Volume11,Number1(ene-jun2017)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
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Neotropical Helminthology, 2017, 11(1), jan-jun: 45-52.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
ANISAKIDAE AND RAPHIDASCARIDIDAE NEMATODES PARASITES OF TUNA
(PERCIFORMES: SCOMBRIDAE) FROM STATE OF RIO DE JANEIRO, BRAZIL
NEMATODOS ANISAKIDAE Y RAPHIDASCARIDIDAE PARÁSITOS DE ATUNES
(PERCIFORMES: SCOMBRIDAE) DEL ESTADO DE RÍO DE JANEIRO, BRASIL
1,* 1,5 2 3
Marcelo Knoff ; Michelle Cristie Gonçalves da Fonseca ; Nilza Nunes Felizardo ; Antonia Lúcia dos Santos ;
2,5 4 1
Sérgio Carmona de São Clemente ; Anna Kohn & Delir Corrêa Gomes
ABSTRACT
We purchased 276 tuna from the fish market, between January/2000 and December/2002 including 107
specimens of Katsuwonus pelamis (Linnaeus, 1758), 5 Auxis thazard (Lacepède, 1800), 92 Thunnus
albacares (Bonnaterre, 1788), 30 Thunnus atlanticus (Lesson, 1830), 25 Thunnus obesus (Lowe, 1839),
and 17 Thunnus thynnus (Linnaeus, 1758) caught offshore of Cabo Frio, State of Rio de Janeiro. Fifty six
(20.28%) of fish were parasitized by at least one parasite. A total of 196 third-stage nematodes larvae were
collected and identified as: Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878), A. physeteris Baylis
1923, Contracaecum sp. and Raphidascaris sp. This study is the first report in Brazil of new hosts records
of A. simplex in T. albacares, T. atlanticus, and T. obesus, A. physeteris in T. albacares, Contracaecum sp.
in T. atlanticus and T. obesus, and Raphidascaris sp. in T. albacares and T. obesus. Their parasite indices
of prevalence, intensity/mean intensity, abundance/mean abundance and range of infection were
presented. The nematodes were collected from up to five sites of infection, stomach, intestine, caecum,
liver and abdominal cavity. A. simplex parasitizing T. obesus presented the higher level of prevalence
(32%), mean intensity (4.6) and mean abundance (1.48); and K. pelamis presented the greater range of
infection (1-17 parasites per fish) and number of sites of infection (stomach, intestine, caecum, liver and
abdominal cavity). The importance of the presence of nematode larvae in these fish for public health was
evaluated.
Neotropical Helminthology
45
Keywords: Anisakid – Auxis thazard – Katsuwonus pelamis – Nematodes – Raphidascaridid – Thunnus albacares –
Thunnus atlanticus – Thunnus obesus – Thunnus thynnus
1Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz -Fiocruz, Rio de
Janeiro, RJ, Brasil
2Laboratório de Inspeção e Tecnologia do Pescado, Universidade Federal Fluminense - UFF, Niterói, RJ, Brasil
3Laboratório de Bioquímica Experimental Computacional em Fármacos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz -
Fiocruz, Rio de Janeiro, RJ, Brasil
4Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz - Fiocruz, Rio de Janeiro,
RJ, Brasil
5Conselho Nacional de Desenvolvimento Cientíco e Tecnológico - CNPq
RESUMEN
Palabras clave: Anisakidos – Auxis thazard – Katsuwonus pelamis – Nematodos – Raphidascarididos – Thunnus albacares –
Thunnus atlanticus – Thunnus obesus – Thunnus thynnus
Para el presente estudio, fueron adquiridos 276 atunes, entre enero de 2000 y diciembre de 2002, en
mercados de peces, siendo 107 ejemplares de Katsuwonus pelamis (Linnaeus, 1758), 5 Auxis thazard
(Lacepède, 1800), 92 Thunnus albacares (Bonnaterre, 1788), 30 Thunnus atlanticus (Lesson, 1830), 25
Thunnus obesus (Lowe, 1839), y 17 Thunnus thynnus (Linnaeus, 1758) pescados en el municipio de Cabo
Frio, Estado de Rio de Janeiro, Brasil. Cincuenta y seis (20,28%) de los peces fueron parasitados por lo
menos con una especie de parásito. Se colectaron un total de 196 nemátodos larvarios y fueron
identificados como: Anisakis (Rudolphi, 1809, det. Krabbe, 1878), A. physeteris Baylis 1923,
Contracaecum sp. y Raphidascaris sp. Este estudio es el primer registro en Brasil con nuevos registros
para los hospederos de A. simplex en T. albacares, T. atlanticus y T. obesus, de A. physeteris en T.
albacares, de Contracaecum sp. en T. atlanticus y T. obesus y de Raphidascaris sp. en T. albacares y T.
obesus. Se presentaron sus índices parasitarios de prevalencia, intensidad/intensidad media,
abundancia/abundancia media y el rango de la variación de la infección. Los nemátodos se colectaron en
la mayoría de los cinco sitios de infección, estómago, intestino, ciego, hígado y cavidad abdominal. A.
simplex parasitando T. obesus presentó el mayor nivel de prevalencia (32%), intensidad media (4,6) y
abundancia media (1,48); y K. pelamis presentó el mayor rango de la variación de la infección (1-17
parásitos por pez) y el número de sitios de infección (estómago, intestino, ciego, hígado y cavidad
abdominal). Se evaluó la importancia de la presencia de larvas de nematodos en estos peces para la salud
pública.
INTRODUCTION
46
fishery products are mainly attributable to
trematodes, cestodes and nematodes. Among these
parasites, the anisakid nematodes are the most
important under the sanitary point of view, since
they are capable to induce pathologies in humans
such as anisakidosis, anisakiosis and
pseudoterranovosis (Klimpel & Palm, 2011). In
humans, these parasitoses can occur after the
ingestion of raw, poor cooked/smoked or
superficially salted fish meat containing infective
larvae (Acha & Szyfres, 2003). These could be
result of combination of two factors: direct action
by the larvae of Anisakidae during tissue invasion;
and interactions between the host immune system
and the substances released by the parasite or
through its presence. Studies including the
possibility to result allergic processes in humans
(Kagei & Isogaki, 1992; Ubeira et al., 2000;
Oomori et al., 2008; Tejada et al., 2015).
The aims of the present study were to investigate
the presence of the anisakid and raphidascaridid
nematode larvae in K. pelamis, A. thazard, T.
albacares, T. atlanticus, T. obesus, and T. thynnus
from the State of Rio de Janeiro, Brazil, identifying
them by morphological characters, stabilish the
parasitary indices of prevalence, intensity, mean
The tuna fish, skipjack tuna Katsuwonus pelamis
(Linnaeus, 1758); frigate tuna Auxis thazard
(Lacepède, 1800); yellowfin tuna Thunnus
albacares (Bonnaterre, 1788); blackfin tuna
Thunnus atlanticus (Lesson, 1830); bigeye tuna
Thunnus obesus (Lowe, 1839), and northern
Bluefin tuna Thunnus thynnus (Linnaeus, 1758)
(Perciformes: Scombridae), usually living in
surface water depth to over 500m (Figueiredo &
Menezes, 2000).
Parasitic nematodes are important pathogens
associated with human and animal health. Some
inhabit the marine environment, where they are
widespread in a variety of hosts. Adults are
commonly found in the digestive tract of marine
mammals. Larvae infect aquatic invertebrates and
non-mammalian vertebrates as intermediate hosts
(Klimpel & Palm, 2011).
Parasitic infections associated with consumption
of fishery products have always been a concern for
the public health and for economy. The main food-
borne zoonoses associated with the consumption of
Neotropical Helminthology, 2017, 11(1), jan-jun Knoff et al.
intensity, abundance, mean abundance, range of
infection, and infection sites; and evaluate the
importance indetecting the presence of nematode
larvae in these fish for public health.
A total of 276 tuna specimens, acquired between
January/2000 and December/2002, i.e., 107 K.
pelamis, (47-81 cm of fork length - FL and 1.8-12
kg of weigh - W), 5 A. thazard (45-53 cm - FL and
1.5-2.9 kg - W), 92 T. albacares (34-83 cm - FL and
1-5.5 kg - W), 30 T. atlanticus (32-55 cm - FL and
1-3.5 kg - W), 25 T. obesus (40-75 cm - FL and 1.6-
8 kg - W), and 17 T. thynnus (50-80 cm - FL and 2,2-
9,4 kg - W), were obtained in small markets selling
fish caught from offshore of the municipality of
Cabo Frio, State of Rio de Janeiro, Brazil. Fish
were necropsied “in loco” and their viscera were
maintained in isothermal boxes with ice and
carried to the Laboratory of Helminth Parasites of
Fish, Oswaldo Cruz Institute, Oswaldo Cruz
Foundation, Rio de Janeiro, Brazil. The tuna
species were identified in accordance with
Figueiredo & Menezes (2000). Internal organs
were examined, and nematode larvae found were
placed in Petri dishes with 0.65% saline.
Nematodes were fixed in AFA (ethanol, formalin,
and acetic acid) at 60 °C, preserved in 70 ºGL
ethanol (Knoff & Gomes, 2012) and sent to
Laboratory of Helminth Parasites of Vertebrates
where the specimens were clarified with Amman's
lactophenol. The taxonomic classification was in
accondance with De Ley & Blaxter (2004) and
larval identification was in accondance with
Felizardo et al. (2009), and Petter & Maillard
(1988). The specimens were observed by bright-
field microscopy (Olympus BX-41). Parasitary
therms used were according to Bush et al. (1997).
Voucher specimens preserved in ethanol 70 °GL
were deposited in the Helminthological Collection
of the Oswaldo Cruz Institute (CHIOC),
FIOCRUZ, Rio de Janeiro, RJ, Brazil.
Fifty six (20.28%) tuna were parasitized by, at
least, one species of nematode parasite larvae.
They were identified as belonging to Anisakidae
Railliet & Henry, 1912, Anisakis Dujardin, 1809:
Anisakis simplex (Fig. 1), Anisakis physeteris (Fig.
2), Contracaecum sp. (Fig. 3); Raphidascarididae
Hartwich, 1954, Raphidascaris Railliet & Henry,
1915: Raphidascaris sp. (Fig. 4). The Anisakidae
and Raphidascarididae specimens collected from
tuna was represented by larval stages, most of them
with high prevalence. A total of 276 third-stage
nematode larvae (L ) were collected. Parasitary
3
indices of prevalence, intensity, mean intensity,
abundance, mean abundance and range of
infection, as well as the infection sites, and the
CHIOC deposit numbers are the depicted in Table
1. The parasitism distribution found in these fish
was: 27 in 107 K. pelamis (25%), 1 in 5 A. thazard
(20%), 12 in 92 T. albacares (13%), 4 in 30 T.
atlanticus (13%), 10 in 25 T. obesus (40%) and 2 in
17 T. thynnus (11%).
The species A. simplex collected of T. obesus, and
A. simplex and A. physeteris collected of A. thazard
occurred with higher parasitary indices of
prevalence (32%, 20%, and 20%, respectively).
The species A. physeteris and Raphidascaris sp. of
T. albacares and Contracaecum sp. of T. atlanticus
and T. obesus occurred with prevalence lower than
10%. The species A. simplex presented the highest
values of mean intensity and mean abundance (8
and 0.94 respectively) in T. thynnus. Anisakis
simplex was observed in the largest number of
infection sites (stomach, intestine, liver, caecum
and abdominal cavity) of K. pelamis.
Single infections occurred in 38 specimens, 30
parasitized with A. simplex, six with A. physeteris
and two with Raphidascaris sp. Co-infections with
two species were observed in 14 fish, i.e., 10 with
Anisakis simplex and A. physeteris, two with
Anisakis simplex and Contracaecum sp., and two
with Anisakis simplex and Raphidascaris sp.
The morphology and morphometry of Anisakidae
A. simplex, A. physeteris and Contracaecum sp. L
3
in the present study was in accordance with the
specimens reported by Petter & Maillard (1988) of
fishes from western Mediterranean sea and by
Neotropical Helminthology, 2017, 11(1), jan-jun Anisakidae and Raphidascarididae of Tuna
MATERIALS AND METHODS
RESULTS
47
DISCUSSION
48
Neotropical Helminthology, 2017, 11(1), jan-jun Knoff et al.
Figure 1. Anisakis simplex from Auxis thazard. A, anterior region, ventral view, showing larval tooth (lt), esophagus (e) and
ventriculus (v); B, detail of larval tooth (lt), ventral view; C, detail of the tail showing mucron (m). Scale bars of A = 1000 µm, B =
50 µm and C = 100 µm.
Figure 2. Anisakis physeteris from Katsuwonus pelamis. A, anterior region, ventral view, showing larval tooth (lt), esophagus (e)
and ventriculus (v); B, detail of larval tooth (lt), ventral view; C, tail without mucron. Scale bars of A = 1000 µm, B = 200 µm and C
= 100 µm.
49
Neotropical Helminthology, 2017, 11(1), jan-jun Anisakidae and Raphidascarididae of Tuna
Figure 3. Contracaecum sp. from Thunnus atlanticus. A, anterior region, ventral view, showing esophagus (e), ventriculus (v),
ventricular appendix (va) and intestinal cecum (ic); B, detail larval tooth (lt), lateral view; C, tail conical, transverse striation,
mucron absent. Scale bars of A = 440 µm, B = 37.5 µm and C = 140 µm.
Figure 4. Raphidascaris sp. from Thunnus obesus. A, anterior region, ventral view, showing larval tooth (lt), nerve ring (nr),
esophagus (e), ventriculus (v) and ventricular appendix (va); B, detail of larval tooth (lt), ventral view; C, tail pointed with well-
dened striations, lateral view. Scale bars of A = 200 µm, B = 50 µm, and C = 400 µm.
50
Neotropical Helminthology, 2017, 11(1), jan-jun Knoff et al.
P (%) I*/MI A/MA RI SI CHIOC
Katsuwonus pelamis
Anisakis simplex
17.7
2.9
0.52
1-17
S, I, L, C, AC
36701, 36702,
36703, 36704
Anisakis physeteris
13.1
1.7
0.22
1-4
S, L, C, AC
36705, 36706,
36707, 36708
Auxis thazard
Anisakis simplex
20
2*
0.40
1-2
S
36721
Anisakis physeteris
20
2*
0.40
1-2
S
36722
Thunnus albacares
Anisakis simplex
11.9
3.7
0.44
1-10
S, I, L, AC
36709, 36710,
36711
Anisakis physeteris
1.1
2*
0.02
1-2
S
38347
Raphidascaris
sp.
1.1
1*
0.01
-
S
36712
Thunnus atlanticus
Anisakis simplex
10
3.3
0.33
1-5
S, I, C, AC
36718, 36719
Contracaecum
sp.
3.3
1*
0.03
-
AC
38348
Thunnus obesus
Anisakis simplex
32
4.6
1.48
1-12
S, I
36713, 36714,
36715, 36716
Raphidascaris sp. 12 1 0.12 - S, I 38349
Contracaecum sp. 4 1* 0.04 - S 36717
Thunnus thynnus
Anisakis simplex 11.7 8 0.94 1-11 S 36720
*Only the intensity is presented, because one specimen was parasitized.
AC = abdominal cavity, S = stomach, I = intestine, L = liver, C = caecum.
Table 1. Prevalence (P), intensity/ mean intensity (I/MI), abundance/ mean abundance (A/MA), range of infection
(RI), sites of infection (SI), and deposit number of Anisakidae and Raphidascarididae third-stage nematode larvae
parasites of Katsuwonus pelamis, Auxis thazard, Thunnus albacares, T. atlanticus, T. obesus, and T. thynnus in
CHIOC, from municipality of Cabo Frio, State of Rio de Janeiro, Brazil.
Alves & Luque (2006) reported K. pelamis
parasitized with Anisakis sp. 1 and Anisakis sp. 2
with prevalence (P), mean intensity (MI) and mean
abundande (MA) of 40%, 2.67, 1.06 and 13.3%,
5.50, 0.73 respectively, comparing with the hosts of
the present study it was parasitized with A. simplex
and A. physeteris with P = 17.7%, MI = 2.9, MA =
0.52 and P = 13.1%, MI = 1.7 and MA = 0.22,
respectively. In Alves & Luque (2006) the site of
infection was the mesentery, differently in the
present study the sites of infections of A. simplex
were stomach, intestine, caecum, liver, and
abdominal cavity and of A. physeteris were
stomach, caecum, liver, and abdominal cavity.
Cardoso et al. (2006) analyzed the parasitism of 79
marine teleosten fish of the State of Rio de Janeiro
from one K. pelamis reporting the presence of a
species of Anisakid not identified. In the present
study, was identified the presence of A. simplex and
A. physeteris.
Felizardo et al. (2009) of Paralichthys isosceles
Jordan, 1890 from the coast of Rio de Janeiro,
Brazil. These larvae have been reported from
various brazilian teleost fish (Knoff et al., 2007,
2013; Felizardo et al., 2009; Fontenelle et al.,
2013; Ribeiro et al., 2014; Fonseca et al., 2016).
The specimens of Raphidascaris sp. larvae
collected in the present study exhibited
morphology consistent with the specimens from
Rio de Janeiro, Brazil by Felizardo et al. (2009).
Mattiucci et al. (2002) investigating frigate tuna
and northem bluefin tuna from Atlantic Coast of
Brazil, found A. typica parasitizing A. thazard and
T. thynnus reported A. typica from both hosts with
prevalence of 100%. Comparing with the present
study A. thazard was parasitized with A. simplex
and A. physeteris, and T. thynnus with A. simplex.
The prevalences were lower in all species (20%,
20%, and 11.7%, respectively).
51
Acha, P & Szyfres, B. 2003. Zoonoses and
Communicable Diseases Common to Man
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and Animals. 3 ed. Vol. III. Scientific and
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Alves, DR & Luque, JL. 2006. Ecologia das
comunidades de metazoários parasitos de
c i n c o e s p é c i e s d e e s c o m b r í d e o s
(Perciformes: Scombridae) do litoral do
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Cardoso, TP, Salgado, RL, Andrade, PF, São
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De Ley, P & Blaxter, M. 2004. A new system for
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characters with molecular trees, and
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monographs and perspectives. E.J. Brill,
Leiden, pp. 633-653.
Felizardo, NN, Knoff, M & Gomes, DC. 2009.
Larval ansakid nematodes of the flounder,
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Neotropical Helminthology, 2017, 11(1), jan-jun Anisakidae and Raphidascarididae of Tuna
Iñiguez et al. (2009) reported A. thazard from
Brazilian coast parasitized with A. physeteris P =
22.2% and A. typica P = 77.8%, comparing with the
present study A. physeteris was very similar and
was found a different species A. simplex P = 20%.
This study is limited to research due some papers
had no complete information about parasitary
indices and sites of infection.
The presence of larval stages of nematodes
indicates the potential of teleostean fish species as
an intermediate hosts in life cycles of parasites,
trophically transmitted in the marine environment
(Klimpel & Palm, 2011; Knoff et al., 2013). The
present study corroborates this statement, since
anisakid larval stages were recovered.
It is necessary to emphasize the higienic-sanitary
importance of Anisakis species found on the
present study, because this larvae causing
anisakiasis worldwide (Klimpel & Palm, 2011).
There is only one reported case of human
“anisakidosis” in Brazil that was identified as
Anisakis-like (Cruz et al., 2010). However, in the
present study anisakid nematode larvae were not
collected from musculature, even in this case it
must be taken into account they where found alive
and with great motility, cause that they are liable to
migrate to the other eatable organs and
musculature, so available to infect humans.
Considering the high number of anisakidosis cases
worldwide, more education programs at all levels
are necessaries focusing on consumption only of
fish that was previously frozen or properly cooked,
therefore, it is recommended that fish should be
gutted on board the boat (Knoff et al., 2007, 2013;
D'amico et al., 2014; Fonseca et al., 2016).
The authors would like to thank Mr. Ricardo
Baptista Schmidt (Serviço de Produção e
Tratamento de Imagens do Instituto Oswaldo
Cruz/FIOCRUZ) for processing the figures. This
work was supported by fellowships CNPq grant
numbers MCGF: 140093/2012-5, SCSC:
308048/2013-0; CAPES grant numbers NNF:
EXPPD000020.
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