Do pathologists thoroughly Evaluate the Greater Omentum Following Gastrectomy for Malignancy: an Audit Based on Histopathology Reports

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_____________________________________________________________________________________________________
*Corresponding author: Email: thifhelimbilu.luvhengo@wits.ac.za,
thifheliluvhengo@gmail.com;
Journal of Cancer and Tumor International
6(1): 1-8, 2017; Article no.JCTI.35246
ISSN: 2454-7360
Do pathologists thoroughly Evaluate the Greater
Omentum Following Gastrectomy for Malignancy:
an Audit Based on Histopathology Reports
O. Tobiko
1,2
, J. Kiluba
2
, C. Jann-Kruger
1,2,3
, M. J. Hale
2,4,5
and T. E. Luvhengo
1,2,6*
1
Department of Surgery, University of the Witwatersrand, South Africa.
2
University of the Witwatersrand,
South Africa.
3
Edenvale Hospital, University of the Witwatersrand, South Africa.
4
Department of Anatomical Pathology, University of the Witwatersrand, South Africa.
5
National Health Laboratory Service, South Africa.
6
Charlotte Maxeke Johannesburg Academic Hospital, University of the Witwatersrand,
South Africa.
Authors’ contributions
This work was carried out in collaboration between all authors. Author OT designed the study as part
of master of surgery degree, did literature search, developed the protocol, collected data, performed
the initial data analysis and reviewed the manuscript. Author JK was involved in data analysis,
statistical analysis, drafting of the manuscript, review of the manuscript and preparation for
submission. Author CJK was involved during protocol development as a co-supervisor, data
collection, review of the manuscript. Author MJH was involved during protocol development as a co-
supervisor, data collection and review of the manuscript. Author TEL was involved in conception of
the idea, protocol development, data collection, writing and review of the manuscript and preparation
for submission. All authors read and approved the final manuscript.
Article Information
DOI: 10.9734/JCTI/2017/35246
Editor(s):
(1) Lingxiang Liu, Bioinformatics & Comp Biology, MD Anderson Cancer Center, Houston, USA And Department of
Oncology,The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu Province, People's Republic of China.
(2)
Severino Rey, Molecular Biology at Albizu University, Miami, Florida And President and CEO of Foundation for Sciences
and Research (FORESC), Florida, USA.
(3)
Sung-Chul Lim, Industry-Academic Cooperation Foundation, Chosun University, South Korea.
Reviewers:
(1) Wagih Mommtaz Elmorsi Ghannam, Mansoura University, Egypt.
(2)
Ihsan Yıldız, Suleyman Demirel University, Turkey.
(3)
Giulia Montori, Papa Giovanni 23 hospital, Italy.
(4)
Nishith M. Paul Ekka, Rajendra Institute of Medical Sciences, India.
(5)
Nicola Basso, Sapienza University of Rome, Italy.
Complete Peer review History:
http://www.sciencedomain.org/review-history/20681
Received 2
nd
July 2017
Accepted 21
st
August 2017
Published 26
th
August 2017
Original Research Article

Tobiko et al.; JCTI, 6(1): 1-8, 2017; Article no.JCTI.35246
2
ABSTRACT
Introduction:
Milky spots in greater omentum are primary sites for seeding of exfoliated cells from
intra-abdominal malignancies. Surgery is the mainstay of treatment of gastric adenocarcinoma and
the greater omentum is usually resected en-bloc.
Aim: To study the histopathological profile of gastric malignancies and to determine if pathologists
routinely analyze the greater omentum submitted following gastrectomy.
Methods: An audit of histopathology records of patients who had gastric malignancies between
2008 and 2012 was undertaken. Data retrieved included patients’ demography, tumour site,
tumour histology and subtypes, Helicobacter pylori status, associated gastritis, types of
gastrectomy and; analysis and finding of omental deposits.
Results: 325 records were found of which 76.6% were adenocarcinomas. The overall male to
female ratio of patients was 192:133 and their average age overall was 59.0 years (range: 23102
years). The average age of patients who had adenocarcinoma was 60.2 years. Around 8.8% of
patients who had adenocarcinoma were younger than 40 years.
Gastric resection was performed in 23.1% adenocarcinomas of which 9.1% was stage I based on
final histology. The greater omentum was part of specimen in 46.6% cases but report regarding
cancer deposits was specified in 25.9% of which 11.1% were positive.
Conclusion: Pathologists do not routinely analyze and report findings on the greater omentum of
patients who had gastrectomy for cancer. It potentially leads to under-staging. Analysis of the
greater omentum for cancer cell deposits should be incorporated into the standard pathology
reporting template for gastric cancer following curative gastrectomy.
Keywords: Gastric cancer; greater omentum; milky spots; cancer deposits.
1. INTRODUCTION
Adenocarcinoma, gastrointestinal stromal tumour
(GIST) and lymphoma are the three most
common malignant tumours of the stomach.
Surgical resection is the mainstay of treatment of
adenocarcinoma and GIST. The goal of surgery
for adenocarcinoma is to obtain cancer free
resection margin, which is achieved by
performing subtotal or total gastrectomy
and appropriate lymphadenectomy; if it is
necessary.
Metastases to certain sites in patients with
gastric adenocarcinoma are difficult to detect
during pre-operative staging investigations [1-
11]. These sites include the peritoneum,
transverse mesocolon, sub-centimeter liver
metastases or metastases near the dome
of the diaphragm or in the greater omentum
[10].
The greater omentum was erroneously
considered a lymph nodes bearing structure until
recently [12,13]. Currently however, finding of
cancer deposit(s) in the greater omentum implies
stage IV disease [10,14,15]. Omentectomy is
routinely included during curative resection even
if it is not grossly involved to eliminate potential
micro-metastases [16,17].
The greater omentum is the first site for trans-
peritoneal spread of exfoliated cancer cells from
a transmural tumour or cells shed during
gastrectomy. Identification of cancer deposits in
the greater omentum is reported to be tedious
and exceedingly difficult. Pathologists rely on
visual inspection and/or palpation of the greater
omentum which may only identify deposits when
they have reached a size of at least 3-5 mm in
diameter or random survey of four quadrants of
submitted specimen of greater omentum.
Detailed evaluation of the greater omentum such
as the use of fat filtration method is rarely
practiced as it is tedious [15]. Real time RT-PCR
for CEA to detect cancer deposits in early gastric
cancers is not freely available and thus
infrequently relied on [18]. The aim of the study
was to study the histopathological profile of
gastric malignancies and to determine if
pathologists routinely perform histopathological
analysis of the greater omentum submitted
following curative gastrectomy.
2. MATERIALS AND METHODS
2.1 Methods
The study was based on an audit of
histopathology records of the National Health
Laboratory Services of the Republic of South
Africa of all patients who were diagnosed with

Tobiko et al.; JCTI, 6(1): 1-8, 2017; Article no.JCTI.35246
3
gastric malignancies at Charlotte Maxeke
Johannesburg Academic Hospital (CMJAH) and
Chris Hani Baragwanath Academic Hospital
(CHBAH) from January 2008 to December 2012.
Data retrieved included patients’ demography,
tumour site, tumour histology and subtypes,
Helicobacter pylori status, associated gastritis,
type of gastrectomy and presence of cancer
deposits in the greater omentum. The Lauren
classification and TNM staging system were
used to classify and to stage the tumour.
Data were entered into Microsoft Excel
spreadsheet and imported into STATA vs 11
(statistical software) for analysis purposes. For
summary of categorical variables data were
reported as frequency and percentages whereas
the mean with standard deviation or median with
range was used to summarize continuous data.
Frequency tables, pie charts and bar graphs
were used when appropriate.
3. RESULTS
Records of 325 patients who had gastric
malignancies were found and majority were
adenocarcinomas (249/325) 76.6% (Fig. 1). The
overall male to female ratio of patients was
192:133 and the average age was 59.0 years
(range: 23-102 years). The average age of
patients who had adenocarcinoma was 60.2
years (Fig. 2). The intestinal and diffuse subtypes
of adenocarcinoma were diagnosed in 35.3%
(88/249) and 21.3% (53/249), respectively
(Fig. 3). The median age of patients who had
diffuse gastric carcinoma, signet ring and
intestinal types were 50.5 years (range: 26-84
years), 63 years (range: 27-90 years) and 64
years (range: 24-88 years), respectively. Around
8.8% (22/249) of patients who had
adenocarcinoma were younger than 40 years.
Chronic gastritis was a concurrent finding in
53.0% (132/249) and 12.0% (30/249) were
histologically positive for Helicobacter pylori
(H. pylori) (Table 1).
Gastric resection was performed in 62 of the
patients of which 58 were adenocarcinomas.
Only 23.1% (58/249) of adenocarcinomas
therefore had some form of gastrectomy. Around
9.1% (5/58) of resected adenocarcinoma cases
were stage I disease and 30.9% (17/58) had
stage IV cancer (Table 2).
Fig. 1. Number of patients with various gastric malignancies, N (Total) = 325
Table 1. Comparison of clinical, treatment and histological findings in gastric malignancies
(N=325)
Parameter
Adenocarcinoma
(n=249)
GIST (n=16)
Lymphoma
(n= 32)
Kaposi (n=22)
M:F Ratio 158:91 5:11 14:18 13:9
Average age 60.2 years 62.6 years 46.6 years 39.7 years
HIV positive (%) 4 (1.6%) 0 (0%) 12 (37.5%) 18/22 (81.8%)
Gastrectomy 58 (23.1%) 2 (12.5%) 0 (0%) 0 (0%)
Gastritis 132 (53.0%) 5 (31.3%) 5 (15.6%) 14 (63.6%)
H-pylori 30 (12.0%) 0 (0%) 4 (12.5) 0 (0%)
249
16
32
22
6
0
50
100
150
200
250
300
Adenocarcinoma
GIST
Lymphoma
Kaposi
Other
(76.6%)
(4.9%)
(9.8%)
(6.8%)
(1.8%)

Tobiko et al.; JCTI, 6(1): 1-8, 2017; Article no.JCTI.35246
4
Fig. 2. Average age of patients with various gastric malignancies in years
Fig. 3. Breakdown of adenocarcinomas according to histological subtypes
Table 2. Breakdown of adenocarcinomas
which were resected according to stage
(n=58)
Stage
Number (%)
Stage I 5 (8.6%)
Stage II 16 (27.6%)
Stage III 16 (27.6%)
Stage IV 18 (31.0%)
Unspecified 4 (6.9%)
Total
58 (100%)
The greater omentum was noted to have been
submitted as part of tissue block and evaluated
by the pathologists in (27/58) 46.6% of the
specimens. However report regarding cancer
deposits in the greater omentum was only
recorded in (7/27) 25.9% of which (3/27) 11.1%
had cancer deposits. For details of patients who
had status of greater omentum reported see
Table 3.
4. DISCUSSION
Adenocarcinoma is the commonest malignant
tumour of the stomach and it affects patients
above the age of 60 years unlike in Nigeria [19]
and Iran [20] where it is commonly diagnosed in
individuals in their 5
th
decade of life. Similar to
what has been reported, majority of patients
affected by gastric adenocarcinoma in the
current study were males and the intestinal
subtype was the most prevalent subtype of
gastric adenocarcinoma [21,22]. Although GIST
.
35
%
21
%
6
%
38
%
Intestinal
Diffuse
Signet ring
Unspecified
60.2
62.6
46.6
39.7
0
10
20
30
40
50
60
70
Adenocarcinoma
GIST
Lymphoma
Kaposi

Tobiko et al.; JCTI, 6(1): 1-8, 2017; Article no.JCTI.35246
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Table 3. Details of patients who had histological status of the greater omentum reported
Case
Gender
Age
Subtype
Differentiation
T status
Deposit
1 M 49 Diffuse Moderate T3 Yes
2 F 66 NS Poor T4 Yes
3 M 40 Diffuse Poor T4 Yes
4 M 80 Intestinal Moderate T3 No
5 M 52 Intestinal Moderate T1 No
6
M
66
Intestinal
Moderate
T4
No
7 F 64 Intestinal Moderate T2 No
NB: In one record omental deposit was reported as representing lymph node metastasis
and lymphoma are supposed to be the next most
common malignancies of the stomach [21,23], in
this study cases of Kaposi’s sarcoma were
almost twice more common than GISTs.
Close to 10% of gastric adenorcarcinomas were
in patients who were less than 40 years old, the
so called early onset cancer. Matley et al. [24] in
a study of patients with gastric cancer at Groote
Schuur Hospital in South Africa found that 5% of
their patients were younger than 35 years. An
even higher incidence (23.2%) of gastric cancer
in young patients was reported by Pishbijari et al.
[20] in a study of gastric cancer in Tehran. The
aggressive variants of adenocarcinoma i.e.
poorly differentiated, diffuse and signet ring
adenocarcinomas were reported in 81.8% of
patients younger than 40 years in the current
Study [24].
Different cut-off ages, ranging from less than 30
years to less than 45 years are used to define
early onset gastric carcinoma [24,25]. A cut-off
age of 40 years was preferred in the current
study as it is presently used to recommend
evaluation for possibility of hereditary gastric
carcinoma [25,26]. We did not set the ceiling age
for early onset gastric cancer at 50 years as in
certain countries majority of patients are
diagnosed in their fifties. Diffuse gastric
adenocarcinoma as compared to intestinal type
is more likely to be hereditary. Other potential
causative factors of early onset gastric cancer
such as H-pylori [27] in the current cohort of
young patients cannot be ruled out. Another
finding which mirrors previous reports is that
gastric adenocarcinoma in young patients in this
study was more prevalent in females
[24].
Unfortunately HIV test result was not available for
all patients. Patients who had Kaposi’s sarcoma
and lymphoma of the stomach were younger
than 50 years. Both Kaposi’s and lymphoma are
linked with HIV infection and it is not surprising
as South Africa is in the epicentre of HIV/AIDS
pandemic. HIV in sub-Saharan Africa is
predominately a disease of individuals who are
younger than 50 years. All patients who had
Kaposi’s sarcoma and had traceable record of
HIV test results tested positive. The above is
understandable as the stomach is most
commonly affected extra-cutaneous organ in
patients with Kaposi’s sarcoma [28]. Gastritis
was an associated finding in majority of patients
(63.6%) who had Kaposi’s sarcoma.
Although around 23% of adenocarcinomas had
gastrectomy majority of them already had
advanced disease including stage IVcancer.
Similar to findings elsewhere other than in East
Asia where close to 70% of patients present with
early gastric carcinoma, the majority of patients
in the current study either had advanced or
metastatic gastric carcinoma . Less than 10% of
patients in this study had early gastric carcinoma.
Pishbijari et al. [20] also reported low levels of
early gastric cancer at presentation in Iran.
Although the greater omentum was mentioned as
part of the block of tissue submitted for
evaluation in 46.6% of the records, finding
following histopathological analysis included the
omentum in only 25.9% of cases. And, in the four
cases (including a case which was reported as
lymph node metastases) in which there were
cancer deposits in the greater omentum the
cancer was either locally advanced (T3 or T4) or
stage IV.
Findings in this study suggest that pathologists
do not routinely assess the greater omentum
even if it is submitted following gastrectomy for
gastric malignancies. It was not possible to
determine predictors of omental deposits in the
current study as pathologists did not report
pathological findings in majority of specimens
submitted; even in T4 cancers from which
shedding-off of malignant cells is more likely. It is
highly likely that not analyzing and reporting
findings in some cases where the greater

Tobiko et al.; JCTI, 6(1): 1-8, 2017; Article no.JCTI.35246
6
omentum was provided might have led to under-
staging of the cancer. Results following analysis
of the greater omentum would potentially be of
therapeutic value such as leading to
consideration of hyperthermic intraperitoneal
chemotherapy (HIPEC) if cancer deposits were
found, and is also of prognostic value [15].
Although removing the greater omentum has
been proven not to be beneficial and actually
harmful in early gastric cancer, the same cannot
be said in cases where the cancer is transmural
i.e. T3 and T4 [16]. The greater omentum acts
like a magnet for spontaneously exfoliating
cancer cells or cells which broke loose during
resection [29,31,32]. One of the reasons why the
greater omentum is attractive to exfoliated
cancer cells in the peritoneal cavity is its reach
blood supply, especially in the areas where there
are aggregates of immune cells, the so called
milky spots [30,32]. The milky spots are able to
sustain viability of exfoliated cancer cells until
implantation. The homing phenomenon is
enhanced by caloric rich environment provided
by abundant adipocytes found in the greater
omentum and vascular endothelial growth factor
(VEGF) elaborated by its mesothelial cells [33].
The greater omentum of patients who have
gastric cancer of Stage 1B or greater is likely to
be harboring cancer cells and therefore
necessitate a thorough histopathological
evaluation. Unfortunately targeted histological
assessment of greater omentum is not part of
standard reporting format of post gastrectomy
specimen of gastric cancer [35]. If the greater
omentum is not thoroughly assessed it is highly
probable that metastases could be missed which
would lead to under-staging of the cancer and
thus wrong prognostication [34]. The reported
difficulties regarding histological assessment of
greater omentum evaluation may be ameliorated
by focusing on the milky spots where cancer
deposits are likely to be found.
The major limitation of this study is that it was a
retrospective study. Some records regarding
histological subtypes of adenocarcinoma, HIV
and H.pylori status, associated gastritis and
definitive treatment were not found. It is therefore
not possible to reach a definitive conclusion
regarding the stage and resectability of gastric
malignancies at presentation. Neither is it
possible to provide a robust comment on the
association between H.pylori infection, gastritis
and HIV with adenocarcinoma of the stomach in
South Africa.
5. CONCLUSION
Adenocarcinoma is the commonest malignant
tumour of the stomach and is a disease of
individuals above the age of 60 years. Kaposi’s
sarcoma should be considered in HIV positive
individuals presenting with gastric tumour and
are younger than 50 years. Majority of patients
with gastric malignancies do not undergo
gastrectomy. Pathologists do not routinely
assess and/or report pathological findings in the
greater omentum following gastrectomy which
potentially leads to under-staging. As the greater
omentum is a magnet for exfoliated malignant
cells, its thorough assessment should be
incorporated into the standard pathology
reporting template following curative
gastrectomy.
6. RECOMMENDATION
Assessment of greater omentum should be
incorporated into the standard pathology
reporting format following gastrectomy.
Omentum preserving gastrectomy should not be
offered to patients who have potentially curable
gastric adenocarcinoma in a setting where
majority of patients present with advanced
disease.
CONSENT
Receiving informed consent from each patient
was waived as the study was retrospective and
based on histopathology records.
ETHICAL APPROVAL
The study was conducted as part of partial
requirement of a Master of Medicine in Surgery
(MMed degree) for the first author. Approval to
conduct the study was received from the Human
Ethics Committee of University of the
Witwatersrand (M121104) and, Research Review
Boards of Charlotte Maxeke Johannesburg
Academic and Chris Hani Baragwanath
Academic Hospitals. Permission to access
histopathology records was obtained from the
Head of Department of Anatomical Pathology of
the National Health Laboratory Services of the
Republic of South Africa. All authors hereby
declare that all experiments have been examined
and approved by the appropriate ethics
committee and have therefore been performed in
accordance with the ethical standards laid down
in the 1964 Declaration of Helsinki.

Tobiko et al.; JCTI, 6(1): 1-8, 2017; Article no.JCTI.35246
7
COMPETING INTERESTS
Authors have declared that no competing
interests exist.
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