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Introduction
Diphyllobothriasis is an intestinal parasitosis caused by the ingestion
of mostly raw freshwater fish containing infectious larvae of the Diphyllobothrium
latum (D. latum) cestode worm. The cycle of this parasite is complex
and involves several hosts [1,2]. Released in water, the eggs mature
within eight to 12 days at a water temperature of 16-20°C, and yield
a procercoid larva that is ingested by a zooplanktonic copepod crustacean
[FIGURE 1]. About 40 copepod species of the Eudiaptomus or Cyclops genus
are likely to be the first intermediate hosts. This larva develops into
a procercoid larva within the general cavity of the copepod. When carnivore
fish ingest planktonic crustaceans, the larva develops into a plerocercoid
larva a few millimetres long. It migrates into the fish musculature
or viscera where it can remain inactive for several years, but can re-encyst
several times in other predatory fish. In Europe, the types of fish
susceptible to host the larvae are perch (Perca fluviatilis), pike (Esox
lucius), charr (Salvelinus alpinus), and burbot (Lota lota). The Coregonidae
(feras) and probably the Salmonidae of Salmo genus (except for the Canadian
Salmonidae of the genus Onchorynchus) do not host D. latum larvae (TABLE
1). Man and other ichtyophagous mammals become contaminated by ingesting
this undercooked fish. The plerocercoid larva can grow between 5 and
20 cm a day [2], and develops into an adult that yields its first eggs
about one month after infestation. D. latum is the longest human parasite
known (about 10 metres long) and can live for several years. Its symptomatology,
although limited, is polymorphous: manifestations may include abdominal
discomfort (abdominal pain, diarrhoea), weight loss, asthenia, and vertigo.
Anaemia due to vitamin B-12 deficiency has been described in case of
prolonged infestation [1]. Human experimental infestations have been
practised [4]. Three volunteers, infected by two to three plerocercoid
larvae, did not present any obvious clinical symptoms except for the
release of proglottis. The two non-treated subjects dewormed spontaneously
seven months (in the first case), and four years and six months (in
the second case) after being infected. The parasite is sensitive to
praziquantel (15 mg/ kg/ day in one dose) and to niclosamide (2 g on
an empty stomach in two doses an hour apart). In 1999, the world prevalence
of diphyllobothriasis was estimated at 9 million cases [3], despite
the difficulty of making precise evaluations because of the existence
of other species either morphologically close or undistinguishable,
such as D. pacificum in Peru, and D. nihonkaiense in Asia [4]. The earliest
description of diphyllobothriasis prevalence in western Europe goes
back to Von Bonsdorff's monograph of 1977 [1]. The objective of our
study is to report the current situation of diphyllobothriasis in western
European countries.
Material and methods
The analysis was carried out with data from literature published since
1980 using the following databases : Medline, Cabi Helminthological
abstract, Inist Pascal, and the Yahoo and Google internet search engines.
Information was collected for each of the 25 countries of the European
Union (with the exception of Malta and Cyprus), and some adjacent European
countries (Switzerland, Hungary, Croatia and Yugoslavia). In March 2003,
we also contacted or sent a questionnaire to a network of European parasitologists
(specialising mainly in food safety), to microbiological laboratories
(those located near lakes and identified through professional directories)
in Savoie, Isère, and Haute-Savoie (France), and Switzerland,
and to university hospital parasitology laboratories in Besançon,
Lyons and Grenoble. The questionnaire concerned the number of human
cases observed in the course of the past 20 years as well as possible
veterinary data (fish and mammal), either personal or published data.
Results
Information was obtained from a network of parasitologists, and from
databases from 23 European countries. For France and Switzerland, data
was completed by the network of laboratories that were contacted. There
are three types of epidemiological situation in Europe: areas where
parasitosis is frequent or relatively frequent, areas where sporadic
or imported cases have been observed, and areas where no parasitosis
was reported [FIGURE 2]. Specific surveillance of diphyllobothriasis
exists only in Estonia, Lithuania, and Poland. In Finland, at least
20 cases are reported each year [S Meri, personal communication]. A
study carried out between 1978-1989 by hospital practitioners showed
that prevalence varied between 0.3 and 3.8% of patients [5]. In Sweden,
10 to 50 cases are observed each year [D Christensson, personal communication].
In Estonia, 440 cases were reported in 1997, compared with 715 cases
in 1990 [6]. Cases are numerous in French and Italian speaking areas
surrounding the Swiss, Italo-Swiss, and Franco-Swiss Alpine lakes. In
1990, one of the authors reported 18 cases on the Swiss shores of Lake
Maggiore [7], bringing the total to 33 cases over the last 20 years
[8]. Golay and Mariaux retrospectively identified seventy three cases
around Lakes Léman, Bienne, and Morat between 1980 and 1994 [9].
Alpine lakes in northern Italy are subject to frequent contamination:
in 1987, Magatelli [10] described eight cases on Lake Iseo [10], and
in 2000, Terramocci et al [11] reported six cases on Lake Como [11].
Several further cases were reported on Lakes Como and Iseo in 2003 [A
Raglio, E Pozio, personal communication]. On the French shores of Lake
Léman, Gregory et al [12] diagnosed two cases in St Julien en
Genevois and, in 2001, the authors published 22 cases diagnosed between
1993-2000 following a survey carried out in 50 laboratories located
in Haute-Savoie [13]. Lake Léman seems to be particularly affected,
with 48 cases identified on its shores in 2001 and 2002. The parasitosis
is absent in Lake du Bourget, and the last case observed was in a professional
fisherman six years ago [C Bernot, personal communication], Lake d'Annecy,
Lake d'Aiguebelette and Lake de Paladru. Rare studies published on the
prevalence of fish infection [7,9,14] have concerned only the Swiss
and Italian Alpine lakes (TABLE 2), and showed a sometimes high infestation
of pikes and perch. In other European countries, parasitosis is reported
less frequently. In Romania, the historical foci of the Danube delta
were subject to massive treatment campaigns, although cases continue
to be reported [CM Cretu, personal communication]. A few cases are reported
each year in Poland [15] and in Lithuania [V Jasulaitene, personal communication].
Five cases were observed in Vienna between 1991 and 2003 [H Aspock and
H Auer, personal communication, [6]]. Two cases were reported in Spain,
one caused by imported salmon from an unknown country [17,18]. Three
cases were reported in Greece [19]. Cases have also been reported infrequently
in Slovakia [20] and in Norway [L Robertson, personal communication].
An imported case was reported in the Czech Republic [21]. In addition
to the foci of Lake Léman, at least six imported cases have been
described in France since 1980 (A Cazin, ME Bougnoux, M Deniau, H Pelloux,
P Marty, and C Tourte-Schaefer, personal communication). To our knowledge,
no autochthonous human case was reported in Denmark, Croatia, Belgium,
the United Kingdom, the Netherlands, Yugoslavia, Macedonia, Hungary
or Germany.
Discussion
The methodology used in this study, without being exhaustive, is original
and could be used as a basis for further studies to evaluate evolution
trends. Human diphyllobothriasis is still present in western Europe,
but when compared with previous studies [1,5,6], can be seen to be decreasing
in Baltic and Scandinavian countries. It seems to be either emerging
or better diagnosed in the French and Italian speaking areas around
Alpine lakes, as shown by the more than 200 cases that have been reported
or published around Lake Léman, Lake de Morat, Lake de Bienne,
Lake Maggiore, Lake Como, Lake Iseo, and Lake Gardia since 1987. German
speaking areas around Alpine lakes did not seem to be affected: Golay
and Mariaux [7] identified only rare cases in the cantons of Freiburg
and Bern compared with around 30 cases in the cantons of Geneva and
Vaud. In 1963 [22], human diphyllobothriasis was rare around Lake Léman:
no cases had been reported for five years at the Lausanne Institute
of Hygiene (Institut d'hygiène de Lausanne), four cases reported
in nine years at the Lausanne Badoux, Bauer and Rochat Laboratory, one
case in four years at the Geneva University Polyclinic (Polyclinique
Universitaire de Genève).
Diphyllobothriasis is associated with ancestral eating habits: consumption
of raw salted or marinated fish fillets in Baltic or Scandinavian countries,
'carpaccio di persico' in northern Italy, 'carpaccio d'omble chevalier'
and 'poissons du lac façon nordique' in French-speaking areas.
Fadish and extreme food choices such as "instinctotherapy"
(a type of raw food diet) and the increasing popularity of sushi could
also be contributory factors. The prevalence of fish infestation in
the Alpine lakes is between 3.7% and 33% (TABLE 2).
The continuation of the diphyllobothriasis cycle is an indicator of
the faecal pollution of lakeside environment. The complex cycle is compensated
by the prolificness of the parasite: one worm alone can yield between
one and several million eggs a day that can infest zooplanktonic crustaceans,
the first intermediary host. No data was found on zooplanktonic species
involved in the transmission or on their level of infestation. Building
waste water treatment plants contributes to fighting the parasitosis
[6] but there are other unrelated habitats. For instance, around Lake
Léman, 89% to 98.6% (according to sources) of the inhabitants
of the drainage basin are connected to 159 wastewater treatment plants
[23,24]. These treatment plants purify only between 95% and 99% of eggs.
The eggs not caught are viable, and the treatment plants may overflow
during storms [1,2].
There is professional and leisure fishing on and around lakes. There
are about 150 professional fishermen and 5000 fishermen on Lake Léman,
who caught around 1000 tons of fish in 1999, of which 47% was perch
and 6.5% was charr [25]. The fish is consumed directly by fishermen,
or sold to fishmongers or to the many restaurants located on the shores
of the lakes, which sometimes offer dishes made with raw fish. Veterinary
data on fish infestation in Lake Léman is scarce and very old:
58% of perch and 95% of burbot were carriers of plerocercoid larvae
in 1909 versus 12.5% of burbot in 1963 [22]. In 2003-2004, we found
plerocercoid larvae in 8% to 12% of perch fillets analysed and the precise
identification of the larvae was carried out with molecular biology
techniques (polymerase chain reaction and sequencing). Faecal pollution
of lakes by the many yachts that sail there can also be considered in
the continuation of the cycle although regulations require that faecal
matter is disposed of in appropriate sanitary facilities [26]. There
is also the issue of faecal pollution of shores by fishermen or by wild
or domesticated carnivores that are numerous on those shores. Cases
of infestation of dogs have been reported in the Geneva area [B Gottstein,
personal communication]. In 1963, around Lake Léman, Bouvier
et al [22] found only two infected dogs out of the 259 one they had
examined. No infestation was found in 179 cats and 31 foxes examined,
but the incidence of parasitosis in man was low at that time. Some cases
of fox infestation have recently been reported in the Tessin, Grisons
and Geneva areas [Deplazes, personal communication]. A wild cycle would
be ensured by trouts and foxes [D Gerdeaux and M Morand, personal communication];
the latter consuming dead genitors on spawning grounds. Elsewhere, diphyllobothriasis
was found in 0.5% of foxes captured in Karlsruhe in Germany [27] and
in 0.2% of dogs captured in Finland [28]. However, it seems that the
parasite does not develop very well in those carnivores who, unlike
man, may only play a minor role in the continuation of the cycle [1,2].
Our study has also shown the relative frequency of imported cases (contracted
during travel abroad or after consumption of imported fish) that could
in certain cases help to maintain the parasite, or to reintroduce it
in areas it had previously disappeared from. This survey is certainly
limited since we can not pretend to have made an exhaustive collection
of cases. In fact, some laboratories from German speaking Switzerland
did not respond to the invitation to participate in the survey. Moreover,
many cases are likely to be treated by general practitioners either
for diphyllobothriasis or for Taenia saginata taeniasis considering
the relative similarity of the proglottis of both species. An in-depth
study of eight clinical cases has shown that severe clinical symptoms
can lead to specialised consultations and expensive complementary analyses,
resulting in an average cost of €400 for the management of a single
diphyllobothriasis case [13]. Finally, comparing the incidence of different
countries is difficult since it would be necessary to know the size
of the exposed populations to calculate the risk. For example, in France
and Italy, exposed populations are limited to the shores of the lakes,
whereas in Finland, the entire population is at risk of exposure. Consumption
studies could be carried out in each of the countries to learn about
eating habits and therefore evaluate a possible risk behaviour.
Conclusion
Diphyllobothriasis is decreasing in Baltic and Scandinavian countries,
but is emerging in French and Italian speaking Alpine areas. The fashion
for carpaccio, sushi and recipes based on raw fish, as well as the proliferation
of restaurants serving these kinds of dishes, will certainly not slow
down this emergence. Work towards ending the disposal of waste water
in lakes has been done, but the imperfect efficiency of waste water
treatment plants, and the many yachtsmen who also fish explain the continuation
of the parasitic cycle. It is therefore necessary to inform consumers
of the risks linked to the consumption of raw or undercooked fish as
well as prophylactic methods. Cooking fish at a temperature of 55°C
kills the plerocercoid larvae in five minutes, and freezing it at -10°C
kills the larvae within 8 to 72 hours, depending on the thickness of
the fish [29]. Smoking fish does not kill the parasite [30]. Changing
food habits is illusory especially when such habits are ancestral as
shown by the discovery of diphyllobothriasis eggs in the archaeological
sediments of neolithic lakeside villages of these areas [31]. Finally,
it would be interesting to monitor the infestation in man and in fish
with regular prevalence surveys to study the evolutive nature of diphyllobothriasis.
Acknowledgements
We wish to thank the numerous French medical analysis laboratories of
Haute-Savoie, Savoie and Isère, and the Riotton Bioanalytical
Laboratory (Geneva), for their collaboration. We also thank those in
France for their help in this survey: Alain Gregory (Saint Julien en
Genevois), Catherine Bernot (Aix les Bains), Daniel Gerdeaux (Station
d'Hydrobiologie lacustre, INRA, Thonon les Bains), Michel Morand (LDA
39, Lons le Saunier), Hervé Pelloux (CHU Grenoble), François
Peyron (CHU Lyon), Renaud Piarroux (CHU Besançon), Laurent Desvois
and Claire Dupouy-Camet. finally, we thank the informal network of European
parasitologists who participated in this survey: Seppo Meri (Finland),
Pavol Dubinski (Slovakia), Christian Kapel (Denmark), Dan Christensson
(Sweden), Bretislav Koudela and Tolarova Vira (Czech Republic), Dragutin
Golubic (Croatia), Antonio Martinez-Fernandez, Guillermo Esteban, Antonio
Clavel and Santiago Mas-Coma (Spain), Georgios Theodoropoulos (Greece),
Bruno Gottstein, Peter Deplazes, Madeleine Van-Saanen and Floriane de
Marval (Switzerland), Lucy Robertson (Norway), Stanny Geerts (Belgium),
Peter Chiodini (UK), Zbigniew Pawlowski (Poland), Nino Ioli, Massimo
Scaglia, Eduardo Pozio and Annibale Raglio (Italy), Joke van der Giessen
(The Netherlands), Carmen Micaela Cretu (Romania), Karsten Noeckler
(Germany), Viktorija Jasulaitene (Lithuania), Horst Aspock and Herbert
Auer (Austria), Liliana Sofronic (Yougoslavia), Tibor Kassai (Hungary).
This work was made possible thanks to a grant from ADERMEPT (Association
pour le Développement Et la Recherche en Médecine Parasitaire
et Tropicale).
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