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Adnexal masses requiring reoperation in women with previous

hysterectomy with or without adnexectomy§

Linda-Dalal J. Shiber a,1,*, Emily J. Gregory a,2, Jeremy T. Gaskins b, Shan M. Biscette a

a University of Louisville School of Medicine, Division of Minimally Invasive Gynecologic Surgery, Department of Obstetrics and Gynecology, Louisville,

KY 40202, United Statesb University of Louisville School of Public Health and Information Sciences, Department of Bioinformatics and Biostatistics, Louisville, KY, United States

Introduction/background

Hysterectomy is one of the most common surgeries performed

in the United States [1]. It is often viewed by women as a cure, and

the final management option, for many gynecologic complaints.

Despite this widely held belief, it is not uncommon for further

gynecologic surgery to occur following hysterectomy. These

subsequent abdominal surgeries are often associated with

increased risks of intraoperative complications related to adhesive

disease and distortion of anatomy [2–4]. Adnexal or pelvic masses

are common reasons women require further surgery following

hysterectomy and their frequency may depend upon whether

total, partial or no adnexectomy is performed at hysterectomy.

Salpingectomy at thetime of hysterectomy hasemerged as a safe,

low risk technique to decreasethe risk of needing future surgery for

benign adnexal masses and, most importantly, ovarian cancer risk

[5,6]. The Society of Gynecologic Oncology (SGO) states thatwomen

with BRCA1 and 2 mutations receive significant cancer riskreduction if salpingectomy oophorectomy is performed  [7]. Fur-

thermore, in women at average risk for ovarian cancer, salpingectomy

at the time of hysterectomy or even sterilizationcould prove beneficial

andshouldbe offeredroutinely. Thisrecommendation hasbeenechoed

by the American College of Obstetricians and Gynecologists as well [8].

It is accepted that the fallopian tube serves no purpose after the

completion of childbearing, and may incur other risks besides a

potential cancer risk, including ‘hydrosalpinx, tubal pregnancy,

torsion, chronic PID, salpingitis, tubal prolapse, TOA’   [9]. The

incidence of these problems has been examined in several studies.

European Journal of Obstetrics & Gynecology and Reproductive Biology 200 (2016) 123–127

A R T I C L E I N F O

 Article history:Received 9 February 2016

Received in revised form 25 February 2016

Accepted 29 February 2016

Keywords:

Adnexal mass

Pelvic mass

Prior hysterectomy

Prophylactic salpingectomy

Reoperation

Salpingectomy at hysterectomy

A B S T R A C T

Objectives:  To characterize the etiologies of adnexal masses requiring reoperation in women with priorhysterectomyand to compare incidence andpathology of these masses based upon whether total,partial

or no adnexectomy was performed at time of hysterectomy. In addition, the average time interval

between hysterectomy and reoperation for a pelvic mass is ascertained.

Study design:   A single-institution, retrospective review spanning 10 years. Using pertinent ICD-9 and

CPT codes, women with a history of hysterectomy who underwent a subsequent surgery for an adnexal

or pelvic mass were identified.

Results:  Over ten years, 250 women returned for gynecologic surgery due to a pelvic mass after prior

hysterectomy. Most had undergone hysterectomy only (76%). 64.8% of these women had masses of 

ovarian origin, 12.4% were tubal in origin, 20% of masses involved both the ovary and tube and a small

proportion arose from non-gynecologic processes. 18% of these women had a malignancy; 80% were

ovarian and 6.7% originated from the fallopian tube. Patients having had a prior hysterectomy and

bilateral salpingectomy returned soonest ( p< 0.0001) and patients with malignant masses returned

after the longest time intervals (HR 0.41,  p < 0.0001).

Conclusions:  The majority of adnexal masses requiring reoperation after hysterectomy are gynecologic

in origin, benign, and arise from the ovary.Women returning with malignant masses after hysterectomy

present after longer time intervals.

  2016 Elsevier Ireland Ltd. All rights reserved.

§ Thisresearchwas presentedas an oralpresentationat the 82nd Annual Meeting

of the Central Association of Obstetricians and Gynecologists, Charleston, SC,

October 21–24, 2015.

*   Corresponding author at: 2500 Metrohealth Drive, Cleveland, OH 44113,

United States. Tel.:+12167784444.

E-mail address:  lindashiber@gmail.com (L.J. Shiber).1 Present address: Metrohealth Hospital, Division of Minimally Invasive Surgery,

Department of Obstetrics and Gynecology, Cleveland, OH 44109, United States.2 Present address: University of Tennessee, Department of Obstetrics and

Gynecology, Knoxville, TN 37920, United States.

Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology andReproductive Biology

j o u r n a l h o m e p a g e :   w w w . e l s e v i e r . c o m / l o c a t e / e j o g r b

http://dx.doi.org/10.1016/j.ejogrb.2016.02.043

0301-2115/  2016 Elsevier Ireland Ltd. All rights reserved.

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A large Danish historical cohort study found that women who had

hysterectomy without salpingectomy had a more than double risk

of subsequent surgery for tubal disease than women undergoing

bilateral salpingectomy at the time of hysterectomy [10]. Another

study found that women undergoing salpingectomy with hyster-

ectomy had lower rates of all type of infectious morbidity  [11].

Morse et al. found that thelifetimerisk of a woman returningto the

operating room for surgical management of hydrosalpinx after

hysterectomy approached 8%   [12]. A 2014 study reviewing

295 patients demonstrated a higher incidence of benign adnexal

pathologies in women who had not had prophylactic salpingect-

omy (26.9%), versus those who had undergone prophylactic

bilateral salpingectomy (13.9%,  p  = 0.02) [13].

Conversely, the risks associated with salpingectomy are low.

Arguments that removing the fallopian tube might decrease

ovarian blood supply and thereby precipitate premature ovarian

failure have been dispelled by multiple studies [14–16]. Salpin-

gectomy at the time of hysterectomy adds minimal time to the

procedure and is not associated with a significant increase in blood

loss or length of hospital stay  [9]. A recent study examining cost

and ovarian cancer risk reduction of salpingectomy at hysterecto-

my versus hysterectomy alone and hysterectomy + BSO found that

performing salpingectomy at time of hysterectomy was less costly

and provided greater reduction in risk  [17].These findings indicate the benign practice of salpingectomy at

time of hysterectomy may decrease future need for gynecologic

surgical intervention with no significant risks to the patient,

certainly when compared with the morbidity associated with

additional surgery. A small Pakistani study performed in

2004 underlined the significant risks posed to women presenting

for repeat pelvic surgery status post hysterectomy. This retrospec-

tive review spanning 3 years found that 43 women with a prior

hysterectomy returned with adnexal masses and 19 required

further surgery. The majority of lesions were ovarian in origin and

benign; 32% were malignant and 16% were related to dilatation of 

the fallopian tube. In addition, complication rates during and after

reoperation were high, with two women suffering small bowel

injuries, two post-operative wound infections and one deep veinthrombosis post-operatively [18].

At our academic institution, patients with complex gynecologic

pathology including malignancies and post-hysterectomy adnexal

masses are often referred from outside facilities for surgical

management. These complex cases pose a challenge for even

seasoned gynecologic surgeons and incur risk to the patient as well

as increased healthcare costs. The practice of performing bilateral

salpingectomy at the time of hysterectomy was adopted early at

this hospital, however many of thewomenreturning with complex

masses underwent hysterectomy at other institutions and return

after varying time intervals, making it difficult to estimate the

effects of our change in practice over time.

This study, thus, aims to review the cases of all women

presenting to our institution for surgical management of anadnexal mass after a prior hysterectomy. The primary objective is

to characterize the etiologies (gynecologic versus non-gynecologic,

benign versus malignant) of these masses and to compare

incidence and pathology in terms of whether total, partial or no

adnexectomy was performed previously. Secondarily, the average

time interval between hysterectomy and reoperation for a pelvic

mass, stratified by pathologic diagnosis and extent of previous

surgery, is ascertained.

We hypothesize that amongst women undergoing reoperation

for adnexal masses post-hysterectomy, most will have undergone

hysterectomy alone without unilateral/bilateral adnexectomy or

salpingectomy. We postulate that most masses will be benign and

of ovarian origin and that the smallest subgroups of women

requiring reoperation will be comprised of women with prior

bilateral salpingo-oophorectomy or bilateral salpingectomy, sup-

porting the effects of removal of fallopian tubes on the risk of 

future reoperation.

Materials and methods

A single-institution, retrospective review spanning 10 years,

2003–2013, was performed at University of Louisville Hospital, an

urban, academic institution. This hospital serves as a state-wide

referral center for women with complicated gynecologic surgical

needs, including gynecologic malignancies. A fair proportion of the

patient population does not present for regular health mainte-

nance exams and many return with advanced, complicated

adnexal masses.

For this review, expedited IRB approval was obtained

(IRB#14.0640). Using pertinent ICD-9 and CPT codes correspond-

ing to surgery for benign and malignant adnexal pathology

(789.39, 789.30, 614.1, 614.2, 620.8, 620.9, and 620.2 and

58700, 58720, 58661, 49320, 49322, and 58862, respectively), a

medical record query was performed to identify women with a

history of hysterectomy who underwent a subsequent surgery for

an adnexal or pelvic mass.

Women whowere eligible forthis study were those with a prior

hysterectomy who had subsequently undergone reoperation for anadnexal mass at University of Louisville from the years 2003 to

2013. Women undergoing surgery for an adnexal mass without a

previous hysterectomy, unavailable operative or pathology reports

from reoperation and any cases occurring outside of above date

range were excluded from the study.

After medical records compiled a list of patients meeting the

above criteria and diagnosis codes, charts were reviewed for

presenting complaints, surgical findings, pathology reports and

surgical history. The remaining women were divided into groups

based upon whether they had previously undergone hysterecto-

my alone, hysterectomy plus bilateral salpingo-oophorectomy

(hyst + BSO), hysterectomy plus unilateral salpingo-oophorecto-

my (hyst + USO) or hysterectomy plus bilateral salpingectomy

(hyst + BS). The indication for hysterectomy and time intervalbetween hysterectomy and reoperation were collected when

available.

Statistical analysis was performed by a statistician who

regularly collaborates with the department. Differences in time

interval from hysterectomy to reoperation as well as differences in

age at return according to previous surgery type were examined

using the log-rank test and hazard ratios from the Cox survival

model.

Results

Over ten years, 250 women with a previous hysterectomy

presented to this institution with a pelvic mass requiring

additional surgery. The majority had undergone hysterectomyalone (n = 190, 76%). 44 (17.6%) had hysterectomy + USO in the

past, 10 (4%) had hysterectomy + BSO, and 6 (2.4%) had hyster-

ectomy + BS (Table 1, Fig. 1).

Indication for prior hysterectomy was available in 122 (48.8%)

of women with most common surgical indications being abnormal

bleeding (n = 33, 27%) and uterine leiomyoma (n = 30, 24.6%). Of 

the women with a known indication for index hysterectomy, 8

(6.6%) underwent hysterectomy for a gynecologic malignancy.

Upon reoperation, only one of those women had a malignant mass;

6 were benign, 1 was borderline (Table 1).

The majority of adnexal masses arising after hysterectomy and

requiring surgery were benign (n  = 205, 82%) while 18% were

malignant (n = 45). Most masses were ovarian in origin (64.8%) and

these ovarian masses accounted for 63.4% of benign and 80% of 

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malignant masses overall. 12.4% of masses arose from the fallopian

tube and comprised 6.7% of malignant and 12.9% of benign masses.

Masses involving both the fallopian tube and ovary made up 20% of 

reoperations and were responsible for 6.7% of malignancies and

21.6% of benign masses. Other etiologies (n = 2, 0.8%) includedbenign fibroadipose tissue and a vaginal cuff leiomyoma. Non-

gynecologic causes (n = 4, 1.6%) were rare and included 3 cases of 

metastatic cancer (B-cell lymphoma, colon and breast) and a

benign peritoneal inclusion cyst (Table 1).

Age at repeat surgery was compared between women with

malignant, benign or inflammatory masses using the log-rank test.

Median age of women returning with malignant adnexal masses

was significantly higher at 69 years than those with benign/

inflammatory masses [median 48.5 and 44 years, respectively. p< 0.0001]. In addition, age at repeat surgery was different based

upon index surgery type, i.e., hysterectomy alone, hyst + BSO,

hyst + USO, hyst + BS with women having had prior hysterectomy

alone returning at older ages than the other subgroups

[ p < 0.0001]. However, when the age at initial surgery was

considered, there was no significant difference between groups.

The time interval between hysterectomy and subsequent

adnexal mass surgery was examined for differences between

subgroups; year of hysterectomy was available in 174 women.

Using the log-rank test, there was strong evidence that time

interval between hysterectomy and adnexal mass surgery differed

between groups ( p< 0.0001). Patients with a prior hysterectomy

and bilateral salpingectomy returned with adnexal masses

4.6 times sooner than women undergoing hysterectomy alone.Patients who had hysterectomy + BSO and those with hysterecto-

my + USO returned 2.9 and 1.5 times sooner, respectively, than

women in the hysterectomy-only group (Fig. 2). These findings are

likely confounded by the fact that most hysterectomy + BS

surgeries were performed more recently, with a shorter interval

to reoperation. In particular, the median year of initial surgery was

1992 for the hysterectomy-only patients compared to 2001 for

hysterectomy + USO, 2006 for hysterectomy + BSO, and 2008 for

hysterectomy + BS.

Time interval between hysterectomy and reoperation also

differed based upon type of adnexal mass, with women having

malignant masses returning after the longest time intervals (HR 

0.41, p < 0.0001, Fig. 3). There was no evidence of a difference in

return time by mass anatomic origin ( p = 0.296).

 Table 1

Age, time to reoperation, and etiology of masses in patients presenting for surgical management.

Total Hysta only Hyst +USOa Hyst+BSOa Hyst+BSa

N  (% of total) 250 190 (76) 44 (17.6) 10 (4) 6 (2.4)

Mean age at return (SD) 53.4 (15.2) 55.6 (14.9) 47.6 (14.3) 45.8 (17.6) 39.0 (6.8)

Indication for hysterectomy N (% of total subjects)   122 (48.8%) 90 (47.4%) 24 (54.5%) 6 (60%) 2 (33.3%)

Abnormal bleeding 33 (27%) 28 (31.1%) 3 (12.5%) 1 (16.7%) 1 (50%)

Fibroids 30 (24.6%) 25 (27.8%) 5 (20.8%) – –

Prolapse 13 (10.7%) 11 (12.2%) 2 (8.3%) – –

Endometriosis 15 (12.3%) 5 (5.6%) 7 (29.2%) 2 (33.3%) 1 (50%)

Pain 7 (5.7%) 4 (4.4%) 3 (12.5%) – –

Cervical dysplasia 11 (9.0%) 9 (10%) 2 (8.3%) – –

Hemorrhage 2 (1.6%) 2 (2.2%) – – –

Infection 1 (.8%) – – 1 (16.7%) –

Mass 2 (1.6%) – 1 (4.2%) 1 (16.7%) –

Malignancyb 8 (6.6%) 6 (6.7%) 1 (4.2%) 1 (16.7%) –

Reoperation

Years to reoperation [range]c 14 [4–29.75] 20 [7–31] 5 [2–19] 4.5 [3.75–8.25] 1.5 [1–5]

Initial operation date [range]c 1995 [1980–2004] 1992 [1978–2001] 2001 [1990–2006] 2004 [2000–2006] 2008 [2004–2011]

Initial operation date missing (%) 76 (30.4) 59 (31.1) 15 (34.1) 2 (20) 0 (0)

 Tumor type N (%)

Benign 205 (82) 150 (78.9) 41 (93.2) 8 (80.0) 6 (100)

Malignant 45 (18) 40 (21.1) 3 (6.8) 2 (20.0) 0 (0)

Origin N (%)

Ovarian 162 (64.8) 120 (63.2) 29 (65.9) 7 (70) 6 (100)Tubal 31 (12.4) 27 (14.2) 3 (6.8) 1 (10) 0 (0)

Ovarian + tubal 50 (20.0) 39 (20.5) 11 (25) 1 (10) 0 (0)

Other 2 (.8) 1 (.5) 0 (0) 1 (10) 0 (0)

Non-gynecologicd 4 (1.6) 3 (1.6) 1 (2.3) 0 (0) 0 (0)

a Hyst, hysterectomy; hyst+ USO, hysterectomy+ unilateral salpingo-oophorectomy; hyst+ BS, hysterectomy+ bilateral salpingectomy; hyst + BSO, hysterectomy+ bi-

lateral salpingo-oophorectomy.b For women with cancer as indication for hysterectomy, 6/8 masses requiring reoperation were benign, 1/8 was malignant and 1/8 was borderline.c Due to lack of normality, the median and first and third quartiles are shown.d For non-gynecologic masses, 1/4 was benign (peritoneal inclusion cyst), 3/4 were malignant (B-cell lymphoma, colon cancer, breast cancer).

[

Fig. 1. Initial surgery by type and year. Bar graph depicting number of patients who

returned for reoperation by year of their hysterectomy (depicted in 5 year

increments) and type of index surgery (i.e., hysterectomy only, hysterectomy

and unilateral or bilateral salpingo-oophorectomy, hysterectomy and bilateral

salpingectomy).

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Comment

Hysterectomy is often a definitive surgery for women and the

final option for a myriad of pathology. It can be extrapolated that

women undergoing hysterectomy have the expectation they will

not require future surgery for gynecologic problems; however, this

is not necessarily true. In this review, over 10 years, 250 women

with a history of hysterectomy returned with adnexal masses

requiring surgery; only a minority (1.6%) were non-gynecologic in

origin and most masses were benign, arising from ovarian tissue.

It is known that additional surgery is associated with additional

risk related to adhesive disease, anesthesia and preexisting

medical co-morbidities [2–4]. Furthermore, healthcare costs rise

with each surgical intervention. If gynecologic surgeons can reduce

the likelihood of a subsequent surgery with benign intervention atthe time of hysterectomy, this can make a great difference in risk

reduction and cost.

Bilateral salpingectomy at the time of hysterectomy has been

advocated in recent years as an intervention that can provide

benefitin decreasing the risk of serous carcinomaas well as benign

pathology that may require future surgery [5–14]. This procedure

hasbeen shown to be efficient andsafe, adding minimal procedural

time and virtually no risk [15–17].

In our cohort, only six women with bilateral salpingectomy at

the time of hysterectomy returned with adnexal masses requiring

reoperation; all of those masses were benign ovarian remnants.

This is in contrast to the 190 women with prior hysterectomy

alone, 40 of whom returned with malignant adnexal masses.

This study is the second to examine the causes for post-

hysterectomy adnexal masses requiring surgery and the first to

stratify reoperation incidence based upon whether the adnexa

were completely or partially resected. One prior review, spanning

only three years and examining a non-US population, looked at the

pathologic etiologies of pelvic masses in women after prior

hysterectomy   [18]. That study predated the consensus that

fallopian tube removal with hysterectomy should be considered

for all women.

The limitations of this study are centered upon its retrospective

nature and the presence of unidentified confounding factors that

may have impacted our findings. First, it was not possible to

identify a baseline ‘n’ representing the total number of women

undergoing hysterectomy against which we might compare the

percent of women returning for reoperation for adnexal masses.

Many women undergoing reoperation at our hospital hadhysterectomies at other institutions and/or decades prior. We

therefore cannot quote a percent risk of requiring future surgery

based upon whether bilateral, unilateral or partial adnexectomy is

performed at time of hysterectomy.

Secondly, the number of women returning for surgery in the

hysterectomy + bilateral salpingectomy group was very small. This

may reflect a decreased risk for future surgery among that cohort

or it may simply indicate an insufficient time interval since this

practice was adopted to truly evaluate how many women will

return with adnexal masses in the future.

Despite the intrinsic limitations of our retrospective study, we

believe our findings have implications for hysterectomy care and

patient counseling. This study provides additional information

regarding what brings women back for gynecologic surgeryfollowing hysterectomy and this is important in discussing the

long term benefits and risks of hysterectomy with no, partial or

bilateral adnexectomy. It is interesting to find that the majority of 

our cohort undergoing reoperation after hysterectomy had benign

masses that were ovarian in origin. Though routine salpingectomy

at hysterectomy can decrease the potential risk of repeat surgery

for masses of tubal origin, based on our findings, it is unlikely to

affect the majority of future reoperations for post-hysterectomy

adnexal masses. That said, we agree with current guidelines and

support routine salpingectomy at hysterectomy as a strategy to

decrease later occurrence of benign pathology as well as ovarian

cancer   [7,8]. We believe that future, prospective research is

necessary to examine the long-termeffects, potential for decreased

re-operative morbidity and healthcare cost savings of this changein practice.

Conflict of interest

The authors report no conflict of interest

Funding 

No funding sources for this study.

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[

Fig. 2. Median time interval from index surgery to reoperation. Bar graph showing

median time in years between hysterectomy and reoperation, grouped by type of 

index surgery and type of pelvic mass.

[

Fig. 3. Median time interval from index surgery to reoperation by mass type. Bar

graph showing median time in years between hysterectomy and reoperation,

grouped by type of pelvic mass only.

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