GASTROENTEROLOGY 1995;109:1415-1420
ALIMENTARY TRACT
Effect of Endogenous Hypergastrinemia on Gastrin Receptor
Expressing Human Colon Carcinoma Transplanted
to Athymic Rats
MING CHU,* FINN CILIUS NIELSEN,* LENNART FRANZI~N, ~ JENS F. REHFELD, ~ JENS J. HOLST, II
and KURT BORCH*
Departments of *Surgery and ~Pathology, UniversityHospital of Link6ping, Link6ping, Sweden; and Departments of tClinical Biochemistry
and IIMedical Physiology, Universityof Copenhagen, Copenhagen, Denmark
Background & Aims: The effect of endogenous hyper-
gastrinemia on growth of human colon carcinoma is
not known. Our aim was to study the growth of human
colon carcinoma in an animal model with endogenous
hypergastrinemia. Methods: Human colon carcinoma
was transplanted to the colon of 40 athymic rats. Of
these, 25 underwent gastric fundectomy to accomplish
endogenous hypergastrinemia, and 15 were sham oper-
ated to serve as controls. The duration of the study
was 8 weeks. During the last week, 12 fundectomized
animals received a gastrin (cholecystokinin B) receptor
antagonist. Metaphase arrest index, local invasion,
and distant spread of the tumor were investigated. Ex-
pression of gastrin and cholecystokinin B receptor mes-
senger RNA was examined by reverse-transcription
polymerase chain reaction. Results: Tumor spread by
direct extension outside the colon was observed in all
animals, and liver metastases were observed in 10 of
the 25 fundectomized animals. Sham-operated animals
showed none of these features. The metaphase arrest
index of the tumor did not differ between fundectom-
ized animals given the cholecystokinin B receptor an-
tagonist and sham-operated animals, whereas it was
significantly increased in fundectomized animals not
given the antagonist. The tumor expressed both gastrin
and cholecystokinin B receptor messenger RNA. Con-
clusions: The results indicate that endogenous hyper-
gastrinemia may promote proliferation and spread of
human colon carcinoma expressing cholecystokinin B
receptor.
l
'n rats and hamsters, pentagastrin, gastrin 17, and
.endogenous hypergastrinemia have been reported to
stimulate growth of the colon mucosa.*-6 Gastrin recep-
tors have been shown in normal colon mucosa in rats
and in normal colon mucosa and colon carcinoma in
humans] -1° Gastric antrum exclusion, leading to hyper-
gastrinemia, has been shown to enhance carcinogenesis
in the colon of the rat. 11 Furthermore, it has been shown
that pentagastrin stimulates the growth of colon carci-
noma xenografts in athymic mice, resulting in reduced
survival. 12 Although there are contradicting studies, I3 iv
these findings indicate that gastrin, at least under certain
circumstances, may stimulate growth of the colon mucosa
and colon carcinoma.
In rats and hamsters, resection of the oxyntic gland
area of the stomach induces hypergastrinemia. <.3'18 The
effect of this model on growth and spread of human
colon carcinoma is not known.
Subcutaneous and intramuscular human tumor xeno-
grafts in immunodeficient mice have low or nonexistent
metastatic capability, even when they are derived from
tumors that are highly metastatic in the patient. 19'2°
However, when histologically intact human colon carci-
noma is transplanted to the colon in the immunodeficient
animal, local and distant spread occurs] 1 We studied the
effect of gastric fundectomy with hypergastrinemia on
the cellular proliferation and spread of a human colon
carcinoma orthotopically transplanted to immunodefi-
cient rats.
Materials and Methods
The study was approved by the local animal wetfare
committee, and the patient from whom tumor tissue was col-
lected gave informed consent regarding the examinations per-
formed.
A fresh tumor specimen was obtained from a 74-year-old
woman undergoing right-sided hemicolectomy for carcinoma
in the ascending colon, There were no liver metastases, and
histological examination showed a poorly differentiated adeno-
carcinoma with moderate to pronounced cellular pleomor-
phism and numerous mitoses. There was local serosal involve-
ment but no lymph node metastases (Dukes' stage B).
Gastroscopy showed normal gastric mucosa, as did histological
© 1995 by the American Gastroenterological Association
0016-5085/95/83.00