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358 Brief Communications and Case Reports Vet Pathol 43:3, 2006

Vet Pathol 43:358–362 (2006)

Gastric Adenocarcinoma and Chronic Gastritis in Two Related Persian Cats

M. M. DENNIS, N. BENNETT AND E. J. EHRHART

Abstract. Two 12.5-year-old castrated male Persian cats from the same household, whose dams were
littermates, presented simultaneously with gastric adenocarcinoma associated with proliferative and
fibrosing gastritis. Intralesional adult Ollulanus tricuspis nematodes and rare surface-associated spiral-
shaped bacteria were identified in one cat. No etiologic agents were identified in tissues from the second
cat; however, gastric mucosa was examined following anthelmintic treatment. Clinical signs in each cat
had commenced 2 months apart and included vomiting, hematemesis, intermittent melena, and weight
loss. This is the first report of gastric adenocarcinoma occurring in housemate cats or cats of common
descent. Carcinogenesis may have been influenced by shared undetermined genetic and environmental
factors, possibly including Ollulanus tricuspis, spiral-shaped bacteria, or other etiologies for chronic
gastritis that remain unidentified.

Key words: Adenocarcinoma; cats; gastritis; Helicobacter; nematodes; neoplasia; Ollulanus tricuspis;
parasite.

Gastric adenocarcinoma is exceedingly uncommon in cut surface of one fundic mass; however, a urea slant
cats. No predisposing factors have been identified in cats bacterial culture grew no urease-producing bacteria. The
that might be associated with gastric mucosal trans- cat was treated with metronidazole, amoxicillin liquid
formation and tumorigenesis. This manuscript reports drops, and famotidine for 2 weeks and sucralfate
the simultaneous occurrence of gastric adenocarcinoma suspension for 5 days.
in two related cats from the same household and Endoscopic biopsies revealed severe, diffuse, fibros-
discusses some potential contributory factors. ing, and proliferative gastritis with intralesional nema-
Two 12.5-year-old, castrated male Persian cats were tode parasites and rare surface-associated spiral-shaped
presented to Colorado State University Veterinary bacteria (Fig. 1). The mucosa was markedly thickened
Teaching Hospital (CSU-VTH), on the same day. with elongated, tortuous to ectatic gastric pits lined by
Clinical signs had emerged 2 months apart and included hyperplastic mucous neck cells. The lamina propria
vomiting, hematemesis, intermittent melena, hyporexia, contained abundant fibrous connective tissue that
and weight loss of 4–6 months duration. The cats were replaced and separated gastric pits. Lymphocytes,
of common maternal lineage because they were born plasmacytes, and few follicular lymphoid aggregates,
from queens that were littermates, although the sires neutrophils, and globule leukocytes were distributed
were unrelated. The cats were raised strictly indoors throughout the lamina propria. Profiles of nematodes
within the same household. They had been the only cats were most often located within superficial dilated gastric
in the household from the time they were young adults. pits. Nematodes averaged 30 mm in diameter and had
There was no known exposure to cats outside of the thin, ridged cuticles, tricuspid tails, and poorly discern-
household. Neither cat had been administered anthel- able platymyarian-meromyarian musculature. The ne-
mintic medication as an adult. matodes were identified as Ollulanus tricuspis based on
Cat No. 1 was referred to CSU-VTH with a diagnosis their morphologic characteristics and location in the
of mild, chronic, multifocal, superficial lymphoplasma- stomach. Rare spiral-shaped bacteria that stained with
cytic gastritis based on endoscopic biopsies taken cresyl echt violet (CEV) were associated with the surface
3 months prior. The referring veterinarian described of luminal epithelial cells. Both cats were treated with
the gross appearance of the fundic mucosa as irregular. fenbendazole.
The cat had been treated with sucralfate, cimetidine, Despite immediate clinical improvement following
cefazolin, enrofloxacin, chlorpheniramine, prednisone, fenbendazole treatment, clinical signs recommenced and
metronidazole, and amoxicillin, with no response. worsened, and cat No. 1 returned 2 weeks later to CSU-
Upon presentation to CSU-VTH, cat No. 1 was in VTH for an exploratory laparotomy. Gastric adenocar-
good body condition and no abnormalities were cinoma was identified in surgical biopsies taken from
detected by physical examination. No significant ab- a dark brown, 1-cm-diameter polypoid mass that
normalities were identified with a complete blood count, protruded from the fundic mucosa (Fig. 2). Dilated
serum biochemistry panel, or urinalysis. Endoscopy gastric pits were segmentally lined by neoplastic
identified coarsely nodular fundic mucosa and three 2- cuboidal to polygonal epithelial cells that piled multiple
to 4-cm-diameter polypoid masses located in the fundic cell layers thick. There was segmental loss of the
and cardiac gastric mucosa. Scant spiral-shaped bacteria glandular basement membrane. The cells had distinct
were identified in an impression smear made from the cell margins; plump, deep basophilic cytoplasm; and
Vet Pathol 43:3, 2006 Brief Communications and Case Reports 359

large, ovoid, basilar, hypochromatic nuclei with large


and multiple nucleoli. Neoplastic cells had high nucle-
ar : cytoplasmic ratio and marked anisokaryosis, and
averaged two mitoses per five high powered fields. A few
of these cells had a ‘‘signet ring’’ appearance, charac-
terized by large cytoplasmic vacuoles that peripherally
displaced and compressed nuclei. Tubuloacinar struc-
tures and nests of similar neoplastic epithelium invaded
the deep lamina propria, submucosa, and muscularis
and were within vessels. Noncancerous areas had
fibrosing and proliferative gastritis as previously de-
scribed. Rare surface-associated spiral-shaped bacteria,
which stained with CEV, were within gastric pits.
Intralesional nematodes were not identified in the
sections examined. In addition, parasites were not
identified with examination of gastric juice (2.5 ml) that
was aspirated at surgery and concentrated using the
Baermann technique.
Cat No. 1 was euthanatized twelve days after surgery.
At necropsy, omentum was adhered to the serosal
surface of a 3-cm-long 3 1.5-cm-thick, oblong, white,
firm mural mass that regionally expanded the wall of the
cranial aspect of the gastric fundus. The mucosa
overlying the mass was thickened and lacked rugal
folds. The remaining mucosa, except in the pyloric area,
was diffusely thickened and coarsely nodular. Histologic
evaluation of the stomach confirmed gastric adenocar-
cinoma and chronic proliferative and fibrosing gastritis.
Intralesional nematodes were not observed, although
spiral-shaped bacteria were. Metastasis was identified in
the liver and the kidney.
Cat No. 2 had developed similar clinical signs
2 months before cat No. 1, but was referred to CSU at
the same time as cat No. 1 with a diagnosis of moderate,
chronic, regional, ulcerative and pleocellular gastritis
with moderate epithelial dysplasia, based on endoscopic
biopsies taken 5 months prior. The referring veterinar-
ian described the gross appearance of the fundic mucosa
as irregular. The cat had been treated with famotidine,
sucralfate, and prednisone with limited response.
On presentation to CSU, cat No. 2 had lost
approximately 2.5 kg of body weight, despite being fed
six to seven meals of pureed, canned cat food per day.
Physical examination revealed a palpable mass in the
right cranial abdomen. Abdominal ultrasonography
revealed diffuse thickening of the stomach wall
(20 mm) with heterogenous echogenicity and loss of

r
Fig. 1. Stomach, endoscopic biopsy; cat No. 1. The
mucosa contains dilated gastric pits that are separated neoplastic epithelium that invade the submucosa. The
by abundant connective tissue and are lined by overlying mucosa is affected with mucous neck cell
hyperplastic mucous neck cells. Profiles of nematodes hyperplasia, lymphoplasmacytic inflammation, and fi-
are within multiple glands. Asterisk denotes the brosis. HE; Bar 5 250 mm.
characteristic tricuspid tail. Inset emphasizes distinctive Fig. 3. Stomach, mucosal surface; cat No. 2. The
longitudinal cuticular ridges (arrows). HE. Bar 5 glandular mucosa is diffusely thickened and coarsely
100 mm. Inset bar 5 10 mm. nodular. Regionally, nodules coalesce to form polypoid
Fig. 2. Stomach, surgical biopsy; cat No. 1. projections that overlay a transmural mass (arrows)
Asterisks denote tubuloacinar structures comprised of with a central area of necrosis (asterisk). Bar 5 1 cm.
360 Brief Communications and Case Reports Vet Pathol 43:3, 2006

gastric layer distinction. A 3-cm 3 1.5-cm mass scopic examination of the vomitus, stomach contents, or
extended from the gastric wall into the lumen of the gastric mucosa, because eggs and larvae are not typically
stomach. There were also several heteroechoic, ill- passed in the feces.11 In one study, evaluation of three
defined nodules throughout the hepatic parenchyma. histologic sections identified organisms in only half of
Cytology from ultrasound-guided percutaneous fine- infected cats;9 therefore, histology is not a sensitive
needle aspirates of gastric and hepatic masses was diagnostic approach.
consistent with carcinoma. Four days after discharge, The pathogenicity of O. tricuspis is poorly un-
the cat was administered fenbendazole, as described derstood. O. tricuspis has been considered clinically
above, based on the endoscopic biopsy results of cat insignificant by some authors.9,19 Clinical signs may be
No. 1 that had demonstrated Ollulanus tricuspis. intermittent and include chronic vomiting, anorexia, or
Cat No. 2 was euthanatized 3 weeks later. At weight loss.8,11 The gastric mucosa may appear grossly
necropsy, examination of the stomach revealed a firm, normal, or may have erosions, excess mucus, or
white, invasive, transmural mass that spanned the a nodular appearance.7,10,19 There may be increased
caudal surface of the body of the gastric fundus and follicular lymphoid aggregates, globule leukocytes, and
regionally extended into the greater and lesser omentum, reactive fibrosis throughout the lamina propria.9,11
spleen, and left limb of the pancreas. The gastric mucosa Dilated gastric pits or glandular atrophy may accom-
overlying the mass was thickened up to four times pany these lesions. Adult O. tricuspis nematodes are
normal with a central area of necrosis (Fig. 3). Except in usually localized to the mucus coating the luminal
the area of the pylorus, the remaining mucosa was surface, or to the lumina of dilated gastric pits.
diffusely thickened and nodular. Hepatic and pulmo- Although epithelial hyperplasia has not been a consistent
nary nodules consistent with metastases were present. finding, trichostrongylids infecting other species, in-
Histologic evaluation identified gastric adenocarcinoma, cluding Ostertagia ostertagia in cattle, Ostertagia
similar to that described for cat No. 1, and confirmed circumsincta in small ruminants, Trichostrongylus
hepatic and pulmonary metastasis. There was severe, axei in horses, and Nochtia nochti in Asian macaques,
diffuse, chronic proliferative and fibrosing gastritis, have been associated with proliferative gastric or
strikingly similar to that of cat No. 1. Nematode abomasal lesions.20,22 Trichostrongylid gastritis in
parasites were not seen in sections examined. Spiral- most species is typically characterized by similar mucous
shaped bacteria were not identified with hematoxylin neck cell hyperplasia and by mild lymphocytic in-
and eosin, Warthin-Starry silver, or CEV stains. flammation.
Gastric adenocarcinoma occurring simultaneously Helicobacter spp. have been associated with gastric
in two cats of the same age and from the same adenocarcinoma in humans, ferrets, and a Syrian
household has not been reported. The unlikelihood of hamster.5,15 Gastric Helicobacter-like organisms
such an event suggests a common environmental, (GHLOs) were associated with gastric adenocarcinoma
genetic, or infectious influence, or a combination of in a cougar.25 Helicobacter spp. have also been
these factors. Gastrointestinal adenocarcinoma is the associated with gastric mucosal fibrosis and with
most common nonhematopoietic gastrointestinal tumor eosinophilic, lymphoplasmacytic, or lymphofollicular
found in the cat.24 However, gastric adenocarcinoma gastritis in cats.4,6,21 The failure of a urea slant bacterial
represents only 1% of all feline gastrointestinal adeno- culture prepared from the gastric mucosa of cat No. 1 to
carcinomas,24 with only eight reported cases.1–3,17,24 detect urease-producing organisms may indicate that
Therefore, it is surprising to detect two cats from the organisms were present in numbers below detection
same household with this disease. Two retrospective level or were not Helicobacter spp. Although GHLOs
studies have reported a male predilection for gastroin- may have contributed to gastritis and carcinogenesis in
testinal adenocarcinoma.3,18 Although approximately cat No. 1, GHLOs are commonly found in normal,
two-thirds of feline gastrointestinal adenocarcinoma is healthy cats, and it is not unusual to incidentally observe
reported in Siamese cats, a heritable pattern has not small numbers in normal feline gastric biopsies.16,21
been recognized.18,24 A familial predisposition for Rare spiral-shaped bacteria were microscopically asso-
gastric adenocarcinoma has recently been identified in ciated with the gastric mucosa of cat No. 1; however,
Chow Chow dogs (E. McNeil, personal communica- prior antibiotic therapy may have reduced bacteria
tion). Because these cats shared maternal lineage, the numbers. In contrast, GHLOs are generally present in
possible influence of genetic factors on carcinogenesis large numbers when associated with gastric inflamma-
should be considered. tion.12
Ollulanus tricuspis is a viviparous trichostrongyle In the two cases described herein, the characteristics
nematode of the feline stomach with a characteristic of the gastritis, although nonspecific, were consistent
life cycle that is capable of completion within a single with either gastric spirochetosis or ollulanosis. It is
host. Cats usually become infected through ingestion of common for multiple cats within the same household to
vomitus that contains any life stage of Ollulanus.11 be simultaneously infected with Ollulanus tricuspis.9
Long-haired cats may transmit these parasites more Nematodes were not detected in cat No. 2. However,
efficiently because of their propensity for hairball- histologic examination was performed after fenbenda-
associated vomiting related to frequent grooming.8 zole therapy, which is considered highly efficacious.26 It
Antemortem diagnosis of the infection requires micro- is possible that cat No. 2 was never infected with
Vet Pathol 43:3, 2006 Brief Communications and Case Reports 361

Ollulanus. However, the clinical history and histologic 10 Hargis AM, Prieur DJ, Blanchard JL, Trigo FJ:
changes, in the absence of spiral-shaped bacteria, Chronic fibrosing gastritis associated with Ollulanus
support infection in cat No. 2 as well. The involvement tricuspis in a cat. Vet Pathol 19:320–323, 1982
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helminths, such as Spirocerca lupi, Schistosoma sp., and J Comp Pathol 112(3): 307–318, 1995
Taenia taeniaeformis larvae, are associated with malig- 13 Johnson RC: Canine spirocercosis and associated
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