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Endometriosis and Adenomyosis Research: Recent Advances and Future Directions

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A special issue of International Journal of Environmental Research and Public Health (ISSN 1660-4601). This special issue belongs to the section "Women's Health".

Deadline for manuscript submissions: closed (10 April 2022) | Viewed by 58397

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Special Issue Editors

Dr. Maria Grazia Porpora

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Leading Guest Editor

Department of Maternal Infantile and Urological Sciences, Policlinico Umberto I, Sapienza University of Rome, 00161 Rome, Italy
Interests: adenomyosis; endometriosis; effects of environmental factors on women’s health infertility; minimally invasive gynecologic surgery; pelvic pain

Prof. Dr. Giuseppe Benagiano

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Guest Editor

Department of Maternal and Child Health, Gynaecology and Urology, Sapienza, University of Rome, Rome, Italy
Interests: reproductive endocrinology; adenomyosis; contraception; endometriosis; placental bed
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Maria Elisabetta Coccia

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Guest Editor

Department of Biomedical, Experimental and Clinical Sciences ‘Mario Serio’, University of Florence, 50121 Florence, Italy
Interests: human reproduction; endometriosis; endoscopy; ultrasound

Dr. Ludovica Imperiale

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Guest Editor

Department of Gynecology and Obstetrics, Erasme Hospital, ULB - Université libre de Bruxelles, 1050 Brussels, Belgium
Interests: endometriosis; adenomyosis; pelvic pain; minimally invasive gynecologic surgery; infertility; ultrasound

Special Issue Information

Dear Colleagues,

Endometriosis affects about 10% of reproductive-aged women; it is often associated with pain symptoms (dysmenorrhea, deep dyspareunia, non-menstrual pelvic pain, and dyschezia) and/or infertility. It significantly impairs women’s quality of life, work efficiency, and sexual life. In adolescents, symptoms may differ from those of older women, often causing a delay in diagnosis. Although research has improved our knowledge of the disease, several aspects remain to be fully understood.

Adenomyosis is a condition characterized by the presence of endometrial glands within the myometrium. Patients often complain of dysmenorrhea, abnormal bleeding, and pelvic pain. Recent studies have confirmed its presence also in young women who may present different symptoms.

Imaging techniques may improve diagnostic accuracy in both conditions, and they should allow pretreatment staging, thus helping in the choice of correct treatment decisions. Hormonal therapies have been widely used in the treatment of endometriosis and adenomyosis; however, these therapies are not curative, and after discontinuation, symptoms often recur. Non-hormonal therapies have also been proposed. Minimally invasive surgical techniques can be effective, particularly if associated with medical therapy, but the disease frequently recurs. Comorbidities may influence symptoms, so a multidisciplinary approach is essential to improve the results. Pregnancy and breastfeeding may interfere positively with the course of endometriosis, although endometriosis may increase the risk of some obstetrical complications.

The aim of this Special Issue is to describe the current state of research on endometriosis and adenomyosis, including future perspectives. Contributions from Obstetricians and Gynecologists as well as other medical specialists and professionals with research articles, reviews, short communications, and case reports are welcome.

Prof. Dr. Maria Grazia Porpora
Prof. Dr. Giuseppe Benagiano
Prof. Dr. Maria Elisabetta Coccia
Dr. Ludovica Imperiale
Guest Editors

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Keywords

endometriosis
adenomyosis
pelvic pain
infertility
pathogenesis
diagnosis
management
pregnancy
research
quality of life

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Published Papers (10 papers)

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Research

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18 pages, 1391 KiB

Open AccessArticle

Endometriosis and Infertility: A Long-Life Approach to Preserve Reproductive Integrity

by Maria Elisabetta Coccia, Luca Nardone and Francesca Rizzello

Int. J. Environ. Res. Public Health 2022, 19(10), 6162; https://doi.org/10.3390/ijerph19106162 - 19 May 2022

Cited by 23 | Viewed by 6497

Abstract

Laparoscopic surgery was originally considered the gold standard in the treatment of endometriosis-related infertility. Assisted reproductive technology (ART) was indicated as second-line treatment or in the case of male factor. The combined approach of surgery followed by ART proved to offer higher chances of pregnancy in infertile women with endometriosis. However, it was highlighted how pelvic surgery for endometriosis, especially in cases of ovarian endometriomas, could cause iatrogenic damage due to ovarian reserve loss, adhesion formation (scarring), and ischemic damage. Furthermore, in the last few years, the trend to delay the first childbirth, recent technological advances in ultrasound diagnosis, and technological progress in clinical and laboratory aspects of ART have certainly influenced the approach to infertility and endometriosis with, ART assuming a more relevant role. Management of endometriosis should take into account that the disease is chronic and involves the reproductive system. Consequently, treatment and counselling should aim to preserve the chances of pregnancy for the patient, even if it is not associated with infertility. This review will analyse the evolution of the management of infertility associated with endometriosis and propose an algorithm for treatment decision-making based on the most recent acquisitions. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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11 pages, 1970 KiB

Open AccessArticle

Challenges in Diagnosis and Prevention of Iatrogenic Endometriosis as a Long-Term Surgical Complication after C-Section

by Radu Neamtu, George Dahma, Adelina Geanina Mocanu, Elena Bernad, Carmen-Ioana Silaghi, Lavinia Stelea, Cosmin Citu, Amadeus Dobrescu, Felix Bratosin, Mirela Loredana Grigoras, Andrei Motoc, Sorin Dema, Marius Craina, Veronica Daniela Chiriac and Adrian Gluhovschi

Int. J. Environ. Res. Public Health 2022, 19(5), 2791; https://doi.org/10.3390/ijerph19052791 - 27 Feb 2022

Cited by 3 | Viewed by 2902

Abstract

Endometriosis is a gynecological condition caused by the development of endometrial tissue outside the uterine cavity. Naturally, it commonly occurs at locations such as the ovaries and pelvic peritoneum. However, ectopic endometrial tissue may be discovered outside of the typical sites, suggesting the possibility of iatrogenic seeding after gynecological operations. Based on this hypothesis, we developed a study aiming to establish the root cause of atypical implantation of endometrial foci, as the main end point, and to determine diagnostic features and risk factors for this condition, as a secondary target. The research followed a retrospective design, including a total of 126 patients with endometriosis who met the inclusion criteria. A group of 71 patients with a history of c-section was compared with a control group of patients with endometriosis and no history of c-section. Endometriosis that developed inside or in close proximity to surgical incisions of asymptomatic patients before surgical intervention was defined as iatrogenic endometriosis. Compared with patients who did not have a c-section, the c-section group had significantly more minimally invasive pelvic procedures and multiple adhesions and endometriosis foci at intraoperative look (52.1% vs. 34.5%, respectively 52.1% vs. 29.1%). The most common location for endometriosis lesions in patients with prior c-section was the abdominal wall (42.2% vs. 5.4%), although the size of foci was significantly smaller by size and weight (32.2 mm vs. 34.8 mm, respectively 48.6 g vs. 53.1 g). The abdominal wall endometriosis was significantly associated with minimally invasive pelvic procedures (correlation coefficient = 0.469, p-value = 0.001) and c-section (correlation coefficient = 0.523, p-value = 0.001). A multivariate regression analysis identified prior c-section as an independent risk factor for abdominal wall endometriosis (OR = 1.85, p-value < 0.001). We advocate for strict protocols to be implemented and followed during c-section and minimally invasive procedures involving the pelvic region to ensure minimum spillage of endometrial cells. Further research should be developed to determine the method of abdominal and surgical site irrigation that can significantly reduce the risk of implantation of viable endometrial cells. Understanding all details of iatrogenic endometriosis will lead to the development of non-invasive disease diagnosis and minimally invasive procedures that have the potential to reduce postoperative complications. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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12 pages, 1398 KiB

Open AccessArticle

Effects of Breastfeeding on Endometriosis-Related Pain: A Prospective Observational Study

by Romana Prosperi Porta, Chiara Sangiuliano, Alessandra Cavalli, Laila Cristine Hirose Marques Pereira, Luisa Masciullo, Ilaria Piacenti, Sara Scaramuzzino, Maria Federica Viscardi and Maria Grazia Porpora

Int. J. Environ. Res. Public Health 2021, 18(20), 10602; https://doi.org/10.3390/ijerph182010602 - 10 Oct 2021

Cited by 7 | Viewed by 4077

Abstract

Endometriosis is a gynecological estrogen-dependent disease whose commonest pain symptoms are dysmenorrhea, dyspareunia, and acyclic chronic pelvic pain (CPP). Hormonal changes occurring during breastfeeding seem to reduce pain and disease recurrence. The aim of this observational prospective study was to assess the effect of breastfeeding on pain and endometriotic lesions in patients with endometriosis and to evaluate a possible correlation between the duration of breastfeeding, postpartum amenorrhea, and pain. Out of 156 pregnant women with endometriosis enrolled, 123 who breastfed were included in the study and were monitored for 2 years after delivery; 96/123 exclusively breastfed for at least 1 month. Mode of delivery, type and duration of breastfeeding, intensity of pain symptoms, and lesion size before pregnancy and during the 24-month follow-up were analyzed. All patients experienced a significant reduction in dysmenorrhea proportional to the duration of breastfeeding. CPP was significantly reduced only in women who exclusively breastfed. No significant improvement in dyspareunia was observed. Ovarian endometriomas were significantly reduced. Therefore, breastfeeding, particularly if exclusive, may cause improvement in dysmenorrhea and CPP proportional to the duration of breastfeeding, as well as a reduction in the size of ovarian endometriomas. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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10 pages, 1611 KiB

Open AccessArticle

Can New ENZIAN Score 2020 Represent a Staging System Improving MRI Structured Report?

by Lucia Manganaro, Veronica Celli, Miriam Dolciami, Roberta Ninkova, Giada Ercolani, Sandra Ciulla, Corrado De Vito, Stefania Maria Rizzo, Maria Grazia Porpora and Carlo Catalano

Int. J. Environ. Res. Public Health 2021, 18(19), 9949; https://doi.org/10.3390/ijerph18199949 - 22 Sep 2021

Cited by 16 | Viewed by 3108

Abstract

Structured reporting systems for endometriotic disease are gaining a central role in diagnostic imaging: our aim is to evaluate applicability and the feasibility of the recent ENZIAN score (2020) assessed by MRI. A total of 60 patients with suspected tubo–ovarian/deep endometriosis were retrospectively included in our study according to the following criteria: availability of MR examination; histopathological results from laparoscopic or surgical treatment; patients were not assuming estro-progestin or progestin therapy. Three different readers (radiologists with 2-, 5-, and 20-years of experience in pelvic imaging) have separately assigned a score according to the ENZIAN score (revised 2020) for all lesions detected by magnetic resonance imaging (MRI). Our study showed a high interobserver agreement and feasibility of the recent ENZIAN score applied to MRI; on the other hand, our experience highlighted some limitations mainly due to MRI’s inability to assess tubal patency and mobility, as required by the recent score (2020). In view of the limitations which arose from our study, we propose a modified MRI-ENZIAN score that provides a complete structured reporting system, more suitable for MRI. The high interobserver agreement of the recent ENZIAN score applied to MRI confirms its validity as a complete staging system for endometriosis, offering a shared language between radiologists and surgeons. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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8 pages, 1903 KiB

Open AccessArticle

Epidemiology of Endometriosis in Spain and Its Autonomous Communities: A Large, Nationwide Study

by Almudena Ávalos Marfil, Enriqueta Barranco Castillo, Raúl Martos García, Nicolás Mendoza Ladrón de Guevara and Maryna Mazheika

Int. J. Environ. Res. Public Health 2021, 18(15), 7861; https://doi.org/10.3390/ijerph18157861 - 25 Jul 2021

Cited by 11 | Viewed by 4198

Abstract

A retrospective population-based study aimed to assess the incidence of endometriosis in the general population in Spain and in each of its autonomous communities. The authors used the incidence of diagnosed endometriosis in the minimum basic dataset at discharge in the national hospital discharge registry of Spain. This analysis was carried out with hospital data with a diagnosis of endometriosis (International Classification of Diseases (ICD)-9 code 617.xx and ICD-10 code N80.xx) and covered the period from 1 January 2014 to 31 December 2017 and a population of 12,775,911 women of reproductive age (15–54 years). The data were then analyzed at the national level and separately for each autonomous community. This nationwide Spanish study estimated the overall incidence of endometriosis among autonomous communities in Spain to be 16.1 per 10,000 women (range, 6.8 to 24). The mean age of the 20,547 women diagnosed with endometriosis during the study period was 36.8 ± 5.4 years. The types (proportions) of endometriosis were uterine (28.4%), tubo-ovarian (35.2%), peritoneal (8.1%), vesical (6.8%) and intestinal (3.2%) endometriosis. Further studies are needed to assess the reasons for the decrease in the observed incidence and for the significant differences in the regional incidence rates of this disease. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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9 pages, 306 KiB

Open AccessArticle

Evaluation of the Diagnostic Accuracy of the Interview and Physical Examination in the Diagnosis of Endometriosis as the Cause of Chronic Pelvic Pain

by Jolanta Nawrocka-Rutkowska, Iwona Szydłowska, Aleksandra Rył, Sylwester Ciećwież, Magdalena Ptak and Andrzej Starczewski

Int. J. Environ. Res. Public Health 2021, 18(12), 6606; https://doi.org/10.3390/ijerph18126606 - 19 Jun 2021

Cited by 10 | Viewed by 2788

Abstract

Background: Chronic pelvic pain affects approximately 15% of reproductive age women. It is mainly caused by adhesions (20–40%). Despite CPP being the main symptom of endometriosis, the disease is confirmed by laparoscopy only in 12–18% of cases. The aim of this study was to evaluate the results of laparoscopy in women with CCP and to assess the sensitivity and specificity of elements of an interview and clinical examination. Materials and methods: The study included 148 women with CPP. Each patient underwent laparoscopy. In laparoscopy, the presence of endometriosis and/or peritoneal adhesions was confirmed. Then, the sensitivity and specificity and the positive and negative predictive value of endometriosis symptoms or abnormalities in the gynecological examination were statistically calculated. Results: After previous surgery, adhesions were found in almost half (47%) of patients. In patients without a history of surgery, adhesions were diagnosed in 6.34% of patients. Endometriosis without coexisting adhesions was more often diagnosed in women without previous surgery (34.9%), compared to 10.58% in the group with a history of surgery (p < 0.05). Conclusions: Intraperitoneal adhesions are most common in women after pelvic surgery and with chronic ailments. The best results for sensitivity, specificity, positive predictive value, and negative predictive value in the diagnosis of endometriosis are found in women with irregular menstruations during which the pain increases. Laparoscopy still remains the primary diagnostic and therapeutic method for these women. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

Review

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14 pages, 1960 KiB

Open AccessReview

New Understanding of Diagnosis, Treatment and Prevention of Endometriosis

by Bedayah Amro, Maria Eugenia Ramirez Aristondo, Shaima Alsuwaidi, Basma Almaamari, Zeinab Hakim, Muna Tahlak, Arnaud Wattiez and Philippe R. Koninckx

Int. J. Environ. Res. Public Health 2022, 19(11), 6725; https://doi.org/10.3390/ijerph19116725 - 31 May 2022

Cited by 39 | Viewed by 12339

Abstract

For 100 years, pelvic endometriosis has been considered to originate from the implantation of endometrial cells following retrograde menstruation or metaplasia. Since some observations, such as the clonal aspect, the biochemical variability of lesions and endometriosis in women without endometrium, the genetic-epigenetic (G-E) theory describes that endometriosis only begins after a series of cumulative G-E cellular changes. This explains that the endometriotic may originate from any pluripotent cell apart from the endometrium, that ‘endometrium-like cells’ can harbour important G-E differences, and that the risk is higher in predisposed women with more inherited incidents. A consequence is a high risk after puberty which decreases progressively thereafter. Considering a 10-year delay between initiation and performing a laparoscopy, this was observed in the United Arab Emirates, Belgium, France and USA. The subsequent growth varies with the G-E changes and the environment but is self-limiting probably because of the immunologic reaction and fibrosis. That each lesion has a different set of G-E incidents explains the variability of pain and the response to hormonal treatment. New lesions may develop, but recurrences after surgical excision are rare. The fibrosis around endometriosis belongs to the body and does not need to be removed. This suggests conservative excision or minimal bowel without safety margins and superficial treatment of ovarian endometriosis. This G-E concept also suggests prevention by decreasing oxidative stress from retrograde menstruation or the peritoneal microbiome. This suggests the prevention of vaginal infections and changes in the gastrointestinal microbiota through food intake and exercise. In conclusion, a higher risk of initiating endometriosis during adolescence was observed in UAE, France, Belgium and USA. This new understanding and the limited growth opens perspectives for earlier diagnosis and better treatment. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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12 pages, 1247 KiB

Open AccessReview

Adenomyosis as a Risk Factor for Myometrial or Endometrial Neoplasms—Review

by Maria Szubert, Edward Kozirog and Jacek Wilczynski

Int. J. Environ. Res. Public Health 2022, 19(4), 2294; https://doi.org/10.3390/ijerph19042294 - 17 Feb 2022

Cited by 10 | Viewed by 5966

Abstract

Adenomyosis is a common benign gynecological condition, defined as an extension of endometrial tissue into the myometrium. Some studies suggest that adenomyosis could be a favorable prediction factor associated with survival outcomes in endometrial cancer. The aim of our systematic review was to investigate the current knowledge regarding adenomyosis and a possible molecular mechanism of carcinogenesis in adenomyotic lesions. In addition, the long-term prognosis for patients with endometrial cancer and coexisting adenomyosis (and endometriosis) was a key point of the research. The current literature was reviewed by searching PubMed, using the following phrases: “adenomyosis and endometrial cancer” and “malignant transformation of adenomyosis”. According to the literature, genetic mutations, epigenetic changes, and inactivation of specific tumor suppressor genes in adenomyosis are still poorly understood. Data regarding the influence of adenomyosis on survival outcomes in endometrial cancer seem to be contradictory and require further clinical and molecular investigation. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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16 pages, 4018 KiB

Open AccessReview

Classifying Adenomyosis: Progress and Challenges

by Marwan Habiba and Giuseppe Benagiano

Int. J. Environ. Res. Public Health 2021, 18(23), 12386; https://doi.org/10.3390/ijerph182312386 - 25 Nov 2021

Cited by 24 | Viewed by 5628

Abstract

Classically, the diagnosis of adenomyosis relied on histological examination of uteri following hysterectomy and classifications focused on the depth of endometrial invasion within the myometrium. There remain uncertainties around the cut-off point for the histological diagnosis. Imaging-based diagnosis enables recognition of the condition in women not undergoing surgery and facilitates the assessment of the extent of adenomyosis within the whole uterus, as well as of affections of the uterovesical pouch and of the pouch of Douglas. In this article, we explore the diagnostic uncertainties, the need to produce a classification of the condition and the challenges towards that goal. A distinction should be drawn between disease mapping and a classification that may link histological or image-based features with clinical characteristics, or with pathophysiology. An agreed system for reporting adenomyotic lesions may enable comparisons of research studies and thus contribute towards an informed classification. To this aim, we outline the features of the condition and explore the characteristics that are considered when producing a taxonomy. These include the latest proposal for subdivision of adenomyosis into an internal and an external variant. We also explore the uncertainties linked to classifying involvement of the uterovesical pouch, the pouch of Douglas and lesions in the outer myometrium. The limitations of currently available evidence suggest that agreement on a hypothesis to underpin a classification is unlikely at present. Therefore, current efforts will probably remain focused on disease mapping. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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12 pages, 2676 KiB

Open AccessReview

Uterine Adenomyosis: From Disease Pathogenesis to a New Medical Approach Using GnRH Antagonists

by Jacques Donnez, Christina Anna Stratopoulou and Marie-Madeleine Dolmans

Int. J. Environ. Res. Public Health 2021, 18(19), 9941; https://doi.org/10.3390/ijerph18199941 - 22 Sep 2021

Cited by 34 | Viewed by 7903

Abstract

Uterine adenomyosis is a common chronic disorder frequently encountered in reproductive-age women, causing heavy menstrual bleeding, intense pelvic pain, and infertility. Despite its high prevalence, its etiopathogenesis is not yet fully understood, so there are currently no specific drugs to treat the disease. A number of dysregulated mechanisms are believed to contribute to adenomyosis development and symptoms, including sex steroid signaling, endometrial proliferation and invasiveness, and aberrant immune response. Abnormal sex steroid signaling, particularly hyperestrogenism and subsequent progesterone resistance, are known to play a pivotal role in its pathogenesis, which is why various antiestrogenic agents have been used to manage adenomyosis-related symptoms. Among them, gonadotropin-releasing hormone (GnRH) antagonists are swiftly gaining ground, with recent studies reporting efficient lesion regression and symptom alleviation. The aim of the present review is to compile available information on the pathogenesis of adenomyosis, explore the etiology and mechanisms of hyperestrogenism, and discuss the potential of antiestrogenic therapies for treating the disease and improving patient quality of life. Full article

(This article belongs to the Special Issue Endometriosis and Adenomyosis Research: Recent Advances and Future Directions)

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