Ovarian function before and after salpingectomy in artificial technology patients
To determine the effect of the removal of the tube on ovarian function we studied 52 artificial reproduction technology cycles in 26 women before and after undergoing laparoscopic salpingectomy for ectopic pregnancy. Ovarian response was measured by the duration and quantity of human menopausal gonadotrophins used in the cycle, the pre-ovulatory concentrations of oestradiol, the number of oocytes retrieved, and the quality of the embryos. All parameters were compared between cycles carried out before and after salpingectomy as well as between affected and unaffected sides. Our findings show no significant difference in any of the parameters studied. We conclude that laparoscopic salpingectomy does not abate ovarian response in artificial reproduction technology cycles that follow the procedure.
Human Reproduction vol.15 no.1 pp.142–144, 2000
Ovarian function before and after salpingectomy in
artiﬁcial reproductive technology patients
tion technology cycle (Mukherjee et al., 1996; Shelton et al.,
1996). Furthermore, it was suggested recently that the
performance of salpingectomy before in-vitro fertilization
Department of Obstetrics and Gynecology, Assaf Harofeh Medical (IVF) in all cases of severe infertility, may improve implanta-
Center, Zeriﬁn 70300, Israel, afﬁliated with the Sackler Faculty of tion and pregnancy rates (Dechaud et al., 1998; Bredkjaer
Medicine, Tel-Aviv University, Tel-Aviv, Israel and
Obstetrics and Gynecology, Albert Einstein College of Medicine/ et al., 1999). However, before embarking on such a radical
Monteﬁore Medical Center, Bronx, NY 10461, USA and irreversible treatment in high-risk patients without
hydrosalpinx, the short- and long-term implications of the
To whom correspondence should be addressed
procedure must be considered. In view of the close anatomical
To determine the effect of the removal of the tube on association of the blood supply and nervous system of these
ovarian function we studied 52 artiﬁcial reproduction organs, potential adverse effects of the physical and functional
technology cycles in 26 women before and after undergoing presence or absence of the tube on ovarian function were
laparoscopic salpingectomy for ectopic pregnancy. Ovarian postulated (McComb and Delbeke, 1984; Rumeu et al., 1987;
response was measured by the duration and quantity of Lass et al., 1998). However, current data are still inconclusive
human menopausal gonadotrophins used in the cycle, the and contradictory. This study was undertaken to determine and
pre-ovulatory concentrations of oestradiol, the number of compare ovarian response in artiﬁcial reproduction technology
oocytes retrieved, and the quality of the embryos. All patients before and after salpingectomy for ectopic pregnancy.
parameters were compared between cycles carried out
before and after salpingectomy as well as between affected
and unaffected sides. Our ﬁndings show no signiﬁcant Materials and methods
difference in any of the parameters studied. We conclude Records between October 1988 and July 1996 were found of 26
that laparoscopic salpingectomy does not abate ovarian women who had artiﬁcial reproduction technology cycles before and
response in artiﬁcial reproduction technology cycles that after undergoing salpingectomy for ectopic pregnancy. All these
follow the procedure. patients met the following criteria: no previous tubal surgery; age at
post-salpingectomy cycle under 40 years; and a period of ⬍3 years
between cycles. The selection of a group of women with proven
Key words: artiﬁcial reproduction technology/ovarian function/
fertility by previous pregnancy raised the possibility of a bias towards
a more favourable sub-group. The design of the study, using women
as the control for themselves, removed this problem.
Ovulation induction in all cases was accomplished with menstrual
long-acting gonadotrophin-releasing hormone (GnRH) analogue/
Introduction human menopausal gonadotrophin (HMG)/human chorionic gonado-
trophin (HCG) protocol described previously (Herman et al., 1990).
The place of salpingectomy in the management of the patho-
IVF was carried out in all but two cycles in which intracytoplasmic
logical tube in a patient who will need assisted reproduction
sperm injection (ICSI) was utilized.
technology is still a dilemma.
Ovarian response was measured by the duration and quantity of
It is well established that ectopic pregnancy is far more HMG used in the cycle, the pre-ovulatory concentrations of oestradiol,
frequent in patients undergoing artiﬁcial reproduction number of oocytes retrieved and quality of embryos (Puissant et al.,
technology for mechanical infertility than in the normal popula- 1987). Ovarian response was compared between cycles before and
tion (Herman et al., 1990; Dubuisson et al., 1991; Zouves after salpingectomy as well as between affected and unaffected sides
et al., 1991). Using multivariate analysis of the risk factors before and after salpingectomy.
for recurrent ectopic pregnancy, a scoring system has been
proposed that allows a selection of information-based treat- Statistical analysis
ments to decrease recurrence (Pouly et al., 1991). Even though Paired t-test was used to compare ovarian response parameters; χ
ectopic pregnancy may still occur following salpingectomy test was used to assess the differences in proportions. Values are
(Chang et al., 1998), for high-risk patients the authors suggested mean ⫾SD; P⬍0.05 was considered statistically signiﬁcant.
a laparoscopic ipsilateral salpingectomy with contralateral
sterilization. In the presence of hydrosalpinx, in which signi- Results
ﬁcantly decreased pregnancy rates were reported (Singhal et al.,
1991; Camus et al., 1999), some investigators recommended The average age of patients before salpingectomy was 31.7 ⫾
3.6 and 33.4 ⫾2.7 years after salpingectomy (P⬍0.05).consideration of salpingectomy before the artiﬁcial reproduc-
142 ©European Society of Human Reproduction and Embryology
The effect of salpingectomy on ovarian function
Table II. Embryo quality before and after laparoscopic salpingectomyTable I. Ovarian response parameters before and after laparoscopic
salpingectomy for ectopic pregnancy
Embryo qualityaBefore After
(degree)Ovarian response parameters BeforeaAftera
Days of HMG (n) 10.81 ⫾2.45 10.68 ⫾2.57 1st 37/56 (66) 30/54 (55.5)
2nd 13/56 (23.2) 19/54 (35.18)HMG ampoules (n) 36.13 ⫾14.45 34.81 ⫾12.47
Oestradiol on day 0 (pg/ml) 1285 ⫾785 1151 ⫾819 3rd and 4th 6/56 (10.7) 5/54 (9.25)
Oocytes retrieved from non-operated side 5.07 ⫾3.08 4.40 ⫾3.68
(n⫽25) Values in parentheses are percentages.
aAccording to Puissant et al. (1987).Oocytes retrieved from operated side 6.06 ⫾3.85 5.31 ⫾4.22
(n⫽27) cχ2test for comparison of proportions; P⫽0.38 with 2 degrees of freedom.
Oocytes suitable for insemination/injection 10.81 ⫾5.75 9.5 ⫾6.98
Fertilization rate (%)b55.5 59.26
Table III. Comparison of oocyte number retrieved between operated and
Transferred embryo (n) 3.56 ⫾0.81 3.37 ⫾0.80
non-operated sides before and after salpingectomy (n⫽25)a
Values are means ⫾SD.
Side of oocyte retrieval
aThere were no signiﬁcant differences (paired t-test) except bχ2test for
comparison of proportions (0.67).
cIn one case bilateral salpingectomy was performed.
HMG ⫽human menopausal gonadotrophin.
Before salpingectomy 6.06 ⫾3.85 5.07 ⫾3.08
After salpingectomy 5.31 ⫾4.22 4.40 ⫾3.68
Gravidity in pre-salpingectomy cycles ranged from zero to six
and parity ranged from zero to one. The main indications Values are means ⫾SD.
aIn one case bilateral salpingectomy was performed.
before the pre-salpingectomy artiﬁcial reproduction technology There were no signiﬁcant differences (paired t-test).
cycle was mechanical infertility (n⫽16), male factor (n⫽
6), anovulation (n⫽1), endometriosis (n⫽1), and unexplained performance in subsequent artiﬁcial reproduction technology
infertility (n⫽2). There was no signiﬁcant difference in cycles. Some studies from the 1980s, before the routine use
semen analysis WHO criteria for each couple between cycles. of operative laparoscopy, reported adverse effects on ovarian
Salpingectomies were performed in all cases by laparoscopy. function following salpingectomy. Signiﬁcantly fewer follicles
Additional surgery was performed in three women. Contralat- appeared in rat ovaries following the division of anastomotic
eral salpingectomy was performed in one case. A contralateral blood vessels between the ovary and the ﬁmbria (McComb
tubal cauterization was done for two other women who and Delbeke, 1984), and a signiﬁcantly lower number of pre-
had had repeated ectopic pregnancies and on laparoscopic ovulatory oocytes in patients after bilateral salpingectomy was
examination had been found to have severe adhesions and/or also noted (Rumeu et al., 1987). Likewise, fewer corpora lutea
hydrosalpinx. Informed consent involved a complete explana- were seen in the ipsilateral ovary after unilateral ﬁmbriectomy
tion of the procedure, the surgical options, and the uncertainty as compared with the number found in the contralateral intact
of subsequent ovarian response to the radical and irreversible ovary (McComb et al., 1981). It was reported that four of
options. seven women who had undergone tubal ligation had oestrogen
Implantation rate and clinical pregnancy rates following the excretion concentrations at ovulation below the tenth percentile
post-salpingectomy cycle were 23.07 and 19.23 respectively. (Cattanach, 1985). Nevertheless, studying 2456 women for 2
One woman had a repeated ectopic pregnancy (3.84%) and a years after tubal sterilization (DeStefano et al., 1983) it was
laparoscopic salpingectomy was performed. In all parameters shown that except for menstrual pain among patients who had
examined to evaluate ovarian performance (Table I) no signi- undergone unipolar electrocoagulation procedures, there was
ﬁcant differences were found before and after the salpingec- no increase in the prevalence of adverse menstrual function
tomy. Moreover, to determine whether the lack of difference after the procedure. The existence of periadnexal adhesions
was due to a decrease in ovarian response on the affected side was also found by some investigators to be associated with
with a compensatory increase in response on the unaffected poor ovarian function (Mahadevan et al., 1985; Molloy et al.,
side, we compared the number of oocytes retrieved from the 1987), but others could not conﬁrm this ﬁnding (Halme et al.,
same ovary before and after surgery. Notwithstanding that the 1982; Imoedemhe et al., 1988).
women were signiﬁcantly older during the post-salpingectomy Some recent studies of ovarian performance following
cycle, no signiﬁcant difference was found (Table I). salpingectomy resulted in different ﬁndings and conclusions.
Additionally, no signiﬁcant difference was found in the Lass et al. compared ovarian response in artiﬁcial reproduction
distribution of embryo quality between pre- and post-salpingec- technology cycles between 29 patients who had undergone
tomy cycles (Table II) or in the number of oocytes retrieved, unilateral salpingectomy because of ectopic pregnancy and 73
between the operated and non-operated side during pre- and patients with no preceding tubal surgery (Lass et al., 1998).
post-salpingectomy cycles (Table III). They found fewer follicles and retrieved oocytes on the
operated side, but no difference in overall number of follicles
Discussion and oocytes as compared to the control group. These ﬁndings
introduce the possibility of a compensatory mechanism in theThe current study demonstrates that laparoscopic salpingec-
tomy apparently has no deleterious impact on ovarian unaffected tube. Our study does not support such a possibility.
P.D ar et al.
Dubuisson, J.B., Aubroit, F.X., Mathieu, L. et al. (1991) Risk factors for
In a study of 26 women who underwent bilateral salpingectomy ectopic pregnancy in 556 pregnancies after in vitro fertilization: implications
(Verhulst et al., 1994) it was found that ovarian performance for preventive management. Fertil. Steril.,56, 686–690.
subsequent to surgery was equivalent to the control group. Halme, J., Rong, Z.J., Wing, R. et al. (1982) The removal of fallopian tubes
has no adverse effect on subsequent ovarian function in rabbits. Fertil.
Moreover, no difference in ovarian function was reported in Steril., 38, 621–624.
ﬁve women before and after bilateral salpingectomy. This Herman, A., Ron-El, R., Golan, A. et al. (1990) The role of tubal pathology
series as well as our own supports the hypothesis that tubal and other parameters in ectopic pregnancies occurring in in vitro fertilization.
Fertil. Steril., 54, 864–868.
removal does not compromise ovarian function. A third study
Imoedemhe, D.A., Waﬁk, A.H. and Chan, R.C. (1988) In vitro fertilization in
compared implantation and pregnancy rates in IVF patients women with ‘frozen pelvis’: clinical outcome of treatment. Fertil. Steril.,
with severe mechanical factor who underwent laparoscopic 49, 268–271.
salpingectomy and those with no prior surgery (Dechaud et al., Lass, A., Ellenbogen, A., Croucher, C. et al. (1998) Effect of salpingectomy
on ovarian response to superovulation in an in vitro fertilization-embryo
1998). The authors found that the antecedent surgery tended transfer program. Fertil. Steril.,70, 1035–1038.
to increase implantation and pregnancy rates. These ﬁndings Mahadevan, M.M., Wiseman, D., Leader, A. et al. (1985) The effects of
were also conﬁrmed by others (Bredkjaer et al., 1999). ovarian adhesive disease upon follicular development in cycles of controlled
stimulation for in vitro fertilization. Fertil. Steril.,44, 489–492.
The most important blood supply for the tube is the medial
McComb, P. and Delbeke, L. (1984) Decreasing the number of ovulations in
tubal artery, which originates at the same level as the median the rabbit with surgical division of the blood vessels between the fallopian
ovarian artery. Laparoscopic surgery, the predominant method tube and ovary. J. Reprod. Med., 29, 827–829.
for treatment of ectopic pregnancy today, in combination with McComb, P.F., Bourdage, R.J. and Halbert, S.A. (1981) Suppressed ovulatory
function and oviductal microsurgeryin the rabbit. Fertil. Steril.,35, 481–482.
early detection of ectopic pregnancy, permits resection of the
Molloy, D., Martin, M., Speirs, A. et al. (1987) Performance of patients with
unruptured tube as close as possible to its surface in the a‘frozen pelvis’in an in vitro fertilization program. Fertil. Steril.,47,
isthmical region. This minimizes the damage to the ovarian 450–455.
Mukherjee, T., Copperman, A.B. and McCaffrey, C. (1996) Hydrosalpinx ﬂuidblood supply and thus may decrease the occurrence of adverse
has embryotoxic effects on murine embryogenesis: a case for prophylactic
effects as reﬂected in our results. salpingectomy. Fertil. Steril.,66, 851–853.
Although not addressed in our study, the long-term impact Pouly, J.L., Chapron, C., Manhes, H. et al. (1991) Multifactorial analysis of
of salpingectomy on ovarian function, such as timing of fertility after conservative laparoscopic treatment of ectopic pregnancy in
a series of 223 patients. Fertil. Steril.,56, 453–460.
menopause, is an important concern. It has been shown (Siddle
Puissant, F., Van Rysselberge, M., Barlow, P. et al. (1987) Embryo scoring as
et al., 1987) that the mean age of ovarian failure was a prognostic tool in IVF treatment. Hum. Reprod.,2, 705–708.
lower in women who had undergone hysterectomy. However, Rumeu, A., Steingold, K., Jones, D. et al. (1987) Signiﬁcance of bilateral
salpingectomy in the outcome of IVF-ET (abstr. Pp159) presented at Fifthsalpingectomy and hysterectomy are scarcely comparable since
World Congress on In vitro Fertilization and Embryo Transfer, April 5–10,
the latter is far more devastating to the ovarian nerve and 1987, Norfolk, Virginia, USA. American Fertility Society, Birmingham,
blood supply than the laparoscopic procedure. Furthermore, Alabama, 1987, pp. 87.
the local hypertension that results from the occlusion of the Shelton, K.E., Butler, L., Toner, J.P. et al. (1996) Salpingectomy improves
the pregnancy rate in in-vitro fertilization patients with hydrosalpinx. Hum.
ovarian ligament may have a role in deterioration of ovarian Reprod.,11, 523–525.
function. Clearly, more studies are needed to elucidate the Siddle, N., Sarrel, P. and Whitehead, M. (1987) The effect of hysterectomy
long-term effects of salpingectomy on the ovary. on the age at ovarian failure: identiﬁcation of a subgroup of women with
premature loss of ovarian function and literature review. Fertil. Steril.,7,
In conclusion, our data suggest that laparoscopic salpingec-
tomy is a safe procedure in regard to conservation of ovarian Singhal, V., Li, T.C. and Cooke, I.D. (1991) An analysis of factors inﬂuencing
response in subsequent artiﬁcial reproduction technology the outcome of 232 consecutive tubal microsurgery cases. Br. J. Obstet.
Gynaecol.,98, 628–636.cycles. In view of the high risk of ectopic pregnancy in patients
Verhulst, G., Vandersteen, N., Van Steirteghem, A.C. et al. (1994) Bilateral
with pathological tubes who will need assisted reproduction, salpingectomy does not compromise ovarian stimulation in an in-vitro
salpingectomy, when indicated, should not be avoided because fertilization/embryo transfer programme. Hum. Reprod.,9, 624–628.
of concern for deterioration of ovarian function. World Health Organization (1995) WHO Laboratory Manual for the
Examination of Human Semen and Semen–Cervical Mucus Interaction. 3rd
edn. Cambridge University Press, Cambridge.
Zouves, C., Erenus, M. and Gomel, V. (1991) Tubal ectopic pregnancy after
References in vitro fertilization and embryo transfer: a role for proximal occlusion or
Bredkjaer, H.E., Ziebe, S., Hamid, B. et al. (1999) Delivery rates after in- salpingectomy after failed distal tubal surgery? Fertil. Steril.,56, 691–695.
vitro fertilization following bilateral salpingectomy due to hydrosalpinges:
a case control study. Hum. Reprod.,14, 101–105. Received on June 14, 1999; accepted on October 8, 1999
Camus, E., Poncelet. C., Gofﬁnet, F. et al. (1999) Pregnancy rates after in-
vitro fertilization in cases of tubal infertility with and without hydrosalpinx:
a meta-analysis of published comparative studies. Hum. Reprod.,14,
Cattanach, J. (1985) Oestrogen deﬁciency after tubal ligation. Lancet,13,
Chang, C.C., Wu, T.H., Tsai, H.D. et al. (1998) Bilateral simultaneous tubal
sextuplets: pregnancy after in-vitro fertilization-embryo transfer following
salpingectomy. Hum. Reprod.,13, 762–765.
Dechaud, H., Daures, J.P., Arnal, F. et al. (1998) Does previous salpingectomy
improve implantation and pregnancy rates in patients with severe tubal
factor infertility who are undergoing in vitro fertilization? A pilot prospective
randomized study. Fertil. Steril.,69, 1020–1025.
DeStefano, F., Huezo, C.M., Peterson, H.B. et al. (1983) Menstrual changes
after tubal sterilization. Obstet. Gynecol., 62, 673–681.