Obesity Surgery (2018) 28:1433–1440

https://doi.org/10.1007/s11695-018-3151-x

REVIEW ARTICLE

Does Bariatric Surgery Affect the Incidence of Endometrial Cancer

Development? A Systematic Review
Alec A Winder 1,2 & Malsha Kularatna 1 & Andrew D. MacCormick 1,3

Published online: 6 March 2018

# Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
Obesity has been linked to an increased prevalence in multiple cancers. Studies have suggested a reduction in the overall risk of
cancer after bariatric surgery. We reviewed the evidence for bariatric surgery reducing the risk of endometrial cancer. Data was
extracted from PubMed, EMBASE, and Medline to perform a systematic review. Thirty-one full text articles were identified from
265 abstracts. Nine observational studies were relevant to endometrial cancer. In the five controlled studies, 462 of 113,032
(0.4%) patients receiving bariatric surgery versus 11,997 of 848,864 (1.4%) controls developed endometrial cancer, odds ratio of
0.317 (95% CI 0.161 to 0.627) using random effects model (P < 0.001). Bariatric surgery seems to reduce the risk of endometrial
cancer; however, more research is required.

Keywords Obesity . Bariatric surgery . Weight loss . Endometrial cancer . Endometrial hyperplasia . Risk reduction . Systematic
review

Introduction menopause, diabetes, polycystic ovarian syndrome (PCOS),

Obesity is an increasing worldwide epidemic. The Lancet
suggested from 2010 to 2030 an addition 65 million people
in the USA and 11 million UK patients alone will be obese
with an estimated 492,000–669,000 additional cancer cases
[1]. A significant increased risk of developing multiple can-
cers including postmenopausal breast cancer, liver, colorectal,
bladder, endometrial, esophageal, and pancreatic in patients
with morbid obesity compared to controls has been noted [2].
Risk factors for endometrial hyperplasia and endometrial
carcinoma include old age, nulliparity, early menarche, late
* Alec A Winder
Malsha Kularatna
malsh87@hotmail.com
Andrew D. MacCormick
Andrew.Maccormick@middlemore.co.nz
1
Department of General Surgery, Middlemore Hospital, Counties
Manukau Health, Auckland, New Zealand
2
London, UK
3
Department of Surgery, University of Auckland, Auckland, New
Zealand
and body mass index (BMI > 27) [3]. Many of these relate to
continuous estrogen stimulation, i.e., chronic anovulation in
PCOS and high estradiol levels in obese people from aroma-
tization of androgens in adipose tissue eventually converted to
estradiol [4]. According to the Million Women Study [5], the
relative risk of endometrial cancer was 2.89 for every 10 units
of BMI above 25 kg m2.
Greater than 10% total weight loss favorably modulates
serum markers including sex hormone-binding globulin,
insulin-like growth factor, C-reactive protein, estradiol, in-
terleukin-6, and tumor necrosis factor alpha [6, 7].
Bariatric surgery however has been shown to achieve
higher and more sustained weight loss compared to inten-
tional weight loss alone [8, 9]. Surgery significantly re-
duces estradiol levels by 35% at 1 and 2 years following
surgery [10] and improves symptoms of menstrual irregu-
larity and PCOS [11]. Casagrande et al. found bariatric
surgery significantly reduced the overall risk of cancer in
morbidly obese patients [12].
Currently, the effect of bariatric surgery on cancers is still to
be determined. The aim of this study was to perform a meta-
analysis of the current literature and determine if bariatric
surgery significantly reduced the risk of developing endome-
trial cancer or pre-malignant endometrial conditions in the
obese female population.
1434
Method
This systematic review was conducted in accordance to the
PRISMA and MOOSE guidelines [13]. Prior to commencing
the review, a protocol was determined between all authors.
Eligibility
Studies Selection
All randomized controlled studies, cohort studies, and case
series were included for analysis including prospective and
retrospective studies. Review articles, expert opinion, com-
mentaries, case studies, posters, abstracts, non-English lan-
guage articles, and unpublished data were excluded. Studies
were selected if they included an endometrial cancer diagnosis
following bariatric surgery or the effects of bariatric surgery
on endometrial hyperplasia and pre-malignant states. Studies
were not excluded based on publication date.
Patient Selection
Inclusion criteria were female patients ≥ 18 years of age with a
history of obesity (BMI > 30 kg m2). Exclusion criteria includ-
ed a pre-existing or concurrent diagnosis of endometrial can-
cer and animal studies.
Patient Intervention
All bariatric surgical procedures were included in the review.
These incorporated gastric banding, vertical sleeve gastrecto-
my, Roux-en-Y gastric bypass, and biliopancreatic diversion.
Gastroenterology procedures were excluded. This was be-
cause endoscopic sleeve gastroplasty is a relatively new pro-
cedure and long-term effects are unknown currently and
intragastric balloon procedures provide less durable weight
loss compared to bariatric surgery [14].
Information Sources
Data was extracted from multiple online libraries, including
PubMed, EMBASE, SCOPUS, Medline, Web of Science,
PsychINFO, and the Cochrane Central Register of
Controlled Trials. Study period included from database incep-
tion to 1 November 2016. Identified full text articles were
examined for additional references.
Search Strategy
The previously mentioned libraries were reviewed using the
search terms listed below and combined using Boolean oper-
ators AND and OR. Search terms are listed in Appendix 1.
OBES SURG (2018) 28:1433–1440
Study Selection
Titles and abstracts identified by the literature search were
independently analyzed by two separate reviewers looking
for relevant articles for full text analysis. The above eligibility
criteria were followed. Disagreements were resolved using a
third party.
Data Extraction and Quality Assessment
Two independent reviewers assessed articles for study design,
location, type of bariatric procedures, number of patients, age,
initial BMI, number of endometrial cancer cases, number of
endometrial cancer deaths, average follow-up period, use of
controls, and how controls were identified. Odds ratios, con-
fidence intervals, and P values were recorded. Percentage
weight loss, comorbidities, and smoking status were also
recorded.
Quality of studies was assessed using the Newcastle-
Ottawa Scale [15] which is designed to assess the quality of
non-randomized studies. Studies were assessed independently
by two reviews under the main headings of Selection,
Comparability, and Exposure. A maximum of nine stars could
be awarded to each article. Only high-quality studies with a
star rating of 7 or greater would be incorporated in the meta-
analysis.
Heterogeneity
For the meta-analysis, heterogeneity of the studies was
assessed using Cochran’s Q test and a significance value of
less than 0.10 was used. The I2 test looking for observed total
variation across studies due to real heterogeneity and not
chance was also used. A value of 0% indicates no observed
heterogeneity, where a larger value shows increased
heterogeneity.
Statistical Analysis
Both a fixed effect and random effect model have been per-
formed for the meta-analysis. In a fixed effects model, it is
assumed that the studies share a common true effect and the
summary effect is an estimate of the common effect size. In
the random effect model, the true effect is assumed to vary
between studies and the summary effect is the weighted aver-
age of the effects in the different studies. The random effect
model tends to give a more conservative estimate.
Results
Overall review of the online databases identified 265 ab-
stracts. This number was reduced to 248 once duplicates were
OBES SURG (2018) 28:1433–1440
removed. After title and abstract review, we excluded 216
articles. One hundred thirty-three articles related to obesity
and not bariatric surgery or cancer; 34 articles related to bar-
iatric surgery but not cancer; 28 articles related to cancers
other than endometrial; and 22 articles related to endometrial
cancer but not bariatric surgery. This left 31 potential papers
for full text screening. One non-English language article was
excluded, five review articles, and two comments. One article
was found to examine cancer and bariatric surgery overall but
was not specific to endometrial cancer. Seven duplicate stud-
ies were excluded and six studies were deemed not relevant. In
total, nine articles remained. A flowchart of this is demonstrat-
ed in Fig. 1.
The nine articles were then subdivided into six controlled
studies. Five studies looking at endometrial cancer and bariat-
ric surgery and one on endometrial hyperplasia. The remain-
ing three were uncontrolled studies looking at endometrial
cancer.
Study Characteristics
Table 1 demonstrates the five controlled studies [8, 16–19]
which incorporated 114,330 patients in the bariatric surgical
arm, of which 113,032 (99%) were women. In the control arm,
852,502 patients were included, of which 848,864 (99%) were
women. The average age of the patients was 43 years in the
surgery arm and 45 years in the control arm; however, this
data for the largest study (Ward et al. [19]) was not incorpo-
rated. The average BMI in both groups was > 40 kg m2, again
excluding Ward et al. The follow-up period varied from 5 to
15 years in four of the studies with one not reporting this data.
Percentage excess weight loss was recorded by Christou et al.
[17] at 67.1% in their surgical group and total percentage
weight loss over 10 years was 16.9% in Sjostrom et al.’s study
Fig. 1 Flow chart demonstrating literature search
1435
[8]. The other three studies [16, 18, 19] have not
commented on this statistic. Comorbidities for both surgi-
cal and control groups are mentioned in Sjostrom’s study
with significantly more smokers in the control group
(p < 0.001) and lower weight and BMI in the control
groups (p < 0.001). McCawley [18] states the comorbidi-
ties of the bariatric group, but not those of the control
group in their study. This information is not commented
on in the other three studies [16, 17, 19].
Endometrial cancer mortality was mentioned in two stud-
ies. Adams et al. noted an 11.2% mortality rate for endometrial
cancer in the control arm compared to 0% in the bariatric
surgery group. Christou et al. noted zero deaths in either
group, but follow-up was shorter.
Table 2 demonstrates the three uncontrolled studies
[20–22] which incorporated 17,672 patients who underwent
a bariatric procedure. The overall female total is unknown as it
is not stated in one study; most studies reviewed multiple
cancers including endometrial and therefore include male pa-
tients. The overall age and preoperative BMI are also not
stated in all these studies.
Pre-malignancy Risk
Only one study (Argenta et al. [23]) examined the effect of
bariatric surgery on endometrial hyperplasia. In 42 patients
with an average BMI of 46.8 kg m2, who underwent Roux-
en-Y gastric bypass and had an average weight loss of 42 kg,
endometrial sampling was performed preoperatively and
1 year later. Both biopsies were analyzed at the same time.
They found endometrial hyperplasia to be present in four
(9.5%) of the patients preoperatively and three at 1 year.
Only one had persistent hyperplasia at the 1-year follow-up
and resolved by 18 months; the other two were de novo. They
concluded the risk was reduced but not eliminated.
Cancer Risk
The total number of endometrial cancers diagnosed in the
bariatric surgical group was 462 (0.4%) and 11,997 (1.4%)
in the control group. A forest plot and odds ratios of the five
controlled studies are summarized in Fig. 2. Individually, two
of the studies demonstrated non-significant results [8, 17] and
three were significant [16, 18, 19]. Overall, the analysis
showed that bariatric surgery is associated with a reduction
in endometrial cancer diagnosis at follow-up using a fixed
effects model, (OR 0.283, confidence interval 0.258–0.311,
P value < 0.001). This effect remained using a random effects
model, (OR 0.317, confidence interval 0.161–0.627, and P
value of < 0.001). Sixty-one patients in the uncontrolled stud-
ies were diagnosed with endometrial cancer (0.3%).
Uniquely, Ward et al. [19] inform us if a patient was obese
or not at the time of hysterectomy. They suggest that the rate
1436 OBES SURG (2018) 28:1433–1440

Table 1 Controlled studies looking at the rate of endometrial cancer after bariatric surgery compared to controls

Bariatric surgery Control

Study Number Female Age (mean BMI No. of Follow-up Number Female (%) Age (mean BMI No. of
(%) years) (mean) cancers years) (mean) cancers

Adams 2009 6596 5654 (86) 38.9 44.9 14 12.3 9442 7872 (83) 39.1 47.4 98
[16]
Christou 2008 1035 679 (65.6) 45.1 > 40 3 5 5746 3678 (64) 46.7 > 40 20
[17]
Sjostrom 2009 1420 1420 (100) 46.1 42.2 21 10 1447 1447 (100) 47.6 41.6 25
[8]
Ward 2014 103,797 103,797 (100) – – 423 – 832,372 832,372 (100) – – 11,728
[19]
McCawley 1482 1482 (100) 41.7 51.6 1 15 3495 3495 (100) 46.9 46.1 126
2009 [18]
Total 114,330 113,032 (99) N/A N/A 462 N/A 852,502 848,864 (99) N/A N/A 11,997

BMI body mass index, N/A non-applicable, No. number

of endometrial cancer is 1.4% in obese patients (BMI > 30 kg/
m2) but decreases to 0.68% in patients who are still obese with
a prior history of bariatric surgery and 0.27% for patients who
are no longer obese after bariatric surgery. Percentage and
absolute weight loss are not commented on.
Heterogeneity
Significant heterogeneity was noted between the studies in
both Cochran’s Q test, < 0.0001 and the I2 test 84.4%. Both
tests suggest significant heterogeneity between studies; how-
ever, both models above give similar results. In this situation,
the random effects model is the more reliable.
Bias
As none of the endometrial cancer studies identified for
this analysis are randomized, there is significant selection
bias. All of the patients chose to have bariatric surgery and
as many of the patients were matched for age and BMI
only, it is not clear why the controls did not choose surgery
or were not eligible. Key information could not be obtained
from the studies. Two studies were matched retrospectively
against databases on BMI, age, and gender [16, 17] and
one study on BMI only, McCawley et al. [18]. Sjostrom
et al.’s study was matched on 18 variables prospectively
[8]. Ward et al. [19], the largest study [19], used the
University Healthsystem Consortium (UHC) database and
evaluated the relationship between BMI and endometrial
cancer adjusting for a prior history of bariatric surgery and
therefore only controlled for obesity (BMI > 30 kg m2).
This incorporates further selection bias and does not pro-
vide information on patient characteristics such as age at
the time of hysterectomy or the time relationship to bariat-
ric surgery. The weight of control subjects and surgical
participants did not seem to be monitored in all of the
controlled studies, and therefore the effectiveness of the
weight loss interventions cannot be determined, a potential
source of outcome bias.
The pre-malignancy study (Argenta et al. [23]) does elim-
inate selection bias by analyzing the effects of bariatric sur-
gery on the individual patients and blinds the participants and
doctors to the results by analyzing them both at the same time;
however, they have not controlled for confounding variables
such as hormone replacement therapy which is present in 27%
of the study population.

Table 2 Uncontrolled studies looking at the incidence of endometrial cancer after bariatric surgery

Study Study design Region Bariatric Number Female Age BMI No. of Cancer Total
procedure (%) (mean) (mean) cancers deaths F/U years

Gagne 2008 [20] Retro case series USA RYGB/SG/LAGB 1566 – – – 1 0 –

Hunsinger 2016 [21] Cohort study USA RYGB 2983 2372 (81) 45.6 47.2 6 – 4
Ostlund 2010 [22] Population SWEDEN SG/GB/RYGB 13,123 10,121 (77) – > 40 54 – 10
cohort
Total N/A N/A RYGB/SG/LAGB 17,672 N/A N/A N/A 61 N/A N/A

RYGB roux-en-Y gastric bypass, SG sleeve gastrectomy, LAGB laparoscopic adjustable gastric band, BMI body mass index, N/A non-applicable, No.
number, F/U follow-up
OBES SURG (2018) 28:1433–1440 1437

Fig. 2 Meta-analysis and forest plot of controlled endometrial cancer studies

Quality despite the heterogeneity between studies. Individually, three

Table 3 demonstrates the quality of each study using the
Newcastle-Ottawa Scale which is designed for assessing the
quality of non-randomized studies. Each study can be
awarded a total of nine stars over three categories—selection,
comparability, and outcomes and exposures. For selection,
two studies gained 4 stars, six 3 stars, and one 2 stars. For
comparability, the controlled studies all receive one or two
stars. The uncontrolled studies received 0 stars for compara-
bility. Finally, for outcomes and exposures, eight studies re-
ceived 3 stars and one 1 star. Overall, the quality of the six
controlled studies was deemed high (7–9/9 stars) whereas the
three uncontrolled studies, one study was deemed low quality
(≤ 4 stars) and the remaining two intermediate (5–6 stars).
Discussion
This meta-analysis demonstrates that bariatric surgery has a
significant effect on the rate of endometrial cancer develop-
ment using both fixed and random effect models (p < 0.001),
of the five studies showed a significant reduction in the rate of
endometrial cancer (16/18–19). The death rate from endome-
trial cancer was reduced from 11 to 0% in one study [16] and
was 0% for both groups in another study [17]. Interestingly,
the follow-up periods of these two studies varied from 5 to
12.5 years. None of the other studies commented on death
rates. Only one study attempted to determine the effect of
bariatric surgery on pre-malignant endometrial changes and
this showed a beneficial change in 42 patients from 9.5% with
endometrial abnormality to 0% after 18 months (p < 0.05)
following bariatric surgery, excluding patients on chemopro-
phylaxis [23].
Overall, the results show a beneficial effect of bariatric
surgery which may provide a cancer protective effect. The
results of this review are in keeping with other studies looking
at the effects of bariatric surgery on cancer overall risk [12],
and on endometrial cancer [24].
BMI has been noted to have a linear relationship to all
cancer risk [25] and is now the third highest risk factor after
smoking and infection and possesses a greater risk for women
[26]. Obesity is thought to account for 20% of all cancer cases

Table 3 Study quality using

Newcastle-Ottawa Scale Study Selection Comparability Outcomes/exposure Total

Adams 2009 [16] ★★★ ★★ ★★★ 8

Christou 2008 [17] ★★★★ ★★ ★★★ 9
Gagne 2008 [20] ★★★ – ★ 4
Hunsinger 2016 [21] ★★★ – ★★★ 6
McCawley 2009 [18] ★★★ ★ ★★★ 7
Sjostrom 2009 [8] ★★★★ ★★ ★★★ 9
Ostlund 2010 [22] ★★ – ★★★ 5
Argenta 2013 [23] ★★★ ★★ ★★★ 8
Ward 2014 [19] ★★★ ★ ★★★ 7
1438
[27]. In fact, the Million Women Study [5] found the relative
risk of endometrial cancer to increase with BMI by 2.89 per
10 kg m2 above 25 kg m2; this was the largest increase of risk
of any cancer reviewed, which included 17 other common
types of cancer. In studies, asymptomatic endometrial abnor-
malities in patients awaiting bariatric surgery have varied from
9 to 28% [23, 28, 29]. Examination and biopsy of the endo-
metrium may be more difficult with higher failure rates in
obese patients [30].
Endometrial cancer has been linked to early menarche, late
menopause, nulliparity, and PCOS. All of these states provide
a longer exposure for females to estrogen which is thought to
be a major contributing factor for endometrial cancer. Excess
weight has been linked to increased pro-inflammatory
markers, excess insulin and insulin-like growth factor, aroma-
tase expression, as well as estradiol levels [31, 32], all associ-
ated with endometrial cancer development.
Intentional weight loss of greater than 10% total body
weight favorably modulates serum markers including sex
hormone-binding globulin, insulin-like growth factor, C-
reactive protein, estradiol, interleukin-6, and tumor necrosis
factor alpha over a 6-month period [6, 7]. Bariatric surgery
commonly provides weight loss far in excess of 10% and is
also effective in improving glucose homeostasis, improved
insulin responsiveness, and inflammatory markers [33].
Adiponectin, a hormone produced in fat cells, is paradoxically
reduced in obese patients and levels are inversely related to
endometrial cancer [34]. Bariatric surgery significantly im-
proves adiponectin levels. Twenty percent of bariatric patients
were found to have PCOS in one study [35], a risk factor for
endometrial cancer, for which bariatric surgery can provide
significant symptomatic improvement [36].
The weight loss effects of bariatric surgery versus inten-
tional weight loss are far more sustained in the morbidly obese
population, and therefore the biochemical effects are likely to
be sustained and provide greater reduction in the risk of de-
veloping endometrial cancer.
Limitations
There were several limitations related to this study. Firstly,
none of the studies were randomized controlled studies. Not
all studies supplied baseline characteristics of patients includ-
ing an average age or weight. For the four studies that did, the
average age of the controls was 2 years greater than that of the
bariatric group; however, this data is not present for the largest
study as they only supplied the average age of all patients
(52.6 years) [19]. Sjostrom [8] noted a greater reduction in
total cancer risk, for all cancers, in postmenopausal women
compared to premenopausal women after bariatric surgery.
None of the studies reviewed pre- and postmenopausal pa-
tients separately for endometrial cancer.
OBES SURG (2018) 28:1433–1440
Ward et al. [19] did state if the patient was obese or not at
the time of diagnosis of endometrial cancer. Christou [17] and
Sjostrom [8] commented on overall percentage excess weight
loss and total percentage weight loss respectively for the bar-
iatric group; however, none of the main studies excluding that
of Ward et al. have commented on weight loss with respect to
patients who developed endometrial cancer.
BMI is an indirect measure of body fat mass and corre-
lates poorly with fat percentage [30], as it does not take
into account bone and muscle mass. Better measures of fat
mass are available such as bioelectrical impedance, DEXA
scan, and MRI, but these are more expensive and were not
used. Matching cases for controls to bariatric patients is
difficult. Only one study [9] matched patients prospective-
ly on 18 variables. The other studies matched patients from
clinical databases; by just BMI in one study [18] and BMI,
age and gender in the other two [16, 17]. The largest study
did not match patients but grouped them based on obesity
or not at the time of cancer diagnosis as well as prior his-
tory of bariatric surgery. This potentially means the control
group may have been more comorbid than the bariatric
group; this all contributes to a selection bias and the sig-
nificant heterogeneity between studies. Finally, there is a
wide variation in the rate of endometrial cancer between
studies. The lowest rate of endometrial cancer in the bar-
iatric surgery group was 0.06% [18] and the highest 1.4%
[8] and in the control groups, the lowest rate was 0.5% [17]
and the highest 3.6% [18]. The reason for this large varia-
tion is not clear.
Conclusions
1. Nine to twenty-eight percent of female patients undergo-
ing bariatric procedures may have asymptomatic endome-
trial abnormalities [23, 28, 29].
2. Bariatric surgery has a beneficial role in pre-malignant
conditions such as endometrial hyperplasia, although fur-
ther studies are required in this field.
3. Bariatric surgery has a significant effect on the rate of
endometrial cancer compared to obese controls.
4. The benefit of bariatric surgery on endometrial cancer
seems to be maintained at least in part even if the patient
subsequently becomes or remains obese. Again, further
studies are required as this is solely based on Ward et al.’s
paper, which was not a randomized trial.
This data may be helpful to surgeons in prioritization
of patients for bariatric procedures. Women with a higher
baseline risk for endometrial cancer could be informed of
the possible risk reductions prior to surgery to aid the
decision process.
OBES SURG (2018) 28:1433–1440
Acknowledgements The authors acknowledge Avinesh Pillai for his as-
sistance with statistical analysis from the University of Auckland.
Compliance with Ethical Standards
For this type of study, formal consent was not required. This article does
not contain any studies with human participants or animals performed by
any of the authors.
Conflict of Interest The authors declare that they have no conflict of
interest.
Appendix 1 - Search terms
OBESITY / MORBID OBESITY / ABDOMINAL
OBESITY / HIGH BODY MASS INDEX / ABDOMINAL
FAT / ADIPOSITY / WEIGHT GAIN / BODY FAT / INTRA-
ABDOMINAL FAT / OVERNUTRITION / BODY
FATNESS / DIABETIC OBESITY / ADIPOSE TISSUE
B A R I AT R I C S U R G E R Y / B A R I AT R I C S /
GASTROPLASTY / STOMACH BYPASS / GASTRIC
B Y PA S S / R O U X - E N - Y / B I L I O PA N C R E AT I C
D I V E R S I O N / B I L I O PA N C R E AT I C B Y PA S S /
JEJUNOILEAL BYPASS / BARIATRIC MEDICINE /
GASTRIC BANDING / LAPAROSCOPIC ADJUSTABLE
GASTRIC BANDING / SLEEVE GASTRECTOMY /
DUODENAL SWITCH
ENDOMETRIAL CANCER / ENDOMETRIAL POLYP /
ENDOMETRIAL HYPERPLASIA / ENDOMETRIAL
ADENOCARCINOMA / PRE-MALIGNANT
ENDOMETRIUM / ENDOMETRIUM CANCER /
ENDOMETRIUM POLPY / ENDOMETRIUM
ADENOCARCINOMA / ENDOMETRIAL TUMOR /
ENDOMETRIUM TUMOR
RISK REDUCTION / RISK / CANCER RISK /
POPULATION RISK / RISK BENEFIT
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