2),
Contracaecum type A (1),
Unknown (17)
Jeju
Shim et al. (1995) [47]2IleumAnisakis sp.Daegu
Cho et al. (1996) [48]7StomachAnisakis sp.Gwangmyeong
Geum et al. (1997) [49]6Stomach (5), duodenum (1)Anisakis sp.Daegu
Kim et al. (1997) [50]1Mesocolic lymphnodeAnisakis sp.Seoul
Cho et al. (1998) [51]1StomachAnisakis sp. (?)Seoul
Guahk et al. (1998) [52]1StomachAnisakis sp.Seoul
Yoon et al. (1998) [53]1Stomach?Gwangju
Lee et al. (1998) [54]1StomachPseudoterranova decipiensGwangmyeong
Koh et al. (1999) [55]1StomachPseudoterranova decipiensChuncheon
Song et al. (1999) [56]39StomachAnisakis type I (27),
Anisakis type II (3),
Pseudoterranova sp. (1),
Unknown (8)
Incheon
Ahn et al. (1999) [57]1StomachAnisakis sp.Seoul
Park CY et al. (1999) [58]1Stomach?Seoul
Kang et al. (1999) [59]2StomachAnisakis sp.Seoul
Park TG et al. (1999) [60]1EsophagusAnisakis sp.Pohang
Choi et al. (2000) [61]2StomachPseudoterranova decipiensSeoul
Chung et al. (2000) [62]10Stomach (2),
small intestine (8)
Anisakis sp.Gwangju
Subtotal225Stomach (208),
intestine (14),
lymph node (1),
omentum (1),
esophagus (1)
Anisakis sp. (45),
Anisakis type I (50),
Anisakis type II (8),
Anisakis simplex (82),
Pseudoterranova sp. (11),
Contracaecum sp. (1),
Unknown (28)
Jeju (109), Incheon (39),
Busan (25), Seoul (21),
Gwangju (12), Daegu (8),
Gwangmyeong (8), Daejeon (1),
Chuncheon (1), Pohang (1)

Only scientific reports dealing with anisakidosis cases (excluding serological tests) were included in this table.

Table 3. Case reports of anisakidosis from 2001 to 2010 in Korea

Study (yr)No. of casesOrgan (s) involvedLarva identifiedLocality of case (s)
Yu et al. (2001) [63]1StomachPseudoterranova decipiensChungju
Yeum et al (2002) [64]1PeritoneumAnisakis simplexJeju
Hwang et al. (2002) [65]3Esophagus??
Choi et al. (2003) [66]1StomachAnisakis sp.Busan
Lim et al. (2003) [67]1StomachAnisakis type IChuncheon
Noh et al. (2003) [68]1StomachAnisakis simplexBusan
Yoon et al. (2004) [69]1Small intestineAnisakis sp.Sungnam
Suh et al. (2004) [70]1Ascending colonAnisakis sp.Seoul
Woo et al. (2004) [71]1Ascending colonAnisakis simplexSeoul
Kwon et al. (2004) [72]1StomachAnisakis sp.Seoul
Kim et al. (2004) [73]1Stomach, ileum,
transverse colon
Anisakis sp.Sooncheon
Song et al. (2004) [74]27Stomach (?)Anisakis sp. (21)
P. decipiens (6)
Seoul
Suh et al. (2005) [75]1StomachAnisakis sp.Seoul
Shin et al. (2006) [76]1Transverse colonAnisakis simplexSeoul
Park SW et al. (2006) [77]3StomachAnisakis sp.Gwangju
Kim YH et al. (2006) [78]3ColonAnisakis sp.Seocheon
Park JY et al. (2006) [79]1Oral cavity, tongueAnisakis type IGangneung
Kim JH et al. (2006) [80]2Stomach (1), esophagus (2)Anisakis sp.Busan
Cho et al. (2006) [81]2CecumAnisakis sp.Iksan
Jang et al. (2006) [82]1RectumAnisakis sp.Daejeon
Kim SH et al. (2006) [83]1StomachAnisakis sp.Jeju
Kim SG et al. (2006) [84]4Stomach?Seoul
Shin et al. (2007) [85]1EsophagusAnisakis sp.Jeonju
Yoo et al. (2008) [86]1Ascending colonAnisakis sp.Seoul
Lee et al. (2008) [87]1IleumAnisakis sp.Busan
Choi et al. (2008) [88]1Ascending colonAnisakis sp.Gwangju
Cho et al. (2009) [89]1Stomach, colonAnisakis sp.Gangneung
Lee et al. (2009) [90]141StomachAnisakis sp.Jinju
Hong et al. (2009) [91]1DuodenumAnisakis sp.Seoul
Choi et al. (2009) [92]10???
Choi et al. (2010) [93]11Stomach (10),
ascending colon (1)
?Seoul
Do et al. (2010) [94]1Ascending colonAnisakis sp.Uijeongbu
Kang et al. (2010) [95]1JejunumAnisakis sp.Iksan
Subtotal229Stomach (195),
intestine (19),
esophagus (6),
oral cavity (1),
peritoneum (1),
unknown (10)
Anisakis sp. (188),
Anisakis type I (2),
Anisakis simplex (4),
Pseudoterranova sp. (7),
Unknown (28)
Jinju (141), Seoul (49),
Busan (5), Gwangju (4),
Iksan (3), Seocheon (3),
Jeju (2), Gangneung (2),
Sungnam (1), Daejeon (1),
Chuncheon (1), Suncheon (1),
Uijeongbu (1), Chungju (1),
Jeonju (1), Unknown (13)

Only scientific reports dealing with anisakidosis cases (including abstracts), excluding serological tests, were included in this table.

Table 4. Case reports of anisakidosis from 2011 to 2022 in Korea

Study (yr)No. of casesOrgan (s) involvedLarva identifiedLocality of case (s)
Kim et al. (2011) [96]4Small intestineAnisakis sp.Seoul
Hwang et al (2012) [97]1DuodenumAnisakis sp.Gwangju
Cho et al. (2012) [98]1Stomach, colonAnisakis sp.Gangneung
Kim et al. (2012) [99]1StomachAnisakis sp.Jeju
Na et al. (2013) [100]1StomachPseudoterranova decipiensCheonan
Yoon et al. (2013) [101]1IleumAnisakis sp.Gwangju
Kim T et al. (2013) [102]59Stomach (29),
small intestine (30)
Anisakis sp.Jeju
Kim SH et al. (2013) [103]1Stomach, colonAnisakis sp.Daejeon
Choi et al. (2014) [104]62StomachAnisakis sp. (52),
Pseudoterranova decipiens (10)
Seoul
Lee et al. (2014) [105]19Small intestineAnisakis sp.Jeju
Kang et al. (2014) [106]1StomachAnisakis sp.Iksan
Sohn et al. (2015) [11]15StomachAnisakis type IJinju
Lim et al. (2015) [107]16StomachAnisakis pegreffii (15)*,
Anisakis simplex (1)
Around Seoul
Choi et al. (2017) [108]1Oral mucosaAnisakis sp.Cheongju
Park et al. (2018) [109]28StomachAnisakis sp.Busan
Kim et al. (2018) [110]1IleumAnisakis sp.Busan
Choi et al. (2019) [111]1ColonAnisakis simplexIncheon
Joo et al. (2019) [112]20ColonAnisakis sp.Seoul
Song et al. (2019) [113]20Stomach (19), colon (1)Anisakis pegreffii*Various localities
Jeong and Ahn (2020) [114]1EsophagusAnisakis sp.Seoul
Joo et al. (2021) [115]1StomachAnisakis sp.Busan
Cha et al. (2022) [116]1Palatine tonsilAnisakis sp.Daegu
Song et al. (2022) [3]12Stomach (11), colon (1)Pseudoterranova decipiensVarious localities
Subtotal268Stomach (184),
intestine (81),
esophagus (1),
oral mucosa (1),
tonsil (1)
Anisakis sp. (193),
Anisakis type I (15),
Anisakis simplex (2),
Anisakis pegreffii (35),
Pseudoterranova decipiens (23)
Seoul (103), Jeju (79),
Busan (30), Jinju (15),
wangju (2), Incheon (1),
Daegu (1), Iksan (1),
Gangneung (1), Daejeon (1),
Cheongju (1), Cheonan (1),
Unknown (32)

Only scientific reports dealing with anisakidosis cases (including abstracts and excluding serological tests) were included in this table. *Molecular studies were performed to identify the species anisakid nematodes involved.

Fig. 1. Number of anisakidosis cases reported in scientific articles in Korea (1971-2022).
Geographic locality of cases

The geographic locations where anisakidosis cases were reported in Korea were variable, including Jeju (229 cases; 26.9%), Seoul (182; 21.4%), Jinju (159; 18.7%), Busan (93; 10.9%), Incheon (42; 4.9%), Gwangju (21; 2.5%), Daegu (21; 2.5%), Pohang (20; 2.4%) and other cities (Fig. 2). A strong trend was observed for cases to be more commonly diagnosed in coastal areas than in inland areas. In addition, the frequency of reports seemed to depend on the number of medical facilities available in each area.

Fig. 2. Number of anisakidosis cases according to localities in Korea (1971-2022).
Source of infection

The possible sources of infection (fish or cephalopod dishes) were mentioned in most articles (Table 5). Of the 851 anisakidosis patients, approximately a quarter (25.4%) stated that they had eaten undefined or mixed f ish dishes (over 2 kinds of fish). The next most common source of infection was sea eel (19.9%), followed by squid (5.2%), yellow corvina (4.2%), Japanese flounder or flatfish (3.4%), codfish (2.6%), yellowtail (1.6%), and rockfish (1.4%) (Table 5). Anchovy, seabream, skate, and shad were the next most common dishes consumed by patients with anisakidosis in Korea (Table 5). It is of special note that approximately 1/5 of the cases involved the consumption of raw or undercooked sea eels. Considering that mixed fish dishes frequently include sea eel, the number of cases associated with sea eel consumption would increase to over 1/3 of all cases. A significant concern related to this is that anisakid larvae are commonly found in the muscles of sea eel, whereas larvae are generally found in the viscera and abdominal cavity of most other types of marine fish [122-126]. Therefore, if the sea eel muscle is consumed raw, it could be possible to be infected with anisakid larvae that are frequently found alive in the muscles of this fish.

Table 5. Marine fish, cephalopods, or other marine food dishes consumed by anisakidosis patients in Korea (1971-2022)

Kinds of dish (Korean name of fish)No. of patients (%)
Mixed fish dish* or undefined marine fish (모듬회, 생선회)216 (25.4)
Sea eel (Conger myriaster or others) (붕장어)169 (19.9)
Squid (Todarodes pacificus and others) (오징어류)044 (5.2)
Yellow corvina (Pseudosciaena manchurica) (조기)036 (4.2)
Flounder (Paralichthys olivaceus or others) (광어, 넙치, 도다리)029 (3.4)
Codfish (Gadus macrocephalus or others) (대구)022 (2.6)
Yellowtail (Seriola quinqueradiata) (방어)014 (1.6)
Rockfish (Sebastes spp.) (우럭) 012 (1.4)
Anchovy (Engraulis japonicus or others) (멸치)008 (0.9)
Seabream (Acanthopagrus schlegeli and others) (도미)006 (0.7)
Skate (Raja porosa and others) (홍어, 간재미)004 (0.5)
Shad (Konosirus punctatus) (전어)003 (0.4)
Others (miscellaneous fish) (기타 생선류 또는 낙지)019 (2.2)
No. of cases without mentioning the source269 (31.6)
Total851 (100.0)

*Cases stating that they consumed more than 2 kinds of fish or cephalopods were included in this group.

Site of infection

Among the 851 cases analyzed in this review, the most frequently involved organs were the stomach (698 cases; 82.0%) followed by the small and large intestines (88 and 40 cases, respectively, 128 cases in total; 15.0%), esophagus (8 cases; 0.9%), tonsils (2 cases; 0.2%), oral cavity/oral mucosa (2 cases; 0.2%), mesocolic lymph nodes (1 case; 0.1%), greater omentum (1 case; 0.1%), peritoneum (1 case; 0.1%), and unknown location (15 cases; 1.8%) (Fig. 3). The involvement of multiple organs, more than 2 of the stomach, ileum, and colon, has been reported in 5 cases [73,80,89,98,103].

Fig. 3. Involved organs in 851 anisakidosis cases reported in Korea (1971-2022).
Species of anisakid larvae in human patients

Regarding the types (or species) of anisakid larvae detected, most of the reports simply described that the worms were anisakid larvae or Anisakis sp. larvae (514; 60.4%). The larvae were designated as Anisakis type I (A. pegreffii or A. simplex larvae) in 80 cases (9.4%), A. simplex larvae in 88 cases (10.3%), and Anisakis type II (probably A. physeteris) in 8 cases (0.9%). Thus, the overall number of cases reported as Anisakis spp. (including type I, type II, A. pegreffii, and A. simplex) was 724 (85.2%). However, molecular analyses of larvae extracted from human infections using the internal transcribed spacer (ITS) region sequences were first reported by Lim et al. [107], and 25 of 26 larvae extracted from 15 cases were confirmed to be A. pegreffii, and only 1 larva (1 case) was A. simplex s.s. Subsequently, Song et al. [113] identified 20 additional human cases of A. pegreffii infection through molecular analyses. Thereby, a total of 35 (4.1%) patients were confirmed to be infected with A. pegreffii. Based on these molecular findings, it is highly likely that the species of anisakid larvae responsible for human infections in Korea is predominantly A. pegreffii. Regarding P. decipiens s.s. (or Terranova type A larvae) infections, 44 cases (5.2%) were reported through morphological and/or molecular analyses. Three cases (0.4%) were caused by Contracaecum spp. or Contracaecum type A larvae [34,46]. The larvae were not identified in 79 patients (9.3%).

Different types of larvae appear to have distinct clinical features, such as affected organs or sites of infection. Of the 725 patients infected with Anisakis sp. larvae (including Anisakis sp., Anisakis type I, Anisakis type II, A. pegreffii, or A. simplex s.s.), 591 (81.5%) had infections in the stomach, 88 (12.1%) in the small intestine (duodenum, jejunum, ileum, or cecum), and 38 (5.2%) in the large intestine (ascending, transverse, descending colon or rectum). However, out of 44 cases infected with P. decipiens s.s. (or Terranova type A) larvae, 42 (95.5%) developed gastric infections, and the remaining 2 (4.5%) had 1 ileal and 1 colonic infection. These results agree with the higher potential of P. decipiens larvae to cause gastric infections than Anisakis spp. larvae. [1].

In Korea, most previous anisakidosis cases in which the extracted larvae were assigned to Anisakis sp. or Anisakis type I larvae might have been A. pegreffii infections; and only a small proportion might have been A. simplex s.s. infections. This trend is different from that in Japan, where 168 (88.9%) of 189 larvae obtained from human patients were molecularly confirmed to be A. simplex s.s., and only a few were A. pegreffii (10 larvae; 5.3%) and P. azarasi (11 larvae; 5.8%) [4]. However, the relative proportion of causative larval species differed according to the localities in Japan; for example, on Kyushu Island (adjacent to South Korea), 33.3% of the patients were infected with A. pegreffii larvae (other 66.7% were infected with A. simplex s.s. larvae), whereas in Hokkaido Island, Honshu, and Shikoku Islands (distant from South Korea), only 4.1%-6.7% of the patients were infected with A. pegreffii larvae [4]. This difference was presumed to be due to differences in larval anisakid distribution in fish caught from the Pacific Ocean, East Sea (Sea of Japan), and Yellow Sea (East China Sea) [4,107,122]. A. simplex s.s. larvae were more commonly detected in fish caught from Hokkaido and eastern Japan than A. pegreffii larvae, whereas in fish from Kyushu and Fukuoka (close to South Korea), A. pegreffii larvae were more frequently detected than A. simplex s.s. larvae [122].

Number of larvae recovered in each case

The number of anisakid larvae detected in each patient was 1 in most cases, but rarely 2-4 larvae were detected [34,56,90,99]. However, more worms were detected on rare occasions. For example, 9 specimens were detected in 2 gastric patients from Jinju [107], and 15 worms in 1 gastric patient from Seoul [107]. Of special note were 2 patients with oral cavity infections, in which over 8 and 20 larvae, respectively, were extracted using forceps; both patients had eaten raw squids [79,108]. Moreover, in an extreme case, 51 larvae were collected from the stomach of a single patient, and 3 months after the removal of these larvae by endoscopy, submucosal tumors were again found in the stomach and transverse colon which were suggested to be due to anisakid larval infections that were not removed at the time of surgery [98].

Clinical features in Korean patients

The chief complaint or major clinical feature of anisakidosis patients (n = 851) in Korea was acute abdomen (including acute epigastric pain) or acute abdominal syndrome, which was observed in 59.9% of all patients (Table 6). The next frequent clinical symptom was nausea and vomiting which was recorded in 11.6% of patients, followed by chronic gastritis or gastric pain (3.6%), intestinal obstruction, ileus, or adhesion (2.6%), diarrhea (1.9%), urticaria and/or edema (1.2%), hematemesis and/or melena (1.1%), esophageal symptoms (0.9%), and intestinal inflammation, including appendicitis (0.6%) (Table 6). Extraintestinal anisakidosis was very rare, having been reported in 7 cases, involving the oral mucosa (2 cases), tonsils (2 cases), greater omentum (1 case), mesocolic lymph nodes (1 case), and peritoneum (1 case). Notably, a considerable proportion of cases (5.3%) were asymptomatic or found incidentally during health check-ups, including endoscopy, in people who had mild gastrointestinal discomfort (Table 6). Cases with over 2 chief complaints comprised 2.4%, and symptoms and signs were not described in 7.9% of the patients.

The clinical features of Korean gastric anisakidosis cases have been reviewed several times [11,34,46,56,90]. Im et al. [34] reported that the most common clinical complaint of gastric anisakidosis among the 39 cases analyzed was sudden onset or intermittent epigastric pain (31; 79.5%), followed by nausea and vomiting (8; 20.5%). Song et al. [56] analyzed the clinical symptoms of 39 gastric anisakidosis patients and found that the most frequent symptoms were epigastric pain (34 cases; 87.2%) and epigastric discomfort (31; 79.5%), followed by nausea and vomiting (18; 46.2%), diarrhea (1; 2.6%), headache (1; 2.6%), and chest pain (1; 2.6%). Lee et al. [90] reported that the most common symptoms in 141 anisakidosis patients were acute epigastric pain (121 cases; 85.8%), followed by nausea and vomiting (40; 28.4%), mild epigastric discomfort (7; 5.0%), and hematemesis/melena (2; 1.4%). Sohn et al. [11] analyzed 15 gastric anisakidosis cases and reported that epigastric pain (14 cases; 93.3%) was the most common followed by nausea and vomiting (5; 33.3%), hematemesis (1; 6.7%), and hemoptysis (1; 6.7%).

Among intestinal anisakidosis cases (n = 128), the most common symptom was acute abdominal pain (including acute epigastric pain) (60 cases; 46.9%), followed by intestinal obstruction, adhesion, or intussusception (23; 18.0%), nausea and vomiting (19; 14.8%), diarrhea (14; 10.9%), asymptomatic or incidental finding (12; 9.4%), intestinal inflammation (5; 3.9%), and others (3; 2.3%). Esophageal anisakidosis was 8 cases [60,65,80,85,114], and the most common clinical complaint was acute epigastric pain (7 cases; 87.5%), followed by nausea and vomiting (2; 25.0%), chest pain (1; 12.5%), and epigastric fullness (1; 12.5%). In 2 oral mucosa cases [79,108], oral or substernal pain was the chief complaint, and in 2 tonsil cases, sore throat, foreign body sensation, and/or dull pain around the pharynx were the major clinical complaints.

Table 6. Clinical symptoms and signs of anisakidosis patients in Korea (1971-2022)

Chief complaints/major signs No. of patients (%)
Acute abdomen, epigastric pain510 (59.9)
Nausea and/or vomiting099 (11.6)
Chronic gastritis, chronic gastric pain031 (3.6)
Intestinal obstruction, ileus, intussusception, adhesion022 (2.6)
Diarrhea016 (1.9)
Urticaria, edema012 (1.4)
Hematemesis, melena009 (1.1)
Esophageal involvement008 (0.9)
Submucosal tumor005 (0.6)
Duodenitis, jejunitis, ileitis, appendicitis005 (0.6)
Oropharyngeal/tonsil involvement004 (0.5)
Asymptomatic/health check-up/incidentally045 (5.3)
Multiple symptoms or miscellaneous types of symptoms*020 (2.4)
Unknown067 (7.9)
Total851 (100.0)

*More than 2 kinds of symptoms or miscellaneous symptoms, including chest pain, fever, and others.

Anisakis allergy

Anisakiasis is often associated with a strong allergic response involving an elevated immunoglobulin (Ig), particularly IgE, in response to A. simplex or A. pegreffii, with clinical symptoms ranging from isolated swelling to generalized urticaria and life-threatening anaphylactic reactions several hours (or 24-36 hours) after ingestion of raw or undercooked fish [1,127-129]. Skin symptoms (especially urticaria) were the most frequent (almost 100% of patients with allergies), followed by digestive symptoms (74%) [129]. Anisakis associated hypersensitivity reactions have been reported particularly in northern Spain [128] but are also known in France, Italy, Portugal, and Japan [128,130]. Genetic predisposition (HLA class II alleles) has been observed in patients with Anisakis allergies [128]. A. simplex is the dominant species implicated in human allergic responses in Spain and other countries; however, A. pegrefii has also been identified as a causative agent in Italy [131,132]. The allergenic potential of P. decipiens has been suggested by several researchers and several P. decipiens allergens have been shown to have proteins homologous to A. simplex; however, further studies are required [133].

In Korea, at least 4 articles have reported allergic reactions due to anisakidosis [83,92,99,134]. The first allergic case was a 33-year-old woman residing in Jeju who complained of repeated episodes of urticaria with severe itching, stomachache, nausea, and vomiting a few hours after eating raw fish. The skin prick test and specific IgE test were positive for Anisakis somatic and excretory-secretory antigens [83]. Subsequently, 10 allergic patients complaining of urticaria (100%), abdominal pain (30%), and anaphylactic reactions (30%) were reported. High serum IgE levels were detected against A. simplex antigens in these patients [92]. On Jeju Island, a 47-year-old male patient complained of generalized urticaria, angioedema, abdominal pain, and dyspnea, and his serum revealed a strongly positive level of Anisakis-specific IgE [99]. Another study on Jeju Island included 15 additional gastroallergic patients positive for Anisakis-specific IgE with clinical complaints of urticaria, abdominal pain, angioedema, nausea, and vomiting [134]. We believe that most of these allergic cases involved infections with A. pegreffii, although the specific diagnosis of the involved larvae was not confirmed in these cases.

Immunological studies on Anisakis allergy

Recurrent anaphylaxis due to A. simplex larva infection was first reported by Audicana et al. [135] in Spain. Now it has been well established that acute allergic symptoms, such as urticaria, angioedema, or anaphylaxis, accompanied by epigastric pain, nausea, and vomiting, called gastroallergic anisakiasis, are elicited by live (not dead or heat-inactivated) third-stage larvae of A. simplex and A. pegreffii [136]. This hypersensitivity reaction is often accompanied by an acute IgE-mediated generalized reaction with cutaneous (urticaria to angioedema) and/or respiratory (asthma and rhinitis) symptoms [136]. IgE bound to mast cells or basophils recognizes specific allergens, and degranulation of these cells leads to local and/or systemic allergic reactions [136]. IgE-producing parasite-derived antigens have been isolated and characterized, including Ani s 1 through Ani s 14, which are somatic antigens, excretory-secretory products (ESP), or of unknown origin [137]. Major allergens, as defined by the recognition of > 50% of sensitized individuals, were 5 kinds, including Ani s 1 (ESP; similar to thermostable serine protease inhibitors), Ani s 2 (somatic antigen; paramyosin), Ani s 7 (ESP; function unknown), Ani s 12 (origin and function unknown), and Ani s 13 (ESP; hemoglobin) [136,137]. Ani s 1 and Ani s 7 have high allergenic potential and no cross-reactivity with other allergens, whereas Ani s 2 is a pan-allergen with cross-reactivity with other foods or inhalant allergens [137].

In Korea, Cho and coworkers [138-142] performed immunological and serological studies on anisakiasis in experimental animals and humans. Kim et al. [138] found that the ESP of A. simplex third-stage larvae (L3) contained important allergens (12 low-molecular-weight bands ranging from 10 to 186 kDa by immunoblotting) necessary to induce Anisakis allergy in rats. In human anisakiasis, the binding patterns of L3-specific antibodies varied depending on the different L3-ESP preparations, and low-molecular-weight proteins appeared to be strong and specific antigens [139]. Choi et al. [140] reported high serum titers of IgG4 and IgE antibodies in 4 of 9 Anisakis allergy patients in Korea. Cho et al. [141] demonstrated that allergic responses induced by L3 oral infection were predominantly caused by reinfection rather than primary infection, accompanied by elevated IgE and IgM levels. The role of specific IgG, especially IgG4, has also been suggested in immune responses to intraperitoneally injected L3, as IgG4 binds to epitopes recognized by specific IgE [143]. In human anisakidosis, the importance of specific IgA has been suggested; however, its role has not been demonstrated in experimental mice and rats [139,142].

Choi et al. [143] reported that A. pegreffii larval extract induced airway inflammation and asthma 4 weeks after the challenge, enhancing the expression of Th2-type immune responses (IL-4, IL-5, and IL-13) in the lungs of mice. Conversely, Park et al. [144] cloned a macrophage migration inhibitory factor (MIF)-like protein from L3 of A. simplex. This MIF-like protein was shown to reduce Th2-related cytokines in the bronchoalveolar lavage fluid and allergen-specific IgG2a in the sera of mice, which is probably associated with host immune modulation. Treg cells were recruited to the spleen and lungs of these MIF-treated mice [144]. Park et al. [145] identified a 24 kDa protein from the ESP of A. simplex larvae as a possible allergen, homologous to the 22U protein of filarial nematodes and distinct from the Ani s 1 antigen, although having the same molecular weight. Park et al. [146] performed repeated intranasal applications of recombinant 22U of A. simplex 6 times and found that this antigen induces airway allergic inflammation accompanied by enhanced lung Th2 and Th17 responses. Kim et al. [147] isolated and characterized an α-methylacetyl CoA racemase originating from the ventriculus of A. simplex larvae, which may have a function in the growth and development of the larvae. Jeon et al. [148] compared the hydrolase activities (esterases, peptidases, proteases, and glycosidases) of ESP and the somatic proteins of A. simplex and A. pegreffii larvae collected from salmon in Yangyang (Namdae Stream) and mackerels in the southern sea of Korea, respectively. Cho et al. [149] studied the allergenicity of Ani s 1 (major antigen) and Ani s 9 (minor antigen) by repeated intranasal inoculation into mice and observed airway inflammation in mice with significantly elevated lung Th2 and Th17 cytokine responses. An interesting study by Cha and Ock [150] demonstrated that antigenic proteins from A. simplex larvae could change cytokine profiles and prevent drug-induced Crohn’s disease in experimental mice.

Relationships between anisakidosis and gastrointestinal cancers

A relationship between chronic anisakid nematode infection and stomach or colon cancers has been suggested [151-154]. Some clinical cases have shown the co-localization of anisakidosis and cancer in the gastrointestinal tract [155,156]. Garcia-Perez et al. [151] provided data showing an epidemiological link between previous Anisakis infections and gastrointestinal cancer. In addition, products from Anisakis were shown to cause inflammation and DNA damage in the host [152], and the complete extract of Anisakis worms could induce changes in epithelial cells in vitro and in vivo (rats) [153]. However, in Korea, only 1 case of the co-existence of ascending colon anisakiasis and sigmoid colon cancer has been reported [86]. It is noteworthy that whereas carcinogenic stimuli should continue for a long time to undergo a neoplastic transformation of the mucosal tissues of the stomach or colon, most anisakidosis cases are detected in the acute stage, and the disease does not continue for a long time. Notably, in experimental anisakiasis in rabbits, the pathological lesions almost completely resolved in the submucosa of the stomach within 5 months after infection, and the worms were calcified, became tiny, and encircled by fibrous tissues infiltrated by inflammatory cells [157]. However, attention should be paid to patients who are repeatedly infected with anisakid nematodes because in such cases mucosal changes in the stomach and/or colon may persist for a considerably long time.

Experimental anisakiasis in laboratory animals

Studies of experimental anisakiasis in laboratory animals (regarding susceptibility, habitat, and pathology/ histopathology) have been reported in at least 3 articles in Korea. Kwon and Chyu [158] observed the distribution of anisakid larvae in 2 experimental rabbits after oral inoculation with 30 L3 from day 2 to 14 post-infection (PI). On days 2-3 PI, a total of 42 larvae (live) were recovered in the stomach (33 larvae), omentum (8), and mesentery (1), and on days 7-14 PI, only 7 larvae (dead) were detected in the abscess cavity (6) and fundus submucosa (1) of the stomach wall [158]. Choi and Kim [159] infected rats and rabbits with Anisakis L3 and chronologically observed the distribution of the larvae within 1 day (rats) and during days 1-14 PI (rabbits); in rats, 1 larva penetrated the stomach wall within 1 hour PI, and a total of 4 larvae were found in the stomach wall by 8 hours PI, while some larvae were found in the omentum, intestinal wall, abdominal cavity, and liver within 24 hours PI. In rabbits, 22 larvae penetrated the stomach wall within 1 day, and some larvae were found in the omentum, intestinal wall, abdominal cavity, and mesentery during days 3-14 PI [159]. Hong and Lee [157] observed larval locations and gross and histopathologic findings in the stomach, small intestine, colon, and mesentery from day 13 to day 150 PI; on day 13 PI, larvae were found in the stomach (15 of 60 larvae inoculated), omentum (1), intestine (2), mesentery (5), and abdominal wall (2), and on day 90 PI, larvae were found in the stomach (12 of 60 larvae inoculated), omentum (3), intestine (2), mesentery (1), and abdominal wall (1). Only 1 larva was detected on day 150 PI in the stomach wall of a rabbit [157]. The involved tissues showed severe histopathological changes, including granuloma formation, inflammatory cell infiltrations, fibrosis, and calcification until day 90 PI, and only a few sections of tiny, calcified larvae were detected in the submucosal layer of the stomach on day 150 PI [157]. Jeon and Kim [160] performed in vitro (agar block plates) and in vivo (rats) experiments on the pathogenic potential of 2 sibling species, A. simplex and A. pegreffii, and found that A. pegreffii had higher penetration ability (in vitro) and longer survival time in rats (in vivo) than A. simplex.

Anisakid larva or adult infection in pigs, cats, and birds in Korea

Anisakis type I larva infection was found in the stomachs of 9 (2.8%) of 318 pigs in Andong, Gyeongsangbuk-do [161], and 11 (0.7%) of 1,531 pigs in Jeollanam-do [162]. One or 2 larvae [161] or 1-9 larvae [162] were observed in each case. Serological tests for swine anisakiasis were performed using indirect hemagglutination and gel diffusion tests [163]. Two studies were performed on the infection of cats with Anisakis sp. larvae; 1 (11.1%) of 9 autopsied cats in Seoul was found to be infected with a total of 14 A. simplex larvae penetrating the stomach [164], and 1 (0.2%) of 438 cats in Busan had A. simplex L3 infection [165]. It is worth mentioning that adult nematodes of Contracaecum rudolphii complex were recovered in the proventriculus of a white pelican (Palecanus onccrotalus) that was imported from Tanzania to Korea [166].

Anisakid larva or adult infection in a porpoise and a whale in Korea

A finless porpoise was stranded on the coast of Jeju Island with adhesive bowel disease (ABD), which is life-threatening, and nematode parasites, including Anisakis sp. larvae and Crassicauda sp., were found at autopsy. The primary cause of ABD is presumed to be a reaction related to these parasitic infections [167]. The first detection of A. simplex s.s. adult nematodes (n = 2) containing eggs was reported by Kim et al. [168] in the gastrointestinal tract of a common minke whale (Balaenoptera acutorostrata Lacépède, 1804) that died in the sea between Namhae and Bangeojin, Korea. The diagnosis was molecularly confirmed using the gene sequences of the mitochondrial cytochrome c oxidase 2 (cox2) [168].

Survey of anisakid larvae in marine fish and cephalopods in Korea

The first detection of anisakid larvae in marine fish in Korea was reported by Chun et al. [169] in 1968 (Table 7). A total of 313 fish specimens (17 species) caught from the western (Yellow Sea) and southern seas were examined, and 312 (99.7%) were found to be infected with anisakid larvae (1-334 larvae per fish) [169]. The next study was reported by Lim [170]; a total of 1,940 fish specimens (15 species) were purchased from 5 localities (caught from western and southern seas) in Korea, and the average number of anisakid larvae per f ish ranged from 0.2 (damselfish; Chromis notata) to 156.0 (yellow corvina; P. manchurica). The third study was a morphological analysis of anisakid larvae collected from the yellow corvina caught in the western sea; a total of 1,026 identifiable anisakid larvae were collected from 30 fish, and Anisakis type I was the most common (859 larvae; 80.4%) followed by Contracaecum type Dʹ (77; 7.2%), Contracaecum type C′ (55; 5.1%), Contracaecum type D (18; 1.7%), Contracaecum type A (13; 1.2%), Contracaecum type V (3; 0.28%), and Raphidascaris sp. (1; 0.09%) [123].

Thereafter, at least 19 studies reported anisakid larval infections in fish and cephalopods in the vicinity of Korean seawater [171-189]. Eight studies that examined more than 7 species of fish or cephalopods are presented in Table 7 [125,169,170,171,177,178,182,183]. Among the 99 species of fish/cephalopods examined, 82 were infected with anisakid larvae (mostly Anisakis spp.) (Table 7). The major (positive in over 3 studies) infected fish/cephalopods were 15 species, including sea eel (C. myriaster), chub mackerel (Scomber japonicus), hairtail (Trichiurus lepturus), anchovy (Engraulis japonicus), silver pomfret (Pampus argenteus), yellow corvina (P. manchurica), yellowtail (Seriola quinqueradiata), jack mackerel (Trachurus japonicus), white croaker (Argyrosomus argentatus), herring (Clupea palassii), red seabream (Pagrus major), Japanese flounder (P. olivaceus), flathead (Platycephalus indicus), rockfish (Sebastes inermis), and Japanese common squid (T. pacificus) (Table 7). The reason why chub mackerels are not ranked among the 12 most common fish consumed by human patients in Korea (Table 5) seems to be that mackerels are less frequently consumed raw by the Korean people.

In addition, chum salmon (Oncorhynchus keta) purchased from the eastern coastal areas (Taep’o Port in Sokcho City and Namdae Stream in Yangyang, Gangwon-do) were examined in 3 studies; the infection rate was 100%, with the mean number of larvae per fish ranging from 28.9 to 108.0 [172,179,181]. Masu salmon (Oncorhynchus masou masou) purchased from the eastern part (Joomunjin) of Gangwon-do were also examined, and the recovered larvae were molecularly identified as A. simplex s.s. L3 by polymerase chain reaction-based restriction fragment length polymorphism (PCR-RFLP) analysis [180]. Sea eels (C. myriaster) were studied 5 more times in Korea; Chai et al. [124] examined 26 sea eels purchased from the Noryangjin Fish Market in Seoul, and among them, 15 (57.5%) were positive for anisakid larvae (90.1 larvae/fish), including Anisakis type I (564/1,351 larvae; 41.7%) followed by Contracaecum spp. (787/1,351; 58.3%). Song and Hwang [126] examined 382 sea eels purchased from Busan, of which 259 (67.8%) were infected with 1,768 anisakid larvae (Anisakis spp. and Contracaecum spp.). Cho et al. [183] examined 20 sea eels caught in Tongyeong City, Gyeongsangnam-do, and recovered 129 Anisakis type I larvae; these larvae were molecularly analyzed using PCR-RFLP and sequencing of the ITS region and cox2 genes, and 112 (86.8%) were confirmed to be A. pegreffii, 10 (7.8%) were Anisakis typica, and 7 (5.4%) were unidentified [183]. Lee et al. [186] examined sea eels (C. myriaster), chub mackerels (S. japonicus), and hairtails (T. lepturus) from the seawater of Korea and performed molecular analyses (PCR-RFLP) on the larvae; 136 (97.1%) of 140 larvae were A. pegreffii, and the remaining 4 (2.9%) were A. typica. Neves [188] also examined sea eels (C. myriaster), chub mackerels (S. japonicus), and yellow croakers (Larimichthys polyactis) caught from the western, southern, and eastern coasts of Korea to detect anisakid larvae. Bak et al. [184] caught chub mackerels from the western, southern, and eastern coasts of Korea and examined them for anisakid larvae; 231 (55.4%) of the 417 mackerels were positive, with a total number of larvae of 1,628 (7.0 larvae/fish). Molecular studies (PCR-RFLP of ITS and sequencing of cox2) of these larvae revealed that most of them were A. pegreffii (94.3%), and small proportions were A. simplex s.s. (0.4%), a hybrid of A. pegreffii and A. simplex (2.5%), or Hysterothylacium sp. (2.8%) [184].

Jeong and Song [176] examined yellow corvina (P. manchurica) (n = 551) purchased from seawater around Jeju Island and recovered 4,386 larvae (8.5 larvae/fish) comprising 3,428 Anisakis type I larvae and 958 Contracaecum spp. larvae. Anchovies were examined in 2 more studies [174,189] in addition to the 4 studies in Table 7 [170,171,177,182]; Song et al. [174] purchased a total of 2,180 anchovies (E. japonica) from the eastern and southern seas and 171 (7.8%) were found to be infected with anisakid larvae (Anisakis type I or II, Anisakis sp., and Contracaecum type B or type C). Chang et al. [189] purchased anchovies from the southern sea and found anisakid larvae in 39 (19.5%) of 200 specimens (51 larvae in total; 1.3/ fish); molecular analyses using ITS gene sequences revealed that 28 larvae were A. pegreffii, 12 were Hysterothylacium sinense, and 11 were H. aduncum. The large-head hairtail (T. japonicus) (n = 9) purchased from Jeju Island was examined for anisakid larvae (1,259; 139.9/fish) using PCR-RFLP of ITS and cox2 sequencing; A. pegreffii larvae (1,243/1,259; 98.7%) were most commonly detected, followed by a hybrid of A. pegreffii and A. simplex s.s. (6/1,259; 0.5%), Hysterothylacium sp. larvae (2/1,259; 0.2%), and unknown species (8/1,259; 0.5%) [187]. Regarding a squid species (T. pacificus), 1 more study was available [175] in addition to 3 studies shown in Table 7 [125,177,182]; 272 squids purchased from Busan (southern sea) were examined, and Anisakis type I, type II, Contracaecum types A and D larvae were recovered.

There may be questions about the possibility of anisakid larval infection in cultured marine fish. As fish farms are usually located near coastal areas, remote from the sea where whales and other sea mammals thrive, and within the farm there seems to be no infected first intermediate host (shrimp-like crustaceans) with anisakid larvae, cultured fish can be regarded to be safe from anisakid larval infection.

Table 7. Species of marine fish examined for anisakid larvae* in Korea (1968-2012)†

Species of fish/cephalopodsKorean common nameChun et al. (1968) [169]Lim (1975) [170]Kim et al. (1988) [171]Woo and Kim (2000) [125]Song et al. (2001) [177]Choi et al. (2009) [178]Choi et al. (2011) [182]Cho et al. (2012) [183]
Locality surveyedWest/ South SeaWest/South seaFish market in SeoulJeju IslandSouth SeaEast/South/West SeasFish market in BusanEast/South/West Sea
Acanthopagrus schlegeli감성돔
Apogon lineatus열동가리돔
Arctoscopus japonicus도루묵
Argyrosomus argentatus보구치
Bodianus oxycephalus사랑놀래기
Branchiostegus japonicus옥돔
Chelidonichthys sp.성대
Chromis notata자리돔
Clupea palassii 청어
Clyptocephalus stellari기름가자미
Cololobis saira꽁치
Conger myriaster붕장어
Cynoglossus semilaevis박대
Ditrema temminckii망상어
Doederleinia beycoides눈볼대
Doryteuthis kensaki한치
Enchelyopus gilli동가시치
Engraulis japonicus멸치
Epinephephelus akaara붉바리
Eptatretus burgeri먹장어
Erispex potti풀미역치
Evynnis japonica붉돔
Gadus macrocephalus대구
Hemiamphus sajori자치어
Hemitripterus villosus삼세기
Hertklotsichthys zunasi밴댕이
Hexagrammos grammus 노래미
Hexagrammos otakii쥐노래미
Hippoglossoides pinetorum용가자미
Ilisha elongata준치
Johnius grypotus민태
Konosirus punctatus전어
Larimichthys crocea참조기
Lateolabrax japonicus농어
Lateolabrax maculatus점농어
Lepidotrigla microptera달강어
Limanda herzensteini 참가자미
Liparis tanakai꼼치
Liparis tesselatus물메기
Loligo bleekeri화살꼴뚜기
Loligo chinensis한치꼴뚜기
Loligo edulis창꼴뚜기
Lophiomus setigerus 아귀
Miichthys miiuy민어
Mugil cephalus숭어
Muraenesox cinereus갯장어
Neoditrema ransonneti인상어
Nibea albiflora수조기
Niphon spinosis다금바리
Octopus minor variabilis낙지
Oncorhynchus masou masou산천어
Oplegnathus fasciatus돌돔
Pagrus major참돔
Pampus argenteus병어
Pampus echinogaster덕대
Paralichthy olivaceus넙치(광어)
Parapristipama trilineatum벤자리
Platycephalus indicus양태
Platyrhina sinensis목탁가오리
Pleurogrammus azonus임연수어
Pleuronectes yohohamae문치가자미
Pleuronichthys cornutus도다리
Priachanthus macrachanthus홍치
Psenopsis anomala샛돔
Pseudolabrus japonicus황놀래기
Pseudosciaena crocea부세
Pseudosciaena manchurica조기
Raja porosa간재미
Saurida undosquamis메퉁이
Scomber japonicus고등어
Scomberomorus niphonius삼치
Scombrops boops 게르치
Scorpaenodes littoralis쏨벵이
Sebastes hubbsi 우럭볼락
Sebastes inermis볼락
Sebastes longispinis흰꼬리볼락
Sebastes pachycephalus우럭
Sebastes schlegeli조피볼락
Sebastes thompsoni불볼락
Sebastiscus marmoratus쏨뱅이
Semicossyphus reticulatus흑돔
Sepia esculenta참갑오징어
Seriola quinqueradiata방어
Silago sihama보리멸
Sparus swinhonis감정돔
Sphyraena pinguis 꼬치고기
Stephanolepis cirrhifer쥐치
Stromateoides argenteus병어
Takifugu chinensis복어
Takifugu niphobles복섬
Takifugu pardalis졸복
Tanakius kitaharai갈가자미
Thamnaconus modestus말쥐치
Theragra chalcogramma명태
Todarodes pacificus살오징어
Trachurus japonicus전갱이
Trichiurus lepturus갈치
Xystrias gregorjewi물가자미
Zoarces gilli등가시치

positive for anisakid larvae; negative for anisakid larvae. *Anisakid larvae recovered were mostly Anisakis type I (A. pegreffii or A. simplex) followed by Contracaecum type A, B, C, C′, D, D′ (probably Contracaecum osculatum for all these types), Contracaecum type V or others, Terranova type A (P. decipiens) or type B (P. decipiens), Raphidascaris sp., and very rarely Anisakis type II (A. physeteris). Only studies which examined more than 7 species of fish were included in this table.

Morphological studies of anisakid larvae in Korea

Various morphological types of anisakid larvae have been reported since the reports by Yamaguti [190], Berland [191], and Koyama et al. [192]. Anisakis type I (A. pegreffii, A. simplex, and A. typica) and type II larvae (A. physeteris) were named by Berland [191]; Contracaecum types I through V by Yamaguti [190]; and Terranova types A (P. decipiens), B (P. decipiens), Contracaecum types A through D (C. osculatum), and Raphidascaris sp. by Koyama et al. [192]. In Korea, Chai et al. [123,124] found variants of Contracaecum types A, C, and D larvae in sea eel and yellow corvina, which were named Contracaecum types A′, C′, and D′, respectively.

Studies on anisakid larvae in fish from Korea started in 1966 but were officially reported in 1968 by Chun et al. [169]. Anisakis type I larvae (as Anisakis sp.) were detected in marine fish from the western and southern seas. Since then, several articles have been published regarding the morphology of anisakid larvae found in Korea. Rim [193] described the morphology of Anisakis type I larvae obtained from marine fish and swine in Gwangju, South Korea. Kim et al. [171,172] detected Anisakis type I; Terranova type B; Contracaecum types A, B, and D; and Raphidascaris sp. larvae in marine fish purchased from fish markets in Seoul and Sokcho (Gangwon-do). Woo and Kim [125] detected Anisakis types I and II, Terranova types A and B, Contracaecum types A, B, C, and D, and Raphidascaris sp. larvae in marine fish purchased from Jeju Island. Sohn and Lee [194] and Sohn [195] observed the sectional morphologies of Anisakis type I, Contracaecum type A, and type D’ larvae by light and transmission electron microscopies. Chai et al. [196] studied the morphologies (light microscopic, sectional, and scanning electron microscopic) of P. decipiens larvae detected from the codfish (Notothenia neglecta) caught in the Antarctic Ocean near the South Pole.

Serological studies on human and animal anisakidosis

Hong and Lee [157] studied the changing patterns of IgG in experimental rabbit anisakiasis for 150 days PI. IgG levels started to increase from day 3 PI, peaked on day 30 PI, maintained a plateau during days 30-90 PI, and then decreased to almost control levels on day 150 PI [157]. The serological diagnosis of human anisakidosis patients in Korea was first reported by Lee et al. [197], who used ELISA on 12 parasiteconfirmed anisakidosis cases and observed significantly elevated optical density values in 11 of the 12 patients (0.229-1.547 in 12 patients vs 0.103-0.353 in 5 controls). They also performed immunoblotting on sera from humans and experimental rabbits and found that the 46 kDa L3 antigen was highly sensitive and specific for Anisakis infection [197]. Quan et al. [198] compared different types of antigens used in ELISA for anisakiasis in rabbits and found that ESP was the most suitable antigen. Yang et al. [199] performed ELISA and immunoblotting to observe the changing patterns of serum IgM and IgG in experimental rabbits and detected at least 41 reactive bands; IgM reacted to 7 bands and IgG reacted to 8 bands. Choi et al. [200] observed the antibody responses of experimental rabbits infected with A. simplex L3 using ELISA and immunoblotting; serum IgG began to increase at days 7-9 PI, reached their maximum levels by days 1215 PI, and then decreased, while serum IgM began to increase from day 5 to 7 PI, reached a peak at day 12 PI, and then decreased. Significantly elevated levels of total and L3-specific IgE were observed in 10 gastroallergic patients [92]. However, serum IgM levels have not been studied in human anisakiasis patients in Korea and require further investigation.

Rim et al. [201] performed a seroepidemiological study using ELISA for 6 major parasitic diseases in 6,074 individuals selected from several localities in Korea. The number of anisakiasis-seropositive cases was 495 (8.1%) and varied by locality; it was higher in the southern areas of Jeollanam-do (16.9%) and some parts of Gyeongsangbuk-do (10.6%) than in other localities. Kim et al. [202] detected 33 seropositive cases by ELISA against A. simplex L3 ESP antigen in 498 health-examined people in 3 hospitals from southern parts of Korea; the allergen of 130 kDa could be a candidate for the serodiagnosis of anisakiasis. Chung and Lee [134] reported that 14 out of 17 patients with suspected gastroallergic anisakiasis on Jeju Island were strongly positive for Anisakis-specific IgE.

Molecular studies and predominance of A. pegreffii larvae in fish, cephalopods, and humans in Korea

In Korea, molecular studies of anisakid larvae were initiated by Kim et al. [203] in 2006 who analyzed the complete mitochondrial genome of A. simplex L3 from sea eel (C. myriaster). Thereafter, at least 23 studies were performed on the molecular genetic characteristics of anisakid larvae from Korean seawater [147,178,180,181,184-189,203-215]. Yu et al. [204] analyzed the cDNA library of A. simplex L3 and detected 493 expressed sequence tags (ESTs), including 21 ESTs that matched previously reported A. simplex genes or proteins in addition to many other EST clones related to cell functions and worm growth and development.

Subsequently, the PCR-RFLP technique was applied to detect anisakid larvae in several fish species caught in Korean seawater [205-207]. Kang et al. [205] molecularly analyzed anisakid larvae from marine fish and squids caught in Korean seawater using PCR-RFLP of the ITS gene and found that they were larvae of A. pegreffii. Lee et al. [206] also molecularly confirmed that most larvae from Korean sea-fish were A. pegreffii (47 of 60 larvae), and small proportions were A. typica (10 larvae), A. simplex s.s. (1 larva), and a hybrid of A. pegreffii and A. simplex (2 larvae). Choi et al. [178] performed molecular studies (18S ribosomal DNA; 18S rDNA) on 10 Anisakis type I larvae recovered from marine fish in Korean seawater, and the larvae demonstrated high identity with A. pegreffii. Park et al. [208] molecularly analyzed 45 anisakid larvae collected from rockfish (S. schlegeli) from the western sea and identified 3 species, which included A. simplex (17 larvae), A. pegreffii (4 larvae), and Hysterothylacium sp. (24 larvae). Kim et al. [209] molecularly analyzed 26 anisakid larvae from fish in the southern sea and found that A. pegreffii was the most common (17 larvae) followed by H. aduncum (2 larvae), Hysterothylacium fabri (1 larva), Raphidascaris lophii (1 larva), and hybrid forms (5 larvae). However, Jeon et al. [180] and Setyobudi et al. [181] reported that the anisakid larvae from masou salmon (O. masou masou) and chum salmon (O. keta), respectively, from the eastern sea analyzed by PCR-RFLP of the ITS region and cox2 gene were A. simplex s.s. Subsequently, this discrepancy was well explained by Setyobudi et al. [210] that A. pegreffii larvae were distributed mainly in the southern (90.7% of all anisakid larvae detected) and western seas (98.9% of all larvae detected) but less in the eastern sea of Korea based on molecular analyses of larvae collected from common squids (T. pacificus). A similar but interesting finding was observed by Sohn et al. [211]; all 48 larvae from 3 species of fish from the Yellow Sea (western sea) were A. pegreffii, whereas 79 of 80 anisakid larvae from 7 species of fish from the southern sea were A. pegreffii, and only 1 larva was A. simplex s.s. In f ish from the eastern sea, the species of anisakid larvae were different depending on the species of fish; the larvae detected in Japanese flounder (P. olivaceus) and rockfish (S. schlegeli) were all A. pegreffii, whereas those found in 2 species of salmon (O. masou masou and O. keta) were determined to be A. simplex s.s. [211]. Salmon fish are considered to have been infected by anisakid larvae when they migrate from the east coast of Korea through Hokkaido (Japan), the northern North Pacific Ocean, and the Bering Sea. Similar features were observed in the distribution of A. pegreffii and A. simplex s.s. larvae in chub mackerel (S. japonicus) caught from the eastern, southern, and western seas [184], and it seemed that A. pegreffii is the dominant species in Korean chub mackerels which are mainly caught from the Tsushima Current stock, whereas Japanese chub mackerels are 2 stocks and harbor 2 kinds of larvae; A. pegreffii in the Tsushima Current stock and A. simplex s.s. in the Pacific Current stock.

The predominance of A. pegreffii larvae was repeatedly observed in different fish species collected from the western and southern seawater of Korea (Fig. 4); sea eel (C. myriaster) [185,186,188], Pacific cod (Gadus macrocephalus) [212], chub mackerel (S. japonicus) [186,188], hairtail (T. lepturus) [186], large-head hairtail (Trichiurus japonicus) [187], yellow croaker (L. polyactis) [188], and anchovy (E. japonica) [189]. Nurhidayat et al. [213] examined walleye pollock (G. chalcogrammus) caught from the East Sea of Korea and found that 73.5% of the anisakids were A. simplex; only 1.4% were A. pegreffii (Fig. 4). Walleye pollock inhabits cold and deep-water columns and is abundant in the northern North Pacific Ocean (Pacific Current) and the Bering Sea [213]. In addition, the predominance of A. simplex larvae in chum salmon caught from the East Sea (Namdae Stream, Yangyang) of Korea was confirmed by Kim et al. [214], who performed comparative transcriptome analyses of the larvae. Kim et al. [215] developed a new genetic technique to discriminate the species of anisakid larvae collected from Korean seawater and the amplification-refractory mutation system (ARMS) was found to be effective in discriminating A. pegreffii, A. simplex, and their hybrids.

In human infections in Korea, specific molecular diagnosis of anisakid larvae has been performed in 3 studies [3,107,113]. Lim et al. [107] performed molecular analyses of 26 larvae extracted from human infections using ITS region sequences, and the larvae from 15 (25 larvae) of 16 cases were confirmed to be A. pegreffii, while the larva from only 1 case (1 larva) was A. simplex s.s. Song et al. [113] performed molecular analyses of anisakid larvae from 20 human cases (health check-up patients) and confirmed that all of them were infected with A. pegreffii. Molecular studies of Pseudoterranova sp. larvae were performed in only 1 study by Song et al. [3]; 12 larvae collected from 12 human cases in Korea were analyzed using sequences of the mitochondrial cox1 and nd1 genes, all of which were confirmed to be P. decipiens s.s. larvae.

Fig. 4. Species of anisakid larvae detected in humans (nationwide, mostly from Seoul) and fish/ squids from the eastern, southern, and western seas of Korea based on molecular analyses [3,107,113,178,180,181,184-189,205-213]. Av, anchovy; Cm, chub mackerel; Cs, chub salmon; Jf, Japanese flounder; Gl, greenling; H, human; Ht, hairtail; Lh, large-head hairtail; Ms, masou salmon; Pc, Pacific cod; Rf, rockfish; Se, sea eel; Sq, squid; Vf, various fish; Wp, walleye pollock.
Resistance of anisakid larvae against physicochemical stimuli, including anthelmintics

In Korea, it has been shown that anisakid larvae are highly resistant to various physicochemical stimuli, including temperature (high and low), chemical substance (salinity, acidity, alcohol, and others), irradiation, ultrasound, hydrostatic pressure, and anthelmintic drugs [170,216-224]. Lee and Chyu [216] reported that anisakid larvae survived 1, 4, 6, 3, and > 30 hours at -20℃, -15℃, -10℃, -5℃, and 0℃, respectively, and were killed when stored at 30% saline for 17 hours, 20% saline for 2 days, and 10% saline for 5 days; however, some (17%-19%) larvae lived > 10 days at 0.85% or 5% saline. In addition, anisakid larvae survived < 1 hour at 20% acetic acid, < 24 hours at 10% acetic acid, < 10 days at 5% acetic acid, < 2 days at 40% ethanol, < 3 days at 20% ethanol, and < 6 days at 10% ethanol. The larvae were highly resistant to variable concentrations of soy sauce, Japanese soy sauce, mustard, and Japanese mustard (wasabi) surviving 1 day or longer [216]. Lim [170] reported similar results. Chai et al. [217] observed high radioresistance of anisakid larvae; they demonstrated active movements even after irradiation with a surprisingly high dose of 10,000 Gy, although their infectivity to experimental rats and rabbits decreased considerably. This radioresistance was suggested to be due to the role of superoxide dismutase [218]. Jeon and Jee [219] studied the inhibitory effects of ivermectin, doramectin, and ethanol in vitro and found that ivermectin and ethanol had some effect on the migration and movement of anisakid larvae, whereas doramectin had no effect. However, the inhibitory effects of ivermectin were lower in vivo in experimental rats [220]. Herbal extracts (Meliae ezadarach, Dryopteris crassirhizoma, and Quisqualis indica var. villosa) have been tested for their inhibitory effects in vitro against anisakid larvae [221]; however, the in vivo effects need to be determined. Oh et al. [222] studied the effects of freezing, salting, and combined treatment with chlorine and ultrasound on anisakid larvae inoculated in salt-fermented squid and pollock tripe; all larvae were inactivated after 48 hours at -20℃ and 24 hours at -40℃. The viability of the larvae was 81.7% and 26.7% in 5% and 10% saline solutions, respectively, after 7 days of storage, and all larvae were inactivated when submerged in 15% saline for 7 days or in 20% saline for 6 days of storage [222]. The viability of the larvae (isolated from the f ish) was significantly reduced after combined treatment with low concentrations (< 2,000 ppm) of chlorine and ultrasound for 5-30 min; however, this combined treatment exerted no effects on the viability of the larvae located within the viscera of heavily infected sea eels [222]. Lee et al. [223] examined the effect of high hydrostatic pressure (HHP) on the viability of anisakid larvae in the flesh of sea eels and found that HHP at 200 MPa for 5 min could be used as a potential measure for the inactivation of anisakid larvae in f ish without changes in color and sensory quality of the fish. Nam et al. [224] observed the larvicidal effects of various food condiments, including soybean sauce, Japanese mustard, vinegar, red pepper paste, saline solution, ethanol, and soju (Korean liquor); all these exhibited significant effects after several hours, but L3 is exposed to these condiments only for seconds before ingestion, so these conditions cannot be used to prevent anisakid larval infections.

Ethics statement

This was not a human population study; therefore, approval by the institutional review board and informed consent were not required.

Conflicts of interest

We have no conflict of interest related to this review.

Acknowledgments

We acknowledge all Korean authors who reported the clinical cases of human and animal anisakidosis between 1971 and 2022. We also appreciate the dedicated works, including molecular studies, on the detection of anisakid larvae in marine fish and cephalopods caught near the western, southern, and eastern seas of Korea.

Funding

None.

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209. Kim WS, Jeon CH, Kim JH, Kim DH, Oh MJ. Current status of anisakid nematode larvae infection in marine fishes caught from the coastal area of Korea between 2010 and 2012. J Fish Pathol 2012;25:189-97. 

210. Setyobudi E, Jeon CH, Choi K, Lee SI, Lee CI, Kim JH. Molecular identification of anisakid nematodes third stage larvae isolated from common squid (Todarodes pacificus) in Korea. Ocean Sci J 2013;48:197-205. 

211. Sohn WM, Kang JM, Na BK. Molecular analysis of Anisakis type I larvae in marine fish from three different sea areas in Korea. Korean j Parasitol 2014;52:383-9.   

212. Jeon CH, Setyobudi E, Kim JH. Occurrence and molecular identification of anisakid nematodes isolated from pacific cod (Gadus microcephalus) caught off Korea. Food Contr 2016;69:100-7. 

213. Nurhidayat SW, Nam UH, Kim JH. Occurrence of anisakid nematodes in Walleye pollock (Gadus chalcogrammus) caught off the East Sea of Korea: their molecular identification and biological implication. Ocean Sci J 2018;53:679-89. 

214. Kim JH, Kim JO, Jeon CH, Nam UH, Subramaniyam S, Yoo SI, et al. Comparative transcriptome analyses of the third and fourth stage larvae of Anisakis simplex (Nematoda: Anisakidae). Mol Biochem Parasitol 2018;226:24-33.  

215. Kim HS, Baek KW, Park MK, Jeon KY, Ko EJ, Cha HJ, et al. Establishment and validation of ARMS (amplification-refractory mutation system) for identification of Anisakis species collected from Korean waters. Gene 2019;691:125-31.  

216. Lee WH, Chyu I. Experiments on the resistance and infectivity of Anisakis larvae. J Catholic Med Coll 1970;18:229-37.

217. Chai JY, Hong ST, Lee SH. Effects of gamma irradiation on the survival and infectivity of Anisakis larvae. Final research co-ordinating meeting on use of irradiation to control infectivity of food-borne parasites; 1993. Mexico City; Joint FAO/IAEA Division of Neclear Techniques in Food and Agriculture; 1993. p 43-8.

218. Seo M, Kho BM, Guk SM, Lee SH, Chai JY. Radioresistance of Anisakis simplex third-stage larvae and the possible role of superoxide dismutase. J Parasitol 2006;92:416-8.  

219. Jeon JH and Jee CH. Larval migration inhibition activity of ivermectin, doramectin and ethanol against Anisakis simplex in vitro. Korean J Vet Res 2007;47:197-202.

220. Lee SH and Jee CH. Effect of ivermectin and doramectin for larval (Anisakis sp.) migratory inhibition in rats. Korean J Vet Serv 31:93-100.

221. Kwon HN and Jee CH. Inhibitory effects of herbal extracts (Meliae ezadarach, Dryopteris crassirhizoma, Quisqualis indica var villosa) on larval migration of Anisakis spp. in vitro. Korean J Vet Res 2008;48:473-80.

222. Oh SR, Zhang CY, Kim TI, Hong SJ, Ju IS, Lee SH, et al. Inactivation of Anisakis larvae in salt-fermented squid and pollock tripe by freezing, salting, and combined treatment with chlorine and ultrasound. Food Contr 2014;40:46-9. 

223. Lee KH, Park SY, Ha SD. Inactivation of Anisakis simplex L3 in the flesh of white spotted conger (Conger myriaster) by high hydrostatic pressure and its effect on quality. Food Addit Contaminants (Part A) 2016;33:1010-5.  

224. Nam UH, Lee SY, Lee JH, Kim JH. Survival of Anisakis species larvae of chub mackerel (Scomber japonicus) in different kinds of condiments. J Fish Pathol 2021;34:249-53.

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18. Lee AH, Kim SM, Choi KY. A case of human infection with the larva of Terranova type A. Korean J Pathol 1985;19:463-7.

19. Lee CY, Lee MH, Hong KW. Four cases of gastric anisakiasis found in Taegu, Korea. Korean J Med Technologists 1986;18:171-6.

20. Yun YK and Whang IW. Eosinophilic gastroenteritis associated with a larval anisakine infestation. Kyungpook Univ Med J 1987;28:224-7.

21. Kim PY, Chung MK, Lee HJ, Kim CS. Clinical review of acute gastric anisakiasis. Youngnam Univ Med J 1987;4:43-7.

22. Chi JG, Sung RH, Cho SY. Tissue parasitic diseases in Korea. J Korean Med Sci 1988;3:51-62.

23. Yang DH, Cho JK, Yoon CM, Suh SP, Kim SJ, Lim YK, et al. Anisakis. Korean J Gastrointest Endosc 1988;8:133-6.

24. Ko GH, Park CK, Kong HJ, Choi CS, Lee SH, Hong SJ. Intestinal anisakiasis. Korean J Pathol 1988;22:154-8.

25. Han DS, Han YB, Park MI, Kim SH, Kim SS. Clinical study of anisakiasis. J Korean Med Assoc 1988;31:645-50.

26. Ahn MH, Min DY, Jung HC, Lee GY. Human infection caused by a larva of Anisakis sp. Korean J Parasitol 1988;26:309.

27. Jang GL, Chung JY, Kim WK, Kim KS, Kim JG. Clinical observation of 12 cases of gastric anisakiasis. Korean J Intern Med 1989;37:403-10.

28. Jin SY, Jung SH, Kim TS. Acute gastric anisakiasis. Korean J Pathol 1989;23:149-53.

29. Lee HS, Kim SJ, Rim KS, Suh JE, Kang JO. Three cases of acute gastric anisakiasis. Human Sci 1989;13:413-6.

30. Lee MS, Cho SW, Kim JH, Cho SW, Shim CS, Moon C, et al. Ileal anisakiasis: a case report. Korean J Gastroenterol 1989;21:639-44.

31. Choi SH, Ahn BM, Kim JK, Han SW, Shim GS, Baek NJ, et al. Five cases of acute gastric anisakiasis. Korean J Gastroenterol 1989;21:593-9.

32. Jung JY, Kim WK, Song JH, Kim KS, Kim JG, Park HC, et al. Eosinophilic enteritis caused by Anisakis infestation. Korean J Gastroenterol 1990;22:434-40.

33. Park SH, Suh JM, Shim KS,Baeg NJ, Kim BS, Moon IS. A case report of intestinal anisakiasis. Korean J Gastrointest Endosc 1990;10:373-5.

34. Im KI, Yong TS, Shin HJ, Kim BH, Moon SI. Gastric anisakiasis in Korea – with review of 47 cases. Yonsei Rep Trop Med 1990;21:1-7.

35. Im KI and Shin HJ. Morphological observation of Terranova sp. larvae found in human stomach wall. Yonsei Rep Trop Med 1991;22:35-41.

36. Kim SE, Kim SL, Lee KS, Kim JM, Jang MY, Cho JG, et al. Nine cases of acute gastric anisakiasis. Korean J Gastrointest Endosc 1991;23:866-72.

37. Kim LS, Lee YH, Kim S, Park HR, Cho SY. A case of anisakiasis causing intestinal obstruction. Korean J Parasitol 1991;29:93-6.

38. Sohn WM, Kho WG, Seol SY, Chung JM. Two cases of gastric anisakiasis caused by Anisakis type I larva. Inje Med J 1991;12:421-5.

39. Shin JT, Oh SJ, Park SM, Kim YH, Park YK. A case of ileal anisakiasis. Ann Surg Treat Res1992;43:152-6.

40. Lee SH, Sin HG, Seol SY, Chung JM. A case of gastric anisakiasis causing gastric ulcer bleeding. Korean J Gastrointest Endosc 1993;13:693-6.

41. Lee HS, Park KS, Jung KT, Yoo SJ, Kho JH, Park PS, et al. A case of chronic gastric anisakiasis with massive bleeding. Korean J Gastrointest Endosc 1993;13:697-700.

42. Kim J, Chung WS, Cho KH. Status of parasitic infection diagnosed by surgical biopsy in Kwangju and Chollanam-do. Korean J Parasitol 1994;32:93-100.

43. Sohn WM and Seol SY. A human case of gastric anisakiasis by Pseudoterranova decipiens larva. Korean J Parasitol 1994;32:53-6.

44. Sohn WM and Seol SY. A case of acute intestinal anisakiasis caused by Anisakis type I larva. Inje Med J 1994;15:355-9.

45. Seol SY, Ok SC, Pyo JS, Kim IH, Lee SH, Chung JM, et al. Twenty cases of gastric anisakiasis caused by Anisakis type I larva. Korean J Gastroenterol 1994;26:17-24.

46. Im KI, Shin HJ, Kim BH, Moon SI. Gastric anisakiasis cases in Cheju-do, Korea. Korean J Parasitol 1995;33:179-86.

47. Shim YR, Kim DS, Lee TS. Ileal anisakiasis-report of two cases. Korean J Pathol 1995;29:915.

48. Cho BS, Moon JW, Ahn JG, Lee BC, Jeon HY, Shin KC, et al. Report on 7 cases of anisakiasis involving the upper gastrointestinal tract. Korean J Gastrointest Endosc 1996;16:242-5.

49. Geum MS, Cho CM, Kim DH, Choi SG, Lee CH, Kweon YO, et al. Six cases of acute anisakiasis. Korean J Gastrointest Endosc 1997;17:680-3.

50. Kim HJ, Park C, Cho SY. A case of extraintestinal anisakiasis involving a mesocolic lymph node. Korean J Parasitol 1997;35:63-6.

51. Cho YJ, Chu JP, Lee JH, Jeong GS, Yang MH. Analysis of parasitic diseases by biopsy in Kyunghee Medical Center (1972-1983). Infect Chemother 1998;30:173-9.

52. Guahk JY, Kim YK, Lee MK, Cho YH, Kim KS, Lee YR, et al. A case of gastric anisakiasis causing Mallory-Weiss syndrome. Korean J Gastrointest Endosc 1998;18:727-31.

53. Yoon BH, Kim WY, Cho CH, Lee SW, Kim KH, Kang MW, et al. Endoscopic ligation therapy for upper gastrointestinal bleeding. Korean J Gastrointest Endosc 1998;18:345-50.

54. Lee IH, Jang S, Lee CY, Park JS, Lee HJ, Kim HJ, et al. A case of human infection of the larvae from Pseudoterranova decipiens. Korean J Gastrointest Endosc 1998;18:732-6.

55. Koh MS, Huh S, Sohn WM. A case of gastric pseudoterranoviasis in a 43-year-old man in Korea. Korean J Parasitol 1999;37:47-9.

56. Song TJ, Cho SW, Joo KH. Endoscopic findings of acute gastric anisakiasis. Korean J Gastrointest Endosc 1999;19:878-84.

57. Ahn SH, Chon JY, Lee SK, Park BK, Choi BH, Lee YC, et al. A case with gastric anisakiasis presented with a submucosal tumor. Korean J Gastrointest Endosc 1999;19:449-53.

58. Park CY, Chang YW, Kim HJ, Kang SW, Hwang IS, Kim KJ, et al. A case of acute gastric anisakiasis causing massive hematemesis. Korean J Gastrointest Endosc 1999;19:445-8.

59. Kang JH, Park EJ, Cho YB, Kim YS, Lee MS, Shim CS. Two cases of submucosal tumors caused by gastric anisakiasis. Korean J Gastrointest Endosc 1999;19:67-72.

60. Park TG, Lee DH, Lee JS, Kim HS, Sung YH, Choi DH. A case of esophageal anisakiasis. Korean J Gastrointest Endosc 1999;19:597-600.

61. Choi CS, Choi HS, Byun JW, Yoon CO, Kang MS, Jun DW, et al. Two cases of gastric anisakiasis caused by Pseudoterranova decipiens with acute abdominal pain and upper gastrointestinal bleeding. Korean J Gastroenterol 2000;35:501-6.

62. Chung TW, Kang HK, Jeong YY, Jeong GW, Seo JJ, Kim YH, et al. Radiographic findings of gastric anisakiasis. J Korean Radiol Soc 2000;43:209-13.

63. Yu JR, Seo M, Kim YW, Oh MH, Sohn WM. A human case of gastric infection by Pseudoterranova decipiens larva. Korean J Parasitol 2001;39:193-6.

64. Yeum CH, Ma SK, Kim SW, Kim NH, Kim J, Choi KC. Incidental detection of an Anisakis larva in continuous ambulatory peritoneal dialysis effluent. Nephrol Dial Transplant 2002;17:1522-3.

65. Hwang MG, Kim JH, Lee CK, Lee JK. The three cases of anisakiasis in esophagus or gastroesophageal junction. Korean J Gastroenterol 2002;40(suppl):313A.

66. Choi P, Hur JW, Lim HJ, Lee JY, Kim DW, Park MI, et al. A case of gastric submucosal tumor suspected to be caused by Anisakis. Korean J Gastrointest Endosc 2003;27:26-30.

67. Choi P, Hur JW, Lim HJ, Lee JY, Kim DW, Park MI, et al. Lim SR, Hong SN, Kim DS. An investigation of instance infected after eating a slice of raw fish of Astroconger myriaster. Korean J Clin Lab Sci 2003;35:86-9.

68. Noh JH, Kim BJ, Kim SM, Ock MS, Park MI, Goo JY. A case of acute gastric anisakiasis provoking severe clinical problems by multiple infection. Korean J Parasitol 2003;41:97-100.

69. Yoon SW, Yu JS, Park MS, Shim JY, Kim HJ, Kim KW. CT findings of surgically verified acute invasive small bowel anisakiasis resulting in small bowel obstruction. Yonsei Med J 2004;45:739-45.

70. Suh YA, Jang HJ, Eun CS, Jang WY, Lee JJ, Kae SH, et al. A case of a submucosal tumor in the ascending colon probably caused by Anisakis. Korean J Gastrointest Endosc 2004;28:2027.

71. Woo DH, Kim HJ, Kim HS, Chang JY, Nam KD, Kim NH, et al. A case of anisakiasis invading the ascending colon. Intest Res 2004;2:120-3.

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73. Kim BH, Park CU, Lee JH, Yeom SM, Chae DY, Kim SP, et al. A case of anisakiasis concurrently invading the stomach, ileocecal valve and transverse colon. Korean J Gastrointest Endosc 2004;28:43-6.

74. Song HO, Ahn MH, Choi HK, Ryu JS, Min DY, Ree HI. Analysis of 205 cases of parasite infection confirmed in clinical specimens. Korean J Clin Microbiol 2004;7:66-71.

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76. Shin CM, Myung SJ, Cho SJ, Kim JW, Lee KL, Park JH, et al. A case of colonic anisakiasis diagnosed by colonoscopy. Korean J Med 2006;70:S137-40.

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78. Kim YH, Choi WB, Lee SC, Choi HW. Three cases of colonic anisakiasis. Korean J Gastrointest Endosc 2006;33:239-43.

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82. Jang ST, Choi IJ, Kim WT, Lee H, Lee SW, Kang SB, et al. A case of rectal anisakiasis. Korean J Gastrointest Endosc 2006;32:156-9.

83. Kim SH, Kim HU, Lee J. A case of gastroallergic anisakiasis. Korean J Med 2006;70:111-6.

84. Kim SG, Jo YJ, Park YS, Kim SH, Song MS, Lee HH, et al. Four cases of gastric submucosal mass suspected as anisakiasis. Korean J Parasitol 2006;44;61-6.

85. Shin KD, An CM, Nam SW, Kim SK, Kim SH, Kim IH, et al. A case of esophageal anisakiasis presenting as chest pain mimicking angina. Korean J Gastrointest Endosc 2007;35:19-22.

86. Yoo HJ, Kim SH, Lee JM, Kim MA, Han JK, Choi BI. The association of anisakiasis in the ascending colon with sigmoid colon cancer: CT sonographic findings. Korean J Radiol 2008;9(suppl): S56-60.

87. Lee CM, Choi JY, Kim JH. Intestinal obstruction caused by anisakiasis. J Korean Surg Soc 2008;74:154-6.

88. Choi SC, Kim K, Lee KR, Cho JH, Park SW, Hong KY, et al. A case of an eosinophilic granuloma mimicking a submucosal tumor in the ascending colon probably caused by Anisakis. Korean J Gastrointest Endosc 2008;37:127-31.

89. Cho MH, Lee SJ, Joung HJ, Lee HS, Kim YD, Jeong WJ, et al. A case of anisakiasis on stomach and colon mimicking submucosal tumor. Int J Infect Dis 2009;13:S93.

90. Lee EJ, Kim YC, Jeong HG, Lee OJ. The mucosal changes and influencing factors in upper gastrointestinal anisakiasis: analysis of 141 cases. Korean J Gastroenterol 2009;53:90-7.

91. Hong SS, Kim JH, Park ST, Chang YW, Kim HJ, Kwon KH, et al. Duodenal anisakiasis presenting as bowel obstruction and fistula formation: a case report. J Korean Soc Radiol 2009;60:419-22.

92. Choi SJ, Lee JC, Kim MJ, Hur GY, Shin SY, Park HS. The clinical characteristics of Anisakis allergy in Korea. Korean J Intern Med 2009;24:160-3.

93. Choi WH, Chu JP, Jiang M, Lee YS, Kim BS, Kim DG, et al. Analysis of parasitic diseases diagnosed by tissue biopsy specimens at Kyunghee Medical Center (1984-2005) in Seoul, Korea. Korean J Parasitol 2010;48:85-8.

94. Do KR, Cho YS, Kim HK, Hwang BH, Shin EJ, Jeong HB, et al. Intestinal helminthic infections diagnosed by colonoscopy in a regional hospital during 2001-2008. Korean J Parasitol 2010;48:75-8.

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