(CANCER RESEARCH 50. 5969-5977. September 15. I990|
Detection of Somatostatin Receptors in Surgical and Percutaneous Needle Biopsy
Samples of Carcinoids and Islet Cell Carcinomas
J. C. Reubi,1 L. K. Kvols, B. Waser, D. M. Nagorney, P. U. Heitz, J. W. Charboneau, C. C. Reading, and C. Moertel
Sando: Research Institute Berne. P. O. Box 2173. CH 31)1)1Berne. Switzerland [J. C. R.. B. H'./: Departments of Oncology, //.. A'. A'., C. M./. Surgery /I). M. \J, and
Radiology ¡J.H'. C. C. C. R./, Mayo Clinic, Rochester, Minnesota 5591)1;and Institute o)'Pathology, L'nirersity of'/.urich, Zurich, Switzerland ¡P.f '. H.J
ABSTRACT
Somatostatin (SS) receptor status was investigated in the tumor tissues
from 62 patients with carcinoid tumors and 15 patients with islet cell
carcinomas using receptor autoradiography techniques with two different
iodinatcd Somatostatin analogues as radioligands, a |Leu*. IHrp '.
Tyr"|somatostatin-28 and a Somatostatin octapeptidc, Tyr'-octreotide.
The carcinoid tumors were either primaries (n = 32) or métastases(n =
43), sampled as surgical specimens or as small needle liver biopsies.
Fifty-four of 62 carcinoid patients had SS receptor-positive tumors (87%).
All 15 islet cell carcinoma patients had positive tumors (4 primaries, 11
métastases), i.e., 3 vipomas, 3 insulinomas, 2 glucagonomas, I gastri-
noma, 2 polyfunctional tumors, and 4 nonfunctioning tumors. Saturation
and competition experiments on tissue sections revealed saturable, high
affinity binding sites pharmacologically specific for bioactive SS ana
logues. In a majority of the tumors, the receptors were densely distributed
and were always homogeneously found in the whole tumor. All except
two tumors were labeled with both radioligands. Multiple liver métastases
(n = 16) from three different patients were all shown to contain a
comparable amount of receptors. SS receptors could be demonstrated
even in very small tissue samples of liver métastases obtained by percu
taneous liver biopsies (mean weight, 6.8 mg). The majority of the eight
SS receptor-negative carcinoids were mainly bronchial carcinoids (n =
5), usually poorly differentiated. On the contrary. SS receptor-positive
cases were never found to be anaplastic. All tumors except one from
patients pretreated with octreotide (3 days to 3.8 years) were SS receptor
positive. In the majority of carcinoids or islet cell carcinomas, the SS
receptor status correlated with the in vivo biochemical response (hormone
inhibition) to octreotide. These data demonstrate (a) the high prevalence
of SS receptors in the primary tumors of both carcinoids and islet cell
carcinomas, (b) their presence in métastasesas well. (<•) their continuous
expression even during long term octreotide therapy. (</) the possibility
of measuring SS receptors in percutaneous needle liver biopsies, and (e)
the evidence of their functionality. This study therefore suggests that
tumoral SS receptors may be the likely molecular basis for octreotide
action and may be an important parameter for predicting the therapeutic
efficacy of SS analogues ¡ncarcinoids and islet cell carcinomas.
INTRODUCTION
The variable symptom complexes associated with malignant
carcinoid tumors and the peptide-producing metastatic islet cell
carcinomas (1, 2) have posed therapeutic challenges to clini
cians since they were first discussed in the medical literature
more than three decades ago. These malignant diseases produce
a constellation of clinical problems which create unique diffi
culties in management for the surgical and medical oncologist
(3).
Recently, however, an analogue of the neuropeptide soma-
tostatin, octreotide (Sandostatin, SMS 201-995), has been syn
thesized and shown to be therapeutically beneficial in reducing
most of the symptomatology in both islet cell carcinoma and
carcinoid patients (4-9).
Received 11/6/89: accepted 6/8/90.
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The exact mechanism of action of the SS2 analogue in these
tumors is not fully understood (10). We have recently shown in
a small study that a high percentage of hormone-producing
islet cell carcinomas such as vipomas, gastrinomas. insulino
mas. or GRFomas do possess specific SS receptors (11-14).
This suggests that SS analogues such as octreotide may have a
direct effect on the tumor tissue itself, by regulation of the
hormone secretion and/or by regulating tumor growth (10, 15,
16). However, because of the numerous actions of SS in the
body (17), an indirect effect through a physiological SS target
still remains conceivable (15. 16). At the present time, infor
mation on SS receptor prevalence is completely lacking for
carcinoids, which represent the largest group of tumors among
the gastroenteropancreatic tumors. Carcinoid tumors arise
most often in small intestine and metastasize early into the
liver: less frequently they arise from other organs such as the
lung, thymus, pancreas, or stomach (18). In all of these cases,
episodic flushing and diarrhea are the most common initial
symptoms, whereas biochemically an increase in serotonin (in
the form of urinary 5-hydroxyindoleacetic acid) and sometimes
substance P can be measured (2, 18).
In the present study, we evaluated for the first time the SS
receptor status of carcinoid tumors in a large number of cases.
We tested additional islet cell carcinomas, including glucagon
omas and nonfunctioning tumors, two types of tumors never
tested for SS receptors before. Furthermore, we evaluated the
feasibility of measuring SS receptors in nonsurgically removed
tumors, i.e., in ultrasound-directed percutaneous needle biop
sies for liver métastases,as an alternative to the SS receptor
measurement in surgical samples. This method permits corre
lation of SS receptor status and the ¡nvivoeffect of octreotide
on hormone levels in these tumors. This may ultimately provide
information about the functionality of these receptors and the
possible predictive value of SS receptor measurements for fu
ture octreotide therapy.
MATERIALS AND METHODS
Tumor samples from 62 carcinoid patients, including 32 primaries
and 43 métastases,were investigated (Table 1). Sixty samples were
obtained after surgical removal: in the remaining cases (n = 15) they
were obtained through percutaneous needle biopsies of the liver métas
tases.
The islet cell carcinomas investigated included three vipomas. three
insulinomas. two glucagonomas, one gastrinoma, as well as two poly-
functional and four nonfunctioning tumors. Nine of these cases were
liver biopsies. The biopsies were performed under local anesthesia. A
Bard Biopty instrument with an 18-gauge Biopty-C'ut biopsy needle
that had a sampling notch of 17 mm was used with ultrasound guidance
(19,20).
All tumor tissue from surgical and needle biopsy sampling was
immediately fro/en and processed later for autoradiography. The cases
in which needle biopsies of the liver were performed were subsequently-
treated with octreotide therapy and had monitoring of hormone levels.
In three cases of carcinoid, multiple liver métastases(nine. four, and
2The abbreviations used are: SS. Somatostatin: GRFoma. a carcinoma thai
secretes growth hormone-releasing factor: ACTH, adrenocorticotropic hormone.
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