10
GYNECOLOGY A retrospective analysis of the effect of salpingectomy on serum antiMu ¨ llerian hormone level and ovarian reserve Xu-ping Ye, BS; Yue-zhou Yang, MS; Xiao-xi Sun, MD OBJECTIVE: To determine whether previous salpingectomy is asso- ciated with serum antiMu ¨ llerian hormone (AMH) level and ovarian reserve in women under 40 years presenting for in vitro fertilization and embryo transfer. STUDY DESIGN: We retrospectively compared serum AMH levels measured on the ovulation induction initiation day in patients with unilateral salpingectomy, bilateral salpingectomy, and no tubal sur- gery, and examined the relationship with length of time after surgery and in vitro fertilization and embryo transfer parameters. RESULTS: A total of 198 women were included; 83 received unilateral salpingectomy, 41 bilateral salpingectomy, and 74 no tubal surgery. The baseline characteristics of the groups were similar. The mean AMH level was significantly higher in women without tubal surgery as compared with those with bilateral salpingectomy (183.48 vs 127.11 fmol/mL; P .037). The mean follicle stimulation hormone level was significantly lower in women without surgery as compared with those with bilateral salpingectomy (7.85 vs 9.13 mIU/mL; P ¼ .048). No significant differences in duration of gonadotropin therapy, amount of gonadotropin used, estradiol level on the human chorionic gonadotropin injection day, thickness of the endometrium, number of oocytes retrieved, number of 2-pronuclei, viable embryos, and good quality embryos were found between the 3 groups. AMH level was not correlated with the number of oocytes or age in women that had undergone unilateral or bilateral salpingectomy. CONCLUSION: Salpingectomy is associated with decreased AMH level and increased follicle stimulation hormone in women seeking in vitro fertilization, though AMH level is not correlated with the number of oocytes retrieved in patients that have undergone unilateral or bilateral salpingectomy. These results suggest that salpingectomy is associ- ated with decreased ovarian reserve. Key words: AMH, antiMu ¨ llerian hormone, IVF-ET, ovarian reserve, salpingectomy Cite this article as: Ye X, Yang Y, Sun X. A retrospective analysis of the effect of salpingectomy on serum antiMu ¨ llerian hormone level and ovarian reserve. Am J Obstet Gynecol 2015;212:53.e1-10. I t is generally recognized that removal of a hydrosalpinx can increase the implantation rate of in vitro fertilization and embryo transfer (IVF-ET). 1,2 How- ever, whether salpingectomy affects ovarian reserve is uncertain, with some studies suggesting that salpingectomy deceases ovarian reserve, 3-5 and other studies indicating that it has no effect on ovarian reserve. 6-9 Various studies, however, have used different measures of ovarian reserve including the duration of gonadotropin stimulation, amount of gonadotropin used, number of follicles, number of oocytes retrieved, fertilization rate, implantation rate, clinical preg- nancy rate, live birth rate, and anti- Müllerian hormone (AMH) level. AMH is a glycoprotein dimer secreted primarily by granulocytes of preantral follicles and small antral follicles. 10 AMH levels are relatively constant thr- oughout the menstrual cycle, 11 correlate with the number of follicles and ovarian reserve, 12-14 and are predictive of both over and poor response to controlled ovarian stimulation. 15,16 For these rea- sons, AMH levels can be used to evalu- ate changes in ovarian reserve after salpingectomy. The purpose of this study was to determine whether previous salpingec- tomy is associated with serum AMH level and ovarian reserve in women under 40 years of age presenting for IVF-ET. P ATIENTS AND METHODS Patients IVF-ET patients who visited Shanghai Ji Ai Genetics and IVF Institute and the Obstetrics and Gynecology Hospital of Fudan University between October 2012 and May 2013 were eligible for in- clusion in this study. Inclusion criteria were age <40 years, regular menstrual cycles, and no history of ovarian surgery. Women with polycystic ovarian syn- drome, ovulatory dysfunction, and endometriosis were excluded from the analysis. Subjects were assigned into 1 of 3 groups according to their history of preIVF tubal surgery: unilateral sal- pingectomy, bilateral salpingectomy, or no tubal surgery. The institutional review board approved this retrospective study. Measurement of hormone levels A 10-mL blood sample was drawn on the third day of menstruation (IVF- ET initiation day). The sample was From Obstetrics and Gynecology Hospital of Fudan University Shanghai (Ms Ye and Dr Sun) and the Genetic and IVF Center of Shanghai Jiai, Shanghai (Mr Yang and Dr Sun), China. Received Feb. 21, 2014; revised June 11, 2014; accepted July 15, 2014. The authors report no conict of interest. Corresponding author: Yue-zhou Yang, MS. [email protected] 0002-9378/$36.00 ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajog.2014.07.027 JANUARY 2015 American Journal of Obstetrics & Gynecology 53.e1 Research ajog.org

A retrospective analysis of the effect of salpingectomy on serum antiMüllerian hormone level and ovarian reserve

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Page 1: A retrospective analysis of the effect of salpingectomy on serum antiMüllerian hormone level and ovarian reserve

Research ajog.org

GYNECOLOGY

A retrospective analysis of the effect ofsalpingectomy on serum antiMullerianhormone level and ovarian reserveXu-ping Ye, BS; Yue-zhou Yang, MS; Xiao-xi Sun, MD

OBJECTIVE: To determine whether previous salpingectomy is asso- with those with bilateral salpingectomy (7.85 vs 9.13 mIU/mL;

ciated with serum antiMullerian hormone (AMH) level and ovarianreserve in women under 40 years presenting for in vitro fertilizationand embryo transfer.

STUDY DESIGN: We retrospectively compared serum AMH levelsmeasured on the ovulation induction initiation day in patients withunilateral salpingectomy, bilateral salpingectomy, and no tubal sur-gery, and examined the relationship with length of time after surgeryand in vitro fertilization and embryo transfer parameters.

RESULTS: A total of 198 women were included; 83 received unilateralsalpingectomy, 41 bilateral salpingectomy, and 74 no tubal surgery.The baseline characteristics of the groups were similar. The meanAMH level was significantly higher in women without tubal surgery ascompared with those with bilateral salpingectomy (183.48 vs127.11 fmol/mL; P � .037). The mean follicle stimulation hormonelevel was significantly lower in women without surgery as compared

From Obstetrics and Gynecology Hospital ofFudan University Shanghai (Ms Ye and Dr Sun)and the Genetic and IVF Center of Shanghai Jiai,Shanghai (Mr Yang and Dr Sun), China.

Received Feb. 21, 2014; revised June 11, 2014;accepted July 15, 2014.

The authors report no conflict of interest.

Corresponding author: Yue-zhou Yang, [email protected]

0002-9378/$36.00ª 2015 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.ajog.2014.07.027

P ¼ .048). No significant differences in duration of gonadotropintherapy, amount of gonadotropin used, estradiol level on the humanchorionic gonadotropin injection day, thickness of the endometrium,number of oocytes retrieved, number of 2-pronuclei, viable embryos,and good quality embryos were found between the 3 groups. AMHlevel was not correlated with the number of oocytes or age in womenthat had undergone unilateral or bilateral salpingectomy.

CONCLUSION: Salpingectomy is associated with decreased AMH leveland increased follicle stimulation hormone in women seeking in vitrofertilization, though AMH level is not correlated with the number ofoocytes retrieved in patients that have undergone unilateral or bilateralsalpingectomy. These results suggest that salpingectomy is associ-ated with decreased ovarian reserve.

Key words: AMH, antiMullerian hormone, IVF-ET, ovarian reserve,salpingectomy

Cite this article as: Ye X, Yang Y, Sun X. A retrospective analysis of the effect of salpingectomy on serum antiMullerian hormone level and ovarian reserve. Am J ObstetGynecol 2015;212:53.e1-10.

t is generally recognized that removal

I of a hydrosalpinx can increase theimplantation rate of in vitro fertilizationand embryo transfer (IVF-ET).1,2 How-ever, whether salpingectomy affectsovarian reserve is uncertain, with somestudies suggesting that salpingectomydeceases ovarian reserve,3-5 and otherstudies indicating that it has no effecton ovarian reserve.6-9 Various studies,however, have used different measures of

ovarian reserve including the duration ofgonadotropin stimulation, amount ofgonadotropin used, number of follicles,number of oocytes retrieved, fertilizationrate, implantation rate, clinical preg-nancy rate, live birth rate, and anti-Müllerian hormone (AMH) level.AMH is a glycoprotein dimer secreted

primarily by granulocytes of preantralfollicles and small antral follicles.10

AMH levels are relatively constant thr-oughout the menstrual cycle,11 correlatewith the number of follicles and ovarianreserve,12-14 and are predictive of bothover and poor response to controlledovarian stimulation.15,16 For these rea-sons, AMH levels can be used to evalu-ate changes in ovarian reserve aftersalpingectomy.The purpose of this study was to

determine whether previous salpingec-tomy is associated with serumAMH leveland ovarian reserve in women under40 years of age presenting for IVF-ET.

JANUARY 2015 Ame

PATIENTS AND METHODS

PatientsIVF-ET patients who visited ShanghaiJi Ai Genetics and IVF Institute andthe Obstetrics and Gynecology Hospitalof Fudan University between October2012 and May 2013 were eligible for in-clusion in this study. Inclusion criteriawere age <40 years, regular menstrualcycles, and no history of ovarian surgery.Women with polycystic ovarian syn-drome, ovulatory dysfunction, andendometriosis were excluded from theanalysis. Subjects were assigned into 1 of3 groups according to their history ofpreIVF tubal surgery: unilateral sal-pingectomy, bilateral salpingectomy, orno tubal surgery. The institutional reviewboard approved this retrospective study.

Measurement of hormone levelsA 10-mL blood sample was drawn onthe third day of menstruation (IVF-ET initiation day). The sample was

rican Journal of Obstetrics & Gynecology 53.e1

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centrifuged for 5 minutes, and the su-pernatant serum was collected andstored at �20� C. Before testing, thesample was thawed and vortexed.Estradiol (E2), progesterone, luteinizinghormone, and follicle stimulating hor-mone (FSH) levels were measured with aBeckman Acoulter Access automatedchemiluminescence immunoassayanalyzer with reagent kits from Beckman(BeckmaneCoulter Inc., Brea, CA).Testing was performed according to themanufacturer’s instructions. AMH levelswere measured by an enzyme linkedimmunosorbent assay using a Bio-RadiMark microplate absorbance readerwith reagent kits from Bio-Rad (Bio-RadLaboratories Inc, Hercules, CA). Per themanufacturer, the interassay coefficientof variability is�10%, and the intraassaycoefficient of variability is �15%.

Determination of antral follicle countOn the third day of menstruation (IVF-ET initiation day), transvaginal sonog-raphy was performed to evaluate thestatus of the uterus and ovaries, measurethe ovarian size, and determine theantral follicle count (AFC). A PhilipsHDII ultrasonography machine (Philips,Amsterdam, the Netherlands) was usedat a probe frequency of 3w7 MHz.

Ovulation induction and IVF protocolsShort controlled ovarianhyperstimulation protocolDaily subcutaneous triptorelin 0.1 mgwas given from the third day of men-struation to the day of human chorionicgonadotropin (hCG) injection. Gonad-otropin 75-300 IU/day by injection wasstarted on the fourth day, and adjustedaccording to ultrasonography resultsand serum E2 level.

Minimal ovarian stimulation protocolOral clomiphene 50-100 mg was givenfrom the third day of menstruation tothe day of hCG injection. Daily humanmenopausal gonadotropin 75-150 IUby injection was given starting on thefifth day of clomiphene. When 1 domi-nant follicle reached 18 mm in diameter,or 2 follicles reached 16 mm in diameter,intramuscular injection of hCG 3000-10000 IU was given. Oocytes were

53.e2 American Journal of Obstetrics & Gynecolo

retrieved under transvaginal ultraso-nography guidance within 34-36 hoursof hCG injection.

IVFQuality sperm was selected for IVF/intracytoplasmic sperm injection. Eigh-teen hours after fertilization, the oocytewas observed to confirm the formationof a pronucleus. After 3 days of culture,the embryo was observed and scoredunder a microscope.

Evaluation of embryo qualityEmbryos of class I-III were consideredviable.Goodquality embryoswere definedas having a normal cleavage rate, even-sized blastomeres, and fragments <10%.

Statistical analysisContinuous variables were presented asmeans and standard deviations (SDs).Categorical variables were presented ascounts and percentages. One-way anal-ysis of variance with Bonferroni post hoctesting was performed to compare thedifferences between women with uni-lateral salpingectomy, with bilateral sal-pingectomy, and without surgery withrespect to baseline characteristics andtreatment-related factors. Because thevariables were normally distributed,Pearson coefficient correlation (r) wasperformed to investigate the linear cor-relation between AMH vs time aftersurgery, number of oocytes, and age inwomen with unilateral salpingectomyand bilateral salpingectomy. A 2-sidedP value < .05 was considered to indi-cate statistical significance. All statisticalanalyses were performed with SPSS17.0 statistics software (SPSS Inc.,Chicago, IL).

RESULTS

Patient characteristicsA total of 198 women were includedin the study, with 83 in the unilateralsalpingectomy group, 41 in the bilateralsalpingectomy group, and 74 in thegroup that had not received tubal sur-gery. Patient characteristics by groupare shown in Table 1. There were nodifferences in age, E2, progesterone,luteinizing hormone, AFC, ovarianstimulation protocol used, the length of

gy JANUARY 2015

secondary infertility, and the reason ofinfertility between the 3 groups (all, P >.05). The mean AMH level was signifi-cantly higher in women without tubalsurgery as compared with those withbilateral salpingectomy (183.48 vs127.11 fmol/mL, P � .037). The meanFSH level was significantly lower inwomen without surgery as comparedwith those with bilateral salpingectomy(7.85 vs 9.13 mIU/mL, P ¼ .048). Themean duration of primary infertility wassignificantly higher in women withoutsurgery as compared with those withunilateral and bilateral salpingectomy(3.6 vs 0.31 and 0.82 years, P < .001).The reasons for having surgery weresignificantly different between the uni-lateral and bilateral salpingectomygroups. The percentage of patients withan ectopic pregnancy was greater in theunilateral salpingectomy group, and thepercentage of patients with a hydro-salpinx was greater in the bilateral sal-pingectomy group (Table 1).

The comparisons of treatment-relatedfactors between the three groups areshown in Table 2. No significant differ-ences in duration of gonadotropin ther-apy, amount of gonadotropin used,E2 level on the hCG injection day,thickness of the endometrium, numberof oocytes retrieved, number of 2-pro-nuclear zygote (2PN), viable embryos,and good quality embryos were foundbetween the 3 groups (all, P > .05).

Correlation between AMH leveland time after surgery and numberof oocytesThe correlations between AMH level andtime after surgery, number of oocytes,and age for women with a unilateralsalpingectomy are shown in Figure 1,and the correlations for women with abilateral salpingectomy are shown inFigure 2. For women with a unilateralsalpingectomy, a significant linear cor-relation was found between AMH leveland time after surgery (r ¼ 0.399, P <.001) (Figure 1, A). No significant linearcorrelations were found between AMHand number of oocytes (r ¼ 0.145, P ¼.192) and age (r ¼ 0.141, P ¼ .202)(Figure 1, B and C, respectively). Forwomen with a bilateral salpingectomy,

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TABLE 1Patient characteristics

CharacteristicUnilateral salpingectomy(n [ 83)

Bilateral salpingectomy(n [ 41)

Without surgery(n [ 74) P value

Age, y 33.02 � 4.66 33.58 � 3.95 33.8 � 4.67 .553

AMH, (fmol/mL) 167.56 � 127.03 127.11 � 93.23 183.48 � 104.37a .037

E2, pg/mL 38.3 � 14.91 41.41 � 16.59 36.49 � 16.77 .291

Progesterone, nmol/L 0.52 � 0.29 0.55 � 0.33 0.54 � 0.32 .848

LH, mIU/mL 4.06 � 1.56 3.94 � 1.75 4.26 � 2.09 .63

FSH, 8.42 � 2.3 9.13 � 3.2 7.85 � 2.69y .048

AFC, 10.7 � 3.62 9.58 � 3.73 11.22 � 4.16 .097

BMI, kg/m2 21.63 � 2.46 21.1 � 2.85 21.43 � 2.83 .582

Testosterone 38.59 � 13.42 32.55 � 9.86 37.42 � 18.02 .152

Protocol .071

Short COH 52 (62.65) 17 (41.46) 38 (51.35)

Minimal ovarian stimulation 31 (37.35) 24 (58.54) 36 (48.65)

Reason for surgery < .001

Tuboovarian abscess 1 (1.2) 1 (2.44) �Ectopic pregnancy 79 (95.18) 24 (58.54) �Hydrosalpinx 3 (3.61) 16 (39.02) �

Primary infertility, y 0.31 � 1.13 0.82 � 1.96 3.6 � 4.15a,b < .001

Secondary infertility, y 2.85 � 2.81 3.23 � 3.24 2.36 � 3.32 .369

Reason of infertility

Unknown 0 (0) 0 (0) 2 (2.7) .184

Oligoasthenoteratospermia 41 (49.4) 15 (36.59) 28 (37.84) .239

Severe oligoasthenoteratospermia 2 (2.41) 1 (2.44) 6 (8.11) .178

Obstructive azoospermia 2 (2.41) 0 (0) 4 (5.41) .245

Both male and female factors 28 (52.83) 15 (55.56) 26 (55.32) .959

Data are presented as mean�standard deviation or count (percentage).

AFC, antral follicle count; AMH, antiMullerian hormone; BMI, body mass index; COH, controlled ovarian hyperstimulation; E2, estradiol; FSH, follicle stimulating hormone; LH, luteinizing hormone.

a P < .05, significantly different with unilateral salpingectomy group; b P < .05, significantly different with bilateral salpingectomy group.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

ajog.org Gynecology Research

no significant linear correlations werefound between AMH level and time aftersurgery (r¼�0.049, P¼ .760), numberof oocytes (r¼ 0.180, P¼ .260), and age(r ¼ �0.277, P ¼ .079) (Figure 2, A, B,and C, respectively). Significant linearcorrelations were found between AFCand number of oocytes in women witha bilateral salpingectomy, but not withunilateral salpingectomy (bilateral: r ¼0.348, P ¼ .028; unilateral: r ¼ �0.026,P ¼ .815) (Appendix; SupplementalFigures 1 and 2). No significant linear

correlations were found betweenAMH level and AFC in women with aunilateral salpingectomy (r ¼ �0.013,P ¼ .904) or with a bilateral salpingec-tomy (r ¼ 0.274, P ¼ .087) (Supple-mental Figures 3 and 4). No significantlinear correlation was found betweenAMH level and age in all women(r ¼ �0.067, P ¼ .352) (SupplementalFigure 5). A significant linear correlationwas found between AMH level and agein women without surgery (r ¼ �0.273,P ¼ .019) (Supplemental Figure 6).

JANUARY 2015 Ame

COMMENTThe results of this study showed thatAMH level was lower and FSH washigher in women that received a bilateralsalpingectomy than in those that hadnot received tubal surgery, although theAFC was similar between the 3 groups.In patients that had received a unilateralsalpingectomy, AMH was correlatedwith time after surgery but not with ageor number of oocytes retrieved andthere was no correlation between AFCand number of oocytes retrieved. In

rican Journal of Obstetrics & Gynecology 53.e3

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TABLE 2Patient treatment-related factors

VariableUnilateral salpingectomy(n [ 83)

Bilateral salpingectomy(n [ 41)

Without surgery(n [ 74) P value

Duration of Gn therapy, d 9.6 � 1.76 9.39 � 2.12 9.78 � 1.62 .523

Gn amount (vials) 23.75 � 10.31 23.77 � 10.79 24.95 � 9.85 .732

E2 level on the hCG injection day, pg/mL 3822.99 � 1630.06 3286.05 � 1629.64 3727.36 � 1891.94 .257

Thickness of endometrium, mm 9.84 � 3.3 8.98 � 2.58 9.84 � 2.95 .27

Number of oocytes retrieved 7.83 � 4.16 6.98 � 4.15 8.42 � 4.04 .199

Number of 2-pronuclear zygote 4.95 � 3.43 4.76 � 3.61 5.49 � 3.06 .453

Number viable embryos 3.39 � 3.03 3.15 � 2.51 3.5 � 2.6 .807

Number of good quality embryos 2.72 � 2.69 2.44 � 2.24 2.69 � 2.39 .826

Data reported as mean � standard deviation.

Gn, gonadotropin; E2, estradiol; hCG, human chorionic gonadotropin.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

Research Gynecology ajog.org

patients with a prior bilateral salpingec-tomy, AMH was not correlated with age,time after surgery, or number of oocytes

FIGURE 1Correlations of AMH level in women w

A, Correlation between AMH and time after sur

B, Correlation between AMH and number of oo

C, Correlation between AMH and age in women w

AMH, antiMullerian hormone.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 20

53.e4 American Journal of Obstetrics & Gynecolo

retrieved, although AFC was correlatedwith the number of oocytes retrieved.AMH and AFC were not correlated in

ith unilateral salpingectomy

gery in women with unilateral salpingectomy.

cytes in women with unilateral salpingectomy.

ith unilateral salpingectomy.

15.

gy JANUARY 2015

either the unilateral or bilateral sal-pingectomy groups, and AMH was notcorrelated with age in all women butcorrelated with age in the women thathad not received tubal surgery. Therewere no significant differences in dura-tion of gonadotropin therapy, amountof gonadotropin used, E2 level on thehCG injection day, thickness of theendometrium, number of oocytesretrieved, number of 2PN, viable em-bryos, and good quality embryos be-tween patients with unilateral orbilateral salpingectomy or those withno tubal surgery.

The fallopian tube is an essentialcomponent of the female reproductivesystem. The ovary is supplied by theovarian artery, but also by the ascendingbranch of the uterine artery in the mes-osalpinx. Some authors have reportedthat salpingectomy reduces the ovarianblood supply, and therefore compro-mises ovarian reserve.4,6 In our previousstudy,17 we compared the outcomes ofcontrolled ovarian hyperstimulationbetween patients before and after sal-pingectomy and found that unilateralsalpingectomy had little effect onovarian response to hyperstimulationtherapy, although bilateral salpingec-tomy was associated with reducedovarian sensitivity to gonadotropin, in-creased duration of gonadotropin ther-apy, and increased amount ofgonadotropin used. In the current study,

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FIGURE 2Correlations of AMH level in women with bilateral salpingectomy

A, Correlation between AMH and time after surgery in women with bilateral salpingectomy.

B, Correlation between AMH and number of oocytes in women with bilateral salpingectomy.

C, Correlation between AMH and age in women with bilateral salpingectomy.

AMH, antiMullerian hormone.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

ajog.org Gynecology Research

there were no statistically significantdifferences in days of gonadotropin use,amount of gonadotropin used, E2 levelon the hCG day, thickness of the endo-metrium, and the number of 2PN, viableembryos, and good quality embryos be-tween patients that had received a uni-lateral or bilateral salpingectomy or hadnot received tubal surgery; however,there was a stepwise trend among them.Fewer oocytes were retrieved from pa-tients who had received a bilateral sal-pingectomy as compared with thosewithout tubal surgery. Although the re-sults of this and our prior study are notidentical, they show a similar trend.

Lin et al9 examined 288 consecutivefresh IVF-ET cycles in 251 women whohad either laparoscopic salpingectomyor prior bilateral tubal sterilization, la-paroscopic tuboplasty, or proximal tubalocclusion, and reported no difference

in any ovarian response parametersbetween the salpingectomy and non-salpingectomy groups, and similar im-plantation rates, clinical pregnancy rates,and live birth rates. In addition, themean number of follicles and oocytesretrieved ipsilateral to the operated sidein the salpingectomy group were similarto that from the nonoperated ovary.Other authors have also reported thatsalpingectomy does not affect ovarianreserve or ovarian response to gonado-tropin stimulation.7,8,18 On the otherhand, Lass et al3 reported that in patientsundergoing IVF-ET who had received aprior salpingectomy significantly fewerfollicles developed and fewer oocyteswere retrieved from the ovary on theoperated side as compared with thenonoperated side. There was, however,no difference in the total number offollicles and oocytes retrieved from

JANUARY 2015 Ame

both ovaries, cycle characteristics, andpregnancy rates between patients thathad a prior salpingectomy and thosewith unexplained or male factorinfertility.

We believe that salpingectomy un-dermines the ovarian reserve. Becausesalpingectomy interrupts the ovarianblood supply from the ascending branchof the uterine artery, the ovary receivesless pituitary hormones, nutrition,and medication associated with IVF-ETtherapy. As a result, ovarian sensitivityto gonadotropin is reduced leading topoorer IVF-ET outcomes. Previousstudies have indirectly assessed theimpact of salpingectomy on ovaryfunction by comparing IVF-ET out-comes, and inconsistency in the litera-ture may be due to the many variablefactors during IVF-ET treatment anddifferent salpingectomy approaches.

In addition to IVF-ET outcomes,other commonly used indicators ofovarian reserve include age, basal FSHlevels, and AFC; however, their predic-tive ability can vary. AMH is a glyco-protein dimer and transforming growthfactor that regulates follicular recruit-ment and development.19 Serum AMHlevels in premenopausal women arerelatively constant, and do not vary withthe different phases of the menstrualcycle.11,13,20 In addition, oral contra-ceptives have little impact on serumAMH level.21,22 Therefore, AMH level,as compared with traditional mea-sures, is a superior indicator of ovarianreserve.11-14,19-22 AMH levels have beenshown to correlate with the number ofoocytes retrieved and percentage of MIIoocytes in patients undergoing IVF-ET.23 Another study has shown thatfollicular fluid AMH level is positivelycorrelated with follicle sensitivity toFSH,24 and has suggested that there isan association between follicular fluidAMH level and the quality of embryosin polycystic ovarian syndrome patientsundergoing IVF-ET.25 Lin et al26 re-ported that AMH level was correlatedwith good quality embryos and blasto-cysts in patients undergoing IVF-ET,and that follicular fluid AMH levelcorrelated with the clinical pregnancyand live birth rates.

rican Journal of Obstetrics & Gynecology 53.e5

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In the current study, the patients inthe 3 groups were of similar age, and thustheir basal hormone levels and AFC werecomparable. The results showed that onthe initiation day of ovulation induction,there was a stepwise decrease in serumAMH levels from patients without tubalsurgery to patients with unilateral sal-pingectomy, and from patients withunilateral salpingectomy to patients withbilateral salpingectomy (P < .05). AMHis secreted primarily by granulocytesof preantral follicles and small antralfollicles.10 With a decreased ovarianblood supply after salpingectomy, therecruitment and development of folliclesis compromised, leading to reducedAMH secretion from follicular gran-ulocytes. This phenomenon may explainthe cause of reduced serum AMH levelsafter salpingectomy. Patients with bilat-eral salpingectomy had a lower AFC thanthose without tubal surgery, whereasthere was no statistically significant dif-ference in AFC between patients withunilateral salpingectomy and thosewithout tubal surgery. In addition, FSHlevel was greater in the bilateral sal-pingectomy group than in the groupthat had not received tubal surgery.Taken together, these data suggest thatsalpingectomy affects ovarian reserve.

To elucidate whether ovary functionis restored after unilateral salpingectomythrough compensation of the bloodsupply from the ovarian artery, we con-ducted a correlation analysis betweenthe duration after unilateral salpingec-tomy and AMH levels, and the analysisrevealed AMH level was correlatedwith time after surgery, but there wasno correlation with age and number ofoocytes retrieved. In the bilateral sal-pingectomy group, there was no corre-lation between AMH level and timeafter surgery, age, or number of oocytesretrieved. Interestingly, Findley et al27

compared AMH levels in patients whoreceived bilateral salpingectomy or nosalpingectomy at the time of laparo-scopic hysterectomy with ovarian pres-ervation and found no difference inAMH levels between the 2 groups at3 months postoperatively, and no de-crease in AMH level from the baselinevalue in either group. Their study, as

53.e6 American Journal of Obstetrics & Gynecolo

stated, only examined levels at 3 monthafter surgery.Studies comparing AMH and AFC

typically see a correlation of AMH withAFC and with the number of oocytesretrieved. In the current study, AFCwas only correlated with the number ofoocytes retrieved in the bilateral sal-pingectomy group; no correlation wasseen in the unilateral group and nocorrelation between AMH and numberof oocytes was seen in either the unilat-eral or bilateral groups. In addition, asignificant correlation between AMHlevel and age in women that had notreceived surgery was seen, but no cor-relations with age were seen in the sal-pingectomy groups. The reasons forthese finding are difficult to determine.In the present study, serum AMH wasused for analysis, not follicle fluid AMH,which may reflect the AMH stimulationstatus more directly. There are also somereports that indicate that AMH mightnot be associated with oocytes numbers,and the possible reasons might be relatedto complicated communication path-ways and the effects of hormones, andthe detailed interactions still requirefurther study.26,28,29 To consider whetherthis may be due to the different pop-ulations assessed, we analyzed whetherAMH level, oocyte number, and AFCdiffered according to the reason forsurgery and found no significant differ-ences (data not shown). In addition,changes of AMH with aging may differwith ethnic background.30

There are some limitations to thisstudy that should be considered. Thenumber of patients was relatively small,and a post hoc power analysis indicatedthat the calculated power was <0.8,the standard of adequacy, for most var-iables. AMH levels before salpingectomywere not available. We did not examineother IVF-ET outcomes such as im-plantation, clinical pregnancy, and livebirth rates. Patients that choose the shortinduction protocol at our institutionalmost all desire to freeze the embryoswith implantation some years later.Thus, pregnancy outcome data are notavailable. Different ovarian inductionprotocols were used making it difficultto compare variables such as dosages of

gy JANUARY 2015

gonadotropins and oocytes retrieved.However, both are short protocols andare known to have similar effects. Lastly,the mean age of the study population islow in comparison with that of womenin most countries applying for IVF. Atour institution, many women choose toundergo ovulation induction and IVFand freezing soon after surgery suchthat the mean age of patients is lowerthan that typically seen in studies ofthis nature.

CONCLUSIONS

Salpingectomy is associated with de-creased AMH level and increased FSHin women seeking IVF, though AMHlevel is not correlated with the numberof oocytes retrieved in patients thathave undergone unilateral or bilateralsalpingectomy. Although the resultsindicate an association, they should notbe interpreted as implying causation. -

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APPENDIX

SUPPLEMENTAL FIGURE 1Correlation between AFC and number of oocytes in womenwith unilateralsalpingectomy

AFC, antral follicle count.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

SUPPLEMENTAL FIGURE 2Correlation between AFC and number of oocytes in women with bilateralsalpingectomy

AFC, antral follicle count.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

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SUPPLEMENTAL FIGURE 3Correlation between AMH and AFC in women with unilateralsalpingectomy

AFC, antral follicle count; AMH, antiMullerian hormone.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

SUPPLEMENTAL FIGURE 4Correlation between AMH and AFC inwomenwith bilateral salpingectomy

AFC, antral follicle count; AMH, antiMullerian hormone.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

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SUPPLEMENTAL FIGURE 5Correlation between AMH and age in all women

AMH, antiMullerian hormone.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

SUPPLEMENTAL FIGURE 6Correlation between AMH and age in women without tubal surgery

AMH, antiMullerian hormone.

Ye. Salpingectomy and ovarian reserve. Am J Obstet Gynecol 2015.

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53.e10 American Journal of Obstetrics & Gynecology JANUARY 2015