Clinical review

Infectious pancreatic necrosis in Atlantic salmon,

Salmo salar L.
R J Roberts
1
and M D Pearson
2
1 University of Idaho, Hagerman Fish Culture Experiment Station, Hagerman, ID, USA
2 Landcatch Natural Selection, Cooperage Way, Alloa, UK
Abstract
A clinical and histopathological review was carried
out of 21 outbreaks of acute infectious pancreatic
necrosis (IPN) in Scottish Atlantic salmon, Salmo
salar L., farms (13 marine and eight fresh water)
during 19912004. A distinctive syndrome was
evident in both post-smolts in sea water and fry in
fresh water, where liver lesions, which had not pre-
viously been associated with IPN, became a consis-
tent nding in addition to the more typical
pancreatic and intestinal changes. Initial cases were
described in post-smolts in Shetland, but by the end
of the period of investigation this type of pathology
had extended down the West coast of Scotland and
into Ireland. Limited viral strain analysis suggested
that similar strains were involved in both fresh water
and sea water and that these differed from earlier
isolates from rainbow trout, Oncorhynchus mykiss
(Walbaum). In fresh water, recovered sh frequently
developed a greatly distended intestine associated
with accumulation of undigested food. In sea water,
after the initial, often signicant (50% or more),
losses, there were many sh which failed to grow and
became chronically emaciated and prone to sea louse
infection. Although use of transfer diets containing
immune enhancers and the selection of IPN resist-
ant broodstock has reduced losses the disease re-
mains a serious cause of economic loss.
Keywords: Atlantic salmon, clinical signs, histo-
pathology, infectious pancreatic necrosis, liver
lesions, Scotland.
Introduction
Infectious pancreatic necrosis (IPN) is a serious
disease of salmonid and a number of other sh
species. It is caused by an archetypal birnavirus a
distinctive, small, non-membraned double-stranded
RNA virus (IPNV). The disease has been a
major concern in brook trout, Salvelinus fontinalis
(Mitchill), and rainbow trout, Oncorhynchus mykiss
(Walbaum), hatcheries, initially in North America,
since early in the 20th century (MGonigle 1940;
McAllister & Bebak 1997) and subsequently in
Europe (Dorson & Torchy 1981). It remains a
signicant cause of high mortality (70%) in rst
feeding fry and ngerlings of most salmonids and,
as it can be vertically transmitted via the egg,
broodstock carrier sh are an important facet of its
pathogenesis (Wolf, Quimby & Bradford 1963;
Reno 1999).
Although some of the earliest descriptions of the
disease related to losses of Atlantic salmon, Salmo
salar L., fry (MGonigle 1940; McKelvie & Artsob
1969), it is only in the past 20 years, as Atlantic
salmon culture has dramatically expanded as a
mariculture technology, that its signicance in the
marine environment has come to be appreciated
(Christie, Havarstein, Djupvik, Ness & Endreisen
1988; Krogsrud, Hastein & Ronningen 1989;
Smail, Bruno, Dear, McFarlane & Ross 1992). It
is now recognized to be the most important disease
Journal of Fish Diseases 2005, 28, 383390
Correspondence Ronald J Roberts, University of Idaho,
Hagerman Laboratory, 3059F Fish Hatchery Road, Hagerman,
ID 83332, USA
(e-mail: heronpisces@btinternet.com)
383
2005
Blackwell Publishing Ltd
in its impact on salmon production in the European
Union and in Norway (Ariel & Olesen 2002;
Murray, Busby & Bruno 2003).
In many salmon producing countries, because of
the risk of major losses in rst-feeding fry infected
from the parent via vertical transmission through
the egg, broodstock are routinely tested for the
presence of cultivable virus from the kidney or
gonadal uids (OIE 2000). Eggs are also routinely
disinfected with buffered iodophore disinfectants at
the same time, but any eggs from parents that
subsequently test positive on tissue culture are
destroyed, as there are considerable doubts as to the
efcacy of iodophore disinfection (Bullock, Rucker,
Amend, Wolf & Stuckey 1976). Atlantic salmon
hatcheries are also, where possible, maintained on
IPNV-free fresh water. Smolt stocks in fresh water
may also be tested by tissue culture annually to
conrm the overall disease status of the producing
farm. Until 2005 only certied IPNV-free stocks of
salmon smolts could be stocked in any sea sites in
Scotland where the condition had not been
recorded, but this regulation no longer applies.
Norway is currently the largest Atlantic salmon
producer and losses there from IPN in 1997 were
estimated at some $US 30M (Christie 1997).
Movement controls do form part of the national
production system but it was here, from the mid-
1980s that outbreaks of acute IPN in marine post-
smolts began to occur for the rst time. These were
generally associated with a specic N subtype of
the main Sp serotype of the virus and have become
increasingly common (Christie, Ness & Djupvik
1990; Melby & Christie 1994). From 1989, similar
losses began to occur in the Shetland Isles, again
generally associated with a specic serotype which
Smail et al. (1992) suggested was a subtype muta-
tion of an Sp strain which they designated the Sh
subtype (Smail, McFarlane, Bruno & McVicar
1995). It is possible, although there is currently no
evidence other than the general clinical and
epidemiological pictures, that the two subtypes are
similar. However, Pryde, Melvin & Munro (1993)
demonstrated that the VP2 protein of the Sp(A2)
strain and the Shetland Sh subtype differed so little
as to suggest that the latter was in fact an Sp(A2)
strain.
More recently the signicance of the different
structural and other proteins, in what is a relatively
small virus, on its pathogenicity, have begun to be
appreciated. As yet their role has not been
elucidated, although in the very similar avibirna-
virus, infectious bursal disease virus, specic
determinants of pathogenicity have been deter-
mined in the amino acid patterns of the structural
proteins (Islam, Zierenberg & Muller 2001). It is
likely that similar determinants exist in the
pathogenic IPN viruses (Sano, Okamoto, Fukuda,
Saneyoshi & Sano 1992; Bruslind & Reno 2000).
Over the past decade, following on the earlier
report of Smail et al. (1992), annual losses from
acute IPN in the months immediately following
smolt transfer have increased such that virtually all
waters in Shetland are considered infected. The
occurrence of these very specic post-transfer
disease outbreaks, usually starting at 712 weeks
after transfer and lasting for up to 3 months, has
extended down the coast of Scotland, reaching the
most southerly farms by 2001 and extending into
Ireland in 2002.
Use of specic post-transfer diets, better transfer
systems and in particular the development of
genetically resistant sh, such as the Landcatch
IPN resistance enhanced strain, have signicantly
reduced the overall losses, but the problems posed
by the disease are still considerable, both in terms of
hatchery and post-smolt mortalities and also the
high costs of individual broodstock testing.
The purpose of the present paper is to review the
distinctive clinical and pathological features associ-
ated with the progress of this serious disease in
Scotland as it has extended its range over the past
decade. The clinical and histopathological material
for the review was made available to us in
condence over the 13 years from 1991 to 2004.
Cases reviewed came from 21 different outbreaks
(13 marine; eight fresh water) in Shetland and the
Scottish mainland, involving sh originating from a
number of different smolt production farms. In all
cases the aetiology was conrmed by virus isolation
from the outbreak. Genotyping of a very limited
number of isolates, from marine and fresh water,
revealed that at the molecular level similar Sp strains
were involved in each case (C. Cunningham, 2003,
personal communication; A. Hamilton, 2004,
personal communication).
IPN in fresh water
Fry
Infectious pancreatic necrosis is traditionally a
disease of rainbow and brook trout fry. In Atlantic
salmon the clinical features and pathology are
Journal of Fish Diseases 2005, 28, 383390 R J Roberts and M D Pearson IPN in salmon
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2005
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similar to those found in rainbow trout (McKnight
& Roberts 1976) with fry, darker in colour, showing
in the surface water lm or at outows, making
distinctive shimmering movements, whirling or
lying on their side and hyperventilating. Outbreaks
normally occur within 3 or 4 weeks of rst feeding
and may result from vertical transmission, poor
biosecurity in the production system or contamin-
ated water supplies. Mortality level is often related to
stocking density (Bebak-Williams, McAllister &
Boston (2002) and can be as high as 90% in very
young fry. Survivors generally progress normally.
The histopathological picture in young fry is one
of severe necrosis of the pancreatic acinar cells,
while endocrine and most of the limited fatty
peripancreatic tissue is normal apart from some
lipid necrosis (Fig. 1). There is necrosis of intestinal
mucosa, which is variable in intensity. The liver
consistently shows areas of severe focal or general-
ized necrosis (Fig. 2), in contradistinction to earlier
observations in rainbow trout (Wolf & Quimby
1969; McKnight & Roberts 1976).
Fingerlings and parr
Where sh have successfully completed the rst
feeding stages and are growing robustly, the onset of
IPN in salmon ngerlings may be less explosive but
nevertheless losses can amount to 70% or more over
a period of about 2 months. Usually however, losses
in older ngerlings are of the order of 10 or 20%
and affected sh develop distinctive clinical fea-
tures. These include darkening in colour, whirling
or hanging head up in the water or lying on their
side hyperventilating.
At post-mortem the abdomen is always slightly
swollen anteriorly. There may be engorgement of
capillaries around the pectoral ns and there is
generally erosion of the dorsal n and swelling of
the vent. Small punctate haemorrhages may be seen
over the pyloric caecal area, although this is very
variable and peritoneal vessels may be engorged.
The liver is particularly distinctive. Usually it is
swollen, pale yellow to white in colour and very
friable (Fig. 3). The intestine of moribund sh
usually contains a whitish yellow exudate, often
referred to as catarrhal within the viscus, which is
usually empty of food.
The histopathological picture is generally one of
severe acute viral infection, with extensive and
progressive destruction of the pancreatic acinar
cells. These may be very pale coloured in haema-
toxylin and eosin (H & E) sections with consider-
able dark staining of disrupted nuclear material.
There is extensive, often generalized, necrosis of the
liver tissue which can be accompanied by inam-
matory inltrates, but is more often characterized
by loss of all cellular architecture (Fig. 4). This is
very different from the condition observed in
Figure 1 Severe acute IPN necrosis in pancreas of rst feeding
Atlantic salmon fry. The acinar tissues are destroyed but
endocrine and lipid tissues remain largely intact (H&E, 180).
Figure 2 Severe acute necrosis of liver of Atlantic salmon fry.
The entire liver is involved (H&E, 160).
Figure 3 Atlantic salmon parr with severe acute IPN. The liver is
very pale and there are punctuate haemorrhages over the
hyperaemic pancreatic area.
Journal of Fish Diseases 2005, 28, 383390 R J Roberts and M D Pearson IPN in salmon
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rainbow trout infected with the virus at this stage,
which generally does not include pathology in the
liver to any signicant degree.
The intestine is also affected. In fry (or in smolts
in sea water, vide infra), the entire intestinal mucosa
of moribund sh may, terminally, slough into the
lumen, forming what is often described as a
cattarhal inltrate. In parr, however, the mucosa
usually remains more or less intact, but there is
always some focal necrosis, particularly in the
mucosa of the pyloric caeca. There may be migra-
tion through the mucosa and release into the lumen
of highly eosinophilic, swollen, hyaline epithelial
cells with swollen dark nuclei. These unusual and
very characteristic cells are believed to be apoptotic
mucosal epithelial cells being expelled from the
membrane and are called McKnight cells after their
original describer (McKnight & Roberts 1976).
They are very frequently found in acute IPN in all
species, but again are less frequent in ngerling
salmon parr than in the other affected stages.
Once deaths have ceased, the surviving popula-
tion soon becomes bimodal, with the majority
starting to grow well and develop to the smolting
stage without further setback. However, a signi-
cant and variable minority grow poorly. The sh
may remain thin and dark and be readily culled or
they may appear to grow, albeit slowly, with often
considerable abdominal distension. The thin sh
have limited body fat at post-mortem and histology
reveals an almost complete absence of acinar tissue
in the pancreas. The second group may appear to
grow to a size where they should smolt. When
transferred to sea water however, they may die
within 48 h or more characteristically linger on for
some weeks. It is characteristic of these sh that
they are often seen taking pellets into their mouths
and spitting them out again. This is not pathogno-
monic, however, as it is also seen in chronic
pancreas disease (Ferguson, Roberts, Collins & Rice
1986) in slightly older sh. Post-mortem of such
sh reveals that the intestine is greatly distended by
accumulated undigested food. Their pancreatic
acinar tissue may be hardly more extensive than
that of the very thin sh, but they generally have
more body fat and have also made some limited
growth.
The livers of such sh may appear normal,
although with little evidence of metabolic activity or
there may be evidence of previous liver damage and
increased cellularity. The intestinal wall, which may
have a food impacted lumen seven or eight times
larger than normal, has reduced villus height and
the muscularis layers are drastically reduced in
thickness (Fig. 5). There is however little evidence
of McKnight cells or epithelial sloughing and these
sh would appear to be affected solely by pancreatic
insufciency.
Post-smolts
Transfer of young salmon to salt water is a
particularly stressful stage in the production cycle.
The complex anatomical and physiological changes
and very high steroid levels incumbent on adapta-
tion to a marine existence also render the sh
extremely susceptible to handling stresses and
particularly to bacterial infections such as furun-
Figure 4 Acute necrosis of the liver of Atlantic salmon parr. The
hepatic structure is lost in this example, but such loss of
architecture is more variable in parr than in fry (H&E, 200).
Figure 5 Grossly distended intestine in chronically affected
Atlantic salmon parr. Note the accumulated food, characteristi-
cally attened mucosal villi and minimal, largely necrotic,
pancreatic acinar tissue (H&E, 50).
Journal of Fish Diseases 2005, 28, 383390 R J Roberts and M D Pearson IPN in salmon
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culosis. Smolts which have recovered from a
freshwater IPN infection, however, generally trans-
fer to sea water well. Residual smolts with distended
intestines will eventually die although they generally
survive for a few days. Also, a small number of
apparently recovered sh will also succumb to a
recrudescence of the condition in the form of acute
necrosis within the regenerating, recovered pancreas
and very severe sloughing of enteric mucosa.
Although most of the acutely affected recrudescent
sh will die quickly, some may hang, dark and thin,
in the water column around the edge of the cage for
weeks or months before succumbing. Thereafter,
however, smolts recovered from a freshwater out-
break of IPN appear solidly immune and no
subsequent losses are generally observed.
Where smolts with no previous exposure to the
IPN virus have transferred from an IPN-free site to
a marine site with a history of the condition, then
almost invariably what is referred to by many
producers as a 3m ( 3-month post-transfer)
event, occurs. This is a very sudden, often
extremely high, acute mortality of smolts which
have hitherto been in excellent condition. It occurs
with great suddenness around 23 months after
transfer. Losses may amount to 50% or more,
although more commonly, with the advent of
improved transfer facilities and special transfer
diets, losses will be in the range of 1025%. Recent
work on genetic selection for IPN resistance has
shown that, as with rainbow trout (Okamoto,
Tayama, Kawanobe, Fujiki, Yasuda & Sano 1993),
losses can be reduced to below 7% even in the most
challenging environments, by the use of virus
resistant stocks.
Affected sh stop feeding; they may be darker,
but generally retain their silver colour. They hang in
the water, may spiral with head up or sink to the
bottom where they die. There may be some agonal
twitching but they succumb very rapidly. Mortal-
ities may start slowly but there is a rapid build up
necessitating the careful removal of dead sh several
times a day if viral loading in the water column is to
be minimized. Fish which show clinical signs rarely
recover.
At post-mortem the principal external character-
istics are again slight anterior abdominal swelling
and oedema at the vent. Grossly, internal organs are
often normal except for a pale and friable liver and a
pink ush over the pyloric caeca, but section of the
intestine always reveals extensive catarrhal exudates
in a gut devoid of food.
The histopathological picture in 3m smolts is of
an extremely severe viraemic disease, similar to that
seen in older ngerlings in fresh water, but much
more acute. In particular the liver shows severe focal
or generalized necrosis (Fig. 6). In addition areas of
necrosis may also be seen in the haemopoietic tissue
of the kidney. The pancreatic acini are largely
destroyed and replaced by a pale necrotic congery of
cellular debris with dark nuclear strands (Fig. 7).
The intestine may lose almost the entire mucosal
epithelium sloughed into the lumen, but more
frequently it will appear intact with large numbers
of individual apoptotic McKnight cells forming in,
and being expelled through, the mucosa. These
exudates appear in section as a mixed cellular and
Figure 6 Pancreas of Atlantic salmon post-smolt which has died
of acute 3m IPN infection. The pancreatic acinar cells are
completely destroyed (H&E, 160).
Figure 7 Pancreas of 3m Atlantic salmon post-smolt with
chronic IPN lesion. The pyknotic nuclei with semi-lunar halos
are characteristic of such infections (H&E, 180).
Journal of Fish Diseases 2005, 28, 383390 R J Roberts and M D Pearson IPN in salmon
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amorphous congery, which may ll the entire
lumen of the organ (Fig. 8).
Although most post-smolts affected by clinical
IPN appear to succumb, there is a relatively small
number of sh which do not die but fail to grow.
These are generally dark in colour, very thin and
become particular targets for heavy sea louse,
Lepeophtheirus salmonis, infestations. Farmers often
refer to such sh as lice magnets and where
possible remove them. Histopathological examina-
tion of such sh shows minimal residual pancreatic
acinar tissue. Normally they do not feed well, nor
do they show the swollen, impacted intestine seen
frequently in such sh in fresh water.
Discussion
Until the advent of intensive marine salmon
culture, IPN of salmon was only an occasional
problem of fry in fresh water and clinically and
histopathologically resembled the disease in trout.
Strains of the ab serotype were generally involved
(Wolf & Quimby 1971; Hastein & Krogsrud
1976). The advent of the more recent and serious
condition in seawater post-smolts, with its modied
pathology and very acute losses, appears to have
coincided with the appearance of specic Sp
serotypes in both Norway and Scotland (Christie
et al. 1988; Smail et al. 1992). There also appears
to have been a successive time-related emergence of
outbreaks from north to south between 1986 in
Norway (Christie et al. 1988) to 2003 when they
reached Northern Ireland (M. McLoughlin, perso-
nal communication) and 2004 when it was diag-
nosed in N. W. France, suggesting the likelihood of
spread via a symptomless marine vector or wild
birds (McAllister & Owens 1992), although spread
via carrier ova or sh cannot be ruled out in all
cases.
Freshwater outbreaks have also changed in nature
over the period. Very high mortalities at the fry
stage have always been a feature of the disease.
However, in our experience, acute mortalities with
consistently observed severe liver lesions at the
ngerling stage and signicant numbers of mortal-
ities from related chronic effects in survivors during
subsequent freshwater and marine stages, have not
been a feature of earlier reports. C. Cunningham &
D. Smail (2003, personal communication) have
compared sequences of IPNV isolates from some
marine and freshwater outbreaks and found close
similarities. The strains they examined did, how-
ever, diverge signicantly from the RNA sequence
of the strain of the virus isolate which they used as a
standard in their laboratory, which was rst isolated
in 1979.
The reasons for the emergence of such an
aggressive and economically important condition,
and its inexorable spread from north to south in just
over a decade are not known but they are likely to
be connected to the considerable increase in
numbers and stocking density of farmed salmon
in sea cages over the period, and also to the increase
in well boat movements with limited biosecurity
precautions. The pathology of the acute cases with
the considerable release of infectious exudate into
the environment would readily enable rapid dis-
semination of infective virus to other stocks,
although there has been no evidence of any clinical
infection in the wild sh population.
Virtually all marine farming waters in the N. E.
Atlantic, from northern Norway to N. W. France,
appear to be infected with IPNV, albeit at differing
levels (Murray et al. 2003). There seems little point,
therefore, in further restricting carrier smolt move-
ments to sea as there are no apparent implications
for wild sh. Therefore, the removal in 2005 of
movement restrictions in this context, throughout
the European Union, was justied. However, the
severe economic and welfare costs of vertical
transmission of virus to freshwater hatcheries with
clean water supplies suggest that concerted efforts,
by reliable broodstock testing, are an important
means of reducing the incidence of the disease in
fresh water and it is unfortunate that this control
has also been removed.
Figure 8 Pancreatic acini of severely IPN-affected Atlantic
salmon post-smolt, undergoing acute necrosis. The pyloric caeca
contain only intra luminal inammatory exudates with large
numbers of interspersed necrotic McKnight cells (H&E, 40).
Journal of Fish Diseases 2005, 28, 383390 R J Roberts and M D Pearson IPN in salmon
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It has been suggested by some producers that all
parr should be deliberately infected with IPNV as a
form of auto-vaccination of survivors, but apart
from the legal and welfare implications of such a
negative strategy this would merely transfer the
losses due to IPN from the marine farm to the
hatchery and perpetuate the subsequent reintroduc-
tion of virus, with carrier sh and via freshwater
efuents, to the marine production environment.
Despite intensive effort, results of vaccine trials
against IPNV have to date been very variable. Thus,
the current strategy of combining husbandry and
transfer improvements with selection for IPN resist-
ance, based on sibling testing by eld exposure under
commercial conditions, is likely to represent the best
hope for future control of this serious disease.
Acknowledgements
We would like to thank the various anonymous
farms which provided material and data in cond-
ence. We also thank Dr David Smail, Dr Carey
Cunningham and Dr Alistair Hamilton for infor-
mation on strain typing and are grateful to Jana
Cole and Tracy J. Brown of the University of Idaho
for assistance with preparation of the paper.
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Blackwell Publishing Ltd