D9125.PDF

Rev. sci. tech. Off. int. Epiz., 16 (1), 146-160
Risk of spread of penaeid shrimp viruses in the
Americas by the international movement of live
and frozen shrimp
D.V. Lightner, R.M. Redman, B.T. Poulos, L.M. Nunan, J.L. Mari &
K.W. Hasson
Department of Veterinary Science, Aquaculture Pathology Group, Veterinary Science/Microbiology Building
#90, Room 114, Tucson, Arizona 85721, United States of America
Summary
Within the past decade, viral diseases have emerged as serious economic
impediments to successful shrimp farming in many of the shrimp-farming
countries of the world. In the western hemisphere, the viral agents of Taura
syndrome (TS) and infectious hypodermal and haematopoietic necrosis have
caused serious disease epizootics throughout the shrimp-growing regions of the
Americas and Hawaii, while in Asia the viral agents of white spot syndrome (WSS)
and yellow head (YH) have caused pandemics with catastrophic losses.
The international transfer of live shrimp for aquaculture purposes is an obvious
mechanism by which the viruses have spread within and between regions in
which they have occurred. Shrimp-eating gulls, other seabirds and aquatic
insects may also be factors in the spread of shrimp viruses between and within
regions.
Another potentially important mechanism for the international spread of these
pathogens is the trade in frozen commodity shrimp, which may contain viruses
exotic to the importing countries. The viral agents of W S S , YH and TS have been
found, and demonstrated to be infectious, in frozen shrimp imported into the
United States market. Mechanisms identified for the potential transfer of virus in
imported frozen products to domestic populations of cultured or wild penaeid
shrimp stocks include: the release of untreated liquid or solid wastes from shrimp
importing and processing plants directly into coastal waters, improper disposal of
solid waste from shrimp importing and processing plants in landfills so that the
waste is accessible to gulls and other seabirds, and the use of imported shrimp as
bait by sports fishermen.
Keywords
Americas - Aquaculture - Diagnosis - Infectious hypodermal and haematopoietic
necrosis - Penaeid shrimp - Taura syndrome - Viral diseases - White spot syndrome Yellow head syndrome.
Introduction
At present, eight viruses (or groups of closely related viruses)
are known to be enzootic in western hemisphere penaeid
shrimp, and four of these have emerged as serious pathogens
in one or more species of cultured shrimp (Appendix and
Table I). Diseases due to the viral agents of infectious hypodermal and haematopoietic necrosis (IHHN) and Taura
syndrome (TS) have caused episodes of major mortality in
cultured shrimp and significant economic losses to the
shrimp-farming industries of the western hemisphere ( 2 2 , 3 6 ,
37, 3 9 ) . Taura syndrome virus (TSV) and IHHN virus
(IHHNV) are. of concern to the shrimp-farming industries of
the Americas because they are established in both wild and
cultured penaeid shrimp in the region, and because these
pathogens are the cause of significant disease losses in
cultured shrimp (37).
147
Rev. scitech.Off. int. Epiz., 16(1]
Table I
Viruses of penaeid shrimp reported from the eastern hemisphere (Asia,
Australia, Europe and Africa) and western hemisphere
(the Americas and Hawaii)
(compiled from 36)
Eastern
hemisphere
Western
hemisphere
MBV group
BMN group
WSSV complex
PHRV
BP
IHHNV
HPV
LPV
SMV
IHHNV
HPV
Picornavirus
None
TSV
Rod-shaped single-stranded
ribonucleic acid
(ssRNA) viruses
YHV
LOV
None
Reo-like viruses
REO-III
REO-IV
REO-III
Toga-like viruses
None
LOW
Rhabdovirus
None
RPS
Iridovirus
None
IRDO
Virus or virus group
Baculo and baculo-like viruses
Parvo and parvo-like viruses
MBV:
BP:
BMN:
Penaeus monodon-type baculovirus
Baculovirus penaei-type virus
baculoviral mid-gut gland
necrosis-type virus
WSSV: white spot syndrome virus
PHRV: haemocyte-infecting non-occluded
baculovirus
IHHNV: infectious hypodermal and
haematopoietic necrosis virus
HPV:
LPV: lymphoidal parvo-like virus
SMV: spawner-isolated mortality virus
TSV: Taura syndrome virus
YHV: yellow head virus
LOV: lymphoid organ virus
REO: reo-like virus
LOW: lymphoid organ vacuolization virus
RPS: rhabdovirus of penaeid shrimp
IRDO: shrimp iridovirus
penaeid shrimp from Asian countries ( 1 5 ) in which WSSV
and YHV are currently enzootic and causing serious
epizootics. Since WSSV and YHV have been demonstrated to
be present in frozen, imported commodity shrimp in the US
market (D.V. Lightner, unpublished data), the threat of
accidental introduction and spread of these pathogens into
the shrimp culture industries, or into wild stocks, may be
significant.
The purpose of this paper is to review the biology, available
diagnostic and detection methods, current status, geographic
distribution and the possible mechanisms for international
transfer of the principal viral diseases which are adversely
affecting the shrimp culture industries of the world.
The viruses of concern
Taura syndrome virus
TSV is perhaps the most recently characterised penaeid
shrimp virus. TSV has been tentatively classified with the
Picomoviridae,
based on its morphology (32 ran nonenveloped icosahedron), cytoplasmic replication, buoyant
density of 1.338 g/ml, genome consisting of a linear,
positive-sense single-stranded ribonucleic acid (ssRNA) of
approximately 9 kilobases (kb) in length, and having three
major polypeptides ( 5 5 , 4 0 and 2 4 kiloDalton [kDa]) and one
minor polypeptide ( 5 8 kDa) comprising its capsid (4, 2 2 , 3 6 ,
37).
hepatopancreatic parvovirus
Infectious hypodermal and haematopoietic
necrosis virus
Viral diseases have also severely affected the shrimp-farming
industries of the eastern hemisphere. In the shrimp-growing
regions of the Indo-Pacific, at least nine viruses, or groups of
closely related viruses, are recognised in cultured shrimp
(Appendix and Table I). Five of the nine virus groups have
been documented as being responsible for serious regional
disease epizootics. Two of the viruses, members of the white
spot syndrome group of baculo-like viruses and of the yellow
head syndrome group (for the purposes of this paper, these
viruses will be called W S S V and YHV, respectively) have
caused massive pandemics in the Indo-Pacific region and
cumulative economic losses well into the billions of United
States (US) dollars.
The Asian viruses of the WSSV and YHV groups, however,
also pose potentially serious threats to the shrimp culture
industries of the Americas. Laboratory studies have shown
some important American penaeids to be susceptible to
infection by WSSV and YHV and to suffer serious disease
when exposed during certain stages of life (Table II).
The United States of America (USA) is a major market for
shrimp, annually importing thousands of tons of cultured
IHHNV is the smallest of the known penaeid shrimp viruses
(1, 3, 3 6 ) . The IHHN virion is a non-enveloped icosahedron
averaging 2 2 n m in diameter, with a density of 1.40 g/ml in
CsCl, containing linear single-stranded deoxyribonucleic acid
(ssDNA) with an estimated size of 4.1 kb, and a capsid that
has polypeptides with molecular weights of 7 4 , 4 7 , 3 9 and
37.5 kDa. As a result of these characteristics, IHHNV has been
classified as a member of the family Parvoviridae (3, 3 6 , 3 7 ) .
White spot syndrome baculovirus complex
At least five viruses in the WSS complex have been named in
the literature, and these appear to be very similar, if not the
same virus. The names of these viruses and the diseases they
cause are summarised in the Appendix. All are very similar in
morphology and replicate in the nuclei of infected cells, which
are typically found in tissues of ectodermal and mesodermal
origin. Infected nuclei in enteric tissues (i.e. mid-gut mucosa
and hepatopancreatic tubule epithelium) are rarely, if ever,
present (36).
Isolated virions from this WSS complex, when contrasted by
negative staining and viewed by transmission electron
microscopy (TEM), are enveloped, elliptical to ovoid in shape,
148
Rev. sci tech. Off. int. Epiz., 16(1)
Table II
Susceptibility to and severity of disease in important American penaeid shrimp to infectious hypodermal and haematopoietic necrosis virus, Taura
syndrome virus, Baculoviruspenaei-type and yellow head virus as determined from natural and experimental infections
IHHNV
Species
L
TSV
wssv
BP
J
A
L
PL
J
A
L
PL
J
A
L
PL
+
+
++
-
++
+
++
++
-H-
++
+
+
?
P. setifews
+
-?
++
+
+
?
-
P. schmitti
+
++
+
-
-
- -
?
++
7
++
?
Penaeus
+
vannamei
+
P. stylirostris
P. aztecus
P. duorarum
P.
californiensis
PL
- -- -- -
+
+
+
7
7
- -
++
+
7
?
+
- -
-
+
+
+
-
YHV
J
A
L
PL
++
++
?
-
?
++
?
?
?
J
++
?
++
?
?
?
?
?
?
?
?
?
-
?
++
++
?
?
-
++
?
++
+
+
?
++
+
?
?
-
++
?
++
+
?
++
+
?
?
-
•H-
?
+
+
+
+
+
?
?
?
?
?
?
?
?
J:
juvenile
-
-
IHHNV:
TSV:
BP:
infectious hypodermal and haematopoietic necrosis virus
Taura syndrome virus
Baculovirus penseMype viruses
A:
adult
-:
neither infection nor disease reported or known
WSSV:
white spot syndrome virus
+
infection occurs but not accompanied by serious disease or mortality
YHV:
yellow head virus
++:
serious disease, some mortalities or reduced performance may accompany infection
t:
larval stage
?:
not known
Pt:
postlarvae
and average approximately 120 nm in diameter by 3 0 0 n m in
length, with size variations ranging from 100 to 140 n m and
2 7 0 to 4 2 0 nm, respectively. Some virions possess a tail-like
appendage at one extremity, which is an extension of the
envelope. Nucleocapsids are rod-shaped with blunted ends,
measure 85 nm by 2 6 0 n m (a range of 7 0 to 9 5 nm by 2 2 0 to
3 0 0 nm, respectively), and display a superficially segmented
appearance with an angle of 90° to the long axis of the
particle. The nucleic acid of WSS viruses is a large single
molecule of circular double-stranded DNA (dsDNA) which is
larger than 150 kilobase pairs (kbp) in length (14, 3 2 , 4 0 , 5 7 ,
61). The characteristics of the WSSV complex most resemble
those of the members of the Baculoviridae (19, 4 3 ) .
Yellow head virus group
A
shrimp which show gross signs of the disease, and bioassay,
which demonstrates the presence of the virus in
asymptomatic carrier shrimp (or other appropriate samples),
using specific pathogen-free (SPF) juvenile Penaeus
vannamei,
which serve as the indicator for the presence of the virus
(Table III). Shrimp with acute, natural or induced TSV
infections display a distinctive histopathology, which consists
of multifocal areas of necrosis of the cuticular epithelium and
subcutis (of the general cuticle, gills, appendages, foregut and
hindgut). The lesion is characterised by the presence of
numerous variably sized eosinophilic to basophilic
cytoplasmic inclusion bodies, which give TSV lesions a
'peppered' or 'buckshot' appearance, which is considered to
be pathognomonic for the disease (7, 8, 2 2 , 3 6 , 3 9 ) .
YHV from South East Asia (5, 11) and the morphologically
similar lymphoid organ virus (LOV) from Australia (54) are
rod-shaped viruses which replicate in the cytoplasm of
infected cells. For the purposes of this paper, these viruses will
be called YHV. Virions of YHV are enveloped and measure 4 4
by 173 nm in length (with a range of 3 8 to 5 0 nm by 160 to
186 nm, respectively), containing cylindrical nucleocapsids of
- 1 5 nm in diameter and a genome composed of a single piece
of ssRNA. While not yet adequately characterised, YHV has
been suggested to be a member of the family Khabdoviridae or
the Paramyxoviridae
(17, 5 4 ) .
A complementary DNA (cDNA) probe has recently been
developed for TSV and has been shown to provide excellent
diagnostic sensitivity when used as a non-radioactive
digoxigenin (DIG) labelled probe with in situ hybridization
assays with fixed tissue (Table III). Intact cells within and near
pathognomonic TS lesions show a very strong reaction with
cDNA probes by in situ hybridization assays ( 2 3 , 3 6 ) . While
the cDNA probe has been used successfully as a diagnostic
Teagent in dot blot assays with partially purified TSV, this
method has not yet been routinely applied to fresh or frozen
tissue homogenates.
Diagnostic methods and
epizootiology
Refinements to the in situ hybridization assay for TSV have
recently been developed. Hesson et al. found that
over-fixation in Davidson's fixative, which is acidic, results in
acid hydrolysis and destruction of the TSV ssRNA genome in
tissues left more than a few days in this fixative (24).
Development of a near-neutral fixative, named the
'RNA-friendly' (R-F) fixative, followed this discovery, and its
use has improved the diagnostic sensitivity of in situ
hybridization assays for TSV. The combination of fixation by
R-F and in situ hybridization is currently the most rapid and
Taura syndrome
Diagnosis of Taura syndrome
The current diagnostic methods for TSV include the
demonstration of diagnostic histopathology in acutely affected
149
Rev. sci tech. Off. int. Epiz., 16(1)
Table III
Summary of diagnostic and detection methods for the major viruses of concern to the shrimp culture industries of the Americas
(modified from 36)
IHHNV
Method
Direct BF/LM
Phase contrast
Dark-field LM
Histopathology
Enhancement/histology
Bioassay/histology
Transmission EM
Scanning EM
HPV
BP
TSV
YHV
WSSV
++
++
++
++
+++
+
+++
•+
-
—
+++
+
++
++
•
•
—
R&D
R&D
R&D
+++
++
++
++
++
+
+
+
+
+
+
R&D
R&D
-
-
-
++
++
++
+
++
++
+
-
R&D
-
—
Fluorescent antibody
R&D
ELISA with PAbs
R&D
ELISA with MAbs
R&D
DNA probes
+++/K
+++/P
++/P
+++/K
R&D
++/K
+++
+++
+++
++/R&D
R&D
+++
PCR
IHHNV:
HPV:
BP:
TSV:
YHV:
WSSV:
-:
+:
++:
+++:
R&D:
K:
P:
infectious hypodernial and haematopoietic necrosis virus
hepatopancreatic parvovirus
Baculovirus penaei-type viruses
Taura syndrome virus
yellow head virus
white spot syndrome virus
no known or published application of technique
application of technique known or published
application of technique considered by authors to provide sufficient diagnostic
accuracy or pathogen detection sensitivity for most applications
technique provides a high degree of sensitivity in pathogen detection
technique in research and development phase
diagnostic kit
digoxigenin-labelled deoxyribonucleic acid probe
sensitive method available for detection of TSV infections in
penaeid shrimp (24).
Application of the polymerase chain reaction (PCR) for the
detection of TSV has recently been accomplished, using
sequence information from cloned cDNA segments of the TSV
genome (J. Mari et al., unpublished findings; L.M. Nunan et
al., unpublished findings). Since the nucleic acid of TSV is
ssRNA instead of DNA, the RNA template is converted to
cDNA using reverse transcriptase (RT) before the target
nucleic acid segment is amplified by. RT-PCR. Primers were
chosen which amplify a small (~ 2 0 0 bp) segment of the TSV
genome. The RT-PCR method has been successfully applied
to the detection of TSV in hemolymph samples, taken from
TSV-infected shrimp in acute, recovery, and chronic phases of
the disease, and tissue homogenates following sucrose
gradient purification of the virus. However, the successful use
of RT-PCR for the detection of TSV in samples prepared from
fresh or frozen tissue homogenates has so far been
problematic and will require further development. This
technical limitation, for now, restricts the application of the
RT-PCR technique to fresh hemolymph samples and
precludes its application to frozen or fresh whole shrimp
samples or to the testing of postlarvae (PL), which are too
small to bleed.
-
Methods
BF:
LM:
EM:
ELISA:
PAbs:
MAbs:
DNA:
PCR:
bright field light microscopy of tissue impression smears, wet-mounts.
stained whole mounts
light microscopy
electron microscopy of sections or of purified or semi-purified virus
enzyme-linked immunosorbent assay
polyclonal antibodies
monoclonal antibodies
deoxyribonucleic acid
polymerase chain reaction
S p e c i e s and life s t a g e s a f f e c t e d
TSV is known to infect a number of penaeid shrimp species
(Table II). It causes serious disease in the PL, juvenile and
adult stages of P. vannamd (8, 3 6 , 39). In larval and early PL
P. vannamd, infection by TSV is apparently not expressed
until about PL-11 or 12 ( 1 1 - to 12-day-old postlarvae) when
severe disease and mortalities have been noted in infected
populations ( 3 6 ) . While experimental infections in the PL
stages of P. setiferus have resulted in serious disease, infection
apparently results in less serious disease in the juvenile and
adult stages of P. setiferus (47) and in the juvenile P. schmitti.
Other important American penaeids, such as P. stylirostris
and P. aztecus, can be infected by TSV in the PL and juvenile
stages, but these species seem to be highly resistant to disease
( 3 6 , 4 7 ) . Of the Asian species challenged in laboratory studies
with TSV, juvenile P. chinensis developed moderate infections
and disease accompanied by some mortalities ( 3 6 ) , while
juvenile P. monodon and P. japonicus were found to be
resistant to infection in similar laboratory challenge studies
(9).
Geographic distribution
Between 1991 and 1 9 9 3 , TS emerged as a major epizootic
disease of P. vannamei in Ecuador, and spread rapidly
150
throughout most of the shrimp-growing regions of Latin
America, often following the introduction of stock from
affected areas (8, 2 2 , 2 3 , 2 8 , 3 6 , 3 7 , 3 9 , 6 0 ) . In 1 9 9 2 and
1993, P. vannamei accounted for more than 9 0 % (about
132,000 metric tons) of the farmed shrimp production in the
Americas or about 1 5 % to 2 0 % of the total world production
of farmed shrimp (50, 5 1 ) . As P. vannamei is the principal
penaeid shrimp species used in aquaculture in the Americas
(52, 59), TS has caused serious losses to the shrimp-farming
industry. The economic impact of TS in the Americas, since its
recognition in Ecuador in 1 9 9 2 and subsequent spread, may
exceed 2 billion US dollars.
In Ecuador, TS was first recognised in commercial penaeid
shrimp farms located near the mouth of the Taura River in the
Gulf of Guayaquil, Ecuador, in mid-1992 ( 2 8 , 3 9 , 6 0 ) .
Retrospective studies have shown that TS was present in at
least one shrimp farm in the Taura region of Ecuador in
September 1 9 9 1 (D.V. Lightner, unpublished data; 2 3 ) and a
TS-like condition has been reported to have occurred even
earlier (February 1990) in cultured P. vannamei in Colombia
(34).
During 1 9 9 4 , TS spread to and occurred on shrimp farms
throughout much of Ecuador, as well as on single or multiple
farm sites in Peru, on both coasts of Colombia, in western
Honduras, El Salvador, Guatemala, Brazil and the USA,
occurring at isolated sites in Florida and Hawaii (8, 3 6 , 3 9 ) .
By mid-1996, the disease had expanded its distribution to
include virtually all of the shrimp-farniing regions of the
Americas. Regions or countries included in its expansion since
1994, demonstrated by documented cases, include: both
coasts of Mexico, Nicaragua, Costa Rica, Panama, and the US
states of Texas and South Carolina (23, 3 6 , 3 7 ) .
TSV has been documented in wild PL and adult P. vannamei
on several occasions. The disease was diagnosed in wild PL
collected during mid-1993 off Puna Island near the mouth of
the Gulf of Guayaquil, Ecuador, in wild adult P. vannamei
collected off the Pacific coast of Honduras and El Salvador,
and from coastal Chiapas in southern Mexico ( 3 5 , 3 6 , 3 7 ) .
The affected adult P. vannamei showed high mortalities and
diagnostic lesions of the disease ( 3 7 ) . Significantly, this
occurrence of Taura syndrome in wild PL and adult
broodstock illustrates the potential for this disease to become
established in wild stocks, where its potential to transmit
infection to commercial penaeid shrimp fisheries is unknown.
This situation has been further complicated by discoveries
that an aquatic insect and seabirds may be involved in the
epizootiology of TS ( 2 1 , 2 2 , 3 7 ) . The salinity-tolerant water
boatman, Trichocorixa
reticulata (Corixidae),
which is a
common inhabitant of shrimp grow-out ponds' in much of the
Americas, was noted initially at a farm site in Ecuador, which
was in the midst of a severe epizootic of TS. TSV was
demonstrated to be present in a sample of the insects by
bioassay with SPF juvenile P. vannamei
( 3 5 ) . In situ
Rev. sci tech. Off. int. Epiz.. 16 (1)
hybridization assays run with histological sections of
T. reticulata, collected from ponds with an ongoing, severe
acute-phase TS epizootic, showed several individuals with
TSV-positive gut contents, but no indication that TSV was
infecting or replicating in the insect. Hence, the available data
suggest that the insect feeds on shrimp which have died from
TS and that the winged adults then transmit the virus from
pond to pond within affected farms or between farms.
Seagulls (laughing gulls, Larus atricilla) have also been shown
to serve as potential vectors of TSV. Gull faeces, collected from
the levees of a TSV-infected pond in Texas during the 1995
epizootic, were found by bioassay with juvenile P. vannamei
to contain infectious TSV ( 2 1 , 3 7 ) . Hence, gulls and other
shrimp-eating seabirds may transmit TSV within affected
farms or to other farms within their flight range. What is not
yet known is how long TSV remains in the gut contents of
gulls or other seabirds and, thus, how important these birds
might be in spreading this disease beyond a given region.
Infectious hypodermal and haematopoietic
necrosis
Diagnosis of infectious h y p o d e r m a l and
h a e m a t o p o i e t i c necrosis virus infections
Traditional methods employing histology and molecular
methods which use non-radioactively labelled gene probes are
the current methods of choice for diagnosis of infection by
IHHNV (Table III) (36, 3 7 , 4 2 ) . Although monoclonal
antibodies (MAbs) have been developed for IHHNV, their use
has been hampered by their cross-reactivity to non-viral
substances in normal shrimp tissue (48). PCR methods have
been developed and successfully applied to the detection of
IHHNV in hemolymph and fresh tissue samples taken from
infected shrimp (36). While not yet available for general use,
PCR methods for IHHNV may provide the greatest sensitivity
for detection of the virus in diseased shrimp and in
asymptomatic carriers.
Histological demonstration of prominent Cowdry type A
inclusion bodies (CAIs) provides a provisional diagnosis of
IHHN. These characteristic inclusion bodies are eosinophilic
(with haematoxylin and eosin [H and E] stains of tissues,
preserved with fixatives that contain acetic acid, such as
Davidson's AFA [acetic acid, formalin, alcohol] and Bouin's
solution), intranuclear inclusion bodies. Such bodies are
found within chromatin-marginated, hypertrophied nuclei of
cells in tissues of ectodermal (epidermis, hypodermal
epithelium of fore and hindgut, nerve cord and nerve ganglia)
and mesodermal origin (haematopoietic organs, antennal
gland, gonads, lymphoid organ and connective tissue) (36).
Intranuclear inclusion bodies due to IHHNV may be easily
confused with developing intranuclear inclusion bodies due
to WSSV. In situ hybridization assay of such sections with a
specific DNA probe to IHHNV provides a definitive diagnosis
of IHHNV infection (36).
151
Rev. sci tech. Off. int. Epiz., 16 (1)
Species and life stages affected
Natural infections by IHHNV have been observed in
P. stylirostris, P. vannamei,
P. ocddentalis,
P. californiensis,
P.monodon,
P. semisulcatus
and P.japonicus.
As other
penaeid species (P. setiferus, P. duorarum and P. aztecus) have
been infected experimentally, natural infections by the virus
probably occur in a number of other penaeid species.
However, species such as P. indicus and P. merguiensis seem
to be refractory to IHHNV ( 3 6 ) . While all life stages of
susceptible host species may be infected by IHHNV, the
juvenile stages are the most severely affected (Table II).
Geographic distribution
The virus of IHHN disease is widely distributed in the shrimp
culture industries of the Americas and has been reported from
virtually every country or region where either P. vannamei or
P. stylirostris is farmed (6, 7, 3 6 ) . IHHNV has been
documented in East and South East Asia (Japan, Singapore,
Malaysia, Indonesia, Thailand, and the Philippines) in slirimp
culture facilities using only captive wild P.japonicus
and
P. monodon broodstock, and where American penaeids had
not been introduced. Except for a single report from the
Philippines, which implicated IHHNV as the cause of a
serious epizootic in P. monodon (49), the virus is increasingly
viewed as a generally insignificant pathogen in Asia ( 2 , 1 6 , 3 6 ,
38). The occurrence of IHHNV in both captive wild
broodstocks and their cultured progeny suggests that East and
South East Asia are within the natural geographic range of the
virus, and that P. monodon and P. japonicus may be among its
natural host species.
In P. stylirostris, IHHNV often causes an acute disease with
very high mortalities in juveniles of the species. Vertically
infected larvae and early PL do not become diseased, but in
juveniles of approximately 3 5 days or older, gross signs of the
disease may be observed, followed by mass mortalities. In
horizontally infected juveniles, the incubation period and
severity of the disease is somewhat size- and/or agedependent, with young juveniles always being the most
severely affected. Infected adults seldom show signs of the
disease or mortalities (36).
IHHN in P. vannamei is typically a chronic disease. Runt
deformity syndrome (RDS) in this species has been linked to
IHHNV infection (30). The severity and prevalence of RDS in
infected populations of juvenile P. vannamei appear to be
related to infection during the larval or early PL stages (7).
Populations of juvenile shrimp with RDS display a relatively
wide distribution of sizes with many smaller than expected
('runted') shrimp. The coefficient of variation (CV = the
standard deviation divided by the mean of different size
groups within a population) for populations with RDS is
typically greater than 3 0 % and may approach 5 0 % , whereas
IHHNV-free (and thus RDS-free) populations of juvenile
P. vannamei usually show CVs of 1 0 % to 3 0 % ( 6 2 ) . Some
members of populations which survive IHHN infections
and/or epizootics apparently carry the virus for life, passing it
onto their progeny and other populations by vertical and
horizontal transmission (36).
White spot syndrome
Diagnosis of white spot syndrome virus infections
The currently available diagnostic and detection methods for
the W S S V complex include reliance on gross signs (i.e.
distinct white
cuticular spots), direct microscopic
examination of wet-mounts, and histological, gene probe,
PCR and bioassay methods (Table III). Wet-mount methods
are applicable in the field and can provide a presumptive
diagnosis of WSS. In experimental infections with American
penaeids, cuticular white spots have not been observed
(D.V. Lightner, unpublished data). Hence, the absence of
grossly visible cuticular white spots does not necessarily rule
out infection by WSSV, and confirmation by more sensitive
methods is required to provide a definitive diagnosis (36).
Stained and unstained wet-mounts, prepared from
WSSV-infected shrimp, can be used in field situations for the
presumptive diagnosis of severe acute WSS. Gills, appendages
or stomach are excised from moribund shrimp suspected of
having WSS, minced and then squashed, dabbed or smeared
onto a slide. The slide is fixed in methanol or by heating, then
stained with an appropriate stain such as Giemsa or other
blood smear stains, and cover-slipped. Alternatively, tissues
fixed for histology can be minced, stained with routine
H and E in depression slides, transferred to standard slides,
cover-slipped, and examined. In such preparations, infected
tissues will display foci of cells with diagnostic hypertrophied
nuclei. These nuclei display marginated chromatin and
amphophilic, eosinophilic to basophilic centres, depending
upon the stain used and upon the stage of development of the
viral inclusion bodies. In severely affected shrimp, such field
diagnostic applications can provide results in less than one
hour, which may be comparable to histological methods (36).
Histological diagnosis of WSS is dependent upon the
demonstration of prominent eosinophilic to pale basophilic
(with H and E stains), Feulgen-positive intranuclear inclusion
bodies in hypertrophied nuclei of (most commonly) the
cuticular epithelial cells and connective tissue cells, and (less
frequently) in the antennal gland, epithelium, lymphoid
organ sheath cells, hemocytes, haematopoietic tissues and in
fixed phagocytes of the heart. Occlusion bodies are absent in
hypertrophied nuclei with WSSV infections. The early stages
of inclusion body development of WSS appear eosinophilic
and centronuclear, and display a halo (an artifact with
Davidson's fixation). These bodies resemble - and are easily
confused with - inclusion bodies due to infection by IHHNV.
However, the two diseases are easily distinguished by the
presence of larger, more fully developed, non-haloed, pale
basophilic inclusion bodies in infected target tissues during
the advanced stages of a WSSV infection. Usually,
Rev. sci tech. Off. int. Epiz., 16 (1)
152
WSSV-infected nuclei contain a single inclusion body but,
occasionally, multiple inclusions occur. Further confirmation
of WSSV infection may be made by TEM demonstration of
WSSV cytopathology in the appropriate target tissue types,
and by the presence of the large rod-shaped to somewhat
elliptical, non-occluded virions of ~ 7 0 to 150 nm x ~ 2 7 5 to
3 8 0 nm in the intranuclear inclusion bodies of affected cells
(12,27, 36, 55, 61).
Molecular detection methods are available for WSSV (Table
III). Non-radioactive DIG-labelled DNA probes for WSSV
complex viruses have been developed in the USA, Taipei
China, Thailand, France and Japan and are commercially
available ( 1 4 , 3 2 , 3 6 ) . WSSV-infected cell nuclei are intensely
marked by a DIG-labelled DNA probe for WSSV with in situ
hybridization assays. Detection of WSSV complex viruses in
penaeid shrimp using PCR has recently been reported by
several research groups ( 3 3 , 4 0 , 4 6 ) . Nunan and lightner (46)
have developed a specific PCR method for WSSV detection
which produces a 7 5 0 bp DNA fragment using arbitrary
primers designed for the penaeid shrimp baculoviruses
Baculovirus
penaei
(BP) and Penaeus
monodon-type
baculoviruses (MBV). Using sequence information from
cloned fragments of white spot syndrome viruses from japan
and Taipei China, Kimura et al. (33) and Lo et al. (40) have
developed highly sensitive methods for PCR detection of the
virus.
Geographic distribution
Following its appearance in 1 9 9 2 to 1 9 9 3 in north-east Asia,
the WSSV complex has spread very rapidly throughout most
of the shrimp-growing regions of Asia and the Indo-Pacific,
presumably with transfers of infected PL or broodstock.
Documented reports of the WSSV epizootics in Asia now
include such countries as Taipei China, the People's Republic
of China, Korea, Thailand, Indonesia, Vietnam, Malaysia,
India and Bangladesh ( 1 0 , 1 2 , 1 3 , 2 5 , 2 6 , 2 7 , 4 0 , 4 4 , 5 7 , 5 8 ,
61).
In the western hemisphere, the first documented case caused
by a WSSV-complex virus appeared in November 1 9 9 5 in
P. setijerus reared in Texas. Following the Texas episode, a
second episode of infection and disease due to WSSV was
documented in crayfish held at the National Zoo in
Washington, DC (36; D. Montali and L. Richman, personal
communication). Shrimp-packing plants located near the
affected farm in Texas may have been the source of the
introduced WSSV because they are major importers and
re-processors of shrimp from affected areas of Asia (36).
Likewise, because captive live crayfish at the National Zoo are
routinely fed frozen shrimp, the source of WSSV may have
been infected frozen shrimp imported from Asia.
Yellow head disease
Diagnosis of yellow head virus infections
Species and life stages affected
The WSSV complex (Appendix, Tables I and II) infects and
causes serious disease in many species of penaeid shrimp and
in a variety of other decapod crustaceans. Among the Asian
penaeids reported to be infected by WSSV complex viruses
are P. monodon,
P. semisulcatus,
P. japonicus,
P. chinensis
(= orientolis), P. penicillatus, P. indicus, P. merguiensis,
Trachypenaeus curvirostris, and Metapenaeus ensis ( 1 0 , 3 6 ,
58). In the American penaeids, natural infections by WSSV
have been documented once, during an outbreak in
November 1995 involving P. setijerus cultured in Texas ( 3 6 ,
53). However, other American penaeids, including the PL and
juvenile stages of P. vannamei,
P. stylirostris, P. setiferus,
P. aztecus and P. duorarum,
have been experimentally
infected by WSSV and shown to suffer significant disease as a
result of infection (36). A particularly disturbing characteristic
of WSSV is its ability to infect other marine and freshwater
decapods (10, 5 8 ; D.V. Lightner, unpublished data). Work
recently conducted in Taipei China indicates that WSSV
infects and causes serious disease in Macrobrachium spp. and
in the North American crayfish, Procambarus clarckii, and
that it can infect, but not cause significant disease in, a variety
of marine crabs and spiny lobsters (10, 5 8 ) . The diagnosis of
natural infections by WSSV in the North American crayfish
Orconectes punctimanus and Procambarus spp. being held at
the US National Zoo confirms that these species are potential
hosts for WSSV (D. Montali and L. Richman, personal
communication).
Methods for the diagnosis of yellow head disease (YHD) in
P. monodon are limited to a combination of clinical signs and
histopathology (Table III) (17, 4 5 ) . A tentative diagnosis of
YHD in P. monodon
is sometimes possible from the
characteristic gross clinical signs (a light yellowish, swollen
cephalothorax) often displayed by juveniles to subadults. This
sign may be limited to P. monodon with acute YHV infections.
Laboratory-reared P. vannamei,
P. stylirostris,
P. setiferus,
P. duorarum and P. aztecus which have been experimentally
infected with YHV do not display cuticular white spots.
Instead, moribund shrimp display a generalised cuticular
pallor (D.V. Lightner, unpublished findings).
While molecular methods using RT-PCR and gene probes
have been reported for the diagnosis and detection of YHV
(18), histopathology remains the most practical diagnostic
method for the disease (Table III). Shrimp with acute YHV
infections display a generalised multifocal to diffuse necrosis,
with prominent nuclear pyknosis and karyorrhexis.
Basophilic, usually spherical, perinuclear cytoplasmic
inclusions occur in affected tissues, especially in hemocytes,
the lymphoid organ, haematopoietic tissues, pillar and
epithelial cells in the gill lamellae, spongy connective tissue
cells in the subcutis, muscle, gut, antennal gland, gonads,
nerve tracts and ganglia, etc. While the general
histopathological presentations of shrimp with Taura
syndrome and yellow head are similar, the diseases can be
easily distinguished by the typically severe necrosis (which is
153
Rev. sci tech. Off. int. Epiz., 16(1)
marked by numerous pyknotic and karyorrhectic nuclei) of
the lymphoid organ in yellow head disease. TSV does not
cause massive necrosis of the lymphoid organ (36).
Diagnosis of YHV infection may be further confirmed by TEM
demonstration
of
non-occluded
enveloped
and
non-enveloped rod-shaped virus particles in perinuclear or
cytoplasmic areas, or within cytoplasmic inclusions of the
target tissues, such as the lymphoid organ and cuticular
epithelial cells of the gills, appendages, or stomach (17, 3 1 ,
41).
Researchers in Thailand have developed a rapid presumptive
field diagnostic method for YHV in acute phase infections
(45). In this method, a hemolymph sample is drawn from the
ventral or cardiac sinuses with a 1-ml syringe, placed on a
glass slide and cover-slipped, and examined directly by phase
contrast microscopy for hemocytes with pyknotic nuclei and
perinuclear inclusion bodies. Alternatively, the hemolymph
sample
can be mixed with
an equivolume of
seawater-formalin as it is drawn into the syringe, then spread
on a clean glass slide and air dried, then stained with a blood
stain (such as Wright's stain) using routine methods.
YHV-infected hemocytes may display nuclear pyknosis,
karyorrhexis, and basophilic perinuclear, cytoplasmic
inclusion bodies (45).
Species and life stages affected
Yellow head virus causes a serious disease in P. monodon in
intensive culture systems in South East Asia and India. The
disease typically occurs in juveniles and subadults, and is
reported in larval or PL stages ( 5 , 1 6 , 1 7 , 3 6 ) .
The brackish water shrimp, Palaemon styliferus and Acetes
spp., which often live in shrimp ponds in Thailand, were
found to carry YHV in bioassays with healthy P. monodon
(17). Although resistant to YHV in ponds, P. merguiensis and
Metapenaeus ensis were found to be able to be experimentally
infected by YHV in laboratory challenge studies (17).
American penaeids were found to be highly susceptible to
experimental infection by YHV. While the PL stages were
refractory to infection, juveniles of P. vannamei, P. stylirostris,
P. setiferus, P. aztecus and P. duorarum were found to be
susceptible to challenge by the virus and to suffer significant
disease (D.V. Lightner, unpublished findings).
Geographic distribution
Yellow head disease seems to be widespread in cultured
stocks of P. monodon in the South East Asian and Indo-Pacific
countries of Thailand, the People's Republic of China,
Malaysia, Indonesia and India ( 1 6 , 1 7 , 1 8 , 3 6 ) . A very similar
virus, LOV, has been reported in P. monodon in Australia (54).
YHV was found in the western hemisphere for the first time in
November 1995, in P. setiferus being reared at a shrimp farm
in Texas. According to farm personnel, the episode was
accompanied by high mortality rates in the affected shrimp
culture ponds. In the affected population of P. setijerus, YHV
occurred in dual infections with WSSV. According to Flegel et
al. ( 1 8 ) , mixed infections of YHV and WSSV are being
observed with increasing frequency in cultured P. monodon in
Thailand and elsewhere in South East Asia. The proximity of
the affected shrimp farm in Texas to major shrimp importing
and re-processing plants suggests that the source of the WSSV
and YHV may have been imported shrimp.
The threat of white spot
syndrome, yellow head and
Taura syndrome to the Americas
In addition to the recognised risks posed by the international
transfer of live penaeid shrimp for aquaculture purposes, the
international trade in frozen shrimp between geographic
regions may also provide a mechanism for the transfer and
introduction of shrimp pathogens. As mentioned earlier in
this review, the USA is a major importer of wild and
farm-raised penaeid shrimp ( 1 5 , 5 3 , 5 6 ) . According to US
Department of Commerce data, imports of penaeid shrimp
have increased markedly in recent years. Since 1 9 6 0 , the
consumption of imported shrimp in the USA has exceeded
landings from its domestic fisheries. Shrimp aquaculture in
the USA constitutes less than 1% of its annual production
(53). By 1 9 9 5 , imports exceeded domestic production by
more than three to one ( 3 5 0 thousand tons imported versus
approximately 100 thousand tons of domestic production)
(56). The largest share of the imported shrimp came from
aquaculture operations in Asia and Latin America (Tables IV
and V) (Fig. 1).
Table IV
Farmed and fished shrimp production (1996) of the major producers in
the world (modified from 53)
Country
Production
(metric tons)
Farmed
shrimp
(%)
Fished
shrimp
(%)
131,000
1
99
Mexico
67,000
18
82
Ecuador
125,000
95
5
Thailand
240,000
67
33
India
290,000
24
76
People's Republic of China
450,000
18
82
Philippines
75,000
34
66
Vietnam
70,000
43
57
240,000
36
64
United States of America
Indonesia
The USA imports thousands of tons of cultured shrimp each
year from countries where WSSV, YHV and TSV are enzootic
and causing serious epizootics ( 1 5 , 18, 3 6 , 3 7 , 5 0 , 5 1 , 5 3 ,
154
Rev. sci tech. Off. int. Epiz., 16(1)
Table V
Shrimp imports (in thousands of metric tons) into the United States of
America from major suppliers for 1990-1996* (56)
20.4
22.9
33.1
22.4
49.2
48.1
51.8
37.3
53.9
66.8
80.8
77.8
55.1
17.5
17.7
19.1
22.6
17.7
16.4
35.1
49.4
31.0
22.9
14.6
6.7
16.6
13.7
54.7
45.5
14.2
57.4
16.8
Ecuador
38.3
Thailand
25.4
India
People's Republic
of China
Indonesia
1996*
48.8
Mexico
Philippines
1995
1993
1990
Vietnam
1994
1992
Country
1991
4.7
6.4
4.4
2.7
2.7
2.1
1.0
N/A
N/A
N/A
N/A
0.6
1.3
2.1
8.6
11.5
13.7
13.3
11.0
5.3
7.6
* Data for 1996 not complete
N/A: not applicable
56). WSSV and YHV have caused serious disease epizootics
throughout most of the shrimp-growing regions of Asia, and
TSV has swept through the shrimp-farming countries of the
Americas ( 9 , 1 8 , 3 6 ) .
Since 1 9 9 4 , WSSV and YHV have been the cause of serious
epizootics in Thailand and India ( 1 8 , 3 6 , 5 3 ) . According to
US Department of Commerce statistics ( 5 6 ) , these two
countries rank first and second, respectively, as suppliers of
shrimp to the US import market from Asia, and first and
fourth when all imported shrimp are considered (Table V)
(Fig. 1). W h e n epizootics, due to these viruses, develop,
emergency harvests are commonly employed in Asia to
salvage marketable shrimp crops (17, 2 9 ) . P. monodon
displaying gross signs of WSSV infection (i.e. cuticular white
spots and reddish pigmentation) was found in retail outlets in
the USA in 1 9 9 5 and 1996. PCR assays of samples from these
shrimp confirmed the presence of WSSV (L.M. Nunan,
unpublished
findings). Bioassay of one sample of
WSSV-positive (by PCR) P. monodon, using P. stylirostris as
the indicator for infectious virus, showed that the sample was
co-infected with WSSV and YHV (L.M. Nunan
D.V. Lightner, unpublished findings).
and
Imported commodity shrimp are distributed throughout the
USA,
and some imported shrimp are reprocessed at
shrimp-packing plants situated on coastal bays and estuaries
where native penaeid nursery grounds also occur. With
infectious WSSV, YHV and TSV present, and perhaps fairly
common, in imported commodity shrimp, the risk of
accidental contamination of wild or cultured stocks of
penaeid shrimp may be significant. The occurrence of
co-infections of WSSV and YHV in cultured P. setiferus in
Texas in November 1 9 9 5 and the occurrence of WSSV in
crayfish at the US National Zoo document that such
introductions can and do occur. Mechanisms for transfer of
exotic viruses such as WSSV, YHV, IHHNV and TSV in
imported, frozen commodity shrimp from importer locations
and distribution channels to shrimp aquaculture facilities or
to wild crustaceans and shrimp may be common in the USA.
Those mechanisms may include such practices as the
following:
- reprocessing of imported shrimp at processing plants
located in fishing ports and the release of untreated liquid and
solid wastes from these plants into coastal waters
- the disposal of solid waste (heads, shells, etc.) in land fills
where seagulls and other shrimp-eating birds consume
virus-infected tissues and then transport the virus to (and
contaminate) shrimp farms or coastal estuaries through their
faeces
- the use of imported shrimp as bait by sports fishermen in
coastal waters
- the use of imported shrimp as a 'fresh food' for the
maintenance of other aquatic species (i.e. as was practised at
the National Zoo with freshwater crayfish, which became
infected with WSSV).
As a result of the very high susceptibility of American
penaeids to WSSV and YHV, the introduction and
establishment of either or both of these pathogens could cause
very serious disease epizootics and economic hardships to the
shrimp-farming industries of the Americas and, perhaps, to its
commercial fisheries.
Acknowledgements
Fig. 1
United States imports of shrimp for 1990-1995 from countries which are
both major producers of farmed shrimp and in which white spot
syndrome virus, yellow head virus or Taura syndrome virus are
enzootic
Much of the original research summarised in this paper was
supported by funds from the Gulf Coast Research Laboratory
Consortium Marine Shrimp Farming Program, Cooperative
State Research, Education and Extension Service (CSREES),
US
Department
of Agriculture under
Grant No.
9 5 - 3 8 8 0 8 - 1 4 2 4 ; the National Sea Grant Program, US
Department of Commerce under Grant No. NA56RG0617;
the US Department of Commerce, National Oceanic and
Atmospheric Administration (NOAA), Saltonstall-Kennedy
Program under Grant No. NA56FD0621 and a grant from the
National Fishery Institute.
a
155
Rev. sci tech. Off. int. Epiz., 16 (1)
Risque de dissémination des virus des crevettes pénéidés dans les
Amériques, lié aux transferts internationaux de crevettes vivantes
et surgelées
D.V. Lightner, R.M. Redman, B.T. Poulos, L.M. Nunan, J.L. Mari &
K.W. Hasson
Résumé
Les maladies virales qui affectent depuis une dizaine d'années les crevettes
d'élevage freinent considérablement la réussite de ce secteur dans nombre de
pays pratiquant cet élevage. En Occident, les virus du syndrome de Taura et de la
nécrose hypodermique et hématopoïétique infectieuse ont gravement affecté les
élevages des côtes américaines et de Hawaï, alors qu'en Asie, les virus du
syndrome des taches blanches et de la maladie de la tête jaune ont provoqué des
pandémies dont l'impact économique est considérable.
Les transferts internationaux de crevettes vivantes pour les besoins de
l'aquaculture sont, à l'évidence, à l'origine de la propagation des virus au sein
d'une même région, ou d'une région à l'autre. Les mouettes qui se nourrissent de
crevettes, ainsi que d'autres oiseaux de mer et insectes aquatiques peuvent
également jouer un rôle dans la dissémination de ces virus.
Les crevettes surgelées peuvent contenir des virus exotiques pour les pays
importateurs et constituent donc un autre facteur important de dissémination.
C'est ainsi que les virus du syndrome des taches blanches, de la maladie de la
tête jaune et du syndrome de Taura isolés aux États-Unis d'Amérique à partir de
crevettes surgelées importées conservaient leur pouvoir pathogène. Les
mécanismes qui permettent aux virus présents dans les produits surgelés
d'importation de se propager parmi les élevages de crevettes ou les populations
sauvages du pays importateur sont les suivants :
- le rejet, directement dans les eaux côtières et sans traitement préalable, des
déchets solides et liquides par les usines qui importent et conditionnent les
crevettes ;
- le dépôt, par ces usines, de leurs déchets solides en décharges ouvertes
accessibles aux mouettes et autres oiseaux de mer ;
- l'utilisation de crevettes importées comme appât par les pêcheurs sportifs.
Mots-clés
Amériques - Aquaculture - Crevettes pénéidés - Diagnostic - Maladie de la tête jaune Maladies virales - Nécrose hypodermique et hématopoïétique infectieuse - Syndrome
des taches blanches - Syndrome de Taura.
156
Rev. sci tech. Off. int. Epiz., 16(1)
Riesgo de propagación de virus de los camarones peneidos en el
continente americano a resultas de los intercambios
internacionales de camarones vivos o congelados
D.V. Lightner, R.M Redman, BT. Poulos, L.M. Nunan, J.L Mari &
K.W. Hasson
Resumen
En el curso del último decenio, las enfermedades víricas se han erigido, para
muchos de los países del mundo productores de camarones, en un serio
obstáculo para el desarrollo de este sector económico. En el hemisferio
occidental, los virus del síndrome de Taura y de la necrosis hipodérmica y
hematopoyética infecciosa han provocado graves epizootias en las regiones
productoras de camarones de Hawai y de las Américas. En Asia, por otra parte,
los virus del síndrome de la mancha blanca y de la enfermedad de la cabeza
amarilla han dado origen a pandemias que se han saldado con pérdidas
catastróficas.
Los intercambios internacionales de camarones vivos con fines de acuicultura
son el más obvio mecanismo por el que los virus se han propagado en una región
o entre las regiones en las que tales casos se han producido. Las gaviotas que se
alimentan de camarones, así como otras aves marinas e insectos acuáticos,
pueden constituir también factores de dispersión de los virus del camarón ya sea
entre regiones diferentes o en el seno de una misma región.
Otro mecanismo susceptible de favorecer la propagación internacional de estos
patógenos es el comercio de camarones congelados, que pueden albergar virus
exóticos para los países de importación.
Los virus del síndrome de la mancha blanca, de la enfermedad de la cabeza
amarilla y del síndrome de Taura han sido detectados a partir de camarones
congelados importados al mercado estadounidense, y su infectividad ha sido
demostrada. Han podido identificarse algunos de los mecanismos por los cuales
estos virus se transmiten, a través de los productos congelados, a las
poblaciones autóctonas -salvajes o de c r í a - de camarones peneidos. Entre
dichos mecanismos se encuentran los siguientes:
- la liberación directa en aguas costeras de residuos líquidos o sólidos no
tratados procedentes de instalaciones de importación o procesado de
camarones;
- el vertido inadecuado de los residuos sólidos de estas fábricas en vertederos, y
el subsiguiente acceso a los mismos de las gaviotas u otras aves marinas;
- la utilización de camarones importados como cebo por parte de pescadores
aficionados.
Palabras clave
Acuicultura - Américas - Camarón peneido - Diagnóstico - Enfermedad de la cabeza
amarilla - Enfermedades virales - Necrosis hipodérmica y hematopoyética infecciosa Síndrome de la mancha blanca - Síndrome de Taura.
•
157
Rev. sci tech. Off. int. Epiz., 16 (1)
Appendix
Viruses of penaeid shrimp
(as of December 1996; modified from 36, except where
noted)
Deoxyribonucleic acid (DNA) viruses
Ribonucleic acid (RNA) viruses
Parvoviruses
Picornavirus
Infectious hypodermal and haematopoietic necrosis virus
(IHHNV)
Reoviruses
Hepatopancreatic parvovirus (HPV)
Reo-like virus type III (REO III)
Lymphoidal parvo-like virus (LPV)
Reo-like virus type IV (REO IV)
Spawner-isolated mortality virus (SMV) ( 2 0 )
Baculoviruses
Taura syndrome virus (TSV)
Toga-like
and baculo-Uke viruses
Baculovirus
penaei-type
viruses (PvSNPV-type sp.)
(BP-type):
- BP strains from the Gulf of Mexico, Hawaii and the
Eastern Pacific
Penaeus monodon-type baculoviruses (PmSNPV-type sp.)
(MBV-type):
- MBV strains from East and South East Asia,
Australia, the Indo-Pacific and India
Baculoviral mid-gut
gland
necrosis-type
(BMN-type):
- BMN from P. japonicus in Japan
- Type C baculovirus of P. monodon
White spot syndrome
(PmNOBII-type):
virus
Lymphoid organ vacuolization virus ( L O W )
Rhabdoviruses
and single-stranded
RNA viruses
Yellow head virus of P. monodon in South East Asia
and Indo-Pacific (YHV/'YHB')
Lymphoid organ virus of P. monodon in Australia
(LOV)
Rhabdovirus of penaeid shrimp (RPS)
viruses
(TCBV)
baculoviruses
(WSSV-type)
-
Systemic ectodermal and mesodermal baculo-like
virus (SEMBV)
-
Rod-shaped virus of P. japonicus
Penaeid acute viremia (PAV)
(RV-PJ)
- Hypodermal
and
haematopoietic
necrosis
baculo-like virus (HHNBV), agent of shrimp
explosive epidemic disease (SEED)
- White spot baculovirus (WSBV)
Hemocyte-infecting
non-occluded
baculo-like
virus
(PHRV)
Iridovirus
Shrimp iridovirus (IRDO)
References
1, Adams J.R. & Bonami J.R. (eds) (1991). - Atlas of
invertebrate viruses. CRC Press, Boca Raton, Florida, 684 pp.
2. Baticados M.C.L., Cruz-Lacíerda E.R., de la Cruz M.C.,
Duremdez-Femandez R.C, Gacutan R.Q., Lavilla-Pitogo C.R.
& Lio-Po G.D. (1990). - Diseases of penaeid shrimps in the
Philippines. Aquaculture Extension Manual No. 16.
Aquaculture Department, South East Asian Fisheries
Development Center (SEAFDEC), Tigbauan, Iloilo,
Philippines, 46 pp.
158
3. Bonami J.R., Brehelin M., Mari J . , Trumper B. &
Lightner D.V. (1990). - Purification and characterization of
IHHN virus of penaeid shrimps. J . gen. Virol., 71, 2657-2664.
4. Bonami J.R., Hasson K.W., Mari J . , Poulos B.T. &
Lightner D.V. (1997). - Taura syndrome of marine penaeid
shrimp: characterization of the viral agent. J. gen. Virol., 78,
313-319.
5. Boonyaratpalin S., .Supamattaya K., Kasornchandra J . ,
Direkbusaracom S., Ekpanithanpong U. & Chantanachooklin
C. (1993). - Non-occluded baculo-like virus, the causative
agent of yellow head disease in the black tiger shrimp
(Penaens monodon). Gyobyo Kenkyu (Fish Pathol) 28 (3),
103-109.
6. Brock J.A. & Lightner D.V. (1990). - Diseases of crustacea:
diseases caused by microorganisms. In Diseases of marine
animals, Vol. III (O. Kinne, ed.). Biologische Anstalt
Helgoland, Hamburg, 245-349.
7. Brock J.A. & Main K. (1994). - A guide to the common
problems and diseases of cultured Penaeus vannamei. Oceanic
Institute, Makapuu Point, Honolulu, 241 pp.
8. Brock J.A., Gose R., Lightner D.V. & Hasson K.W. (1995). An
overview on Taura syndrome, an important disease of farmed
Penaeus vannamei. In Swimming through troubled water
(C.L. Browdy & J.S. Hopkins, eds). Proc. special session on
shrimp farming, Aquaculture '95. World Aquaculture
Society, Baton Rouge, Louisiana, 84-94.
Rev. sci tech. Off. int. Epiz., 16(1)
15. Filose J . (1995). - Factors affecting the processing and
marketing of farmed raised shrimp. In Swimming through
troubled water (C.L. Browdy & J.S. Hopkins, eds). Proc.
special session on shrimp farming, Aquaculture '95. World
Aquaculture Society, Baton Rouge, Louisiana, 227-234.
16. Flegel T.W., Fegan D.F. & Sriurairatana S. (1995). Environmental control of infectious diseases in Thailand. In
Diseases in Asian aquaculture, Vol. II (M. Shariff, J.R. Arthur
& R.P. Subasinghe, eds). Proc. second symposium on
diseases in Asian aquaculture. Phuket, Thailand, 25-29
October 1993. Fish Health Section, Asian Fisheries Society,
Manila, 65-79.
17. Flegel T.W., Sriurairatana S., Wongteerasupaya C ,
Boonsaeng V., Panyim S. & Withyachurrmamkul B. (1995). Progress in characterization and control of yellow-head virus
of Penaeus monodon. In Swimming through troubled water
(C.L. Browdy & J.S. Hopkins, eds). Proc. special session on
shrimp farming, Aquaculture '95. World Aquaculture
Society, Baton Rouge, Louisiana, 76-83.
18. Flegel T.W., Boonyaratpalin S. & Withyachumnamkul B.
(1996). - Current status of research on yellow-head virus and
white-spot virus in Thailand. In World aquaculture '96. Book
of abstracts. World Aquaculture Society, Baton Rouge,
Louisiana, 126-127.
19. Francki R.I.B., Fauquet C.M., Knudson D.L. & Brown F.
(eds). (1991). - Classification and nomenclature of viruses:
Fifth report of the International Committee on Taxonomy of
Viruses. Springer Verlag, Vienna & New York. Arch. Virol.,
Suppl. 2, 450 pp.
9. Brock JA., Gose R.B., Lightner D.V. & Hasson K. (1997). Recent developments and an overview of Taura Syndrome of
farmed shrimp in the Americas. In Diseases in Asian
aquaculture, Vol. III. Proc. aquatic animal health sections,
Asian Fish Health Section/World Aquaculture Society '96
meeting. Bangkok, 29 January-2 February 1996 (in press).
20. Fraser C.A. & Owens L. (1996). - Spawner-isolated mortality
virus from Australian Penaeus monodon. Dis. aquat. Organisms,
27, 141-148.
10. Chang P.S., Lo C.F., Wang Y.C. & Kou G.H. (1997). Detection of white spot syndrome associated virus (WSSV) in
experimentally infected wild shrimp, crabs and lobsters by in
situ hybridization. Aquaculture (in press).
21. Garza J.R., Hasson K.W., Poulos B.T., Redman R.M., White
B.L. & Lightner D.V. (1997). - Demonstration of infectious
Taura syndrome virus in the feces of sea gulls collected during
an epizootic in Texas. J. aquat. Anim. Health (in press).
11. Chantanachookin C , Boonyaratpalin S., Kasornchandra J . ,
Direkbusarakom S., Ekpanithanpong U., Supamataya K.,
Sriurairatana S. & Flegel T.W. (1993). - Histology and
ultrastructure reveal a new granulosis-like virus in Penaeus
monodon affected by yellow head disease. Dis. aquat.
Organisms, 17 (2), 145-157.
22. Hasson K.W., Lightner D.V., Poulos B.T., Redman R.M.,
White B.L., Brock J.A. & Bonami J.R. (1995). - Taura
syndrome in Penaeus vannamei: demonstration of a viral
etiology. Dis. aquat. Organisms, 2 3 , 115-126.
12. Chen S.N. (1995). - Current status of shrimp aquaculture in
Taiwan. In Swimming through troubled water (C.L. Browdy
& J.S. Hopkins, eds). Proc. special session on shrimp farming,
Aquaculture '95. World Aquaculture Society, Baton Rouge,
Louisiana, 29-34.
13. Chou H.Y., Huang C.Y., Wang C.H., Chiang H.C & Lo C F .
(1995). - Pathogenicity of a baculovirus infection causing
white spot syndrome in cultured penaeid shrimp in Taiwan.
Dis. aquat. Organisms, 2 3 , 165-173.
14. Durand S., Lightner D.V., Nunan L.M., Redman R.M., Mari J .
& Bonami J.R. (1996). - Application of gene probes as
diagnostic tool for the white spot baculovirus (WSSV) of
penaeid shrimps. Dis. aquat. Organisms, 27, 59-66.
23. Hasson K.W., Lightner D.V., Mari J . , Bonami J.R., Poulos
B.T., Mohney L.L., Redman R.M. & Brock J.A. (1997). - The
geographic distribution of Taura syndrome virus in the
Americas: determination by histopathology and in situ
hybridization using TSV-specific cDNA probes. In Proc. IVth
Symposium on aquaculture in Central America, focusing on
shrimp and tilapia (D.E. Alston, B.W. Green & H.C. Clifford,
eds). Tegucigalpa, Honduras, 22-24 April. Asociación
Nacional de Acuicultores de Honduras/Latin American
Chapter of the World Aquaculture Society, 154-156.
24. Hasson K.W., Hasson J., Aubert H., Redman R.M. & Lightner
D.V. (1997). - A new RNA-friendly fixative for the
preservation of penaeid shrimp samples for virological assays
using cDNA probes. J. virol. Meth. (submitted for
publication).
Rev. sci tech. Off. int. Epiz, 16 (1)
25. Huang J., Song X.L., Yu J. & Yang C.H. (1995). - Baculoviral
hypodermal and hematopoietic necrosis: study on the
pathogen and pathology of the explosive epidemic disease of
shrimp. Marine Fish. Res., 16 (1), 1-10.
26. Inouye K., Miwa S., Oseko N., Nakano H., Kimura T.,
Momoyama K. & Hiraoka M. (1994). - Mass mortalities of
cultured kuruma shrimp Penaeus japonicus in Japan in 1993:
electron microscopic evidence of the causative virus. Gyobyo
Kenkyu (Fish Pathol), 29, 149-158.
27. Inouye K., Yamano K., Ikeda N., Kimura T., Nakano H.,
Momoyama K , .Kobayashi J . & Miyajima S. (1996). - The
penaeid rod-shaped DNA virus (PRDV), which causes
penaeid acute viremia (PAV). Gyobyo Kenkyu (Fish Pathol.),
31, 39-45.
28. Jimenez R. (1992). - Síndrome de Taura (resumen).
Acuacultura del Ecuador. Rev. Especial Cámara Nac. Acuacult.,
1, 1-16.
29. Jory D.E. (1996). - Marine shrimp farming in the kingdom of
Thailand: Part II Aquaculture, 22 (4), 71-78.
30. Kalagayan G., Godin D., Kanna R., Hagino R., Sweeney J . ,
Wyban J . & Brock J . (1991). - IHHN virus as an etiological
factor in runt-deformity syndrome of juvenile Penaeus
vannamei cultured in Hawaii. J. Wld aquacult. Soc, 22,
235-243.
31. Kasomchandra J . , Boonyaratpalin S. & Supamattaya K.
(1995). - Electron microscopic observations on the
replication of yellow-head baculovirus in the lymphoid organ
of Penaeus monodon. In Diseases in Asian aquaculture, Vol. I
(M. Shariff, J.R. Arthur & R.P. Subasinghe, eds). Fish Health
Section, Asian Fisheries Society, Manila, 99-106.
32. Kasomchandra J. & Boonyaratpalin S. (1996). - Red disease
with white patches or white spot disease in cultured penaeid
shrimp in Asia. Asian Shrimp News, 273 (3), 4.
33. Kimura T., Yamano K., Nakano H., .Momoyama K., Hiraoka
M. & Inouye K. (1996). - Detection of penaeid rod-shaped
DNA virus (PRDV) by PCR. Gyobyo Kenkyu (Fish Pathol), 3 1 ,
93-98.
34. Laramore R. (1995). - Taura syndrome: before Ecuador.
Research notes from Shrimp Culture Technologies, Inc., Fort
Pierce, Florida. No. 2, 1-3.
35. Lightner D.V. (1995). - Taura syndrome: an economically
important viral disease impacting the shrimp farming
industries of the Americas including the United States. In
Proc. Ninety-ninth annual meeting U.S. Animal Health
Association (USAHA). Reno, Nevada, 28 October-3
November. USAHA, Richmond, Virginia, 36-52.
36. Lightner D.V. (1996). - A handbook of shrimp pathology and
diagnostic procedures for diseases of cultured penaeid
shrimp. World Aquaculture Society, Baton Rouge, Louisiana,
304 pp.
37. Lightner D.V. (1996). - Epizootiology, distribution and the
impact on international trade of two penaeid shrimp viruses
in the Americas. In Preventing the spread of aquatic animal
diseases (B.J. Hill & T. Hästein, eds). Rev. sci. tech. Off. int.
Epiz., 15 (2), 579-601.
159
38. Lightner D.V., Bell T.A., Redman R.M., Mohney L.L.,
Natividad J.M., Rukyani A. & Poemomo A. (1992). - A
review of some major diseases of economic significance in
penaeid prawns/shrimps of the Americas and Indo-Pacific. In
Diseases in Asian aquaculture, Vol. I (M. Shariff, R.
Subasinghe & J.R. Arthur, eds). Fish Health Section, Asian
Fisheries Society, Manila, 57-80.
39. Lightner D.V., Redman R.M., Hasson K.W. & Pantoja C.R.
(1995). - Taura syndrome in Penaeus
vannamei:
histopathology and ultrastructure. Dis. aquat. Organisms, 2 1 ,
53-59.
40. Lo C.F., Leu J.H., Chen C.H., Peng S.E., Chen Y.T.,
Chou C.M., Yeh P.Y., Huang C.J., Chou H.Y., Wang CH. &
Kou G.H. (1996). - Detection of baculovirus associated with
white spot syndrome (WSBV) in penaeid shrimps using
polymerase chain reaction. Dis. aquat. Organisms, 2 5 ,
133-141.
41. Lu Y., Tapay L.M., Loh P.C. & Brock J.A. (1995). - Infection
of the yellow head baculo-like virus in two species of penaeid
shrimp, P. stylirostris and P. vannamei. J. Fish Dis., 17,
649-656.
42. Mari J . , Bonami J.R. & Lightner D.V. (1993). - Partial cloning
of the genome of infectious hypodermal and haematopoietic
necrosis virus, an unusual parvovirus pathogenic for penaeid
shrimps; diagnosis of the disease using a specific probe. J. gen.
Virol, 74, 2637-2643.
43. Murphy F.A., Fauquet C.M., Mayo M.A., Jarvis A.W.,
Ghabrial S.A., Summers M.D., Martelli G.P. & Bishop D.H.L.
(1995). - The classification and nomenclature of viruses.
Springer Verlag, Vienna & New York. Arch. Virol, Suppl. 2,
586 pp.
44. Nakano H., Koube H., Umezawa S., Momoyama K., Hiraoka
M., Inouye K. & Oseko N. (1994). - Mass mortalities of
cultured kuruma shrimp, P. japonicus, in Japan in 1993:
epizootiological survey and infection trials. Gyobyo Kenkyu
(Fish Pathol), 29, 135-139.
45. Nash G., Akarajamorn A. & Withyachumnamkul B. (1995). Histological and rapid haemocytic diagnosis of yellow-head
disease in Penaeus monodon. In Diseases in Asian aquaculture,
Vol. I (M. Shariff, J.R. Arthur & R.P. Subasinghe, eds). Fish
Health Section, Asian Fisheries Society, Manila, 89-98.
46. Nunan L.M. & Lightner D.V. (1997). - Development of a
non-radioactive gene probe by PCR for detection of white
spot syndrome virus (WSSV). J. virol. Meth., 63, 193-201.
47. Overstreet R.M., Lightner D.V., Hasson K.W., McIlwain S. &
Lotz J . (1997). - Susceptibility to TSV of some penaeid
shrimp native to the Gulf of Mexico and southeast Atlantic
Ocean.J. Invertebr. Pathol, 69, 165-176.
48. Poulos B.T., Lightner D.V., Trumper B. & Bonami J.R.
(1994). - Monoclonal antibodies to the penaeid shrimp
parvovirus, infectious hypodermal and hematopoietic
necrosis vims (IHHNV). J. aquat. Anim. Health, 6, 149-154.
49. Rosenberry B. (1992). - IHHN virus hits Philippines. In
World shrimp farming, 1992. Aquaculture Digest, San Diego,
California, 6-7.
160
50. Rosenberry B. (1993). - Taura syndrome hits farms in
Ecuador - again. Shrimp News International, 18 (3), 6.
51. Rosenberry B. (1994). - Update on Taura syndrome in
Ecuador. Shrimp News International, 19 (3), 2-4.
52. Rosenberry B. (ed.) (1994). - World shrimp farming, 1994.
Aquaculture Digest, San Diego, California, 68 pp.
53. Rosenberry B. (ed.) (1996). - World shrimp farming, 1996.
Aquaculture Digest, San Diego, California, 164 pp.
54. Spann K.M., Vickers J.E. & Lester R.J.G. (1995). - Lymphoid
organ virus of Penaeus monodon. Dis. aquat. Organisms, 26,
127-134.
55. Takahashi Y., Itami T., .Kondo M., Maeda M., Fujii R.,
Tomonaga S., Supamattaya K. & Boonyaratpalin S. (1994). Electron microscopic evidence of bacilliform virus infection
in kuruma shrimp (Penaeus japonicus). Gyobyo Kenkyu (Fish
Pathol), 2 9 , 1 2 1 - 1 2 5 .
56. United States Department of Commerce (USDC) (1996). Shrimp imports. US Department of Commerce, Bureau of the
Census, Foreign Trade Division, Washington, DC. http://
remora.ssp.nmfs.gov/FTPUBLIC/owa/mrfss.FT_IMPORTS.
RESULTS.
57. Wang C.H., Lo C.F., Leu J.H., Chou C.M., Yeh P.Y.,
Chou H.Y., Tung M.C, Chang C.F., Su M.S. & Kou G.H.
(1995). - Purification and genomic analysis of baculovirus
associated with white spot syndrome (WSBV) of Penaeus
monodon. Dis. aquat. Organisms, 23, 239-242.
Rev. sci tech. Off. int Epiz.,16(1)
58. Wang Y.C., Lo C.F., Chang P.S. & Kou G.H. (1997).-White
spot syndrome associated virus (WSSV) infection in cultured
and wild decapods in Taiwan. Aquaculture (in press).
59. 'Weidner D. & Rosenberry B. (1992). - World shrimp
fanning. In Proc. special session on shrimp fanning
(J. Wyban, ed.). World Aquaculture Society, Baton Rouge,
Louisiana, 1-21.
60. Wigglesworth J . (1994). - 'Taura syndrome' hits Ecuador
farms. Fish Farmer, 17 (3), 30-31.
61. Wongteerasupaya C , Vickers J.E., Sriurairatana S.,
Nash G.L., Akarajamorn A., Boonsaeng V., Panyim S.,
Tassanakajon A., Withyachumnamkul B. & Flegel T.W.
(1995). - A non-occluded, systemic baculovirus that occurs
in cells of ectodermal and mesodermal origin and causes high
mortality in the black tiger prawn, Penaeus monodon. Dis.
aquat. Organisms, 21 (1), 69-77.
62. Wyban J.A., Swingle J.S., Sweeney J.N. & Pruder G.D.
(1992). - Development and commercial performance of high
health shrimp using specific pathogen free (SPF) broodstock
Penaeus vannamei. In Proc. special session on shrimp farming
(J. Wyban, ed.). World Aquaculture Society, Baton Rouge,
Louisiana, 254-260.