Review Article

The Effect of Salpingectomy on Ovarian Function

Alexander Kotlyar, MD*, Julian Gingold, MD, PhD, Shirley Shue, MS, and
Tommaso Falcone, MD
From the Department of Obstetrics and Gynecology and Women’s Health Institute, The Cleveland Clinic (Drs. Kotlyar, Gingold, and Falcone), and Case
Western Reserve University School of Medicine (Dr. Shue), Cleveland, Ohio.

ABSTRACT Tubal surgery is performed for a variety of indications in gynecology. Salpingectomy is the most aggressive form of tubal
surgery and may be performed for potential risk reduction for epithelial ovarian cancer, sterilization, and ectopic pregnancy
and as a method to enhance fertility in the setting of hydrosalpinx. Depending on the indication, alternatives include conser-
vative therapy alone, tubal occlusion, and salpingostomy. However, aggressive tubal surgery may impact fertility and ovarian
reserve because of its effects on adjacent ovarian tissue. Ovarian damage may manifest as alterations in serum and sono-
graphic markers of ovarian function as well as in vitro fertilization (IVF) response and, ultimately, impair outcomes in assisted
reproductive and spontaneous conception cycles. We performed a review of articles from PubMed, Cochrane, and MEDLINE
from 1946 to 2016 and included 48 relevant publications. For most indications for salpingectomy, ovarian reserve is not
impacted. Although there are several conflicting studies suggesting a slight impairment of the parameters of ovarian reserve,
these studies were mostly in patients who underwent salpingectomy for an ectopic pregnancy. For patients attempting to
conceive naturally, salpingectomy overall does not confer a substantial decrease in conception. Conservative options may in-
crease their risk for persistent trophoblastic disease. In patients planning on IVF, salpingectomy does not appear to signifi-
cantly affect ovarian stimulation parameters or clinical pregnancy rates. Furthermore, salpingectomy is recommended in
cases of hydrosalpinx. Overall, salpingectomy has no significant effects on ovarian reserve. However, the impact on IVF suc-
cess and spontaneous pregnancy rates must be weighed by the indication for possible salpingectomy. A review of these risks
and benefits should aid in choosing between salpingectomy and less aggressive alternatives. Journal of Minimally Invasive
Gynecology (2017) 24, 563–578 Ó 2017 AAGL. All rights reserved.
Keywords: Antim€ullerian hormone; Antral follicle count; Epithelial ovarian cancer; Follicle-stimulating hormone; Hydrosalpinx; Ovarian function;
Ovarian hyperstimulation; Ovarian reserve; Salpingectomy

Salpingectomy (i.e., the removal of all or some of the fal-
lopian tube) is performed for various indications in current
gynecologic practice. This includes ectopic pregnancy
with rupture, gross hemoperitoneum, or if medical manage-
ment is unlikely to cause resolution [1]. Patients may un-
dergo salpingectomy as a form of sterilization, in addition
to the common alternatives of banding, ligation, and electro-
coagulation. Salpingectomy may also be indicated to
enhance fertility if any hydrosalpinx has been discovered
[1]. More recently, it has been used as a prophylactic mea-
sure to reduce the risk for epithelial ovarian cancer, which
The authors declare that they have no conflict of interest.
Corresponding author: Alexander Kotlyar, MD, The Cleveland Clinic, 9500
Euclid Ave, Ste A81, Cleveland, OH 44195.
E-mail: kotlyaa@ccf.org
Submitted November 8, 2016. Accepted for publication February 13, 2017.
Available at www.sciencedirect.com and www.jmig.org
1553-4650/$ - see front matter Ó 2017 AAGL. All rights reserved.
http://dx.doi.org/10.1016/j.jmig.2017.02.014
appears to derive from the fallopian tube and endometrium
rather than the ovary [2–6].
Given the increasing incidence of salpingectomy during
gynecologic surgery as well as the availability of less aggres-
sive surgical alternatives for many indications, a comprehen-
sive assessment of its effects on ovarian function is
warranted. This question is especially important for younger
patients still seeking fertility or those at risk for early meno-
pause. The fallopian tubes derive their blood supply from
branches of the uterine and ovarian arteries. Therefore, sal-
pingectomy may potentially diminish collateral blood flow
to the ovaries [7]. In addition, lateral thermal spread from
electrocoagulation on the tubes as well as surgical manipu-
lation of ovarian tissue may lead to direct ovarian damage.
Therefore, we sought to review the current literature on sal-
pingectomy and its effects on ovarian function, which
include measures of ovarian reserve and ovulation. The
direct consequences of salpingectomy will be assessed in
564
the context of both spontaneous conception and assisted
reproductive cycles.
Methods
A search was performed in PubMed, the Cochrane Li-
brary, and Ovid MEDLINE. Phrases used in the search
were suited for each individual database and included ‘‘sal-
pingectomy AND ovarian reserve,’’ ‘‘salpingectomy AND
AMH,’’ ‘‘salpingectomy AND FSH,’’ ‘‘salpingectomy
AND antral follicle count,’’ ‘‘salpingectomy AND fertility,’’
‘‘salpingectomy AND IVF,’’ ‘‘salpingectomy AND ovarian
hyperstimulation,’’ ‘‘salpingectomy AND oocyte,’’ ‘‘salpin-
gectomy AND tubal occlusion,’’ and ‘‘salpingectomy AND
menopause.’’ Our search period spanned from 1946 to
2016. Two hundred forty-nine articles were found. These ar-
ticles were then assessed for relevance and quality by the au-
thors. Only studies published in English were included.
Forty-eight of these articles were included as part of this re-
view. A manual review of the references in each of the cited
sources was performed to ensure that any relevant resource
was not excluded.
The primary outcome of this review was to determine if
salpingectomy performed for any of the aforementioned rea-
sons affected ovarian reserve. Markers for ovarian reserve
included serum concentrations of antim€ ullerian hormone
(AMH), basal follicle-stimulating hormone (FSH), and
antral follicle count (AFC). Secondary outcomes were indi-
rect measures of ovulatory function and capacity, including
pregnancy and live birth rates in natural and ART (assisted
reproductive technologies) cycles as well as in vitro fertiliza-
tion (IVF)-specific parameters (e.g., gonadotropin dose,
duration of stimulation, and oocytes retrieved) and timing
of menopause.
Articles were selected as relevant if they were (1) pro-
spective or retrospective studies or meta-analyses involving
reproductive-age women who underwent bilateral or unilat-
eral salpingectomy for benign indications and (2) reported
AMH levels, baseline AFC, FSH levels, IVF cycle character-
istics (e.g., number of follicles, oocytes retrieved, and fertil-
ized embryos), and clinical pregnancy or live birth rates.
Studies were excluded if they were (1) case reports, system-
atic reviews, abstracts, or expert opinion articles; (2) did not
include an analysis of patients who underwent salpingec-
tomy; (3) included patients who underwent any gonadotoxic
therapy such as chemotherapy; (4) included patients who
had any active genital or gonadal infectious or inflammatory
processes; or (5) did not involve humans or used any animal
or in vitro models.
Results
The systematic literature search yielded 249 articles.
Only 48 of these articles met the inclusion criteria (Fig).
These articles are outlined by author, study type, indications,
outcomes, strengths, weaknesses, and findings (Tables 1–3).
Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017
Nearly all of the salpingectomies were performed lapa-
roscopically. Over a quarter of the articles were randomized
controlled trials. The remainder were retrospective and pro-
spective cohort studies. Two case-control studies were
included with 1 case series.
Salpingectomy and Ovarian Reserve
One major concern is that salpingectomy may inadver-
tently damage the ovarian reserve and affect the hormonal
milieu required for normal ovulation and pregnancy mainte-
nance. The purpose of ovarian reserve testing, according to
the American Society for Reproductive Medicine, is to
determine who is at risk of diminished ovarian reserve. Pa-
tients with diminished ovarian reserve are defined as those
who have regular menses but produce a limited response
to ovarian stimulation and have reduced fecundity [8]. Per
the American Society for Reproductive Medicine, the most
reliable markers of ovarian reserve are AMH and AFC.
Basal FSH, inhibin B, and the clomiphene citrate challenge
test have more limited reliability [8]. Coagulation of the
blood supply in the mesosalpinx during salpingectomy
may impact collateral blood flow to the ovaries or directly
damage ovarian tissue by lateral thermal spread [9].
Severing the common blood supply during surgery could
decrease ovarian perfusion and negatively impact steroid
production and follicular development within the ovary [9].
Although there is no accepted direct measure of
‘‘ovarian damage,’’ several surrogates of ovarian reserve
that are known to change with age have also been shown
to change after exposure to gonadotoxic surgery or drugs.
For example, unilateral salpingo-oophorectomy or cystec-
tomy for ovarian endometrioma significantly decreased
AMH (254% and 266%, respectively; p 5 .001) but
not FSH or AFC [10]. Similar findings were observed after
endometrioma excision [11].
The potential harm from salpingectomy, if any, is more
challenging to detect, in part because the damage is inher-
ently more subtle. The effect of salpingectomy alone was
compared with other forms of adnexal surgery in a retrospec-
tive cross-sectional cohort of over 3000 women, of whom
138 underwent salpingectomy, 36 underwent unilateral
salpingo-oophorectomy, and 40 underwent cystectomy for
endometrioma. Using statistical regression, the study found
that salpingectomy appears to have no appreciable impact on
ovarian reserve compared with untreated women as
measured by changes in AMH, AFC, and FSH [12]. Wide
excision of the mesosalpinx at the time of prophylactic bilat-
eral salpingectomy also appeared to have no effect on AMH,
AFC, or FSH compared with standard salpingectomy [12].
AMH was comparable between patients undergoing IVF
who had salpingectomy compared with controls with
blocked tubes who did not undergo salpingectomy [13].
Similar findings were observed in a randomized
controlled trial (RCT) that evaluated the effect of prophylac-
tic salpingectomy at the time of abdominal hysterectomy.
Kotlyar et al. Effect of Salpingectomy on Ovarian Function 565

Fig
Study assessment flow diagram.

Records idenfied through Addional records idenfied

database searching through other sources
(n = 568 ) (n = 0 )

Records aer duplicates removed

(n = 446 )

Records excluded: case

Records screened reports, expert opinion,
(n = 446 ) systemac reviews
(n = 197)

Full-text arcles assessed Full-text arcles excluded,

for eligibility with reasons: Did not
(n = 249 ) include an analysis of
paents that underwent
salpingectomy, included
paents that underwent
Studies included in any gonadotoxic therapy
qualitave synthesis such as chemotherapy,
(n = 53 ) included paents that had
any acve genital or
gonadal infecous or
inflammatory processes,
Studies included in Did not involve humans or
quantave synthesis ulized any animal or in-
(meta-analysis) vitro models
(n = 0 ) (n = 196 )

The addition of salpingectomy did not significantly impact
FSH, LH (luteinizing hormone), estradiol values, or ovarian
volume [14]. These findings are further supported by a retro-
spective study of 56 patients undergoing unilateral salpin-
gectomy that found no difference in AFC, follicle number,
or the number of oocytes retrieved [15]. Another RCT eval-
uating the effect of opportunistic salpingectomy at the time
of laparoscopic hysterectomy also found no difference in
postoperative AMH in patients randomized to salpingec-
tomy versus no salpingectomy [16], which is consistent
with an earlier pilot study [17]. An open-label prospective
trial of 60 patients undergoing benign hysterectomy with
or without salpingectomy or fimbriectomy found no signifi-
cant differences in FSH, AMH, ovarian volume, ovarian ar-
tery systolic/diastolic ratio, or ovarian artery resistance
index at 6 weeks after surgery [18]. A recent cohort study
of 71 women followed 3 to 5 years after hysterectomy
with prophylactic bilateral salpingectomy found that ovarian
age, which was computed through a model incorporating
AMH, FSH, AFC, and ovarian vascular index and flow,
was not significantly different from a control group of 652
patients with an intact uterus and adnexae [19].
This lack of effect of salpingectomy on AMH levels has
also been further confirmed by a prospective cohort study
of patients undergoing salpingectomy versus methotrexate
versus both treatments for ectopic pregnancy. In this study,
no difference was observed between pretreatment AMH
and the 3-month postoperative AMH level [20]. A separate
meta-analysis also looking at ovarian reserve in patients
involved in ART cycles failed to confirm an association be-
tween salpingectomy and ovarian response to gonadotropin
stimulation in the short-term [21].
However, other studies have reported detectable adverse
effects on the very same markers of ovarian reserve. Ye
et al [22] reported lower AMH (183.48 vs 127.11 fmol/
mL, p % .037) and higher FSH levels (7.85 vs 9.13 mIU/
mL, p 5 .048) in IVF patients under 40 years old with a his-
tory of bilateral salpingectomy compared with controls with
intact tubes. The bilateral salpingectomy patients underwent
surgery for ectopic pregnancy (n 5 24), hydrosalpinx
 566
Table 1
Study summary involving salpingectomy and ovarian reserve

Authors Study design Indications Outcomes Strengths Weaknesses Findings

Orvieto Retrospective Hydrosalpinx Number of developing follicles, Wide variety of Limited sample size and Decreased total follicle number
et al, cohort number of follicles .15 mm on outcomes assessed underpowered for desired and follicles .15 mm in
2011 trigger day, number of oocytes outcomes patients who underwent
retrieved, and number of salpingectomy
transferred embryos
Rustamov Retrospective Various AMH, FSH, and AFC Large sample size and Analysis of retrospective Salpingectomy does not affect
et al, cohort multivariable logistic data AMH, FSH, or AFC
2016 regression analysis
performed
Venturella RCT Prophylactic AMH, FSH, AFC, VI, FI, and VFI Large sample size No multivariable analysis Standard vs wide resection: no
et al, salpingectomy for confounding significant difference in ovarian
2015 reserve or vascular flow
parameters with salpingectomy
Ni et al, Prospective Various AMH and IVF-ET outcome data Comparison of various No analysis for No differences in ovarian reserve
2013 cohort tubal surgery methods confounding of IVF-ET outcomes
Sezik RCT Prophylactic FSH, LH, estradiol value, ovarian No significant difference Small sample size No effect on ovarian reserve but
et al, salpingectomy volume, mean pulsatility index, in baseline data and less of an increase in blood flow
2007 resistance index, and S/D ratio compared preoperative after salpingectomy
and postoperative results
in both patient groups

Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017

Demir Retrospective Hydrosalpinx, AFC, controlled ovarian Comparison of outcomes for 2 Small sample size and single No difference in AFC or follicle
et al, cohort ectopic pregnancy hyperstimulation parameters, indications for tubal surgery; center number of retrieved oocytes on
2015 and number of collected patients served as internal operated or nonoperated side
oocytes controls
Song et al, RCT Prophylactic AMH Conducted in multiple No measurement of other No significant difference between
2016 salpingectomy institutions ovarian reserve markers groups
Findley RCT Prophylactic AMH 4–6 weeks and 3 months Prospective, randomized Small sample size and lack No difference in AMH levels at
et al, salpingectomy postoperatively of long-term follow-up any postoperative time point
2013
Naaman Open-label, Hysterectomy alone, AMH, FSH, S/D ratio, and RI in Prospective, multiple Single institution, underpowered, No significant difference in
et al, prospective hysterectomy 1 ovarian artery before surgery treatment arms and no long-term follow-up AMH, FSH, or ovarian blood
2016 cohort salpingectomy, and 6 weeks afterward flow parameters
hysterectomy 1
fimbriectomy
Venturella Observation Prophylactic AMH, FSH, AFC, VI, FI, and Prospective, long term follow-up No control for comparison No significant difference in any of
et al, study bilateral VFI all combined into an the parameters up to 3–5 years
2017 salpingectomy 1 ovarian age model postoperatively
TLH
(Continued )
 Kotlyar et al.
Table 1

Continued

Authors Study design Indications Outcomes Strengths Weaknesses Findings

Effect of Salpingectomy on Ovarian Function

Sahin Prospective Ectopic Pre- and posttreatment Large sample size and comparison Lack of randomization Decreased AMH 1 month
et al, cohort pregnancy AMH measured of medical treatment to and lack of long term posttreatment; no difference
2016 salpingectomy follow-up at 3 months
Qin et al, Meta-analysis Various AMH, FSH, estradiol, and ovarian 13 studies analyzed Heterogeneity of studies No short-term effects on
2016 volume outcomes; possible long-term
detrimental impact on ovarian
reserve
Ye et al, Retrospective Unspecified AMH, duration of gonadotropin Compared groups with unilateral Small sample size and Lower AMH in women after
2015 cohort therapy, gonadotropin amount, E2 and bilateral salpingectomy underpowered based bilateral salpingectomy
endometrial thickness, oocyte with no surgery on post hoc analysis
number, and viable embryos
Lass et al, Cohort Ectopic Mean ovarian volume, follicle Compared response of both ovaries Small sample size No effect on IVF outcomes after
1998 pregnancy number, oocyte number, embryo after ovarian stimulation for IVF unilateral salpingectomy but
number, endometrial thickness, in same patient fewer follicles and oocytes
peak E2 levels, duration of retrieved from ipsilateral ovary
gonadotropin therapy,
gonadotropin amount, and clinical
pregnancy rate
Grynnerup Cross-sectional Various AMH and number of oocytes Multisite study Limited number of AMH is lower in
et al, retrieved outcomes assessed and salpingectomized patients
2013 no multivariable
analysis
Silva et al, Prospective Ectopic Pregnancy rate Large sample size and life table Lack of randomization No change in pregnancy rates except
1993 cohort pregnancy analysis performed for those with prior tubal damage
Fan et al, Meta-analysis Various Dose gonadotropin, duration of Variety of outcomes and Use of retrospective studies, Salpingectomy led to increased
2016 stimulation, estradiol, number of assessment of publication bias no assessment of AMH, gonadotropin dose and decreased
oocyte retrieved, and basal FSH and heterogeneity of follicles and retrieved oocytes
surgical technique
in studies
Li et al, Retrospective Hydrosalpinx Gonadotropin dose, oocyte Large sample size Retrospective analysis No effect with salpingectomy
2009 cohort retrieved, and implantation
and clinical pregnancy rates
Dubuisson Retrospective Ectopic Intrauterine pregnancy and ectopic Large sample size 30.4% of patients lost No effect with salpingectomy
et al, cohort pregnancy rates to follow-up so long as contralateral tube
1996 is not pathological

AFC 5 antral follicle count; AMH 5 antim€ullerian hormone; E2 5 estradiol; FI 5 flow index; FSH 5 follicle-stimulating hormone; IVF 5 in vitro fertilization; RCT 5 randomized controlled trial; S/D 5 systole/diastole;
VFI 5 vascular flow index; VI 5 vascular index.

567
 568
Table 2
Study summary for salpingectomy and pregnancy outcomes

Authors Study design Indications Outcomes Strengths Weaknesses Findings

Bangsgaard Retrospective cohort Ectopic pregnancy Intrauterine pregnancy
et al, 2003 with questionnaire rate and recurrence rate
of ectopic pregnancy
after surgery
Chan et al, Case series Ectopic pregnancy AFC, ovarian volume,
2003 ovarian blood flow
using 3D power
Doppler indices
Mol et al, 2014 RCT Ectopic pregnancy Intrauterine pregnancy
rate, persistent
trophoblast, repeat
ectopic pregnancy,
ongoing pregnancy
after ovulation
induction, intrauterine
insemination, or IVF
Compared salpingectomy Selection bias may cause Higher intrauterine
(radical surgery) with overestimated pregnancy rate in
salpingostomy pregnancy rates salpingostomy group
(conservative surgery) compared with
salpingectomy group
Assessor measuring No control group and AFC and ovarian blood
outcomes was blinded small sample size flow were significantly
to the treatment the decreased on the
patients received operated side in the
unilateral laparoscopic
salpingectomy group
Large sample size and Study participants were No significant difference
researchers were not masked to their in pregnancy rate
unaware of treatment assigned intervention, between groups and
allocation 20% of salpingotomy increased risk of
group were converted to persistent trophoblast
salpingectomy, and with salpingotomy
varying level of
experience of different

Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017

surgeons
Fernandez RCT Ectopic pregnancy Intrauterine pregnancy Multicenter trial, divided Smaller than expected No significant difference
et al, 2013 rate and ectopic patients into 2 arms: sample size and power between groups
pregnancy recurrence less active vs more ,80%
active ectopic
pregnancies
Lagana et al, Retrospective cohort Ectopic pregnancy IUP, recurrent ectopic Large sample size and up Single-center, No difference in
2016 pregnancy, and to 4 months of follow- retrospective study subsequent IUP rates
persistent trophoblastic up and increased recurrent
disease rate ectopic and persistent
trophoblastic disease
seen in salpingectomy
arm
Strandell et al, Retrospective cohort Hydrosalpinx Pregnancy rate (% of Compared pregnancy rate No analysis of other Pregnancy and delivery
1994 embryo transfers) and and delivery rate after ovarian reserve rates were significantly
delivery rate fresh and frozen function markers and higher in patients
embryo transfer no analysis of surgical without hydrosalpinx
intervention
(Continued )
 Kotlyar et al.
Table 2

Continued

Authors Study design Indications Outcomes Strengths Weaknesses Findings

Effect of Salpingectomy on Ovarian Function

Chanelles Retrospective cohort Hydrosalpinx Clinical pregnancy rate, Compared spontaneous 27% lost to follow-up Salpingostomy should be
et al, 2011 IVF pregnancy, and pregnancy rates and considered in patients
spontaneous pregnancy IVF success in patients with good tubal
receiving prognosis; 20.5% of
salpingostomy vs patients attempting
salpingectomy spontaneous conception
became pregnant after
salpingostomy
Chu et al, 2015 Meta-analysis Hydrosalpinx Clinical pregnancy rate 22 studies with over 2800 Clinical heterogeneity Clinical pregnancy rate
and ectopic pregnancy patients included because of patient after salpingsotomy;
rate characteristics, surgical IVF-ET patient is
technique, and follow- 25.5% at 18 months
up postoperative
Sagoskin et al, Retrospective cohort Hydrosalpinx Spontaneous pregnancy Multicenter study and Small sample size Shorter time to achieve
2003 rate and time to examined time to pregnancy in
pregnancy pregnancy salpingectomy group
compared with
proximal tubal ligation
and no significant
difference in pregnancy
rate

AFC 5 antral follicle count; AMH 5 antim€ullerian hormone; FI 5 flow index; FSH 5 follicle-stimulating hormone; IUP 5 intrauterine pregnancy; IVF 5 in vitro fertilization; IVF-ET 5 in vitro fertilization embryo transfer;
RCT 5 randomized controlled trial; S/D 5 systole/diastole; VFI 5 vascular flow index; VI 5 vascular index.

569
 570
Table 3
Study summary for salpingectomy and in vitro fertilization

Authors Study design Indications Outcomes Strengths Weaknesses Findings

Dechaud et al, RCT Tubal infertility Embryo implantation rate, No significant difference Small sample size and Increased embryo
1998 pregnancy rate, and live between age, duration results not statistically implantation rate and
birth rate of infertility, or interval significant pregnancy rate per IVF
between laparoscopy cycle in salpingectomy
and IVF in 2 groups group
Yoon et al, Meta-analysis Hydrosalpinx or Amount of gonadotropin 1482 patients included Majority of studies were No differences in any of
2016 ectopic used, peak estradiol, retrospective the outcomes
pregnancy number of oocytes, and
number of pregnancies
Tal et al, 2002 Case control Ectopic pregnancy Follicle count, retrieved Controlled for age, No analysis of clinical No effect on IVF
oocytes, and cleaved amount gonadotropin, pregnancy or live birth outcomes after
embryos timing of gonadotropin rates unilateral
salpingectomy
Almog et al, Retrospective Various Estradiol, FSH dose, and Multivariable analysis No subgroup analysis for No change in outcomes
2011 cohort follicle and oocyte method of
count salpingectomy
Lin et al, 2013 Retrospective Ectopic pregnancy Duration of stimulation, Large sample size and No analysis of No difference in any
cohort or hydrosalpinx amount of excluded mixed salpingectomy to time outcome

Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017

gonadotropin, follicle surgeries of IVF and possible
number, oocyte selection bias
number, implantation,
fertilization, and
clinical pregnancy rate
Dar et al, 2000 Retrospective Ectopic pregnancy Duration and quantity of Compared ovarian Small sample size No significant difference
cohort hMG, preovulatory response between in ovarian function
concentrations of cycles before and after before and after
estradiol, number of unilateral salpingectomy for
oocytes retrieved, and salpingectomy and ectopic pregnancy
quality of embryos between affected and
unaffected sides
Xi et al, 2012 Retrospective Ectopic pregnancy Serum FSH and estradiol, Wide array of outcomes No multivariable No differences in any of
cohort length of stimulation, analyzed regression analysis for the outcomes
number of follicles, and confounding
retrieved or fertilized
oocytes
(Continued )
 Kotlyar et al.
Table 3

Continued

Effect of Salpingectomy on Ovarian Function

Authors Study design Indications Outcomes Strengths Weaknesses Findings
Pereira et al, Retrospective Ectopic pregnancy Basal FSH, total days of Adequately powered and No data on AMH values No difference in outcomes
2015 cohort stimulation, dose of wide array of outcomes and lack of confounder aside from increased
gonadotropins, number analyzed analysis FSH dosage in
of mature oocytes, salpingectomy group
clinical pregnancy, and
live birth
Periera et al, Retrospective Ectopic pregnancy, Ovarian stimulation Large sample size and Single center, Increased duration of
2017 cohort hydrosalpinx, parameters, total adequately powered retrospective, and small gonadotropin
hemato- or oocytes retrieved, sample size of stimulation and amount
pyosalpinx fertilization rates, salpingectomy group of gonadotropin
implantation rates, and administered; no
clinical pregnancy rates difference in
fertilization or
implantation rate
€
Odesj€
o et al, Retrospective Ectopic pregnancy Number of retrieved Multivariable regression Single center, No difference in oocyte
2015 cohort oocytes and clinical analysis retrospective, and no number or clinical
pregnancy and live birth comparison between pregnancy or live birth
rates ipsilateral and rates between
contralateral ovary salpingectomy and
salpingostomy
Bredkjaer Case control Hydrosalpinx Delivery rate per IVF Evaluated outcomes for Small sample size Bilateral salpingectomy
et al, 1999 cycle, implantation rate multiple cycles of IVF due to hydrosalpinx
per IVF cycle, number restores normal
of embryos, cleavage delivery rate and
stage, embryo implantation rate per
morphology score, and cycle of IVF, normal
live birth rate live birth rate, and high
implantation rate for at
least 3 IVF cycles after
bilateral salpingectomy
Strandell et al, RCT Hydrosalpinx Clinical pregnancy rate, No significant difference Power ,80%, bilateral Significantly higher
1999 delivery rate, and in background variables hydrosalpinges implantation rate,
implantation rate between groups except significantly more clinical pregnancy rate,
bilateral vs unilateral frequent in and delivery rate in
hydrosalpinges salpingectomy group, patients with bilateral,
and study based only on ultrasound-visible
first cycle of IVF hydrosalpinges
(Continued )

571
 572
Table 3

Continued

Authors Study design Indications Outcomes Strengths Weaknesses Findings

Strandell et al, Cohort Hydrosalpinx Dose and duration of FSH Patients served as their Small sample size and did Laparoscopic
2001 and number of retrieved own control and not analyze ovarian salpingectomy before
and fertilized oocytes compared ovarian function on separate IVF does not
response before and side (most cases were compromise ovarian
after salpingectomy bilateral function
salpingectomy)
Strandell et al, RCT Hydrosalpinx Cumulative birth rate and Analyzed cumulative IVF Does not examine other Significantly higher
2001 clinical pregnancy rate cycles; both measures of ovarian cumulative birth rate
randomized groups had function and clinical pregnancy
similar age and rate in salpingectomy
obstetric history group, especially with
ultrasound-visible
hydrosalpinges
Surrey et al, Retrospective Hydrosalpinx Uterine artery Doppler Compared salpingectomy Selection bias and small No significant difference
2001 cohort flow, ovarian with proximal tubal sample size between groups
hyperstimulation occlusion and similar
response, implantation, baseline characteristics,
and clinical pregnancy except slightly older

Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017

rate age in 1 group
Kontoravdis RCT Hydrosalpinx Implantation rate, clinical Comparable subject Small sample size No significant difference
et al, 2006 pregnancy rate, characteristics between between proximal tubal
ongoing pregnancy groups, prospective occlusion and
rate, abortion rate, and randomized study salpingectomy before
ectopic pregnancy rate supports prior IVF
retrospective studies’
findings
Gelbaya et al, Retrospective Hydrosalpinx FSH, hMG, E2, number of Compares salpingectomy Small sample size Prophylactic
2006 cohort follicles, number of with proximal tubal salpingectomy may
oocytes retrieved and division in patients have a negative effect
fertilized, pregnancy undergoing IVF on ovarian reserve
rate, and miscarriage without affecting
rate pregnancy rates
Dreyer et al, RCT Hydrosalpinx Ongoing pregnancy rate Randomized, 2 center No blinding, small sample Ongoing pregnancy rates
2016 after 1 IVF/ICSI cycle size, and no long-term were less for
follow-up hysteroscopic tubal
occlusion versus
salpingectomy
(Continued )
Kotlyar et al. Effect of Salpingectomy on Ovarian Function 573

(n 5 16), or a tubo-ovarian abscess (n 5 1). In a cross-

AFC 5 antral follicle count; AMH 5 antim€ullerian hormone; E2 5 estradiol; FI 5 flow index; FSH 5 follicle-stimulating hormone; hMG 5 human menopausal gonadotropin; ICSI 5 intracytoplasmic sperm injection; IVF 5 in vitro
salpingectomy improve
sectional study of 71 patients with tubal factor infertility,
All 3 methods improve

No difference between
AMH was significantly lower in the infertile patients who

ongoing pregnancy
clinical pregnancy

sclerotherapy and
rates; only tubal
underwent salpingectomy compared with those with intact

salpingectomy
occlusion and
tubes (16.1 vs 23.4 pmol/L, p 5 .04) [23]. Another study
found significantly fewer follicles in the ovary on the oper-
Findings

rates
ated side after unilateral salpingectomy for tubal pregnancy
than in the nonoperated side (4.4 vs 8.2, p , .0001) [24].
Laparoscopic salpingectomy for ectopic pregnancy led to
decreased AFC (5.0 vs. 7.4, p 5 .014) and ovarian blood
flow (flow index 5 24.97 vs 27.79, p 5 .020; vascular
Small study effects could

the limited number of

not be assessed given

retrospective, and no
confounder analysis flow index 5 0.14 vs 0.37, p 5 .020) on the operated versus
Small sample size,

nonoperated side [25]. It is of note that for the majority of the

studies noting a detrimental effect of salpingectomy on
Weaknesses

ovarian reserve, the indication for salpingectomy was for

studies

removal of an ectopic pregnancy.

The previously described RCT comparing prophylactic
salpingectomy at the time of abdominal hysterectomy also
used ovarian stromal Doppler velocimetry using pelvic ul-
trasound. Hysterectomy led to an unexpectedly decreased
Only RCTs were included

mean pulsatility index, resistance index, and systole/diastole

outcomes analyzed
Day 3 FSH and IVF

ratio at both 1 and 6 months compared with baseline, consis-

tent with an overall increase in blood flow to the ovaries after
surgery [16]. However, the decline in the pulsatility index
Strengths

was less in the total salpingectomy group (p 5 .02), suggest-

ing that salpingectomy slightly attenuates this hysterectomy-
related increase in ovarian blood flow.
In a meta-analysis performed by Fan and Ma [26]
comparing 25 studies with 1935 patients who underwent
oocytes, and pregnancy
clinical pregnancy rate,
ectopic pregnancy rate,
Ongoing pregnancy rate,

salpingectomy versus 2983 controls, the total dose of

Day 3 FSH, number of

gonadotropin required in IVF embryo transfer was signifi-

and miscarriage

cantly higher after salpingectomy for hydrosalpinx or tubal

ectopic pregnancy. The number of oocytes retrieved from
Outcomes

the ipsilateral ovary compared with the contralateral ovary

rates

was also significantly reduced [26]. Another study found

that salpingectomy may also decrease basal AFC [27].
Thus, studies on surgery confined to the tubes or
mesosalpinx are generally reassuring regarding the ovarian
S/D 5 systole/diastole; VFI 5 vascular flow index; VI 5 vascular index.

reserve although the possibility of detectable gonadal

Hydrosalpinx

Hydrosalpinx

injury cannot be excluded. This is especially the

Indications

case when ectopic pregnancy was the indication for sal-

pingectomy.
fertilization; RCT 5 randomized controlled trial;

Salpingectomy and Pregnancy Outcomes

Meta-analysis

Retrospective

Patients requiring tubal surgery for ectopic pregnancy or

Study design

hydrosalpinx typically have a strong interest in pursuing

cohort

further pregnancy and spontaneous conception. Surgical in-

terventions include salpingectomy, salpingostomy, and tubal
occlusion. Unfortunately, the only readily available outcome
for such patients is pregnancy, which reflects an ovulatory
Na et al, 2016

state but only indirectly reflects ovarian reserve. Moreover,

Tsiami et al,
Continued

analysis of pregnancy rates is confounded by the potential

Table 3

Authors

2016

detrimental impact of abnormal tubes. However, subtle dam-

age to ovarian tissue may be reflected in a decreased preg-
nancy rate among patients, particularly toward the end of
574
their reproductive years. The risks and benefits of these op-
tions on spontaneous conception are discussed later.
Tubal Surgery for Ectopic Pregnancy
The effect of laparoscopic salpingectomy for ectopic
pregnancy on cumulative spontaneous intrauterine preg-
nancy rates remains controversial. Early studies on the man-
agement of ectopic pregnancy appeared to show comparable
intrauterine pregnancy rates after either laparoscopic salpin-
gectomy or salpingostomy/conservative treatment [25,28].
This view was challenged by a retrospective cohort study
of patients attempting to conceive after the first ectopic
pregnancy that found an elevated cumulative intrauterine
pregnancy rate in patients undergoing salpingostomy
compared with salpingectomy (88% vs 66%, p , .05)
[29]. In addition, a prospective study showed a higher cumu-
lative intrauterine pregnancy rate within 24 months in the
salpingostomy group compared with salpingectomy (76%
vs 67%) [30]. Although this difference was not significant
in the entire population, in a multivariate subgroup analysis
of patients .35 years old or with a history of infertility or
tubal disease (n 5 430), patients who received ‘‘conserva-
tive’’ medical or surgical treatment with salpingostomy
experienced significantly higher live birth rates compared
with those undergoing ‘‘radical’’ surgical management by
salpingectomy (hazard ratio 5 1.52; 95% CI, 1.14–2.02)
[30]. This age-dependent effect offers weak evidence that
salpingectomy may inflict clinically relevant ovarian dam-
age on older patients desiring spontaneous pregnancy.
Key updates to the role of aggressive tubal surgery for
ectopic pregnancy were introduced in 2014 after the Euro-
pean Surgery in Ectopic Pregnancy (ESEP) trial, an open-
label RCT of 446 women. The ESEP trial failed to identify
a difference in spontaneous conception at 36 months be-
tween salpingostomy and salpingectomy (60.7% vs 56.2%,
p 5 .678) [31]. This study did report an increased risk of
persistent trophoblast in the salpingostomy group (7% vs
,1%, relative risk 5 15.0; 95% CI, 2.0–113.4) [28]. As a
result, the authors concluded that salpingectomy should be
considered the standard surgical treatment for ectopic preg-
nancy [31]. These findings were largely consistent with the
DEMETER study, a trial of 199 women requiring surgery
for ectopic pregnancy randomized to either salpingostomy
plus intramuscular methotrexate or laparoscopic salpingec-
tomy. This study found comparable cumulative 24-month in-
trauterine pregnancy rates in both the salpingostomy and
salpingectomy groups (70% vs 64%, hazard ratio 5 1.07;
95% CI, 0.69–1.67) [32]. Similar comparable outcomes
were noted by a retrospective cohort study looking at 57
women who underwent salpingectomy and 75 undergoing
salpingostomy. The 24-month postoperative intrauterine
pregnancy rates were 56.1% and 60%, respectively [33].
Still, some have disputed the conclusions of the ESEP
study and pointed to retrospective studies suggesting a small
(w9%) benefit to salpingostomy over salpingectomy, noting
that ESEP was only powered to detect a 15% difference in
Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017
pregnancy rate [34]. They also suggested that surgeon inex-
perience might have limited the benefits of salpingostomy in
the ESEP study [31].
As a result, this topic remains controversial. Moreover, it
remains unclear to what extent an improved pregnancy rate
after conservative tubal surgery can be attributed to the pres-
ervation of ovarian function. The absence of convincing im-
provements in pregnancy rate with salpingostomy despite a
clearly elevated rate of persistent trophoblastic tissue sup-
ports salpingectomy for the surgical management of ectopic
pregnancy. Individualized decisions should be made for
older patients.
Tubal Surgery for Hydrosalpinx
The role of salpingectomy versus conservative surgical
therapy for tubal disease/hydrosalpinx in patients desiring
spontaneous conception is also controversial [35]. Because
exposure to hydrosalpingeal fluid approximately halves the
pregnancy rate during IVF, sterilizing surgery with either
salpingectomy or tubal occlusion is the standard of care
for the management of tubal infertility in patients planning
to undergo IVF [36]. Unfortunately, the assessment of
ovarian function in spontaneous pregnancy in the presence
of damaged dilated tubes is not possible because such pa-
tients are expected to have a very low spontaneous preg-
nancy rate. Certain patients appear to benefit from
salpingostomy [37–39] or proximal tubal occlusion (PTO)
[40] for hydrosalpinges. Because clinical benefits for conser-
vative therapy over salpingectomy likely have little to do
with ovarian function, these studies remain outside the scope
of this review.
Salpingectomy and IVF
Because patients planning IVF do not require functional
tubes, no role exists for maintaining tubal patency through
less aggressive surgery. Therefore, the main question is
whether salpingectomy will create a more favorable envi-
ronment for implantation than it will potentially harm the
ovarian response to hyperstimulation.
A small study found that salpingectomy decreased the
ovarian response during controlled ovarian hyperstimulation
for IVF, with significantly fewer follicles developing on the
day of human chorionic gonadotropin administration in the
ovary whose adjacent tube was removed compared with
the contralateral one (5.6 vs 4.7, p , .02) [8]. A prospective
randomized study examining patients with severe tubal
infertility suggested the possibility of an increased IVF em-
bryo implantation rate after salpingectomy (10.4% vs 4.6%,
p 5 .43) and pregnancy rate per cycle of IVF (23.7% vs
16.3%, p 5 .47) although the study was underpowered to
make any conclusions [41]. One meta-analysis of 25 studies
comparing 1935 patients who underwent salpingectomy
with 2983 controls found that the total dose of gonadotropin
required in IVF embryo transfer was significantly higher af-
ter salpingectomy for hydrosalpinx or tubal ectopic
Kotlyar et al. Effect of Salpingectomy on Ovarian Function
pregnancy (inverse variance 5 0.10; 95% CI, 0.03–0.16;
I2 5 30%). The number of oocytes retrieved from the ipsilat-
eral ovary compared with the contralateral ovary was
also significantly reduced (inverse variance 5 0.25; 95%
CI, 20.40 to 20.10; I2 5 48%) [24].
In contrast, a meta-analysis by Yoon et al [42] found
that the number of oocytes retrieved and the total gonado-
tropin dose used were not significantly different before and
after salpingectomy [42]. However, the latter study
included less than half the patients in the study of Fan
and Ma [26]. Several other analyses have found that unilat-
eral salpingectomy did not affect the ipsilateral ovarian
response to IVF treatment cycles. No difference in the
number of follicles, oocytes, or cleaved embryos was
found between patients undergoing IVF treatment with
and without a history of unilateral salpingectomy [43].
The number of oocytes retrieved after ovarian hyperstimu-
lation pre- and postsalpingectomy was also comparable
[44]. Similarly, the number of follicles and oocytes
retrieved after IVF embryo transfer cycles in patients
with a unilateral salpingectomy was reported to be compa-
rable between the ovary ipsilateral to the operated side and
the contralateral ovary [45].
IVF Outcomes After Tubal Surgery for Ectopic Pregnancy
Patients with ectopic pregnancy who underwent salpin-
gectomy and controls whose tubes were left intact and sub-
sequently underwent IVF experienced similar implantation
rates, clinical pregnancy rates, and live birth rates [17].
This was supported by a retrospective study that found no
significant difference in ovarian function before and after
salpingectomy in 26 patients undergoing 52 ART cycles.
There was no difference among the duration and quantity
of human menopausal gonadotrophins, preovulatory con-
centrations of estradiol, number of oocytes retrieved, or
quality of the embryos [46]. A similar study from China
found that the initial and total gonadotropin doses were
higher after salpingectomy for ectopic pregnancy but identi-
fied no other changes in basal FSH, E2 (estradiol), stimula-
tion length, or follicle or oocyte number [47]. This was
echoed by a study from Canada noting higher required doses
of gonadotropins after salpingectomy for ectopic pregnancy
compared with controls treated with methotrexate to obtain
the same number of oocytes [48]. These studies, although
underpowered, suggest that ovarian effects of salpingectomy
for ectopic pregnancy in patients undergoing IVF are negli-
gible. A more recent retrospective study looking at 135 pa-
tients who underwent salpingectomy for various
indications including tubal ectopic pregnancies found
similar trends in gonadotropin stimulation. However, this
study did not find any difference in oocytes retrieved, fertil-
ization, implantation, or clinical pregnancy rates compared
with age- and time-matched controls [49]. This study
confirmed similar findings from a Swedish group showing
no difference in IVF outcomes [50].
575
IVF Outcomes After Tubal Surgery for Hydrosalpinx
Hydrosalpinx is known to have a detrimental effect on
IVF embryo transfer outcome [38]. Implantation and preg-
nancy rates are both reduced by approximately 50%, and
higher miscarriage rates are observed compared with women
without hydrosalpinx [35,51]. Some theories explain this
detrimental effect as stemming from potential embryotoxic
factors contained within the hydrosalpinx fluid. A
hydrosalpinx may also exert a negative influence on
oocytes in early follicular recruitment during IVF
stimulation [42].
Outcomes are markedly improved when salpingectomy
is performed for hydrosalpinx in the context of planned
IVF [42]. This is supported by a case-control study that
found that bilateral salpingectomy caused by hydrosalpinx
restores normal delivery and implantation rates after IVF
treatment [52]. This was also confirmed in an RCT in
Scandinavia studying IVF outcomes of 204 women with
hydrosalpinx. These patients were randomized to receive
either a laparoscopic salpingectomy or no intervention
before IVF. They found significantly higher implantation
rates (25.6% vs 12.3%, p 5 .038), clinical pregnancy rates
(45.7% vs 22.5%, p 5 .029), and delivery rates (40.0% vs
17.5%, p 5 .038) in patients with bilateral, ultrasound-
visible hydrosalpinges who received salpingectomy [53].
In a follow-up study of 26 patients from Scandinavia with
hydrosalpinx who underwent conservative management and
failed 1 or 2 IVF cycles, prophylactic salpingectomy led to
no significant difference in the ovarian response before
and after surgery, leading the authors to conclude that pro-
phylactic salpingectomy did not compromise ovarian func-
tion [54]. The same authors further analyzed the effect of
salpingectomy on the cumulative birth rate in a separate
RCT. Their findings of increased implantation (27.2% vs
20.2%, p 5 .03) and birth rates (95% CI, 1.6–3.6,
p 5 .014) further support the use of salpingectomy before
IVF in patients with hydrosalpinx. The differences were
even larger when the subgroup of patients with ultrasound-
visible hydrosalpinges was analyzed [55].
An alternative management strategy for hydrosalpinx is
PTO, which is performed laparoscopically using bipolar
electrosurgery at 2 sites on the isthmus approximately
1 cm apart. Theoretically, this entails less disruption of the
ovarian blood supply and still prevents reflux of embryotoxic
fluid into the uterine cavity. Surrey and Schoolcraft [56]
retrospectively examined outcomes of 94 patients undergo-
ing IVF who received either laparoscopic salpingectomy
or laparoscopic PTO. No difference was noted in the mean
ovarian artery pulsatility index or ovarian response nor
was any difference observed in implantation and clinical
pregnancy rates (29.2% 6 5.9% vs 19.4% 6 6.1%, respec-
tively, and 57.1% vs 46.7%, respectively). However, a retro-
spective British study of patients with hydrosalpinges found
increased day 2 FSH and decreased day 8 E2 levels in pa-
tients who underwent salpingectomy compared with those
576
who underwent PTO or conservative treatment [57]. Never-
theless, fertilization rates and implantation rates per cycle
did not differ between the 2 groups.
Tubal occlusion can also be performed hysteroscopically.
A recent RCT comparing hysteroscopic tubal occlusion with
laparoscopic salpingectomy failed to find a difference in the
number of retrieved and fertilized oocytes or the measures of
embryo quality despite evidence that hysteroscopic PTO
leads to inferior pregnancy rates (14.1% vs 36.7%,
p 5 .003) [58]. This study suggests that there is little role
for the hysteroscopic management of hydrosalpinges and
supports the safety of salpingectomy on ovarian function.
The previously mentioned studies on salpingectomy in
hydrosalpinx IVF patients overall support its routine use
and safety although laparoscopic PTO is a less-studied yet
promising alternative. Collectively, these studies fail to iden-
tify any benefit for PTO in planned IVF and argue against
hysteroscopic PTO. A meta-analysis comparing salpingec-
tomy, tubal occlusion, fluid aspiration, and no intervention
to treat hydrosalpinx before IVF found that all 3 surgical in-
terventions significantly increased clinical pregnancy rates
compared with no intervention. However, the differences be-
tween the surgical interventions were not statistically signif-
icant [59].
Ultrasound-guided aspiration of hydrosalpinx with injec-
tion of a sclerosing agent has also been assessed as a nonsur-
gical alternative to the management of hydrosalpinx. One
retrospective study found comparable clinical pregnancy
and ectopic rates in patients undergoing sclerotherapy with
those undergoing salpingectomy [60].
Overall, the benefits from removing embryotoxic fluid
from the uterine and ovarian microenvironment with salpin-
gectomy clearly outweigh the risks to ovarian tissue in IVF.
There may be a small decrease in ovarian response to ovarian
hyperstimulation after salpingectomy. Other alternatives
have been poorly characterized.
Conclusions
Overall, it appears that salpingectomy is unlikely to have
a substantial adverse impact on ovarian reserve. The major-
ity of existing studies have reported reassuring findings, and
no clear evidence exists to recommend against salpingec-
tomy when tubal surgery is otherwise indicated. Still, reports
of alterations in FSH, AMH, AFC, or the ovarian pulsatility
index cannot be completely discounted.
Of note, the indication for salpingectomy in the majority
of the studies noting a detrimental effect on ovarian reserve
was the removal of an ectopic pregnancy or hydrosalpinx. It
is possible that a unilateral tubal pathology that necessitated
the salpingectomy may have been the cause of the reported
ipsilateral decreased ovarian function. Similarly, case-
control studies comparing patients who required salpingec-
tomy with patients with intact tubes cannot adequately adjust
for the altered ovarian milieu in the salpingectomy patients.
Journal of Minimally Invasive Gynecology, Vol 24, No 4, May/June 2017
The overall significance of any measured alterations in
ovarian reserve is likely to remain contentious because exist-
ing markers do not reliably predict a reproductive-age wom-
an’s ability to conceive [8]. Long-term outcomes including
age at menopause remain relatively unknown although
follow-up after elective salpingectomy at 3 to 5 years ap-
pears reassuring.
Salpingectomy likely has a minimal impact on the
spontaneous conception rate after ectopic pregnancy
because patients conceive at comparable levels when
treated with salpingectomy or tube-sparing surgery [28].
The main clinical differences between aggressive and
more conservative management of ectopic pregnancy are
unlikely to be a consequence of altered ovarian function.
However, a small clinical benefit for salpingostomy in
ectopic pregnancy may exist in select patients with existing
tubal disease or who are .35 years. Given that conserva-
tive therapy risks leaving persistent trophoblastic tissue
and confers higher repeat ectopic rates, tube-sparing sur-
gery for the purpose of preserving potential ovarian func-
tion may be considered as an alternative to
salpingectomy in older patients with mild tubal disease
reluctant to undergo IVF.
For patients planning IVF, aggressive tubal surgery
should be performed whenever indicated. Salpingectomy
is now considered the standard of care for the management
of hydrosalpinx in patients undergoing IVF. There is rela-
tively weak evidence suggesting that gonadotropin require-
ments are increased in IVF cycles after salpingectomy and
limited evidence of a decrease in cycle day 2 FSH or day 8
E2, but this is not accompanied by a decrease in pregnancy
rates.
Patients considering prophylactic salpingectomy, espe-
cially at the time of gynecologic surgery, should be advised
of the small potential for diminished ovarian function.
Without longer follow-up and more conclusive studies, no
clear recommendation can be made. However, the over-
whelming majority of studies support the safety of this pro-
cedure to the ovaries.
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