{"paper_id":"f656909e-099f-4e64-9bbf-299fe2720dc6","body_text":"RESEARCH Open Access\n© The Author(s) 2023. Open Access  This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, \nsharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and \nthe source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this \narticle are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included \nin the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will \nneed to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The \nCreative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available \nin this article, unless otherwise stated in a credit line to the data.\nKomatsu et al. BMC Pregnancy and Childbirth          (2023) 23:579 \nhttps://doi.org/10.1186/s12884-023-05895-w\nBMC Pregnancy and Childbirth\n*Correspondence:\nHiroaki Komatsu\nkomatsu.h.med@gmail.com\n1Department of Obstetrics and Gynecology, Tottori University School of \nMedicine, 36-1 Nishicho, Tottori prefecture, Tottori 683-8504, Japan\n2Tottori University, Tottori, Japan\nAbstract\nBackground A previous study investigated the effect of adenomyosis on perinatal outcomes. Some studies have \nreported varying effect of adenomyosis on pregnancy outcomes in some patients and dependence on the degree \nand subtype of uterine lesions. To elucidate the impact of adenomyosis on perinatal outcomes.\nMethods This large-scale cohort study used the perinatal registry database of the Japan Society of Obstetrics \nand Gynecology. A dataset of 203,745 mothers who gave birth between January 2020 and December 2020 in \nJapan was included in the study. The participants were divided into two groups based on the presence or absence \nof adenomyosis. Information regarding the use of fertility treatment, delivery, obstetric complications, maternal \ntreatments, infant, fetal appendages, obstetric history, underlying diseases, infectious diseases, use of drugs, and \nmaternal and infant death were compared between the groups.\nResults In total, 1,204 participants had a history of adenomyosis and 151,105 did not. The adenomyosis group \nhad higher rates of uterine rupture (0.2% vs. 0.01%, P = 0.02) and placenta accreta (2.0% vs. 0.5%, P < 0.001) than the \nnon-adenomyosis group. A history of adenomyosis (odds ratio: 2.26; 95% confidence interval: 1.43–3.27; P < 0.001), \nuterine rupture (odds ratio: 3.45; 95% confidence interval: 0.89–19.65; P = 0.02), placental abruption (odds ratio: 2.11; \n95% confidence interval: 1.27–3.31; P < 0.01), and fetal growth restriction (odds ratio: 2.66; 95% confidence interval: \n2.00–3.48; P < 0.01) were independent risk factors for placenta accreta.\nConclusion Adenomyosis in pregnancies is associated with an increased risk of placenta accreta, uterine rupture, \nplacental abruption, and fetal growth restriction.\nTrial registration Institutional Review Board of Tottori University Hospital (IRB no. 21A244).\nKeywords Placental abruption, Adenomyosis, Fertility, Fetal growth restriction, Japan, JSOG database, Miscarriage, \nPlacenta accreta, Pregnancy, Uterine rupture\nImpact of adenomyosis on perinatal \noutcomes: a large cohort study (JSOG \ndatabase)\nHiroaki Komatsu1*, Fuminori Taniguchi1 and Tasuku Harada2\n\nPage 2 of 7\nKomatsu et al. BMC Pregnancy and Childbirth           (2023) 23:579 \nBackground\nAdenomyosis is defined as the presence of endome -\ntrial glands and stroma within the myometrial layer. The \ntrue prevalence of adenomyosis is unknown, with over -\nall reported rates of 1–70%, but it is thought to be 20%, \nspecifically in women of reproductive age [ 1]. Previously, \nadenomyosis was considered to be associated with multi -\nparity, not infertility. Since non-surgical diagnosis using \nultrasound images and magnetic resonance imaging \nbecame possible, an association between adenomyosis \nand fertility or miscarriage was suggested [2].\nDuring pregnancy, as it becomes difficult to evaluate \nthe entire myometrial layer in the second trimester, the \npresence or absence of adenomyosis should be assessed \nbefore conception or in early pregnancy. A previous \nstudy investigated the effect of adenomyosis on perinatal \noutcomes [2]. Some studies have reported varying effect \nof adenomyosis on pregnancy outcomes in some patients \nand dependence on the degree and subtype of uterine \nlesions. The impact of endometriosis or uterine adeno -\nmyosis on perinatal outcomes was previously reported, \nusing data from a large cohort of the Japan Environment \nand Children’s Study [ 3, 4]. The study concluded that \nadenomyosis increased the risk of placental abruption \nand fetal growth restriction (FGR), but the number of \ncases in the study, approximately 300, was not very large. \nNo study has examined the effect of adenomyosis using \nlarge-scale data of > 1,000 individuals [5].\nHere, we conducted a large-scale cohort study using \nthe perinatal registry database of the Japan Society of \nObstetrics and Gynecology (JSOG), aiming to elucidate \nthe impact of adenomyosis on perinatal outcomes in \nanother population.\nMethods\nThe perinatal registry database is a project managed by \nthe JSOG that includes data from 408 facilities that pro -\nvide perinatal care in Japan (107 university hospitals, 29 \nNational Organization hospitals, 34 Red Cross hospitals, \nand 238 other facilities). The registry collects delivery \ndata annually, and 95 of 110 general perinatal centers \n(86.3%) and 207 of 298 regional perinatal centers (69.5%) \nin Japan are included in the database. Patients who give \nbirth after 22 weeks of gestation are enrolled in the \ndatabase.\nData from 203,745 to 840,832 mothers (24.2%) who \ngave birth in Japan from January 2020 to December \n2020 were included in this study. The participants were \ngrouped into adenomyosis and non-adenomyosis groups \nbased on their history of adenomyosis. Participant \ncharacteristics (age, pregnancy and delivery histories, \nmedical history, and body mass index), fertility treat -\nments, delivery data (delivery method, inclusion of hys -\nterectomy, induction/labor acceleration, instrumental \nprocedures, heart rate, and non-reassuring fetal status), \nobstetric complications, maternal treatments, infant \ndata (gestational age, sex, height, weight, Apgar scores, \nand malformation), fetal appendage data, obstetric his -\ntory, underlying diseases, infectious diseases, drugs used, \nmaternal death data, and infant death data were com -\npared between the groups.\nThis study was approved by the Institutional Review \nBoard of Tottori University Hospital (IRB no. 21A244) \nand JSOG IRB committee (IRB no. 2021-17). All patients \nprovided written informed consent following the institu -\ntional guidelines. All methods were carried out in accor -\ndance with relevant guidelines and regulations.\nStatistical analysis\nContinuous data are presented as mean and standard \ndeviation. Categorical data are presented as number and \nfrequency. The Mann-Whitney U-test and chi-squared or \nFisher’s exact test were used to compare the variables. A \nmultivariate analysis using a logistic regression analysis \nwas performed. Statistical significance was set at P < 0.05. \nAll statistical analyses were performed using GraphPad \nPrism 8.3 software (GraphPad Software, Inc., La Jolla, \nCA, USA).\nResults\nOf the 203,745 pregnancies in the database, there were \n1,653 adenomyosis cases and 202,092 non-adenomyosis \ncases. Excluding cases with a history of cesarean section \nand twin pregnancies, this study examined 1,204 adeno -\nmyosis cases (adenomyosis group) and 151,105 non-ade -\nnomyosis cases (non-adenomyosis group).\nInformation on patient background is provided in \nTable 1.\nThe adenomyosis group was significantly older and had \nlarger proportions of primiparas and pregnancies result -\ning from assisted reproductive technology (ART) than \nthe non-adenomyosis group (adenomyosis vs. non-ade -\nnomyosis; 20.6% vs. 9.6%, P < 0.01). Further, the adeno -\nmyosis group had higher rates of cesarean Sect. (20.9% vs. \n8.3%, P < 0.01) and premature deliveries (10.6% vs. 9.6%, \nP < 0.01) than the non-adenomyosis group. Additionally, \nthe adenomyosis group had higher rates of premature \ndelivery (19.3% vs. 12.5%, P < 0.01), uterine rupture (0.2% \nvs. 0.01%, P = 0.02), placental abruption (1.6% vs. 0.9%, \nP = 0.02), preeclampsia (10.0% vs. 6.5%, P < 0.01), and \nintrauterine growth restriction (5.3% vs. 3.8%, P < 0.01) \nthan the non-adenomyosis group.\nWe then examined placental malposition. The adeno -\nmyosis group had significantly higher rates of placental \nmalposition (total placenta previa, edge placenta previa, \npartial placenta previa, and low placenta) and placenta \naccreta (2.0% vs. 0.5%, P < 0.01) than the non-adenomy -\nosis group (Table 2).\n\nPage 3 of 7\nKomatsu et al. BMC Pregnancy and Childbirth           (2023) 23:579 \nA multivariate analysis identified ART pregnancies \n(odds ratio (OR): 7.20; 95% confidence interval (CI): \n6.26–8.28; P < 0.001), complication of adenomyosis (OR: \n2.26; 95% CI: 1.43–3.27; P = 0.001), and history of uter -\nine myomectomy (OR: 2.62; 95% CI: 1.5–4.22; P < 0.01) \nas independent risk factors for placenta accreta (Fig.  1) \n[5]. In an examination of risk factors for uterine rupture, \nadenomyosis (OR: 3.45; 95% CI: 0.89–19.65; P = 0.02) was \nidentified as an independent risk factor, in addition to \nART pregnancies (OR: 2.88; 95% CI: 1.30–5.97; P < 0.01), \npremature delivery (OR: 6.99; 95% CI: 0.12–11.70; \nP = 0.42), and uterine myomectomy (OR: 7.41; 95% CI: \n12.56–82.94; P < 0.01) (Fig. 2). Adenomyosis was an inde-\npendent risk factor for placental abruption and FGR (OR: \n2.11; 95% CI: 1.27–3.31; P < 0.01, and OR: 2.66; 95% CI: \n2.00–3.48; P < 0.01, respectively) (Figs. 3 and 4).\nDiscussion\nPrincipal findings\nThe present study investigated the impact of adeno -\nmyosis on perinatal outcomes using the JSOG Perinatal \nRegistry Database and identified adenomyosis as a risk \nfactor for placenta accreta as well as an independent fac -\ntor for uterine rupture, placental abruption, and FGR. \nThis indicates that perinatal management of pregnancies \ncomplicated by adenomyosis should be conducted con -\nsidering these risks.\nResults in the context of what is known\nSeveral studies have investigated the effect of adeno -\nmyosis on perinatal outcomes. Cozzolino et al. reported \nthat pregnancies complicated by adenomyosis should \nbe managed at a tertiary facility due to its adverse effect \non perinatal outcomes, such as miscarriage, prema -\nture birth, and premature rupture of membranes [ 6]. In \naddition, adenomyosis requires due attention, as it may \nincrease the risk of placental malposition and preeclamp-\nsia [ 7]. A previous Japanese study of 314 patients with \nadenomyosis reported an association of the condition \nwith premature birth and low birth weight [ 8]. Similarly, \nShin et al. reported that adenomyosis was a risk factor for \npremature birth and low birth weight, emphasizing the \nTable 1 Patient characteristics\nVariable Adenomyosis\n (n = 1,204)\nNon-adenomyosis \n (n = 151,105)\nP-value\nAge (years) 35 32 0.02\nNumber of pregnancies P0 878 (72.9%) 86,455 (57.2%) < 0.01\nP1 or more 326 (27.1%) 64,651 (42.8%)\nART 349 (20.6%) 14,581 (9.6%) < 0.01\nType of delivery Spontaneous 588 (48.8%) 102,749 (67.9%) < 0.01\nInstrumental 148 (12.3%) 14,069 (9.3%)\nSelective Cesarean section 216 (18.0%) 21,708 (14.3%)\nEmergency Cesarean section 252 (20.9%) 12,552 (8.3%)\nGestational age at delivery (weeks) 22–36 193 (16.0%) 16,045 (10.6%) < 0.01\n37–41 1,007 (83.6%) 134,683 (89.1%)\n42+ 3 (0.2%) 284 (0.2%)\nUnknown 1 (0.08%) 91 (0.06%)\nMaternal morbidities PROM 67 (5.6%) 9,031(6.3%) < 0.01\nThreatened premature labor 233 (19.3%) 19,017 (12.5%) < 0.01\nUterine rupture 2 (0.2%) 27 (0.01%) 0.02\nPlacental abruption 19 (1.6%) 1,449 (0.9%) 0.02\nHDP 121 (10.0%) 9,884 (6.5%) < 0.01\nInfant morbidity FGR 64 (5.3%) 5,739 (3.8%) < 0.01\nInfant mortality 1 (0.1%) 11 (0.007%) NS\nAbbreviations: ART, assisted reproductive technology; PROM, premature rupture of membranes; HDP, Hypertensive disorders in pregnancy; FGR, fetal growth \nrestriction; NS, not significant\nTable 2 Frequencies of abnormal placenta\nAdenomyosis\n (n = 1,204)\nNon-adenomyosis\n (n = 151,105)\nP-value\nAbnormal placenta Total placenta previa 37 (3.7%) 888 (0.5%) < 0.01\nEdge placenta previa 16 (0.9%) 884 (0.5%) < 0.01\nPartialplacenta previa 11 (1.3%) 298 (0.1%) < 0.01\nLow placenta 31 (2.5%) 1,509 (0.9%) < 0.01\nPlacenta accreta 25 (2.0%) 822 (0.5%) < 0.01\n\nPage 4 of 7\nKomatsu et al. BMC Pregnancy and Childbirth           (2023) 23:579 \nFig. 2 Risk factors for uterine rupture. Aadenomyosis (OR: 3.45; 95% CI: 0.89–19.65; P = 0.02) was identified as an independent risk factor, in addition to \nART pregnancies (OR: 2.88; 95% CI: 1.30–5.97; P < 0.01), premature delivery (OR: 6.99; 95% CI: 3.36–14.32; P < 0.01), and uterine myomectomy (OR: 12.56; \n95% CI: 7.42–82.94; P < 0.01)\n \nFig. 1 Risk factors for placenta accreta. A multivariate analysis identified ART pregnancies (odds ratio (OR): 7.20; 95% confidence interval (CI): 6.26–8.28; \nP < 0.001), complication of adenomyosis (OR: 2.26; 95% CI: 1.43–3.27; P = 0.001), and history of uterine myomectomy (OR: 2.62; 95% CI: 1.5–4.22; P < 0.01) \nas independent risk factors for placenta accreta\n \n\nPage 5 of 7\nKomatsu et al. BMC Pregnancy and Childbirth           (2023) 23:579 \nimportance of ultrasound findings [ 9]. A previous study \non a large cohort reported that the presence of endome -\ntriosis and adenomyosis significantly increased the prev -\nalence of obstetrics complications, after adjusting for the \ninfluence of ART outcomes [4].\nFew studies investigated the association between \nadenomyosis and placental position. A Japanese study \nreported an increased frequency of perinatal complica -\ntions in cases where the placental formation was at the \nsite of the adenomyosis lesion [10]. In particular, placenta \nprevia was reported in 23.1% of endometriosis patients \nFig. 4 Risk factors for placental abruption. Adenomyosis was an independent risk factor for placental abruption (OR: 2.66; 95% CI: 2.00–3.48; P < 0.01)\n \nFig. 3 Risk factors for FGR. Adenomyosis was an independent risk factor for FGR (OR: 2.11; 95% CI: 1.27–3.31; P < 0.01)\n \n\nPage 6 of 7\nKomatsu et al. BMC Pregnancy and Childbirth           (2023) 23:579 \nwith severe adenomyosis [ 11]. In the present study, pla -\ncenta previa was found in 7.8% (95/1204) of the cases, \nand the frequency may be higher in those with severe \nadenomyosis.\nSeveral studies have examined the association between \nadenomyosis and uterine rupture. Vimercati et al. \nreported that adenomyosis diagnosed prior to pregnancy \nwas associated with the risk of uterine rupture during \ndelivery [12]. They stated that appropriate pre-pregnancy \ncounseling is important and that patients with adenomy -\nosis should be advised of the risk of uterine rupture. A \nnationwide survey in Japan on the incidence and progno -\nsis of uterine rupture reported that uterine rupture dur -\ning ongoing labor resulted in poor perinatal outcomes \nand particularly increased the frequency and risk of hys -\nterectomy and cerebral palsy in newborns [ 13]. However, \nthe frequency and risk of uterine rupture in these reports \nvary, as they may be affected by various environmen -\ntal factors, such as the method of delivery management \nand mode of delivery at each facility, as well as timing of \ndelivery.\nOur present, large-scale study showed that adenomy -\nosis increased the risk of uterine rupture as well as pla -\ncenta accreta and that the incidence of uterine rupture \nwas significantly higher in patients with adenomyosis \nthan in those without adenomyosis. Furthermore, adeno-\nmyosis in pregnancies increases the frequency of placen -\ntal abruption or FGR [ 4], and the present study, with far \nmore than 300 cases, shows that it is an independent risk \nfactor for both diseases.\nOn the other hand, although a previous Japanese study \nshowed that adenomyomectomy was a risk factor for \nuterine rupture, the present study did not evaluate the \npresence or absence of adenomyomectomy. There have \nbeen few reports on the course of pregnancy after ade -\nnomyomectomy, and the management of adenomyosis \nis complex [ 14, 15]. Therefore, well-designed studies are \nneeded in the future.\nIn recent years, there have been increasing number of \nreported adenomyomectomy cases. Zhou et al. reported \nthat the use of the double-flap method for diffuse adeno -\nmyosis improved the prognosis of pregnancy [ 16]. Osada \net al. and Nishida et al. have established their own sur -\ngical procedure for adenomyomectomy and reported a \nreduced risk of uterine rupture during pregnancy [17, 18]. \nA systematic review by Younes et al. stated that surgical \ntreatment for refractory adenomyosis leads to improve -\nment of symptoms and fertility. However, an optimal and \ndefinitive treatment has not been proposed, as there have \nbeen varying reports on pregnancy status after treatment \n[19]. The present study did not determine the effect of \nsurgery since the presence or absence of adenomyomec -\ntomy could not be properly evaluated. However, surgery \nfor adenomyosis likely increases the frequency and risk of \nperinatal complications, as is the case of myomectomy.\nThese findings suggest that adenomyosis increases \nthe risk of premature birth, low birth weight, placental \nmalposition, and uterine rupture. Therefore, pregnant \npatients with adenomyosis should be managed at an ade -\nquate perinatal facility.\nClinical implications\nIt is important to understand that adenomyosis can be \ndiagnosed only before conception or during early preg -\nnancy, and the myometrium needs to be carefully exam -\nined by ultrasonography if adenomyosis is detected in \nearly pregnancy. To our knowledge, there are no reports \nwith data on > 1000 patients with adenomyosis. It is \nimportant to conduct clinical trials in which transvaginal \nultrasonography and pelvic MRI are performed early in \npregnancy, and tumor markers such as CA125 are mea -\nsured, followed by evaluation of the pregnancy course.\nResearch Implications\nIn future, we plan to conduct studies with higher accu -\nracy, using multi-year databases, and to examine the \nperinatal outcomes of patients undergoing adenomyo -\nmectomy. With the social advancement of women and \nfurther popularization of infertility treatments, such as \nART, pregnancies may face a variety of increased peri -\nnatal risks in the future, and procedures such as uterine \nsurgery at a reproductive age should be performed with \ncaution. In particular, further study will be conducted on \nthe nature of infertility treatment, the number of ART \nprocedures performed, history of miscarriage surgery \nand adenomyosis incidence, and obstetric complications.\nStrengths and Limitations\nThis study has some limitations. First, the location of \nlesions was unknown (anterior, posterior, or diffuse dis -\ntribution), and details of severity were also unclear. As \nthe effect of adenomyosis on delivery may be dependent \non the location or extent of the lesion, further analyses \nare required. Second, the nature of relationship between \nplacental malposition and location of adenomyosis lesion \nwas unknown. If implantation occurs at an invasion site \nof the endometriosis lesion into the muscle layer, the \nrisk of developing placenta accreta may be increased. To \ninvestigate this in detail, further studies of adenomyosis \nlesions and placental position are needed.\nConclusions\nThe present study showed that pregnancies complicated \nby adenomyosis may be associated with an increased risk \nof developing placenta accreta, placental abruption, and \nFGR.\n\nPage 7 of 7\nKomatsu et al. BMC Pregnancy and Childbirth           (2023) 23:579 \nAbbreviations\nFGR  Fetus growth restriction\nJSOG  Japan Society of Obstetrics and Gynecology\nART  Assisted reproductive technology\nAcknowledgements\nWe would like to express our sincere gratitude to Editage for \nproviding　assistance in language correction and writing and for their \nproofreading services for this manuscript.\nAuthors’ contributions\nHK analyzed and interpreted the patient data. HK was a major contributor in \nwriting the manuscript. All authors read and approved the final manuscript.\nFunding\nThis research did not receive any specific grant from funding agencies in the \npublic, commercial, or not-for-profit sectors.\nData Availability\nAll data generated or analysed during this study are included in this published \narticle.\nDeclarations\nEthics approval and consent to participate\nThis study was approved by the Institutional Review Board of Tottori University \nHospital (IRB no. 21A244) and JSOG IRB committee (IRB no. 2021-17). All \npatients provided written informed consent following the institutional \nguidelines. All methods were carried out in accordance with relevant \nguidelines and regulations.\nConsent for publication\nNot applicable.\nCompeting interests\nThe authors declare no competing interests.\nReceived: 12 June 2023 / Accepted: 2 August 2023\nReferences\n1. Wendel MP , Magann EF. The impact of adenomyosis on pregnancy and \npregnancy outcomes: a review. 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J Minim Invasive Gynecol. 2018;25:265–76.\nPublisher’s Note\nSpringer Nature remains neutral with regard to jurisdictional claims in \npublished maps and institutional affiliations.","source_license":"CC0","license_restricted":false}