Original Research
Incidence and Timing of Thromboembolic
Events in Patients With Ovarian Cancer
Undergoing Neoadjuvant Chemotherapy
Patricia S. Greco, MD, Ali A. Bazzi, MD, Karen McLean, MD, PhD, R. Kevin Reynolds, MD,
Ryan J. Spencer, MD, Carolyn M. Johnston, MD, J. Rebecca Liu, MD, and Shitanshu Uppal,
OBJECTIVE: To identify the incidence and timing of venous
thromboembolism as well as any associated risk factors in
patients with ovarian, fallopian tube, or primary peritoneal
cancer undergoing neoadjuvant chemotherapy.
METHODS: We conducted a retrospective cohort study
of patients diagnosed with ovarian, fallopian tube, and
primary peritoneal cancer and receiving neoadjuvant
chemotherapy from January 2009 to May 2014 at a single
academic institution. The timing and number of venous
thromboembolic events for the entire cohort were
categorized as follows: presenting symptom, during
neoadjuvant chemotherapy treatment, after debulking
surgery, and during adjuvant chemotherapy.
RESULTS: Of the 125 total patients with ovarian cancer
undergoing neoadjuvant chemotherapy, 13 of 125 pa-
tients (10.4%, 95% confidence interval [CI] 6.1–17.2%)
had a venous thromboembolism as a presenting symp-
tom and were excluded from further analysis. Of the 112
total patients at risk, 30 (26.8%, 95% CI 19.3–35.9%)
experienced a venous thromboembolism. Based on the
phase of care, 13 (11.6%, 95% CI 6.8–19.1%) experienced
a venous thromboembolism during neoadjuvant chemo-
See related editorial on page 971.
From the Division of Gynecologic Oncology and the Institute for Healthcare
Policy and Innovation, University of Michigan, Ann Arbor, and the Department
of Obstetrics and Gynecology, St. John Hospital, Detroit, Michigan; and the
Division of Gynecologic Oncology, University of Wisconsin, Madison, Wisconsin.
Presented as a poster at the Annual Meeting on Women’s Cancer, Society of
Gynecologic Oncology, March 19–22, 2016, San Diego, California.
Each author has indicated that he or she has met the journal’s requirements for
authorship.
Corresponding author: Shitanshu Uppal, MBBS, University of Michigan, 1500
E Medical Drive, Ann Arbor, MI 48109; email: uppal@med.umich.edu.
Financial Disclosure
The authors did not report any potential conflicts of interest.
© 2017 by The American College of Obstetricians and Gynecologists. Published
by Wolters Kluwer Health, Inc. All rights reserved.
ISSN: 0029-7844/17
VOL. 0, NO. 0, MONTH 2017
Copyright Ó by The American College of Obstetricians
and Gynecologists. Published by Wolters Kluwer Health, Inc.
Unauthorized reproduction of this article is prohibited.
MBBS
therapy, six (5.4%, 95% CI 2.4–11.5%) developed a
postoperative venous thromboembolism, and 11
(9.9%, 95% CI 5.5–17%) developed a venous thrombo-
embolism during adjuvant chemotherapy. Two of the
four patients with clear cell histology developed
a venous thromboembolism in this cohort.
CONCLUSION: Overall new diagnosis of venous throm-
boembolism was associated with one fourth of the
patients undergoing neoadjuvant chemotherapy for
ovarian cancer with nearly half of these diagnosed during
chemotherapy cycles before interval debulking surgery.
Efforts to reduce venous thromboembolism so far have
largely focused on the postoperative period. Additional
attention to venous thromboembolic prophylaxis during
chemotherapy (neoadjuvant and adjuvant) in this patient
population is warranted in an effort to decrease the rates
of venous thromboembolism.
(Obstet Gynecol 2017;0:1–7)
DOI: 10.1097/AOG.0000000000001980
P
atients with ovarian cancer have a 10–22% incidence
of venous thromboembolism.1,2 Previously identi-
fied risk factors include obesity, age older than 65 years,
histology, advanced stage, CA 125 greater than 500,
debulking surgery, and the use of antiangiogenic
agents.1,2 Thromboembolism in malignancy is also asso-
ciated with lower survival and poor quality of life.3,4 It is
unclear whether venous thromboembolism is causally
related to a reduction in overall survival or reflects
a higher tumor burden, more aggressive tumor biology,
or both. Nevertheless, preventing thromboembolism is
of paramount importance to avoid short- and long-term
complications. In addition to the perioperative thrombo-
embolic prophylaxis, prolonged prophylaxis is becom-
ing a standard of care in women with ovarian cancer.
Recent studies show decreased thromboembolic events
in patients receiving prolonged postoperative prophy-
laxis for 4 weeks.5,6
OBSTETRICS & GYNECOLOGY 1
 However, studies have shown a continued risk of
venous thromboembolic events well beyond the
perioperative and prolonged prophylaxis periods.
During adjuvant chemotherapy, venous thromboem-
bolism occurs in up to 12.5% of the patients.7 These
data suggest that active ovarian cancer is a hypercoag-
ulable state. Despite multiple studies examining the
perioperative and postoperative phases of care in
women with ovarian cancer, the rates of thromboem-
bolism in patients undergoing neoadjuvant chemo-
therapy remain unknown. The recommended initial
treatment for patients with advanced-stage ovarian
cancer is surgical debulking followed by adjuvant plat-
inum and taxane chemotherapy.8 However, patients
with high likelihood of not achieving optimal debulk-
ing or high surgical morbidity frequently receive neo-
adjuvant chemotherapy.8,9 Given that these factors
influencing the choice of neoadjuvant chemotherapy
have all been associated with increased risk of throm-
boembolism, we hypothesized that patients receiving
neoadjuvant chemotherapy have a high rate of venous
thromboembolism.
MATERIALS AND METHODS
We performed a descriptive retrospective cohort
study of women diagnosed with ovarian, fallopian
tube, or primary peritoneal cancer at the University of
Michigan from January 1, 2009, to May 31, 2014.
These dates were selected based on a 5-year time-
frame calculated from the time of institutional review
board approval of this study. Individual patient
electronic medical record review and data collection
were carried out using the University of Michigan
Health System Electronic Medical Record Search
Engine patient data search engine.10 Study data were
collected and managed using Research Electronic
Data Capture electronic data capture tools hosted at
the University of Michigan Medical School.11
STrengthening the Reporting of OBservational stud-
ies in Epidemiology guidelines were used.12 The insti-
tutional review board of the University of Michigan
Health System approved this study (protocol #HUM
00095719).
The primary outcome of this study was the number
and timing of venous thromboembolic events in the
neoadjuvant chemotherapy ovarian cancer patient
population. The secondary objective of our study was
to identify patient or treatment factors associated with
increased risk of venous thromboembolism.
Women 18 years of age or older with ovarian,
fallopian tube, or primary peritoneal carcinoma of
high-grade histology undergoing one or more cycles
of chemotherapy before undergoing debulking
2 Greco et al Venous Thromboembolism During Neoadjuvant Chemotherapy
Copyright Ó by The American College of Obstetricians
and Gynecologists. Published by Wolters Kluwer Health, Inc.
Unauthorized reproduction of this article is prohibited.
surgery were considered as undergoing neoadjuvant
chemotherapy and were included in this report.
Patients seeking a second opinion or those who
underwent surgery at the University of Michigan but
received chemotherapy elsewhere were not included
as a result of concerns of incomplete follow-up and
limited access to detailed medical records from outside
hospitals. For this study, we categorized age as younger
than 65 years or 65 years or older, race as white
compared with nonwhite, and tobacco use as having
smoked within the prior year or not. Date of diagnosis,
date of recurrence, date of the last contact, and vital
status were recorded.
Medical comorbidities were abstracted from the
medical chart and the Charlson comorbidity score
was calculated.13 Comorbidities included in the
Charlson score are diabetes mellitus (categorized as
diet-controlled, noninsulin-dependent, or insulin-
dependent), hypertension (if previously diagnosed or
multiple recorded blood pressure readings greater
than 140/90 mm Hg), obesity (categorized as nonob-
ese if body mass index [calculated as weight (kg)/
[height (m)]2] less than 30 or obese if body mass index
30 or greater), history of cardiovascular-related
issues (including congestive heart failure, myocardial
infarction, percutaneous coronary intervention, and
peripheral vascular disease), neurovascular diseases
(including transient ischemic attack and cerebrovascu-
lar accidents with or without neurologic deficit),
chronic obstructive pulmonary disease, chronic kid-
ney disease, and the functional status of the patient
(categorized as dependent or independent with regard
to performance of basic activities of daily living). Dis-
ease histology was categorized as serous, endome-
trioid, clear cell, mucinous, or other. The primary
tumor site was recorded as ovarian, fallopian tube,
or primary peritoneal. CA 125 levels were recorded
at multiple time points, which included: 1) initial diag-
nosis, 2) after the completion of neoadjuvant chemo-
therapy, 3) postoperatively, and 4) postadjuvant
chemotherapy. Imaging data were reviewed and dis-
ease distribution was dichotomized based on the loca-
tion of the tumor seen on the images as follows: upper
abdomen disease (transverse colon, stomach, liver,
liver parenchyma, intraparenchymal hepatobiliary
system, diaphragm), mid- and lower abdominal dis-
ease (small bowel and corresponding mesentery), the
presence of ascites (categorized as minimal or moder-
ate to significant), and the presence or absence of
omental disease. The stage of the cancer was re-
corded. Residual disease at the time of interval cytor-
eduction was defined as microscopic, less than 5 mm,
5–10 mm, 11–20 mm, or greater than 20 mm.
OBSTETRICS & GYNECOLOGY
Chemotherapy regimen, route of administration, the
platinum sensitivity of the chemotherapy treatment,
and the timing of any blood transfusions were
recorded.
The number and timing of venous thromboem-
bolic events were placed in one of four time periods:
venous thromboembolism before neoadjuvant che-
motherapy (at the time of diagnosis), venous throm-
boembolism development during neoadjuvant
chemotherapy before interval cytoreductive surgery,
postoperatively (from the time of cytoreduction until
reinitiating chemotherapy), or during adjuvant che-
motherapy after surgery. Patients were diagnosed with
a venous thromboembolism by either a computed
tomography scan or Doppler ultrasonography. Pa-
tients with venous thromboembolic disease at the time
of presentation were excluded from further analysis
because they were already on full anticoagulation
before initiation of neoadjuvant chemotherapy.
Throughout the study, all patients received sequential
compression devices and subcutaneous heparin dur-
ing their hospitalization postoperatively. The institu-
tional policy of prolonged postoperative prophylaxis
started at the University of Michigan Hospitals mid-
way through the study period. Therefore, data collec-
tion included whether the patient received prolonged
prophylactic anticoagulation postoperatively for 28
days after discharge from the hospital. The Khorana
score is a risk assessment tool used by medical
oncologists for predicting venous thromboembolism
during outpatient adjuvant chemotherapy.14,15 This
model is relatively simple and contains parameters
that are easily obtained during a routine outpatient
evaluation for oncology patients. This score uses
hemoglobin level, platelet count, and white blood cell
count at the time of initial diagnosis along with tumor
histology to assign a patient’s risk of a venous throm-
boembolic event during chemotherapy.14 To examine
whether this model could serve as a predictor in our
study cohort, these laboratory values were collected at
each time point and the Khorana score was calculated
for each patient.
Descriptive analyses of the patient information
were performed. Pearson x2 tests and Fisher exact test
were used for categorical variables. Multivariable
regression modeling and predictive analyses were
not performed as a result of low sample size.
RESULTS
Six hundred twenty patients with ovarian cancer were
identified in the study period. Of these, 161 patients
received neoadjuvant chemotherapy and 36 of these
patients were excluded because they did not receive
their care primarily at the University of Michigan. Of
the remaining 125 patients who received neoadjuvant
chemotherapy primarily at the institution of study, 13
patients (10.4%, 95% confidence interval [CI] 6.1–
17.2%) had a venous thromboembolism before or at
the time of diagnosis. These patients were excluded
from further analysis, leaving 112 patients in the final
cohort who had the potential for a new venous throm-
boembolism during their cancer care and met all
inclusion criteria (Fig. 1).

Fig. 1. Study flow diagram. VTE, venous thromboembolism.

Greco. Venous Thromboembolism During Neoadjuvant Chemotherapy. Obstet Gynecol 2017.

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Unauthorized reproduction of this article is prohibited.
 An overview of the timing and incidence of
venous thromboembolism at three different time
points is provided in Figure 1. Of the 112 total pa-
tients at risk, 30 (26.8%, 95% CI 19.3–35.9%) experi-
enced a venous thromboembolism. Based on the
phase of care, 13 (11.6%, 95% CI 6.8–19.1%) experi-
enced a venous thromboembolism during neoadju-
vant chemotherapy (with one death as a result of
venous thromboembolism), six (5.4%, 95% CI 2.4–
11.5%) developed a postoperative venous thrombo-
embolism, and 11 (9.9%, 95% CI 5.5–17%) developed
a venous thromboembolism during adjuvant chemo-
therapy. The mean age of the patients who developed
a clot during neoadjuvant chemotherapy was 70.1
(613.4) years. Eight patients had serous histology;
10 were white, 11 were nonsmokers, and nine were
nonobese. Moderate to significant ascites was present
in 7 of the 13 patients. Upper abdominal disease was
present in 10 of the 13 patients as was omental disease
on initial diagnostic imaging. None of the patients in
this cohort had a medical history of venous thrombo-
embolic disease.
Figure 2 provides a more detailed analysis of the
timing of venous thromboembolism. Patients receiv-
ing prolonged postoperative prophylaxis for 28 days
after discharge had a lower postoperative venous
thromboembolic event rate compared with those not
receiving prolonged prophylaxis. From the 112 at-risk
patients, there were only four patients with clear cell
histology, but two of them developed a venous throm-
boembolism during neoadjuvant chemotherapy. The
rate of thromboembolism in those with nonclear cell
histology was 9.4% (10/107). On the univariate anal-
ysis, there were no predictors of venous thromboem-
bolism identified for patients undergoing interval
debulking after receiving neoadjuvant chemotherapy
(Table 1).
DISCUSSION
Our data demonstrate that one in four patients
undergoing neoadjuvant chemotherapy developed
a new venous thromboembolism throughout the
timeframe of initial treatment of their cancer. Specif-
ically, 1 in 10 patient developed a venous thrombo-
embolism during neoadjuvant chemotherapy, an
additional 10% during adjuvant chemotherapy after
debulking surgery and the remainder during the
postoperative phase. These data are important for
several reasons: 1) we observed a venous thrombo-
embolism rate similar to previously reported in the
adjuvant chemotherapy phase of care (approximately
10%). However, a similar percentage of patients
experiencing thromboembolic events before surgery
4 Greco et al Venous Thromboembolism During Neoadjuvant Chemotherapy
Copyright Ó by The American College of Obstetricians
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during neoadjuvant chemotherapy has not been pre-
viously reported; 2) despite a low incidence of post-
operative thromboembolism after hysterectomy
(approximately 2%), prevention of venous thrombo-
embolic disease in the perioperative phase is currently
considered a quality-of-care indicator.16,17 In compar-
ison, our data show that the rate of thromboembolism
during neoadjuvant and adjuvant chemotherapy is
greater than 10%. Based on these data, we recom-
mend that randomized controlled trials of prophylac-
tic anticoagulation during neoadjuvant and adjuvant
chemotherapy in ovarian cancer should be strongly
considered.
Overall, venous thromboembolism complicated
the treatment of one fourth of the patients undergoing
neoadjuvant chemotherapy. This is in comparison
with previous reports that have demonstrated an
overall incidence of venous thromboembolism of
approximately 22% in patients with ovarian cancer.1,2
The clinical decision to administer neoadjuvant che-
motherapy is generally influenced by the high tumor
burden and patient frailty. Because these two factors
are also the risk factors for developing thromboem-
bolic disease, it is unsurprising that the incidence of
venous thromboembolism was higher in this cohort.
Additionally, although we only had four patients with
clear cell histology, two (50%) developed a venous
thromboembolism during neoadjuvant chemother-
apy. These results are similar to previous studies in
patients with ovarian cancer in whom clear cell histol-
ogy has been associated with higher risk of venous
thromboembolism.2,18
Previous studies, in other malignancies, examining
the risk of thromboembolism during neoadjuvant
chemotherapy have shown similar results as the current
study. In esophageal cancer, the incidence of venous
thromboembolism during neoadjuvant chemotherapy
is 12.5%.19 Similarly, in transitional cell carcinoma of
the urinary bladder, 25% of the patients receiving
platinum-based chemotherapy developed thromboem-
bolic disease (Botten J, Sephton M, Tillett T, Masson S,
Thanvi N, Herbert C, et al. Thromboembolic events
with cisplatin-based neoadjuvant chemotherapy for
transitional cell carcinoma of urinary bladder [abstract].
J Clin Oncol 2013;31(suppl 6):277.). In rectal cancer,
patients receiving neoadjuvant chemotherapy concur-
rently with radiation had an overall 13% incidence of
thromboembolic events.20 These consistently high
numbers of thromboembolic events in several cancer
sites further suggest that patients receiving neoadjuvant
chemotherapy have a very high risk of developing clots.
After the institutional policy of prolonged post-
operative prophylaxis was started at the University of
OBSTETRICS & GYNECOLOGY
Fig. 2. Detailed demonstration of timing and number of thromboembolic events throughout the course of therapy for
patients with ovarian cancer undergoing neoadjuvant chemotherapy. VTE, venous thromboembolism.
Greco. Venous Thromboembolism During Neoadjuvant Chemotherapy. Obstet Gynecol 2017.

Michigan Hospital, we observed a reduction in the
rate of thromboembolic events in the postoperative
setting (6.2% compared with 2.9%). Because our study
was not powered to detect the efficacy of prolonged
prophylaxis, we are unable to comment on the
efficacy of this intervention from these data. However,
recent data from other studies support the use of
prolongation of postoperative prophylaxis to 4 weeks
in patients with ovarian cancer who undergo debulk-
ing surgery.6 The institution of this policy midway
through our study period does not affect the main
finding of our study, which is the high rate of venous
thromboembolism during neoadjuvant chemother-
apy. Based on these data, as a quality measure, we
propose that the institutional-level metrics of the
cumulative incidence of thromboembolic disease, in

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Table 1. Patient Demographics During Neoadjuvant Chemotherapy, With Patients Categorized by Who
Did and Did Not Experience a Venous Thromboembolism Before Interval Debulking Surgery

No Venous Thromboembolism Venous Thromboembolism

Patient Characteristic (n599) (n512) P

Age (y) .761

Younger than 65 40 (91) 4 (9)
65 or older 59 (88) 8 (12)
BMI (kg/m2) 1.000
Nonobese 70 (88.6) 9 (11.4)
Obese 29 (90.6) 3 (9.4)
Race .631
White 88 (89.8) 10 (10.2)
Nonwhite 11 (84.6) 2 (15.4)
Smoker 1.000
No 86 (88.7) 11 (11.3)
Yes 13 (92.9) 1 (7.1)
No. of comorbidities in the Charlson Comorbidity .758
Index
0 22 (95.7) 1 (4.3)
1 29 (87.9) 4 (12.1)
2 25 (86.2) 4 (13.8)
Greater than 3 23 (88.5) 3 (11.5)
Stage of disease .753
III 63 (90.0) 7 (10.0)
IV 36 (87.8) 5 (12.2)
Khorana scoring .964
Less than 3 25 (89.3) 3 (10.7)
Greater than 3 37 (88.1) 5 (11.9)
Unknown 37 (90.2) 4 (9.8)
Blood transfusion during neoadjuvant .731
chemotherapy
No 77 (89.5) 9 (10.47)
Yes 22 (88.0) 3 (12.0)
Moderate to significant ascites on initial imaging 1.000
No 40 (88.9) 5 (11.1)
Yes 59 (89.4) 7 (10.6)
Omental disease on initial imaging 1.000
No 21 (91.3) 2 (8.7)
Yes 78 (88.6) 10 (11.4)
Upper abdomen disease on initial imaging .134
No 49 (94.2) 3 (5.8)
Yes 50 (84.8) 9 (15.2)
Lower abdomen disease on initial imaging .362
No 49 (86.0) 8 (14.0)
Yes 50 (92.6) 4 (7.4)
History of prior venous thromboembolism NA
No 99 (100) 12 (100)
Yes 0 (0) 0 (0)
Clear cell histology .057
No 97 (90.7) 10 (9.3)
Yes 2 (50) 2 (50)
BMI, body mass index; NA, not applicable.
Data are n (%) unless otherwise specified.
Groups were compared using Fisher’s exact test.
Table excludes one patient who experienced a fatal pulmonary embolism and did not undergo interval debulking.

patients with ovarian cancer, during all phases of care Our study has several limitations worth consid-
(neoadjuvant, postoperative, and adjuvant chemother- ering. First, this is a retrospective study with a rela-
apy) and just the postoperative phase of care should tively small sample size. Factors such as Khorana
be the focus of future studies. score and extensive upper abdominal disease have

6 Greco et al Venous Thromboembolism During Neoadjuvant Chemotherapy OBSTETRICS & GYNECOLOGY

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been previously validated in large cohorts. Given
a small sample size, to prevent type II error, we did
not attempt any predictive analysis of known factors
in our study. Second, the generalizability of our results
may be limited because our study was performed at
a single-institutional tertiary referral center. This
could have led to an overestimation of overall risk
of thromboembolism, because patients in referral
centers tend to have more extensive disease. Third,
the limited sample size also precluded us from
performing meaningful survival analysis. Finally, we
do not compare the rate of venous thromboembolism
in patients with ovarian cancer who did receive
neoadjuvant chemotherapy with those who did not.
That is currently the subject of our ongoing investi-
gation. However, we identified such a high incidence
of venous thromboembolism in the neoadjuvant
chemotherapy cohort that we felt these data needed
to be reported given the lack of literature on this
subject. Despite these limitations, there are several
strengths to our study. The use of a detailed individual
patient medical record review allowed for thorough
analyses. The retrospective nature of the study also
allowed us to identify the temporal sequence and
timing of events with relation to phases of care.
Our study identifies the neoadjuvant chemotherapy
ovarian cancer population as an extremely high-risk
population of developing a venous thromboembolism
during the course of their treatment. Thromboembolic
prophylaxis in these patients may decrease the inci-
dence of venous thromboembolic events and poten-
tially affect overall survival. This becomes especially
relevant because the proportion of patients with ovarian
cancer receiving neoadjuvant chemotherapy is rapidly
increasing in the United States.21
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