Shunichiro Tsuji 1, Takashi Murakami 1, Fuminori Kimura 1,SatoshiTanimura 2, Masataka Kudo 3, Makio Shozu 4, Hisashi Narahara 5 and Norihiro Sugino 6
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1 doi: /jog J. Obstet. Gynaecol. Res. Vol. 41, No. 9: , September 2015 Management of secondary infertility following cesarean section: Report from the Subcommittee of the Reproductive Endocrinology Committee of the Japan Society of Obstetrics and Gynecology Shunichiro Tsuji 1, Takashi Murakami 1, Fuminori Kimura 1,SatoshiTanimura 2, Masataka Kudo 3, Makio Shozu 4, Hisashi Narahara 5 and Norihiro Sugino 6 1 Department of Obstetrics and Gynecology, Shiga University of Medical Science, Shiga 2 Department of Obstetrics and Gynecology, Toyama Prefectural Central Hospital, Toyama 3 Department of Obstetrics and Gynecology, Hokkaido University, Hokkaido 4 Department of Obstetrics and Gynecology, Chiba University, Chiba 5 Department of Obstetrics and Gynecology, Oita University Faculty of Medicine, Oita; and 6 Department of Obstetrics and Gynecology, Yamaguchi University Hospital, Yamaguchi, Japan Abstract Aim: The aim of this study was to examine the current status and management of secondary infertility following cesarean section in Japan. Material and Methods: A two-step questionnaire survey was performed in 1092 facilities, including teaching hospitals and artificial reproductive technology clinics, registered with the Japan Society of Obstetrics and Gynecology. In our questionnaires, we obtained data about symptoms, clinical findings, diagnostic methods, and pregnancy outcomes. Treatments were sorted into three groups, namely typical infertility treatment (group A), conservative treatment (group B), and operative treatment (group C). Results: Of the 1092 facilities, 616 (56%) sent back reply forms to the first questionnaire; 56 (32%) of 176 facilities answered the second questionnaire, and 189 cases were able to be analyzed after completion of the two questionnaires. The commonest symptom was abnormal uterine bleeding during the follicular phase (91 cases; 48% of the 189 eligible cases), and the commonest clinical finding was fluid pooling in the area of cesarean scar dehiscence during the ovulatory phase (142 cases; 75%). The most commonly used diagnostic method was transvaginal ultrasound (153 cases, 81%). The pregnancy rate was 33% in group A, 50% in group B, and 60% in group C. In patients with abnormal uterine bleeding, painful symptoms and fluid pooling at the cesarean scar dehiscence, the pregnancy rate was significantly higher in group C (64%) than in group A (16%; P = ). Conclusions: We recommend operative treatment for secondary infertility following cesarean section with painful symptoms and fluid pooling at the site of cesarean scar dehiscence. Key words: cesarean scar dehiscence, cesarean scar syndrome, secondary infertility. Introduction As in other countries, in Japan the cesarean section rate is increasing each year: by 2011, it had reached 19.2%. 1 With this increase, obstetricians and gynecologists are seeing increased numbers of cases of postmenstrual abnormal uterine bleeding, pelvic pain, and infertility following cesarean section. These various symptoms were reported for the first time by Morris as cesarean scar syndrome (CSS). 2,3 The cause of secondary infertility Received: February Accepted: April Reprint request to: Assistant Professor Shunichiro Tsuji, Department of Obstetrics and Gynecology, Shiga University of Medical Science, Seta Tsukinowa-cho, Ohtsu, Shiga , Japan. tsuji002@belle.shiga-med.ac.jp 2015 Japan Society of Obstetrics and Gynecology 1305
2 S. Tsuji et al. following cesarean section was considered to be the pooling of blood in the cesarean scar defect. 4,5 This blood has negative effects on sperm in the uterus and can lead to implantation failure of the embryo. However, protocols for the diagnosis and treatment of secondary infertility caused by CSS have not been established. Therefore, we (the Subcommittee of the Reproductive Endocrinology Committee of the Japan Society of Obstetrics and Gynecology [JSOG]) decided to perform a two-step questionnaire survey. We have already presented a brief summary of the data as an annual report in Japanese. 6 Here, we analyze the data in more detail and suggest a protocol for managing secondary infertility following cesarean section. Methods We performed a postal, two-step questionnaire survey. 6 The first questionnaire was sent to 1092 facilities, namely 666 teaching hospitals and 426 artificial reproductive technology (ART) clinics registered with the JSOG. A second questionnaire was sent to the 176 facilities that had stated in the first questionnaire that they had managed secondary infertility caused by CSS. These facilities were required in the second questionnaire to give detailed data on their cases. We analyzed the interrelation among symptoms, clinical findings and treatments minutely for suggesting a therapeutic principle for this clinical condition. In regards to cesarean scar dehiscence, we surveyed scar length, defect size, residual myometrial thickness and scar width. Statistical evaluation was performed with GraphPad Prism 5. Continuous variable data were analyzed using the Mann Whitney U-test. Fisher s exact test was used between two groups, and the Kruskal Wallis test was used among three groups. A P-value of <0.05 was considered to indicate statistical significance. The survey was approved by the Ethics Committee of Shiga University of Medical Science (approval number; ). bleeding during the follicular phase (48%), ovulatory phase (42%), or luteal phase (12%); dysmenorrhea (30%); and chronic pelvic pain (11%). Multiple answers were allowed. The clinical findings were uterine anteversion (55%) and retroversion (31%); fluid pooling in the area of cesarean scar dehiscence during the follicular phase (70%), ovulatory phase (75%), or luteal phase (29%); and fluid pooling in the uterine cavity during the follicular phase (44%), ovulatory phase (44%), or luteal phase (9%). Multiple answers were allowed. Almost all of the gynecologists used transvaginal ultrasound to diagnose cesarean scar dehiscence. Approximately 81% of gynecologists considered transvaginal ultrasound to be the most useful examination method for diagnosis. The survey assessed cesarean scar size. In regards to cesarean scar dehiscence, we surveyed scar length, defect size, residual myometrial thickness and scar width (Fig. 1a). The median craniocaudal length of the scar was 8.9 mm, the median defect depth was 6.2 mm, the median residual myometrial thickness was 3.2 mm, and the median scar width was 17.5 mm (Fig. 1b). Results As reported previously, of 1092 facilities (56%) returned reply forms to the first questionnaire; 496 of 616 facilities (81%) answered that they were aware of CSS, 61% of facilities had experienced cases of CSS, and 29% facilities had seen secondary infertility following cesarean section. Fifty-six of 176 facilities (32%) answered, and 189 cases were enrolled. The symptoms were: prolonged menstruation (38%); abnormal uterine Figure 1 (a) We surveyed the size of the cesarean scar dehiscence. 1 Scar length. 2 Defect depth. 3 Residual myometrial thickness. 4 Scar width. (b) Size of the cesarean scar dehiscence. Values are medians. shows outliers Japan Society of Obstetrics and Gynecology
3 Managing post-cesarean infertility Treatments for secondary infertility following cesarean section were sorted into three groups, namely typical infertility treatment, such as ovulation induction, intrauterine insemination, or in vitro fertilization embryo transfer (group A); conservative treatment, such as suction drainage of the pooled fluid and insertion of oxidized cellulose into the uterine defect (group B); and operative treatment, such as laparotomy, laparoscopy, or hysteroscopy (group C). There were no significant differences in cesarean scar size among the three groups, although there were significant differences in residual myometrial thickness of all patients (Table 1). Pregnancy rate after treatments was known in 165 of the 189 cases. The pregnancy rate was 33% (35 of 107 cases) in group A, 50% (8 of 16 cases) in group B, and 60% (25 of 42 cases) in group C. The pregnancy rate was significantly higher in group C than in group A (P = ). In group A, various treatments were given to achieve pregnancy (Fig. 2), although there were no significant differences among the different treatments. In group B, there were also no significant differences among the different treatments. In group C, there were no significant differences in pregnancy rates among patients who received laparotomy (57%: 9 of 16 cases), Table 1 Association between cesarean scar size (mm) and treatment group Group A Group B Group C P-value All patients ( ) 9.8 ( ) 9.5 ( ) ( ) 7.3 ( ) 7.9 ( ) ( ) 5.2 ( ) 3.0 ( ) ( ) 16.3 ( ) 18.0 ( ) Patients achieving pregnancy ( ) 10.0 ( ) 10.5 ( ) ( ) 6.5 ( ) 6.4 ( ) ( ) 4.6 ( ) 3.3 ( ) ( ) 16 ( ) 18.3 ( ) Numbers are medians (with ranges). 1 Scar length. 2 Scar defect depth. 3 Residual myometrial thickness. 4 Scar width. Group A, typical infertility treatment group; Group B, conservative treatment group; Group C, operative treatment group. Figure 2 (a) Management of patients in group A before ovulation. (b) Management of patients in group A around the time of fertilization. (c) Pre-ovulation management of those patients in group A who became pregnant. (d) Pre-fertilization management of those patients in group A who became pregnant. (a, c) ( )Natural.( ) Clomiphene citrate. ( ) Human menopausal gonadotrophin. ( ) Controlled ovarian stimulation. (b,d) ( )Natural. ( ) Intrauterine insemination. ( ) In vitro fertilization. ( ) Intracytoplasmic sperm injection Japan Society of Obstetrics and Gynecology 1307
4 S. Tsuji et al. laparoscopic surgery (50%: 10 of 20 cases), or hysteroscopic surgery (100%: 6 of 6 cases). Major symptoms were sorted into three groups, namely an abnormal uterine bleeding group, a dysmenorrhea group, and a chronic pelvic pain group. Distribution analysis showed that patients with chronic pelvic pain were included among patients with dysmenorrhea, and patients with dysmenorrhea were included Figure 3 (a) Distributions of the three main symptoms in patients with secondary infertility following cesarean scar syndrome. Numbers of patients are shown in the circles. ( ) Abnormal uterine bleeding group. ( ) Dysmenorrhea group. ( ) Chronic pelvic pain group. (b) Association between pregnancy rate and treatment group in asymptomatic patients. Group A, 41 patients; group B, 4 patients; group C, 3 patients. (c) Association between pregnancy rate and treatment group in symptomatic patients. Group A, 66 patients; group B, 12 patients; group C, 43 patients. (d) Association between pregnancy rate and treatment group in patients with abnormal uterine bleeding only. Group A, 47 patients; group B, 10 patients; group C, 17 patients. (e) Association between pregnancy rate and treatment group in patients with dysmenorrhea or chronic pelvic pain. Group A, 16 patients; group B, 2 patients; group C, 26 patients. Group A, typical infertility treatment; group B, conservative treatment; group C, operative treatment Japan Society of Obstetrics and Gynecology
5 Managing post-cesarean infertility among patients with abnormal uterine bleeding (Fig. 3a). Analysis of the association between symptoms and pregnancy rate revealed no significant difference in pregnancy rates in asymptomatic patients among groups A, B, and C (Fig. 3b). In symptomatic patients, the pregnancy rate was significantly higher in group C than in group A (P = ; Fig. 3c), although in patients with abnormal uterine bleeding only, there were no significant differences among the three groups (Fig. 3d). In patients with not only abnormal uterine bleeding but also dysmenorrhea and chronic pelvic pain, the pregnancy rate was significantly higher in group C than in group A (P = ; Fig. 3e). The major clinical findings were sorted into two groups, namely fluid pooling in the cesarean scar dehiscence and fluid pooling in the uterine cavity. Distribution analysis showed that the patients with fluid pooling in the uterine cavity included those with fluid pooling in the area of cesarean scar dehiscence (Fig. 4a). Analysis of the association between clinical findings and pregnancy rate revealed no significant difference in pregnancy rate between group A and C patients with no fluid pooling in the uterine cavity (Fig. 4b), although there was no patient in group B. In patients with fluid pooling in the cesarean scar dehiscence, the pregnancy rate was significantly higher in group C patients than in group A ones (P = ; Fig. 4c). In patients with fluid pooling in the uterine cavity, the pregnancy rate was significantly higher in group C than in group A(P = ; Fig. 4d). These results did not change among times of the menstrual cycle when clinical examination was performed. In patients with uterine anteversion or uterine retroversion, pregnancy rates were also significantly higher in group C than in group A (P = , P = , respectively). Discussion Our survey reflects the present management of secondary infertility following cesarean section in general gynecological hospitals and clinics in Japan. The variety of Figure 4 (a) Distributions of the two main clinical findings in cesarean scar syndrome patients. Numbers of patients are shown in the circles. ( ) Pooling of fluid in the cesarean scar dehiscence. ( ) Pooling of fluid in the uterine cavity. (b) Association between pregnancy rate and treatment in patients with no clinical findings. Group A, 10 patients; group C, 1 patient. (c) Association between pregnancy rate and treatment in patients with pooling of fluid in the cesarean scar dehiscence. Group A, 90 patients; group B, 16 patients; group C, 45 patients. (d) Association between pregnancy rate and treatment in patients with pooling of fluid in the uterine cavity. Group A, 49 patients; group B, 14 patients; group C, 30 patients. Group A, typical infertility treatment; group B, conservative treatment; group C, operative treatment Japan Society of Obstetrics and Gynecology 1309
6 S. Tsuji et al. management strategies used shows that a firm protocol for treating secondary infertility following cesarean section has not yet been established. However, the existence of the disease is gradually becoming known. Our survey also revealed that the symptoms and clinical findings of secondary infertility following cesarean section had characteristic distributions. Therefore, we suggest that the disease can be staged according to the clinical symptoms and findings (Fig. 5). Although there were no statistically significant differences among staging, the pregnancy rate tended to decrease with increasing staging. In other words, it was difficult to treat cases with painful symptoms by using general infertility treatment. Our analysis of the clinical findings suggested that pooled fluid flowed from the area of cesarean scar dehiscence into the uterine cavity. Therefore, treatment in this regard also needs to be established according to disease staging. We suggest a classification of cases into four classes on the basis of the survey data and our deliberations (Table 2a). There were no specific differences in treatment recommendation among classes 1 and 2 (Table 2b), but in class 3 there was a non-significant trend toward better pregnancy outcome in groups B and C than in group A (Fig. 6a), and in class 4 there was a significantly better pregnancy outcome in group C than in group A (P = ; Fig. 6b). Therefore, we recommend operative treatment for patients with painful symptoms (Table 2b). There were no significant differences in pregnancy rate among laparotomy, laparoscopic surgery, and hysteroscopic surgery. However, interestingly, the pregnancy rate after hysteroscopic surgery was very high. This result agrees with those of many past reports Although hysteroscopic surgery is superior, the problem of indications remains, because there is a risk of uterine perforation during surgery. Li et al. 11 Table 2a Proposed classification of secondary infertility following cesarean section Class Abnormal genital bleeding Symptom Dysmenorrhea or chronic pelvic pain Clinical finding Fluid pooling in cesarean scar 1 〇 or 〇 or 2 〇 3 〇 〇 4 〇 〇 〇 ( 〇 )Present.( ) Not present. Table 2b Strategies for treating secondary infertility following cesarean section Treatment General infertility treatment Conservative treatment Operative treatment Class 1 〇 〇 〇 2 〇 〇 〇 3 Δ 〇〇 4 Δ 〇 ( ) Treatment strongly recommended. ( 〇 ) Treatment recommended. (Δ) Other treatments may be better. recommended hysteroscopic treatment of patients with residual myometrial thickness of 3.5 mm or a defect that accounted for <50% of the anterior uterine wall. In these days, it was reported to vaginal repair with the laparoscopy, laparoscopic repair with complete resection of the fibrotic tissue and robotic repair of uterine dehiscence The choice of an optimal operative method will become clearer in the near future, as additional cases are reported. Donnez et al. 13 reported patients who had blood retention in the dehiscent scar, with pelvic pain and Figure 5 Staging of patients with secondary infertility following cesarean scar syndrome according to (a) clinical symptoms and (b) clinical findings. (a) ( ) Abnormal uterine bleeding group. ( ) Dysmenorrhea group. ( ) Chronic pelvic pain group. (b) ( ) Pooling of fluid in the cesarean scar dehiscence. ( ) Pooling of fluid in the uterine cavity. Arrows show expected pathologic progression Japan Society of Obstetrics and Gynecology
7 Managing post-cesarean infertility group A consisted of only 107 cases. There was no CSP in groups B and C, and there have been no cases of CSP in many past reports of operative treatment Although the total number of cases in groups B and C and in past reports is less than about 200, our results and those of these other reports suggest that surgical treatment may not only increase pregnancy rates and decrease pelvic pain but also prevent CSP. However, we need to be aware of the possible occurrence of CSP in patients treated hysteroscopically, because with these procedures, the cesarean scar may not completely vanish. To our knowledge, ours was the first survey to compare the various treatments for secondary infertility following cesarean section and to attempt to develop a management protocol. However, a weakness of our study is that it was retrospective and used a questionnaire survey. Both the accumulation of additional cases and a prospective study are required. Acknowledgments This survey was fully supported by JSOG. We thank the 401 medical institutions training clinical fellows and the 215 clinics and hospitals registered with JSOG to perform ART for responding to the questionnaires in this survey. Figure 6 (a) Association between pregnancy rate and treatment group in class 3. Group A, 44 patients; group B, 10 patients; group C, 17 patients. (b) Association between pregnancy rate and treatment group in class 4. Group A, 14 patients; group B, 2 patients; group C, 25 patients. Group A, typical infertility treatment; group B, conservative treatment; group C, operative treatment. dysmenorrhea, and whose pelvic pain and dysmenorrhea disappeared after laparoscopic surgery. Therefore, retention of old blood in the cesarean scar dehiscence may result in the production of substances such as cytokines that obstruct embryo implantation and induce painful symptoms. The single case of cesarean scar pregnancy (CSP) we observed in group A was not a matter that could be ignored (data not shown), because patients with CSP are at severe risk of hemorrhagic shock and uterine rupture. 15 The incidence of CSP has increased over the last decade: Kutuk et al. 16 found that rates of CSP have increased and are now 1 in However, our Disclosure The authors have no conflict of interest to declare. References 1. Ministy of Health, Labour and Welfare. Health care facilities report [Cited 26 May 2014]. Available from mhlw.go.jp/toukei/list/dl/130-25_2.pdf 2. Morris H. Surgical pathology of the lower uterine segment caesarean section scar: Is the scar a source of clinical symptoms? Int J Gynecol Pathol 1995; 14: Morris H. Caesarean scar syndrome. SAfrMedJ1996; 86: Florio P, Filippeschi M, Moncini I, Marra E, Franchini M, Gubbini G. Hysteroscopic treatment of the cesarean-induced isthmocele in restoring infertility. Curr Opin Obstet Gynecol 2012; 24: Fabres C, Aviles G, De La Jara C et al. The cesarean delivery scar pouch: Clinical implications and diagnostic correlation between transvaginal sonography and hysteroscopy. JUltrasoundMed 2003; 22: Sugino N. Annual report of Reproductive Endocrinology Committee, Japan Society of Obstetrics and Gynecology, Acta Obstet Gynaecol Jpn 2015; 67 (forthcoming). (In Japanese.) 2015 Japan Society of Obstetrics and Gynecology 1311
8 S. Tsuji et al. 7. Gubbini G, Casadio P, Marra E. Resectoscopic correction of the isthmocele in women with postmenstrual abnormal uterine bleeding and secondary infertility. J Minim Invasive Gynecol 2008; 15: Fabres C, Arriagada P, Fernández C, Mackenna A, Zegers F, Fernández E. Surgical treatment and follow-up of women with intermenstrual bleeding due to cesarean section scar defect. J Minim Invasive Gynecol 2005; 12: Gubbini G, Centini G, Nascetti D et al. Surgical hysteroscopic treatment of cesarean-induced isthmocele in restoring fertility: Prospective study. J Minim Invasive Gynecol 2011; 18: Fernandez E, Fernandez C, Fabres C, Alam VV. Hysteroscopic correction of cesarean section scars in women with abnormal uterine bleeding. J Am Assoc Gynecol Laparosc 1996; 3 (Suppl 4): S Li C, Guo Y, Liu Y, Cheng J, Zhang W. Hysteroscopic and laparoscopic management of uterine defects on previous cesarean delivery scars. J Perinat Med 2014; 42: Klemm P, Koehler C, Mangler M, Schneider U, Schneider A. Laparoscopic and vaginal repair of uterine scar dehiscence following cesarean section as detected by ultrasound. JPerinat Med 2005; 33: Donnez O, Jadoul P, Squifflet J, Donnez J. Laparoscopic repair of wide and deep uterine scar dehiscence after cesarean section. Fertil Steril 2008; 89: La Rosa MF, McCarthy S, Richter C, Azodi M. Robotic repair of uterine dehiscence. J Soc Laparoendosc Surg 2013; 17: Ash A, Smith A, Maxwell D. Caesarean scar pregnancy. Br J Obstet Gynaecol 2007; 114: Kutuk MS, Uysal G, Dolanbay M, Ozgun MT. Successful medical treatment of cesarean scar ectopic pregnancies with systemic multidose methotrexate: Single-center experience. J Obstet Gynaecol Res 2014; 40: Japan Society of Obstetrics and Gynecology
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