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Intussusception caused by intestinal neoplasia in mature rainbow trout ( Oncorhynchus mykiss , Walbaum 1792)

Authors:
  • Hungarian University of Agriculture and Life Sciences

Abstract

The aquaculture industry is growing and includes the farming and breeding of more than 580 aquatic species worldwide. The rainbow trout (Oncorhynchus mykiss, Walbaum 1792) is the most commonly bred trout species in Hungary. As broodfish form the basis of most fish farms, investigation into tumours occurring in trout, although under‐researched, has proven to be a valuable and necessary field of study. During our investigation, we examined a broodstock of 3‐ to 6‐year‐old rainbow trouts (800) affected with idiopathic intestinal tumours (3%) which had consequentially led to ileus (40%). While performing necropsy, initial pathological observations showed intussusceptions. Tumours were discovered upon opening the body cavity, as well as metastasis forming in the livers and in the vessels of the gills. Histopathological and immunohistochemical tests allowed us to identify the neoplasms. The primary adenocarcinoma was found to have been developed within the intestines of the fish. The tumour tissue broke through the basal membrane and infiltrated the propria, protruding asymmetrically into the lumen of the mid‐intestines, causing it to narrow significantly. This subsequently led to passage disorders, invagination of the intestinal segment and finally the emaciation of the fish. Histopathological and immunohistochemical inspection of the tumour cells displayed a high mitotic index, confirming malignancy.
J Fish Dis. 2021;00:1–6. wileyonlinelibrary.com/journal/jfd
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1 | INTRODUCTION
The rainbow trout (Oncorhynchus mykiss, Walbaum 1792) is an
anadromous fish species which is cultured in substantial quantities
across Euro pe and whose consumption has be en increasing in our diet
each year (“Eurostat – Fishery statistics,” 2017). Healthy broodstocks
are valuable assets to fish farms, since they ensure the continuity of
production. Fish only reach maturity by the age of 2 to 3 years. A
single broodfish may produce tens of thousands of eggs during its
lifetime, thus providing spawn, both for the market and for the brood-
stock itself (Hoitsy, 2002). The death of such a broodfish means a
considerable financial loss for the farm, as the cost of cultivation,
feeding and possible treatment over the nearly 3- year- long period
until the specimen reaches maturity is wasted. The investigation into
commonly occurring trout tumours is a pioneering area of research.
Intestinal intussusception (invaginatio intestini), the folding of in-
testinal sections into each other, is commonly observed by patholo-
gists in domestic animals. As this condition is well known in cattle,
Received: 16 November 2 020 
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  Revised: 18 Jan uary 2021 
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  Accepted: 19 January 2021
DOI: 10.1111/jfd.13347
RESEARCH ARTICLE
Intussusception caused by intestinal neoplasia in mature
rainbow trout (Oncorhynchus mykiss, walbaum 1792)
Márton Hoitsy1| György Hoitsy2| Csaba Jakab3| Tamás Molnár1| János Gál4|
Ferenc Baska4
1Kaposvár Campus, Institute of
Environmental Sciences and Nature
Conservation, Szent István University,
Kaposvár, Hungary
2Hoitsy és Rieger Kft., Miskolc, Hungar y
3Vet- Med- Labor, Budapest, Hungary
4Department of Exotic Animal and Wildlife
Medicine and Clinic, University of Veterinary
Medicine, Budapest, Hungary
Correspondence
Márton Hoitsy, Szent István University,
Kaposvár Campus, Institute of
Environmental Sciences and Nature
Conser vation, Kaposvár, 7400 Guba S. 40.
Hungary.
Email: hoitsym@gmail.com
Abstract
The aquaculture industry is growing and includes the farming and breeding of more
than 580 aquatic species worldwide. The rainbow trout (Oncorhynchus mykiss,
Walbaum 1792) is the most commonly bred trout species in Hungary. As broodfish
form the basis of most fish farms, investigation into tumours occurring in trout, al-
though under- researched, has proven to be a valuable and necessary field of study.
During our investigation, we examined a broodstock of 3- to 6- year- old rainbow trouts
(800) affected with idiopathic intestinal tumours (3%) which had consequentially led
to ileus (40%). While performing necropsy, initial pathological obser vations showed
intussusceptions. Tumours were discovered upon opening the body cavity, as well as
metastasis forming in the livers and in the vessels of the gills. Histopathological and
immunohistochemical tests allowed us to identify the neoplasms. The primary adeno-
carcinoma was found to have been developed within the intestines of the fish. The tu-
mour tissue broke through the basal membrane and infiltrated the propria, protruding
asymmetrically into the lumen of the mid- intestines, causing it to narrow significantly.
This subsequently led to passage disorders, invagination of the intestinal segment and
finally the emaciation of the fish. Histopathological and immunohistochemical inspec-
tion of the tumour cells displayed a high mitotic index, confirming malignancy.
KEYWORDS
adenocarcinoma, invagination, Oncorhynchus mykiss, Rainbow trout
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© 2021 The Authors. Journal of Fish Diseases published by John Wiley & Sons Ltd.
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   HOITSY eT al.
horses, dogs and cats (Constable et al., 1997; Greet, 1992; Levitt &
Bauer, 1992), the pathological progression of the disease has been
well researched and documented. The condition occurs when a con-
tracted, proximal intestinal segment (intussusceptum), together with
the mesentery, invaginates into the adjacent distal portion (intussus-
cipiens), which is in a more- relaxed state, and, after some time in that
position, becomes embedded there permanently. Caught between
the intestinal walls, the veins of the mesentery become contracted,
leading to the serosanguineous infiltration of the intussusceptum and
the swelling of the proximal portion. This invagination is then solidi-
fied by fibrinous exudate, which accumulates between the overlap-
ping intestinal serous membranes. Intestinal invagination leads to
ileus and eventually causes the death of the animal (Kardeván, 1976).
Several studies have discussed the various factors, which are likely to
be the cause of this disorder. For example, gastroenteritis and acute
enteritis may both lead to intestinal intussusception (Rallis et al., 2000).
Intussusception has been described in different fish species,
for instance in tilapia hybrids (Oreochromis sp.) and in channel
catfish (Ictalurus punctatus, Rafinesque, 1818). In the case of the
catfish, the primary cause of the condition was found to be bac-
terial infection which could have been caused by Hafnia spp.,
Stenotrophomonas spp. or Aeromonas spp. (Cao et al., 2016; Liu
et al., 2009; Montelongo- Alfaro et al., 2018). This condition may
have also been induced by unicellular parasites (Eimeria spp.) or
helminths (Anoplocephala spp.), infecting the host animals in great
numbers (Barclay et al., 1982; Tafti, 1999). Foreign bodies in the
intestinal lumen are often the source of the disorder (Allman &
Pastori, 2013), and any intraluminal mass which hinders the pas-
sage of faeces can also cause intussusception. As it has been ad-
equately described in scientific literature, dissection often reveals
diphtheroid crusts or neoplasms in the intestine of many species,
including fish (Kardeván, 1976). Although tumour- induced intussus-
ception in other animal species, for example in horses, has been
well documented (Zauscher et al., 2015), and the development of
tumours has been described extensively in salmonids as well as in
other fish species, reports about tumour- induced intussusception in
fish remain scarce (Dale et al., 20 09; Kasantikul et al., 2016). Several
factors can lead to tumour development in fish. Contaminants and
toxins due to human activities, mycotoxins in the environment or
in the feed, high amounts of antinutrients in phytogenic feed ad-
ditives and oncogenic viruses are all capable of inducing the for-
mation of neoplastic masses (Baeverfjord & Krogdahl, 1996; Bailey
et al., 1996; Black & Baumann, 1991; Dale et al., 2009).
In this article, we present the symptomatology, macroscopic and
microscopic findings accompanying adenocarcinoma- induced intes-
tinal intussusception in rainbow trout.
2 | MATERIALS AND METHODS
An entire broodstock of approximately 80 0 rainbow trout was ex-
amined externally by the authors on a Hungarian trout- breeding
farm during the breeding season.
According to the owner of the farm, some of the fish began to
show clinical signs in the days leading up to the examination, such
as lying separated at the bottom of the pool and a noticeable loss
of appetite. In the days which followed, the fish began to swim on
their sides, later stretching out in a state of agony. The rainbow trout
were anaesthetized with MS- 222 with a concentration of 100 mg/L
(Wedemeyer, 1970). During the physical examination of the fish, the
condition of the gills was examined, and the body cavity was pal-
pated. Where an abdominal mass was found, MS- 222 was used at
250 mg/L to kill the animals.
After removing the abdominal wall with a single cut, the pericar-
dial and abdominal cavities were able to be examined intact and in
one piece. During the course of the research, only the macroscopic
tumorous alterations and unaffected macroscopical tissue were
sampled. Affected tissues (gastrointestinal system, liver and gills)
were removed and placed into an 8% buffered formaldehyde fixative
(Berod et al., 1981).
Histological samples were kept in fixative at room tem-
perature for 24 hr and then processed with an automated tis-
sue sample preparation system. From the paraffin- embedded
tissue blocks, 3– 4- μm- thick slices were prepared and stained with
haematoxylin– eosin.
For immunohistochemistr y, soft tissue samples were fixed in 8%
neutral- buffered formalin (Berod et al., 1981) for 24 hr at room tem-
perature, dehydrated in a series of ethanol and xylene, and embed-
ded in paraffin. The 3- 4 μm- thick sections were routinely stained
with haematoxylin and eosin (HE). Slides for the immunohistochem-
ical reaction were deparaffinized in xylene and graded ethanol.
After antigen retrieval (Target Retrieval Solution; DAKO), at pH 6,
in a microwave oven for 30 min, the deparaffinized sections were
treated with primary antibodies against cy tokeratin AE1- AE3 or pan-
cytokeratin (diluted 1:100, mouse monoclonal, DAKO), E- cadherin
(diluted 1:100, mouse monoclonal, DAKO), claudin- 5 (diluted 1:100,
mouse monoclonal, DAKO), vimentin (diluted 1:200, mouse mono-
clonal, DAKO), α- SMA (smooth muscle actin) (diluted 1:1,200, mouse
monoclonal, Sigma), S- 100 protein (diluted 1:50, rabbit monoclonal,
DAKO) and c- Kit or CD117 (diluted 1:100, rabbit polyclonal, DAKO)
at room temperature for 60 min. Immunohistochemical staining
was performed using the streptavidin– peroxidase procedure. The
antigen- bound primary antibody was detected using a standard
avidin- biotin immunoperoxidase complex (LSAB2 Kit, DAKO). The
chromogen substrate was diaminobenzidine (DAB), and Mayer's
haemalaun was used for counter- staining. For negative control, the
slides were stained with the omission of primary antibody. The fol-
lowing external positive controls were implemented: tumour cells
from the simple infiltrating carcinoma of the canine mammary gland
for pancytokeratin, intact epidermal layers of canine skin for E-
cadherin, canine cutaneous haemangioma for claudin- 5, canine vag-
inal fibroma for vimentin, canine vaginal leiomyoma for α- SMA and
canine peripheral nerve sheath tumour for S- 100 protein.
The prepared slides were examined with a Nikon Optishot- 2 light
microscope and scanned with Panoramic MIDI II (3DHistech); pho-
tographs were made by CaseViewer (3DHistech).
  
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HOITSY e T al.
3 | RESULTS
Disease monitoring is part of the daily routine in the trout farm. The
veterinarian is monitoring the fishes' health status, checking for ex-
ternal parasites, performing bacteriological tests and post- mortem
examinations. Fresh water is provided by a spring which is tested by
laboratories.
As a result of the findings from the first dissection, the entirety of
the rainbow trout broodstock was examined externally on the affected
trout farm. Among the examined fish— about 800 specimen— the prev-
alence of macr oscopic tumours re ached 3%. Am ong the fish with intes-
tinal growths, intussusception was observed in 40% of the cases.
External examination revealed marked signs of anorexia in some
cases, and a loss of musculature was observed along the spine from
the head to the tail. No signs of external trauma or parasites could be
observed on the skin of the trout. In several cases, minor damage was
detected on the upper part of the caudal fins, which was most probably
caused by biting during instances of rivalry. The oral cavities were inta ct.
During necropsy, intussusceptions in the proximal part of the
intestines became visible, where the proximal segment of the
mid- intestine (intussusceptum) was found to be folded into the dis-
tal portion (intussuscipiens). At the site of the invagination, the veins
became contracted and a congestion formed, which consequently
led to the swelling of the intestines and the formation of fibrinous
exudate, anchoring the two segments together (Figure 1).
The mid- intestine became distorted as the intestinal lumen
narrowed, becoming denser to the touch. Upon opening the in-
testinal lumens, tumour- like growths at the pylorus, from 10 to
FIGURE 1 Hyperaemia and congestion in the intestinal
invagination
FIGURE 2 (a) Tumour protruding from the mucosal surface of
the intestine (white arrow). (b) Tumour inside the invagination
(a)
(b)
FIGURE 3 Metastasis in the liver
FIGURE 4 Metastasis in the gill (white arrow)
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   HOITSY eT al.
32 mm in diameter at the site of the intussusception, and lumps
from 2 to 46 mm in diameter were found in the intestine. All fish
having invaginations had tumours at least in their intestinal tracts
(Figure 2a- b). The intestinal lumen of the fish was filled with mucus,
and whitish, filamentary pseudofaeces could be observed at the
anal region.
Following incision, macroscopic examination of the cross section
of the lumps revealed a whitish and dr y surface, having a shine re-
sembling that of lard, with a homogeneous structure. Within the big-
ger masses, red- coloured, irregular nodules, segmented by whitish
trabeculae of connective tissue were found, bleeding areas were ob-
served in the tissue of the lumps, and metastases were found in the
livers (Figure 3). After elevating the healthy operculum, tumour- like,
distinct, whitish nodules became apparent between the gill arches
and the gill filaments (Figure 4). The data of the examined fish are
shown in the following table (Table 1).
The histopathological examination revealed adenocarcinomas
at different parts of the midgut, originating from the intestinal ep-
ithelium which broke through the basal lamina in multiple places
(Figure 5). The tumour cells showed heterogeneous, glandular mor-
phology which differed significantly from the healthy acinar struc-
ture of the intestinal epithelium with the cells arranged in nests and
only a few segments enclosed with the basal lamina. The nuclei of
the adenocarcinoma cells were heteromorph and euchromatic with
marked hyperchromatosis around the nuclear membrane and prom-
inent nucleoli. Cell division was frequently observed implying a high
level of malignity, and the number of goblet cells was also elevated.
Over the course of the examinations, distant metastases were
found in the gills and the livers of the fish. A cellular structure iden-
tical to that of the mid- intestine tumours led us to conclude that the
Age (year) Weight (kg) Gender Primary location Metastasis
1. 30.8 Male Small intestine
2. 31.3 Female Small intestine Gill
3. 41.5 Male Small intestine Liver
4. 41.6 Male Small intestine Pyloric caeca
5. 31.7 Female Small intestine Pyloric caeca
6. 42.3 Female Small intestine Pyloric caeca,
liver
7. 42.5 Female Small intestine,
stomach
Liver
8. 52.8 Male Small intestine,
stomach
9. 42.9 Female Small intestine Gill, liver
10. 53.1 Female Small intestine,
stomach
TABLE 1 Data of examined rainbow
trouts with intussusception
FIGURE 5 The tumour protrudes into the intestinal lumen
(asterisk) Haematoxylin and eosin (HE), Bar = 200 μm
FIGURE 6 (a) Low- power view of the metastatic, secondary
adenocarcinoma in the liver (red arrows). "L” indicates the intact
liver tissues. Haematoxylin and eosin (HE), Bar = 500 μm. (b) In the
high- power view picture of the poorly differentiated, metastatic
adenocarcinoma can be seen with mitotic figures (red arrows).
Haematoxylin and eosin (HE), Bar = 50 μm
(a)
(b)
  
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HOITSY e T al.
metastases had formed rapidly, allowing us to identify the neoplasm
as grade III adenocarcinoma (Figures 6a- b and 7a- b).
The immunohistochemical examination of the intestinal carci-
noma revealed E- cadherin and pancytokeratin positivity (Figure 8a-
b). Additionally, the endothelial cells of the peritumoural vessels
showed claudin- 5 positivity. The following antibody tests produced
negative results during the investigation: anti- vimentin, anti- α- SMA ,
c- Kit and the anti- S- 100 protein.
Tumours protruding into the lumen of the intestine were pushed
into the direction of the rectum by the peristalsis, pulling the proximal
intestinal segment along with them. Thus, it became possible for the
proximal intestine to fold itself into the distal segment, where, as the
disease progressed, it consequently became anchored. This congestion
led to circulatory collapse and inevitably to the death of the animal.
4 | DISCUSSION
Our research focused on the close examination of glandular neo-
plasms originating from the intestinal walls of rainbow trout and
their resulting intussusception, as sampled from a broodstock of the
species. The disease could only be obser ved in mature fish, of a mini-
mum of 3– 4 years in age. One viable explanation could be, that, even
in a species having a relatively short lifespan such as trout, the de-
velopment of tumours requires time. The number of goblet cells was
found to be elevated on the histological slides which were prepared
from the tumours. This larger number of cells precipitates increased
mucus secretion. This elevated secretion may also thereafter reduce
the rate of absorption from the intestines, leading to a worsening
of the fishes' overall condition. Tumours protruding to the intestinal
lumen due to the peristalsis initially cause partial, then complete, ob-
struction or intussusception.
Ulcers may form, which break the continuity of the epithelium.
The damaged intestinal epithelium's capacity to function as a pro-
tective barrier against infections then decreases. At the site of these
ulcers, bacteria are able to invade the deeper tissue layers, poten-
tially leading to septicaemia. Feed material and foreign bodies may
become stuck in the ulcers as well as in the tumours themselves.
It is probable that, apart from viral infections, feed material may
also play a significant role in the development of tumours in the in-
testines of fish, as Dale et al. have already aptly demonstrated (Dale
et al., 2009). The presence of mycotoxins in the fodder, their car-
cinogenic potential and their impact on the immune system pres-
ent a question worthy of further investigation (Canton et al., 1975).
Spurre d by the results of our c urrent finding s, the need for mycotoxin
feeding studies has become apparent and is planned, during which
the state of the immune systems of the trout may be monitored.
FIGURE 7 (a) Gill metastasis, haematoxylin and eosin (HE)
Bar = 200 μm. (b) Gill metastasis, haematoxylin and eosin (HE)
Bar = 50 μm
(a)
(b)
FIGURE 8 (a) Diffuse, intense cytoplasmic pancytokeratin
positivity Bar = 50 μm. (b) E- cadherin immunostaining shows
intense positivity along the cytoplasmic membrane in intestinal
carcinoma Bar = 50 μm
(a)
(b)
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   HOITSY eT al.
Further research should be carried out targeting the development
of an alternative feed composition which is able to replace, to an
ever- increasing extent, those pellets that contain phytogenic com-
ponents. This may explain the growing popularity of insect- protein-
based fish fodder, also mentioned by Li et al., and may eventually
prove to offer a viable alternative to phytogenic proteins. However,
the additional possibility of hereditability should not be excluded at
this point, which would give justification for a selection- based ap-
proach to brood management (Li et al., 2020).
In aquaculture, a foundation bloodstock consisting of progeni-
tors of a particular breed plays a key role in production. Neoplastic
disorders reduce the number of broodfish; thus, investigation into
their causes and the elimination of them, which has proven to be a
challenge for animal healthcare professionals, could make a signifi-
cant economic impact. Clear identification of the actual risk factors
involved requires further research in this field.
ACKNOWLEDGEMENTS
The authors would like to thank the staff of the Department of
Pathology at the University of Veterinary Medicine, Budapest, for
their assistance, as well as the trout farm for providing the fish and
for making publication of this case possible.
CONFLICT OF INTEREST
The authors hereby declare no conflict of interest.
ORCID
Márton Hoitsy https://orcid.org/0000-0003-0354-1892
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How to cite this article: Hoitsy M, Hoitsy G, Jakab C ,
Molnár T, Gál J, Baska F. Intussusception caused by intestinal
neoplasia in mature rainbow trout (Oncorhynchus mykiss,
walbaum 1792). J Fish Dis. 2021;00:1– 6. ht t ps: //doi.
org /10.1111/jfd.13347
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