D9055.PDF

Rev. sci. tech. Off. int. Epiz., 1996, 15 (2), 533-549
Disease problems of salmonid fish in Japan
caused by international trade
M. YOSHIMIZU *
Summary: The author details the connection between disease outbreaks in
salmonid fish and imports of salmonid eggs into Japan since the 1950s. The
following diseases and species are involved:
- infectious pancreatic necrosis in rainbow trout (Oncorhynchus mykiss)
- infectious haematopoietic necrosis in sockeye (or 'kokanee')
(0. nerka) and masu salmon (O. masu)
salmon
- cold water disease, erythrocyte inclusion body syndrome, and bacterial
kidney disease (caused by Renibacterium salmoninarum) in coho salmon
(O. kisutch), ayu (Plecoglossus altivelis), rainbow trout and masu salmon.
The author also discusses the strategies aimed at controlling the risk of
disease spread through international trade in salmonid fish and fish products
in Japan. Essential in these strategies are the following actions:
- exchange of information on controlling disease problems
- studies to establish standard methods to identify or detect fish pathogens
- fish health certification.
KEYWORDS: Bacterial kidney disease - Cold water disease - Erythrocyte
inclusion body syndrome - Infectious haematopoietic necrosis - Infectious
pancreatic necrosis - International trade - Salmonid fish.
INTRODUCTION
Many disease problems of aquatic animals have been reported recently (11), and
some of these were caused by new pathogens imported with animals via international
trade. In Japan, many species of marine fish larvae were imported from Asian countries
as seed for aquaculture. Also, eggs of rainbow trout (Oncorhynchus mykiss), chinook
salmon (O. tshawytscha),
sockeye salmon (imported O. nerka) and coho salmon
(O. kisutch) were originally imported for aquaculture from the United States of
America (USA). In the 1950s, eggs of rainbow trout were transplanted to Japan from
the USA, and it is believed that the first occurrence of infectious pancreatic necrosis
(IPN) in Japan was as early as 1955 (24). In 1967, a project for transplantation of eggs
of sockeye salmon from Alaska to Hokkaido was commenced (22). In 1971 and 1972,
infectious haematopoietic necrosis (IHN) occurred in hatched fry of sockeye salmon
* Laboratory of Biochemical Process Technology, Department of Marine Bioresources Chemistry,
Faculty of Fisheries, Hokkaido University, Minato 3-1-1, Hakodate, Hokkaido 041, Japan.
534
and in kokanee salmon (Japanese O. nerka), the eggs of which had been incubated
together with imported eggs (3). Two years later, the first outbreak of IHN occurred
on rainbow trout farms in mainland Japan, causing severe economic damage (19).
In 1975, inspections of imported eggs began, using tissue culture methods for fish
pathogenic viruses, or the fluorescent antibody test (FAT) for
Renibacterium
salmoninarum (4). For several years, heavy R. salmoninarum
contamination was
found on eggs, but this gradually decreased in subsequent years. Between 1985 and
1990, erythrocyte inclusion body syndrome (EIBS) and cold water disease were first
observed in coho salmon (21). Cold water disease then spread to rainbow trout and
masu salmon (Oncorhynchus
masu).
INFECTIOUS PANCREATIC NECROSIS
In the 1930s, rainbow trout were first transplanted to Japan from the U S A and
cultured on the mainland of Japan. In the 1950s, however, the marketability of cultured
trout greatly increased, and the demand for rainbow trout eggs among farmers could
not be satisfied by domestic production in Japan. Importations of rainbow trout eggs
from the U S A were therefore resumed. As early as 1955, the first outbreak of a severe
infectious disease occurred in rainbow trout farms, but the pathogen was not identified
until ten years later (the disease was initially designated as 'unknown disease of
rainbow trout') (24). The clinical signs and histopathology of affected fish were similar
to those of IPN as reported by Wood et al. (23) in the USA (14). This disease spread
to a number of locations, and fresh outbreaks occurred each year (Table I and Fig. 1).
The unknown disease was finally diagnosed as IPN by Sano (15). This was the first
description of IPN in Japan, and the first viral disease of fish to be reported in the
country.
TABLE I
Numbers of Japanese Prefectures reporting outbreaks of infectious
pancreatic necrosis in rainbow trout (Oncorhynchus mykiss)
between 1960 and 1970
Year(s)
1960-1964 (total)
1965
1966
1967
1968
1969
1970
No. of Prefectures
reporting/not reporting outbreaks
6/21
8/23
8/23
9/22
12/19
7/24
16/16
The geographical and seasonal distribution of IPN was studied, together with the
susceptibility of freshwater salmonids of the genus Oncorhynchus (16, 17), and IPN
virus (IPNV) was determined to be widely distributed in Japan (Fig. 2).
535
FIG.
1
Outbreaks of infectious pancreatic necrosis in rainbow trout (Oncorhynchus
and amago salmon (O. rhodurus) farms between 1970 and 1988
mykiss)
Experimentally, IPNV was pathogenic for the fry of rainbow trout, amago salmon
(0. rhodurus) and kokanee salmon, but was not pathogenic for the fry of yamame
(landlocked masu salmon, also known as yamabe) (18). To date, the main species of
fish affected by IPNV have been rainbow trout and amago salmon, but IPNV was also
isolated from coho salmon (5), as well as char (Salveninus fontinalis) and masu salmon
cultured with rainbow trout in Japan. In recent years, the fry of rainbow trout have
been observed to be less susceptible to IPNV (12), and the damage attributed to IPN
has decreased.
INFECTIOUS HAEMATOPOIETIC NECROSIS
From 1967 to 1971, Hokkaido Salmon Hatchery (National Hatchery, Fisheries
Agency) imported eggs of chinook salmon from Washington State, USA, to establish
new salmon resources, and the hatched fry were released into the ocean from
Hokkaido. These chinook salmon, however, never returned to Hokkaido. At the same
time, the eggs of sockeye salmon were imported from Alaska, USA (22). An outbreak
of a severe infectious disease occurred in July 1971 at Mori Hatchery (one branch of
Hokkaido Fish Hatchery, belonging to the Hokkaido Government [2]), in the fry of
kokanee salmon originating from Shikotsu Lake in Hokkaido which were cultured
together with imported sockeye salmon eggs at the Chitose Hatchery. In May and June
1972, the same disease occurred in kokanee salmon fmgerlings originating from
Shikotsu Lake and Nishibetsu River. IHN also occurred in sockeye salmon fmgerlings
hatched - at Nijibetsu Hatchery (part of the Hokkaido Salmon Hatchery) and a private
hatchery near Obihiro - from eggs imported from Alaska. These were the first cases
of IHN in Japan (3). The routes of egg transportation and the years of IHN outbreaks
are shown in Figure 3. At Mori Hatchery, mortality reached 80-100% (Fig. 4). At first,
the disease was diagnosed as a bacterial infection, and terramycin was administered
as a therapeutic measure but to no effect. At Nijibetsu Hatchery, the mortality rates of
536
FIG.
2
Distribution of infectious pancreatic necrosis in Japan between 1975 and 1988
kokanee salmon and sockeye salmon were markedly different. Japanese kokanee
salmon were more sensitive to the disease than imported sockeye salmon fingerlings
(Fig. 5). In view of the characteristics of the isolated virus and the occurrence of
necrosis among the granular cells in the stratum compactum of the digestive tract, the
disease was tentatively identified as IHN. At that time, the anti-IHN virus (IHNV)
neutralising serum was not available in Japan, and serological confirmation was
conducted in 1973 at Leetown, West Virginia, U S A (3). Since 1967, eggs of chinook
and sockeye salmon have been imported from North America, but no disease was
recorded in kokanee salmon cultured together with chinook salmon until 1970.
Sockeye salmon eggs were imported from Fire Lake Hatchery, Alaska (USA) in 1970
and Kitoi Hatchery, Alaska (USA) in 1971, prior to recognition of the first IHN
outbreak in Japan. IHN virus was presumably introduced to Hokkaido with the eggs
of sockeye salmon. From 1972, all imported eggs were disinfected with iodine, and
no further outbreaks of IHN have been recorded among imported fish in Hokkaido.
•537
Washington
(chinook salmon
Alaska
(sockeye salmon
[Oncorhynchus
tshawytscha})
[imported O. nerka])
Shikotsu Lake
(kokanee salmon
Chuzenji Lake
(kokanee salmon)
[Japanese O. nerka])
Nishibetsu River
(sockeye salmon)
Chitose Hatchery
67
Nijibetsu Hatchery*
Mori Hatchery*
N-Fish Farm*
* an outbreak of IHN observed
FIG.
3
Routes of egg transportation and years of infectious haematopoietic necrosis (IHN)
outbreaks in Hokkaido
In 1973, IHNV was isolated from chum salmon (O. keta) in Toyama Prefecture,
Japan (19), and IHN has rapidly spread to rainbow trout farms in Honshu Island since
1974 (Fig. 6), where it caused great economic losses for rainbow trout farmers. No
relationship was reported, however, between the outbreak of IHN in kokanee or
sockeye salmon in Hokkaido and the outbreaks of IHN in rainbow trout in Honshu
Island. IHNV was also isolated from masu and amago salmon ( 1 , 19), chum salmon
(26, 27) and ayu (25). Recently, IHN outbreaks have markedly increased in Japan
among kokanee, amago and masu salmon, and among rainbow trout of commercial
size (body weight > 50-80 g) (9, 8, 20).
At present, IHN control projects are under way in Japan using the following
methods (10):
a) All collected eggs to be used for pond culture are disinfected with iodine just
after fertilisation and then again at the early eyed stage.
b) Fish at fry stages with high susceptibility to IHN virus are reared in well-water
or ultraviolet-treated river water (28).
c) When the fish have passed the stage in which they are highly sensitive to IHNV,
they may be transferred to the usual pond.
4
Cumulative mortality of salmon (Japanese Oncorhynehus nerka) from infectious haematopoietic necrosis at Mori Hatcherv in 1971
The kokanee salmon eggs were incubated with sockeye salmon (imported O. nerka)eggs
FIG.
538
5
Mortality rate of Japanese kokanee and imported sockeye salmon (Oncorhynchus nerka) fry reared at
Nijibetsu Hatchery in 1972
FIG.
539
540
FIG. 6
Distribution of infectious haematopoietic necrosis in Japan between 1974 and 1988
BACTERIAL KIDNEY DISEASE
In 1973 and 1974, a disease occurred among juvenile chinook salmon, kokanee
salmon, pink salmon (Oncorhynchus gorbuscha) and yamabe, cultured at the Chitose
culture pond of the Hokkaido Fish Hatchery and the Chitose Branch of Hokkaido
Salmon Hatchery (7). This was shown to be the first case of bacterial kidney disease
(BKD) in Japan (3). Subsequently, seven outbreaks of BKD were confirmed in
Hokkaido. Most of these occurred at the hatcheries which had imported eggs of
chinook or coho salmon from the USA, and it was therefore assumed that the pathogen
had been brought from overseas (6). From 1975, the government Fisheries Agency in
Japan decided to investigate the importation of eggs, and two laboratories in Hokkaido
University and Tokyo University of Fisheries agreed to conduct these inspections.
Imported eggs were collected at Narita (Tokyo) Airport and at least sixty eggs from
each shipping carton were sampled, washed using p h o s p h a t e 4 3 i r f f e r e d saline (pH 7.2)
541
and then centrifuged. Sediments in the centrifuge tubes were spread onto glass slides.
After fixation, specimens were stained using a direct fluorescent antibody test (FAT)
with fluorescein isothiocyanate-conjugated anti-R. salmoninarum rabbit serum, or an
indirect FAT. Detection of the R. salmoninarum antigen on the surface of imported
eggs between 1980 and 1982, and between 1983 and 1992, is shown in Tables II and
III, respectively. Between 1980 and 1989, R. salmoninarum antigen was detected in
imported eggs, but it was difficult to determine whether this R. salmoninarum was
alive or killed. Outbreaks of BKD occurred, however, at all locations where the
FAT-positive eggs were incubated and where hatched fish were cultured (Fig. 7). The
effect of iodophore on the infectivity of R. salmoninarum
is shown in Figure 8.
R. salmoninarum was killed by washing with iodophore at a concentration of 100 parts
per million (ppm) for 20 min. However, R. salmoninarum with 50% KDM-2 (kidney
disease medium - a growth medium for kidney disease bacterium, could not be killed
by iodophore at 100 ppm for 20 min (6). On the basis of this data, it was assumed that
some R. salmoninarum detected on the surface of imported eggs might still be alive.
However, contamination of R. salmoninarum on imported eggs gradually decreased
each year. It may have been the case that eggs were washed and disinfected and that
some of the mature broodfish were treated with erythromycin prior to export, which
would explain the results of the inspection of broodstock at export and inspections of
eggs after import.
ERYTHROCYTE INCLUSION BODY SYNDROME AND COLD
WATER DISEASE IN JAPAN
In 1986, severe anaemia with less than 20% haematocrits was observed in coho
• salmon cultured in Miyagi Prefecture. Erythrocytes had characteristic inclusion bodies
which contained enveloped viral particles with a diameter of approximately 77 nm (21,
13). This disease occurred each subsequent year, and almost all eggs of the coho
salmon involved had been imported from Washington or Oregon States, USA. In
Japan, Prefectural Fisheries Experimental Stations and several aquaculture companies
are continually attempting to produce eggs from mature coho salmon, but the
percentage of imported eggs in pen-culture projects is still high (Fig. 9).
Epizootiological data show that EIBS is a major contributor to the mortality of coho
salmon (20-30%; sometimes 60-90%) reared in saltwater and freshwater culture in
Japan, and causes great economic loss to the industry.
In 1990, Cytophaga (Flexibacter) psychrophila was first isolated in Japan from
diseased coho salmon in Miyagi and Iwate Prefectures. Imported eggs were inspected
by Miyagi Prefectural Fisheries Experimental Station, using the method described
above for BKD, and the C. psychrophila antigen was detected by FAT. This disease
has now spread to ayu, rainbow trout and masu salmon cultured in Japan.
DISCUSSION
Until 1955, viral diseases such as IPN or IHN were not recorded among rainbow
trout, kokanee and masu salmon cultured in Japan. Eggs of rainbow trout have been
transplanted to Japan from the U S A since 1950, and the first IPN outbreaks in Japan
origin
FAT:fluorescentantibody test
USA: United States of America
- negative
? doubtful
11 December 1980
Oregon State, USA
20 December 1980
Oregon and Washington States, USA
24 December 1980
Oregon State, USA
12 January 1981 Oregon State, USA
12 December 1981
Washington State, USA
12 December 1981
Oregon State, USA
14 December 1981
Oregon State, USA
19 December 1981
Oregon State, USA
19 December 1981
Washington State, USA
24 December 1981
Washington State, USA
12 January 1982 Oregon State, USA
16 January 1982 Oregon State, USA
17 January 1982 Oregon State, USA
11 December 1982
Washington State, USA
18 December 1982
Oregon State, USA
22 December 1982
Washington State, USA
28 December 1982
Washington State, USA
6 January 1983
Washington State, USA
20 January 1983
Washington State, USA
2 March 1983
Soviet Union
Date
TABLE II
Gram stain
+
0:
1:
2:
3:
positive
no cells on the glass slide
a few cells
1 to 10 cells/field (x 40)
many cells
Detection of R. salmoninarum antigen
Co-agglutination test
FAT
Detection of Renibacterium salmoninarum antigen on the surface of eggs imported
into Japan between December 1980 and March 1983
542
543
TABLE
III
Detection of Renibacterium salmoninarum antigen on the surface of coho salmon
(Oncorhynchus kisutch) eggs imported into Japan between 1984 and 1992
Year
No. of eggs
(x 1,000)
No. of
specimens
1984
1985
1986
1987
1988
1989
1990
1991
1992
12,000
18,408
29,000
27,770
43,000
50,802
45,601
30,170
27,336
66
135
129
148
186
294
330
228
294
No. (%) positive for
R. salmoninarum
antigen
20
10
12
21
4
10
0
0
0
(30.3)
(7.4)
(9.3)
(14.2)
(2.2)
(3.4)
(0)
(0)
(0)
Virus isolation
(%)
0
1
0
0
0
0
0
0
0
(0)
(0.7)
(0)
(0)
(0)
(0)
(0)
(0)
(0)
occurred in the early 1950s. The causative virus was not identified, however, and the
epizootic was designated 'unknown disease of rainbow trout'. Some control or
prevention measures were attempted by several prefectural experimental stations, but
the disease spread rapidly to many locations, and recurred each subsequent year. This
unknown disease was finally diagnosed as IPN by Sano in 1971 (15). This was the first
fish viral disease to be recognised in Japan.
In 1967, the transplantation of eggs of chinook salmon from Washington State
(USA) to Hokkaido (Japan) was initiated. Prior to 1970, no outbreaks of disease were
recorded in kokanee salmon cultured together with imported chinook salmon. In 1970,
eggs of sockeye salmon were imported from Alaska. Each following year, IHN
outbreaks occurred among Japanese kokanee salmon fmgerlings cultured with
imported sockeye salmon. The same disease occurred again in kokanee salmon
fmgerlings and sockeye salmon fmgerlings in the following years. These were the first
outbreaks of IHN in Japan. The mortality rates of Japanese kokanee salmon and
sockeye salmon were different, and native kokanee salmon were more sensitive to this
disease than imported sockeye salmon fingerlings. It is assumed that IHNV was
introduced to Japan with the eggs of imported sockeye salmon. The first outbreaks of
IHN in rainbow trout farms in mainland Japan occurred two years later. Many farms
have subsequently been severely damaged.
Since 1975, the government Fisheries Agency in Japan has funded a project on the
inspection of imported eggs. Between 1975 and 1990, most of the imported salmon
eggs were inspected using tissue culture methods for fish pathogenic viruses and the
FAT for R. salmoninarum. The first years showed that the surfaces of imported eggs
were very dirty (with mud or debris of aquatic plants) and were frequently found to
be contaminated with R. salmoninarum
antigen. This heavy contamination of
R. salmoninarum on eggs decreased each year. Over the fifteen years in which these
inspections were conducted, no fish pathogenic viruses have been isolated, except in
one specimen where IPNV (serotype VR-299) was isolated from imported coho
544
FIG. 7
Confirmed outbreaks of bacterial kidney disease in Japan between 1973 and 1980
salmon eggs. Since 1990, the inspection project on imported eggs has been continued
by the Fish Disease Centre (FIDIC) of the Japan Fisheries Resource Conservation
Association. Until now, R. salmoninarum antigen has been detected only occasionally.
Between 1985 and 1990, EIBS and cold water disease were observed in coho
salmon culture facilities in Japan and subsequently spread to ayu, rainbow trout and
masu salmon. Imported coho egg inspections conducted by the Miyagi Prefectural
Fisheries Examination Centre have detected a high incidence of
Cytophaga
psychrophila antigen.
Recently, larvae of many species of marine fish and shellfish have been imported
to Japan from South-East Asian countries, as seed for mariculture. In this case,
disinfection by chemicals of the larval stage of fish and shellfish is impossible. The
celles
FIG.
8
and treated with 100 ppm iodophore for 20 min
- • - cells suspended in 50% KDM-2
Effect of iodophore on the infectivity of Renibacterium salmoninarum
KDM: growth medium for kidney disease bacterium
ppm: parts per million
washed cells treated with 100 ppm iodophore for 20 min
suspended in 50% KDM-2 and treated with 50 ppm iodophore for 20 min
washed cells treated with 50 ppm iodophore for 20 min
control (without treatment)
OD: optical density
*
545
546
FIG.
9
Number of eggs imported and inspected, and eggs from coho salmon
(Oncorhynchus kisutch) matured in Japan, from 1982 to 1990
following considerations are therefore very important to prevent and control the
disease problems caused by pathogens imported with these animals:
a) exchange of disease information between exporter and importer
b) establishment of standard methods to detect new fish pathogens
c) health certification of animals for import.
* *
MALADIES DES SALMONIDÉS
INTERNATIONAL. - M. Yoshimizu.
AU
JAPON,
LIÉES
AU
COMMERCE
Résumé : L'auteur analyse la corrélation existante entre les foyers de maladies
chez les salmonidés et les importations d'œufs de saumon au Japon depuis les
années 1950. Les maladies et espèces concernées sont les suivantes :
- nécrose pancréatique infectieuse de la truite arc-en-ciel (Oncorhynchus
mykiss) ;
- nécrose hématopoiétique infectieuse du saumon rouge (ou
(O. nerka) et du saumon masou (O. masu) ;
sockeye)
547
- maladie de l'eau froide, nécrose érythrocytaire et rénibactériose (due à
Renibacterium salmoninarum) chez le saumon coho (O. kisutch), l'ayu
(Plecoglossus altivelis), la truite arc-en-ciel et le saumon masou.
L'auteur analyse également les stratégies visant à prévenir la propagation
de maladies liée aux échanges internationaux de salmonidés et des produits de
la pisciculture au Japon. Ces stratégies reposent essentiellement sur les
mesures suivantes :
— échange d'informations sur la lutte contre les maladies ;
— études en vue d'élaborer des méthodes normalisées applicables à la
reconnaissance ou la recherche d'agents pathogènes spécifiques des poissons ;
— certificats sanitaires destinés aux poissons.
MOTS-CLÉS : Commerce international - Maladie de l'eau froide - Nécrose
érythrocytaire - Nécrose hématopoïétique infectieuse Nécrose
pancréatique infectieuse — Rénibactériose - Salmonidés.
*
*
*
ENFERMEDADES DE LOS SALMÓNIDOS EN JAPÓN CAUSADAS POR EL
COMERCIO INTERNACIONAL. - M. Yoshimizu.
Resumen: El autor examina las relaciones existentes entre brotes de
enfermedad en peces salmónidos y la importación de huevos de salmónido a
Japón desde la década de 1950. Están implicadas en tales procesos las
siguientes especies y enfermedades:
— necrosis pancreática
mykiss);
infecciosa en la trucha arco iris (Oncorhynchus
- necrosis hematopoyética infecciosa en el salmón rojo (O. nerka) y en el
salmón japonés (O. masu);
- enfermedad del agua fría, síndrome necrotico eritrocitario y
renibacteriosis (causada por Renibacterium salmoninarum) en el salmón coho
(O. kisutch), el ayu (Plecoglossus altivelis), la trucha arco iris y el salmón
japonés.
El autor
dispersión
salmónidos
estrategias
describe asimismo las estrategias para controlar el riesgo de
de enfermedades derivado del comercio internacional de
y productos pesqueros en Japón. Esenciales para el éxito de dichas
resultan las actuaciones siguientes:
— intercambio de información sobre cuestiones de control sanitario;
- estudios para el establecimiento de métodos normalizados
identificación o detección de patógenos piscícolas;
- certificados sanitarios para peces.
de
PALABRAS CLAVE: Comercio internacional - Enfermedad del agua fría Necrosis hematopoyética infecciosa - Necrosis pancreática infecciosa Peces salmónidos - Renibacteriosis - Síndrome necròtico eritrocitario.
*
*
*
548
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