―Case Reports―
Krukenberg Tumor: Metastasis of Meckel s Diverticular Adenocarcinoma to Ovaries Sujit V. Sakpal1, Nitin Babel1, Rajiv Pulinthanathu2, Thad R. Denehy3 and Ronald S. Chamberlain1 1
Department of Surgery, Saint Barnabas Medical Center, USA
2
Department of Pathology, Saint Barnabas Medical Center, USA
3
Department of Obstetrics & Gynecology, Saint Barnabas Medical Center, USA
Abstract A 56-year-old female presented with abdominal pain, weight loss and fatigue. Computed tomography revealed an abdominopelvic mass and ascites. At surgery she had carcinomatosis and bilateral ovarian metastases arising from a cancer in a Meckel s diverticulum. Histology identified the primary to be a signet-ring cell adenocarcinoma within the Meckel s with ovarian metastases. This is the first report of a Krukenberg tumor from a Meckel s diverticulum. A discussion of malignancies within a Meckel s diverticulum is provided. (J Nippon Med Sch 2009; 76: 96―102) Key words: Meckel s diverticulum, Krukenberg tumor, signet-ring cell gastric adenocarcinoma, ovaries
metastatic signet-ring cell adenocarcinoma, thus defining
Introduction
itself
as
an
unusual
Krukenberg.
A
Krukenberg tumor, rare in itself, is found mostly in commonest
young pre-menopausal women and is bilateral in
congenital anomaly of the small intestine. Located on
more than 80% of cases. The most common site of
the antimesenteric border of the ileum, it results
the primary tumor is the stomach (70%). The tumor
from
the
may also originate in the colon, appendix or breast.
omphalomesenteric duct during embryogenesis. The
The prognosis of a Krukenberg tumor is very poor
majority of Meckel s diverticula are benign and
with no established treatment. Early diagnosis and
discovered incidentally, though rarely they may
surgical resection of localized disease are the only
present with gastrointestinal bleeding, obstruction,
hope for a favorable outcome.
Meckel s
diverticulum
incomplete
is
the
obliteration
of
diverticulitis, or as a neoplastic process. We report a case of signet-ring cell gastric adenocarcinoma
Case Report
arising from ectopic gastric tissue in a Meckel s diverticulum of a 56-year-old female. The tumor
A 56-year-old Dominican female was admitted to
presented as bilateral ovarian masses from a
our institution for an elective total abdominal
Correspondence to Ronald Chamberlain, MD, MPA, FACS, Department of Surgery, Saint Barnabas Medical Center, 94 Old Short Hills Road, Livingston, New Jersey 07039, USA E-mail:
[email protected] Journal Website (http:! ! www.nms.ac.jp! jnms! ) 96
J Nippon Med Sch 2009; 76 (2)
A Unique Krukenberg Tumor
Fi g.1 CT s c a no ft hepe l vi sde mo ns t r a t e sal a r ge , s o l i d,r i ghta dne xa lma s s( ar r ow) .Thema s s m i nl a r ge s tdi a me t e ra nd me a s ur e d6 . 7c wa ss ur r o unde dbya s c i t i cf l ui d.
Fi g.3 Lo ngi t udi na lc r o s s s e c t i o no ft he e nl a r ge d ( 1 0c m)r i ghto va r ywi t hKr uke nbe r gt umo r . o l i dt e xt ur e ,a nd f i r m, The s mo o t ha nd s no dul a ra ndbo s s e l a t e dc o nt o uri st ypi c a lo f y. me t a s t a t i ci nvo l ve me nto ft heo va r
Fi g.2 CT s c a n o ft he a bdo me n e xhi bi t sl o w de ns i t y me s e nt e r i c ma s s e s( ar r ows )wi t h ugge s t i ng s ur r o undi ngs o f tt i s s ues t r a ndi ngs ai nf l a mma t o r yo rne o pl a s t i cpr o c e s s .
hysterectomy and bilateral salpingo-oophorectomy. The patient had presented a month prior to the date of surgery with symptoms of abdominal pain,
Fi g.4 A di s s e c t e dvi e wo ft heul c e r a t e dMe c ke l ’ s di ve r t i c ul um ( ar r ow)a ndi l e um ( s t ar ) .The e e n a dhe r e nt t o t he di ve r t i c ul um i s s a dj a c e ntl o o po fs ma l lbo we l( t r i angl e ) .
fatigue, weight loss (14 kg), and decreased appetite of
several
months
duration.
tomography (CT) of the
A
abdomen
computed and
screening exams included a Papanicolaou (Pap)
pelvis
smear, a colonoscopy, an upper gastrointestinal
performed as part of the work-up revealed a large,
endoscopy, and a mammogram. All tests were
solid right adnexal mass (6.7 cm in largest diameter),
normal except for the Pap smear that revealed a
trace ascites (Fig. 1), and several low density
low-grade squamous intraepithelial lesion (LGSIL).
mesenteric masses (Fig. 2). Her
past
included
total abdominal hysterectomy, bilateral salpingo-
gastroesophageal reflux disease treated with proton-
oophorectomy. At surgery, a 10 cm, smooth, firm
pump inhibitors. Surgical history included a breast
and nodular right ovary was noted and excised (Fig.
biopsy (benign), breast reduction, and a pilonidal cyst
3). Frozen section of the right ovary (weighing 221 g
excision. She was G4P3013, and three years post-
and measuring 11.5
menopausal. Her family history was significant for
fallopian tube (measuring 6.5 cm long) revealed a
prostate cancer (father), ovarian carcinoma (sister),
serous carcinoma. A total abdominal hysterectomy
and
and
stomach
medical
The patient was taken to the operating room for a
cancer
history
(maternal
J Nippon Med Sch 2009; 76 (2)
aunt).
Recent
left
9.5
5.5 cm) along with the
salpingo-oophorectomy
was
completed. 97
SV. Sakpal, et al
Fi g.5 Pho t o mi c r o gr a ph o ft hehe ma t o xyl i ne o s i ns t a i ne ds pe c i me nso ft her i ght nd Me c ke l ’ sdi ve r t i c ul um ( 5 C)de mo ns t r a t i ng ( 5 A)a nd l e f t( 5 B)o va r i e s ,a i s t e do ft wo i nva s i vepo o r l ydi f f e r e nt i a t e da de no c a r c i no ma .Thet umo rc o ns c o mpo ne nt s :s t r o ma la nd e pi t he l i a l ,t hel a t t e ri sc o mpo s e do fmuc i nl a de n t he c c e nt r i chype r c hr o ma t i cnuc l e i ,c ha r a c t e r i s t i co fa s i gne t r i ng c e l l swi o s i no phi l i ca ndgr a nul a r , Kr uke nbe r gt umo r .Thec e l l ul a rc yt o pl a s mc a nbee pa l ea nd va c uo l a t e d( ar r ows ,5 C) ,o rbul l ’ se ye / t a r ge t o i d( ar r ows ,5 A)i n a r a nc ewi t hac e nt r a le o s i no phi l i cbo dyc o mpo s e do famuc i ndr o pl e t . a ppe
Fi g.6 Sl i de1( Ova r y)a ndSl i de2( Me c ke l ’ sdi ve r t i c ul um)e xhi bi ti mmuno r e a c t i vi t yt oe pi t he l i a lma r ke r s uc ha sc yt o ke r a t i ns .Ti s s ues pe c i me nsf r o m bo t ht heo va r i e sa ndMe c ke l ’ sdi ve r t i c ul um we r e s l i kea ndde mo ns t r a t e ds i mi l a ri mmuno hi s t o c he mi c a lr e a c t i o ns ―s t a i ni ngpo s i t i ve hi s t o l o gi c a l l ya r ke r s ―de pi c t i ngme t a s t a t i ca de no c a r c i no mao fe c t o pi c f o rCK 7 ,CK 2 0a ndpo l yc l o na lCEA ma udi ngpr i ma r yc o l o ni co ro va r i a no r i gi n. ga s t r i ct i s s uei naMe c ke l ’ sdi ve r t i c ul um, e xc l 98
J Nippon Med Sch 2009; 76 (2)
A Unique Krukenberg Tumor
Further examination of the abdomen revealed an
disappears by the seventh week of gestation. The
ulcerated mass at the tip of Meckel s diverticulum
incidence of Meckel s diverticulum is reported to be
with involvement of adjacent small bowel loops (Fig.
0.5―2% in autopsy series1. In the developing embryo,
4) adherent to the superior mesenteric artery (SMA).
the vitelline duct is lined with pluripotent cells,
The right hemi-abdomen was notable for miliary
having the ability to differentiate into many different
spread of the tumor over Gerota s fascia and up to
tissue types. The most common type of heterotopic
and involving the right hemidiaphragm. A right
tissue found within a Meckel s diverticulum is
hemicolectomy with resection of 32 cm of small
gastric mucosa (50%), with pancreatic and colonic
bowel including a 3 cm Meckel s diverticulum and
mucosa
omentectomy
diverticulum
was
performed.
The
SMA
was
occurring is
less
the
frequently.
most
A
common
Meckel s congenital
skeletonized to debulk the tumor. There was
anomaly of the small bowel and is typically
obvious lymph node involvement at the base of the
asymptomatic in all age groups. However, as age
small bowel mesentery in addition to the peritoneal
increases the incidence of symptomatic Meckel s
deposits noted above. The appendix appeared
diverticular disease decreases from 5% at infancy to
normal.
1.5% by age 40.
Histopathological
right
Generally speaking, Meckel s diverticulum follows
poorly
the rule of 2 s: it affects 2% of the population, 2% of
differentiated adenocarcinoma with focal signet-ring
patients are symptomatic, it is usually found 2 feet
intracellular mucin (Fig. 5A); a left ovary with poorly
from the ileocecal valve on the antimesenteric side,
differentiated adenocarcinoma (Fig. 5B); and an
symptoms normally manifest before the age of 2
ulcerated 3.5 cm invasive poorly differentiated
years, ectopic tissue can be found in 1 out of 2
adenocarcinoma arising in a Meckel s diverticulum
patients, most are about 2 inches long, and the ratio
(Fig. 5C). The tumor was transmural and invaded
of male-to-female incidence is 2 : 1. Meckel s
into an adjacent small bowel wall up to the
diverticula are a true diverticulum which means
muscularis
and
they possess all layers of the small bowel from the
lymphovascular invasion was noted with metastatic
mucosa to the serosal layer. Typically they receive
disease in two of eight mesenteric lymph nodes.
their blood supply from a remnant of the vitelline
Tumor found in the ovary and the Meckel s
artery which emanates from the SMA2.
fallopian
tube
evaluation
and
propria.
ovary
revealed
a
containing
Extensive
perineural
diverticulum was histopathologically similar. Tissues
Ectopic
gastric
mucosa
within
a
Meckel s
of the left fallopian tube, uterine endometrium,
diverticulum may secrete hydrochloric acid which
omentum,
appendix
can lead to peptic ulceration and bleeding. Hence, it
revealed no evidence of malignancy or metastasis.
may present with painless lower GI bleeding, called
The
diverticulosis. This is the most common presentation
ileum,
cervix
colon,
revealed
cecum LGSIL
and and
squamous
metaplasia as seen on the Pap smear.
in children. Symptomatic ulceration may also mimic
Post-operatively, the patient s hospital course was
symptoms of appendicitis, with right lower quadrant
complicated by a urinary tract infection, a prolonged
pain, diarrhea, nausea or vomiting, and fever. Moore
post-operative ileus, and an intra-abdominal abscess
et al. published a series of 50 symptomatic patients
requiring
drainage
who were found to have Meckel s diverticula3. A
catheter and bowel rest. She was subsequently
preoperative diagnosis of acute appendicitis was
discharged home in stable condition.
made 40% of the time. Yamaguchi et al.4 reported on
CT-guided
placement
of
a
600 patients, 287 of which were symptomatic, and Discussion
only 34 of which had a pre-operative diagnosis of Meckel s diverticulum. In this report, Meckel s
Meckel s diverticulum is the persistent remnant of
diverticula were associated with a variety of
the proximal end of the embryonic yolk stalk, or the
complications: obstruction, 36.5%; intussusception,
omphalomesenteric! vitelline duct, which typically
13.7% ;
J Nippon Med Sch 2009; 76 (2)
diverticulitis,
12.7% ;
perforation,
7.3% ; 99
SV. Sakpal, et al
Ta bl e1 Co mpa r a t i ves ympt o ms ,i ni t i a ldi a gno s e s ,me t a s t a s e s ,t r e a t me nta ndo ut c o meo fMe c ke l ’ sdi ve r t i c ul a r de no c a r c i no ma sr e po r t e di nt hel i t e r a t ur e a Sympt o ms / I ni t i a l di a gno s i s
Re f e r e nc e 2 5 Ma r t i ne ta l .
Re c t a l he mo r r ha ge I nt e s t i na l l ympho ma Pr o gr e s s i ve dys pha gi a wi t hwe i ght l o s s Ga s t r o e s o pha ge a l ma s s Obs t r uc t i ve s ympt o ms wi t h l e uko c yt o s i s Ac ut e a bdo me n Chr o ni c i nt e r mi t t e nt o bs t r uc t i o n wi t hwe i ght l o s s Sma l lbo we l t umo r Po s t pr a ndi a l a bdo mi na l pa i n Sma l lbo we l t umo r Ac ut e o bs t r uc t i ve s ympt o ms Obs t r uc t i ve s i gmo i d ma l i gna nc y Abdo mi na l pa i n, f a t i gue a ndwe i ght l o s s Ova r i a n ma l i gna nc y
9 Ri e be re ta l .
8 Li ppee ta l .
1 Pa r e nt ee ta l .
5 Kus umo t oe ta l .
2 6 Li ne ta l .
Cur r e ntCa s e
Hi s t o l o gyo f t umo ri nMe c ke l ’ s
Me t a s t a t i c s i t e( s )
Ade no c a r c i no ma , we l l di f f e r e nt i a t e d
Me s e nt e r i c l ymphno de s
Sur gi c a l e xc i s i o n
No t r e po r t e d
Ade no c a r c i no ma , e a r l ymo de r a t e l ydi f f e r e nt i a t e d wi t hi na na r e ao f me t a pl a s i a
Sync hr o no us ga s t r i c a de no c a r c i no ma ( no tme t a s t a t i c )
Sur gi c a l e xc i s i o n
No r e c ur r e nc e a t1ye a r
Si gne t r i ngc e l l a de no c a r c i no ma , po o r l ydi f f e r e nt i a t e d
Pe r i t o ne um, l i ve r
Sur gi c a l e xc i s i o na nd c he mo t he r a py
De a t h1 4 we e ksa f t e r di a gno s i s
Ade no c a r c i no ma , mo de r a t e l ydi f f e r e nt i a t e d
Li ve r , me s e nt e r i c l ymphno de s
Sur gi c a l e xc i s i o n ( unr e s e c t a bl e me t a s t a s e s ) a nd c he mo t he r a py
Al i vewi t h nodi s e a s e pr o gr e s s i o n a t4mo nt hs po s t o p
Ade no c a r c i no ma , mo de r a t e l ydi f f e r e nt i a t e d
Ur i na r y bl a dde r , me s e nt e r i c l ymphno de s
Sur gi c a l e xc i s i o na nd c he mo t he r a py
Al i vewi t h nodi s e a s e pr o gr e s s i o n a t6mo nt hs po s t o p
Ade no c a r c i no ma , we l l di f f e r e nt i a t e d
No ne
Sur gi c a l e xc i s i o n ( Ha r t ma nn’ s pr o c e dur e )
No r e c ur r e nc e dur i ng c o l o s t o my r e ve r s a la t6 mo nt hs
Si gne t r i ngc e l l a de no c a r c i no ma , po o r l ydi f f e r e nt i a t e d
Lymphno de s , r i ghtf a l l o pi a n t ube , o va r i e s
Sur gi c a l e xc i s i o na nd c he mo t he r a py
Al i vewi t h di s e a s e pr o gr e s s i o n a t4mo nt hs po s t o p
Tr e a t me nt
Out c o me
hemorrhage, 11.8%; neoplasm, 3.2%; and fistula, 1.7%.
carcinoid tumors2,6, GIST tumors7, and signet-ring cell
Approximately 50% of the patients were adults and
adenocarcinomas8. Stromal or carcinoids are the
in this population intestinal obstruction occurred far
most
more often than hemorrhage at a ratio of 5 : 1. The
Occurrence
etiology of intestinal obstruction in adults was
diverticulum is very rare with only 16 cases
attributed
reported before 1963, and another 9 cases between
to
intussusception,
volvulus,
internal
commonly of
found
tumors
adenocarcinoma
at in
this a
site.
Meckel s
1963 and 19905. Clinical features and physical
hernia, or a neoplasm. A primary malignant tumor arising within a
findings associated with a neoplasm in a Meckel s
Meckel s diverticulum is extremely rare, with an
diverticulum may range from acute abdomen with
1
5
incidence of 1.5―3.2% , and has a male predominance .
severe gastrointestinal hemorrhage or perforation, to
Several neoplasms have been reported arising in the
chronic
Meckel s diverticulum such as benign lipomas2,
Factors
100
symptoms
of
contributing
obstruction towards
and
anemia.
malignant
J Nippon Med Sch 2009; 76 (2)
A Unique Krukenberg Tumor
degeneration of ectopic gastric mucosa remain
a Meckel s diverticular malignancy appears poor,
unclear. Some speculate that ectopic gastric mucosa
and dependent upon multiple factors including age
may have an increased malignant potential in
of the patient, metastasis, histological type and
comparison to normal bowel mucosa5. Helicobacter
biologic aggressiveness of the neoplastic process.
pylori is a well known carcinogen that is implicated
Tumors
from
distant
primary
sites
can
in the pathogenesis of gastric adenocarcinoma and
metastasize to the ovary, accounting for 5―6% of all
mucosa-associated
ovarian
lymphoid
tissue
( MALT )
1
malignancies.
Commonly,
the
tumors
lymphoma . However, its role in pathogenesis of
originate from the female genital tract, breast and
primary
Meckel s
gastrointestinal tract. A unique type of metastatic
9
ovarian tumor is a Krukenberg tumor, which is a
malignancy
diverticulum reported
remains
a
case
within doubtful. of
the Reiber
synchronous
et
al.
gastric
metastatic
signet-ring
cell
adenocarcinoma.
It
adenocarcinoma with a second primary in the
accounts for 1―2% of all ovarian tumors with higher
Meckel s diverticulum. They detected numerous
frequency (17.8%) in Japan where gastric carcinoma
Helicobacter pylori in the moderately differentiated
is more prevalent14,15. The most common primary site
adenocarcinoma from the gastroesophageal junction,
is the stomach (70%) followed by the colon, appendix
but none in the neoplastic tissue of the Meckel s
and breast. Rare cases originating from carcinomas
diverticulum.
of the gallbladder16, the ampulla of Vater17 and the
The diagnosis of a Meckel s diverticulum is
urinary tract18 have also been reported.
difficult to make preoperatively let alone identifying
Krukenberg tumors are found most often in
a neoplasm within it. Most Meckel s diverticula are
young women usually in their fifth decade of life.
diagnosed incidentally on a barium study or at
Common presenting symptoms are abdominal pain
laparotomy, laparoscopy or autopsy. A Meckel s
and distension. It may be associated with virilization
scan, in which 99-m-technetium-pertechnetate is
secondary to ovarian stromal hormone secretion, and
infused and preferentially taken up by gastric
ascites. Krukenberg tumors with right hydrothorax
mucosa (of at least 1.8 cm2) can be useful but the
and ascites referred to as Pseudo-Meigs syndrome
accuracy in adults (46%) is much less than in
have also been reported19,20. The lymphatic system is
children10,11. Adjunctive agents such as pentagastrin
the
(increases Tc uptake) and cimetidine (decreases Tc
Krukenberg tumor, but cases without lymphatic
release by gastric mucosa) may enhance detection
involvement have also been reported suggesting
rates12,13. Interestingly, angiography of the SMA may
peritoneal seeding21. Krukenberg tumors are bilateral
also be useful if a vitelline artery is identified feeding
in more than 80% of cases. The ovaries are usually
the Meckel s diverticulum, but this is present only
solid
10% of the time.
asymmetrically enlarged (Fig. 3). Microscopically,
most
probable
with
route
smooth
of
capsular
metastasis
in
surfaces
a
and
Treatment of a neoplasm within a Meckel s
the tumor characteristically reveals mucin-laden
diverticulum typically involves diverticulectomy and
signet-ring cells within the ovarian stroma (Fig. 5).
an
Immunohistochemical
appendectomy
with
primary
small
bowel
evaluation
may
aid
in
anastomosis. More extensive procedures, as in the
distinguishing primary ovarian carcinomas from
presented case, are individualized if additional
metastatic
carcinomas. +
Ovarian
neoplasms
are
disease or metastases are present. The role and
cytokeratin (CK) 7
benefit of adjuvant chemotherapy (5-fluorouracil,
primaries are CK 7 and CK 20+. CK 7+ and CK 20+
cisplatin, oxaliplatinin or mitomycin-C) has not been
suggest
1,5
a
and CK 20 , and colonic
metastatic
upper
gastrointestinal
8
carcinoma, mainly gastric (Fig. 6C2 and 6C4). The
reported on a young female with a signet-ring cell
mortality of Krukenberg tumor is significantly high,
adenocarcinoma in a Meckel s diverticulum who
with most patients surviving less than 2 years22,23.
received post-operative chemotherapy but lived only
The prognosis is worse and surgical resection futile
14 weeks post-diagnosis. In general, the prognosis of
if the primary tumor remains covert or residual
defined but is usually provided . Lippe et al.
J Nippon Med Sch 2009; 76 (2)
101
SV. Sakpal, et al
disease is present after intervention. To date, adjuvant chemotherapy used (irinotecan, cisplatin or mitomycin-C) appears to have no significant effect on prognosis21,24. Adenocarcinoma arising out of ectopic gastric mucosa in a Meckel s diverticulum has been only rarely reported (6 cases) (see Table 1)1,5,8,9,25,26. To the best of our knowledge this report is the only case of metastases
to
the
ovaries,
by
definition
a
Krukenberg tumor, from ectopic gastric mucosa in a Meckel s diverticulum. In our case, the diagnosis of gastric adenocarcinoma was established only after precise immunohistochemical analysis of the tissue obtained from surgically excised ovaries and the Meckel s diverticulum (Fig. 6). Despite lack of demonstrable benefit, given the young age and excellent performance status of our patient, adjuvant chemotherapy with oxaliplatin and 5-fluorouracil was started. References 1．Parente F, Anderloni A, Zerbi P, et al.: Intermittent small-bowel obstruction caused by gastric adenocarcinoma in a Meckel s diverticulum. Gastrointest Endosc 2005; 61: 180―183. 2．Dumper J, Mackenzie S, Mitchell P, Sutherland F, Quan ML, Mew D: Complications of Meckel s diverticula in adults. Can J Surg 2006; 49: 353―357. 3．Moore T, Johnston AO: Complications of Meckel s diverticulum. Br J Surg 1976; 63: 453―454. 4．Yamaguchi M, Takeuchi S, Awazu S: Meckel s diverticulum. Investigation of 600 patients in Japanese literature. Am J Surg 1978; 136: 247―249. 5．Kusumoto H, Yoshitake H, Mochida K, Kumashiro R, Sano C, Inutsuka S: Adenocarcinoma in Meckel s diverticulum: report of a case and review of 30 cases in the English and Japanese literature. Am J Gastroenterol 1992; 87: 910―913. 6．Green M, Oratz R, Muggia FM: Carcinoid syndrome from a tumor of meckel s diverticulum. Am J Med 1987; 83: 184―186. 7．Hager M, Maier H, Eberwein M, et al.: Perforated Meckel s diverticulum presenting as a gastrointestinal stromal tumor: a case report. J Gastrointest Surg 2005; 9: 809―811. 8．Lippe P, Berardi R, Latini L, Bracci R, Cellerino R: Severe prognosis of signet-ring cell adenocarcinoma occurring in Meckel s diverticulum. Ann Oncol 2001; 12: 277. 9．Rieber JM, Weinshel EH, Nguyen T, Sidhu GS, Bini EJ: Synchronous gastric adenocarcinomas in a patient with Meckel s diverticulum. J Clin Gastroenterol 2001; 33: 78―80. 10．Priebe CJ, Marsden DS, Lazarevic B: The use of 99m-technetium pertechnetate to detect transplanted gastric mucosa in the dog. J Pediatr Surg 1974; 9:
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(Received,
October 28, 2008)
(Accepted, December 17, 2008)
J Nippon Med Sch 2009; 76 (2)
