Cesarean scar endometriosis: presentation of 198 cases and literature review

Background: Cesarean scar endometriosis (CSE) is the most common type of abdominal wall endometriosis (AWE). The aim of this study was to systematically identify the clinical features of CSE and recommend precautionary measures.

A large, retrospective study was undertaken with CSE patients treated surgically at our hospital between January 2005 and December 2017.

A total of 198 CSE patients were enrolled, with a mean age of 32.0 ± 4.0 years. The main complaint of the patients was abdominal mass (98.5%), followed by cyclic pain (86.9%). The latency period of CSE was 31.6 ± 23.9 months, and the duration between the onset of symptoms and this surgery was 28.3 ± 25.0 months. A majority (80.8%,n = 160) of the patients had undergone a Pfannenstiel incision, and a minority (19.2%,n = 38) a vertical midline incision. The latency period of CSE in the case of a Pfannenstiel incision was significantly shorter than that in thec a s eo fav e r t i c a lm i d l i n e incision (24.0 vs 33.0 months,P = 0.006). A total of 187 (94.4%) patients had a single endometrioma, 11 (5.6%) patients had multiple endometriomas, and the 11 multiple-endometrioma patients had all undergone a Pfannenstiel incision. Lesions of endometrioma were common in corner sites, after either incision: 142/171 (83.0%) in Pfannenstiel incision scars and 32/38 (84.2%) in vertical incision scars. Conclusions:The findings of this study indicate that the Pfannenstiel incision carries a higher risk of CSE than the vertical midline incision. Thorough cleaning at the conclusion of CS, particularly of both corner sites of the adipose layer and the fascia layer, is strongly recommended for CSE prevention. Further studies might provide additional recommendations.

Cesarean scar endometriosis, Abdominal wall endometriosis, Cesarean section, Pfannenstiel incision

Endometriosis is a sex hormone-dependent gynecological disease that is characterized by the growth of endometrial tissue outside the uterine cavity [ 1]. It usually occurs in the pelvis, at sites such as the ovaries and the pelvic peri- toneum. However, ectopic endometrial tissue can also be found outside the pelvis, at sites such as the lung, brain, bowel, and abdominal wall [ 2–4]. The presence of ectopic endometrial tissue embedded in the subcutaneous adipose layer and the muscles of the abdominal wall is called ab- dominal wall endometriosis (AWE). AWE can occur spontaneously, but usually develops in association with a previous surgical procedure, such as a cesarean section (CS), hysterectomy, or appendectomy [5–7]. Cesarean scar endometriosis (CSE) is the most com- monly reported type of AWE [ 8]. Nominato et al. sug- gested that CS greatly increased the risk of developing AWE [9]. The pathophysiology of CSE may be due to the direct implantation of endometrial tissue in the cesarean incision (the implantation theory) [8]. During cesarean de- livery, the endometrial tissue is inoculated directly in the cesarean incision. With an appropriate supply of nutrients and hormonal stimuli, these endometrial cells survive and proliferate, which finally leads to CSE. Although it is an unusual disease, with a reported incidence of 0.03 –0.45%, CSE may cause long-term discomfort involving cyclic lower abdominal pain [ 10, 11]. Case reports of malignant transformation of CSE have also been sporadically re- ported [12–14]. * Correspondence: [email protected]; [email protected] †Ping Zhang and Yabing Sun contributed equally to this work. 2Department of Assisted Reproduction, Shanghai Ninth People ’s Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200011, China 1The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200030, China © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. BMC Women's Health (2019) 19:14 https://doi.org/10.1186/s12905-019-0711-8 Generally, few publications have focused on CSE, and a majority of them are either case series or case reports [15–18]. As a large obstetric and gynecologic hospital, we have treated many CSE patients and were very interested in identifying the characteristics associated with CSE. Here, we report our findings in managing CSE over ap- proximately the last decade, and we discuss the clinical features and prevention strategies of this rare disease.

This retrospective study was conducted in the Depart- ment of Obstetrics and Gynecology of the International Peace Maternity and Child Health Hospital (IPMCH). The study was approved by the ethical review committee of the IPMCH. This study included patients diagnosed with CSE who received surgical treatment at IPMCH between January 2005 and December 2017. The inclusion criteria were the following: (1) patient had a history of at least one CS and the symptoms occurred after the cesarean delivery; (2) surgical excision with surrounding clear margins was performed; and (3) pathological diagnosis for each ex- cised lesion was endometriosis. The baseline characteristics and surgical processes of all of the patients were recorded in the database of our hospital. We conducted a computerized search of the database according to the disease name. The preliminar- ily selected items were further checked and screened ar- tificially following the inclusion criteria. The main symptoms of CSE included a palpable mass, under or away from the scar, with cyclic pain and swelling during menstruation. The latency period was defined as the time between CS and the onset of symptoms. The following in- formation was extracted: age, age at CS, parity, delivery history, incision type, symptoms, size of the mass, latency period, duration between symptoms and surgery, opera- tive findings, and histopathological evaluations. The normality of continuous variables was tested using the Shapiro –Wilk test. The comparisons of normally distributed, continuous data were made with the Student t test and an analysis of variance. Two sets of nonnor- mally distributed, continuous data were analyzed with Mann–Whitney U tests; otherwise, Kruskal –Wallis H tests were employed. The categorical data were analyzed with χ2 and Fisher exact tests. The differences were con- sidered statistically significant when the P-value was less than 0.05. Statistical analysis was performed using SPSS version 17.0 (SPSS Inc., Chicago, IL, USA).

Following the inclusion standards described above, a total of 198 CSE cases were ultimately enrolled and all the cases were pathologically confirmed. Baseline char- acteristics of the patients are summarized in Table 1. The mean age of the patients was 32.0 ± 4.0 years, and the mean age at the time of CS was 27.1 ± 3.5 years. Par- ity of the patients ranged from 1 to 2. All of the patients had a history of CS: 186 (93.9%) patients had 1 CS, and 12 (6.1%) had 2. The latency period of CSE ranged from 1 to 120 months, with a mean of 31.6 ± 23.9 months. The duration between the onset of symptoms and sur- gery was 28.3 ± 25.0 months. Symptoms and CSE sites of the study patients are also shown in Table 1. The most common symptom of the patients was a palpable painful abdominal mass under or Table 1 Baseline characteristics, symptoms, and CSE sites of the patientsa Characteristic n (%) Mean ± SD (range) Age of the patients (years) 32.0 ± 4.0 (21 –43) Age at CS (years) 27.1 ± 3.5 (19 –37) Parity 1 175 (88.4) 2 23 (11.6) No. of CSs 1 186 (93.9) 2 12 (6.1) Latency period (months) 31.6 ± 23.9 (1 –120) Duration between symptoms and surgery (months) 28.3 ± 25.0 (1–180) Symptoms Abdominal mass 195 (98.5) Cyclic pain 172 (86.9) Noncyclic pain 26 (13.1) Dysmenorrhea 64 (32.3) Incision type Pfannenstiel 160 (80.8) Vertical midline 38 (19.2) No. of endometriomas Single 187 (94.4) Multiple 11 (5.6) Endometrioma location Pfannenstiel incision No. of endometriomas 171 (81.8) Left corner 65 (38.0) Middle 29 (17.0) Right corner 77 (45.0) Vertical midline incision No. of endometriomas 38 (18.2) Upper corner 15 (39.5) Middle 6 (15.8) Lower corner 17 (44.7) aValues are given as mean ± SD or as number (percentage) Zhang et al. BMC Women's Health (2019) 19:14 Page 2 of 6 adjacent to the incision, accompanied with either cyclic pain (86.9%, n = 172) or noncyclic pain (13.1%, n =2 6 ) . A majority (80.8%, n = 160) of the patients had undergone a Pfannenstiel incision, and a minority (19.2%, n =3 8 )av e r - tical midline incision. In the group of 198 study patients, 187 (94.4%) patients had a single endometrioma and 11 (5.6%) patients had multiple endometriomas. The 11 multiple-endometrioma patients had all undergone a Pfannenstiel incision. In total, 209 abdominal wall endo- metriomas were excised. Specifically, 171 and 38 endome- triomas were excised from Pfannenstiel incision and vertical midline incision scars, respectively. A majority of the endometriomas were located in corner sites, after either incision: 142/171 (83.0%) in Pfannenstiel incision scars and 32/38 (84.2%) in vertical incision scars. We introduced an “upper bound ” and a “lower bound ” to describe the locations of the endometriomas for the first time. The abdominal wall was divided into the adi- pose layer, the fascia layer, the muscular layer, and the peritoneal layer. The bladder was considered the deepest layer involved. As shown in Tables 2, 64.6% ( n = 135) of the endometriomas were located between the adipose layer and the fascia layer; 14.8% ( n = 31) were located be- tween the adipose layer and the muscular layer. Of the 209 endometriomas, 16 (7.7%) invaded the peritoneum; 1 (0.5%) invaded into the abdominal cavity; and 2 (1.0%) invaded the bladder. To identify the risk factors for CSE, we calculated the difference in latency period based on the patients ’ baseline characteristics (T able 3). Age at CS, parity, previous CS, and dysmenorrhea showed no significant correlation with the latency period. Location of the endometriomas, such as under or away from the scar, or in the corner or in the middle of the scar, also showed no correlation with the la- tency period. However, the latency period showed signifi- cant correlation with the incision type, i.e., the latency period of the CSE in patients with Pfannenstiel incision was significantly shorter than that in patients with vertical midline incision (24.0 vs 33.0 months, P =0 . 0 0 6 ) . T h e l o - cation of the lower bound of the endometriomas also showed a correlation with the latency period ( P =0 . 0 1 1 ) , i.e., the latency period was longer when the endometrio- mas invaded down to the peritoneum or the bladder. To confirm the difference in latency period based on inci- sion type, baseline character istics of the patients with Pfannenstiel incisions or vertical midline incisions were fur- ther compared. As shown in Table 4, no significant differ- ence was identified in the patients’ baseline characteristics.

CSE is an uncommon iatrogenic disease caused by endo- metrium implantation in the incision during cesarean delivery. In the present study, we investigate 198 cases of CSE over a period of 13 years, providing detailed in- formation that helps us to better understand the clinical characteristics of this rare condition. Several theories about the pathogenesis of AWE have been proposed, such as the implantation theory, the coelomic metaplasia theory, and the lymphatic or hema- togenic dissemination theory [ 8, 19]. As the most com- mon type of AWE, CSE is best explained by the iatrogenic direct implantation theory. During cesarean delivery, endometrial tissue is seeded into the wound. With an appropriate supply of nutrients and hormonal stimuli, these endometrial cells survive and proliferate, finally leading to CSE. In the present study, most of the endometriomas were located in a corner of the incision scar: 83.0% in Pfannenstiel incision scars and 84.2% in vertical midline incision scars. In another large retro- spective study, conducted by Yan Ding et al., similar re- sults were obtained [ 20]. In their study, 77.1% of the endometriomas were located in the corners of the scars. This is probably because endometrial cells are less easily removed from the corners of the incisions during CS. Thus, our data also support the iatrogenic cell implant- ation theory. However, the implantation theory alone cannot completely explain the pathogenesis of CSE, given the low incidence of CSE. Residual endometrial cell contamination of the wound during CS occurs often and sometimes is inevitable, but CSE is rare. Hereditary predisposition may confer susceptibility to the develop- ment of CSE [ 21]. CS is one of the most common surgical procedures performed on women worldwide. Pfannenstiel incision and vertical midline incision are the two most frequently used abdominal skin incisions. The vertical midline inci- sion has the advantages of speed of abdominal entry and less bleeding, but has a higher risk of incisional hernia and results in a less cosmetically pleasing scar. Con- versely, the Pfannenstiel incision has a lower risk of Table 2 Location of the endometriomas in the abdominal wall Lower bound AL, n (%) FL, n (%) ML, n (%) PL, n (%) AC, n (%) B, n (%) Upper bound AL 12 (5.7) 135 (64.6) 31 (14.8) 11 (5.3) 1 (0.5) 1 (0.5) FL / 0 (0) 12 (5.7) 3 (1.4) 0 (0) 0 (0) ML / / 0 (0) 2 (1.0) 0 (0) 1 (0.5) AL = adipose layer, FL = fascia layer, ML = muscular layer, P = peritoneum layer, AC = abdominal cavity, B = bladder Zhang et al. BMC Women's Health (2019) 19:14 Page 3 of 6 incisional hernia and results in a better cosmetic appeal. However, the Pfannenstiel incision usually involves more dissections, and the blood loss following dissection may be greater [ 22]. CSE is a complication of cesarean surgery. Unfortu- nately, the relationship between the CS incision type and the pathogenesis of CSE is still unknown. The Pfannenstiel incision is the most commonly reported type for the oc- currence of CSE; however, because of the disease rarity and the need for the pathological confirmation of the diagnosis, it is difficult to estimate the population-wide in- cidence of CSE for different incision types [ 19, 20]. Demiral et al. speculated that Pfannenstiel incisions confer a higher risk of CSE than do midline incisions, but Table 3 Difference in latency period based on patients ’ baseline characteristics, symptoms, and CSE sites a Characteristic n (%) Latency period (months) P-value Median (quartiles) Age at CS (years) 0.941 ≥ 35 6 (3.0) 30.0 (10.5 –48.0) 25–34 143 (72.2) 24.0 (12.0 –40.0) ≤ 24 49 (24.8) 24.0 (12.0 –48.0) Parity 0.273 Nulliparous 178 (89.2) 24.0 (12.0 –36.0) Multiparous 20 (10.1) 21.0 (6.0 –48.0) One previous CS 0.452 Yes 21 (10.6) 24.0 (6.0 –48.0) No 177 (89.4) 24.0 (12.0 –36.0) Dysmenorrhea 0.473 Yes 64 (32.3) 19.0 (12.0 –36.0) No 134 (67.7) 24.0 (12.0 –36.0) Incision type 0.006 Pfannenstiel 160 (80.8) 24.0 (12.0 –36.0) Vertical midline 38 (19.2) 33.0 (24.0 –60.0) No. of endometriomas 0.078 Single 187 (94.4) 24.0 (12.0 –48.0) Multiple 11 (5.6) 16.0 (12.0 –24.0) Location of the endometriomas I 0.253 Under the scar 111 (56.1) 24.0 (12.0 –36.0) Away from the scar 87 (43.9) 24.0 (12.0 –48.0) Location of the endometriomas II 0.153 Corner of the scar 167 (84.3) 24.0 (12.0 –48.0) Middle of the scar 31 (15.7) 30.0 (24.0 –38.0) Upper bound of the endometriomas 0.073 Adipose layer 181 (91.4) 24.0 (12.0 –39.0) Fascia layer 14 (7.1) 24.0 (18.0 –49.5) Muscular layer 3 (1.5) 48.0 (48.0 –56.0) Lower bound of the endometriomas 0.011 Adipose layer 10 (5.1) 27.0 (18.0 –39.0) Fascia layer 130 (65.7) 24.0 (12.0 –36.0) Muscular layer 41 (20.7) 24.0 (16.0 –48.0) Peritoneum 12 (6.1) 48.0 (27.0 –60.0) Abdominal cavity 3 (1.5) 30.0 (9.0–30.0) Bladder 2 (1.0) 40.0 (24.0–40.0) aMann–Whitney U test for comparing two sets; Kruskal –Wallis H test for comparing multiple sets Zhang et al. BMC Women's Health (2019) 19:14 Page 4 of 6 without sufficient evidence [ 23]. In this study, the latency period of CSE was 31.6 ± 23.9 months, which was compar- able with that reported in other studies [ 19, 24]. However, when comparing the latency period of CSE in patients with Pfannenstiel incisions to those with vertical midline incisions, we observed a significantly shorter latency in Pfannenstiel incisions (24.0 vs 33.0 months, P =0 . 0 0 6 ) (T able3). In other words, CSE in patients with Pfannen- stiel incisions occurred earlier than in patients with verti- cal incisions. This indicates that, compared to the vertical incision, the Pfannenstiel incision might be more favorable to the implantation and proliferation of the residual endometrial cells. We suggest two possible causes for the favorable role of the Pfannenstiel incision. First, the Pfan- nenstiel incision involves wider dissection planes and more gaps, rendering tissue irrigation difficult and indu- cing much more endometrial cell contamination [ 22]. The second cause is a larger nutrient supply. Due to the longi- tudinal pattern of the abdominal vessels and the large dis- section, more capillaries are cut off during a Pfannenstiel incision than in a vertical incision, causing more blood loss. Endometrial cells require an adequate blood supply to survive in their ectopic sites, and angiogenesis plays an important role in the pathogenesis of endometriosis [ 25]. Therefore, more blood loss in the Pfannenstiel incision would provide a relatively rich nutritional environment for the implantation and growth of residual endometrial cells, favoring the occurrence of CSE. Consistent with this explanation, all 11 patients in this study who had multiple endometriomas had Pfannenstiel incisions. These research findings demonstrate that the Pfannenstiel incision prob- ably carries a higher risk of CSE than the vertical midline incision. Another interesting result from this study is that deeper endometrioma locations are correlated with longer latency periods. This is probably due to the fact that the deeper endometriomas could not be easily noticed. Although CSE is a rare event, it manifests as a painful subcutaneous mass and usually bothers the patient for several years. Additionally, CSE can undergo malignant change, which is rapidly fatal and has a survival rate of only 57% [ 14]. Hence, it is necessary to take precautions to prevent or reduce the occurrence of CSE. On the basis of the implantation theory, we propose a variety of measures: careful flushing and irrigating before closure; using separate needles for uterine and abdominal clos- ure; and not using a sponge to clean the endometrial cavity following complete delivery. Extending the breast- feeding period to delay menstruation has also been pro- posed for preventing CSE, but without scientific corroboration [ 21]. In our study, 83.3% (174/209) of the scar endometriomas were located in corner sites of the wound. Therefore, the abdominal wound should be cleaned thoroughly with saline solution before closure, especially the corner sites. Additionally, endometriomas were more common in superficial parts of the abdominal wall, i.e., 12/209 (5.7%) were present in the adipose layer and 135/209 (64.6%) between the adipose layer and the fascia layer, accounting for 70.3% of the total endome- triomas. Therefore, careful flushing and irrigation of the adipose layer and fascia layer during closure is critical. All of the patients in our study underwent surgical ex- cision for the treatment of CSE. Generally, surgical treat- ment offers the best chance for both making a definitive diagnosis and treating CSE. Medical therapy has a low success rate is associated with adverse effects. As a retrospective study, some limitations in this study could not be avoided. For example, the data about the CS procedures lacked details such as the layers of clos- ure, type of suture materials, and operation duration. These factors might also affect the occurrence of CSE. To address these questions, further studies will be re- quired in the future.

Concerning the rising CS rate, CSE may occur more fre- quently than generally assumed. Early diagnosis, treat- ment, and prevention of CSE are worthy of our attention. In our large, retrospective study, we systemat- ically reviewed the clinical features of CSE and we pro- vide the first evidence that the Pfannenstiel incision carries a higher risk of CSE than the vertical midline in- cision. The findings in this study will help us to better understand CSE and devise precautionary measures to reduce the occurrence of the disease. Abbreviations AWE: Abdominal wall endometriosis; CS: Cesarean section; CSE: Cesarean scar endometriosis Table 4 Comparison of the baseline characteristics between patients with Pfannenstiel incision or vertical midline incision a Characteristic Pfannenstiel Vertical midline P-value n (%) n (%) Age at CS (years) 0.334 ≥ 35 4 (2.5) 2 (5.2) 25–34 119 (74.4) 24 (63.2) ≤ 24 37 (23.1) 12 (31.6) Parity 0.195 Nulliparous 146 (73.7) 32 (16.2) Multiparous 14 (7.1) 6 (3.0) One previous CS 0.248 Yes 15 (7.6) 6 (3.0) No 145 (73.2) 32 (16.2) Dysmenorrhea 0.782 Yes 51 (25.8) 13 (6.6) No 109 (55.1) 25 (12.6) aFisher exact test Zhang et al. BMC Women's Health (2019) 19:14 Page 5 of 6 Funding This study was supported by the Natural Science Foundation of Shanghai City, China (No. 15ZR1444100; No. 16ZR1419500; and No. 17411972800). The funding agency had no influence on the design of the study; the collection, analysis, and interpretation of data; and the writing of the manuscript. Availability of data and materials The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. Authors’ contributions PZ proposed the study concept and design, assisted by HX. YBS, YPY, and LNZ acquired and checked the data. CZ and NLW carried out the data analyses. PZ drafted the manuscript. All of the authors approved the final version of the manuscript. Ethics approval and consent to participate The study was approved by the ethical review committee of the International Peace Maternity and Child Health Hospital (IPMCH). Consent for publication Consent was obtained from the patients for the publication of this report. Competing interests The author declares that they have no competing interests. Publisher’sN o t e Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Received: 27 June 2018 Accepted: 3 January 2019

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