hum. reprod.-2014-muzii-humrep-deu199.pdf

7/25/2019 Hum. Reprod.-2014-Muzii-humrep-deu199.pdf

1/9

META-ANALYSISGynaecology

The effect of surgery for endometrioma

on ovarian reserve evaluated by antral

follicle count: a systematic review and

meta-analysis

Ludovico Muzii*, Chiara Di Tucci, Mara Di Feliciantonio,

Claudia Marchetti, Giorgia Perniola, and Pierluigi Benedetti Panici

Department of Obstetrics and Gynecology, Sapienza University of Rome, Viale del Policlinico 155, Rome 00161, Italy

*Correspondence address. Tel: +39-06-4940550; Fax: +39-06-49973128; E-mail: [email protected]

Submitted on May 14, 2014; resubmitted on June 16, 2014; accepted on July 8, 2014

study question: Does surgical treatmentof endometriomas impact on theovarian reserve as evaluated with antralfollicle count (AFC)?

summaryanswer: Thismeta-analysisof published datashows thatsurgeryfor endometrioma does not significantly affect ovarian reserve

as evaluated by AFC.

what is known already: Surgical excision of an ovarian endometrioma significantly affects ovarian reserve evaluated with anti-Mul-

lerian hormone (AMH) levels. Data for other reliable markers of ovarian reserve, such as AFC, have not been pooled in meta-analyses.

study design, size, duration: A systematicreviewwith electronic searchesof PubMed, MEDLINEand Embase up to April 2014was

conductedto identifyarticlesevaluatingAFC before andafter surgery forovarianendometriomas, or before or aftersurgery forthe affectedversus

the contralateral ovary.

participants/materials, setting, methods: Of the24 studies evaluatedin detail, 13 were included fordata extraction and

meta-analysis, including a total of 597 patients. The primary outcome at pooled analysis was AFC (mean and SD) for affected ovaries before andafter surgery. Secondary outcomes were AFC for the affected ovary versus the contralateral ovary before surgery, and AFC for the operated

versus the contralateral ovary after surgery. The data were pooled using the RevMan software by the Cochrane Collaboration. Heterogeneity

between studies was based on the results of the x2 andI2 statistics. A random-effect model was used for the meta-analysis because of high het-

erogeneity between studies.

main results and the role of chance: AFC for the operated ovary did not change significantly after surgery (mean difference

0.10, 95% CI 21.45 to 1.65;P 0.90). Lower AFC for the diseased ovary compared with the contralateral one was present before surgery,

although the difference was not significant (mean difference 22.79, 95% CI 27.10 to 1.51; P 0.20). After surgery, the operated ovary

showed a significantly lower AFC compared with the contralateral ovary (mean difference 21.40, 95% CI 22.27 to 20.52;P 0.002).

limitations, reasons for caution: Heterogeneityamong the selected studies washigh; therefore, limiting the conclusions of the

present systematic review.

wider implications of the findings: Ovarian reserve evaluated with AFC is not reduced after surgical treatment of an endo-

metrioma. A lower AFC is present for the affected ovary both before and after surgery. Recently, concerns have been raised as to the reliabilityof AMH as a marker of ovarian reserve. Based on the present findings, surgical treatment of an endometrioma may be considered safer for the

ovarian reserve than previously thought.

study funding/competing interests: No external funding was sought or obtained for this study. No conflicts of interest are

declared.

Keywords: antral follicle count / endometrioma / endometriosis / laparoscopy / ovarian reserve

& The Author 2014. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved.

For Permissions, please email: [email protected]

HumanReproduction, Vol.0,No.0 pp.19, 2014

doi:10.1093/humrep/deu199

Hum. Reprod. Advance Access published August 1, 2014


2/9

Introduction

Ovarian endometriomas are present in 1744% of patients with endo-

metriosis, and may be associated with infertility, dysmenorrhea and

chronic pelvic pain (Gelbaya and Nardo, 2011).

The standard approach to the ovarian endometrioma is laparoscopic

excision of the cyst capsule with the stripping technique ( Hart et al.,

2008). Evidence-based guidelines suggest surgical excision in case of

symptomatic or large (.3 cm) endometriomas (Leylandet al., 2010;

Dunselmanet al., 2014).

Recently, however, concerns have been raised as to the possibility of

damage to the ovarian reserve after excision of the endometrioma

(Shah et al., 2014). Poorer responses to gonadotrophin stimulation

for in vitro fertilization (IVF) have been reported for ovaries which

have been subjected to excisional surgery (Nargundet al., 1996;Loh

et al., 1999;Somiglianaet al., 2003;Shahet al., 2014). A higher prema-

ture ovarian failure rate (Busacca et al., 2006) and a younger age at

menopause (Cocciaet al., 2011) have also been reported after excision

of bilateral ovarian endometriomas. Two recent systematic reviews

have reported consistent evidence on the reduction of ovarian

reserve, evaluated with serum anti-Mullerian hormone (AMH) levels,after excisional surgery for endometriomas (Raffiet al., 2012;Somigli-

anaet al., 2012). Non-excisional techniques for the surgical treatment

of ovarian endometriomas have been suggested by some authors as

more respectful of ovarian reserve (Flyckt and Falcone, 2013).

However, no study on non-excisional techniques was found in one of

the two systematic reviews (Raffi et al., 2012), whereas such studies

were intentionally excluded from the second systematic review

(Somiglianaet al., 2012).

AMH has gained wide popularity as a marker of ovarian reserve as it

offers several advantages compared with other markers; it is stable

throughout the menstrual cycle and it is relatively independent of the

use of hormonal therapy (Practice Committee of the American Society

for Reproductive Medicine, 2012; Rosen et al., 2012; Nelson, 2013;Toner and Seifer, 2013;Shahet al., 2014). Although an ever-expanding

body ofliteratureis availableon theeffectof surgical excisionof endome-

triomas on modifications of the levels of AMH, some methodological

problems, such as sample instability, have recently emerged and some

authorsaffirm thatcautionshouldpresently be exercisedin theinterpret-

ation of AMHlevels in the clinical setting (Rustamovet al., 2012; Ledger,

2014;Muziiet al., 2014).

Antral follicle count (AFC) has been demonstrated to be a reliable

marker of ovarian reserve, since it correlates significantly with the

age-related follicle count decline,and withovarianresponse to IVFstimu-

lation cycles (Practice Committee of the American Society for Repro-

ductive Medicine, 2012;Rosenet al., 2012;Nelson, 2013). Compared

with AMH, AFC has the advantage of correlating directly with the

ovarian reserve of a single ovary. On the other hand, AMH, being a sys-

temic serum marker, expresses the ovarian reserve of both ovaries,

where a balancing effect of a healthy ovary may compensate for a

reduced ovarian reserve in the contralateral, affected ovary. In the

setting of possible damage to theovarianreserveattributableto thepres-

enceoftheendometrioma,toitssurgicaltreatment,ortoboth,AFCmay

control forthe laterality of thedisease andtherefore be a more accurate

marker than AMH.

No systematic review on the use of AFC to evaluate the effect of sur-

gical treatment of endometriomas on ovarian reservehas beenpublished

in the literature so far. The aim of the present systematic review and

meta-analysis was to answer the question of whether surgery for an

ovarian endometrioma has an impact on theovarianreserveas evaluated

by AFC.

Materials andMethods

The present systematic review included all published research articles thatevaluated AFC as a marker of ovarian reserve in patients undergoing

surgery of ovarian endometriomas and reported comparisons of AFC

before and after surgery in the same patients, or before or after surgery for

the affected ovary versus the contralateral, unaffected ovary.

All articles reporting complete surgical excision of the endometrioma

were included. Articles reporting alternative surgical techniques, such as

vaporization or coagulation of the cyst wall, or a combination of the above,

were also included. Non-excisional techniques were pooled separately

from excisional techniques in meta-analysis.

Studies were excluded if reporting surgery for recurrence of endometrio-

mas.Studieswere alsoexcludedif medical therapy,either withGnRH analogs

or oral contraceptives, was used in the cycle in which AFC measurements

were obtained. Articles reporting measurements of AFC obtained at ovula-

tion inductionforIVF were includedonlyif anearlyfollicular phaseAFC meas-urement was reported, and if no GnRH agonist or oral contraceptives were

used in the induction protocol.

Studies considered were randomized clinical trials (RCTs), prospective

controlled studies, prospective cohort studies or retrospective studies.

Onlyarticles written in English wereincluded. Proceedingsof scientific meet-

ings were not included.

An electronic database search was performed using MEDLINE, PubMed

and Embase for the identification of articles published until 30 April 2014,

using the combination of the following search terms: endometriosis,

endometrioma, endometriotic cyst, ovarian reserve, AFC, laparoscopy,

laparotomy, cystectomy, excision, laser, ablation techniques and bipolar co-

agulation. The above search was conducted independently by three investi-

gators. Following the search, all articles considered pertinent on the basis of

the title and abstract were retrieved, and their reference lists were searchedfor additional potential studies.

Subsequently, three investigators independently read the full text of the

pre-selectedarticlesin orderto verifythepertinenceof thearticles tothe sys-

tematic reviewon AFCas a markerof ovarianreserveafter surgical treatment

of ovarian endometriomas. After confirmation of pertinence, studies were

excluded if they were reporting an ad interim analysis subsequently published

as full reportor reportingduplicate data sets.In case of data judgedas pertin-

entbutreportedin formsnot appropriatefor meta-analysis, incaseof incom-

plete data or incaseof uncertainty on any of the above issues, the authors of

the original articles were contacted in order to obtain the information

needed.

In the event of disagreement on the inclusion or exclusion of the pre-

selected studies for the meta-analysis, or for any other disagreement

through the review process as outlined above, consensus was reachedafter discussion, or after involvement of further investigators. Data from

included studies wereindependentlycollectedby threeinvestigators on stan-

dardized forms.

The primary analysis was aimed at evaluation of the change in AFC after

surgery, with the primary outcome output expressed as the mean weighted

difference in AFC values after surgery compared with AFC values before

surgery. Additional analyses wereperformedto evaluate two secondaryout-

comes: the difference in mean AFCs between the ovary with the endome-

trioma and the contralateral, unaffected ovary before surgery and the

difference in mean AFCs between the operated ovary and the contralateral

ovary after surgery.

2 Muziiet al.


3/9


4/9


5/9

.................................................................................................................................................................................................

TableI Characteristics of the studies included in the systematic review.

Author,

year

Study

design

Number of

patients

Mean age+++++SD

(years)

Mean cyst

diameter+++++SD (cm)

Unilateral/

bilateral

Follow-up

timing

(months)

Diamete

AFC me

Alborziet al.

(2014)

Prospective

cohort

193 28.4+5.4 NR 121/72 3 210

Auberet al.

(2011)

Retrospective 10 32.4+6.2 4.8+2.8 10/0 35 NR

Biacchiardi et al.

2011)

Prospective

cohort

43 34.2+5.4 3.7+1.1 33/10 3, 9 .3

Celiket al.

(2012)

Prospective

cohort

65 28.4+5.7 6.4+2.8 46/19 1.5, 6 210

Donnezet al.

(2010)

Prospective

cohort

20 29.2+3.7 4.6+1.3 20/0 6 NR

Ercanet al.

(2011)

Prospective

cohort

36 29.4+4.6 5.2+1.4 36/0 2nd day, 3 NR

Muzii and Panici

(2010)

Prospective

cohort

12 NR NR 12/0 6 NR

Takashima et al.

(2013)aRetrospective 44 36.2+1.9 (Arm a)

35.3+1.6 (Arm b)

6.7+0.9 (Arm a)

6.2+0.7 (Arm b)

44/0 3 210

Tsolakidiset al.

(2010)

RCT 20 32.8+1.7 3.8+0.5 NR 6 ,9

Uncuet al.

(2013)

Prospective

cohort

30 29.0+5.4 4.3 (IQR 3.95.2) 15/15 1, 6 29

Urmanet al.

(2013)

Prospective

cohort

25 32.7+6.1 5.2+1.5 25/0 1, 6 210

Varet al. (2011) RCT 48 27.0+3.9 4.4 (SD NR) 0/46 6 ,9

Zaitounet al.

(2013)

RCT 61 24.2+3.1 NR 61/0 6, 12, 18 NR

SD, standard deviation; AFC, antral follicle count; NR, not reported; RCT, randomized controlled trial; IQR, interquartile range.aArm a suture; Arm b bipolar coagulation.

byguestonDecember22,2015 http://humrep.oxfordjournals.org/ Downloadedfrom
http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/http://humrep.oxfordjournals.org/


6/9

after conservative surgery, especially for ovarian endometriomas

(Nargundet al., 1996;Raffiet al., 2012;Somiglianaet al., 2012).

Among other markers of ovarian reserve, AMH and AFC have been

shown to best correlate with the pattern of age-related oocyte loss

observed histologically (Rosenet al., 2012), and are therefore consid-

ered the most reliable non-invasive methods of ovarian reserve evalu-

ation (Practice Committee of the American Society for Reproductive

Medicine, 2012;Nelson, 2013).

Surgical excision is considered the mostappropriate techniquefor the

treatment of ovarian endometriomas (Hartet al., 2008;Leylandet al.,

2010;Dunselmanet al., 2014). Recently, however, some concern has

been raisedas tothe possibilitythatsurgicalexcision of theovarianendo-

metrioma may negatively impact on the ovarian reserve of the operated

ovary. The decrease in the ovarian reserve after surgery may be due to

the inadvertent excision of unaffected ovarian tissue together with the

diseased tissue (Hachisuga and Kawarabayashi, 2002; Muzii et al.,

2002;Muziiet al., 2007).

Evidence of a reduced ovarian reserve has been published in two

recent systematic reviews (Raffi et al., 2012;Somigliana et al., 2012),

reporting a decrease of the levels of AMH after surgery. In the

meta-analysis performed byRaffiet al. (2012), a statistically significant

fall of 38% for AMH levels was reported after excisional surgery, with a

weighted mean difference of 21.13 ng/ml (95% confidence interval

21.88 to 20.37) following cyst excision. No study was identified for

non-excisional techniques.Somiglianaet al. (2012), reporting that 9 of

the 11 studies included in their systematic review documented a

Figure 2 Meta-analysis. Weighted mean difference in AFC before and after excisional surgery for endometrioma performed at laparoscopy (LPS).

Figure 3 Meta-analysis. Weighted mean difference in AFC beforeand after non-excisional surgery for endometrioma performed at laparoscopy (LPS).

Figure 4 Meta-analysis. Weighted mean difference in AFC for the affected versus unaffected ovary before surgery.

6 Muziiet al.


7/9


8/9

onlybe consideredafterthe efficacyof surgicaltreatment on the present-

ingsymptom(s)has beenaccountedfor. Surgeryfor theovarianendome-

trioma is efficacious when pain or infertility is present ( Vercellini et al.,

2009;Leylandet al., 2010;Duffyet al., 2014;Dunselmanet al., 2014).

The possibility of a reduced ovarian reserve should be discussed with

the patient, but this issue should not however change the well-defined

indications to surgery, especially when the evidence supporting

damage to the ovarian reserve are inconclusive or inconsistent, as is

the case for surgery for the ovarian endometrioma.

In conclusion, surgery for the endometrioma has beenassociated with

impaired ovarian reserve. Systematic reviews on AMH as a marker for

the reduced ovarian reserve, however, have highlighted the heterogen-

eity of the published studies and the difficulty in pooling the data (Raffi

et al., 2012; Somigliana et al., 2012). AFC may be a more specific

markerof ovarian reserve related to surgery, since it controls for lateral-

ity of the possible damage. In the present systematic review and

meta-analysis, AFC did not appear to change significantly after surgery.

The affected ovary had lower AFC both before and after surgery.

Further researchis requiredto betterclarifythe relativeroleof theendo-

metrioma perse orof surgical excision in thedetermination of damageto

the ovarian reserve. Additional studies witha direct comparison of AMHandAFCin a long-termfollow-upareneededin orderto betterclarify the

role of both markers in the assessment of the impact of surgery on the

ovarian reserve. RCTs with adequate sample sizes are necessary to

compare different surgical techniques. Investigation of the impact of

surgery for the endometrioma on ovarian reserve should still be consid-

ered a research priority in reproductive medicine.

Authors roles

All authors made substantial contributions to the conception and design

of the study, acquisition of data,analysis and interpretationof data,draft-

ingof thearticleor criticalrevisions for importantintellectualcontentand

final approval of the manuscript.

Funding

No external funding was sought or obtained for this study.

Conflict of interest

None declared.

ReferencesAlborzi S, Keramati P, Younesi M, Samsami A, Dadras N. The impact of

laparoscopic cystectomy on ovarian reserve in patients with unilateral

and bilateral endometriomas.Fertil Steril2014;101:427434.

Almog B, Sheizaf B, Shalom-PazE, Shehata F, Al-TalibA, Tulandi T. Effects of

excision of ovarianendometriomaon theantral follicle countand collected

oocytes forin vitrofertilization.Fertil Steril2010;94:23402342.

Auber M,Bourdel N, Mokdad C, Martin C, Diguet A, Marpeau L, Roman H.

Ultrasound ovarian assessments after endometrioma ablation using

plasma energy.Fertil Steril2011;95:26212624.

BiacchiardiCP, PianeLD, Camanni M, Deltetto F,DelpianoEM, MarchinoGL,

Gennarelli G, Revelli A. Laparoscopic stripping of endometriomas

negatively affects ovarian follicular reserve even if performed by

experienced surgeons.Reprod Biomed Online2011;23:740746.

Bongioanni F, Revelli A, Gennarelli G, Guidetti D, Delle Piane LD, Holte J.

Ovarian endometriomas and IVF: a retrospective case-control study.

Reprod Biol Endocrinol2011;9:81.

Busacca M, Riparini J, Somigliana E, Oggioni G, Izzo S, Vignali M, Candiani M.

Postsurgical ovarian failure after laparoscopic excision of bilateral

endometriomas.Am J Obstet Gynecol2006;195:421425.

Candiani M, Barbieri M, Bottani B, Bertulessi C, Vignali M, Agnoli B,

Somigliana E, Busacca M. Ovarian recovery after laparoscopic enucleation

of ovarian cysts: insights from echographic short-term postsurgicalfollow-up. J Minim Invasive Gynecol2005;12:409414.

Carmona F,Martnez-ZamoraMA, RabanalA, Martnez-Roman S, Balasch J.

Ovarian cystectomy versus laser vaporization in the treatment of ovarian

endometriomas: a randomized clinical trial with a five-year follow-up. Fertil

Steril2011;96:251254.

Celik HG, Dogan E, Okyay E, Ulukus C, Saatli B, Uysal S, Koyuncuoglu M.

Effect of laparoscopic excision of endometriomas on ovarian reserve:

serial changes in the serum antiMullerian hormone levels. Fertil Steril

2012;97:14721478.

Chang HJ, Han SH, Lee JR, Jee BC, Lee BI, Suh CS, Kim SH. Impact of

laparoscopic cystectomy on ovarian reserve: serial changes of serum

anti-Mullerian hormone levels.Fertil Steril2010;94:343349.

Coccia ME,Rizzello F, MarianiG, Bulletti C, Palagiano A, Scarselli G. Ovarian

surgery for bilateral endometriomas influences age at menopause.HumReprod2011;26:30003007.

Coric M, Barisic D, Pavicic D, Karadza M, Banovic M. Electrocoagulation

versus suture after laparoscopic stripping of ovarian endometriomas

assessed by antral follicle count: preliminary results of randomized

clinical trial.Arch Gynecol Obstet2011;283:373378.

Donnez J, Lousse JC, Jadoul P, Donnez O, Squifflet J. Laparoscopic

management of endometriomas using a combined technique of

excisional (cystectomy) and ablative surgery.Fertil Steril2010;94:2832.

Duffy JM,Arambage K, CorreaFJ, Olive D, Farquhar C, Garry R, Barlow DH,

Jacobson TZ. Laparoscopic surgery for endometriosis. Cochrane Database

Syst Rev2014;4:CD011031.

Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, DHooghe T, De

Bie B,Heikinheimo O,Horne AW, Kiesel L,Nap A etal. ESHREguideline:

management of women with endometriosis. Hum Reprod 2014;29:400412.

Ercan CM, Duru NK, Karasahin KE, Coksuer H, Dede M, Baser I.

Ultrasonographic evaluation and anti-Mullerian hormone levels after

laparoscopic stripping of unilateral endometriomas. Eur J Obstet Gynecol

Reprod Biol2011;158:280284.

Flyckt RL, Falcone T. Optimizing the surgical management of endometriomas.

J Minim Invasive Gynecol2013;20:539540.

Gelbaya TA, Nardo LG. Evidence-based management of endometrioma.

Reprod Biomed Online2011;23:1524.

Hachisuga T, Kawarabayashi T. Histopathological analysis of laparoscopically

treated ovarian endometriotic cysts with special reference to loss of

follicles.Hum Reprod2002;17:432435.

Hart RJ, Hickey M, Maouris P, Buckett W. Excisional surgery versus ablative

surgery for ovarian endometriomata. Cochrane Database Syst Rev2008;

2:CD004992.

Jang WK, Lim SY, Park JC, Lee KR, Lee A, Rhee JH. Surgical impact on serum

anti-Mullerian hormone in women with benign ovarian cyst: a prospective

study.Obstet Gynecol Sci2014;57:121127.

KitajimaM, DefrereS, DolmansMM,Colette S,SquiffletJ, VanLangendoncktA,

Donnez J. Endometriomas as a possible cause of reduced ovarian reserve in

women with endometriosis.Fertil Steril2011;96:685691.

Ledger WL. Measurement of antiMullerian hormone: not as straightforward

as it seems.Fertil Steril2014;101:339.

Leyland N, Casper R, Laberge P, Singh SS. Endometriosis: diagnosis and

management. J Obstet Gynaecol Can2010;32:S1S32.

8 Muziiet al.


9/9

Li CZ, Liu B, Wen ZQ, Sun Q. The impact of electrocoagulation on ovarian

reserve after laparoscopic excision of ovarian cysts: a prospective clinical

study of 191 patients.Fertil Steril2009;92:14281435.

Loh FH, Tan AT, Kumar J, Ng SC. Ovarian response after laparoscopic

ovarian cystectomy for endometriotic cysts in 132 monitored cycles.

Fertil Steril1999;72:316321.

Maneschi F, MarasaL, Incandela S, Mazzarese M, Zupi E. Ovarian cortex

surrounding benign neoplasms: a histologic study. Am J Obstet Gynecol

1993;169:388393.Muzii L, Miller CE. The singer, not the song. J Minim Invasive Gynecol2011;

18:666667.

Muzii L, Panici PB. Combined technique of excision and ablation for the

surgical treatment of ovarian endometriomas: the way forward? Reprod

Biomed Online2010;20:300302.

Muzii L, Bianchi A, CroceC, Manci N, Panici PB. Laparoscopic excision of

ovarian cysts: is the stripping technique a tissue-sparing procedure?Fertil

Steril2002;77:609614.

Muzii L, Angioli R, Zullo M, Panici PB. The unexpected ovarian malignancy

found during operative laparoscopy: incidence, management, and

implications for prognosis.J Minim Invasive Gynecol2005;12:8189.

Muzii L,Bianchi A,Bellati F,Cristi E,Pernice M, Zullo MA,Angioli R,Panici PB.

Histologic analysis of endometriomas: what the surgeon needs to know.

Fertil Steril2007;87:362366.Muzii L,Luciano AA,ZupiE, PaniciPB. Effectof surgery forendometrioma on

ovarian function: a different point of view.J Minim Invasive Gynecol2014;

21:531533.

Nargund G, Cheng WC, Parsons J. The impact of ovarian cystectomy on

ovarian response to stimulation during in vitro fertilization cycles. Hum

Reprod1996;11:8183.

NelsonSM. Biomarkers of ovarian response:current and future applications.

Fertil Steril2013;99:963969.

Pados G, Tsolakidis D, Assimakopoulos E, Athanatos D, Tarlatzis B.

Sonographic changes after laparoscopic cystectomy compared with

three-stage management in patients with ovarian endometriomas: a

prospective randomized study.Hum Reprod2010;25:672677.

Practice Committee of the American Society for Reproductive Medicine.

Testing and interpreting measures of ovarian reserve: a committeeopinion.Fertil Steril2012;98:14071415.

Raffi F,MetwallyM, Amer S.The impactof excision ofovarian endometrioma

on ovarianreserve: a systematic review and meta-analysis.J Clin Endocrinol

Metab2012;97:31463154.

Roman H, Auber M,MokdadC, Martin C, Diguet A, Marpeau L, Bourdel N.

Ovarianendometrioma ablation usingplasma energyversuscystectomy: a

step toward better preservation of the ovarian parenchyma in women

wishing to conceive.Fertil Steril2011;96:13961400.

Rosen MP, Johnstone E, McCulloch CE, Schuh-Huerta SM, Sternfeld B,

Reijo-Pera RA, Cedars MI. A characterization of the relationship of

ovarian reserve markers with age.Fertil Steril2012;97:238243.

Rustamov O, Smith A, Roberts SA, Yates AP, Fitzgerald C, Krishnan M,

Nardo LG, Pemberton PW. Anti-Mullerian hormone: poor assay

reproducibility in a large cohort of subjects suggests sample instability.

Hum Reprod2012;27:30853091.

Shah DK,MejiaRB,LebovicD. Effectof surgery forendometrioma onovarian

function.J Minim Invasive Gynecol2014;21:203209.

Somigliana E, Ragni G, Benedetti F, Borroni R, Vegetti W, Crosignani PG.

Does laparoscopic excision of endometriotic ovarian cysts significantly

affect ovarian reserve? Insights from IVF cycles. Hum Reprod 2003;

18:24502453.

Somigliana E, Berlanda N, Benaglia L, ViganoP, Vercellini P,Fedele L. Surgical

excision of endometriomas and ovarian reserve: a systematic review on

serum antiMullerian hormone level modifications. Fertil Steril 2012;98:15311538.

Sugita A, Iwase A, Goto M, Nakahara T, Nakamura T, Kondo M, Osuka S,

Mori M, Saito A, Kikkawa F. One-year follow-up of serum antiMullerian

hormone levels in patients with cystectomy: are different sequential

changes due to different mechanisms causing damage to the ovarian

reserve?Fertil Steril2013;100:516522.

Takashima A, Takeshita N, Otaka K, Kinoshita T. Effects of bipolar

electrocoagulation versus suture after laparoscopic excision of ovarian

endometrioma on the ovarian reserve and outcome of in vitro

fertilization.J Obstet Gynaecol Res2013;39:12461252.

Tang Y, Chen SL, Chen X, He YX, Ye DS, Guo W, Zheng HY, Yang XH.

Ovarian damage after laparoscopic endometrioma excision might be

related to the size of cyst.Fertil Steril2013;100:464469.

TonerJP, SeiferDB. Why we mayabandon basalfollicle-stimulating hormonetesting: a sea change in determining ovarian reserve using antiMullerian

hormone.Fertil Steril2013;99:18251830.

Tsolakidis D, Pados G, Vavilis D, Athanatos D, Tsalikis T, Giannakou A,

Tarlatzis BC. The impact on ovarian reserve after laparoscopic

ovarian cystectomy versus three-stage management in patients with

endometriomas:a prospective randomizedstudy.Fertil Steril2010;94:7177.

Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B.

Prospective assessment of the impact of endometriomas and their

removal on ovarian reserve and determinants of the rate of decline in

ovarian reserve.Hum Reprod2013;28:21402145.

Urman B, Alper E, Yakin K, Oktem O, Aksoy S, Alatas C, Mercan R, Ata B.

Removal of unilateral endometriomas is associated with immediate and

sustained reduction in ovarian reserve. Reprod Biomed Online 2013;

27:1216.Var T, Batioglu S, Tonguc E, Kahyaoglu I. The effect of laparoscopic ovarian

cystectomy versus coagulation in bilateral endometriomas on ovarian

reserve as determined by antral follicle count and ovarian volume: a

prospective randomized study.Fertil Steril2011;95:22472250.

Vercellini P, Somigliana E, ViganoP, Abbiati A, Barbara G, Crosignani PG.

Surgery for endometriosis-associated infertility: a pragmatic approach.

Hum Reprod2009;24:254269.

Yu HT, Huang HY, Soong YK, Lee CL, Chao A, Wang CJ. Laparoscopic

ovarian cystectomy of endometriomas: surgeons experience may affect

ovarian reserve and live-born rate in infertile patients with in vitro

fertilization-intracytoplasmic sperm injection. Eur J Obstet Gynecol Reprod

Biol2010;152:172175.

Zaitoun MM, Zaitoun MM, El Behery MM. Comparing long term impact on

ovarian reserve between laparoscopic ovarian cystectomy and open

laparotomy for ovarian endometrioma.J Ovarian Res 2013;6:76.

Antral follicle count after endometrioma surgery 9

hum. reprod.-2014-muzii-humrep-deu199.pdf

Documents