Gut, 1988, 29, 843-847

Case report

Anisakiasis caused by herring in vinegar:a little known medical problemM A M VERHAMME AND C H R RAMBOER

From the Department ofGastroenterology, Kliniek Maria's Voorzienigheid, Kortrijk, Belgium

SUMMARY Six cases of intestinal anisakiasis, or herring worm disease, diagnosed over a two yearperiod in a Belgian gastroenterology unit are described. They presented mainly as intestinalobstructions and larvae of this marine nematode were found in the intestinal wall of two of the fourpatients who were operated on. In two other patients awareness of the diagnosis permittedconservative treatment and spontaneous healing. In five patients symptoms developed after they hadeaten herring marinated in vinegar, a hitherto little known source of the herring worm disease.

Anisakiasis or the herring worm disease is theinfestation of man by species of marine nematodelarvae belonging to the subfamily Anisakainae, whichis further divided into three types: Anisakis,Contracoecum and Phocanema. The adult round-worms are intestinal parasites of marine mammalssuch as seals and dolphins. Ova passed in the faecesof these mammals hatch in the water, where theresulting larvae are ingested by crustaceans, which inturn are eaten by fish and squid. The larvae mature inthe viscera and muscles of the fish, ultimately reach-ing an infective stage.When inadequately prepared fish is eaten by man,

the Anisakis larvae penetrate the mucosa of thestomach, the small intestine, or even the colon,causing an acute focal inflammation. Commonlyeaten fish like herring, salmon, cod, pollack, andmackerel are frequently infected with the larvae,' 2

which are resistent to environmental changes.Anisakiasis is often diagnosed in Japan, where it is ahealth hazard because of Japanese culinary habits. Itis remarkable that this syndrome is rarely diagnosedin most European countries except the Netherlands,and reports from North America are extremelyrare. ' k5

Over a two year period six presumed cases ofintestinal anisakiasis were seen in our unit, five ofAddress for correspondence: Dr M Verhamme, Klinick MV. Loofstraat 43, B85(X) Kortrijk Belgium.Received for publication 4 December 1987.

them occurring after the patients had eaten herringcommercially pickled in vinegar, a little knownsource of the disease.

Case reports

PATIENT 1

This 43 year old man, who had had an appendec-tomy, was admitted for vomiting and abdominal painon 5 April, 1984. An x-ray examination of theabdomen suggested a small bowel obstruction; abarium enema proved normal. The white cell countwas 7200. He underwent surgery on the same day.The abdomen contained dark fluid, and a bowelsegment in the midileum was severely inflamed andso was resected. Pathological examination showedconsiderable oedema of the bowel wall along withdense infiltration with inflammatory cells and eosino-phils, and some interstitial haemorrhage. In thesubmucosa a transverse section through a parasiteconsistent with Anisakis Marina larva was noted(Fig. 1). Later, the patient reported he frequently ategreen herring, and two days before admission he hadeaten pickled herring.

PATIENT 2

This 65 year old man, who had had surgery for aninguinal hernia, was admitted to hospital on 25 May,1984 after a day of vomiting and abdominal cramps.The day before, he had eaten pickled herring, which

843

on February 26, 2020 by guest. P

rotected by copyright.http://gut.bm

j.com/

Gut: first published as 10.1136/gut.29.6.843 on 1 June 1988. D

ownloaded from

Verhamtne and Ratmiboer

Fig. 1 Transverse section through a larva ofAnisakismarina in the inflamed ileum ofpatient 1.

he consumed almost weekly. The white cell countwas 10 300 with 3% eosinophils. An x-ray examina-tion of the abdomen showed a bowel obstruction.Laparotomy one day later revealed the presence ofserous peritoneal fluid and a acutely inflamedterminal ileum with thickening of the mesenterium.In view of the major bowel obstruction a resection ofthe inflamed segment was carried out. Histologicalexamination revealed acute eosinophilic enteritis.

PATIENT 3This 53 year old man was admitted on 7 June, 1984with abdominal cramps and a history of passing bloodin the stools. The white cell count was 10 300 with 1%eosinophils. A barium enema showed a circularstenosing mass in the caecum very suggestive of atumour (Fig. 2). Dilated small bowel loops indicatedan obstruction. When a laparotomy was done fivedays later the tumour seemed to have vanished,although there was still a localised thickening of thecaecum wall. A right hemicolectomy was carried outand histological examination showed oedema anda predominantly eosinophilic infiltrate. Laterquestioning revealed that the patient was accustomedto eat herring pickled in vinegar and had done so onthe day before his admission.

Fig. 2 Pseudotumouralform ofanisakiasis in patient3.Note the circularstenosing mass in ascending colon.

PATIENT 4During a journey in South America, this 62 year oldbusinessman ate fish in Chili and also raw salmonduring a flight from Chili to Brazil. Eight hours laterhe suffered abdominal cramps and returned toBelgium. On admission on 27 November, 1985 aradiograph showed an obstruction of the smallbowel. The white cell count was 4900 (4%eosinophils). Conservative treatment reduced theabdominal cramps, and the radiological signs ofintestinal obstruction disappeared. A barium mealfive days later showed slow intestinal transit with anarea of oedematous folds at the transition of a slightlydilated jejunum to a normal ileum. A repeat bariummeal three weeks later was completely normal.

PATIENT 5This 44 year old man complained of abdominalcramps some 12 hours after eating herring pickled invinegar. He was admitted on 20 January, 1986, andradiograph showed an obstruction of the smallbowel. The white-cell count was 11 100 (2%eosinophils). In view of the anamnestic data,a conservative approach was selected withprednisolone intravenously 50 mg/day. A bariumenema showed no abnormalities, and a barium meal

844

on February 26, 2020 by guest. P

rotected by copyright.http://gut.bm

j.com/

Gut: first published as 10.1136/gut.29.6.843 on 1 June 1988. D

ownloaded from

Anisakiasis caused by herring in vinegar: a little known medicalproblem

Fig. 3 Transverse section through an Anisakis marina larva found in the wall of the terminal ileum ofpatient 6.

four days later revealed only a slight dilatation ofsome small bowel loops. He made an uneventfulrecovery.

PATIENT 6This 56 year old woman ate herring pickled in vinegaron 6 and 7 February, 1986. A few hours later shecomplained of diffuse abdominal pain. On admissionthe next day there was a marked tenderness of theright iliac fossa, and a white cell count of 9500. As anacute appendicitis was suspected she was operatedon. An inflammation of the ileocaecal valve andcaecum was found and a limited resection of this areawas carried out. Pathological examination revealedan acute inflammatory and eosinophilic infiltratetogether with the presence of a worm larva in theileum mucosa, which was considered an Anisakismarina larva (Fig. 3).

Discussion

Anisakiasis or the herring worm disease is perhaps anuncommon but possibly also an underestimateddisease in Belgium and in most European countries.Documented reports from Belgium,"9 the UnitedKingdom,""' France,'"'4 and North America' '5,5 arefew and usually give only one case. Anisakiasis is acommon problem in Japan""18 and one could expectan increasing incidence in the West as enthusiasm forraw fish is growing, reflected in the popularity of

Japanese restaurants with their uncooked seafoodand the socalled 'sushi-bars'.'

Before 1968, it was a common problem in theNetherlands largely because of the consumption ofgreen herring ('maatjes') which is only lightlysalted.2'-"4 Since then, compulsory freezing to -20°Cof all fish before marketing has virtually eradicatedanisakiasis in this country. The infective larvae arekilled by freezing at -17° to -20°C for 24 hours andalso by heating at 60°C for a few minutes.'526 Theyare, however, quite resistant to the environment andare unaffected by salting, smoking, or pickling invinegar.'226 Early evisceration of the fish immedi-ately after being caught, once thought to be useful, isprobably of little value in preventing infection in manas most fish have larvae in the muscles as well as in theviscera.Most cases of anisakiasis occur after ingestion of

raw or undercooked fish. As far as we know, therehave been no documented case reports of anisakiasiscaused by herring pickled in vinegar. Although wedid not examine pickled herring for the presence oflarvae, living larvae of Anisakis marina were recentlyrecovered from pickled herring in The Netherlands.27During the course of two years we dealt with six casesof anisakiasis, five of which occurred after eating ofherring commercially pickled in vinegar. One caseoccurred after eating raw fish in South America.

Experimental studies in rabbits26 29 have shown thefollowing pathological sequence: penetration of the

845

on February 26, 2020 by guest. P

rotected by copyright.http://gut.bm

j.com/

Gut: first published as 10.1136/gut.29.6.843 on 1 June 1988. D

ownloaded from

Verhamme and Ramboer

larvae into the mucosa and submucosa provokesoedema, followed some 24 to 48 hours later byinfiltration with predominantly eosinophilic granulo-cytes, and, after about 96 hours, local necrosis andhaemorrhage and the death of the larvae. Thishistological picture of acute eosinophilic phlegmonwas found in all our operated patients. Some reportsdescribe granuloma formation, but this was not seenin our patients, perhaps because the time betweenthe initial manifestation and surgery was rather short.To explain the discrepancy between a probably

considerable consumption of larvae bearing fish andthe seemingly low incidence of clinical anisakiasis,the hypothesis of 'the double strike' was developedbased on experiments in rabbits:26 28 the initialpenetration of the mucosa usually provokes only aminor reaction, but leaves a local hypersensitivitythat gives rise to intense inflammation when a newpenetration occurs. This reaction would then beworse the closer the two penetrations are in time anddistance. Most of our patients were, indeed, regularconsumers of herring. A first penetration, however,might also provoke a florid inflammation.2sThe site of the penetration (stomach, jejunum,

ileum or colon) determines the clinical form. All ourpatients presented acute abdominal pain togetherwith an intestinal obstruction or an appendicitis likesyndrome. Four were operated on, partially becausewe were unfamiliar with the syndrome but also toexclude either other causes of intestinal obstruction(patients 1, 2, 3) or acute appendicitis (patient 6). Wedid not see a gastric form of anisakiasis, in which ithappens to find penetrating larvae and to removethem by gastroscopy, thereby making a correctdiagnosis and at the same time providing an effectivetherapy.'3'48 Few cases of gastric anisakiasis havebeen described in Europe, whereas in Japan it seemsto be the predominant form.'8 It has been suggestedthat a relatively high frequency of gastric achlor-hydria or hypochlorhydria in Japan could play apredisposing role. 7 These gastric cases present acuteepigastric pain, nausea, and vomiting a few hoursafter ingestion of infected fish. A more chronic formwith granuloma formation and a more indolentsymptomatology is also known.241' Gastricanisakiasis can be misdiagnosed as peptic ulcer, acutegastritis, food poisoning, polyps, or neoplasia.

In Europeans, the intestine seems to be the mostcommon site of anisakiasis. The symptoms mayinclude diffuse abdominal tenderness or colickyabdominal pain, nausea, and vomiting. The syn-drome is often incorrectly diagnosed as acuteappendicitis or regional ileitis. Further differentialdiagnosis includes intussusception, ileus, diverticu-litis, and neoplasia. Especially the colonic form,which is infrequent, may simulate a tumour of the

colon as was the case in patient 3. In rare cases thelarvae migrate into the mesenterium and evenmigration into the liver, pancreas, greater omentumof gall bladder has been described.

It is usually stated that the symptoms occur withinseven days after the ingestion of the infected fish, butall our patients had symptoms within two days.Although an abdominal condition requiring surgeryis often simulated, the natural course of intestinalanisakiasis is usually good in the absence of perfora-tion and peritonitis. On the other hand, the diagnosisis difficult to make clinically and is dependent uponan accurate history, an appropriate degree ofsuspicion and a close follow up of the patient.Radiological investigations are useful in excludingother conditions. The white cell count and bloodeosinophilia do not help in making the diagnosis andserological tests are of limited value." Mostcommonly the final diagnosis hinges upon surgicalresection and the pathologist's search for larvalfragments within the inflamed tissue, this being thefinal proof of the diagnosis (see patients 1 and 6).Larvae cannot always be found in resectedspecimens,2 however, as they may disappear bymigration, desintegration, and resorption. So thepathognomonic presence of the larvae can not be aclaim for the diagnosis of anisakiasis. We thereforesuggest that the combination of an acute regionaleosinophilic enteritis, along with a history of recentingestion of potentially infected fish, should allow thediagnosis (our patients 2, 3). In a Japanese series of1531 cases of acute and chronic regional enteritis, itwas suggested on re-examination of the histologicpreparation that half of the cases might have beenanisakiasis. 7 Furthermore surgery is usually unneces-sary as most cases resolve spontaneously. So, theparadox of anisakiasis is that the medical treatment isthe treatment of choice for a condition that can onlybe definitely diagnosed by finding larvae in a resectedspecimen. We propose, however, that in the absenceof dramatic abdominal signs and in the presence of asuggestive history (recent ingestion of infected fish)the diagnosis of anisakiasis is acceptable and aconservative treatment should be followed. We areaware that in these cases the diagnosis is ratherspeculative but one may avoid unnecessary surgery,as in our patients 4 and 5. In the latter the disappear-ance of inflammation seems to have been acceleratedby the administration of corticosteroids which maywell be a helpful adjuvant therapy. Penetration of thelarvae through the intestinal wall indeed provokes aflorid inflammatory reaction that is usually self-limiting and results in the death of the parasite. Ashort anti-inflammatory treatment thus seemsjustified instead of anti-helmintic agents which areineffective.

846

on February 26, 2020 by guest. P

rotected by copyright.http://gut.bm

j.com/

Gut: first published as 10.1136/gut.29.6.843 on 1 June 1988. D

ownloaded from

Anisakiasis caused by herring in vinegar: a little known medicalproblem 847

In conclusion, we suggest that anisakiasis might bemore common than expected, as only the worst casesare admitted into the hospital, and even then onlysome are properly diagnosed. It seems likely thatonly the tip of the iceberg is seen and that many of theless severe cases remain undiagnosed, the conditionbeing considered transient gastroenteritis. Patientswith recent abdominal pain or intestinal obstructionshould always be asked about the intake of herring orother uncooked fish. In this way, unnecessarysurgical procedures may be prevented. The disease iscompletely preventable either by proper preparationof the fish or by general measures such as prolongedfreezing of the fish before marketing.

The authors wish to thank Dr N Inderadjaja whoreviewed the slides and identified the parasites, andDrs P Hinnekens and H Ceuppens for the surgicalfindings, and Mrs Magda Demeijer-Ducatteeuw forpreparing the manuscript.

References

1 Valdiserri RO. Intestinal anisakiasis. Report of a caseand recovery of larvae from market fish. Am J ClinPathol 1981; 76: 329-33.

2 Rosset JS, McClatchey KD, Higashi GI, Knisely AS.Anisakis larval type I in fresh salmon. Am J Clin Pathol1982; 78: 54-7.

3 Pinkus GS, Coolidge, C, Little MD. Intestinalanisakiasis. First case report from North America. Am JMed 1975; 59: 114-20.

4 Appleby D, Kapoor W, Karph M, Williams S.Anisakiasis. Nematode infestation producing small-bowel obstruction. Arch Surg 1982; 117: 836.

5 Rushovich AM, Randall EL, Caprini JA, WestenfelderGO. Omental anisakiasis: a rare mimic of acuteappendicitis. Am J Clin Pathol 1983; 80: 517-20.

6 Hinnekens P, Van Landuyt JC. Een geval vanharingwormziekte. Tijdschr Gastroenterol 1969; 12:251-9.

7 Fain A, Van Roy M, Fontanelle E. Een geval vanharingwormziekte in Belgie. Tijdschr Geneesk 1970; 26:40-2.

8 Rutgeerts L, De Coster M, Tytgat G, Tanghe W.Eosinofiel flegmoon van de dunne darm door Anisakis.Tijdschr Gastroenterol 1975; 18: 113-8.

9 Dehertog, P. Een pseudo-tumorale vorm vanharingwormzietke. Tijdschr Gastroenterol 1976; 19:205-13.

10 Lucas SB, Cruse JP, Lewis AAM. Anisakiasis in theUnited Kingdom. Lancet 1985; ii: 843-4.

11 Watt IA, McLean NR, Girdwood RWA, Kissen LH,Fyfe AHB. Eosinophilic gastroenteritis associated witha larval anisakine nematode. Lancet 1979; ii: 893-4.

12 Picard D, Herbinet B, Alexandre JH. Syndromesabdominaux aigus et anisakiase. Revue de la litterature

a propos d'un nouveau cas recent. Sem H6p Paris 1979;55: 1284-8.

13 Cocheton JJ, Gombeaud Th, Ferroir JP. Anisakiaseduod6nale aigue. Extraction endoscopique. Presse MMd1984; 13:744.

14 Fabresse FX, Essioux H, Meyran M, et al. Polyarthritede I'anisakiase. Presse Med 1984; 13: 1004.

15 Kliks MM, Burns JA. Anisakiasis in the western UnitedStates: four new case reports from California. Am JTrop Med 1983; 31: 526.

16 Yokogawa M, Yoshimura H. Clinicopathologic studieson larval anisakiasis in Japan. Am J Trop Med Hyg 1967;16: 723-8.

17 Oshima T. Anisakis and anisakiasis in Japan andadjacent area. Prog Med ParasitolJpn 1972; 4: 301-93.

18 Sugimachi K, Inokuchi K, Ooiwa T, Fujino T, Ishii Y.Acute gastric anisakiasis. JAMA 1985; 253: 1012-3.

19 Brasitus TA. 'Sushi' anyone? Gastroenterology 1984;86: 368.

20 Van Thiel PH, Kuipers FC, Roskam RT. A nematodeparasitic to herring, causing acute abdominal syndromesin man. Trop Geogr Med 1960; 2: 97-113.

21 Kuipers FC, Van Thiel PH, Rodenberg W, WielingaWJ, Roskamn RT. Eosinophilic phlegmon of thealimentary canal caused by a worm. Lancet 1960; ii:1171-3.

22 Daniels, JJHM. De eosinofiele flegmone van hetmaagdarmkanaal veroorzaakt door de haringworm.Ned Tijdschr Geneesk 1962; 106: 131-2.

23 Van Thiel PH, Van Houten H. The localisation of theherring worm Anisakis Marina in and outide the humangastro-intestinal wall. Trop Geogr Med 1967; 19: 56-62.

24 Van Thiel PH, Bakker PM. Wormgranulomen in demaag in Nederland en in Japan. Ned Tijdschr Geneesk1981; 125: 1365-70.

25 Ruitenberg EJ, Berkvens JM, Duyzings MJM.Experimentele Anisakis Marina infectie bij het konijn.Ned TijdschrGeneesk 1970; 114: 1404-9.

26 Ruitenberg EJ, Berkvens JM, Duyzings MJM.Experimental Anisakis Marina infections in rabbits.J Comp Pathol 1971; 81: 157-63.

27 Bijkerk H. Haringwormziekte (anisakiasis) en zureharing (produkten). Ned Tijdschr Geneesk 1987; 131:73.

28 Kuipers FC, Kampelmacher EH, Steenbergen F.Onderzoekingen over haringwormziekte bij konijnen.Ned Tijdschr Geneesk 1963; 107: 990-5.

29 Kuipers FC. Pathogenese van de haringwormflegmonebij de mens. Ned Tijdschr Geneesk 1964; 108: 304.

30 Asami K, Watanuki T, Sakai H, Imano H, Okamoto R.Two cases of stomach granuloma caused by Anisakislike larval nematodes in Japan. Am J Trop Med Hyg1965; 14:119.

31 Ruitenberg EJ, Steerenberg PA. De serodiagnostiekvan anisakiasis. Ned Tijdschr Geneesk 1970; 114:1950-3.

32 Ashby BS, Appleton PJ, Dawson 1. Eosinophilicgranuloma of the gastrointestinal tract caused by herringparasite Eustoma rotundatum. Br MedJ 1964; i: 1141-5.

on February 26, 2020 by guest. P

rotected by copyright.http://gut.bm

j.com/

Gut: first published as 10.1136/gut.29.6.843 on 1 June 1988. D

ownloaded from