Iatrogenic endometriosis harbors somatic cancer-driver mutations
Open accessAbstract
STUDY QUESTION: Does incisional endometriosis (IE) harbor somatic cancer-driver mutations? SUMMARY ANSWER: We found that approximately one-quarter of IE cases harbor somatic-cancer mutations, which commonly affect components of the MAPK/RAS or PI3K-Akt-mTor signaling pathways. WHAT IS KNOWN ALREADY: Despite the classification of endometriosis as a benign gynecological disease, it shares key features with cancers such as resistance to apoptosis and stimulation of angiogenesis and is well-established as the precursor of clear cell and endometrioid ovarian carcinomas. Our group has recently shown that deep infiltrating endometriosis (DE), a form of endometriosis that rarely undergoes malignant transformation, harbors recurrent somatic mutations. STUDY DESIGN, SIZE, DURATION: In a retrospective study comparing iatrogenically induced and endogenously occurring forms of endometriosis unlikely to progress to cancer, we examined endometriosis specimens from 40 women with IE and 36 women with DE. Specimens were collected between 2004 and 2017 from five hospital sites in either Canada, Germany or the Netherlands. IE and DE cohorts were age-matched and all women presented with histologically typical endometriosis without known history of malignancy. PARTICIPANTS/MATERIALS, SETTING, METHODS: Archival tissue specimens containing endometriotic lesions were macrodissected and/or laser-capture microdissected to enrich endometriotic stroma and epithelium and a hypersensitive cancer hotspot sequencing panel was used to assess for presence of somatic mutations. Mutations were subsequently validated using droplet digital PCR. PTEN and ARID1A immunohistochemistry (IHC) were performed as surrogates for somatic events resulting in functional loss of respective proteins. MAIN RESULTS AND THE ROLE OF CHANCE: Overall, we detected somatic cancer-driver events in 11 of 40 (27.5%) IE cases and 13 of 36 (36.1%) DE cases, including hotspot mutations in KRAS, ERBB2, PIK3CA and CTNNB1. Heterogeneous PTEN loss occurred at similar rates in IE and DE (7/40 vs 5/36, respectively), whereas ARID1A loss only occurred in a single case of DE. While rates of detectable somatic cancer-driver events between IE and DE are not statistically significant (P > 0.05), KRAS activating mutations were more prevalent in DE. LIMITATIONS, REASONS FOR CAUTION: Detection of somatic cancer-driver events were limited to hotspots analyzed in our panel-based sequencing assay and loss of protein expression by IHC from archival tissue. Whole genome or exome sequencing, or epigenetic analysis may uncover additional somatic alterations. Moreover, because of the descriptive nature of this study, the functional roles of identified mutations within the context of endometriosis remain unclear and causality cannot be established. WIDER IMPLICATIONS OF THE FINDINGS: The alterations we report may be important in driving the growth and survival of endometriosis in ectopic regions of the body. Given the frequency of mutation in surgically displaced endometrium (IE), examination of similar somatic events in eutopic endometrium, as well as clinically annotated cases of other forms of endometriosis, in particular endometriomas that are most commonly linked to malignancy, is warranted. STUDY FUNDING/COMPETING INTEREST(S): This study was funded by a Canadian Cancer Society Impact Grant [701603, PI Huntsman], Canadian Institutes of Health Research Transitional Open Operating Grant [MOP-142273, PI Yong], the Canadian Institutes of Health Research Foundation Grant [FDN-154290, PI Huntsman], the Canadian Institutes of Health Research Project Grant [PJT-156084, PIs Yong and Anglesio], and the Janet D. Cottrelle Foundation through the BC Cancer Foundation [PI Huntsman]. D.G. Huntsman is a co-founder and shareholder of Contextual Genomics Inc., a for profit company that provides clinical reporting to assist in cancer patient treatment. R. Aguirre-Hernandez, J. Khattra and L.M. Prentice have a patent MOLECULAR QUALITY ASSURANCE METHODS FOR USE IN SEQUENCING pending and are current (or former) employees of Contextual Genomics Inc. The remaining authors have no competing interests to declare. TRIAL REGISTRATION NUMBER: Not applicable.
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Some iatrogenic endometrioses have a cancer-driving mutation, which may be related to the mechanism of malignant transformation.
“It has been reported that some iatrogenic endometrioses have a cancer‐driving mutation, 17 which may be related to the mechanism of malignant transformation.”
From Extra-pelvic endometriosis: a review. (2020) · cites this paper as [17]
Scar endometriosis is considered the most frequent of the abdominal wall endometrioses and may be defined as an iatrogenic endometriosis.
“Scar endometriosis is considered to be the most frequent of the abdominal wall endometrioses and may be defined as an iatrogenic endometriosis.”
From Extra-pelvic endometriosis: a review. (2020) · cites this paper as [17]
Molecular biology techniques using next-generation sequencing have provided clues to the origin of endometriosis and pathogenesis that cannot be elucidated by epidemiological investigations alone.
“Recently, molecular biology techniques using a next‐generation sequencing have also provided clues to the origin of endometriosis and pathogenesis that cannot be elucidated by epidemiological investigations alone.”
From Extra-pelvic endometriosis: a review. (2020) · cites this paper as [17]
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“Women with endometriosis have a two- to four-fold increased chance of acquiring these tumors; in addition, mutational investigations have shown a clonal link between endometriosis-associated ovarian carcinomas and endometriotic lesions [16].”
Background
- Authors
- Lac, V, Verhoef, L., Aguirre-Hernandez, R., Nazeran, T. M., Tessier-Cloutier, B., Praetorius, T., Orr, N. L., Noga, H., Lum, A., Khattra, J., Prentice, L. M., Co, D., Köbel, M., Mijatovic, V, Lee, A. F., Pasternak, J., Bleeker, M. C., Krämer, B., Brucker, S. Y., Kommoss, F., Kommoss, S., Horlings, H. M., Yong, P. J., Huntsman, D. G., & Anglesio, M. S.
- Affiliations
- University of British Columbia (CA)
- The Netherlands Cancer Institute (NL)
- Contextual Genomics, 2389 Health Sciences Mall #204, Vancouver, British Columbia, Canada
- Vancouver General Hospital (CA)
- Department of Pathology and Laboratory Medicine, Rm G227, 2211 Wesbrook Mall, University of British Columbia, Vancouver, British Columbia, Canada
- Universitätsklinikum Tübingen (DE)
- Department of Molecular Oncology, BC Cancer Research Centre, Room 3-218, 675 West 10th Ave, Vancouver, British Columbia, Canada
- University of Calgary (CA)
- Vrije Universiteit Amsterdam (NL)
- Medizin Campus Bodensee (DE)
- Corresponding author
- Anglesio, M S
- ORCID
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-11-14
- Volume
- 34
- Issue
- 1
- Pages
- 69-78
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- PMC
- PMC6296213
- OpenAlex
- W2900810975
- Cited by
- 99
- References
- 51
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 11 · 2023: 14 · 2022: 13 · 2021: 13 · 2020: 21 · 2019: 11
- FWCI
- 12.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Human Reproduction (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (submittedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Canadian Cancer Society Impact (701603)
- Canadian Institutes of Health Research Transitional Open Operating (MOP-142273)
- Canadian Institutes of Health Research Foundation (FDN-154290, Janet D. Cottrelle Foundation through the BC Cancer Foundation)
- BC Women’s Hospital and Health Centre Foundation and Women’s Health Research Institute
- BC Women’s Centre for Pelvic Pain and Endometriosis
- BC Cancer Foundation
- VGH and UBC Hospital Foundation
- Canadian Institutes of Health Research
- V. Lac. The Dutch Cancer Society (KWF 2013-5869)
- H.M. Horlings. The Janet D. Cottrelle Foundation Scholars
- Canada Research Chairs
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Keywords
- deep infiltrating endometriosis, somatic mutations, cancer driver mutations, iatrogenic endometriosis, PTEN loss, ARID1A loss, KRAS mutation, PIK3CA, ERBB2, CTNNB1, PI3K/AKT/mTOR pathway, endometriosis-associated cancer
- MeSH terms
- Adult, Canada, Endometriosis, Endometrium, Female, Germany, Humans, Iatrogenic Disease, Middle Aged, Mutation, Neoplasms, Netherlands, Retrospective Studies, Gynecologic Surgical Procedures, Biomarkers, Tumor, Signal Transduction, Disease Progression, Carcinogenesis
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