{"paper_id":"0254f9b3-8e98-4e42-883f-f792a54ec28a","body_text":"Is there a risk to ovarian reserve and fertility from ovarian cystectomy? \nNeerujah Balachandren 1, Ephia Yasmin 2, Dimitrios Mavrelos 3 and Ertan Saridogan 4 \n \nAbstract \n \nKey Content \n Physiology of benign ovarian cysts, their risk of recurrence, rate of growth and possible impact \non fertility \n Management of benign ovarian cysts in children and adolescents \n Impact of ovarian torsion on ovarian reserve  \n Impact of ovarian cystectomy on spontaneous conception, ovarian reserve and IVF outcomes.  \n Comparison of surgical techniques on the basis of fertility outcomes \n Good practice points when planning a cystectomy for benign ovarian cysts  \n \nLearning objectives  \n Consider performing ovarian reserve assessments prior to any surgery on the ovary in women \nwho have not completed their family.  \n Assess patients who may be at risk for compromised ovarian reserves and discuss fertility \npreservation options prior to any surgery on the ovaries.  \n Children and adolescents presenting with pathological ovarian cysts require a multi-\ndisciplinary team approach and where possible fertility sparing treatment should be offered. \n Laparoscopic detorsion appears to preserve ovarian reserve and this should remain the \noptimal treatment for ovarian torsion \n Obtain appropriate consent prior to any surgery on the ovary, including the risks of \noophorectomy or reduced ovarian reserve. \n\n Take anatomical considerations into account in order to reduce the risk of bleeding and \nminimise damage to healthy ovarian tissue \n \n \nEthical Issues \n Oocyte freezing is not routinely funded by the NHS for benign conditions. \n Although it would be ideal to do pre-operative ovarian reserve testing on all women of child \nbearing age who have not yet completed their family, the lack NHS funding and financial \nconstraints present ethical concerns to the clinician and patient. \n \n  \nKey words \nOvarian cysts, ovarian cystectomy, fertility, ovarian reserve assessments, endometriomas, dermoid \ncysts  \n \n \n \n \n \n \n \n \n\nIntroduction  \n \nOvarian cystectomy is a frequently performed surgical procedure for the management of benign \novarian cysts in pre-menopausal women (1, 2). The procedure is usually performed to prevent cyst \ncomplications such as pain, rupture or torsion, or due to concern of malignancy, whilst preserving \nfertility in those of reproductive age (3). It is not however, easy to determine the impact of the cyst or \na cystectomy on a woman’s future fertility. This will depend on various factors such as the nature of \nthe cyst, size and number, risk of recurrence, age of the patient, ovarian function, surgical history and \nthe presence of other aetiologies that could be a cause of subfertility in her or her partner (3). The \nscope of this review article, is to understand how these individual factors can have an impact on the \ndecision to perform a cystectomy as well as determine when and how a cystectomy can be performed \nin order to reduce the risk of damage to a woman’s reproductive potential. We will begin by examining \nthe physiology and natural history of common benign ovarian cysts and whether or not these cysts \ncan have an impact on fertility. \n \nFunctional ovarian cysts and their impact on fertility \nThe ovary has two main functions, folliculogenesis and steroidogenesis. The process of \nfolliculogenesis, i.e. the progression of primordial follicles into large pre-ovulatory follicles, makes the \novary intrinsically prone to developing functional cysts. Functional ovarian cysts have been described \nas non-pathological follicular cysts which failed to ovulate, a persistent corpus luteum cyst, or other \nunspecified ovarian cysts measuring more than 20 mm (4). They are the most frequently occurring \novarian cysts in adults and children and account for 46 -53% of all adnexal pathologies (5). They almost \nalways regress spontaneously within 1 to 3 menstrual cycles and therefore should not require any \nsurgical or hormonal interventions (6). Thus, since functional ovarian cysts are simply by-products of \n\novulation, in theory, they should not have any impact on fertility. This is with the exclusion of luteal \ncysts. Luteal cysts are thought to result from failure of the ovulatory follicle to rupture (7). The \nunruptured follicle undergoes luteinization under the action of luteinizing hormone (LH) and still \nproduces normal levels of progesterone and have the same duration of luteal phase (8). Luteal cysts \nare observed in 10% of natural menstrual cycles in fertile women, but is thought to occur more \nfrequently in the infertile population (8). Qublan and colleagues found that luteal cysts occurred in \n25% of intrauterine insemination (IUI) cycles in couples with unexplained infertility (8).                                 \n \nThe second exception, are persistent functional cysts such as those seen in women undergoing \ncontrolled ovarian stimulation (COS) as part of IVF treatment, or those with extensive periovarian \nadhesions. Women with low ovarian reserve and those on a GnRH agonist cycles are at increased risk \nof developing functional cysts (9). The incidence of these cysts in those undergoing COS is reported to \nrange between 8% and 53% (10). The impact of functional cysts on IVF success remains contentious. \nAlthough some studies suggest very poor outcome of cycles where functional cysts were detected, \nincluding high cancellation, decreased follicular recruitment and low pregnancy rates (11, 12), others \nhave failed to report a difference in any outcome (13). The first line of treatment in these patients is \nusually prolonged downregulation with either a progesterone only pill or the combined contraceptive \npill and as a last resort, ultrasound or laparoscopy guided drainage of the functional cyst.  \n \nDermoid cysts and their impact on fertility \nA dermoid cyst or a mature teratoma is a benign type of germ cell tumour that arises from totipotent \novarian cells  which develop into fully differentiated ectodermal, mesodermal, and endodermal tissue \nand are the most common pathological cysts in pre-menopausal women (14). They are bilateral in 10-\n20% of cases and grow at a rate of 1.7-1.8mm per year (3).  The recurrence rate following cystectomy \n\nis 3-4% (14). There are very few studies that have looked at the impact of dermoid cysts on ovarian \nfunction and fertility and have so far not shown any evidence of a negative effect. Kim and colleagues \ncompared anti-mullerian hormone (AMH) levels in women with unilateral and bilateral dermoid cysts \nto controls and found no significant difference (15). The mean size of the dermoid cysts in their study \nwas 6.3 +/- 0.3cm (15). Schubert and colleagues, performed histological assessments on the ovarian \ncortex surrounding dermoid cysts, serous cysts and endometriomas taken at cystectomy (16). The \nfollicular density was found to be higher in dermoid cysts compared to endometriotic and serous cysts. \nFurthermore, there was a clear limit between the dermoid cyst and the ovarian cortex and thus the \novarian cortex only seemed to be stretched but not damaged by the dermoid cyst (16). Maneschi and \ncolleagues also studied the ovarian cortical tissue surrounding benign cysts removed at cystectomy \n(17). The cortical tissue surrounding dermoid cysts showed normal morphological patterns and regular \nvascular network similar to those of the normal ovarian cortex in 92% and 84% of the samples \nrespectively (17). One small study also looked at IVF outcomes in 6 patients with dermoid cysts with \na mean size of 2.4 cm and showed no difference in the number of eggs collected (18). Overall, it \nappears that the presence of a dermoid cyst has very little or no impact on fertility. However, dermoid \ncysts do occur in both ovaries in some women and have a relatively high recurrence rate (1). These \nfactors along with their ability to grow to relatively large sizes can lead to repeated surgery, bilateral \nprocedures and relatively large cystectomies; all of which can have an adverse impact on fertility.  \nThus, the decision on whether or not to operate and when to operate can be a complex one.  \nOperating early while the cyst is still small may prevent the need for a large cystectomy and thus lower \nthe impact on the ovarian reserve.  \n \nEndometriomas and their impact on fertility \n  \n\nEndometriomas or ovarian endometriotic cysts are reported in 17 to 44% of women with \nendometriosis and is a marker of more severe and deeper disease (19). Furthermore, 28% of \nendometriomas are bilateral (20). There are several theories on the pathogenesis of endometriomas \nincluding invagination and subsequent metaplasia or collection of menstrual debris from \nendometriotic implants and colonization of functional ovarian cysts by endometriotic cells (19). The \nrisk of recurrence of endometriomas in the same ovary or contralateral ovary following surgery is high, \nwith cumulative rates of 12 to 30% after 2 to 5 years of follow-up (21). Exacoustos and colleagues \nreported that 81% had recurrence in the treated ovary, 11% on the contralateral untreated ovary and \n8% in both the treated and untreated ovaries (22). Overall, the majority of recurrence occurs in the \ntreated ovary, suggesting that the recurring cysts seem to grow from the residual loci (22). The mean \nmonthly rate of growth of endometriomas following post-operative recurrence was about 0.48 cm in \nthose not using any hormonal therapies (21). \n \nThe impact of endometriosis and endometriomas on fertility has been extensively studied and overall \nshows a detrimental effect. Several causes have been implicated including chronic inflammation which \ncan affect the quality of the oocytes and impair ovarian function resulting in defective folliculogenesis \nand fertilisation; poor oocyte and embryo quality secondary to an altered follicular environment, \nleading to impaired fertilisation and embryos with reduced implantation capacity; poor ovarian \nreserve with a significant reduction in the primordial follicle cohort secondary to fibrosis from \nincreased tissue oxidative stress (23) and finally, anatomical distortion and tubal damage or occlusion \nsecondary to pelvic adhesions.  \n \nThe evidence for poorer oocyte and embryo quality in patients with endometriosis and \nendometriomas remains patchy and inconclusive as majority of studies have only evaluated this \nindirectly. An example of indirect assessments of embryo quality are studies looking at miscarriage \n\nrates. Two such studies found higher rates of miscarriages in patients with \nendometriosis/endometriomas compared to healthy controls following spontaneous conception (24, \n25). Sanchez and colleagues performed a systematic review of the literature to evaluate the effect of \nendometriosis on oocyte quality from a clinical and biological perspective (26). They found that \noocytes retrieved from women affected by endometriosis are more likely to fail in vitro maturation \nand showed altered morphology and a lower cytoplasmic mitochondrial content compared to women \nwith other causes of infertility (26). A meta-analysis of 36 published studies involving women with all \nstages of endometriosis, found that clinical pregnancy rate was significantly lower for endometriosis \npatients (odds ratio, 0.78; 95% confidence interval, 0.65–0.94) when compared to women without \nendometriosis (27). These patients also demonstrated a significant decrease in the number of oocytes \nretrieved similar miscarriage rates. Another meta-analysis showed that live birth rates were not \nstatistically different in women with and without endometriosis, although those with endometriosis \nhad lower clinical pregnancy rates (28). Similarly, a further meta-analysis looking specifically at the \nimpact of endometriomas on IVF outcomes included 30 retrospective and 3 randomized controlled \nstudies and found similar live birth rates and clinical pregnancy rates but a lower mean number of \neggs retrieved and higher cancellation rates in women with endometriomas compared with no \nendometriomas (29). \n \nWith regards to impact on ovarian reserve, two prospective studies demonstrated lower AMH levels \nand antral follicle counts (AFC) in women with endometriomas compared to age matched controls \n(30, 31). In a systematic review and meta-analysis looking at the impact of surgery for endometriomas, \npooled analysis of preoperative AFC showed that the mean AFC for the ovary with the endometrioma \nwas lower than the contralateral one (mean difference −2.79, 95% confidence interval [CI] −7.10 to \n1.51), but statistical significance was not reached (p = 0.20) (32). On histological studies, Schubert et \nal., showed that endometriotic cysts had lower follicular density compared to dermoid and serous \n\ncysts (16).  Furthermore, endometriotic cysts showed invasion of the surrounding cortex resulting in \nfibrosis and the surrounding cortical tissue had abnormal morphological patterns and irregular \nvascular network (16, 17). Endometriomas were also thought to negatively affect ovulation with one \nstudy showing lower ovulation rates in ovaries containing endometriomas over 10mm in size \ncompared to the healthy contralateral ovary (33). However, more recently Maggiore and colleagues \nconducted a larger prospective study involving 244 women all of whom had a unilateral \nendometrioma more than 20mm in size and performed US monitoring for ovulation over 6 cycles (34). \nThey found no difference in the ovulation rates between the affected ovary and healthy ovary (50.3% \nversus 49.7%, p=0.919) (33).  \n \nOccasionally, persistent hemorrhagic cysts can be mistaken for endometriomas on ultrasound scan \nand at laparoscopy. A hemorrhagic cyst is the result of bleeding into a follicular or corpus luteum cyst.  \nMajority will spontaneously resolve like other functional cysts but occasionally they can become \ntrapped by pelvic adhesions which can cause them to persist. These can be difficult to differentiate  \nfrom endometriomas on ultrasound scan and at laparoscopy and the only way to confirm the diagnosis \nis by histology. Like other functional cysts, hemorrhagic cysts are unlikely to have any impact on \nfertility and thus a cystectomy for a hemorrhagic cyst is more likely to have an adverse effect. \n \nOther benign ovarian cysts and their impact on fertility  \nOvarian cystadenomas are common benign epithelial neoplasms of which serous and \nmucinous are two of the most common types seen (35, 36). Serous cystadenomas are more \nprevalent in menopausal women whilst the mucinous type mainly occurs during the 3rd to \nsixth decade (37). Mucinous cystadenomas are usually unilateral but they can grow large in \n\nsize, on average between 15 - 30cm (38, 39). To the best of our knowledge there is no \nliterature on the impact of a mucinous cystadenoma on fertility. However, owing to the \nrelatively large sizes of these cysts, there is a greater chance of oophorectomy. In addition, \nsurgical spill of mucinous material can lead to pelvic adhesions and subsequent infertility.   \n \nBenign ovarian cysts in children and adolescents \nMalignant ovarian cysts are uncommon in children and adolescents but despite this, oophorectomy is \nfrequently performed in in this age group when presenting with ovarian cysts. One study found that \n75% of oophorectomies in children and adolescents had being carried out for benign ovarian cysts \n(40). Functional ovarian cysts account for about 45% of all paediatric adnexal abnormalities (5) and \nusually resolve spontaneously. Teratomas constitute for about half of all ovarian neoplasms in children \n(41) and 1% of these are malignant immature teratomas (42). Since laparoscopic cystectomy has \nbecome the accepted practice for the management of mature cystic teratomas in adults, the same \napproach should apply to children and adolescents (42). With greater use of pre-operative \ninvestigations including pelvic imaging and tumour markers, along with a multidisciplinary team \napproach and more conservative surgery we should be able to better protect the future fertility of \nthese young girls.  \n \nOvarian torsion and impact on fertility \nOvarian torsion is a rare gynaecological emergency with approximately 3% of all emergency \ngynaecological surgery being performed for ovarian torsion (43, 44).  One study found the \ncumulative incidence of ovarian torsion in women with ovarian tumours, over a 24-month \nperiod was 0.3% (45). Torsion usually involves the ovary and Fallopian tube and is more \n\ncommonly seen with benign cysts over 5cm in size (44). It can also occur in normal ovaries, \nparticularly in pre-menarchal girls who have elongated infundibulopelvic ligaments (46).  \n \nConservative management, which involves laparoscopic unwinding of the twisted ovary \nregardless of the macroscopic appearance  has become the mainstay of treatment for ovarian \ntorsion (47). When an ovary undergoes torsion and detorsion, it results in haemorrhage, \ncongestion and apoptosis secondary to ischemia which can affect the ovarian reserve (48). To \nour knowledge, only one study has assessed ovarian reserve post detorsion and found no \ndifference in the AFC between the affected and contralateral ovary at 3 months post op (48). \nSimilarly, they found no difference in the AMH taken pre-operatively on the day of detorsion \nand at 1 month and 3 months post-op (48). Thus, laparoscopic detorsion appears to preserve \novarian reserve and this should remain the optimal treatment for ovarian torsion.  \n    \nOvarian cystectomy and its impact on ovarian reserve  \nThere are several methods of performing ovarian cystectomy but in principle, it involves incising the \novarian cortex to identify the cyst capsule, removing the cyst wall with or without draining the cyst \nand finally applying haemostatic measures using monopolar or bipolar coagulation, suturing or \nintraovarian sealant agents  (19).  The size and nature of the cyst being removed, bilaterality and/or \nrepeated surgery, method of cystectomy, method of haemostasis and of course the skill and \nexperience of the surgeon are all important factors that will determine how much of an impact, if any, \nthe cystectomy will have on future ovarian reserve.    \n \n\nThe stripping and removing of the cyst wall and the thermal damage provoked by coagulation can lead \nto loss of healthy ovarian tissue and the subsequent reduction in the follicle density. Muzzi et al (2002) \nperformed histological analysis on the excised specimens following laparoscopic excision of ovarian \ncysts using the stripping technique (49). The primary outcome in this study was to evaluate the \npresence and nature of ovarian tissue adjacent to the cyst wall. 54% of ovarian tissue was \ninadvertently excised along with the cyst wall in those with endometriotic cysts compared to 6% in \nthose with non-endometriotic cysts (35). Furthermore, the excised ovarian tissue did not show \nmorphological characteristics seen in normal ovarian tissue (35).   \n \nSeveral other studies have also demonstrated a reduction in the ovarian reserve following cystectomy \nfor endometriomas, including a meta-analysis of 7 published studies showing a 30% decrease in the \npost-op AMH levels and a systematic review also demonstrating a decline in the ovarian reserve \nfollowing surgery (3, 50, 51). Furthermore, two prospective longitudinal studies, showed partial \nrecovery of AMH levels 3 months post operatively to about 65% of the preoperative level in both \nendometriotic and non-endometriotic cysts (52, 53). Similar findings of reduced ovarian reserve were \nseen in studies assessing ovarian reserve following cystectomy for non-endometriotic cysts, primarily \ndermoid cysts (52, 54, 55). \n \nIn contrast, Muzii et al (2014) analysed data from 13 publications which reported AFC pre- and post-\nendometrioma surgery and showed that ovarian reserve as assessed by AFC did not change \nsignificantly.  The differences between the changes of these two surrogate markers (AMH and AFC) \ncan probably be explained by the fact that AFC assessment is likely to be less reliable in the presence \nof endometriomas and that the preoperative AFC underestimates the value. This may then obscure \nthe postoperative reduction in AFC (56).  \n. \n\n \nThe size of the cyst being removed is another important factor when determining the impact on \novarian reserve and future fertility. Using histological measurements of endometrioma cystectomy \nspecimens, Roman et al. found an average loss of 200 µm of ovarian tissue per centimeter increase in \nendometrioma diameter (57).  Several other studies also demonstrated a more significant decline in \novarian reserve following removal of endometriomas over 5 -7 cm in size (31, 58, 59). Additionally, \nthere is a higher risk of oophorectomy when performing cystectomies for larger cysts which can \nfurther reduce a woman’s reproductive potential. Clinicians frequently advise patients to delay \nsurgery until a cyst reaches a particular size, when there is a significant risk of ovarian torsion. \nHowever, knowing that larger cystectomies are more likely to have a greater negative impact on a \nwoman’s future fertility, it may better to proceed with surgery when the cyst is still small; especially \nin those with mucinous cystadenomas which have a propensity to grow into very large cysts (60).  \n \nBilateral cystectomy can lead to a greater decline in the ovarian reserve compared to those having \nunilateral surgery (3, 61). In particular, women having surgery for bilateral endometriomas have been \nshown to have an increased risk of developing premature ovarian failure (20, 62).  \n \nOvarian cystectomy and spontaneous conception \nHigher rates of spontaneous conception have been shown in infertile women who had surgical \ntreatment for endometriomas (63). Maggiore and colleagues looked at spontaneous pregnancy rates \nof women who tried to conceive spontaneously for a year and had known rectovaginal endometriosis \nwith or without endometriomas and treated with expectant or surgical management (33).  The crude \nand cumulative spontaneous pregnancy rate was higher in those with endometriomas and treated \nsurgically than in those managed expectantly (30.4% and 34.5% versus 11.7% and 18.0% respectively) \n\n(33). It has to be emphasized that this data applies to women who have a history of infertility and it \nwould be difficult to recommend routine surgical treatment of endometriomas to improve chances of \nspontaneous conception in those without proven infertility. Even in the infertile woman with an \nendometrioma, the potential benefit of improving her chances of spontaneous conception through \nsurgical management must be balanced with the risk of reducing her ovarian reserve and worsening \nthe pelvic anatomy. The ESHRE Guideline Group for the management of women with endometriosis \nrecommends that clinicians counsel women about the risk of a reduction in the ovarian reserve along \nwith the possible loss of the entire ovary, in particular for those who have had previous ovarian surgery \n(55). \n \nOvarian cystectomy and IVF outcomes \n \nCystectomy prior to IVF treatment is not routinely recommended as it has not been shown to improve \nIVF outcomes. A Cochrane review assessed the effectiveness of surgery versus no treatment for \nimproving reproductive outcomes among women with endometrioma prior to undergoing assisted \nreproductive technology (ART) (64). They included two trials comparing surgery (aspiration and \ncystectomy) with expectant management and found no evidence of benefit for clinical pregnancy \nrates (65, 66). One study in fact, showed a decreased ovarian response to gonadotrophins following \ncystectomy (65). \n \nHowever, there are still some clinical circumstances when surgery should be considered. Garcia-\nVelasco and Somigliana have created the following table to help guide clinicians on the clinical \nvariables than need to be considered when deciding whether to perform surgery or not in women \nwith endometriomas selected for IVF (67). \n\n \nTable I  \n \nCharacteristics  Favours surgery  \nFavours expectant \nmanagement  \nPrevious interventions for \nendometriosis  None  ≥1  \nOvarian reservea  Intact  Damaged  \nPain symptoms  Present  Absent  \nBilaterality  \nMonolateral \ndisease  Bilateral disease  \nSonographic feature of malignancyb  Present  Absent  \nGrowth  Rapid growth  Stable  \n \naOvarian reserve is estimated based on serum markers or previous hyperstimulation cycles;  bsonographic \nfeature of malignancy refers to solid components, locularity, echogeniety, regularity of shape, wall, septa, \nlocation and presence of peritonal fluid. \n \nReprinted from “Management of endometriomas in women requiring IVF: to touch or not to touch; by Garcia-\nVelasco, J. A. and Somigliana, E, 2009, Hum Reprod, 24, 496-501.  \n \n  \nImpact of surgical technique on fertility outcomes \nApart from cyst excision, there are several other surgical techniques available for treating \novarian cysts including drainage and bipolar coagulation or ablation using plasma or laser \nenergy.  A systematic review of two RCTs revealed cystectomy to be superior to drainage and \nbipolar coagulation in terms of spontaneous pregnancy rates, lower risk of recurrence and \n\npain symptoms amongst sub-fertile patients with endometriomas greater than 3cm (68). \nHowever, there have also been several comparative studies that have shown better \npreservation of ovarian reserve when using laser ablation or plasma energy compared to \ncystectomy (69-71). On the other hand, higher recurrence rates were seen at 1 year post laser \nablation compared to cystectomy (72).  \n \nThere are also several methods of achieving haemostasis after a cystectomy which may have \nan impact on the ovarian reserve; these include bipolar diathermy, suturing or haemostatic \nsealants. A systematic review and meta-analysis of 12 published controlled trials showed that \nlaparoscopic suturing was superior to bipolar coagulation when comparing AMH and AFC \neven at 12 months post surgery (73). In the comparison between bipolar and hemostatic \nsealants, the results favored the use of hemostatic agents (73). \n \n \nRecommendations for ovarian cystectomy  \n1) Perform ovarian reserve assessments \nOvarian reserve assessments should be carried out prior to any cystectomy in the following \nsituations:  \n Women who have not completed their family \n  Those requiring repeat surgery on the same or contralateral ovary \n\n Women diagnosed with severe endometriosis and bilateral endometriomas \n Those with co-existent aetiologies for subfertility including low sperm parameters in \nthe male partner  \n Women of advanced reproductive age  \n Women with co-existent risk factors for premature ovarian insufficiency.  \n \n These patients are more likely to need ART to help them conceive in the future and/or are at increased \nrisk of premature ovarian failure. Ovarian cystectomy can reduce a woman’s ovarian reserve and a \nlow ovarian reserve can hinder the chance of success with IVF treatment (74).  \n \nOvarian reserve assessments will comprise of follicular phase follicle stimulating hormone (FSH) taken \nat the same time as an oestradiol level, a pelvic ultrasound scan for AFC and serum AMH. The accuracy \nof these tests in the presence of ovarian cysts have not been studied well. AFC and serum AMH have \nbeen shown to be lower in the presence of endometriomas but they did not appear to be affected by \nthe presence of other types of cysts (30, 31, 75). The reduced AFC associated with endometrioma \ncould be due to the inability to visualize the antral follicles on ultrasound scan in the presence of an \nendometrioma (76). This theory is further supported by Lima at al. who analyzed the number of \noocytes retrieved during IVF/ICSI cycle in women with a unilateral endometrioma (77).  Although the \nAFC was reduced in the ovaries with an endometrioma, the median number of oocytes retrieved was \nsimilar (P = 0.60) between ovaries with an endometrioma (2.0 (IQR, 0.5–5.0)) and the contralateral \novaries (2.0 (IQR, 0.0–4.0) (73).   \n \n \n\n \n2) Discuss fertility preservation options \nIf the ovarian reserve is already compromised or there is a significant risk of permanent infertility from \nperforming an ovarian cystectomy, fertility preservation in the form of oocyte or embryo \ncryopreservation should be discussed.  For post-pubertal females, egg or embryo storage following \novarian stimulation is an established technique that allows for subsequent IVF and embryo transfer \n(78).  If the ovarian reserve is already severely compromised, ovarian stimulation may be unsuccessful. \nThe disadvantages of fertility preservation prior to cystectomy include delay in surgery,  ovarian \nhyperstimulation syndrome which is uncommon when ovarian reserve is already compromised and \nsmall risk of visceral injury during egg collection and pelvic infection from accidental puncture of the \ncyst at egg collection (79).   \n \nNHS funding is not routinely available for oocyte or embryo cryopreservation other than for oncology \npatients. However, if there is a significant risk of permanent infertility, for example if the patient has \nhad previous oophorectomy for ovarian torsion of a dermoid cyst and now has a recurrence of the \ndermoid cyst on the contralateral ovary, individual funding requests can be made to the relevant \nclinical commissioning group to consider NHS funded oocyte freezing prior to performing a \ncystectomy. The same would apply to patients with severe endometriosis requiring repeat surgery.  \n \nOvarian tissue cryopreservation is another method of fertility preservation but one that is still \nconsidered experimental. It involves either taking an ovarian cortical biopsy or a complete unilateral \noophorectomy. The ovarian tissue is subsequently re-implanted back in the pelvis and gradual \nresumption of ovarian follicle growth and endocrine activity have been seen; worldwide, only a small \nnumber of children have been born following reimplantation of frozen/thawed ovarian tissue (80). \n\nThis method of fertility preservation however may not be suitable for patients affected by ovarian \ncysts as it would cause a further reduction in the already compromised ovarian reserve.  \n \n3) Perform pelvic ultrasound scan and a bimanual examination \nAssess type, size, number and location (unilateral or bilateral) of the ovarian cysts before surgery \nusing pelvic ultrasound and bimanual examination. Greater impact of bilateral cystectomies \nshould be taken into account. \n \n4) Obtain appropriate consent \n The patient should be fully informed of all possible risks associated with the surgical procedure, \nincluding a potentially reduced ovarian reserve, and the small risk of oophorectomy \n \n5) Refer the woman to a centre of expertise \nIf the surgery cannot be performed or completed safely, the patient should be referred to a centre \nof expertise. Good surgical technique and expertise is of utmost importance in order to reduce \nthe risk of injury to a woman’s reproductive potential as well as avoid serious complications.  \n \n \nAnatomical consideration during cystectomy  \nThe ovary receives its blood supply from two sources, the ovarian artery and an anastomosis between \nthe ovarian artery and the ascending branch of the uterine artery/tubal artery. The ovarian artery \napproaches the ovary through the infundibulopelvic ligament whilst the uterine/tubal artery are \nfound within the ovarian ligament.  These intra-ovarian vessels are found in the anterolateral aspect \n\nof the ovary, at the insertion of the mesovarium. The surgeon needs to avoid excessive bleeding which \nmight lead to destruction of healthy ovarian tissue through cauterisation and disruption of ovarian \nblood supply (19).  \n \nSurgical recommendations  \nNon-endometriotic cysts \n1. Make an incision on the anti-mesenteric surface of ovarian cortex (Figure 1A) \n2. Identify the plane between the cyst wall and the ovarian cortex, develop this plane \nfurther (Figure 1B) \n3. Enucleate the cyst or cyst wall (if the contents spilled or aspirated) by a combination \nof blunt and sharp dissection, traction and counter traction. \n4. Achieve haemostasis by targeted coagulation of blood vessels (Figure 1C) or suturing \n(Figure 1D). Avoid indiscriminate use of diathermy and consider using haemostatic \nsealants instead of excessive diathermy.  \nA               B    \n\n\n C               D     \n   \nFigure 1 \nOvarian cystectomy. A – reveal cleavage plane. B – dissect the cyst wall from the ovarian parenchyma. \nC & D – achieve haemostasis by targeted coagulation and/or suturing and then reconstruct the ovary.  \n \nEndometriotic cysts  \nThe ESGE/ESHRE/WES Working Party on the surgical techniques for ovarian endometriomas \nrecommends the following approaches (18): \n1) Mobilise the ovary and drain the cyst (Figure 2A and 2B).  \n2) Make incision to reveal the cleavage plane (2C).  This may be either on the edge of the cyst \nopening or a central incision, which divides the cyst into two halves. With both approaches, \nthe incision should be away from the blood vessels in the hilum/mesovarium. Use of cold cut \nat the edge of the cyst opening may assist in identifying the cleavage plane.  \n3) To aid dissection and identification of the cyst wall, saline or diluted synthetic vasopressin \nsolution (0.1–1 unit/ml) may be injected under the cyst capsule (Figure 2D). The diluted \nsynthetic vasopressin injection has the additional advantage of reducing bleeding during cyst \nremoval. \n\n\n4) Once the cleavage plane is identified, use gentle traction and counter-traction with \nappropriate instruments to dissect the cyst capsule from the ovarian parenchyma (Figure 2E \nand 2F). Avoid use of excessive force to separate a highly adherent cyst from the ovary. This \nis likely to cause tearing of the ovarian tissue, excessive bleeding, and the need for coagulation \nor diathermy, which will further damage the normal ovarian tissue.  \n5) Careful identification of the cleavage plane and precise spot bipolar coagulation is the key to \nachieve haemostasis (Figure 2G). This will prevent unnecessary damage to healthy tissue and \navoids blind or excessive diathermy.  \n6) Ensure final haemostasis after complete removal of the cyst capsule. Bipolar coagulation, \nsuturing or intraovarian haemostatic sealant agents may also be used for this purpose. It is \nimportant to avoid damaging the major blood supply at the hilum coming in from the ovarian \nand infundibulopelvic ligaments at this stage.  \n7) After removal of large cysts, reconstruct the ovary and achieve haemostasis with \nmonofilament sutures. For small cysts, suturing is often not required as the ovarian opening \nusually approximates spontaneously. If a suture is used, it should ideally be placed inside the \novary, as the exposed suture may be prone to adhesion formation.  \n8) Small cyst walls may be retrieved directly through a port. Large cyst walls can be removed in \na specimen retrieval bag.  \n \n \n\n \nA        B   \n \n\n\nC         D    \n \nFigure 2 \nOvarian cystectomy of an endometrioma. A - Right ovarian endometrioma and adherent right ovary  \nB- drainage of  endometrioma after mobilizing the ovary. C - exposure of the plane between the cyst \nwall and ovarian cortex D – vasopressin injection under the cyst capsule. E - dissect cyst capsule from \nthe ovarian parenchyma. F- Cyst capsule after complete removal G – precise spot bipolar diathermy \nto achieve haemostasis. \n \n \nTwo-step approach for large endometriomas (19) \nAfter opening and draining the endometrioma as described previously, the cyst wall is inspected and \na biopsy taken. Gonadotropin-releasing hormone agonist (GnRHa) therapy is then given for 3 months \nto reduce the thickness of the cyst wall through atrophy and reduction in stromal vascularisation (81). \nThe surgery is completed with a second laparoscopy in the form of either cystectomy, CO2 \nvaporisation, bipolar diathermy or plasma ablation of the cyst wall lining of the cyst (19). Although \nwomen have to undergo two invasive procedures, the potential benefit is that this may facilitate the \nmanagement of larger ovarian endometriomas, reduce recurrence rates and limit decrease in ovarian \nreserve (19). \n \nConclusion \n\n\nFunctional ovarian cysts and dermoid cysts do not appear to have a significant impact on fertility. \nEndometriomas appear to have a negative effect on oocyte quality and ovarian reserve. Surgical \nmanagement has been shown to improve the chances of spontaneous conception in infertile women \nwhilst reducing the ovarian reserve as determined by AMH levels. Ovarian response in those \nundergoing IVF treatments appears to be compromised after endometrioma surgery. Performing \novarian reserve assessments would be recommended in all women having repeated surgery, in those \nwith severe endometriosis or if there is a high chance of needing ART to conceive. Regardless of \nwhether or not a cystectomy is performed, it is imperative that the risk to fertility and ovarian function \nis discussed with all patients and that information on fertility preservation is given to those in whom \nthe ovarian reserve is already compromised. \n \nThe management of benign ovarian cysts in women of reproductive age, children and adolescents is \ncomplex. The patient’s symptom(s) is likely to have the biggest impact on the decision-making process. \nThose experiencing significant pain related to the cyst and unsuitable for hormonal therapy will often \nrequire surgery.  Prior to an ovarian cystectomy, the surgeon should take careful consideration of the \nage of the patient, the nature of the cyst, rate of growth, risk of recurrence, surgical history, future \nfertility plans and assess for other causes of subfertility which would increase the likelihood of needing \nART in the future, including the partners sperm parameters (3). \n \nSocietal changes in the Western world have resulted in trends towards pregnancy at older age with \nthe average age of mothers in the UK now at 30.4 (82). With increasing age, there is a decline in the \nquality and quantity of oocytes which is accelerated from 37-38 years of age (83). At present we do \nnot know the precise incidence of sub-fertility secondary to ovarian cystectomy. However, it is likely \nthat the impact of cystectomy on future fertility will be worse in those women choosing to delay \nchildbearing, in whom the ovarian reserve is already compromised. Hence, in the future, it is likely \n\nthat we may see a higher incidence of subfertility secondary to ovarian cystectomy. In the presence \nof a benign ovarian cyst, our recommendation of a fertility-focused approach, along with fertility-\nconserving surgery, will be the key to protecting a woman’s reproductive potential.    \nEthical approval \nNot required.  \n \nDisclosure of interests \nThere are no conflicts of interest. \n  \nContribution to authorship \n NB and ES conceived the topic. NB planned the scope of the article, researched and wrote the initial \ndraft. EY, DM and ES reviewed and revised the manuscript. All authors approved the final version.  \n \nAcknowledgements \nThe authors would like to thank the Editor of TOG for accepting this topic. No funding has been \nreceived for this work. \n \nReferences   \n1. Westhoff C, Clark CJ. Benign ovarian cysts in England and Wales and in the United States. Br J \nObstet Gynaecol. 1992;99(4):329-32. \n2. Mimoun C, Fritel X, Fauconnier A, Deffieux X, Dumont A, Huchon C. [Epidemiology of \npresumed benign ovarian tumors]. J Gynecol Obstet Biol Reprod (Paris). 2013;42(8):722-9. \n\n3. Legendre G, Catala L, Morinière C, Lacoeuille C, Boussion F, Sentilhes L, et al. Relationship \nbetween ovarian cysts and infertility: what surgery and when? Fertility and Sterility. 2014;101(3):608-\n14. \n4. Baerwald AR, Pierson RA. Ovarian follicular development during the use of oral contraception: \na review. Journal of obstetrics and gynaecology Canada : JOGC = Journal d'obstetrique et gynecologie \ndu Canada : JOGC. 2004;26(1):19-24. \n5. Spinelli C, Di Giacomo M, Cei M, Mucci N. Functional ovarian lesions in children and \nadolescents: when to remove them. Gynecological endocrinology : the official journal of the \nInternational Society of Gynecological Endocrinology. 2009;25(5):294-8. \n6. Grimes DA, Jones LB, Lopez LM, Schulz KF. Oral contraceptives for functional ovarian cysts. \nThe Cochrane database of systematic reviews. 2014(4):CD006134. \n7. Vermesh M, Kletzky OA, Davajan V, Israel R. Monitoring techniques to predict and detect \novulation. Fertil Steril. 1987;47(2):259-64. \n8. Qublan H, Amarin Z, Nawasreh M, Diab F, Malkawi S, Al-Ahmad N, et al. Luteinized unruptured \nfollicle syndrome: incidence and recurrence rate in infertile women with unexplained infertility \nundergoing intrauterine insemination. Human reproduction (Oxford, England). 2006;21(8):2110-3. \n9. Keltz MD, Jones EE, Duleba AJ, Polcz T, Kennedy K, Olive DL. Baseline cyst formation after \nluteal phase gonadotropin-releasing hormone agonist administration is linked to poor in vitro \nfertilization outcome. Fertil Steril. 1995;64(3):568-72. \n10. Qublan HS, Amarin Z, Tahat YA, Smadi AZ, Kilani M. Ovarian cyst formation following GnRH \nagonist administration in IVF cycles: incidence and impact. Human Reproduction. 2006;21(3):640-4. \n11. Keltz MD, Jones EE, Duleba AJ, Polcz T, Kennedy K, Olive DL. Baseline cyst formation after \nluteal phase gonadotropin-releasing hormone agonist administration is linked to poor in vitro \nfertilization outcome *. Fertility and Sterility. 1995;64(3):568-72. \n12. Biljan MM, Lapensée L, Mahutte NG, Bissonnette F, Hemmings R, Tan SL. Effects of functional \novarian cysts detected on the 7th day of gonadotropin-releasing hormone analog administration on \nthe outcome of IVF treatment. Fertility and Sterility. 2000;74(5):941-5. \n13. Sampaio M, Serra V, Miro F, Calatayud C, Castellvi RM, Pellicer A. Development of ovarian \ncysts during gonadotrophin releasing hormone agonists (GnRHa) administration. Human \nReproduction. 1991;6(2):194-7. \n14. O'Neill KE, Cooper AR. The approach to ovarian dermoids in adolescents and young women. \nJournal of pediatric and adolescent gynecology. 2011;24(3):176-80. \n15. Kim JY, Jee BC, Suh CS, Kim SH. Preoperative serum anti-mullerian hormone level in women \nwith ovarian endometrioma and mature cystic teratoma. Yonsei medical journal. 2013;54(4):921-6. \n16. Schubert B, Canis M, Darcha C, Artonne C, Pouly J-L, Déchelotte P, et al. Human ovarian tissue \nfrom cortex surrounding benign cysts: a model to study ovarian tissue cryopreservation. Human \nReproduction. 2005;20(7):1786-92. \n17. Maneschi F, Marasa L, Incandela S, Mazzarese M, Zupi E. Ovarian cortex surrounding benign \nneoplasms: a histologic study. American journal of obstetrics and gynecology. 1993;169(2 Pt 1):388-\n93. \n18. Caspi B, Weissman A, Zalel Y, Barash A, Tulandi T, Shoham Z. Ovarian stimulation and in vitro \nfertilization in women with mature cystic teratomas. Obstetrics and gynecology. 1998;92(6):979-81. \n19. Saridogan E, Becker CM, Feki A, Grimbizis GF, Hummelshoj L, Keckstein J, et al. \nRecommendations for the surgical treatment of endometriosis-part 1: ovarian endometrioma. \nGynecological surgery. 2017;14(1):27. \n20. Coccia ME, Rizzello F, Mariani G, Bulletti C, Palagiano A, Scarselli G. Ovarian surgery for \nbilateral endometriomas influences age at menopause. Human reproduction (Oxford, England). \n2011;26(11):3000-7. \n21. Seracchioli R, Mabrouk M, Frasca C, Manuzzi L, Montanari G, Keramyda A, et al. Long-term \ncyclic and continuous oral contraceptive therapy and endometrioma recurrence: a randomized \ncontrolled trial. Fertil Steril. 2010;93(1):52-6. \n\n22. Exacoustos C, Zupi E, Amadio A, Amoroso C, Szabolcs B, Romanini ME, et al. Recurrence of \nendometriomas after laparoscopic removal: sonographic and clinical follow-up and indication for \nsecond surgery. Journal of minimally invasive gynecology. 2006;13(4):281-8. \n23. The Effect of Surgery for Endometriomas on Fertility: Scientific Impact Paper No. 55. BJOG : \nan international journal of obstetrics and gynaecology. 2018;125(6):e19-e28. \n24. Hjordt Hansen MV, Dalsgaard T, Hartwell D, Skovlund CW, Lidegaard O. Reproductive \nprognosis in endometriosis. A national cohort study. Acta obstetricia et gynecologica Scandinavica. \n2014;93(5):483-9. \n25. Vercellini P, Parazzini F, Pietropaolo G, Cipriani S, Frattaruolo MP, Fedele L. Pregnancy \noutcome in women with peritoneal, ovarian and rectovaginal endometriosis: a retrospective cohort \nstudy. BJOG : an international journal of obstetrics and gynaecology. 2012;119(12):1538-43. \n26. Sanchez AM, Vanni VS, Bartiromo L, Papaleo E, Zilberberg E, Candiani M, et al. Is the oocyte \nquality affected by endometriosis? A review of the literature. J Ovarian Res. 2017;10(1):43. \n27. Hamdan M, Dunselman G, Li TC, Cheong Y. The impact of endometrioma on IVF/ICSI \noutcomes: a systematic review and meta-analysis. Hum Reprod Update. 2015;21(6):809-25. \n28. Harb HM, Gallos ID, Chu J, Harb M, Coomarasamy A. The effect of endometriosis on in vitro \nfertilisation outcome: a systematic review and meta-analysis. BJOG : an international journal of \nobstetrics and gynaecology. 2013;120(11):1308-20. \n29. Hamdan M, Omar SZ, Dunselman G, Cheong Y. Influence of endometriosis on assisted \nreproductive technology outcomes: a systematic review and meta-analysis. Obstetrics and \ngynecology. 2015;125(1):79-88. \n30. Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B. Prospective assessment \nof the impact of endometriomas and their removal on ovarian reserve and determinants of the rate \nof decline in ovarian reserve. Human reproduction (Oxford, England). 2013;28(8):2140-5. \n31. Chen Y, Pei H, Chang Y, Chen M, Wang H, Xie H, et al. The impact of endometrioma and \nlaparoscopic cystectomy on ovarian reserve and the exploration of related factors assessed by serum \nanti-Mullerian hormone: a prospective cohort study. Journal of ovarian research. 2014;7:108-. \n32. Muzii L, Di Tucci C, Di Feliciantonio M, Marchetti C, Perniola G, Panici PB. The effect of surgery \nfor endometrioma on ovarian reserve evaluated by antral follicle count: a systematic review and meta-\nanalysis. Human reproduction (Oxford, England). 2014;29(10):2190-8. \n33. Benaglia L, Somigliana E, Vercellini P, Abbiati A, Ragni G, Fedele L. Endometriotic ovarian cysts \nnegatively affect the rate of spontaneous ovulation. Human reproduction (Oxford, England). \n2009;24(9):2183-6. \n34. Leone Roberti Maggiore U, Scala C, Tafi E, Racca A, Biscaldi E, Vellone VG, et al. Spontaneous \nfertility after expectant or surgical management of rectovaginal endometriosis in women with or \nwithout ovarian endometrioma: a retrospective analysis. Fertil Steril. 2017;107(4):969-76.e5. \n35. Seidman JD, Mehrotra A. Benign ovarian serous tumors: a re-evaluation and proposed \nreclassification of serous “cystadenomas” and “cystadenofibromas”. Gynecologic Oncology. \n2005;96(2):395-401. \n36. El-Agwany AS. Recurrent Bilateral Mucinous Cystadenoma: Laparoscopic Ovarian Cystectomy \nwith Review of Literature. Indian J Surg Oncol. 2018;9(2):146-9. \n37. Saba L, Acharya UR, Guerriero S, Suri JS. Ovarian Neoplasm Imaging: Springer Science & \nBusiness Media; 2014. \n38. Cowan RA, Haber EN, Faucz FR, Stratakis CA, Gomez-Lobo V. Mucinous Cystadenoma in \nChildren and Adolescents. Journal of pediatric and adolescent gynecology. 2017;30(4):495-8. \n39. Posabella A, Galetti K, Engelberger S, Giovannacci L, Gyr T, Rosso R. A huge mucinous \ncystadenoma of ovarian: a rare case report and review of the literature. Rare Tumors. 2014;6(2):5225-\n. \n40. Hernon M, McKenna J, Busby G, Sanders C, Garden A. The histology and management of \novarian cysts found in children and adolescents presenting to a children's hospital from 1991 to 2007: \n\na call for more paediatric gynaecologists. BJOG : an international journal of obstetrics and \ngynaecology. 2010;117(2):181-4. \n41. Azizkhan RG, Caty MG. Teratomas in childhood. Current opinion in pediatrics. 1996;8(3):287-\n92. \n42. Templeman CL, Hertweck SP, Scheetz JP, Perlman SE, Fallat ME. The management of mature \ncystic teratomas in children and adolescents: a retrospective analysis. Human Reproduction. \n2000;15(12):2669-72. \n43. Hibbard LT. Adnexal torsion. American Journal of Obstetrics & Gynecology. 1985;152(4):456-\n61. \n44. Houry D, Abbott JT. Ovarian torsion: a fifteen-year review. Annals of emergency medicine. \n2001;38(2):156-9. \n45. Froyman W, Landolfo C, De Cock B, Wynants L, Sladkevicius P, Testa AC, et al. Risk of \ncomplications in patients with conservatively managed ovarian tumours (IOTA5): a 2-year interim \nanalysis of a multicentre, prospective, cohort study. Lancet Oncol. 2019;20(3):448-58. \n46. Celik A, Ergun O, Aldemir H, Ozcan C, Ozok G, Erdener A, et al. Long-term results of \nconservative management of adnexal torsion in children. Journal of pediatric surgery. 2005;40(4):704-\n8. \n47. Ben-Rafael Z, Bider D, Mashiach S. Laparoscopic unwinding of twisted ischemic hemorrhagic \nadnexum after in vitro fertilization. Fertil Steril. 1990;53(3):569-71. \n48. Yasa C, Dural O, Bastu E, Zorlu M, Demir O, Ugurlucan FG. Impact of laparoscopic ovarian \ndetorsion on ovarian reserve. The journal of obstetrics and gynaecology research. 2017;43(2):298-\n302. \n49. Muzii L, Bianchi A, Crocè C, Manci N, Panici PB. Laparoscopic excision of ovarian cysts: is the \nstripping technique a tissue-sparing procedure? Fertility and Sterility. 2002;77(3):609-14. \n50. Raffi F, Metwally M, Amer S. The impact of excision of ovarian endometrioma on ovarian \nreserve: a systematic review and meta-analysis. The Journal of clinical endocrinology and metabolism. \n2012;97(9):3146-54. \n51. Somigliana E, Berlanda N, Benaglia L, Vigano P, Vercellini P, Fedele L. Surgical excision of \nendometriomas and ovarian reserve: a systematic review on serum antimullerian hormone level \nmodifications. Fertil Steril. 2012;98(6):1531-8. \n52. Chang HJ, Han SH, Lee JR, Jee BC, Lee BI, Suh CS, et al. Impact of laparoscopic cystectomy on \novarian reserve: serial changes of serum anti-Mullerian hormone levels. Fertil Steril. 2010;94(1):343-\n9. \n53. Amooee S, Gharib M, Ravanfar P. Comparison of anti-mullerian hormone level in non-\nendometriotic benign ovarian cyst before and after laparoscopic cystectomy. Iran J Reprod Med. \n2015;13(3):149-54. \n54. Somigliana E, Ragni G, Infantino M, Benedetti F, Arnoldi M, Crosignani PG. Does laparoscopic \nremoval of nonendometriotic benign ovarian cysts affect ovarian reserve? Acta obstetricia et \ngynecologica Scandinavica. 2006;85(1):74-7. \n55. Sarmadi S, Ahmadi FS, Ejtemaei Mehr S, Ghaseminejad A, Mohammad K, Nekuie S, et al. \nHistopathologic and sonographic analysis of laparoscopic removal ovarian nonendometriotic cyst: the \nevaluating effects on ovarian reserve. Acta Med Iran. 2014;52(5):341-4. \n56. Ata B, Urman B. Endometrioma excision and ovarian reserve; do assessments by antral follicle \ncount and anti-Mullerian hormone yield contradictory results? Human reproduction (Oxford, \nEngland). 2014;29(12):2852-4. \n57. Roman H, Tarta O, Pura I, Opris I, Bourdel N, Marpeau L, et al. Direct proportional relationship \nbetween endometrioma size and ovarian parenchyma inadvertently removed during cystectomy, and \nits implication on the management of enlarged endometriomas. Human reproduction (Oxford, \nEngland). 2010;25(6):1428-32. \n\n58. Henes M, Engler T, Taran FA, Brucker S, Rall K, Janz B, et al. Ovarian cyst removal influences \novarian reserve dependent on histology, size and type of operation. Women's health (London, \nEngland). 2018;14:1745506518778992. \n59. Mehdizadeh Kashi A, Chaichian S, Ariana S, Fazaeli M, Moradi Y, Rashidi M, et al. The impact \nof laparoscopic cystectomy on ovarian reserve in patients with unilateral and bilateral endometrioma. \nInternational journal of gynaecology and obstetrics: the official organ of the International Federation \nof Gynaecology and Obstetrics. 2017;136(2):200-4. \n60. Farahani L, Morgan S, Datta S. Reprint of: Benign ovarian cysts. Obstetrics, Gynaecology and \nReproductive Medicine. 2017;27(7):226-30. \n61. Hirokawa W, Iwase A, Goto M, Takikawa S, Nagatomo Y, Nakahara T, et al. The post-operative \ndecline in serum anti-Mullerian hormone correlates with the bilaterality and severity of \nendometriosis. Human reproduction (Oxford, England). 2011;26(4):904-10. \n62. Busacca M, Riparini J, Somigliana E, Oggioni G, Izzo S, Vignali M, et al. Postsurgical ovarian \nfailure after laparoscopic excision of bilateral endometriomas. American Journal of Obstetrics & \nGynecology. 2006;195(2):421-5. \n63. Vercellini P, Somigliana E, Vigano P, Abbiati A, Barbara G, Crosignani PG. Surgery for \nendometriosis-associated infertility: a pragmatic approach. Human reproduction (Oxford, England). \n2009;24(2):254-69. \n64. Benschop L, Farquhar C, van der Poel N, Heineman MJ. Interventions for women with \nendometrioma prior to assisted reproductive technology. The Cochrane database of systematic \nreviews. 2010(11):Cd008571. \n65. Demirol A, Guven S, Baykal C, Gurgan T. Effect of endometrioma cystectomy on IVF outcome: \na prospective randomized study. Reproductive biomedicine online. 2006;12(5):639-43. \n66. Alborzi S, Ravanbakhsh R, Parsanezhad ME, Alborzi M, Alborzi S, Dehbashi S. A comparison of \nfollicular response of ovaries to ovulation induction after laparoscopic ovarian cystectomy or \nfenestration and coagulation versus normal ovaries in patients with endometrioma. Fertil Steril. \n2007;88(2):507-9. \n67. Garcia-Velasco JA, Somigliana E. Management of endometriomas in women requiring IVF: to \ntouch or not to touch. Human reproduction (Oxford, England). 2009;24(3):496-501. \n68. Hart RJ, Hickey M, Maouris P, Buckett W. Excisional surgery versus ablative surgery for ovarian \nendometriomata. The Cochrane database of systematic reviews. 2008(2):Cd004992. \n69. Tsolakidis D, Pados G, Vavilis D, Athanatos D, Tsalikis T, Giannakou A, et al. The impact on \novarian reserve after laparoscopic ovarian cystectomy versus three-stage management in patients \nwith endometriomas: a prospective randomized study. Fertil Steril. 2010;94(1):71-7. \n70. Candiani M, Ottolina J, Posadzka E, Ferrari S, Castellano LM, Tandoi I, et al. Assessment of \novarian reserve after cystectomy versus 'one-step' laser vaporization in the treatment of ovarian \nendometrioma: a small randomized clinical trial. Human reproduction (Oxford, England). \n2018;33(12):2205-11. \n71. Roman H, Auber M, Mokdad C, Martin C, Diguet A, Marpeau L, et al. Ovarian endometrioma \nablation using plasma energy versus cystectomy: a step toward better preservation of the ovarian \nparenchyma in women wishing to conceive. Fertil Steril. 2011;96(6):1396-400. \n72. Carmona F, Martinez-Zamora MA, Rabanal A, Martinez-Roman S, Balasch J. Ovarian \ncystectomy versus laser vaporization in the treatment of ovarian endometriomas: a randomized \nclinical trial with a five-year follow-up. Fertil Steril. 2011;96(1):251-4. \n73. Baracat CMF, Abdalla-Ribeiro HSA, Araujo R, Bernando WM, Ribeiro PA. The Impact on \nOvarian Reserve of Different Hemostasis Methods in Laparoscopic Cystectomy: A Systematic Review \nand Meta-analysis. Rev Bras Ginecol Obstet. 2019;41(6):400-8. \n74. Leijdekkers JA, Eijkemans MJC, van Tilborg TC, Oudshoorn SC, McLernon DJ, Bhattacharya S, \net al. Predicting the cumulative chance of live birth over multiple complete cycles of in vitro \nfertilization: an external validation study. Human reproduction (Oxford, England). 2018;33(9):1684-\n95. \n\n75. Almog B, Shehata F, Sheizaf B, Tulandi T. Effect of different types of ovarian cyst on antral \nfollicle count. Fertil Steril. 2010;94(6):2338-9. \n76. Cranney R, Condous G, Reid S. An update on the diagnosis, surgical management, and fertility \noutcomes for women with endometrioma. Acta obstetricia et gynecologica Scandinavica. \n2017;96(6):633-43. \n77. Lima ML, Martins WP, Coelho Neto MA, Nastri CO, Ferriani RA, Navarro PA. Assessment of \novarian reserve by antral follicle count in ovaries with endometrioma. Ultrasound Obstet Gynecol. \n2015;46(2):239-42. \n78. Balachandren N, Davies M. Fertility, ovarian reserve and cancer. Maturitas. 2017;105:64-8. \n79. Moini A, Riazi K, Amid V, Ashrafi M, Tehraninejad E, Madani T, et al. Endometriosis may \ncontribute to oocyte retrieval-induced pelvic inflammatory disease: report of eight cases. Journal of \nassisted reproduction and genetics. 2005;22(7-8):307-9. \n80. Anderson RA, Wallace WH. Fertility preservation in girls and young women. Clinical \nendocrinology. 2011;75(4):409-19. \n81. Donnez J, Nisolle M, Gillet N, Smets M, Bassil S, Casanas-Roux F. Large ovarian \nendometriomas. Human reproduction (Oxford, England). 1996;11(3):641-6. \n82. Office of National Statistics. Births in England and Wales: 2017 2018, July 18 [Available from: \nhttps://www.ons.gov.uk/peoplepopulationandcommunity/birthsdeathsandmarriages/livebirths/bull\netins/birthsummarytablesenglandandwales/2017#the-number-of-live-births-and-the-total-fertility-\nrate-decreased-in-2017. \n83. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of \novarian follicles in mid-life: implications for forecasting menopause. Human reproduction (Oxford, \nEngland). 1992;7(10):1342-6.","source_license":"CC0","license_restricted":false}