Tohoku
J. exp.
Diagnostic
Med.,
1975,
Value
116, 173-177
of Secretin
Provocation
Test
AKIRA ISHIMORI,* KATSUJI TSUDA, SUSUMU YAMAGATA, YOSHIKUNI MIURA, TAKESHI KAWAMURA, HIROYUKI SAKURADA, and SHOICHI YAMAGATA
The Third Department of Internal Medicine, Tohoku University School of Medicine, Sendai ISHIMORI, A., TSUDA, K., YAMAGATA, SU., MIURA, Y., KAWAMURA,T., SAKURADA, H. and YAMAGATA,S. Diagnostic Value of Secretin Provocation Test. Tohoku J. exp. Med., 1975, 116 (2), 173-177-Plasma gastrin response to the intravenously administered secretin was investigated in various clinical entities. The marked increase of plasma gastrin was found in response to secretin in a case of suspected Zollinger-Ellison syndrome in contrast to various degrees of plasma gastrin decrease seen in patients with ordinary or postoperative recurrent peptic ulcer. The diagnostic value of secretin provocation test was stressed especially in relation to differentiation between Zollinger-Ellison syndrome and recurrent ulcer due to retained pyloric antrum kept away from the food-passing route, both of which are characterized by hypergastrinemia and acid hypersecretion. - gastrin; secretin; peptic ulcer; Zollinger-Ellison syndrome; surgical exclusion of pyloric antrum
Since the blood gastrin-decreasing effect of secretin had been well documented (Hansky et al. 1971; Bunchman et al. 1971; Ishimori et al. 1973), the report of Isenberg et al. (1972) that the exogenously administered secretin produced significant increases in serum gastrin and gastric acid secretion in a patient with Zollinger-Ellison syndrome has been regarded to provide a reliable method in diagnosis of this syndrome. Furthermore, it has been confirmed by Bradley et al. (1973) that this unusual response of serum gastrin to secretin in the Zollinger-Ellison syndrome could not be reversed by total gastrectomy, indicating the specific na ture of pancreatic adenoma-producing gastrin. In the present investigation plasma gastrin response to the exogenously administered secretin was compared in patients with ordinary or postoperative recurrent ulcer, and a case of suspected Zollinger-Ellison syndrome, and its diagnostic value was discussed. SUBJECTS AND METHODS All patients firmed to have
with ordinary or postoperative recurrent ulcer were endoscopieally open ulcer lesions at the time of secretin provocation test.
con
A clinical diagnosis of the Zollinger-Ellison syndrome was made by confirming the coexistence of hypergastrinemia and the elevated basal acid secretion in a 21 year-old male who had a history of duodenal ulcer of about 1 year duration. In this case fasting plasma gastrin level ranged from 88 to 402 pg/ml. Normal level determined in Received for publication, March 14, 1975. * Correspondences should be addressed to Dr. Akira 173
Ishimori.
174
A. Ishimori
our
laboratory
was
AOC-tetrapeptide et
al.
of
11.8
ulcer,
1970)
revealed
mEq/hr multiple
the
stomach.
nor
metastatic
47.1•}22.8 in
a
dose
basal and
of acid
pg/ml.
Gastric
4 ƒÊg/kg
body
output
BAO/MAO
scar
of
formations
Angiography lesion.
were and
The
patient
at
observed
is
of the
scintigraphy
analysis weight
(BAO) 0.9
et al.
10.7
time
the
mEq/hr, of
the
under
the
and
periodic
the liver
by
(Yamagata
acid Besides
and
stimulation
stimulus
maximal
along
pancreas
after
maximal
admission.
endoscopically of
still
before as
output open
lesser revealed
(MAO) duodenal
curvature no
of tumor
observations.
Following multiple sampling of fasting blood in 40 to 60 min, secretin (Boots Pure Drug Co., England) of either 1 or 3 emits/kg body weight was injected intravenously in 3 min and blood specimen was collected frequently thereafter. In most of the cases, intragastric pH was measured simultaneously during the experiment using PH Telemetering Capsule Model TPH-04 (Matsushita Elect. Indust. Co., Osaka, Japan). Plasma gastrin was assayed by the charcoal method using a kit available from the CEA-IRE-SORIN association.
RESULTS
An average response of plasma gastrin in 16 patients with peptic ulcer to secretin 1 unit/kg body weight was shown in Fig. 1. A tendency of plasma gastrin to decline was seen around 10 min after the administration of secretin, although it was not significant statistically. It is noticed that plasma gastrin level remained within normal limits during the test in this group. Fig. 2 demonstrates the decrease in plasma gastrin in response to secretin observed clearly in a case of recurrent ulcer due to retained pyloric antrum kept away from the food-passing route. Fasting plasma gastrin was maintained relatively constant around 450 pg/ml in this case. In Fig. 3 the paradoxical response of plasma gatrin to secretin observed in a case of suspected Zollinger-Ellison syndrome was shown. The highest peak of plasma gastrin seen at 10 min after administration of secretin 3 units/kg body weight recorded 1100 pg/ml which exceeded the relatively high level of fasting plasma gastrin by nearly 900 pg/nil.
Fig.
1. Response Shaded area
of plasma represents
indicate S.D.
n=16.
gastrin to exogenous secretin in patients with the normal range of fasting plasma gastrin .
peptic
ulcer . Vertical bars
Diagnostic
Value
of Secretin
Provocation
Test
175
Fig. 2. Response of plasma gastrin to exogenous secretin in a case (G.M., 33 years old male) of recurrent ulcer due to retained pyloric antrum kept away from the food passing route. Shaded area represents the normal range of fasting plasma gastrin.
Fig. 3. Paradoxical response of plasma gastrin to exogenous secretin in a case (Y.S., 21 years old male) of suspected Zollinger-Ellison syndrome. Shaded area represents the normal range of fasting plasma gastrin.
Fig. 4 illustrates the responses in intragastric pH and plasma gastrin level in a case of peptic ulcer which showed a false positive results probably due to an eleva tion of intragastric pH. However, it is noted that the increase of plasma gastrin in response to secretin was just minimal. DISCUSSION It that
the
has
been
release
reported of gastrin
concerning from
the
pancreatic
diagnosis
of Zollinger-Ellison
adenoma
fluctuates
variably
syndrome resulting
in
176
Fig.
A. Ishimori
4.
Simultaneous
years
old
plasma
measurement
male)
of
gastrin. •ü,
peptic plasma
of plasma ulcer.
Shaded
gastrin; •œ,
et al.
gastrin area
and
intragastric
represents
intragastric
pH
the
in
normal
a case range
(A.T., of
21
fasting
pH.
the change in acid secretion of the stomach (Winship and Ellison 1967; Thompson et al. 1972). Therefore, typical hypergastrinemia could not be expected in all cases of Zollinger-Ellison syndrome especially in the early stage. could
On the contrary not guarantee
it is also pointed the diagnosis
postoperative recurrent ed pyloric antrum kept hypergastrinemia
out that even a finding of hypergastrinemia of Zollinger-Ellison syndrome in cases
ulcer, since certain operative away from the food-passing
and hypersecretion
of gastric
of
procedures which leave retain route may lead to develop both
acid in patients
with ordinary
peptic
ulcer. It method
is clear,
therefore,
is necessary
that
to differentiate
the
development the
of another
Zollinger-Ellison
reliable
syndrome
from
diagnostic ordinary
peptic ulcer in these border line or operated cases. The secretin provocation was examined from such a point of view in the present investigation.
test
As to diagnosis of border line cases which do not show typical hypergastrinemia, the secretin provocation test was found to be useful to differentiate the ZollingerEllison syndrome from ordinary peptic ulcer as shown in Figs. 1 and 3. However, false positive results can be obtained occasionally as shown in Fig. 4 owing to the elevation of intragastric pH which promotes the release of gastrin from gastric mucosa into blood stream through the negative feedback mechanism. The eleva tion of intragastric pH may be caused by direct inhibition of acid secretion at the parietal cell level (Johnson and Grossman 1969; Chey et al. 1970; Ishimori et al. 1973) and by regurgitation of alkaline duodenal content into the stomach. Therefore, it is recommended to measure intragastric pH simultaneously during the secretin provocation test in order to discriminate false positive results. Anyway it would be safe that the minimal increase of plasma gastrin is interpreted as an indication of further examination. In general the secretin provocation test is regarded to be useful in diagnosis of border line cases as already stated by Saeuberli et al. (1974).
Diagnostic
Value
of Secretin
Provocation
Test
177
An application of secretin provocation test to the differentiation of Zollinger - Ellison syndrome and recurrent ulcer due to retained pyloric antrum kept away from the food-passing route has never been reported to our knowledge. Since both conditions could show hypergastrinemia and acid hypersecretion , and since a suspicion of Zollinger-Ellison syndrome could be placed for the first time on postoperative recurrence of ulcer, the establishment of a reliable diagnostic method is quite important for treatment. Indeed the case of postoperative recurrent ulcer presented here has been successfully treated by the repair of the food-passing route. It should be mentioned concerning the reliability of this test that vagotomy does not alter the preoperative response of blood gastrin to secretin as reported by Me Laughlin et al. (1974). Although
the mechanism
with ordinary - Ellison
peptic
syndrome,
indicate
remains
the usefulness
- Ellison
by which
secretin
ulcer, while it increases unsolved,
decreases
the results
of the secretin
blood gastrin
blood gastrin
in patients
obtained
provocation
in patients
with Zollinger
in the present
investigation
test for the diagnosis
of Zollinger
syndrome. References
1)
Bradley,
E.L.,
relationship 2)
Bunchman, gastrin
Chey,
W.Y.,
58,
Hitanant,
J.,
J.I.,
H.
&
Y.K.
73,
in
(1973)
(1971)
Effect
Surg.
Lorber,
Secretin-gastrin
550-556.
dog. S.H.
gastric
of
Forum,
(1970)
secretion
Me
H.,
.
Die
secretin 22,
Effect
in
on
the
303-304. of secretin
man.
and
Gastroenterology,
J.C., measurements
Winship,
D.H.
without
1970)
& the
Yamagata, Nose,
F.
S., T.,
Gastric Med.,
101,
M.,
&
the
secretion 103-117.
in
&
Saik,
R.P.
66,
gastrin
as
Grossman,
M.I.
gastric
acid
Tsuda,
secretory
62, K.,
626-631.
Shimoyama,
response
gastric
(1972) secretion
of
and
M.,
the
stomach
duodenal
ulcer.
W.
E.H.
104,
K.,
stimulated
Human
Das
of
gastric
secre
A.,
by
response
to
Gastrin. ‡U bei
verschiedenen
745-751. H.H.
Variability
Uematsu,
gastrin
Magenantrumhormon
(1972)
syndrome.
syndrome. Ishimori,
inhibition
Gastrinbestimmung
Bunchman,
(1967)
(1974)
(1974)
der
&
of
743.
Zollinger-Ellison
H.,
&
Gastroenterology,
Characteristics
Vetter,
D,D.
Kawai,
serum
1401-1404.
med. Wocheaschr.,
Ellison,
on
and
T.,
between
217,
Zollinger-Ellison
Masuda,
Masuda,
syndrome.
Bedeutung
in
E.W.
Kawamura,
(1969)
G.W.
Reeder,
secretin
calcium,
Difference
Physiol.,
praktische
Moore,
serum
Gastroenterology,
Largiader,
of
62-68.
353-362.
Peskin,
Schweiz.
Thompson,
Jr.,
Y.,
(1973)
M.I. J.
vagotomy.
Saeuberli,
and
Grossman,
M.H.,
post
E.,
depressants 8,
Amer.
Laughlin,
Teil:
S.
Effect
61,
gastrin,
Miura,
secretory
&
secretin.
(1971)
Zollinger-Ellison
japonica, L.R.
by
M.G.
serum
Su.,
Yamagata,
gastric
Johnson,
exp.
J.
Passaro,
on
suspected
&
various
gastrin
12)
Chan,
J.C.
and
and
Korman,
J.H.,
Yamagata,
Krankheiten.
11)
Hendricks,
&
secretin
with A.,
ecretin
10)
man
Gastroenterology,
Walsh,
Gastroenterologia
tion
C.
of
a patient
Ishimori,
to
9)
Thompson,
in
emptying
immunoassay.
effect
akurada,
8)
S.,
&
Surgery,
&
a meal
gastric
Soveny, by
Isenberg,
in
7)
C.R.
820-827.
Hansky,
Unusual
6)
D.D. to
in
measured 5)
Lobley, syndrome.
Reeder,
response
cholecystokinin
4)
J.T.,
Zollinger-Ellison
H.H.,
serum 3)
Galambos, in
of Lancet,
Inoue,
S., T.,
gastrin-like
Clinical
Amer. gastric 1,
role
Surg.,
secretion
of
124, in
serum
250-261.
patients
with
Kinoshita,
H.,
1128-1130.
Wada,
Sato,
J.
T., H.,
Sato,
Yunoki,
AOC-tetrapeptide.
K., K.
&
Sasahira, Tohoku
S. J.
J. exp.
Diagnostic
Med.,
1975,
Value
116, 173-177
of Secretin
Provocation
Test
AKIRA ISHIMORI,* KATSUJI TSUDA, SUSUMU YAMAGATA, YOSHIKUNI MIURA, TAKESHI KAWAMURA, HIROYUKI SAKURADA, and SHOICHI YAMAGATA
The Third Department of Internal Medicine, Tohoku University School of Medicine, Sendai ISHIMORI, A., TSUDA, K., YAMAGATA, SU., MIURA, Y., KAWAMURA,T., SAKURADA, H. and YAMAGATA,S. Diagnostic Value of Secretin Provocation Test. Tohoku J. exp. Med., 1975, 116 (2), 173-177-Plasma gastrin response to the intravenously administered secretin was investigated in various clinical entities. The marked increase of plasma gastrin was found in response to secretin in a case of suspected Zollinger-Ellison syndrome in contrast to various degrees of plasma gastrin decrease seen in patients with ordinary or postoperative recurrent peptic ulcer. The diagnostic value of secretin provocation test was stressed especially in relation to differentiation between Zollinger-Ellison syndrome and recurrent ulcer due to retained pyloric antrum kept away from the food-passing route, both of which are characterized by hypergastrinemia and acid hypersecretion. - gastrin; secretin; peptic ulcer; Zollinger-Ellison syndrome; surgical exclusion of pyloric antrum
Since the blood gastrin-decreasing effect of secretin had been well documented (Hansky et al. 1971; Bunchman et al. 1971; Ishimori et al. 1973), the report of Isenberg et al. (1972) that the exogenously administered secretin produced significant increases in serum gastrin and gastric acid secretion in a patient with Zollinger-Ellison syndrome has been regarded to provide a reliable method in diagnosis of this syndrome. Furthermore, it has been confirmed by Bradley et al. (1973) that this unusual response of serum gastrin to secretin in the Zollinger-Ellison syndrome could not be reversed by total gastrectomy, indicating the specific na ture of pancreatic adenoma-producing gastrin. In the present investigation plasma gastrin response to the exogenously administered secretin was compared in patients with ordinary or postoperative recurrent ulcer, and a case of suspected Zollinger-Ellison syndrome, and its diagnostic value was discussed. SUBJECTS AND METHODS All patients firmed to have
with ordinary or postoperative recurrent ulcer were endoscopieally open ulcer lesions at the time of secretin provocation test.
con
A clinical diagnosis of the Zollinger-Ellison syndrome was made by confirming the coexistence of hypergastrinemia and the elevated basal acid secretion in a 21 year-old male who had a history of duodenal ulcer of about 1 year duration. In this case fasting plasma gastrin level ranged from 88 to 402 pg/ml. Normal level determined in Received for publication, March 14, 1975. * Correspondences should be addressed to Dr. Akira 173
Ishimori.
174
A. Ishimori
our
laboratory
was
AOC-tetrapeptide et
al.
of
11.8
ulcer,
1970)
revealed
mEq/hr multiple
the
stomach.
nor
metastatic
47.1•}22.8 in
a
dose
basal and
of acid
pg/ml.
Gastric
4 ƒÊg/kg
body
output
BAO/MAO
scar
of
formations
Angiography lesion.
were and
The
patient
at
observed
is
of the
scintigraphy
analysis weight
(BAO) 0.9
et al.
10.7
time
the
mEq/hr, of
the
under
the
and
periodic
the liver
by
(Yamagata
acid Besides
and
stimulation
stimulus
maximal
along
pancreas
after
maximal
admission.
endoscopically of
still
before as
output open
lesser revealed
(MAO) duodenal
curvature no
of tumor
observations.
Following multiple sampling of fasting blood in 40 to 60 min, secretin (Boots Pure Drug Co., England) of either 1 or 3 emits/kg body weight was injected intravenously in 3 min and blood specimen was collected frequently thereafter. In most of the cases, intragastric pH was measured simultaneously during the experiment using PH Telemetering Capsule Model TPH-04 (Matsushita Elect. Indust. Co., Osaka, Japan). Plasma gastrin was assayed by the charcoal method using a kit available from the CEA-IRE-SORIN association.
RESULTS
An average response of plasma gastrin in 16 patients with peptic ulcer to secretin 1 unit/kg body weight was shown in Fig. 1. A tendency of plasma gastrin to decline was seen around 10 min after the administration of secretin, although it was not significant statistically. It is noticed that plasma gastrin level remained within normal limits during the test in this group. Fig. 2 demonstrates the decrease in plasma gastrin in response to secretin observed clearly in a case of recurrent ulcer due to retained pyloric antrum kept away from the food-passing route. Fasting plasma gastrin was maintained relatively constant around 450 pg/ml in this case. In Fig. 3 the paradoxical response of plasma gatrin to secretin observed in a case of suspected Zollinger-Ellison syndrome was shown. The highest peak of plasma gastrin seen at 10 min after administration of secretin 3 units/kg body weight recorded 1100 pg/ml which exceeded the relatively high level of fasting plasma gastrin by nearly 900 pg/nil.
Fig.
1. Response Shaded area
of plasma represents
indicate S.D.
n=16.
gastrin to exogenous secretin in patients with the normal range of fasting plasma gastrin .
peptic
ulcer . Vertical bars
Diagnostic
Value
of Secretin
Provocation
Test
175
Fig. 2. Response of plasma gastrin to exogenous secretin in a case (G.M., 33 years old male) of recurrent ulcer due to retained pyloric antrum kept away from the food passing route. Shaded area represents the normal range of fasting plasma gastrin.
Fig. 3. Paradoxical response of plasma gastrin to exogenous secretin in a case (Y.S., 21 years old male) of suspected Zollinger-Ellison syndrome. Shaded area represents the normal range of fasting plasma gastrin.
Fig. 4 illustrates the responses in intragastric pH and plasma gastrin level in a case of peptic ulcer which showed a false positive results probably due to an eleva tion of intragastric pH. However, it is noted that the increase of plasma gastrin in response to secretin was just minimal. DISCUSSION It that
the
has
been
release
reported of gastrin
concerning from
the
pancreatic
diagnosis
of Zollinger-Ellison
adenoma
fluctuates
variably
syndrome resulting
in
176
Fig.
A. Ishimori
4.
Simultaneous
years
old
plasma
measurement
male)
of
gastrin. •ü,
peptic plasma
of plasma ulcer.
Shaded
gastrin; •œ,
et al.
gastrin area
and
intragastric
represents
intragastric
pH
the
in
normal
a case range
(A.T., of
21
fasting
pH.
the change in acid secretion of the stomach (Winship and Ellison 1967; Thompson et al. 1972). Therefore, typical hypergastrinemia could not be expected in all cases of Zollinger-Ellison syndrome especially in the early stage. could
On the contrary not guarantee
it is also pointed the diagnosis
postoperative recurrent ed pyloric antrum kept hypergastrinemia
out that even a finding of hypergastrinemia of Zollinger-Ellison syndrome in cases
ulcer, since certain operative away from the food-passing
and hypersecretion
of gastric
of
procedures which leave retain route may lead to develop both
acid in patients
with ordinary
peptic
ulcer. It method
is clear,
therefore,
is necessary
that
to differentiate
the
development the
of another
Zollinger-Ellison
reliable
syndrome
from
diagnostic ordinary
peptic ulcer in these border line or operated cases. The secretin provocation was examined from such a point of view in the present investigation.
test
As to diagnosis of border line cases which do not show typical hypergastrinemia, the secretin provocation test was found to be useful to differentiate the ZollingerEllison syndrome from ordinary peptic ulcer as shown in Figs. 1 and 3. However, false positive results can be obtained occasionally as shown in Fig. 4 owing to the elevation of intragastric pH which promotes the release of gastrin from gastric mucosa into blood stream through the negative feedback mechanism. The eleva tion of intragastric pH may be caused by direct inhibition of acid secretion at the parietal cell level (Johnson and Grossman 1969; Chey et al. 1970; Ishimori et al. 1973) and by regurgitation of alkaline duodenal content into the stomach. Therefore, it is recommended to measure intragastric pH simultaneously during the secretin provocation test in order to discriminate false positive results. Anyway it would be safe that the minimal increase of plasma gastrin is interpreted as an indication of further examination. In general the secretin provocation test is regarded to be useful in diagnosis of border line cases as already stated by Saeuberli et al. (1974).
Diagnostic
Value
of Secretin
Provocation
Test
177
An application of secretin provocation test to the differentiation of Zollinger - Ellison syndrome and recurrent ulcer due to retained pyloric antrum kept away from the food-passing route has never been reported to our knowledge. Since both conditions could show hypergastrinemia and acid hypersecretion , and since a suspicion of Zollinger-Ellison syndrome could be placed for the first time on postoperative recurrence of ulcer, the establishment of a reliable diagnostic method is quite important for treatment. Indeed the case of postoperative recurrent ulcer presented here has been successfully treated by the repair of the food-passing route. It should be mentioned concerning the reliability of this test that vagotomy does not alter the preoperative response of blood gastrin to secretin as reported by Me Laughlin et al. (1974). Although
the mechanism
with ordinary - Ellison
peptic
syndrome,
indicate
remains
the usefulness
- Ellison
by which
secretin
ulcer, while it increases unsolved,
decreases
the results
of the secretin
blood gastrin
blood gastrin
in patients
obtained
provocation
in patients
with Zollinger
in the present
investigation
test for the diagnosis
of Zollinger
syndrome. References
1)
Bradley,
E.L.,
relationship 2)
Bunchman, gastrin
Chey,
W.Y.,
58,
Hitanant,
J.,
J.I.,
H.
&
Y.K.
73,
in
(1973)
(1971)
Effect
Surg.
Lorber,
Secretin-gastrin
550-556.
dog. S.H.
gastric
of
Forum,
(1970)
secretion
Me
H.,
.
Die
secretin 22,
Effect
in
on
the
303-304. of secretin
man.
and
Gastroenterology,
J.C., measurements
Winship,
D.H.
without
1970)
& the
Yamagata, Nose,
F.
S., T.,
Gastric Med.,
101,
M.,
&
the
secretion 103-117.
in
&
Saik,
R.P.
66,
gastrin
as
Grossman,
M.I.
gastric
acid
Tsuda,
secretory
62, K.,
626-631.
Shimoyama,
response
gastric
(1972) secretion
of
and
M.,
the
stomach
duodenal
ulcer.
W.
E.H.
104,
K.,
stimulated
Human
Das
of
gastric
secre
A.,
by
response
to
Gastrin. ‡U bei
verschiedenen
745-751. H.H.
Variability
Uematsu,
gastrin
Magenantrumhormon
(1972)
syndrome.
syndrome. Ishimori,
inhibition
Gastrinbestimmung
Bunchman,
(1967)
(1974)
(1974)
der
&
of
743.
Zollinger-Ellison
H.,
&
Gastroenterology,
Characteristics
Vetter,
D,D.
Kawai,
serum
1401-1404.
med. Wocheaschr.,
Ellison,
on
and
T.,
between
217,
Zollinger-Ellison
Masuda,
Masuda,
syndrome.
Bedeutung
in
E.W.
Kawamura,
(1969)
G.W.
Reeder,
secretin
calcium,
Difference
Physiol.,
praktische
Moore,
serum
Gastroenterology,
Largiader,
of
62-68.
353-362.
Peskin,
Schweiz.
Thompson,
Jr.,
Y.,
(1973)
M.I. J.
vagotomy.
Saeuberli,
and
Grossman,
M.H.,
post
E.,
depressants 8,
Amer.
Laughlin,
Teil:
S.
Effect
61,
gastrin,
Miura,
secretory
&
secretin.
(1971)
Zollinger-Ellison
japonica, L.R.
by
M.G.
serum
Su.,
Yamagata,
gastric
Johnson,
exp.
J.
Passaro,
on
suspected
&
various
gastrin
12)
Chan,
J.C.
and
and
Korman,
J.H.,
Yamagata,
Krankheiten.
11)
Hendricks,
&
secretin
with A.,
ecretin
10)
man
Gastroenterology,
Walsh,
Gastroenterologia
tion
C.
of
a patient
Ishimori,
to
9)
Thompson,
in
emptying
immunoassay.
effect
akurada,
8)
S.,
&
Surgery,
&
a meal
gastric
Soveny, by
Isenberg,
in
7)
C.R.
820-827.
Hansky,
Unusual
6)
D.D. to
in
measured 5)
Lobley, syndrome.
Reeder,
response
cholecystokinin
4)
J.T.,
Zollinger-Ellison
H.H.,
serum 3)
Galambos, in
of Lancet,
Inoue,
S., T.,
gastrin-like
Clinical
Amer. gastric 1,
role
Surg.,
secretion
of
124, in
serum
250-261.
patients
with
Kinoshita,
H.,
1128-1130.
Wada,
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