- Email: [email protected]
Anisakidosis: Report of 25 cases and review of the literature
~ Pergamon
Comp. Immun. Microbiol.infect. Dis. Vol. 18, No. 2, pp. 75-84, 1995 0147-9571(94)00025--5
Copyright © 1995 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0147-9571/95 $29.00 + 0.00
REVIEW ANISAKIDOSIS: REPORT OF 25 CASES A N D REVIEW OF THE LITERATURE P A T R I C E B O U R E E , .1 A N D R I ~ P A U G A M 2 and JEAN-CLAUDE PETITHORY 3 ~Department of Parasitology, Bicetre Hospital, Paris-XI University, 94275 Kremlin-Bicetre, France, 2Department of Parasitology, Cochin Hospital, 75 Paris and 3Medical Biology Unit, Gonesse Hospital, 95 Gonesse, France
(Received for publication 21 December 1994) Abstraet--Anisakidosis (previously known as anisakiasis) is a disease caused by the accidental ingestion of larval nematodes (Anisakis and sometimes Pseudoterranova) in raw fish. Two groups of patients are studied: 5 clinical cases and 20 serological diagnoses. 55 French cases are already published. Most of them complained of acute symptoms, which occurred within 12 h of eating the seafood meal--epigastric pain, occlusion, diffuse abdominal pain, and appendicitis. Larvae were attached to the gastric mucosa (25 cases), inciting an inflammatory response (erythema, oedema ulceration). Diagnosis of anisakiasis is made by gastroscopy which allows removal of the worms, and cures the patients. In gastro-intestinal tract X-rays, oedema in the mucosa, pseudo tumour formation, and filling defects (worm) were observed. In chronic infections, cases with intermittent feelings of ill health and abdominal pain, lasting from several weeks to months, were misdiagnosed as another intestinal disease. Positive serological reactions are helpful, and surgery is necessary for resection of the lesion; diagnosis is made histologically by an eosinophilic granuloma, and the presence of a larva with Y shaped lateral cords. Infestation rate is high in fishes: cod (88%), rock fish (86%), herring (88%), salmon, mackerel. Public health education should discourage the eating of raw fish. Thorough cooking to 70°C or adequate freezing to -20°C for 72 h are the best preventive measures. Such legislation is only in force in the Netherlands, where cases have decreased dramatically.
Key words: Anisakis simplex, Pseudoterranova, anisakidosis, epigastric pain, gastroscopy. R6sum~-L'anisakidose (ancienne appellation: anisakiase) est une affection due fi l'ingestion de poisson contenant des larves d'Anisakis ou parfois de Pseudoterranova. Deux s6ries de patients sont analys6es: 5 observations cliniques et 20 diagnostics s6rologiques, par immuno61ectrophor6se. 55 cas franqais sont actuellement recens6s, montrant une majorit6 de cas aigus, survenant dans les 48 h suivant le repas infestant. Les troubles sont surtout des 6pigastralgies (18 cas), et une occlusion (8 cas). Des douleurs abdominales erratiques ont 6t6 retrouv6es chez 5 sujets, et un syndrome appendiculaire chez 3 patients. Les larves &aient localis6es dans la paroi gastrique (25 cas), responsables d'alt6ration de la muqueuse (6ryth6me, oed6me, parfois ulc6ration). Le diagnostic repose sur la raise en 6vidence de la larve par fibroscopie qui permet son extraction, et gu6rit le patient. La radiographie digestive montre des zones d'o6d6me, des aspects pseudo-tumoraux, et parfois visualise le ver. Dans les infections chroniques, r6alisant un granulome 6osinophile de l'intestin gr~le, les malaises intermittents 6voquent d'autres diagnostics d'atteinte digestive. A c e stade, la s6rologie est positive, et le traitement chirurgical est n6cessaire. Le taux d'atteinte chez les poissons est 61ev6: merlu 88%, s6baste 86%, hareng 82%, merlan 71%, saumon, maquereau. L'6ducation sanitaire devrait d6conseiller la consommation de poisson cru. Mais la seule prophylaxie efficace est la cuisson profonde fi 70°C ou la cong61ation gt -20°C pendant au moins 72 h, mesures non encore obligatoires dans la C.E.E., sauf en Hollande, ayant entrain6 une chute de l'incidence de l'anisakidose humaine.
Mots-clefs: Anisakis simplex, Pseudoterranova, Anisakidose, 6pigastralgies, fibroscopie. *Author for correspondence. 75
76
P. Bouree et al.
INTRODUCTION Anisakidosis is an uncommon parasitic disease. Because of some recent cases, a general review of the literature offers the opportunity of stating precisely the epidemiological, clinical and diagnostic features of this zoonose. CASE REPORTS Two groups of patients with anisakidosis were studied. The first group included 5 cases of patients with acute abdominal pain and confirmed diagnosis of anisakidosis (Table 1). The second group consisted of 20 patients with positive serodiagnosis (several bands in immunoelectrophoresis), including 9 acute and 11 chronic cases. The patients complained of epigastric pain (8 cases) and of intestinal disturbances (8 cases). The worms were located in the stomach (6 cases), in the intestine (6 cases), or their location was not determined (8 cases). The first group was an all male group, but in the second group, there was no significant difference between the sexes (11 males and 9 females). In all the cases, the patients had eaten raw fish, and 4 patients had eaten in an Asian restaurant. One of the cases was very interesting. A 32 year old female who had complained of digestive problems for 7 y had 710 eosinophiles/mm 3. Repeated stools examination were negative, but serological tests were positive for anisakidosis. After 10 days of treatment with thiabendazole, the clinical and biological symptoms disappeared. Four years later, on account of a dysphagy, fibroscopy analysis showed polyadenomatous polyps. It seems logical to find acute cases in the first group, where diagnosis was established using fibroscopy in 4 cases and retrospectively by serological analysis in 1 case. In the second group, where diagnosis was based only on serological tests, the chronic forms were the more frequent. Likewise, in the first group, the worms were in the stomach, whereas in the second group they were mostly in the intestine, with only 6 gastric locations out of 20 cases. DISCUSSION AND LITERATURE REVIEW The first description of a worm in fish was made in the 13th century. However, it was not until 1845 that Dujardin described a worm in dolphins as Anisakis (from the greek anisos = unequal and akis = point), a Class of Nematoda, Order Ascaridida, and Family Anisakidae. Table 1. Clinical features and diagnosis of 5 patients with acute anisakidosis Age (y)
Sex Symptoms
Gastroendoscopy
Other examinations
54
M
Sudden epigastric pain
Normal abdominal ultrasonography
20
M
Pseudo-ulcus pain
53 21 31
M M M
Acute epigastric pain Sudden retro-sternal pain Nocturnal epigastric pain with paroxysms
Hyperemia mucosa 1 larva Intestinal gastritis 1 larva 3 white nematodes 10 larvae fixed in the mucosa Not carried out
Normal ultrasonography and biological tests Normal ultrasonography WBC: DI: 19 800 leukocytes (89% Neutrophilic polymorphonucl) D30: 8 600 leukocytes (12% Neutrophilic polymorphonucl) serodiagnosis: 4 bands
Anisakidosis: a review
77
The first human case of anisakidosis (this name is now preferred to anisakiasis) was diagnosed in Holland in an eosinophilic granuloma, and in 1960 van Thiel established the relationship between the human disease and eating infested raw herring [1]. In 1968, a larva of Anisakis was observed directly for the first time using gastroendoscopy [2]. The first case in France was observed in a case of ileal eosinophilic granuloma, in 1969, by Calvet [3] and the first case in the U.S.A. was observed in 1975 by Pinkus [4].
Epidemiology The adult worm of Anisakis simplex also called herringworm or whaleworm (ranging from 3 to 15 cm in length), lives in the stomach of large marine mammals (dolphins, whales) or pinnipedia (seals, sea lions) [5]. After fecundation, the females lay eggs (40 x 50 #m, ovoid) which are distributed in the sea water. At a temperature of 5-7°C, the eggs hatch, and the young free-living larvae (stage 1) are ingested by the first intermediate host, small crustaceans (Euphausia) where the larvae moult from stage II to III. These larvae, after ingestion by fish, cross the digestive wall and live in the hemocele [6]. The older the fish, the more they are infested. These fish are then devoured by larger marine mammals, where the larvae moult into adult worms [7] (Fig. 1). The infested fishes are mostly sea fish, but some infested fishes have been found in briny and even in fresh water.
MARINE MAMMAL (definitive hosts) stomach adult worm
HUMANS .c (accidental hosts)
> feces eggs
(ingestion)
stage larvae
III
L
free eg! s in the ocean
larvae stage I
squids
fishes
larva~stage II
hatch out
(ingestion)
PLANKTONIC .., CRUSTACEANS
(intermediate hosts) Fig. I. Life cycle of Anisakis.
L
(ingestion)
P. Bouree et al.
78
Table 2. Pathogenesis of anisakidosis Delay after infection
Parasite
Host parasite reaction
Pathogenesis
~
Adhesion to mucosa and
Secretion of proteolytic enzymes
Haemorrhage, formation of a gallery
4-6 days
in the sub-mucosa Penetration of the mucosa
Secretion of chemotactic factor (ECF)
Eosinophilic granuloma, oedema,
7 14 days
Granuloma around the larva
/> 15 days
Dead larva
Immediate and delayed hypersensitivity Regression of the granuloma, persistent inflammation
necrosis Local and general allergic reaction*, crateriform lesion Spontaneous recovery, chronic ulceration
*Mostly in sensitized patients. ECF, eosinophil chemotactic factor.
It is possible that fresh water fishes are infested by eating larvae which were free living after the death of briny water fishes that swam up rivers [8]. Human infestation occurs by consuming raw fish. The larvae (stage III) invade the gastric mucosa. Eosinophilic granulomas are probably due to protease production by the parasites [9], with a host parasite cell-mediated hypersensitive reaction (Table 2). In the French cases, infestation was due mostly to the ingestion of raw herring (rollmops and red herring), and also mackerel, salmon or hake. Other animals may become infected by Anisakis, such as amphibians (bullfrogs), reptiles (turtles) or piscivorous birds (fulmars). Anisakidosis is more frequent in Asia (100-200 cases a year) but is seen also in Europe (5-25 cases a year) [10], in the U.S.A. [11], and more rarely in New Zealand [12] and in Egypt [13]. A total of more than 12,500 cases have been reported in Japan, and more than 500 in other countries, mostly in The Netherlands [14]. This disease can occur with other genera such as Contraceum osculatum (rarely) and Pseudoterranova (previously known as Phocanema) [15]. Pseudoterranova decipiens, also called codworm or sealworm, shows some differences to Anisakis [10] (Table 3). Pseudoterranovosis is found in the U.S.A. and in Japan. The larvae are located in the throat and in the stomach, but the intestinal chronic stage is very infrequent. Larvae of Anisakis and Pseudoterranova may be identified in histologic sections [16], and by electron microscopy [l 7]. Clinical aspects Among the 55 cases already published in France (probably underestimated), including our cases, 30 suffered from acute disease, 7 from chronic disease, while 18 were not Table 3. Differences between Anisakis and Pseudoterranova Geographical distribution
L(/# Q'ele Definitive hosts Eggs 1st intermediate host 2rid intermediate host
Larvae (Stage III) Size Colour Cuticle Histologic section
Anisakis simple.,:
Pseudoterranova decipiens
World wide polar zones+ +
Both temperate and polar zones
Whales
Seals
Ocean Euphausiids Zooplankton-feeding fish, squid Long ventriculus 28.4 x 0.49 mm (Japan) 17.0 x 0.41 mm (China) White Thin, without electron dense nods Y-shaped lateral cords
Ocean Benthic copepods, amphipods, decapods Zoobenthos-feeding fish Ventriculus partly covered with cecum
60-80 intestinal cells
32.6 x 0.80 mm Red Thick, with electron dense nods Butterfly-shaped lateral cords /> 100 intestinal cells
Anisakidosis: a review
79
Table 4. Delay in the appearance of symptoms after ingestion of raw fish [18] Location Delay (h)
Gastric
Intestinal
3 6 12 24 48 />48 unknown
15% 41% 16% 2% 3% 3% 20%
4% 4% 4% 18% 20% 11% 39%
Table 5. Study of 55 French cases of anisakidosis Contamination
Location of larvae or of eosinophilic granulomas
Symptoms
Herring Other fish Asian restaurant Not determined
18 26 2 9
Epigastralgy Obstruction Appendicular syndrome Abdominal pain Various Chance detection Not determined
18 8 3 3 4 I 18
Gastric Intestinal Colic Mesenteric Rhino-pharyngeal Not determined
25 16 3 1 1 9
determined. The disorders appeared with varying delays according to the location of the worm (Table 4) [18]. Generally, the clinical symptoms of acute intestinal anisakidosis include violent epigastric pain [19], nausea, vomiting, diarrhoea (Table 5), and sudden abdominal pain similar to an acute abdominal syndrome such as intestinal obstruction [20], appendicitis [21] or peritonitis [22]. Additional disorders have been reported such as urticaria [23], pulmonary disturbances [24], allergic oedema [25], hypersialorrhoea [26] or polyarthritis [27]. Sometimes, the disorders decrease spontaneously and definitively within a few days [28] even in cases of tumours, hence the term "vanishing tumour" of the stomach [14]. In some cases, the disease is asymptomatic, as shown by Spehn who accidentally found larvae when using gastroendoscopy for a case of oesophageal candidiasis [29]. Chronic anisakidosis produces mild symptoms such as abdominal pain, nausea, vomiting, with diarrhoea followed by constipation, and sometimes bloody stools, suggesting a colonic tumour of the stomach [30].
Table 6. Serological cross-reactions in a patient infested with anisakidosis Serodiagnosis Blood eosinophilia Anisakiasis Filariasis Larva migrans Trichinellosis Hydatidosis Schistosomiasis Hypodermosis Fasciolasis *Non significant rate.
D.30 1050/mm3
D. 150 70/mm 3
4 bands 1/80°* N 1/400°* 1/500° 1 band 1/80<~* 1 band 1/160<'*
N N N N N N 1/80°* N 1/160<'*
Methods Immuno-electrophoresis Indirect fluorescent antibody test counter-electrophoresis indirect fluorescent antibody test haemagglutination counter-electrophoresis haemagglutination lmmuno-electrophoresis Haemagglutination
P. Bouree et al.
80
Table 7. Macroscopic findings in anisakidosis Location Gastric
Acute
Chronic
Larvae move actively in the early phase of penetration, and move slowly later Site of penetration: oedematous erosion and bleeding
Intestinal
Erosion or ulcer Oedema Tumour-like nodule
Ascitis fluid, with free worms
Mild symptoms
30% eosinophil cells
Granulomatous changes which induce narrowing of the intestinal lumen
Omentum: mild oedema with hyperemia, and inflammation Fibrinous adhesions
Larvae pass through the wall creating granulomas in the peritoneal cavity
Inflammatory changes in the terminal ileum
Diagnosis and treatment
During the first week after infection, blood tests do not show any disturbances. The blood eosinophilia count increases after 8-15 days [31] and parasitic stools examination remains negative. Immunodiagnosis tests become positive after the tenth day and are negative between 6 and 12 months [32]. A micro-Elisa test [14] with monoclonal antibodies seems very specific [33], as is the Western Blot test [34]. Serodiagnosis is of no use in acute disease, when diagnosis and treatment are decided within a few hours of the onset of the disease. There is a great deal of cross reactivity (Table 6). However, serological tests are very important in chronic anisakidosis where diagnosis by endoscopy is not possible. An increase in specific IgE, with the RAST test [35] has been noticed over a period of about 2 months [36]. Table 8. Histological findings in anisakidosis Location Gastric
Acute stage Thickening of gastric wall Intact and clearly visible larvae in the submucosal layer Oedema and massive eosinophilia mixed with neutrophil, macrophage and lymphocyte infiltration
Chronic stage Ist stage: phlegmonous type = " a n Arthus-type" reaction, eosinophilic infiltration with occasionally living larvae 2nd stage: abcess type slightly degenerating larvae surrounded by necrotic tissue with oedema and fibrin exudation 3rd stage: abscess granuloma type > 6 months from the time of infection; debris of larvae surrounded by granulatous tissue and lymphocyte infiltration 4th stage: granuloma type larval debris surrounded by granulomatous tissue with fibrosis, foreign body giant cell lymphocytes
Intestinal
Thickening of the wall by intensive oedema
Similar to mild type of gastric anisakidosis
Numerous eosinophils, neutrophils, macrophages and lymphocytes
I st stage: phlegmonous type similar to acute type
Fibrin exudation
2nd stage: abcess type slightly degenerating larva surrounded by massive necrotic tissue
Small haemorrhages Hyperplasia of lymphoid follicles
3rd stage: abcess granuloma type intensively degenerated worm at the centre of lymphocyte infiltration 4th stage: granuloma type (rare) unidentified debris in a granuloma
A n i s a k i d o s i s : a review
81
The gastroendoscopic findings, which represent an urgent examination, include oedema and hyperaemia of the mucosa [37], sometimes with ulcerations [38]. Anisakis larvae can be detected with gastroscopy, and easily removed during the acute stage, following which the epigastric pains disappear immediately [39, 40]. The macroscopic findings vary according to the stage of the anisakidosis (Table 7). Gastric X-rays show thickened and rigid longitudinal gastric mucosal folds (81%), and sometimes the larva itself as a filiform shadow of the nematode (48%) [4!]. Moreover, digestive disturbances can appear as dilatation of the intestinal lumens [42] or ascitis fluid [43]. With ultrasonography, it is possible to observe an enlarged local or general wall [44]. Endoscopy, with 0.1% indigo carmin solution, shows a good contrast with the larvae being more visible. At the chronic stage, diagnosis is established through the histopathology of the lesion, showing eosinophilic granulomas and cross sections of Anisakis larvae, with the characteristic Y lateral cords [45]. The pathological features differ according to the stage of the disease and the location of the larvae (Table 8). The larvae do not migrate, and degenerate in about 8 weeks [46]. Some extra gastro-intestinal locations of Anisakis larvae have been described in Japan, e.g. in the abdominal wall, omentum, mesentery, liver, pancreas, ovary, lymph mode, pleural cavity tongue, and even uvula [14]. In relation to the observation of chronic anisakidosis with a polyadenoma [47], it is very interesting to note that in countries where gastric cancer is very frequent, such as Japan and Chile, raw fish is a very common meal. The development of eosinophilic granulomas into cancer is a hypothesis which requires further examination.
Prophylaxis Surveys in several fish markets have revealed significant infection of herring and mackerel [48, 49] (Table 9). After several alarmist campaigns in different countries (e.g. Germany and Italy), the consumption of sea fish dramatically decreased [50]. In order to avoid discriminatory measures towards any country, the European Union has suggested some procedures in relation to fishing, because this parasitosis is seen in all European fisheries [51]. Early evisceration is recommended because the worms leave the digestive tract within a few days to go into the muscles [52], in addition, freezing at - 2 0 ° C for 3 days, or heating to 70°C, as larvae often survive at 50°C. Microwave oven cooking
Table 9. Fish parasitism in fish-markets
Boulogne 1986 [49] Fishes Herring Whiting Mackerel Hake Rose fish Chinchard Gurnard Sardines Anchovy Plaice
Paris 1986 [48]
Paris 1990 [13]
No. investigated
No. infested
No. investigated
% infested
No. investigated
No. infested
I0 4 8
8 4 5
682 84 214 35 36 40 29 22 27
82% 71% 30% 88% 86% 62% 86% 4% 3%
6 13 30 i0
5 9 15 I0
5
0
82
P. Bouree et al,
w o u l d be insufficient to d e s t r o y larvae [53]. The larvae resist salting, s m o k e - c u r i n g a n d m a r i n a d i n g , a n d 51 d a y s in vinegar [16]. Several factors m a y explain the s p r e a d i n g o f a n i s a k i d o s i s [13]. The p r o t e c t i o n o f cetacea a n d p i n n i p e d i a leads to the p r o l i f e r a t i o n o f definitive hosts. The p o p u l a t i o n o f Euphausia, i n t e r m e d i a t e hosts and the prey o f choice for herring, a n d an increase in p l a n k t o n , could c o n t r i b u t e to infection o f the fishes. In line with m o d e r n m e t h o d s o f fishing, fish are n o t gutted immediately, b u t are stored in a cold r o o m . Thus, the larvae leave the gut a n d enter the muscles [54]. The evisceration o f fishes, within a few h o u r s after fishing, seems insufficient, as larvae m i g r a t e very early into the flesh [55]. The present fashion o f " n a t u r a l c o o k i n g " with raw f o o d also increases the risk. Sometimes, careful e x a m i n a t i o n o f a meal can lead to the detection o f some larvae by chance [56]. Finally, the absence o f i n t e r n a t i o n a l rules a b o u t this question results in ineffective protection. However, in The N e t h e r l a n d s , o b l i g a t o r y freezing before sale has led to the virtual d i s a p p e a r a n c e o f this disease, whereas with J a p a n e s e culinary traditions, anisakidosis is a real public health p r o b l e m . A n i s a k i d o s i s has shown a m a r k e d increase in recent years because o f the fashion o f eating raw fish, p a r t i c u l a r l y herring. A c u t e cases, gastric in J a p a n a n d intestinal in E u r o p e , m u s t be considered when digestive disorders occur a few hours after the c o n s u m p t i o n o f raw fish. C h r o n i c anisakidosis is m o r e difficult to diagnose, b u t at the m o m e n t , i m m u n o l o g i c a l tests are the most suitable.
REFERENCES 1. Van Thiel P, H., Kuipers F. C. and Roskam R. A nematode parasite to herring, causing acute abdominal syndromes in man. Trop. geogr. Med. 2, 97 ll3 (1960). 2. Namiki M. A history of research into gastric anisakiasis in Japan. In Gastric Anisakiasis in Japan (Edited by H. Ishikura and N. Namiki), pp. 13-18. Springer-Verlag, New York (1989). 3. Calvet J. P., Zuckmann P. and Texier J. Granulome 6osinophile allergique parasitaire de l'il6on. M~m. Acad. Chit. 95, 648-651 (1969). 4. Pinkus G. S., Coolidge C. and Little M. D. Intestinal anisakiasis. First case report from North America. Am. J. Med, 59, 114-120 (1975). 5. Smith J. W. and Wootten R. Anisakis and Anisakiasis. Adv. Parasit. 16, 93-163 (1978). 6. Petithory J. C. and Many B. L'anisakiase en France. Lettre Infectiologue III, 2, 96-99 (1988). 7. Bouree P. Anisakiase. Encyel. M~d. Chir. Mal. Inf. 8118, Bl0 (1989). 8. Shiraki T. Larval nematode of family anisakidae in the northern sea in Japan, as a causative agent of eosinophilic phlegmon or granuloma in the human gastro intestinal tract. Acta. reed. biol. 22, 57-98 (1974). 9. Sakanari J. A. Anisakis, from the platter to the microfuge. Parasit. Today 6, 323-327 (1990). 10. Feldmeier H., Poggensee G. and Poggensee U. The epidemiological, natural history and diagnosis of human Anisakiasis. Europ. Microb. 2, 30-36 (1993). ll. Malkin J. E., Lafaix C., Prazuck T., Haroche G., Fish A. Anisakiase. Med. Hyg. 45, 680-687 0987). 12. Paltridge G. P., Faoagali J. L. and Angus H. B. Intestinal anisakiasis: a new New-Zealand disease. N.Z. Med. J. 558-559 (1984). 13. Cocheton J. J., Cabout I. and Lecomte I. Anisakiase et infection par les anisakid6s. Annls M~d. int. 142, 121-130 (1991). 14. Ishikura H., Kikuchi K., Nagasawa K., Ooiwa T., Takamiya H., Sato N. and Sugane K. In Anisakidae and Anisakidosis in Tsieh Sun, Progress in Clinical Parasitology. Springer-Verlag, New York (1993), 15. Huang W. and Bussieras J. Anisakides et anisakidoses humaines. Premidre partie: donn6es bibliographiques. Annls Parasit. hum. comp. 63, 119-132 (1988). 16. Sakanari J. A. and McKerrow J. H. Anisakiasis. Clin. Microb. Rev. 2, 278-284 (1989). 17. Fredericksen D. W. and Specian R. D. The value of cuticular fine structure in identification of juvenile anisakine nematodes. J. Paras#. 67, 647-655 (1981). 18. Asaihi K., Nishino C., Totsuka M., Hayasaka H. and Suzuki T. Studies on the etiologie mechanism of anisakiasis. Epidemiologic study of inhabitants and questionnaire survey in Japan. Gastro-emeroL Jap. 15, 128-134 0980).
Anisakidosis: a review
83
19. Bouree P., Taugourdeau Ph., Juette P. and Blanquart A. Anisakiase. Apropos de 5 cas. Bull. Soc.fr. Parasit. 8, 267 270 (1990). 20. Boucaut P., Chome J., Lame C. and Holier C. Occlusion r6v61atrice d'un granulome 6osinophile parasitaire de l'intestin gr61e. Nouv. Presse Mdd. 9, 2918 (1980). 21. Rushovch A. M., Randall E. L., Caprini J. A. and Westenfelder G. O. Omental anisakiasis: a rare mimic of acute appendicitis. Am. J. clin. Path. 80, 517-520 (1983). 22. Yokogawa M. and Yoshimura H. Clinicopathologic studies on larval anisakis in Japan. Am. J. trop. Med. Hyg. 6, 723-724 (1967). 23. Kasuya S., Hamano H. and Izumi S. Mackerel induced urticaria and anisakis. Lancet 335, 665 (1990). 24. Kobayashi A., Tsuji M. and Wilbur D. L. Probable pulmonary anisakiasis accompanying pleural effusion. Am. J. trop. Med. Hyg. 34, 310-313 (1985). 25. Godeau P., Danis M., Bouchareine A. and Nozais J. P. Une cause inhabituelle d'oed6me segmentaire: l'anisakiase. Presse Med. 15, 1246-1247 (1985). 26. Letoquart J. P., Friguet J. L., Bigant E. and Mambrini A. Un nouveau cas d'anisakiase gastrique et p6riton6ale. J. Chir. 124, 389 390 (1987). 27. Fabresse F. X., Essioux H., Meyran M., Laroque P. and Celton H. Polyarthrite de ranisakiase--Premier cas. Presse Mkd. 13, 1004 (1984). 28. Bouree P. and Zetlaoui J. Anisakiase aigue avec r6gression spontan6e. Presse Med. 18, 1885 (1989). 29. Spehn J., Schonbeck S., Koperski K. and Butzow G. H. Atypical anisakiasis in an acquired immune deficiency syndrome patient. D. Med. Wschr. 24, 983-984 (1988). 30. Shirahama M., Koga T., Uchida S., Miyamoto Y. and Ohta Y. Colonic anisakiasis simulating carcinoma of the colon. Am. J. Roentgen 155, 895 (1990). 31. Petithory J. C., Verrier F. and Guyet-Rousset P. Etude biologique d'un cas d'anisakiase colique. Revue de la litt6rature. Path. Biol. 40, 47-51 (1992). 32. Petithory J. C., Lapierre J., Rousseau M. and Clique M. T. Diagnostic s6rologique de l'anisakiase (granulome ~osinophile digestif) par pr6cipitation en milieu g61ifi& (Ouchterlony, 61ectrosyn6r~se, immuno61ectrophor6se). Med. Mal. Inf. 3, 157-162 (1986). 33. Yagihashi A., Sato N., Takahashi S., Ishikura H. and Kikuchi K. A serodiagnostic assay by microenzymelinked immunosorbent assay for human anisakiasis, using a monoclonal antibody specific for anisakiasis larvae antigen. J. infect. Dis. 161, 995-998 (1990). 34. Petithory J. C., Rousseau M. and Siodlak F. Donn6es s6ro6pid6miologiques sur l'anisakiase. Cons6quences prophylactiques pour les produits de la p6che. Bull. Acad. natn. Med. 175, 273 279 (1991). 35. Desowitz R. S., Raybourne R. B., Ishikura H. and Kliks M. M. The radio allergo sorbent test (RAST) for the serological diagnosis of human anisakiasis. Trans. Roy. Soc. trop. Med. Hyg. 75, 256~59 (1985). 36. Deardorff T. L., Fukumura T. and Raybourne R. B. Invasive anisakiasis. A case report from Hawai. Gastro-ent~rol. 90, 1047-1050 (1986). 37. Fugino T., Ooiwat T. and Ishi Y. Clinical, epidemiological and morphological studies on 150 cases of gastric anisikiasis in Fukuoka Prefecture. Jap. J. Parasit. 33, 73-92 (1984). 38. De Montigny S., Prevot S. and Basset D. Anisakiase gastrique: gu6rison apr6s extraction endoscopique retard6e. Presse M~d. 20, 180 (1991). 39. Bouree P., Juette P. and Kloeti G. Anisakiase: diagnostic et extraction par endoscopie gastrique. Presse Med. 1484-1485 (1987). 40. Ikeda K., Kumashiro R. and Kifune T. Nine cases of acute gastric anisakiasis Gastro-intestinal Endosc. 35, 304-308 (1989). 41. Sugimachi K., Inokuchi K., Ooiwa T., Fujino T. and Ishii Y. Acute gastric anisakis--Analysis of 178 cases. J.A.M.A. 253, 1012-1013 (1985). 42. Watt I. A., McLean N. R., Girwood R. W., Kissen L. H. and Fyfe A. H. B. Eosinophilic gastroenteritis associated with a larval anisakine nematode. Lancet ii, 893-894 (1979). 43. Picard D., Herbinet B. and Alexandre J. H. Syndromes abdominaux aigus et anisakiase: revue de la litt6rature ~i propos d'un cas r~cent. Ann. Chit. 33, 40-44 (1979). 44. Yano M., Yokomizo S. and Nakayama T. Ultrasonic examination. In Gastric Anisakiasis in Japan (Edited by H. Ishikura and N. Namiki), pp. 77-84. Springer-Verlag, Berlin (1989). 45. Dooley J. R. and Neafie R. C. Anisakiasis. In Pathology of Tropical and Extraordinary Diseases, (Edited by C. Binford and D. Conner), pp. 475-481 Armed Forces Inst. Pathol., Washington, U.S.A. (1976). 46. Hsiu J. G., Gamsey A. J., Ives C. E., D'Amato N. A. and Hiller A. N. Gastric anisakiasis: report of a case with clinical, endoscopic and histological findings. Am. J. Gastro-ent. 81, 1185-1187 (1986). 47. Petithory J. C., Paugam B., Buyet-Rousset P. and Paugam A. Anisakis simplex, a co-factor of gastric cancer? Lancet 2, 1002 (1990). 48. Huang W. Anisakides et anisakidoses. Enqu6te sur les anisakid6s de poissons commerciaux du march6 parisien. Annls Parasit. hum. comp. 63, 197-208 (1988). 49. Mudry J., Lefebvre P., Dei-Cas E., Vernes A., Doirriel J., Debat M., Marti R., Binot A. and Cortot A. Anisakiase humaine: 5 cas dans le Nord de la France. Gastro-ent. clin. Biol. 10, 83-87 (1986).
84
P. Bouree et al.
50. Hubert B., Bacou J. and Belveze H. Epidemiology of human anisakiasis: incidence and sources in France. Am. J. trop. Med. Hyg. 40, 301-303 (1989). 51. Angot V. and Brasseur P. Epid6miologie et prophylaxie de l'Anisakiase. Enqu6te sur l'infestation de 3 especes de consommation courante en France. Bull. Epid. Hebd. Paris 14, 59-60 (1993). 52. Declerck D. Pr6sence de larves de Anisakis simplex dans le hareng (Clupea harangus). Rev. Agric. 41, 971-980 (1988). 53. O.M.S. Anisakiase. Un cas dans l'Alberta. Rel. Epid. Hebd. Gen~ve 14, 106-107 (1990). 54. Acha P. N. and Szyfres B. Anisakidose in Zoonoses. Ed. Off. int. Epiz. 854-861 (1989). 55. Smith J. W. and Wooten R. Experimental studies on the migration of Anisakis sp larval into the flesh of herring Clupea harrengus. Int. J. Parasit. 5, 133-136 (1975). 56. Pelloux H., Pinel C. and Ambroise-Thomas P. Larves d'Anisakidae: d6tection dans la chair des poissons et pr6vention de l'anisakiase humaine. Med. Mal. Inf. 22, 939-940 (1992).
Comp. Immun. Microbiol.infect. Dis. Vol. 18, No. 2, pp. 75-84, 1995 0147-9571(94)00025--5
Copyright © 1995 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0147-9571/95 $29.00 + 0.00
REVIEW ANISAKIDOSIS: REPORT OF 25 CASES A N D REVIEW OF THE LITERATURE P A T R I C E B O U R E E , .1 A N D R I ~ P A U G A M 2 and JEAN-CLAUDE PETITHORY 3 ~Department of Parasitology, Bicetre Hospital, Paris-XI University, 94275 Kremlin-Bicetre, France, 2Department of Parasitology, Cochin Hospital, 75 Paris and 3Medical Biology Unit, Gonesse Hospital, 95 Gonesse, France
(Received for publication 21 December 1994) Abstraet--Anisakidosis (previously known as anisakiasis) is a disease caused by the accidental ingestion of larval nematodes (Anisakis and sometimes Pseudoterranova) in raw fish. Two groups of patients are studied: 5 clinical cases and 20 serological diagnoses. 55 French cases are already published. Most of them complained of acute symptoms, which occurred within 12 h of eating the seafood meal--epigastric pain, occlusion, diffuse abdominal pain, and appendicitis. Larvae were attached to the gastric mucosa (25 cases), inciting an inflammatory response (erythema, oedema ulceration). Diagnosis of anisakiasis is made by gastroscopy which allows removal of the worms, and cures the patients. In gastro-intestinal tract X-rays, oedema in the mucosa, pseudo tumour formation, and filling defects (worm) were observed. In chronic infections, cases with intermittent feelings of ill health and abdominal pain, lasting from several weeks to months, were misdiagnosed as another intestinal disease. Positive serological reactions are helpful, and surgery is necessary for resection of the lesion; diagnosis is made histologically by an eosinophilic granuloma, and the presence of a larva with Y shaped lateral cords. Infestation rate is high in fishes: cod (88%), rock fish (86%), herring (88%), salmon, mackerel. Public health education should discourage the eating of raw fish. Thorough cooking to 70°C or adequate freezing to -20°C for 72 h are the best preventive measures. Such legislation is only in force in the Netherlands, where cases have decreased dramatically.
Key words: Anisakis simplex, Pseudoterranova, anisakidosis, epigastric pain, gastroscopy. R6sum~-L'anisakidose (ancienne appellation: anisakiase) est une affection due fi l'ingestion de poisson contenant des larves d'Anisakis ou parfois de Pseudoterranova. Deux s6ries de patients sont analys6es: 5 observations cliniques et 20 diagnostics s6rologiques, par immuno61ectrophor6se. 55 cas franqais sont actuellement recens6s, montrant une majorit6 de cas aigus, survenant dans les 48 h suivant le repas infestant. Les troubles sont surtout des 6pigastralgies (18 cas), et une occlusion (8 cas). Des douleurs abdominales erratiques ont 6t6 retrouv6es chez 5 sujets, et un syndrome appendiculaire chez 3 patients. Les larves &aient localis6es dans la paroi gastrique (25 cas), responsables d'alt6ration de la muqueuse (6ryth6me, oed6me, parfois ulc6ration). Le diagnostic repose sur la raise en 6vidence de la larve par fibroscopie qui permet son extraction, et gu6rit le patient. La radiographie digestive montre des zones d'o6d6me, des aspects pseudo-tumoraux, et parfois visualise le ver. Dans les infections chroniques, r6alisant un granulome 6osinophile de l'intestin gr~le, les malaises intermittents 6voquent d'autres diagnostics d'atteinte digestive. A c e stade, la s6rologie est positive, et le traitement chirurgical est n6cessaire. Le taux d'atteinte chez les poissons est 61ev6: merlu 88%, s6baste 86%, hareng 82%, merlan 71%, saumon, maquereau. L'6ducation sanitaire devrait d6conseiller la consommation de poisson cru. Mais la seule prophylaxie efficace est la cuisson profonde fi 70°C ou la cong61ation gt -20°C pendant au moins 72 h, mesures non encore obligatoires dans la C.E.E., sauf en Hollande, ayant entrain6 une chute de l'incidence de l'anisakidose humaine.
Mots-clefs: Anisakis simplex, Pseudoterranova, Anisakidose, 6pigastralgies, fibroscopie. *Author for correspondence. 75
76
P. Bouree et al.
INTRODUCTION Anisakidosis is an uncommon parasitic disease. Because of some recent cases, a general review of the literature offers the opportunity of stating precisely the epidemiological, clinical and diagnostic features of this zoonose. CASE REPORTS Two groups of patients with anisakidosis were studied. The first group included 5 cases of patients with acute abdominal pain and confirmed diagnosis of anisakidosis (Table 1). The second group consisted of 20 patients with positive serodiagnosis (several bands in immunoelectrophoresis), including 9 acute and 11 chronic cases. The patients complained of epigastric pain (8 cases) and of intestinal disturbances (8 cases). The worms were located in the stomach (6 cases), in the intestine (6 cases), or their location was not determined (8 cases). The first group was an all male group, but in the second group, there was no significant difference between the sexes (11 males and 9 females). In all the cases, the patients had eaten raw fish, and 4 patients had eaten in an Asian restaurant. One of the cases was very interesting. A 32 year old female who had complained of digestive problems for 7 y had 710 eosinophiles/mm 3. Repeated stools examination were negative, but serological tests were positive for anisakidosis. After 10 days of treatment with thiabendazole, the clinical and biological symptoms disappeared. Four years later, on account of a dysphagy, fibroscopy analysis showed polyadenomatous polyps. It seems logical to find acute cases in the first group, where diagnosis was established using fibroscopy in 4 cases and retrospectively by serological analysis in 1 case. In the second group, where diagnosis was based only on serological tests, the chronic forms were the more frequent. Likewise, in the first group, the worms were in the stomach, whereas in the second group they were mostly in the intestine, with only 6 gastric locations out of 20 cases. DISCUSSION AND LITERATURE REVIEW The first description of a worm in fish was made in the 13th century. However, it was not until 1845 that Dujardin described a worm in dolphins as Anisakis (from the greek anisos = unequal and akis = point), a Class of Nematoda, Order Ascaridida, and Family Anisakidae. Table 1. Clinical features and diagnosis of 5 patients with acute anisakidosis Age (y)
Sex Symptoms
Gastroendoscopy
Other examinations
54
M
Sudden epigastric pain
Normal abdominal ultrasonography
20
M
Pseudo-ulcus pain
53 21 31
M M M
Acute epigastric pain Sudden retro-sternal pain Nocturnal epigastric pain with paroxysms
Hyperemia mucosa 1 larva Intestinal gastritis 1 larva 3 white nematodes 10 larvae fixed in the mucosa Not carried out
Normal ultrasonography and biological tests Normal ultrasonography WBC: DI: 19 800 leukocytes (89% Neutrophilic polymorphonucl) D30: 8 600 leukocytes (12% Neutrophilic polymorphonucl) serodiagnosis: 4 bands
Anisakidosis: a review
77
The first human case of anisakidosis (this name is now preferred to anisakiasis) was diagnosed in Holland in an eosinophilic granuloma, and in 1960 van Thiel established the relationship between the human disease and eating infested raw herring [1]. In 1968, a larva of Anisakis was observed directly for the first time using gastroendoscopy [2]. The first case in France was observed in a case of ileal eosinophilic granuloma, in 1969, by Calvet [3] and the first case in the U.S.A. was observed in 1975 by Pinkus [4].
Epidemiology The adult worm of Anisakis simplex also called herringworm or whaleworm (ranging from 3 to 15 cm in length), lives in the stomach of large marine mammals (dolphins, whales) or pinnipedia (seals, sea lions) [5]. After fecundation, the females lay eggs (40 x 50 #m, ovoid) which are distributed in the sea water. At a temperature of 5-7°C, the eggs hatch, and the young free-living larvae (stage 1) are ingested by the first intermediate host, small crustaceans (Euphausia) where the larvae moult from stage II to III. These larvae, after ingestion by fish, cross the digestive wall and live in the hemocele [6]. The older the fish, the more they are infested. These fish are then devoured by larger marine mammals, where the larvae moult into adult worms [7] (Fig. 1). The infested fishes are mostly sea fish, but some infested fishes have been found in briny and even in fresh water.
MARINE MAMMAL (definitive hosts) stomach adult worm
HUMANS .c (accidental hosts)
> feces eggs
(ingestion)
stage larvae
III
L
free eg! s in the ocean
larvae stage I
squids
fishes
larva~stage II
hatch out
(ingestion)
PLANKTONIC .., CRUSTACEANS
(intermediate hosts) Fig. I. Life cycle of Anisakis.
L
(ingestion)
P. Bouree et al.
78
Table 2. Pathogenesis of anisakidosis Delay after infection
Parasite
Host parasite reaction
Pathogenesis
~
Adhesion to mucosa and
Secretion of proteolytic enzymes
Haemorrhage, formation of a gallery
4-6 days
in the sub-mucosa Penetration of the mucosa
Secretion of chemotactic factor (ECF)
Eosinophilic granuloma, oedema,
7 14 days
Granuloma around the larva
/> 15 days
Dead larva
Immediate and delayed hypersensitivity Regression of the granuloma, persistent inflammation
necrosis Local and general allergic reaction*, crateriform lesion Spontaneous recovery, chronic ulceration
*Mostly in sensitized patients. ECF, eosinophil chemotactic factor.
It is possible that fresh water fishes are infested by eating larvae which were free living after the death of briny water fishes that swam up rivers [8]. Human infestation occurs by consuming raw fish. The larvae (stage III) invade the gastric mucosa. Eosinophilic granulomas are probably due to protease production by the parasites [9], with a host parasite cell-mediated hypersensitive reaction (Table 2). In the French cases, infestation was due mostly to the ingestion of raw herring (rollmops and red herring), and also mackerel, salmon or hake. Other animals may become infected by Anisakis, such as amphibians (bullfrogs), reptiles (turtles) or piscivorous birds (fulmars). Anisakidosis is more frequent in Asia (100-200 cases a year) but is seen also in Europe (5-25 cases a year) [10], in the U.S.A. [11], and more rarely in New Zealand [12] and in Egypt [13]. A total of more than 12,500 cases have been reported in Japan, and more than 500 in other countries, mostly in The Netherlands [14]. This disease can occur with other genera such as Contraceum osculatum (rarely) and Pseudoterranova (previously known as Phocanema) [15]. Pseudoterranova decipiens, also called codworm or sealworm, shows some differences to Anisakis [10] (Table 3). Pseudoterranovosis is found in the U.S.A. and in Japan. The larvae are located in the throat and in the stomach, but the intestinal chronic stage is very infrequent. Larvae of Anisakis and Pseudoterranova may be identified in histologic sections [16], and by electron microscopy [l 7]. Clinical aspects Among the 55 cases already published in France (probably underestimated), including our cases, 30 suffered from acute disease, 7 from chronic disease, while 18 were not Table 3. Differences between Anisakis and Pseudoterranova Geographical distribution
L(/# Q'ele Definitive hosts Eggs 1st intermediate host 2rid intermediate host
Larvae (Stage III) Size Colour Cuticle Histologic section
Anisakis simple.,:
Pseudoterranova decipiens
World wide polar zones+ +
Both temperate and polar zones
Whales
Seals
Ocean Euphausiids Zooplankton-feeding fish, squid Long ventriculus 28.4 x 0.49 mm (Japan) 17.0 x 0.41 mm (China) White Thin, without electron dense nods Y-shaped lateral cords
Ocean Benthic copepods, amphipods, decapods Zoobenthos-feeding fish Ventriculus partly covered with cecum
60-80 intestinal cells
32.6 x 0.80 mm Red Thick, with electron dense nods Butterfly-shaped lateral cords /> 100 intestinal cells
Anisakidosis: a review
79
Table 4. Delay in the appearance of symptoms after ingestion of raw fish [18] Location Delay (h)
Gastric
Intestinal
3 6 12 24 48 />48 unknown
15% 41% 16% 2% 3% 3% 20%
4% 4% 4% 18% 20% 11% 39%
Table 5. Study of 55 French cases of anisakidosis Contamination
Location of larvae or of eosinophilic granulomas
Symptoms
Herring Other fish Asian restaurant Not determined
18 26 2 9
Epigastralgy Obstruction Appendicular syndrome Abdominal pain Various Chance detection Not determined
18 8 3 3 4 I 18
Gastric Intestinal Colic Mesenteric Rhino-pharyngeal Not determined
25 16 3 1 1 9
determined. The disorders appeared with varying delays according to the location of the worm (Table 4) [18]. Generally, the clinical symptoms of acute intestinal anisakidosis include violent epigastric pain [19], nausea, vomiting, diarrhoea (Table 5), and sudden abdominal pain similar to an acute abdominal syndrome such as intestinal obstruction [20], appendicitis [21] or peritonitis [22]. Additional disorders have been reported such as urticaria [23], pulmonary disturbances [24], allergic oedema [25], hypersialorrhoea [26] or polyarthritis [27]. Sometimes, the disorders decrease spontaneously and definitively within a few days [28] even in cases of tumours, hence the term "vanishing tumour" of the stomach [14]. In some cases, the disease is asymptomatic, as shown by Spehn who accidentally found larvae when using gastroendoscopy for a case of oesophageal candidiasis [29]. Chronic anisakidosis produces mild symptoms such as abdominal pain, nausea, vomiting, with diarrhoea followed by constipation, and sometimes bloody stools, suggesting a colonic tumour of the stomach [30].
Table 6. Serological cross-reactions in a patient infested with anisakidosis Serodiagnosis Blood eosinophilia Anisakiasis Filariasis Larva migrans Trichinellosis Hydatidosis Schistosomiasis Hypodermosis Fasciolasis *Non significant rate.
D.30 1050/mm3
D. 150 70/mm 3
4 bands 1/80°* N 1/400°* 1/500° 1 band 1/80<~* 1 band 1/160<'*
N N N N N N 1/80°* N 1/160<'*
Methods Immuno-electrophoresis Indirect fluorescent antibody test counter-electrophoresis indirect fluorescent antibody test haemagglutination counter-electrophoresis haemagglutination lmmuno-electrophoresis Haemagglutination
P. Bouree et al.
80
Table 7. Macroscopic findings in anisakidosis Location Gastric
Acute
Chronic
Larvae move actively in the early phase of penetration, and move slowly later Site of penetration: oedematous erosion and bleeding
Intestinal
Erosion or ulcer Oedema Tumour-like nodule
Ascitis fluid, with free worms
Mild symptoms
30% eosinophil cells
Granulomatous changes which induce narrowing of the intestinal lumen
Omentum: mild oedema with hyperemia, and inflammation Fibrinous adhesions
Larvae pass through the wall creating granulomas in the peritoneal cavity
Inflammatory changes in the terminal ileum
Diagnosis and treatment
During the first week after infection, blood tests do not show any disturbances. The blood eosinophilia count increases after 8-15 days [31] and parasitic stools examination remains negative. Immunodiagnosis tests become positive after the tenth day and are negative between 6 and 12 months [32]. A micro-Elisa test [14] with monoclonal antibodies seems very specific [33], as is the Western Blot test [34]. Serodiagnosis is of no use in acute disease, when diagnosis and treatment are decided within a few hours of the onset of the disease. There is a great deal of cross reactivity (Table 6). However, serological tests are very important in chronic anisakidosis where diagnosis by endoscopy is not possible. An increase in specific IgE, with the RAST test [35] has been noticed over a period of about 2 months [36]. Table 8. Histological findings in anisakidosis Location Gastric
Acute stage Thickening of gastric wall Intact and clearly visible larvae in the submucosal layer Oedema and massive eosinophilia mixed with neutrophil, macrophage and lymphocyte infiltration
Chronic stage Ist stage: phlegmonous type = " a n Arthus-type" reaction, eosinophilic infiltration with occasionally living larvae 2nd stage: abcess type slightly degenerating larvae surrounded by necrotic tissue with oedema and fibrin exudation 3rd stage: abscess granuloma type > 6 months from the time of infection; debris of larvae surrounded by granulatous tissue and lymphocyte infiltration 4th stage: granuloma type larval debris surrounded by granulomatous tissue with fibrosis, foreign body giant cell lymphocytes
Intestinal
Thickening of the wall by intensive oedema
Similar to mild type of gastric anisakidosis
Numerous eosinophils, neutrophils, macrophages and lymphocytes
I st stage: phlegmonous type similar to acute type
Fibrin exudation
2nd stage: abcess type slightly degenerating larva surrounded by massive necrotic tissue
Small haemorrhages Hyperplasia of lymphoid follicles
3rd stage: abcess granuloma type intensively degenerated worm at the centre of lymphocyte infiltration 4th stage: granuloma type (rare) unidentified debris in a granuloma
A n i s a k i d o s i s : a review
81
The gastroendoscopic findings, which represent an urgent examination, include oedema and hyperaemia of the mucosa [37], sometimes with ulcerations [38]. Anisakis larvae can be detected with gastroscopy, and easily removed during the acute stage, following which the epigastric pains disappear immediately [39, 40]. The macroscopic findings vary according to the stage of the anisakidosis (Table 7). Gastric X-rays show thickened and rigid longitudinal gastric mucosal folds (81%), and sometimes the larva itself as a filiform shadow of the nematode (48%) [4!]. Moreover, digestive disturbances can appear as dilatation of the intestinal lumens [42] or ascitis fluid [43]. With ultrasonography, it is possible to observe an enlarged local or general wall [44]. Endoscopy, with 0.1% indigo carmin solution, shows a good contrast with the larvae being more visible. At the chronic stage, diagnosis is established through the histopathology of the lesion, showing eosinophilic granulomas and cross sections of Anisakis larvae, with the characteristic Y lateral cords [45]. The pathological features differ according to the stage of the disease and the location of the larvae (Table 8). The larvae do not migrate, and degenerate in about 8 weeks [46]. Some extra gastro-intestinal locations of Anisakis larvae have been described in Japan, e.g. in the abdominal wall, omentum, mesentery, liver, pancreas, ovary, lymph mode, pleural cavity tongue, and even uvula [14]. In relation to the observation of chronic anisakidosis with a polyadenoma [47], it is very interesting to note that in countries where gastric cancer is very frequent, such as Japan and Chile, raw fish is a very common meal. The development of eosinophilic granulomas into cancer is a hypothesis which requires further examination.
Prophylaxis Surveys in several fish markets have revealed significant infection of herring and mackerel [48, 49] (Table 9). After several alarmist campaigns in different countries (e.g. Germany and Italy), the consumption of sea fish dramatically decreased [50]. In order to avoid discriminatory measures towards any country, the European Union has suggested some procedures in relation to fishing, because this parasitosis is seen in all European fisheries [51]. Early evisceration is recommended because the worms leave the digestive tract within a few days to go into the muscles [52], in addition, freezing at - 2 0 ° C for 3 days, or heating to 70°C, as larvae often survive at 50°C. Microwave oven cooking
Table 9. Fish parasitism in fish-markets
Boulogne 1986 [49] Fishes Herring Whiting Mackerel Hake Rose fish Chinchard Gurnard Sardines Anchovy Plaice
Paris 1986 [48]
Paris 1990 [13]
No. investigated
No. infested
No. investigated
% infested
No. investigated
No. infested
I0 4 8
8 4 5
682 84 214 35 36 40 29 22 27
82% 71% 30% 88% 86% 62% 86% 4% 3%
6 13 30 i0
5 9 15 I0
5
0
82
P. Bouree et al,
w o u l d be insufficient to d e s t r o y larvae [53]. The larvae resist salting, s m o k e - c u r i n g a n d m a r i n a d i n g , a n d 51 d a y s in vinegar [16]. Several factors m a y explain the s p r e a d i n g o f a n i s a k i d o s i s [13]. The p r o t e c t i o n o f cetacea a n d p i n n i p e d i a leads to the p r o l i f e r a t i o n o f definitive hosts. The p o p u l a t i o n o f Euphausia, i n t e r m e d i a t e hosts and the prey o f choice for herring, a n d an increase in p l a n k t o n , could c o n t r i b u t e to infection o f the fishes. In line with m o d e r n m e t h o d s o f fishing, fish are n o t gutted immediately, b u t are stored in a cold r o o m . Thus, the larvae leave the gut a n d enter the muscles [54]. The evisceration o f fishes, within a few h o u r s after fishing, seems insufficient, as larvae m i g r a t e very early into the flesh [55]. The present fashion o f " n a t u r a l c o o k i n g " with raw f o o d also increases the risk. Sometimes, careful e x a m i n a t i o n o f a meal can lead to the detection o f some larvae by chance [56]. Finally, the absence o f i n t e r n a t i o n a l rules a b o u t this question results in ineffective protection. However, in The N e t h e r l a n d s , o b l i g a t o r y freezing before sale has led to the virtual d i s a p p e a r a n c e o f this disease, whereas with J a p a n e s e culinary traditions, anisakidosis is a real public health p r o b l e m . A n i s a k i d o s i s has shown a m a r k e d increase in recent years because o f the fashion o f eating raw fish, p a r t i c u l a r l y herring. A c u t e cases, gastric in J a p a n a n d intestinal in E u r o p e , m u s t be considered when digestive disorders occur a few hours after the c o n s u m p t i o n o f raw fish. C h r o n i c anisakidosis is m o r e difficult to diagnose, b u t at the m o m e n t , i m m u n o l o g i c a l tests are the most suitable.
REFERENCES 1. Van Thiel P, H., Kuipers F. C. and Roskam R. A nematode parasite to herring, causing acute abdominal syndromes in man. Trop. geogr. Med. 2, 97 ll3 (1960). 2. Namiki M. A history of research into gastric anisakiasis in Japan. In Gastric Anisakiasis in Japan (Edited by H. Ishikura and N. Namiki), pp. 13-18. Springer-Verlag, New York (1989). 3. Calvet J. P., Zuckmann P. and Texier J. Granulome 6osinophile allergique parasitaire de l'il6on. M~m. Acad. Chit. 95, 648-651 (1969). 4. Pinkus G. S., Coolidge C. and Little M. D. Intestinal anisakiasis. First case report from North America. Am. J. Med, 59, 114-120 (1975). 5. Smith J. W. and Wootten R. Anisakis and Anisakiasis. Adv. Parasit. 16, 93-163 (1978). 6. Petithory J. C. and Many B. L'anisakiase en France. Lettre Infectiologue III, 2, 96-99 (1988). 7. Bouree P. Anisakiase. Encyel. M~d. Chir. Mal. Inf. 8118, Bl0 (1989). 8. Shiraki T. Larval nematode of family anisakidae in the northern sea in Japan, as a causative agent of eosinophilic phlegmon or granuloma in the human gastro intestinal tract. Acta. reed. biol. 22, 57-98 (1974). 9. Sakanari J. A. Anisakis, from the platter to the microfuge. Parasit. Today 6, 323-327 (1990). 10. Feldmeier H., Poggensee G. and Poggensee U. The epidemiological, natural history and diagnosis of human Anisakiasis. Europ. Microb. 2, 30-36 (1993). ll. Malkin J. E., Lafaix C., Prazuck T., Haroche G., Fish A. Anisakiase. Med. Hyg. 45, 680-687 0987). 12. Paltridge G. P., Faoagali J. L. and Angus H. B. Intestinal anisakiasis: a new New-Zealand disease. N.Z. Med. J. 558-559 (1984). 13. Cocheton J. J., Cabout I. and Lecomte I. Anisakiase et infection par les anisakid6s. Annls M~d. int. 142, 121-130 (1991). 14. Ishikura H., Kikuchi K., Nagasawa K., Ooiwa T., Takamiya H., Sato N. and Sugane K. In Anisakidae and Anisakidosis in Tsieh Sun, Progress in Clinical Parasitology. Springer-Verlag, New York (1993), 15. Huang W. and Bussieras J. Anisakides et anisakidoses humaines. Premidre partie: donn6es bibliographiques. Annls Parasit. hum. comp. 63, 119-132 (1988). 16. Sakanari J. A. and McKerrow J. H. Anisakiasis. Clin. Microb. Rev. 2, 278-284 (1989). 17. Fredericksen D. W. and Specian R. D. The value of cuticular fine structure in identification of juvenile anisakine nematodes. J. Paras#. 67, 647-655 (1981). 18. Asaihi K., Nishino C., Totsuka M., Hayasaka H. and Suzuki T. Studies on the etiologie mechanism of anisakiasis. Epidemiologic study of inhabitants and questionnaire survey in Japan. Gastro-emeroL Jap. 15, 128-134 0980).
Anisakidosis: a review
83
19. Bouree P., Taugourdeau Ph., Juette P. and Blanquart A. Anisakiase. Apropos de 5 cas. Bull. Soc.fr. Parasit. 8, 267 270 (1990). 20. Boucaut P., Chome J., Lame C. and Holier C. Occlusion r6v61atrice d'un granulome 6osinophile parasitaire de l'intestin gr61e. Nouv. Presse Mdd. 9, 2918 (1980). 21. Rushovch A. M., Randall E. L., Caprini J. A. and Westenfelder G. O. Omental anisakiasis: a rare mimic of acute appendicitis. Am. J. clin. Path. 80, 517-520 (1983). 22. Yokogawa M. and Yoshimura H. Clinicopathologic studies on larval anisakis in Japan. Am. J. trop. Med. Hyg. 6, 723-724 (1967). 23. Kasuya S., Hamano H. and Izumi S. Mackerel induced urticaria and anisakis. Lancet 335, 665 (1990). 24. Kobayashi A., Tsuji M. and Wilbur D. L. Probable pulmonary anisakiasis accompanying pleural effusion. Am. J. trop. Med. Hyg. 34, 310-313 (1985). 25. Godeau P., Danis M., Bouchareine A. and Nozais J. P. Une cause inhabituelle d'oed6me segmentaire: l'anisakiase. Presse Med. 15, 1246-1247 (1985). 26. Letoquart J. P., Friguet J. L., Bigant E. and Mambrini A. Un nouveau cas d'anisakiase gastrique et p6riton6ale. J. Chir. 124, 389 390 (1987). 27. Fabresse F. X., Essioux H., Meyran M., Laroque P. and Celton H. Polyarthrite de ranisakiase--Premier cas. Presse Mkd. 13, 1004 (1984). 28. Bouree P. and Zetlaoui J. Anisakiase aigue avec r6gression spontan6e. Presse Med. 18, 1885 (1989). 29. Spehn J., Schonbeck S., Koperski K. and Butzow G. H. Atypical anisakiasis in an acquired immune deficiency syndrome patient. D. Med. Wschr. 24, 983-984 (1988). 30. Shirahama M., Koga T., Uchida S., Miyamoto Y. and Ohta Y. Colonic anisakiasis simulating carcinoma of the colon. Am. J. Roentgen 155, 895 (1990). 31. Petithory J. C., Verrier F. and Guyet-Rousset P. Etude biologique d'un cas d'anisakiase colique. Revue de la litt6rature. Path. Biol. 40, 47-51 (1992). 32. Petithory J. C., Lapierre J., Rousseau M. and Clique M. T. Diagnostic s6rologique de l'anisakiase (granulome ~osinophile digestif) par pr6cipitation en milieu g61ifi& (Ouchterlony, 61ectrosyn6r~se, immuno61ectrophor6se). Med. Mal. Inf. 3, 157-162 (1986). 33. Yagihashi A., Sato N., Takahashi S., Ishikura H. and Kikuchi K. A serodiagnostic assay by microenzymelinked immunosorbent assay for human anisakiasis, using a monoclonal antibody specific for anisakiasis larvae antigen. J. infect. Dis. 161, 995-998 (1990). 34. Petithory J. C., Rousseau M. and Siodlak F. Donn6es s6ro6pid6miologiques sur l'anisakiase. Cons6quences prophylactiques pour les produits de la p6che. Bull. Acad. natn. Med. 175, 273 279 (1991). 35. Desowitz R. S., Raybourne R. B., Ishikura H. and Kliks M. M. The radio allergo sorbent test (RAST) for the serological diagnosis of human anisakiasis. Trans. Roy. Soc. trop. Med. Hyg. 75, 256~59 (1985). 36. Deardorff T. L., Fukumura T. and Raybourne R. B. Invasive anisakiasis. A case report from Hawai. Gastro-ent~rol. 90, 1047-1050 (1986). 37. Fugino T., Ooiwat T. and Ishi Y. Clinical, epidemiological and morphological studies on 150 cases of gastric anisikiasis in Fukuoka Prefecture. Jap. J. Parasit. 33, 73-92 (1984). 38. De Montigny S., Prevot S. and Basset D. Anisakiase gastrique: gu6rison apr6s extraction endoscopique retard6e. Presse M~d. 20, 180 (1991). 39. Bouree P., Juette P. and Kloeti G. Anisakiase: diagnostic et extraction par endoscopie gastrique. Presse Med. 1484-1485 (1987). 40. Ikeda K., Kumashiro R. and Kifune T. Nine cases of acute gastric anisakiasis Gastro-intestinal Endosc. 35, 304-308 (1989). 41. Sugimachi K., Inokuchi K., Ooiwa T., Fujino T. and Ishii Y. Acute gastric anisakis--Analysis of 178 cases. J.A.M.A. 253, 1012-1013 (1985). 42. Watt I. A., McLean N. R., Girwood R. W., Kissen L. H. and Fyfe A. H. B. Eosinophilic gastroenteritis associated with a larval anisakine nematode. Lancet ii, 893-894 (1979). 43. Picard D., Herbinet B. and Alexandre J. H. Syndromes abdominaux aigus et anisakiase: revue de la litt6rature ~i propos d'un cas r~cent. Ann. Chit. 33, 40-44 (1979). 44. Yano M., Yokomizo S. and Nakayama T. Ultrasonic examination. In Gastric Anisakiasis in Japan (Edited by H. Ishikura and N. Namiki), pp. 77-84. Springer-Verlag, Berlin (1989). 45. Dooley J. R. and Neafie R. C. Anisakiasis. In Pathology of Tropical and Extraordinary Diseases, (Edited by C. Binford and D. Conner), pp. 475-481 Armed Forces Inst. Pathol., Washington, U.S.A. (1976). 46. Hsiu J. G., Gamsey A. J., Ives C. E., D'Amato N. A. and Hiller A. N. Gastric anisakiasis: report of a case with clinical, endoscopic and histological findings. Am. J. Gastro-ent. 81, 1185-1187 (1986). 47. Petithory J. C., Paugam B., Buyet-Rousset P. and Paugam A. Anisakis simplex, a co-factor of gastric cancer? Lancet 2, 1002 (1990). 48. Huang W. Anisakides et anisakidoses. Enqu6te sur les anisakid6s de poissons commerciaux du march6 parisien. Annls Parasit. hum. comp. 63, 197-208 (1988). 49. Mudry J., Lefebvre P., Dei-Cas E., Vernes A., Doirriel J., Debat M., Marti R., Binot A. and Cortot A. Anisakiase humaine: 5 cas dans le Nord de la France. Gastro-ent. clin. Biol. 10, 83-87 (1986).
84
P. Bouree et al.
50. Hubert B., Bacou J. and Belveze H. Epidemiology of human anisakiasis: incidence and sources in France. Am. J. trop. Med. Hyg. 40, 301-303 (1989). 51. Angot V. and Brasseur P. Epid6miologie et prophylaxie de l'Anisakiase. Enqu6te sur l'infestation de 3 especes de consommation courante en France. Bull. Epid. Hebd. Paris 14, 59-60 (1993). 52. Declerck D. Pr6sence de larves de Anisakis simplex dans le hareng (Clupea harangus). Rev. Agric. 41, 971-980 (1988). 53. O.M.S. Anisakiase. Un cas dans l'Alberta. Rel. Epid. Hebd. Gen~ve 14, 106-107 (1990). 54. Acha P. N. and Szyfres B. Anisakidose in Zoonoses. Ed. Off. int. Epiz. 854-861 (1989). 55. Smith J. W. and Wooten R. Experimental studies on the migration of Anisakis sp larval into the flesh of herring Clupea harrengus. Int. J. Parasit. 5, 133-136 (1975). 56. Pelloux H., Pinel C. and Ambroise-Thomas P. Larves d'Anisakidae: d6tection dans la chair des poissons et pr6vention de l'anisakiase humaine. Med. Mal. Inf. 22, 939-940 (1992).