{"paper_id":"6cb2563f-2684-439b-9e9a-4b0c5754e6d9","body_text":"22\nORIGINAL PAPER\nCorresponding author: \nDariusz Owczarek, Department of Endoscopic Gynecology and Oncological Gynecology, Institute of Polish \nMother’s Health, Rzgowska 281/289, 93-338 Lodz, e-mail: siwusek79@op.pl\nSubmitted: 3.08.2017 \nAccepted: 22.11.2017\nOvarian reserve evaluation after laparoscopic cyst \nenucleation, depending on applied haemostasis tech-\nnique and with particular consideration of endometrial \ncysts.\nEndometriosis is defined as an extrauterine occur -\nrence of adenocytes (gland cells) and of endometrial \nstroma. The percentage of diagnosed cases of endome-\ntriosis varies – acc. to various estimates – from 6 to \n10% of women in reproductive age [1]. Of the numerous \ntheories that explain how the onset of endometriosis \ndevelops, a few can be isolated and grouped into the \nfollowing three categories: theory of endometriosis de-\nvelopment in situ, theories of transmittable infections, \nand inductive theories. Among the theories of transmit-\ntable infections, the theory of retrograde menstruation, \nproposed by Sampson, should be perceived as leading. It \nis based on the observation of a backward flow of some \nOvarian reserve evaluation after laparoscopic cyst enucleation, depending  \non applied haemostasis technique and with particular consideration  \nof endometrial cysts\nDariusz Owczarek, Andrzej Malinowski, Miłosz Wilczyński\nDepartment of Endoscopic Gynecology and Oncological Gynecology, Institute of Polish Mother’s Health, Lodz, Poland\nAbstract \nAim of the study was an evaluation of the effects, exerted by obtained haemostasis on ovarian reserve, \ndepending on haemostasis technique, applied after laparoscopic enucleation of endometrial cysts.\nMaterial and methods: Sixty-six female patients, at the age of 20-35 years, were included into the study. \nThe diameters of the cystic lesions were within 40-70 mm. The patients were randomly assigned to two study \ngroups. Group 1 involved patients after laparoscopic enucleation of ovarian cysts, in whom haemostasis was \nachieved by ovary suturing, while Group 2 included patients with haemostasis achieved by bipolar coagulation \ntechnique. Cyst enucleation was performed in all the patients by the stripping method. Ovarian reserve markers: \nAFC (antral follicle count), AMH (anti-Müllerian hormone), and inhibin B were assayed before and three months \nafter the surgery. \nResults: The preoperative values of AMH, AFC, and inhibin B were similar in both studied groups. After \na three-month follow up, the post-operative levels of AMH and inhibin B were significantly lower (p < 0.05), \nwhile the numbers of antral follicles did not reveal any statistical differences (p > 0.05). While comparing en-\ndometrial and dermoid cysts in the sutured group of patients, the difference, regarding AMH, was statistically \nsignificant (2.13 vs. 4.69, p = 0.03). In the group of patients after bipolar coagulation, the corresponding differ -\nences did not attain statistical significance (2.21 vs. 6.51, p = 0.86)\nConclusions: Comparing pre- and post-operative levels of AMH and inhibin B, regardless of the applied \nhaemostasis technique, a statistically significant reduction of the ovarian reserve was observed in either group. \nComparing both haemostasis techniques, no method was demonstrated that would have decreased less the \nlevels of AMH, AFC, or inhibin B.\nKey words: cyst enucleation, ovarian reserve, bipolar coagulation, ovary suturing, haemostasis.\nmenstrual blood through the ovarian ducts to the peri-\ntoneal cavity. This flow carries live and able for implan-\ntation, desquamated cells of the endometrium [2]. This \ntheory does not, however, explain all the doubts which \nare associated with the pathogenesis of the disease. If \nretrograde menstruation occurs in 90% of women, then \nwhy does endometriosis develop only in some of them? \nThe answer to this question has, in part, been provided \nby the theory of immunological deficit [3]. According to \nthis theory, disturbed functions of macrophages, NK \ncells, and cytotoxic lymphocytes of the peritoneal fluid, \nobserved in women with endometriosis, are significant \nfor survival of displaced endometrial cells. These cells \nare responsible for phagocytosis of erythrocytes, mor -\nphotic elements of menstrual blood, or damaged tis-\nsue fragments. A number of other disturbed responses \nof the immune system, both cellular and humoural in \nDOI: https://doi.org/10.5114/pm.2018.74899\nMenopause Rev 2018; 17(1): 22-27\n\nMenopause Review/Przegląd Menopauzalny 17(1) 2018\n23\ncharacter, were found in the peritoneal fluid of women \nwith endometriosis [4]. \nThe disease is manifested mainly by pain sensa-\ntions, compromised fertility, menorrhoea disturbances, \nor by a  concomitant incidence of these disorders [5]. \nThe ovary is a frequent location of endometriosis – per-\nhaps for its surface irregularities, which favour the for -\nmation of endometrial cysts [6]. A standard procedure \nin the surgical treatment of endometrial cysts is pseu-\ndocapsule enucleation [7]. The stripping method – as \nit were – involves the use of two atraumatic gripping \ninstruments to pull away the cystic capsule and the nor-\nmal ovarian parenchyma in opposite directions.\nA  systematic review and meta-analysis indicate, \nhowever, a negative effect of ovarian cysts capsule enu-\ncleation on the ovarian reserve. The commonly accept-\nable markers of ovarian reserve include the anti-Mulle-\nrian hormone (AMH), the antral follicle count (AFC), the \nfollicle-stimulating hormone (FSH), and inhibin B. There \nis a problem with normal antral follicles, which may be \neither removed in the course of capsule enucleation \nprocedure or damaged during haemostasis, achieved by \nmeans of electrical energy or intraperitoneal suturing. \nOn one hand, the use of electrical energy requires very \nhigh precision and accuracy due to the risk of damage \nto the surrounding normal ovarian tissue, while intrao-\nvarian suturing may increase the intraovarian blood \npressure, leading to local ischaemia on the other. There-\nfore, the selection of an appropriate technique of hae-\nmostasis still remains a rather controversial issue, thus \ndemanding further research, comparing ovarian coagu-\nlation with ovarian suturing in female patients undergo-\ning the surgical procedure of ovarian cyst enucleation. \nAim of the study\nThe goal of the reported study was an evaluation of \nthe effects exerted by applied haemostasis techniques \non ovarian reserve following laparoscopic enucleation \nof endometrial cysts. \nMaterial and methods\nThe study was carried out during the years 2014-\n2016 in patients admitted to the Department of Endo-\nscopic Surgical Gynaecology and Oncological Gynaecol-\nogy. Female patients, at the age of 20-35 years, were \nincluded into the study with cystic lesions of 40-70 mm \nin diameter. All the patients provided written, informed \nconsent to participate in the clinical study on a specially \nprepared form approved by the Bioethical Committee. \nThe patients were randomly assigned to two study \ngroups. Group 1 involved patients after laparoscopic \nenucleation of ovarian cysts, in whom haemostasis was \nachieved by ovarian suturing, while group 2 included pa-\ntients with haemostasis achieved by bipolar coagulation \ntechnique. Patients with history of cyst enucleation were \ndisqualified from the study. In total, 66 patients were \nqualified and subsequently submitted to cyst enucleation \nprocedure. The mean age of the patients in either group \nwas similar at 31 ±5.18 vs. 33 ±4.78 years (p = 0.871).\nIn 33 patients, haemostasis was achieved by sutur -\ning of the ovary. The sutured group included 24 cases \nof diagnosed endometrial cysts, six cases with dermoid \ncysts, and three with simple cysts. In group 2, haemosta-\nsis was done by electric energy. The coagulated group \nincluded 16 cases of diagnosed endometrial cysts, eight \ncases with dermoid cysts, and nine with simple cysts. \nPreoperative blood samples provided material for \nroutine complete blood count (CBC), ionogram, and co-\nagulology plus AMH and inhibin B levels were assayed. \nDuring standard pre-operative sonographic diagnostic \nimaging, the number of AFCs was evaluated. Similar \nlaboratory tests and US examination were repeated \nthree months after the surgery. The US was carried out \nby the same physician.\nThe laparoscopic cyst enucleation procedure was \ndone by two surgeons. The patients were laid in the \nTrendelenburg position. Using a  Veress needle, pneu-\nmoperitoneum was produced. When the intraabdomi-\nnal pressure attained 14 mm Hg, two 5-mm trocars \nwere inserted via lateral punctures. Then, following \novarian incision, the cyst was enucleated by means of \ntwo autraumatic instruments. Some extraordinary situ-\nations demanded the use of surgical scissors. The cysts \nwere removed by means of endo bags. Haemostasis \nby bipolar coagulation required electric power of 40 W, \nwhile in the sutured group, ovarian haemostasis was \nachieved, using Vicryl 2-0 continuous suture. \nResults \nThe pre-operative mean levels of AMH, inhibin B, \nand AFC did not show statistically significant differenc-\nes in either group, see Table 1. Also, the observed differ-\nences did not attain the level of statistical significance \nTable 1. Comparison of pre-operative AMH, inhibin B, and AFC levels \nPre-operatively\nGroup I – suturing (n = 33)\nPre-operatively \nGroup II – coagulation (n = 33)\nP – the level \nof statistical significance \nAMH 5.66 ±4.48 4.93 ±4.12 0.773\nInhibin B 60.71 ±47.25 61.25 ±55.75 0.783\nAFC 8 ±5.27 7 ±4.10 0.839\n\nMenopause Review/Przegląd Menopauzalny 17(1) 2018\n24\nwhen the same parameters were compared between \nthe sutured group and the coagulated group 3 months \nafter the procedure (Table 2).\nComparing pre- and post-operative levels of AMH \nand inhibin B, regardless of the applied haemostasis \ntechnique, a  statistically significant reduction of the \novarian reserve was observed in either group. In the \ncase of AFC, those differences were not statistically sig-\nnificant, see (Fig. 1, 2).\nIn further analysis, the effects of haemostasis tech-\nnique on ovarian reserve were compared in the group \nof patients with endometrial cysts. The mean AMH \nlevel, assayed three months after the surgery, was 2.39 \nin the patients with ovarian endometriosis and haemo-\nstasis, achieved by suturing. Whereas in the patients \nin whom haemostasis was done by electric energy, the \nmean AMH level was 4.54. The numbers of antral folli-\ncles (AFC) and the levels of inhibin B were also analysed \n– their differences did not, however, attain statistical \nsignificance (Table 3) \nWhile comparing the ovarian reserve factors among \nthe patients with endometrial and dermoid cysts, the \nTable 2. Comparison of post-operative (after 3 months) AMH, inhibin B, and AFC levels \nPre-operatively\nGroup I – suturing (n = 33)\nPre-operatively \nGroup II – coagulation (n = 33)\nP – the level of statistical \nsignificance \nAMH 3.92 ±5.10 3.50 ±2.97 0.205\nInhibin B 74.82 ±25.95 21.66 ±20.51 0.636 \nAFC 7 ±4.54 9 ±5.267 0.814\nFig. 1A-C. The effects of haemostasis technique on ovarian reserve in the group of patients with applied suturing\n6\n5\n4\n3\n2\n1\n0\n8.5\n8\n7.5\n7\n6.5\n70\n60\n50\n40\n30\n20\n10\n0\nA B C\npre-operative post-operative pre-operative post-operative pre-operative post-operative\nAMH – suturing AFC – suturing Inhibin B – suturing\np < 0.05 p > 0.05 p < 0.05\nFig. 2A-C. The effects of haemostasis technique on ovarian reserve in the group of patients with applied electric \nenergy \n6\n4\n2\n0\n10\n8\n6\n4\n2\n0\n80\n60\n40\n20\n0\nA B C\npre-operative post-operative pre-operative post-operative pre-operative post-operative\nAMH – coagulation AFC – coagulation Inhibin B – coagulation\np < 0.05 p > 0.05 p < 0.05\n\nMenopause Review/Przegląd Menopauzalny 17(1) 2018\n25\ndifferences in AMH levels were statistically significant \nin the group where haemostasis was obtained by sutur-\ning. However, no statistical significance was observed \nfor AMH values in the group of women with applied bi-\npolar coagulation (Fig. 3B). Table 4 demonstrates the \ndifferences between AFC and inhibin B. \nDiscussion\nEndometriosis is a  chronic disease; therefore, the \nstart of treatment always requires a therapeutic man-\nagement plan for the whole life of the affected patient, \nwhich is associated with the quality of life of the pa-\ntients with endometriosis. One of the projects trying to \ncope with this problem was a study by Bergqvist and \nTheorell [8]. They evaluated the quality of life during \nhormonal therapy. A group of 48 women participated; \nthe quality of life was assessed by a  questionnaire, \nstaging the intensity of symptoms, such as depressive-\nanxiety disorders, sleep disorders, and quality of life. \nThe authors observed a significantly higher prevalence \nof depressive-anxiety disorders and sleep problems in \nwomen with endometriosis: a six-month therapy with \nprogestogen brought about a  considerable regression \nof the disease. Endometriosis may also significantly af-\nfect the sexual life of affected patients. Denny et al. [9] \ndemonstrated that pain sensations during sexual inter-\ncourse of patients with diagnosed endometriosis are \nresponsible for limited sexual activity of those women, \nwhich in turn leads to downgraded self-esteem and de-\nteriorated relations with the partner. \nRegardless of endometriosis progression, laparos-\ncopy is the preferred technique of surgical treatment \n[10]. Pharmacological treatment may be an element of \nthe patient’s preparation to surgical procedure, while \na  properly administered pharmacotherapy in postop-\nerative management leads to suppression of further \ndisease recurrence. In this situation, the first-line me-\ndicinal agents include: non-steroidal analgesic agents, \nhormonal bi-component contraceptives, and progesto-\ngens. Dienogest is characterised by a high clinical ef-\nficacy. Dienogest is a  hybrid progestogen because it \ndemonstrates properties that are characteristic for \nderivatives of both 19-norethisterone and 17-OH pro-\nTable 3. The effects of haemostasis technique on ovarian reserve in the group of patients with endometrial cysts 3 months after \nthe surgery\nAMH AFC Inhibin B\nOvary coagulation 4.54 2.37 21.98\nOvary suturing 2.39 4.28 21.82\nStatistical significance p = 0.373 p = 0.351 p = 0.912\nFig. 3A, B. Comparison of AMH \nvalues among the patients with \nendometrial and dermoid cysts, in \nwhom haemostasis was obtained \nby suturing or coagulation of the \novary \n5\n4\n3\n2\n1\n0\n7\n6\n5\n4\n3\n2\n1\n0\nA B\nendometrial cysts dermoid cysts endometrial cysts dermoid cysts\nAMH – suturing AMH – coagulation\np = 0.03 p = 0.86\nTable 4. Comparison of the ovarian reserve (AFC and Inhibin B) among the patients with endometrial and dermoid cysts,  \nin whom haemostasis was obtained by bipolar coagulation or suturing of the ovary\nHaemostasis by\novary suturing\nThe level of \nstatistical \nsignificance\nHaemostasis by \ncoagulation\nThe level of \nstatistical \nsignificance\nEndometrial cysts Dermoid cysts Endometrial cysts Dermoid cysts\nInhibin B 23.07 21.33 p = 0.17 32.6 31.2 p = 0.960\nAFC 7.8 2.06 p = 0.18 8.6 4.6 p = 0.173\n\nMenopause Review/Przegląd Menopauzalny 17(1) 2018\n26\ngesterone. The results of many studies indicate that \ndienogest inhibits the angiogenesis and proliferation \nof endometrial cells, while also suppressing the activity \nof aromatase and cyclooxygenase-2 (COX-2), and leads \nto a decreased synthesis of e2 prostaglandin. It means \nthat dienogest not only changes the hormonal profile \nof treated patients but it also directly influences the en-\ndometrial cells, inhibiting their growth and leading to \ntheir atrophy [11, 12]. Medicinal agents still in the phase \nof studies are aromatase inhibitors, selective oestrogen \nreceptor modulators (SERMs), selective progesterone \nreceptor modulators (SPRM), and immunomodulators.\nThe indications to treatment of endometrial cysts \ninclude, first of all, pain, infertility, and next – the risk of \nmalignant transformation. Various techniques of endo-\nscopic treatment of ovarian endometriosis have been \nreported, including drainage and coagulation, the strip-\nping technique (surgical separation of cyst capsule), or \nthe combined and three-stage technique, proposed by \nDonnez et al. [13]. The surgical standard in the treat-\nment of endometrial cysts is the enucleation of cystic \npseudocapsule. The stripping method – as discussed \nherein – involves the use of two atraumatic gripping \ninstruments, by which the cyst capsule and the normal \novarian parenchyma are pulled apart in two opposite \ndirections. Some investigators have questioned the \nlaparoscopic technique of endometrial cysts enuclea-\ntion from the ovary because it poses a risk of removing \nnormal ovarian tissue during cystic capsule separation, \nleading to the loss of follicles [14, 15]. It was demon-\nstrated in the studies by Donnez et al. that only at the \nhilar region, the ovarian tissue, removed together with \na pseudocapsule, contained primary and secondary fol-\nlicles [16]. In the other parts of the ovary its tissues, \nwhich adhered to the pseudocapsule, did not demon-\nstrate any morphological features of normal ovarian \nparenchyma – in the majority of cases, either few pri-\nmary follicles or no follicles were observed. In all the \npatients qualified to surgery, the technique of ovarian \ncyst enucleation was the same, i.e. the stripping tech-\nnique. The only difference was the technique of obtain-\ning haemostasis. It was then possible to compare the \neffects of ovary suturing and bipolar coagulation on the \novarian reserve.\nThe ovarian reserve determines the fertility poten-\ntial of woman: the degree of egg cell resource usage, \nmore accurately, of the primary follicles of which egg \ncells are formed. A woman is born with a definite pool \nof egg cells, which are then used up in puberty, ado-\nlescence, and then in subsequent monthly cycles until \nmenopause, when they completely disappear. An evalu-\nation of the ovarian reserve enables us to identify to \nwhich stage of the process a woman can be assigned. \nIt also makes it possible to assess the current repro-\nductive ability of the ovaries and anticipate a probable \nreaction of the ovaries to the stimulation of ovulation. \nThe number of AFC (antral follicle count), serum AMH \nconcentration, and serum FSH and inhibin B concentra-\ntions, assayed on the second or the third day of the \ncycle, are the most reliable methods of ovarian reserve \nevaluation.\nAMH is a  dimeric glycoprotein, belonging to the \ngroup of transforming β growth factors [17, 18]. It oc-\ncurs both in women and men but plays a different role \nin each gender. In women, a  significant presence of \nAMH is perceived only after puberty in granule cells of \nprimary ovarian follicles with diameter 4-6 mm, where \nit is produced [19, 20]. The fact of the exclusively ovar -\nian origin of AMH was confirmed by La Marca et al. in \ntheir study, in which AMH levels were undetectable in \nwomen after 3-5 days form bilateral ovariectomy [21]. \nThe serum AMH level corresponds to the pool of small \novarian follicles, which is demonstrated by decreased \nAMH levels in peripheral blood prior to the fall in the \nnumber of growing follicles. A  constant level of AMH \nduring the menstrual cycle makes AMH a  unique en-\ndocrine parameter, evaluating the functions of female \nsex gonads.\nThe number of antral follicles is the best sonograph-\nic determinant of the ovarian reserve. The antral fol-\nlicles are follicles in the ovaries, of 2-8 mm in diameter, \nready to grow under the influence of natural gonado-\ntropins, produced by the pituitary gland, or of the same \nhormones administered from the outside in therapeutic \ncourse. While growing, the antral follicles become dom-\ninating follicles and egg cells mature in them. Inhibin B \nis another marker of the ovarian reserve. It is produced \nby the granule cells of early antral follicles and released, \nfirst of all, during the follicular phase of the menstrual \ncycle. Its concentration in the early follicular phase re-\nflects the number and quality of ovarian follicles.\nIn our study, we compared the effects of two hae-\nmostasis techniques (ovary suturing and bipolar coagu-\nlation) on the ovarian reserve, following laparoscopic \ncyst enucleation. The mechanism of ovarian reserve re-\nduction is not yet fully recognised. Bipolar coagulation \nmay cause damage to surrounding tissues, as well as \nischaemia [22]. Ovary suturing may also lead to ischae-\nmia and reduced ovarian reserve. Another proposed \nmechanism, which reduces the ovarian reserve, is the \ndevelopment of anti-Mullerian antibodies after laparo-\nscopic cyst enucleation. These antibodies decrease the \novarian reserve, but there are no reports about their \npost-operative occurrence [23]. A considerable decrease \nof post-operative AMH levels was observed in a  few \nstudies vs. pre-operative AMH values, both in patients \nwith endometrial cysts and in those with non-endome-\ntrial cysts; however, the studies concentrated on the \nfirst month after laparoscopic surgery [24, 25]. One of \nthe studies demonstrated a big fall in AMH level during \nthe first seven days after surgery, followed by a gradual \nincrease of the anti-Mullerian hormone level, which – \n\nMenopause Review/Przegląd Menopauzalny 17(1) 2018\n27\nafter three months – obtained 65% of its baseline value \n[26]. It was confirmed by the studies of Chang et al. \n[26], where the ovarian reserve was decreased imme-\ndiately after cyst enucleation and which gradually re-\nturned to its pre-operative value within three months \nafter surgery. \nCanis et al. showed that the coefficient of getting \npregnant and the number of egg cells, obtained be-\nfore the procedures of medically assisted reproduc-\ntive technology, was not significantly decreased after \nlaparoscopic enucleation of ovarian cysts [27]. In turn, \nMuzii et al. [28] described in their studies an ovarian \ntissue, adhering to the wall of cystic capsule, in 6% of \nremoved non-endometrial and in 54% of endometrial \nlesions; however, the adhered and removed tissues did \nnot present the morphological features of normal ovar-\nian tissue.\nWe found in our study that both ovary suturing and \nbipolar electrocoagulation, applied after laparoscopic \nenucleation of cysts, decreased the ovarian reserve. \nComparing both haemostasis techniques, no method \nwas demonstrated that would have exerted a smaller \nimpact on AMH, AFC, or inhibin B levels. \nConclusions \nLaparoscopic enucleation of cysts leads to decreased \novarian reserve, regardless of haemostasis technique. \nTherefore, the use of either intraperitoneal sutures or \nelectrocoagulation should be very precise and delicate \nto minimise the extent of damage to normal ovarian \ntissue. \nDisclosure\nAuthors report no conflict of interest.\nReferences\n1. Owczarek D, Malinowski A. 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Laparoscopic excision of ovarian \ncysts does not result in antiovarian humoral autoimmunity. Fertil Steril \n2005, 84: 1772-1774.\n24. Bussaca M, Riparini J, Somniagliana E, et al. Postsurgical ovarian failure \nafter laparoscopic excision of bilateral endometriosis. Am J Obstet Gy-\nnecol 2006; 195: 421-425.\n25. Iwase A, Hirokawa W, Goto M, et al. Serum anti-Müllerian hormone \nlevel is a useful marker for evaluating the impact of laparoscopic cys-\ntectomy on ovarian reserve. Fertil Steril 2010; 94: 2846-2849.\n26 Chang H, Han S, Lee J, et al. Impact of laparoscopic cystectomy on ovar-\nian reserve: serial changes of serum anti- Müllerian hormone. Fertil \nSteril 2010; 94: 343-349.\n27. Canis M, Pouly JL, Tamburro S, et al. Ovarian response during IVF-em-\nbryo transfer cycles after laparoscopic ovarian cystectomy for endome-\ntriotic cysts of 3 cm in diameter. Hum Reprod 2001; 16: 2583-2586.\n28. Muzii L, Bianchi A, Croce C, et al. Laparoscopic excision of ovarian cysts: \nis the stripping technique a tissue sparing procedure? Fertil Steril 2002, \n78: 876-878.","source_license":"CC0","license_restricted":false}