Crassicauda boopis in a ﬁn whale (Balaenoptera physalus)
ship-struck in the eastern North Atlantic Ocean
*, MORGAN DELOBELLE
, MARJAN DOOM
, ETIENNE LEVY
, BERTRAND LOSSON
and THIERRY JAUNIAUX
Faculty of Veterinary Medicine,University of Liège,Center for Fundamental and Applied Research for Animal and
Health (FARAH),Laboratory of Parasitology and Parasitic Diseases,Quartier Vallée 2,Av de Cureghem,6 B43a-4000
Faculty of Veterinary Medicine,Department of Morphology,University of Ghent,Salisbuylaan 133,9820 Merelbeke,
Royal Belgian Institute of Natural Sciences,Operational Directorate Natural Environment,3de en 23ste
Faculty of Veterinary Medicine,University of Liège,Center for Fundamental and Applied Research for Animal and
Health (FARAH),Pathology Unit,Quartier Vallée 2,Av de Cureghem,6 B43a-4000 Liège,Belgium
(Received 23 January 2017; revised 14 June 2017; accepted 14 June 2017)
On 9 November 2015, a juvenile male ﬁn whale of 11·60 m length was observed on the bulb of a merchant vessel in the
Channel Terneuzen –Ghent (The Netherlands –Belgium). A severe parasitosis was present in the right heart ventricle
and caudal caval vein. Parasites were identiﬁed as Crassicauda boopis based on macroscopic and microscopic observations.
The sequence of the 18S rRNA gene obtained from the parasite samples was 100% similar to the sequence of the 18S rRNA
gene from Crassicauda magna available on GenBank. While adults of C. boopis and C. magna are morphologically distinct
and found at diﬀerent locations in the body, the molecular analysis of the 18S rRNA gene seems insuﬃcient for reliable
species identiﬁcation. Although numerous C. boopis were found, the cause of death was identiﬁed as due to the collision
with the ship, as suggested by the presence of a large haematoma, and the absence of evidence of renal failure. The
young age of this whale and the absence of severe chronic reaction may suggest that the infestation was not yet at an
advanced chronic stage.
Key words: Crassicauda boopis,ﬁn whale, kidney, caudal caval vein.
The ﬁn whale (Balaenoptera physalus) is a marine
mammal belonging to the suborder of baleen
whales (Cetacea, Mysticeti). It is the second-largest
animal on earth after the blue whale (Balaenoptera
musculus). Although ﬁn whales are found in all
major oceans and a number of seas, from polar to
tropical waters, it is rare in the southern North
Sea, and in most cases solitary animals are seen
(Camphuysen and Peet, 2006). It feeds by
ﬁltering a large volume of seawater, enabling to
harvest large zooplankton mainly Northern krill
(Meganyctiphanes norvegica) but also small schooling
ﬁsh such as herring (Clupea harengus), squid and
crustaceans including copepods (Lambertsen,
1986; Ruys and Soulier, 2013). Cetaceans serve as
hosts to numerous parasites, including many nema-
tode species such as crassicaudids (Nematoda,
Spirurida) (Lambertsen, 1986). Crassicauda spp.
occur under the skin or in deep tissues of the
mammary glands, in cranial sinuses and the urogeni-
tal system (Geraci and St. Aubin, 1987; Lambertsen,
1986; Zucca et al. 2004; Jabbar et al. 2015). Three
nominal species of adult Crassicauda have been
described in the urogenital system of the ﬁn whale,
namely C. crassicauda,C. boopis and C. paciﬁca
(Lambertsen, 1985,1986). The former is the smal-
lest of the three, and occupies the lower urinary
tract (urethra), whereas the latter two infect the
kidneys and are considered as taxonomically syn-
onymous as morphologically indistinguishable
Crassicauda boopis (Tetrameridae, Baylis, 1920) is
a round worm attaining a length of approximately
1·5–2 m. The parasite shows a large anterior part
(5 mm wide), which is often observed protruding
in the blood ﬂow and an attenuated posterior
portion (1 mm wide) traversing the ureteric epithe-
lium and lying free within renal ducts. Larvated
eggs are observed and larvae can be found in urine
of infected animals (Rees, 1953; Lambertsen,
1985). Of several known crassicaudid infections,
those caused by C. boopis are highly pathogenic.
Infections with adult C. boopis can be associated
with a marked thrombophlebitis of the vascular
system draining the kidneys. The tissue reaction
* Corresponding author: Faculty of Veterinary Medicine,
Laboratory of Parasitology and Parasitic Diseases,
University of Liège, Quartier Vallée 2, Av de Cureghem,
6 B43a, 4000 Liège, Belgium. E-mail: llempereur@ulg.
Parasitology Open (2017), Vol. 3, e9; page 1 of 6. ©Cambridge University Press 2017. This is an Open Access article, distributed under
the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives licence (http://creativecommons.org/licenses/by-nc-nd/
4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is unaltered and is
properly cited. The written permission of Cambridge University Press must be obtained for commercial re-use or in order to create a
can cause multiple obstructions of the primary renal
veins. The osmotic stress experienced by the whale
in its naturally saline environment is then aggravated
by a pathologic stress to the kidneys. Consequently,
severe infections with C. boopis could reduce blood
ﬂow from the kidneys to such a level that the whale
succumbs to congestive renal failure. Moreover,
the ﬁnding of intravascular parasitic masses and
associated thrombi supports the possibility of a
thromboembolism in crassicaudiosis. This is espe-
cially true in case of pulmonary lesions with parasite
fragments and mineralized lesions (Lambertsen,
The life cycle of C. boopis is not entirely known
yet. It is largely hypothetical based on the pattern
of lesions observed, and the frequent report of het-
eroxenous transmission for marine Spirurida
(Lambertsen, 1986; Rhode, 2005). This suggests a
somatic migration of C. boopis larvae from the gut
after their ingestion by the whale. The primary
infective route is assumed to involve penetration of
the wall of the gastrointestinal tract by C. boopis
larvae that are ingested by the whale and migration
of these larvae up the mesenteric arteries and the
aorta (Lambertsen, 1986; Díaz-Delgado et al.
2016). Entry of C. boopis into the kidneys, its deﬁni-
tive habitat, could well involve larval movements via
two diﬀerent routes: from the aorta directly within
the wall of the arterial system or by the arterial
blood ﬂow. Thereafter, the developing larvae
would have easy access to both the urinary ductwork
and the renal veins. Finally, by further developing in
the venous system of the kidney, the adult stage
could then extend from the urinary ducts to the
caval vein. Persistent larvae migrans are suggested
by lesions induced by developing C. boopis larvae
that are not carried by the arterial bloodstream to
the kidneys but rather lodge in the capillaries of
other tissues (Lambertsen, 1992).
The ﬁnding of larvae and larvated eggs in the
urine suggest that the primary portal of exit is the
urinary tract. The presence of eggs in the pulmonary
airspace is also compatible with low levels of shed-
ding via the whale’s blow (Lambertsen, 1986).
Krill, such as M. norvegica, which is the principal
prey of ﬁn whales in the northern Atlantic Ocean,
could potentially play a role as an intermediate
host (Lambertsen, 1985; Sigurjonsson and
Vikingsson, 1995; William et al. 2009).
The ﬁnding of young calves infected with C.
boopis suggests either a transplacental transmission
or the urinary contamination of the environment fol-
lowed by an oral infection of the calf before being
able to feed by itself. Finally, galactogenic transmis-
sion cannot entirely be disregarded (Díaz-Delgado
This paper aims at describing a rarely reported
case of C. boopis in ﬁn whale and its molecular
screening for parasite identiﬁcation improvement.
MATERIALS AND METHODS
On 9 November 2015, a ﬁn whale was observed on
the bulb of a vessel in the Channel Terneuzen –
Ghent (The Netherlands –Belgium). According to
the captain of the vessel, the whale had not been
present on the bulb 2 days prior to the observation
(Jan Haelters, personal communication). The ship
(204 m long, cruising speed of 18–20 kts) had
sailed from Porto de Santos (Brazil) to Ghent in 12
days. The ﬁn whale was removed from the bulb in
the port of Ghent and transported to shore for nec-
ropsy (Fig. 1) following a standardized procedure
(Jauniaux et al. 2002).
Parasites from veins and kidneys were preserved
in 80% alcohol for morphological and molecular
identiﬁcation. Cephalic and genital regions of the
parasite were microscopically investigated after
clearing in lactophenol. Renal tissue was preserved
in 10% buﬀered formaline and embedded in
paraﬃn wax. Sections were stained with haematoxy-
lin and eosin for histopathological examination.
Genomic DNA was isolated from 10 worms using
DNeasy Blood & tissue kit (Qiagen, Germany) fol-
lowing the manufacturer’s recommendations. The
18S rRNA gene was ampliﬁed from genomic DNA
by PCR using G18S4-F (5′-GCTTGTCTCAA
AGATTAAGCC-3′) and reverse 136-R (5′TG
(Nadler et al. 2007; Jabbar et al. 2015).
PCRs were conducted in 25 µL volumes con-
taining Taq polymerase master mix (Qiagen,
Germany). PCR cycling conditions were 94 °C for
5 min, then 35 cycles of 94 °C for 30 s, 55 °C
for 30 s and 72 °C for 80 s, followed by 72 °C for
7 min. Amplicons were observed on 2% agarose
gel. A PCR amplifying internal portion of the
18S rRNA gene was designed using primers
TT-3′) and reverse Crassic352F (5′-AAACGGCT
ACCACATCCAAG-3′) in order to facilitate the
sequencing. Examination of PCR amplicons was
done on a 2% agarose gel. PCR products were subse-
quently puriﬁed using MinElute PCR puriﬁcation
kit (Qiagen, Germany) and subjected to automated
DNA sequencing in both directions (Giga genomic
platform, University of Liège). Sequences were
aligned using Clustal Omega (http://www.ebi.ac.
uk) and a consensus was submitted to Blastn
Clinical presentation and post-mortem ﬁndings
The ﬁn whale was a juvenile male of 11·60 m length
showing a slight emaciation with a blubber thickness
2Laetitia Lempereur and others
of 50 mm (dorsal), 35 mm (median) and 35 mm
(ventral) (Fig. 1). The eyes were clear, with a trans-
parent lens and the presence of gas bubbles, which
suggested, together with observation reported by
the captain, that the time of the death was about
2–3 days ago. External observations of the body
showed an impact zone with cutaneous lacerations
of about 1·65 m wide. When the abdominal cavity
was opened, an associated free haemorrhagic and
ﬁbrinous liquid was present. An intestinal haema-
toma of 40 cm in length was observed at the
impact zone. A thrombus was observed in the right
lung and parasite fragments were present in the pul-
monary vessels (Fig. 2). A severe parasitosis was
present in the lumens of the right heart ventricle
and the caudal caval vein (Fig 2). These parasites
(approximately 50) were white to reddish round
worms of approximately 1 m long and 5 mm in
diameter. A renal thrombosis was also observed,
with the presence of round worms of 20 cm in
length and 1 mm in diameter (Fig. 2).
Several parasites found in the caudal caval vein were
observed microscopically. A cephalic extremity was
found on a large striated worm portion of 5 mm in
diameter with a tapering apex (Fig. 3). The head
was located at the very tip of this tapering section
and exhibited a constriction; the mouth bore two
lateral lips (Fig. 3). Worms found in the renal
veins showed a typical posterior extremity on an
attenuated worm section (1 mm in diameter). The
posterior extremity of female worms was distin-
guished by the presence of a constriction before a
rectangular end (Fig. 3). No male posterior extrem-
ity was observed. Larvated eggs measuring 50 µMin
length were found on the parasite cuticle (Fig. 4).
These observations allowed us to identify two frag-
ments most probably belonging to C. boopis.
Parasite fragments found in the lungs were not
Microscopically, signiﬁcant lesions were located
in the kidneys. In the renal thrombosis, a nematode
with larvated eggs was observed in an arteriole
(Fig. 4). A subacute arteritis and periarteritis was
characterized by the inﬁltration of lymphocytes
and macrophages in and around the blood vessel.
In the renal interstitial tissue, worms were sur-
rounded by an area of lymphocytes and macrophages
with the presence of a multinucleate giant cell
Amplicons of about 1700 bp and an internal portion
of 808 bp were visualized on 2% agarose gel. A con-
sensus sequence (GenBank KY263809) was made
based on sequences obtained from these PCR pro-
ducts and was submitted to Blastn (http://blast.
ncbi.nlm.nih.gov) showing 100% similarity with
Crassicauda magna (GenBank KM233410).
Crassicaudiosis is one of the main parasitic diseases
of ﬁn whales (Lambertsen, 1986). The diﬃculties
in ﬁeld sampling, limited possibilities for experi-
mental work and diﬃculties to observe these
specimens in the marine environment make infor-
mation on C. boopis scarce (Lambertsen, 1985;
Balbuena and Simpkin, 2014; Jabbar et al. 2015).
The life cycle is not yet entirely elucidated, and
little is known about potential intermediate hosts.
Fig. 1. Fin whale (Balaenoptera physalus) on the necropsy site.
3Crassicauda boopis in a ﬁn whale (Balaenoptera physalus) ship-struck in the eastern North Atlantic Ocean
Moreover, transmission to calves, which are regu-
larly and heavily infested (Lambertsen, 1992), is sus-
pected to be transplacental, whereas galactogenic
transmission has to be considered even though up
to now no larvae were found in milk or mammary
tissue (Díaz-Delgado et al.2016). Direct transmis-
sion to calves by urine contamination was evoked
(Lambertsen, 1986), which suggests emission of
infective larvae in the environment and therefore a
bypass in the need of an intermediate host. This
suggestion seems unlikely because of the obvious
thick shells of the eggs of C. boopis usually encoun-
tered in environmentally resistant eggs and the fact
that habronematoids are known to use arthropod
intermediate hosts consistently (Anderson, 2000).
In this present case, the size of the juvenile ﬁn
whale corresponds to a recently weaned ﬁn whale,
in which weaning occurs at an age of 6–7 months
and a body size of 11–13 m (William et al. 2009).
Therefore, the present report supports the theory
that infestation could occur transplacentally or
Fig. 2. Nematode segments found in lungs (top), the
caudal caval vein (middle) and the renal vein (bottom) of
the ﬁn whale.
Fig. 3. Anterior extremity (20×) (top), (400×) (middle)
and posterior extremity of female Crassicauda boopis (20×)
4Laetitia Lempereur and others
Crassicaudiosis due to C. boopis is typically a
chronic disease and has proven to be potentially
lethal, mainly due to congestive kidney failure, or
to cause substantial morbidity in those animals
which survive (Lambertsen, 1985,1992; Jauniaux
et al. 2000; Díaz-Delgado et al.2016). In some indi-
viduals, a more acute inﬂammatory reaction sur-
rounds the parasites with exudate or pus. Lesions
associated with C. boopis occur less commonly in
the lungs, which can contain necrotic fragments of
nematodes, as described in this present case, with
mineral deposits (Lambertsen, 1992). Although
numerous C. boopis and lesions similar to those
described by Lambertsen (1986) and Jauniaux
et al.(2000) were found in the ﬁn whale case pre-
sented here, the cause of death could be established
as the collision with the ship on the basis of the pres-
ence of large haematoma at the impact zone and the
absence of evidence of renal failure. The young age
of this whale and the absence of severe reaction
may suggest that the infestation was not at an
advanced chronic stage yet.
Crassicauda genus is represented by large size
nematodes with C. boopis as the second longest
nematode in whales. Consequently, obtaining intact
specimens from host tissues is a real challenge and
the species is frequently only described from frag-
ments, leading to uncertainty in their identiﬁcation.
Therefore, molecular biology could be useful in
the identiﬁcation of these specimens. Consensus
sequence of 18S rRNA gene obtained from these
present samples was similar to the sequence obtained
from parasites found in subcutaneous tissues of a
pygmy sperm whale (Kogia breviceps) and identiﬁed
as C. magna (Jabbar et al. 2015). Additionally, this
sequence was similar to the partial sequence of a
worm located in the kidney of a Cuvier’s beaked
whale (Ziphius cavirostris) (Díaz-Delgado et al.
2016). While adults of C. boopis and C. magna are
morphologically distinct and found in diﬀerent
body sites, molecular analysis of the 18S rRNA
gene seems insuﬃcient for reliable species identiﬁca-
tion. This could be a major restriction mainly for
It is noteworthy that all morphological classiﬁca-
tions to date have included Crassicauda spp. in the
order Spirurida, superfamily Habronematoidea,
family Tetrameridae and subfamily Crassicaudinae
(Lambertsen, 1985; Jabbar et al. 2015), while
recent phylogenetic analysis based on the 18S
rRNA gene showed C. magna as a member of the
Acuarioidea superfamily (Jabbar et al. 2015). The
18S rRNA gene shows highly conserved regions,
and although this gene is often used for deep
phylogenetic relationship investigation, multigene
analysis should be performed to reﬁne this phylo-
This ﬁn whale arrived in Belgium probably after a
ship-strike in the Bay of Biscay or in the Western
English Channel, given the track of the ship and
the estimation of period of death. Fin whales
are large, long-distance swimmers that often occur
far oﬀshore, and not many causes of natural mortal-
ity are known, such as predation or starvation which
are probably of minor signiﬁcance. However, decline
of major zooplankton populations (Steinberg and
Landry, 2017) could lead to poor nutrition and
therefore to an increase in the severity of endemic
parasitism by compromising disease resistance
(Lambertsen, 1992). For this reason, Lambertsen
(1986) suggested that diseases like crassicaudiosis
may be the most signiﬁcant mortality factor in
large balaenopterid whales (Raga et al. 1997).
Further research should be able to collect informa-
tion on animals infected by parasites especially
C. boopis in order to implement a model including
the eﬀect of parasitism in calf and adult whale
Crassicaudiosis is potentially the most signiﬁcant
mortality factor in large balaenopterid and reported
Fig. 4. Larvated eggs of Crassicauda boopis (400×) (top);
histopathological examination of renal tissue: nematode
with larvated eggs in an arteriole. The subacute arteritis
and periarteritis is characterized by inﬁltration of
lymphocytes and macrophages (bottom).
5Crassicauda boopis in a ﬁn whale (Balaenoptera physalus) ship-struck in the eastern North Atlantic Ocean
cases are scarce. Further research is surely needed in
order to elucidate the life cycle of the parasite, its
taxonomy and impact on whale populations.
However, the present report supports the theory
that infestation could occur transplacentally or
The species is frequently only described from
fragments, leading sometimes to uncertainty in
their identiﬁcation. Therefore, molecular biology
could be useful in the identiﬁcation of these speci-
mens with multigene analysis helping to reﬁne iden-
tiﬁcation and phylogenetic analysis.
The authors are very grateful to Allison Balin, Jurgen
Decraene, Bart De Pauw, Françoise Maréchal, Michael
Sarlet and Patrick Vervaet. The authors also thank the
volunteers of the veterinary Faculty of Ghent University
and the veterinary Faculty of Liege University. They are
grateful for the excellent cooperation with the crew of
the Premium do Brasil, the local authorities of the city of
Ghent, port authorities, the Federal public service
health, food chain safety and environment, Citrosuco
(and in particular Jean-Pierre Vandecasteele), the Civil
Protection Unit, and many others for their role in securing
the animal and making the scientiﬁc investigation possible.
This research did not receive any speciﬁc grant from
funding agencies in the public, commercial or not-for-
proﬁt sectors. The work was carried out in the framework
of the Marine Animals Research and Intervention
Network (MARIN), coordinated by the RBINS.
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