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kiRci-lives
FISHERIES AND MARINE SERVICE
Translation Series No. 3671
Infestation of sea fishes with larval nematodes and its significance for nutritional hygiene
by K. Priebe
Original title: Die lebensmittelhygienische Bedeutung des Nematoden-larvenbefalls bei Seefischen
From: Archiv Lebensmittelhyg. 22(9): 193-200, 1971
Translated by the Translation Bureau(KMF) Multilingual Services Division
Department of the Secretary of State of Canada
Department of the Environment Fisheries and Marine Service
Pacific Biological Station Nanaimo, B.C.
1976
25 pages typescript
TRANSLATED FROM - TRADUCTION DE
German INTO - EN
English
PUBLISHER- ÉDITEUR
not shown
22 1971
TRANSLATION BUREAU NO. NOTRE DOSSIER N0 1089423 REQUESTING DEPARTMENT
MINISTÉRE-CLIENT Environment
SECRÉTARIAT D'ÉTAT
BUREAU DES TRADUCTIONS
DEPARTMENT OF THE SECRETARY OF STATE
MULTILINGUAL SERVICES
TRANSLATION BUREAU
DIVISION DES SERVICES
tr* Fq /n • t.r
11,.."•„a CANADA
DIVISION MULTILINGUES
tr •- VY■ t-t- 3 G, (
AUTHOR - AUTEUR
K. Priebe
TITLE IN ENGLISH - TITRE ANGLAIS
Infestation of sea fishes with larval nematodes and its significance for nutritional hygiene.
TITLE IN FOREIGN LANGUAGE (TRANSLITERATE FOREIGN CHARACTERS) TITRE EN LANGUE ÉTRANGÈRE (TRANSCRIRE EN CARACTÉRES ROMAINS)
Die lebensmittelhygienische Bedeutung des Nematoden-larvenbefalls bel Seefischen.
REFERENCE IN FOREIGN LANGUAGE (NAME OF BOOK OR PUBLICATION) IN FULL. TRANSLITERATE FOREIGN CHARACTERS.
RÉFÉRENCE EN LANGUE ÉTRANGÈRE (NOM DU LIVRE OU PUBLICATION), AU COMPLET, TRANSCRIRE EN CARACTÈRES ROMAINS.
Archiv ftir Lebensmittelhygiene
REFERENCE IN ENGLISH - RÉFÉRENCE EN ANGLAIS
Archives for Food Hygiene
DATE OF PUBLICATION DATE DE PUBLICATION
PAGE NUMBERS IN ORIGINAL NUMÉROS DES PAGES DANS
L'ORIGINAL
193 - 200 YEAR
ANNÉE VOLUME
PLACE OF PUBLICATION LIEU DE PUBLICATION
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ISSUE NO. NUMÉRO
9
NUMBER OF TYPED PAGES NOMBRE DE PAGES
DACTYLOGRAPHIÉES
2 5
BRANCH OR DIVISION TRANSLATOR (INITIALS) Fisheries & Marihe Service KMF
DIRECTION OU DIVISION TRADUCTEUR (INITIALES)
Pacific Biological Stqtion e Nanaimo, B.C.
PERSON REQUESTING DEMANDÉ PAR Dr. L. Margolis
YOUR NUMBER VOTRE DOSSIER NO
DATE OF REQUEST DATE DE LA DEMANDE January 7, 1976
MAR 1 9 1 97(ei
7 ;),
FfO I1 r,cAil:2rocni
SOS.200.10.8 (REV. 2/60 7530.21-02D•5333
'‘ DEPARTMENT OF THE sEcreLTARY or srArr. TRANSLATION BUREAU
TARIAT D'ÉTAT
BUREAU DES TRADUCTIONS
MULTILINGUAL SERVICES
DIVISION
DIVISION DES SERVICES
MULTILINGUES
CLI ENIS -170. • N° DU CLIENT
10891123
MINISTÙIE
Env ir onme nt
LANGUAGE
LANGUE
German
DIVISION/BRANCH CITY
DIVISION/DIRECTION VILLE
Fisheries Parine Servie Pacific Biological Staipn Nanaino, B.C.
BUREAU NO.
N° DU BUREAU TRANSLATOR (INITIALS)
TRADUCTEUR (INITIALES)
IÇIÎF MAR 1 9 1976
Archly fuer Lebensmittelhygiene 22, 9 (1971) pp. 193 — 200
Infestation of sea fishes with larval nematodes
and its significance for nutritional hygiene*
K. Priebe
(From the Federal Veterinary Bureau in Bremerhaven, Director: Vet. Dir. Dr. U. Kietzmann)
Sea fishes fulfill tha function of intermediate host for the
development cycle of numerous species of nematodes which parasitize
animals of marine biotopes. In marine species caught by maritime
fishing operations one frequently finds the third larval stage of
nematodes from the family of Heterocheilidae, which represent the
stage ready for invasion of marine mammals and birds feeding on sea
fishes which serve as the final host.
Morphologically, this third larval stage is only little
differentiated which explains why these larval nematodes were until
recently assigned to various other genera or species and why the
*Based on a lecture on the occasion of the 14th work session of the Sector "Food Hygiene" of the DVG (German Veterinary Society) on Sept. 29, 1971 in Freiburg/Breisgau.
UNEDITED TRANSLATION
For information only
TRADUCTiON Information sculemour
SC:15-2, 00-I 0-31
-, 1•2
— 2 —
question as to specificity of the intermediate and final host frequent-
ly remained unanswered. Larvae of the same morphology occur in
different species of sea fishes (e.g. Anisakis in herring, salmon,
mackerel, redfish ), while, on the other hand, various species of
larval nematodes infect one and the same species of sea fish ((e.g.
Terranova sp. and Porrocaecum sp. in Gadus callarias (Templeman et
al., 1957; Grainiger, 1958)).
The larva occurring in the herring (Clupea harengus) of the
North Atlantic is classified as belonging to the species Anisakis
marina which, in its adult form, can be found particularly in the
stomach of the Gr3y Seal (Halichoerus grypus) , the White—beaked
Dolphin (Lagenorhynchus albirostris) and the Common Porpoise (Phocaena
phocaena)(van Thiel, 1966). The Japanese literature reports on
Anisakis—type larvae which are found primarily in the cod (G , morhua
macrocephalus) , in the Alaska Pollack (Therogra chalcogramma) , in
the Japanese Mackerel (Pneumatophorus japonicus japonicus) , the Horse-
mackerel (Trachurus japonicus), in the herring (Clupea harengus pallasi)
as well as in the cuttlefish of the Pacific (Todaro pacificus) (Kagei,
1968). We, ourselves, determined an almost 100% infestation with a
larval nematode in imports of several hundred tons of Pacific herring
(Clupea harengus pallasi) which clearly differed in size from Anisakis
marina of the Atlantic herring (Clupea harengus harengus).
The reports concerning the frequency of infestation of sea fish
with larval nematodes are numerous. As a rule, the proportion of in-
fested sea fishes of the catch is surprisingly high, percentages close
to 100 not being rare (Kietzmann et al., 1969). On the other hand,
3
populations of sea fishes in which no larval nematodes were detected
or if so, only in a few specimens, are much less frequent. The wide
distribution of larval infestation in the fishes of the open sea is
therefore comparable to the parasitic infestation of domestic live-
stock raised under unsanitary conditions. One promoting factor is
undoubtedly life in dense schools as well as the migratory habits of
the fishes. As a rule, the life span of the larval nematodes exceeds
that of the intermediate host, the sea fish, resulting in an accumula-
tion in the sea fishes (stock host) which manifests itself in the in-
tensity of infestation per fish relative to its age.
In spot-check examinations carried out in Bremerhaven during
the years 1969 to 1971 on 10 herrings each of a total of 85 herring
catches from different fishing areas, or imports from various countries,
only 10 samples (= 11.8%) were found to be free from larval nematodes,
while in 42 samples (= 49.4%) 50% and more of all examined herrings
and in 33 samples (= 38.8%) less than half of the examined herrings
were infected.
Localization of the larvae within the'sea fishes varies. In
the main, the following conditions are observed:
1. Occurrence in the body cavity. In this case, the larvae,
surrounded by thin membranes resembling connective tissues, lie between
the mesentery or below the more or less curved, serous covering of
the organs or the wall of the body cavity. This form of occurrence
is observed most frequently in sea fishes, such as in herring, cod,
redfish, pollock. Due to the proper motility and the migratory abi-
lity of the larvae after the death of the sea fish, the larvae are
.ei-N • •
Se.
55 b
often found freely moving in the body cavity. This condition is there-
fore encountered mainly in fishes which reach the market only partly
or not at all eviscerated (e.g. smoked or salted herring). A method
of examination which leaves the fish intact in unknown (Fig. 1).
Fig. 1
Coiled agglomeration of Anisakis marina between the lobes of the roe in the body
cavity of a herring
Inspection is possible only by opening the body cavity of
selected random samples. Due to the generally high degree of in-
festation, a small number of samples is sufficient to provide an
overview. With medium or low intensity of infestation a greater
number of random samples would have to be selected; however, in-
fection of individual fishes belonging to the samples group cannot
be excluded in this case.
2. Occurrence in the muscles. Here too, the larvae are im-
bedded in a thin membrane of connective tissue formed by the body of
the intermediate host from which the larvae emerge after the death
of the fish. Of the main species of sea fish brought ashore in
Germany, this condition can be found primarily with the Brosme and
the Bluefish. The larvae occur deep within the filet as well as in on
that part which isiethe side of the body cavity and frequently also
on the side of the dermis (Fig. 2).
Fig, 2
Larval nematodes on the dermis side and deep within the filet of a Brosme.
Fig. 3 Larval nematodes under the intact skin of a smelt,
visible from the outside.
— 6 —
In fishes with transparent skin (smelt) the larvae can shine
through the skin, in which case the infestation with larval nematodes
in the fishes is recognizeable from the outside (Fig. 3).
The detection of larval nematodes in skinned filets, depending
on their thickness, is possible on a sufficiently illuminated back-
ground (intensity of illumination at filet height approx. 10,000 lux).
According to Canadian investigations on the cod, a maximum of 25% of
infected filets can be recognized due to the thickness of commercially
sliced filets, whereas the rate of detection can be raised to 95% and
over if sliced lengthwise to a filet thickness of 143 cm (Power, 1961).
According to our own observations the detectability of larval nematodes
in transmitted light is limited also in such species of fish (e.g.
Bluefish) whose silvery dermis which adheres to the filet is very
pronounced (Fig. 4).
Fig. 4
Table with illuminated glass plate for the detection of parasites, fishbones, etc., in filets during the processing of fishes.
- 7 -
The occurrence of larval nematodes in the bodyis muscles can
also be caused by a migration of the larvae from the natural location
which they occupy in the body cavity into the muscles after the death
of the fishes. This can frequently be observed where the fishes are
not eviscerated soon after they have been caught. Thus, for instance,
no larvae were detected in the muscles of mackerels whose entrails
were removed immediately after they were caught. However, if a period
of 24 hours elapsed until the fishes were gutted, larvae were detected
already in the muscles of 0.5% of the mackerels. This proportion was
increased to 10 - 13% if the entrails were removed only 3 - 4 days
after the catch (Vik, 1966) . .
The same phenomena can also be observed in herring. The
of herrings in whose muscles larval nematodes are imbedded
depends on the period of time which elapses until gutting and on the
number of larvae present in the body cavity. As a rule, no larval
nematodes are detected in the herring muscles, immediately after the
catch. With an average number of larval nematodes in the body cavity
of 3 per herring, almost e of the fishes. showed an infection of the
muscles after storage on ice for 4 - 8 days (calculated according to
the experimental results by Kuipers et al. (1960) and provided that
the muscles of each herring were only infected with one larval nema-
tode). On the other hand, Houwing (1969) determined 27 larval nema-
todes in machine-sliced filets in a catch of 50 herrings with an
average number of 15.4 larval nematodes per herring. We t ourselves,
examined 1,000 machine-sliced, washed herring lobes with the serous (195)
covering of the wall of the body cavity removed by machine,by thorough
4.
—8
visual inspection and, in suspicious cases by dissection, for the
presence of larval nematodes; this material originated from a herring
catch with an average number of 5 larval nematodes per herring. In
12 herring lobes we determined 1 larval nematode each (1.e). The
larvae were present mainly in the depth of the muscles of the gastric
lobes and were noticeable either by a blood—reddish or brownish colour
of the surrounding muscle tissue or by parts of the larval nematode
which protruded from the surface of the lobe. The detection of larval
nematodes in herring lobes must be considered difficult. On the other
hand, it is certain that a relatively large proportion of larval nema-
todes can be found on herring lobes whose serous wall of the body
cavity has not been removed because the larvae sometimes occur sub-
serously already in vivo on the wall of the body cavity. Evisceration
of the herrings for the purpose of removal of larval nematodes would
therefore have to include also the parietal lobe of the serous membrane
of the body cavity.
3. Infection of the visceral organs. The liver of the cod is
frequently affected. While larval nematodes are normally found alive
in freshly—caught sea fishes — possibly because of the relatively
short life—span of the fishes — the cod liver contains mainly dead
larvae, frequently in conjunction with extensive liver necroses. This
probably involves the larval invasion of a non—adapted species of
nematodes (Fig. 5).
-9
Fig._5
Surface of a cod liver with roundish necrotic areas caused by larval nematodes.
Approximately 10 years ago a Dutch group of researchers
(Kuipers et al. 1960) found that the consumption of raw or half—raw
fish dishes causes disorders in man through the ingestion of live
larval nematodes; these disorders exhibit symptoms of eosinophilic-
infiltrated granulomas tending to abscess formation in the wall of
the stomach or the intestine, or in organs of the adjacent abdominal
cavity (literature survey by Ruitenberg 1970). It became obvious that
these larval nematodes possess an active boring capacity long after
the death of their intermediate host, the sea fish, which enables them
to penetrate the gastro—intestinal wall which is, however, quite un-
specific with respect to the animal species or its tissue to be in-
vaded. This ability to penetrate is therefore retained not only in
the specific final host in whose gastro—intestinal wall the larva
undergoes its final development to return as an adult worm into the
-10 -
intestinal lumen which it then parasitizes, but also in non-adapted
false hosts (e.g. man) where, however, larva III soon dies due to
the body's defense mechanism and where, as a foreign substance, it
produces the above-mentioned symptoms. Thus the histological profile
frequently shows foreign body giant cells (Asayama, 1967). In the
specific final host, on the other hand, only slight, eosinophilic
cell infiltration is caused which heals again after the larvae leave
the gastro-intestinal wall. The same symptoms as observed in humans
can also be reproduced in experimental animals (rat, rabbit, guinea
pig, dog). They can also be observed in marine mammals in zoological
gardens if sea fishes are offered as feed which contain larval nema-
todes not adapted to the particular animal species (Gembardt et al.,
1971; Young and Lowe, 1969).
Due to the fact that mostly larval nematodes of the species
Anisakis were found to be the cause for the disorder * this is designated
as anisakiasis by the majority of authors, while other names such as
heterocheilidiasis or herringworm disease are less common. The number
of cases in humans which were reported up to 1970 amounts to approxima-
tely 300. Of these, most cases occurred in Holland and in Japan. Only
few cases were mentioned from other countries, such as England and
Scandinavia. In Germany only one case of illness was reported to date
in a young man who, during a camping holiday on the Baltic Sea had pre-
sumably consumed a half-cooked herring (Schaum and Mueller, 1967).
Particular habits of consumption or manner of preparation carry the
sole responsibility for the cases of illness in the countries involved
in which the boring capacity of the existing larval nematodes is retained.
- 11-
Thus, in Holland it was the so-called "groene" (green) herring, an
incompletely eviscerated, very lightly salted and practically raw
herring which underwent a certain curing during cool storage. In
Japan many sea fishes are consumed raw or are merely subjected to a
light, short-term vinegar-salt treatment in the form of the dishes
II sashimi" or "sunomono" (Yokogawa and Yoshimura, 1967). In Norway, (196)
the fish dish "gravfisk" is considered dangerous; in this the fish
is kept lightly salted and sugared for 1 to 2 days and is then
served in a wine sauce (Vik, 1966).
Except in animal experiments, the boring capacity of larval
nematodes can easily be tested in vitro according to a suggestion by
Ruitenbera and Roskam (1969), by placing the larvae to be examined
onto the surface of semi-solid agar (1% in physiological salt solution)
roughened with tweezers in half-filled test tubes and by adding several
drops of herring blood or Ringer solution and by incubating the material
for 2 days at 37 0C. The larvae with boring capacity can then be found
deep in the column of agar. The effect of fish processing methods
on the viability and thus the boring capacity of larval nematodes can
therefore be tested in a relatively simple manner whereas in expensive
animal experiments the greater part of viable larvae, depending on
peristalsis and gastro-intestinal contents, passes through the intestine
without adhering to it.
Experimental investigations have shown that if the brine which
develops in the salting of herring reaches a density of over 200
Baume (corresponds to 20.9 weight % table salt) no live larval nema-
todes are found in these herrings after 10 days, whereas the lifespan
— 12—
of the larvae can be prolonged considerably at lower salt contents
(Souwing et al., 1967). In dry table salt the larvae die within 10
minutes, in a saturated sali solution (26.3 weight percent at 10°C)
within one day, while in a 5% salt solution the larvae remain alive
for weeks. Similarly, freezing to —20°C within 24 hours or to —100C
within 48 hours causes the loss of the boring capacity, whereas
shorter freezing times. and higher freezing temperatures result in a
large proportion of surviving larvae. Temperatures of 50 — 52°C also
result in loss of the boring capacity within 10 seconds (Houwing et al.,
1967; Houwing, 1969b; Khalil, 1968). During the production of cold-
marinated fish it became evident that in barrel curing, a curing
process which in Germany is used almost exclusively by industry,
where — due to the high starting concentration of vinegar (approx. 7%)
and table salt (approx. 15%) at a herring/curing bath ratio of about
2 : 1 — the herring floats in the liquid, the larvae are killed after
30 days; on the other hand, curing in open containers at lower con-
centrations of vinegar and table salt (4 and 6% respectively) and a
herring : curing bath ratio of 1 : I produced certain destruction of
the larvae only after 70 days (Houwing, 1969a). Radioactive irradia-
tion of 0.1 — 0.6 Mrad resulted in a loss of the boring capacity of
the larvae after 2 hours (Ruitenberg, 1970). When investigating the
question, to what extent mechanical damage to the larvae (act of chew-
ing, comminution during the processing of the fish) results in the loss
of the boring capacity, it was determined that of cross—sectioned larval
nematodes a mere 20% of the larval front ends exhibited a decreased
boring capacity for several hours, whereas the rear ends of the larvae,
—13—
i.e. all larvae whose front ends (length of esophagus and ventricular
section) had been severed, ceased to move. These larval nematodes
are therefore not endowed with any particular regenerative ability —
a characteristic which holds true for all representatives of the class
of roundworms (Nemathelminthes)(Jaeckel, 1955) (Table 1).
In accordance with this information and the customary manner
of preparation and consumption of the herring, "herring regulations"
were passed in Holland in 1968 and 1969 to protect human health; these
were designed to eliminate any health hazards through binding regula-
tions and strict control measures and to remove the fear of the public
of damages to health through consumption of herring. In accordance
with these regulations the caught herring which is intended for the
market as a fresh fish, must be deep—frozen within 18 hours after the
catch in such a manner that within 12 hours a temperature of —20°C is
attained within the herring which must be maintained for 24 hours.
This freezing method is mandatory also for those herring products
which will not undergo or have not been subjected to the following
treatment during processing:
1. In salt curing a density of at least 20 ° Baumé must be attained in the
brine after 10 days.
2. During heat treatment (smoking, baking, etc.) a minimum temperature
of 50°C must be attained.
3. During the curing process of cold marinades in which the fish re-
mains in the curing bath for at least 30 days, at a herring:
curing bath ratio of 2.2 : 1 at the most, a maximum pH value of 4.0
and a minimum salt concentration of 6.5% must be attained.
SA
- 14 -
In view of these Dutch regulations governing food hygiene
it is evident that there are a number of herring products also in
the Federal Republic of Germany which would be subject to strict
regulations in Holland. It should therefore be well worthwhile to
consider and examine whether such measures are necessary also in
Germany even if here a general distribution of this disease is un-
known in man and an acute danger is not evident at this time. No
doubt, such measures are also in the interests of the fish industry
if they will serve to remove any recurring uncertainty on the part
of the consumers through one-sided or unfactual reports by the mass
media.
These considerations refer particularly to the fresh, mildly-
salted herring seasoned with herbs as well as to cold-marinated fish
and products of cold-smoking which have not undergone adequate salt
treatment. On the other hand, products of hot-smoking, canned fish
and fish processed by baking and boiling seem to be free from danger
because these products are subjected to sufficient heating during
processing. It should further be pointed out that at least periodically
the major portion of all fish products is produced from deep-frozen
raw material and, furthermore, consists of those parts of the herring
(filet or lobes) where the incidence of larval nematodes can be re-
garded as low.
The fresh or green herring which is sold raw, eviscerated or
non-eviscerated is a popular item of consumption in Germany. Compared
to Dutch eating habits following curing in a mild brine, the green
114
— 15 —
herring — similar to other fresh sea fishes — is eaten in Germany
only after heating (usually baked). If the fish is marinated in
the kitchen the starting material is never raw, but always heat-
treated herring. A kitchen—technological marinating is to be con-
sidered not as a cooking process but rather as a special flavouring.
In this way, the fresh herring — just like any fresh fish — (197)
does not represent a health problem in Germany because any larval
nematodes which may be present are destroyed by processing in the
kitchen before consumption. Even from the point of food regulations,
a herring infected with larval nematodes cannot be regarded as a
health hazard because a foodstuff, according to the official reason-
ing behind Section 3 of the Food Regulations, is a health hazard
only if it possesses this characteristic in the edible state since
the consumption of many foods which are, in themselves, quite sound
may in a raw or improperly prepared state cause disorders for which
the person who markets such food cannot be made responsible.
Despite the legal implications of these food regulations one
should not, however, fail to inform the public that the consumption
of insufficiently cooked fish dishes (faulty product) can be dangerous
and that attention must therefore be paid to proper preparation (through
baking or boiling). The drafting of regulations covering the fresh
herring would therefore also require regulations governing the trade
with fresh sea fishes in general for which, however, no compelling
reason exists due to our customary aating habits because fresh fish
still seems to be considered nutritionally more valuable than thawed-
out deep—frozen fish.
-16-
Of the ready—to—eat herring products produced by the German
fish industry, the mildly salted herring (Matjes) and salads prepared
from it is much favoured by large parts of the German population.
These products can, in fact, prove a possible risk upon consumption
if they contain larval nematodes, a possibility which from a quanti-
tative point of view must be regarded as very slight. In order to
remove any such.doubts it should certainly be considered to eliminate
the possibility of the presence of live larval nematodes in these
foods by registering all producers and all imports of such products,
by stipulating the salt content and curing period or by freezing,
and by the application of suitable control measures.
No information is available to date concerning the behaviour
of larval nematodes in herb—flavoured herrings which were cured in
a salt brine with the addition of sugar and spices. The risk seems
to be small here because a period of over 6 weeks is estimated for
curing.
From the Dutch point of view, cold marinades also present a
danger for human health. Here too, one can proceed from the fact
that the slices cut from the herrings (marinated filet) as well as
the small herrings (Kronsild) contain only a very small number of
larval nematodes anyway. Although Dutch regulations requiring a
curing period of at least 30 days at a final maximum pH value of 4.0
and a minimum salt concentration of 6.5% seem to result in the loss
of the boring ability of any larvae present, the application of such
a curing time would reduce the usefulness of this method because
leaving the herring in the brine after curing is completed (approx.
-17-
4-6 days) decreases the keeping quality of the finished product due
to progressive protein hydrolysis. Here too, deep-freezing appears
to be the best method for practical purposes.
For the sake of completeness it should be mentioned in connec-
tion with the human anisakiasis that the occurrence of eosinophilic
meningoencephalitis in persons on Hawaii, Taiwan and French Polynesia
is caused by migrating larvae of the lungworm of the rat (AnziosIroAgylms
cantonensis) which are transmitted to man by the consumption of
mussels and prawns (Rosen et al., 1967); similarly, the human form of
gnathostomiasis should also be mentioned which manifests itself in
disorders of liver, eyes and skin and occurs in various parts of the
world (Japan, Thailand, China, Palestine) and is transmitted by the
consumption of raw or half-raw fresh-water fish which harbour these
larvae (Miyazaki 1960).
Another problem is the presence of larval nematodes in fishes
or fish products as a nausea-arousing factor as such. The nausea-
causing condition of a food is regarded as a considerable deviation
from the normal condition which greatly impairs edibility. Such foods
are considered spoiled according to Section 4, Paragraph 2 of the Food
Regulations and if not sufficiently identified as such, are therefore
excluded from the market as a food item. Undoubtedly; the nauseous
quality of infestation with larval nematodes depends on the subjective
attitude on the part of the consumer. The degree of nausea aroused
by nematode infestation in animal foods is frequently felt more keen-
ly than in plant foods. The reactions by the consumer are by no means
uniform. Apart from the fact that nobody will experience an increase
—18—
in appetite upon finding larval nematodes when eating a dish, the
following main reactions are possible depending on attitude, experience
and knowledge of the consumer:
1. Total refusal of an y future consumption of sea fishes.
2. The dish just objected to is not eaten, but a sound meal
is again consumed at any time.
3. The dish is eaten if it is possible to remove the larval
nematodes.
To investigate the reactions of the consumers seems to be the
task for a public—opinion poll during which not questions but fish
dishes infested bith larval nematodes should be presented. The number
of larvae found while eating seems to be of secondary importance for
a complaint. One larva seems to be just as nauseating as many. Apart
from this, the distribution and localization of the larvae in the fish
seem to be of decisive significance whether the dish is eaten or not.
Upon presentation of the objective evidence, namely the larval nema-
todes, the complaints voiced by the consumer because of nausea are in-
contestable. For this reason fish and fish products have repeatedly
been rejected as spoiled according to Section 4, Paragraph 2 of the
Food Regulations and correspondingly, preliminary— and criminal pro-
ceedings were instituted. Of 38 known preliminary proceedings in the
years 1963 — 1971 (Marwitz, 1971) where the infestation of sea fishes
with larval nematodes was criticized, 34 were dismissed by the pro-
secution already before arraignment. Only in 4 cases a verbal trial
took place. Of these, two cases were dismissed, while one case re-
sulted in an acquittal and another in a sentence. It becomes clear
‘11,
— 19 —
from this number that even prosecuting authorities such as courts in (198)
the main see no cause for punishment when dealing with such complaints.
If one proceeds from the fact that the Food Regulations as a
penal by—law serve, among other things, the purpose of protecting the
food consumer from fraud and cheating, it becomes clear that this ob-
jective where it concerns complaints because of nausea in cases of
larval nematode infestation in sea fishes has certainly not been
accomplished nor, it is safe to say, will it be accomplished in the
future. The inadequate detection of nematode infestation — with
respect to examining of filets in transmitted light as well as random
testing of uneviscerated sea fishes — and the heavy and wide—spread
infection of sea fishes with larval nematodes in most fishing areas
will continually lead to complaints even though it is not always
possible to lay the blame on any one individual. Although prudent,
general identification of nematode infestation when trading with sea
fish products solves the problem from a legal point of view so as to
prevent lawsuits under the present laws, it does not take into account
the importance of the sea fish as a food inasmuch as most products do
not possess this shortcoming; its occurrence is limited to special
products (salted, smoked herring) or to individual cases where de-
tection and removal of the larvae during processing was not possible.
The consistent legal prosecution in cases of trade with sea-
food infested with larval nematodes would have to be equated with
the prohibition of these products for which there exists no substitute.
The ocean fishing industry which catches sea fish at great expense
and must process the catch on board ship in order to land it in as
—20 —
fresh a condition as possible would, if larval nematodes were detected,
be forced to dump the catch into the sea or to land it as raw material
for fish meal at prices which would in no way cover the costs of the
catch.
Herring Salt content etc. Storage Maximum life Product Recipe of brine or final tempera— span of larval
curing bath ture nematodes
Matjes 11 kg salt Herring 20 litres 17% (immature salt solution 15.5% salt 0°C 14 days herring) 95 kg headed herring
Matjes 9 kg salt Herring 20 litres le
salt solution 18.6% salt 0°C 20 days 95 kg headed herring
Matjes 14 kg salt Herring 30 litres 17% Nordic salt solution 17.8% salt 0°C 23 days Variety 2 kg sugar
95 kg headed herring
Spiced 14 kg salt Herring 13 litres 17%
o 26 days salt solution 19.7% salt 0 C 4 kg sugar 1 kg spices
95 kg headed herring
riSat.Ler, 35 litres brine with 5e salt 4 0 eyL n 7.% acetic acid and 2.1% acetic
14% salt acid 4°C 37 days 84 kg headed herring pH 4.6 .
Table 1
Experimental results on the maximum lifespan of larval nematodes in herring products
-21—
Even proposals which call for the eviscerating of herring
or of certain herring products as a binding requirement would only
partly solve the problem even for herring without eliminating it in
a satisfactory and permanent manner for all sea fishes.
Thus the expedient of manufacturers of smoked herring to de-
viate from the tradition of herring smoking which dates back to the
13th century, namely to smoke the herring in an eviscerated state
(without larval nematodes) was not appreciated by the consumer be-
cause a herring sliced up in this manner suffers losses of oil and
moisture during smoking and lacks the usual taste of smoked herring.
For thesc,. reasons it is proposed to refrain from the applica-
tion of Section 4, Paragraph 2 of the Food Regulations in the case
of infestation of sea fishes with larval nematodes and to ensure
within the framework of the revised German Food Regulations that re-
course to criminal charges is not intended in the case of deviations
in foods due primarily to natural causes which cannot be influenced
when acquired or processed and remain concealed depending on the pre-
vailing state of the art but which detract from the enjoyment of the
food due to arising nausea when detected by the consumer. Rather,
it should be considered adequate if such complaints are settled by
civil law (extent, concealment at time of sale) so that the person
who introduces such foods into the market is not absolved from his
responsibility to avoid such shortcomings. On this basis it seems
reasonable that no confusion would ensue in this food sector because
of this deficiency nor would the consumer be less well protected. As
far as it is known from the practical side of the fish trade, fish
stores are willing to make refunds in cases of such complaints. (199 )
-22—
In my opinion it is more important to explain the true facts
to the consumer. In the sale of smelts (Osmerus eperlanus) whose
infection with larval nematodes is well known by the coastal popula-
tion, complaints are virtually unknown, despite the fact that the
degree infestation of the smelt with larval nematodes is very high
and the worms (Porrocaecum decipiens) can hardly be overlooked because
of their size. The degree of information of the coastal population
by itself solves the problem in such a manner that one part of the
population abstains from eating smelts on its own accord while others
appreciate the taste of the fish and accept to carefully examine the
fish (which is commercially available mainly in uneviscerated state)
during preparation and remove the worms themselves.
It would be important to explain the following points to the
consumer:
1. Infestation of sea fishes with nematodes is natural and is
not rare. It is not a sign of decomposition and has nothing to do
with pollution — in particular that of ocean fishing grounds.
2. For technological reasons and in connection with biological
factors such infestation can frequently be observed in certain fish
products (smoked or salted herring) or in certain species of fish,
whereas other products can be considered as virtually free of larval
nematodes because the entrails which harbour the larvae are removed
soon after the catch.
3. With the preparation of sea fishes (boiling, baking) common
in Germany and the customary procedures in the processing of fishery
products (particularly cans, products of hot—smoking, boiled and baked
- 23 -
fish products) and - where it is deemed necessary - upon observance
of certain processing specifications such as deep-freezing or keeping
a certain period of time during curing or marinating while monitoring
the salt concentration etc., the consumption of such food does not
constitute a health hazard because the larval nematodes are killed.
However, it should be pointed out that such a hazard may ensue
from the consumption of raw or half-raw herrings if they contain live
larval nematodes. When cooking these, attention should be paid to
uniform heating.
4. Recause fish or fish products infected with larval nematodes
may induce nausea, a refund may be requested from the seller according
to civil law.
Summarx
The occurrence of larval nematodes in sea fishes is not rare.
Due to inadequate detection methods in the processing of fish and
despite observance of the necessary care in the trade, it cannot be
prevented entirely that sea fish products may at times be infected with
larval nematodes. Disorders in man may occur when live larval nema-
todes are ingested during the consumption of fish dishes (anisakiasis).
This possibility can be ruled out for the form of consumption of fresh
sea fish including fresh herring common in Germany (boiling, baking)
as well as for most ready-to-eat fishery products (deep-frozen, canned,
fried, boiled, salted, smoked fish products). In mildly salted herring
products (salt content of the water in the fish tissue under 20e) and
cold marinades any larvae present are not necessarily destroyed so
' 1 t,
- 24 -
that a health hazard cannot be excluded when eating these products.
It is therefore proposed to examine whether these herring products
should be produced from deep,—frozen herrings or whether the products
themselves should be deep—frozen or whether — e.g. in the case of
cold marinades — a curing duration of at least 30 days, a final
maximum pH value of 4.0 and a final salt content of at least 6.5
should be ovserved. It should be in the interest of the public at
large if such measures would eliminate with certainty all possibility
of a health hazard through the consumption of fish products infested
with larval nematodes. It is further proposed not to prosecute
(according to the Food Regulations) the marketing of sea fishes and
fish products infested with larval nematodes for causing nausea sinch
according to present experience and because of the lack of suitable
examination methods in connection with the widespread infestation of
sea fishes with larval nematodes, the threat of punishment according
to Section 4, Paragraph 2 of the Food Regulations was not successful
in the sense of effective consumer protection.
The settlement of such deficiency rulings should be left to
the civil law (refunds). For the rest, it is commensurate with the
importance of the food item "sea fish" and appears to be in the in-
terest of all concerned that the consumer should be thoroughly in-
formed of all facts, honestly and without bias.
-25-
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Author's Address: OVR Dr. K. Priebe, 285 Bremerhaven-F Halle 10
FEDERAL REPUBLIC OF GERMANY