Long term follow-up of inguinal endometriosis

Background: Inguinal endometriosis (IEM) is a rare extra pelvic endometriosis. Here, we study the clinical characteris- tics, management strategies, and long-term gynecological outcomes of IEM patients at Beijing Chaoyang Hospital. Case presentation: Three patients presented with a total of four lesions (one on the left side, one on the right side, and one bilaterally). The diameters of the four lesions were 2 cm, 2 cm, 3.5 cm and 1.5 cm, respectively. Two patients were admitted with inguinal hernias. Two patients were admitted with endometrioses—one with ovarian endometri- osis and one with pelvic endometriosis. The hernia sac was repaired concomitantly via excision of the round ligament in two patients. One patient underwent a concomitant laparoscopy for gynecologic evaluations, including an ablation to the peritoneal endometriosis, and resection of the left uterosacral ligament endometriosis and pelvic adhesiolysis. All lesions were located on the extraperitoneal portion of the round ligament and were diagnosed histologically. No recurrence was observed in the inguinal region. All patients diagnosed with adenomyosis were treated with medica- tion alone without any complaints.

Inguinal endometriosis can occur simultaneously with pelvic endometriosis. In most cases, a concomi- tant hernia sac appears together with groin endometriosis. Clinical management should be individualized and per- formed in tandem with general practitioners and obstetrics & gynecology experts. Pelvic disease, in particular, should be followed-up by a gynecologist.

Endometriosis, Inguinal endometriosis, Hernia, Follow up, Gynecological results © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

As a rare extra pelvic endometriosis, Inguinal endome - triosis (IEM) has been reported in 0.3–0.6% of endome - triosis patients [1]. IEM is also a possible site of deep endometriosis [2]. As case reports of IEM increase, so does the inci - dence of IEM [3]. These studies outline the clinical characteristics and the optimal diagnostic and therapeu - tic strategies for treating IEM [4]. However, long term recovery and gynecological follow-up from IEM patients remains unknown for both gynecologists and general surgeons. Here, we review cases from 3 patients with IEM who were treated in our hospital. We are the first to report the gynecological results from long-term follow-ups in IEM patients. Case presentation We identified three patients who were admitted to our hospital between 2009 and 2014 with pathologi - cally proven IEM using data from stromal cells within the endometrial glands of the connective tissue in the Open Access *Correspondence: [email protected]; [email protected] 1 Department of Obstetrics and Gynecology, Beijing Chao-Yang Hospital Affiliated To Capital Medical University, 8 Gongtinanlu, ChaoYang District, Beijing 100020, People’s Republic of China 3 Department of Obstetrics and Gynecology, Peking Union Medical College (PUMC) Hospital, No. 1 Shuaifuyuan Wangfujing, Dongcheng District, Beijing 100730, People’s Republic of China Full list of author information is available at the end of the article Page 2 of 6Mu et al. BMC Women’s Health (2021) 21:90 inguinal lump (Fig. 1A and B). The clinical characteristics of these cases are summarized in Table  1. Institutional review board (IRB) approval was provided. The durations from complaint to diagnosis were 14 months, 6 years, 0.5 years, and 2 years, respectively, for each lesion. Cyclic discomfort in the inguinal region and concomitance with the menstrual period was reported in 2 patients, while 1 complained of dysmenorrhea. Two lesions were reported to change in size during strenu - ous events such as coughing. One patient previously underwent a right ovarian cystectomy to address endo - metriosis and infertility 15  months prior. Pre-operative magnetic resonance imaging (MRI) in 2 patients detected a solid, irregular lesion with a hypointense signal and small hemorrhagic foci with hyperintense signals using T1-weighted imaging in the right inguinal area (Fig.  2A, B). 2 patients consulted with a gynecologist and 1 patient was seen by a general surgeon initially. Pre-operative CA125 levels were normal in 1 patient, at 25.6U/ml, and elevated in another, at 78.48 (normal range, 0–35) U/ ml. 2 patients were tentatively diagnosed with inguinal (round ligament) endometriosis. We assessed 3 patients with a collective total of 4 lesions (1 patient had a lesion on the left side, 1 had a lesion on the right side, and one had bilateral lesions). The diameters of the lesions were 2  cm, 2  cm, 3.5 and 1.5  cm, respectively. 2 patients were diagnosed with inguinal hernias, 2 were diagnosed with endometriosis, one was diagnosed with ovarian endometriosis, and 1 was diagnosed with pelvic endometriosis. Two type III (Case1, left lesion of Case3) lesions adhered to the extra - peritoneal portion of the round ligament (Fig. 3A, B). Two patients underwent procedures to remove the lump and repair the hernia sac. One patient had a lapa - roscopic ovarian cystectomy in another hospital, and then underwent a procedure 15 months later to remove the lump and repair the hernia. One patient underwent laparoscopy for gynecologic evaluations, including a peritoneal endometriosis ablation, a left uterosacral liga - ment endometriosis resection and a pelvic adhesiolysis. The patient was discharged two days after the opera - tion. All lesions were diagnosed histologically (Fig.  4) as ER and PR positive in the glandular and stroma (Fig.  4), and CD10 positive in the stroma (Fig.  4). The patients received regular follow-up evaluations and no recurrent lesions were observed. All patients developed adenomyo - sis, which was treated medicinally and followed-up in our department.

Inguinal endometriosis, a rare form of extra-genital endometriosis, often coincides with pelvic endome - triosis. However, a concomitant hernia sac with groin endometriosis should also be considered in the context of inguinal endometriosis. Comprehensive evaluation of patient medical histories should be performed in tan - dem with imaging and individualized clinical manage - ment strategies for IEM patients. Patients who present with both pelvic and inguinal symptoms and are surgical candidates for both procedures should undergo both pro- cedures concomitantly through collaboration between both general surgery and gynecology. Follow-up evalua - tions should be specifically completed by a gynecologist to check for pelvic disease. Three clinical types of IEM are reported depending on the site of the lesion: type 1 lesions are located at a her - nia sac or hydrocele of Nuck’s canal, type II lesions are on the round ligament, and type III lesions are located under the skin [4]. Type III lesions have been associated Fig.1 Histopathological examination comprising an endometrial glandular structure lined by columnar epithelium, surrounded by endometrial-type stroma with dense fibrosis; (hematoxylin–eosin, original magnification: A ×100; B, ×200) Page 3 of 6 Mu et al. BMC Women’s Health (2021) 21:90 with the hernia sac, which is an observation that differs between studies [5, 6]. Two of the 3 patients and 2 of the 4 lesions in our report presented with concomitant her - nia sacs in the groin. Inguinal endometriosis often pre - sents concomitantly with hernia sacs in the groin region [7]. Understanding this characteristic could be helpful to effectively direct therapeutic strategies. Ultrasonography is the first-line diagnostic method for inguinal endometrioses and is used to identify con - comitant hernia sacs. However the presentation of ingui - nal endometriosis in ultrasound is variable, including solid masses, cystic masses, and combined cystic and solid masses [8]. MRI is particularly useful in diagnos - ing lesions in the extraperitoneal area, and can also be used to identify sub-peritoneal endometriotic deposits [9]. MRI scans of IEM have distinct characteristics [2], including hyperintense T1-weighted images of hemor - rhagic micro cysts that provide diagnostic clues for IEM [10]. Differential diagnoses of IEM include inguinal her - nia, hydrocele for cystic masses, sarcoma, lymphoma, hematoma, and abscesses for solid masses. Most IEM patients were initially admitted and treated by general surgeons with a false diagnosis of incarcerated hernia. Increased catamenial size and pain during menstrua - tion are hallmarks of an IEM diagnosis. The direct rela - tionship between symptoms and menstruation often successfully rule out other inguinal pathologies [11]. However, surgeons should be aware of the possibility of inguinal endometriosis in fertile women with a lump in the groin region [6 ]. Surgery involves en bloc radical excision of the lesion along with the extraperitoneal portion of the round lig - ament [12]. A careful gynecological assessment should be conducted during surgery given that intraperitoneal localization is observed in the majority of cases (91%) [13]. Minimally invasive surgery is the gold standard diagnostic technique for identifying endometriosis Table 1 Characteristics of three patients with inguinal endometriosis Case 1 Case 2 Case 3 Age at diagnosis 32 40 36 Gravidity and parity 2/1 0/0 3/0 Presenting symptoms Right inguinal mass with catamenial pain for 14mon Left inguinal incarcerated mass 2y Left inguinal mass with catamenial pain 6y and right inguinal incarcer- ated mass 0.5y History of surgery Appendectomy in 2004 Right ovarian cystectomy in March, 2011; Infertility Induced abortion 3 times; dysmenor- rhea Physical findings Tender 2 cm nodule Tender 2 cm nodule Tender 3 cm left inguinal mass, 1.5 cm right inguinal nodule; uterine leiomyoma MRI findings isointense and small scattered hyperintense both on T1- and T2-weighted images NA Left: hyperintense both on T1- and T2-weighted images Right: hypointense on T1- and T2-weighted images Type III I Left: III Right: I Tentative diagnosis Pelvic and inguinal endometriosis Incarcerated hernia Inguinal endometriosis Operative date 2014-2-14 2012-8-14 2011-11-28 Surgical diagnosis and treatment Endometriosis of right round liga- ment excision and pelvic endome- triosis ablation Left round ligament endometriosis excision; repaired the hernia; Bilateral round ligament endometrio- sis excision; Hernia sac was found in the right groin and was repaired Follow-up 70mon Adenomyosis; no recurrence 88mon Adenomyosis; no recurrence 96mon Adenomyosis; no recurrence Page 4 of 6Mu et al. BMC Women’s Health (2021) 21:90 [13– 16]. Laparoscopy allows for the direct visualization of implants and nodules and aids in excising implants, amplifying minimal lesions, obtaining tissue for diag - nosis and stage determination, and treating the disease appropriately. Hormonal treatment has been underreported as a therapeutic strategy for inguinal endometriosis [14]. It can be an option if the patient does not want to undergo surgery or does not want reoperation after recurrence, and it also could be indicated in patients with con - comitant pelvic endometriosis [17]. Arakawa et  al. [1 ] reported that Dienogest effectively managed pain in patients who did not want surgery or reoperation after disease recurrence. The expression of estrogen recep - tors and progesterone receptors furthers the basis for using hormonal therapies for inguinal endometriosis.

Long-term follow-up data regarding IEM is limited to a few patients, and operative charts are often missing. Due to its rarity, IEM often lacks thorough investigation. This study provides data from long term follow-ups with IEM patients and provides a deeper understanding of IEM treatment. Follow-up evaluations should continue to be completed by a gynecologist to monitor for intra- abdominal disease and to inform patients of its impact on fertility. Fig.2 The magnetic resonance imagining reveals an inguinal mass, isointense with muscle, which infiltrate the edge (arrow) of the abdominis rectus muscle, in Axial T1-weighted imagine (A). Axial T2-weighted image, obtained at the same level (B) Fig.3 The mass is freed from the adhesions with the internal oblique muscle and the transversalis fascia at the deep inguinal orifice. The inguinal segment of the round ligament was excised with the lesion (A). Multi-locular cysts containing dark hemorrhagic content was revealed by gross specimen (B) Page 5 of 6 Mu et al. BMC Women’s Health (2021) 21:90 Abbreviations IEM: Inguinal endometriosis; MRI: Magnetic resonance imaging; ER: Estrogen receptor; PR: Progesterone receptor.

Not applicable. Authors’ contributions MHL contributed to the design of the study, data collection and analysis, inter- pretation of the analyses, writing and revising the manuscript. JHL contributed to the analysis, writing, and revising of the manuscript. ZhQZh and BRM contributed substantially to the study’s conception and design, drafted the article, and revised the approved final version to be published. ChDL, KNZh and ShHL contributed to the design of the study and revising the manuscript. All authors approved the final version of the manuscript and agreed to be responsible for all aspects of the work. Funding This work was supported by funding from the National Key R&D Program of China Number: 2017YFC1001204. Availability of data and materials All data generated or analyzed during this study are included in this published article. Declarations Ethical approval and consent to participate This study protocol was approved by the Institutional Review Board (IRB) of Beijing Chao-Yang Hospital affiliated to Capital Medical University (IRB no. 2016-science-166). All patients received information on the purpose and procedures of this study, and provided written, informed consent. Fig.4 Focal endometriosis, which consisted of endometrial gland and stroma inside the tissue (H&E ×200) of case 1, 2, 3 respectively. ER and PR were positive in glandular and stroma, and CD10 was positive in stroma (× 200) Page 6 of 6Mu et al. BMC Women’s Health (2021) 21:90 • fast, convenient online submission • thorough peer review by experienced researchers in your field • rapid publication on acceptance • support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year • At BMC, research is always in progress. Learn more biomedcentral.com/submissions Ready to submit y our researc hReady to submit y our researc h ? Choose BMC and benefit fr om: ? Choose BMC and benefit fr om: Consent for publication Written informed consent was acquired from each patient for this publica- tion using a BMC consent form and is available for review by the editor of this journal. Competing interests The author(s) declared no potential conflicts of interest with the research, authorship, and/or publication of this article. Author details 1 Department of Obstetrics and Gynecology, Beijing Chao-Yang Hospital Affiliated To Capital Medical University, 8 Gongtinanlu, ChaoYang District, Beijing 100020, People’s Republic of China. 2 Department of Pathology, Beijing Chao-Yang Hospital Affiliated to Capital Medical University, 8 Gongtinanlu, ChaoYang District, Beijing 100020, People’s Republic of China. 3 Department of Obstetrics and Gynecology, Peking Union Medical College (PUMC) Hospital, No. 1 Shuaifuyuan Wangfujing, Dongcheng District, Beijing 100730, People’s Republic of China. Received: 10 September 2020 Accepted: 22 February 2021

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