Regression of Type II Gastric Carcinoids in Multiple Endocrine Neoplasia Type 1
Patients with Zollinger-Ellison Syndrome after Surgical Excision of All
Gastrinomas
Melanie L. Richards, M.D.,
1
Paul Gauger, M.D.,
2
Norman W. Thompson, M.D.,
2
Thomas J. Giordano, M.D., Ph.D.
3
1
Department of Surgery, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, Texas 78284, USA
2
Department of General Surgery, Division of Endocrine Surgery, University of Michigan Hospital, 1500 E. Medical Drive,
Ann Arbor, Michigan 48109, USA
3
Department of Pathology, University of Michigan Hospital, 1500 E. Medical Drive, Ann Arbor, Michigan 48109, USA
Published Online: June 16, 2004
Abstract. Enterochromaffin-like (ECL) tumors are documented in pa-
tients with hypergastrinemia secondary to chronic atrophic gastritis or
with Zollinger-Ellison syndrome and multiple endocrine neoplasia type 1
(ZES-MEN-1). In patients with ECL tumors and atrophic gastritis, nor-
mogastrinemia after antrectomy has resulted in resolution, regression, or
stabilization of ECL tumors. The natural history of ECL tumors associated
with ZES-MEN-1 following normalization of gastrin levels after gastri-
noma resection has not been previously reported. The purpose of this study
was to determine the course of ECL tumors in patients with ZES-MEN-1
following normalization of serum gastrin levels after gastrinoma resection.
Two patients with ZES-MEN-1 had biopsy-proven ECL tumors on endo-
scopic evaluation. They then underwent surgical exploration that included
distal pancreatectomy, enucleation of pancreatic head tumors, duode-
notomy with excision of submucosal tumors, and peripancreatic lymphad-
enectomy. Gastric ECL tumors larger than 1.0 cm were locally excised. Pa-
tients underwent long-term follow-up with biochemical and endoscopic
surveillance. Normogastrinemia was achieved and sustained following gas-
trinoma resection in two patients with ZES-MEN-1. Periodic endoscopic
surveillance over a 6-year period showed complete resolution of the ECL
tumors. The development of ECL tumors associated with ZES-MEN-1 is
multifactorial. Studies identified a genetic influence on tumor growth with
loss of heterozygosity at the MEN-1 gene locus in ECL tumors. The reso-
lution of ECL tumors in ZES-MEN-1 patients who are normogastrinemic
indicates that an elevated gastrin level is a primary initiator for develop-
ment of these tumors. Therefore both genetic defects and hypergastrinemia
are causative agents. Normalization of serum gastrin levels is critical for
the prevention of aggressive forms of ECL tumors.
Enterochromaffin-like (ECL) tumors are primarily documented in
patients with hypergastrinemia; they are secondary to chronic atro-
phic gastritis or are seen in patients with the Zollinger-Ellison syn-
drome (ZES) and multiple endocrine neoplasia type 1 (MEN-1)
[1]. These endocrine cell neoplasms are frequently referred to as
multiple gastric carcinoids in both conditions. Hyperplasia of the
ECL cells, as well as tumors, develop primarily as the result of the
trophic effect of chronic hypergastrinemia on all of the neuroendo-
crine cells of the proximal stomach.
A literature review of 224 ECL tumors found them to be associ-
ated with chronic atrophic gastritis in 79% of patients; 10% of pa-
tients had ZES, and 11% were sporadic [1]. The sporadic tumors
were solitary, and they were larger and more biologically aggressive
than those that are gastrin-dependent. Of patients with ZES, 92%
had documented MEN-1. The incidence of ECL tumors in ZES-
MEN-1 patients may be as high as 30%, compared to 5% in patients
with chronic atrophic gastritis and hypergastrinemia [2–5]. Because
of the rarity of ECL tumors in sporadic cases of ZES, a genetic
factor related to the gene mutation has been considered an impor-
tant contributing, if not primary, cause of their occurrence in
MEN-1 patients.
In patients with ECL tumors, atrophic gastritis, and hypergas-
trinemia, normogastrinemia after antrectomy has resulted in reso-
lution, regression, or stabilization of ECL tumors [6–8]. The natu-
ral history of ECL tumors in ZES-MEN-1 patients following
normalization of gastrin levels after gastrinoma resection has not
been previously reported. We report two patients with ZES-
MEN-1 and ECL tumors who underwent operative treatment for
their gastrinomas resulting in normalization of gastrin levels. We
also document the effect on the remaining ECL tumors.
Patients and Methods
Two patients with ZES-MEN-1 had biopsy-proven ECL tumors on
endoscopic evaluation. Endoscopic evaluation was performed for
surveillance and diagnostic purposes. Smaller tumors were not
completely excised because of their extent. Both patients then un-
derwent surgical exploration that included distal pancreatectomy,
enucleation of pancreatic head tumors, duodenotomy with excision
of submucosal tumors, and peripancreatic lymphadenectomy. Gas-
tric ECL tumors larger than 1.0 cm were locally excised. All pa-
tients were then followed biochemically and with endoscopic sur-
veillance. Correspondence to: Melanie L. Richards, M.D.
WORLD
Journal of
SURGERY
© 2004 by the Socie ´te ´
Internationale de Chirurgie
World J. Surg. 28, 652–658, 2004
DOI: 10.1007/s00268-004-7345-0