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SEE-FIM Protocol

From EverybodyWiki Bios & Wiki


  • Schematic of the components of the fallopian tube (upper right). Below are microscopic images taken from cross sections of the ampulla (left) and longitudinal sections of the infundibulum and fimbria (center right). A focus of early high grade serous carcinoma discovered in the fimbria is seen at the far right. The left panel illustrates the SEE-FIM protocol.
    Schematic of the components of the fallopian tube (upper right). Below are microscopic images taken from cross sections of the ampulla (left) and longitudinal sections of the infundibulum and fimbria (center right). A focus of early high grade serous carcinoma discovered in the fimbria is seen at the far right. The left panel illustrates the SEE-FIM protocol.

SEE-FIM Protocol

1 Definition

The SEE-FIM protocol is a pathology dissection protocol for Sectioning and Extensively Examining the Fimbria (SEE-FIM). This and similarly designed protocols are intended to provide for the optimal microscopic examination of the distal fallopian tube (fimbria) to identify either cancerous or precancerous conditions in this organ.[1][2]

2 Background

2.1 Functional anatomy of the fallopian tube

The fallopian tube originates from the Mullerian (paramesonephric) ducts during development and lies in the broad ligament between the uterus and the ovary. These tissues comprise the adnexa. It consists of three components; the isthmus, nearest the uterus, the midportion termed the ampulla and the more distal portion consisting of the infundibulum which opens into the peritoneal cavity and is lined by projections termed the fimbria. The principal function of the fallopian tube is to serve as a conduit for the passage of both sperm and fertilized egg followed by implantation in the uterine cavity.

2.2 Benign disorders of the fallopian tube.

Prior to the 21st century, the most commonly recognized disorders of the fallopian tube were those impacting on its role in pregnancy. Removal or pathologic examination of the tube most commonly was conducted to evaluate abnormal implantation of the embryo (ectopic pregnancy), confirm the presence of infectious or inflammatory conditions (salpingitis or pelvic inflammatory disease) remove ectopic deposits of endometrial tissue (endometriosis), or benign tumors such as fibroids (leiomyomata).

2.3 Extrauterine high grade serous cancer (HGSC) of the Ovary and Fallopian tube

Ovarian cancer eventually afflicts approximately 1.3% of women with approximately 24,000 cases each year in the United States and 15,000 deaths. High-grade serous cancer (HGSC) is the most common epithelial ovarian cancer, accounting for two thirds of all cases. Traditionally most HGSCs were assumed to arise on the ovarian surface epithelium or cortical epithelial inclusions in the ovary. Approximately 95% are discovered after they have become symptomatic and when diagnosed, over 90% are at least stage 2 or greater, meaning they have extended beyond the site of origin to involve other tissues including the fallopian tube and peritoneal surfaces. Consequently, the mortality from this disease is high, with 5 and 10-year survival rates of only 50 and 20% respectively. The high mortality is a combination of lack of effective screening, advanced stage when diagnosed and limited therapeutic options. Most patients respond initially to chemotherapy but in most cases the tumors will develop chemoresistance and the patients will eventually die of their disease.[3]

Malignant tumors of the fallopian tube, including HGSC were considered uncommon in earlier reports.[4] They were estimated to comprise less than one percent of gynecologic cancers in 1992.[5] A screening study in 1994 using serum CA125 assay to detect HGSCs provided a higher estimate for a tubal origin, detecting one fallopian tube for every 6 ovarian cancers.[6] However, although the widespread nature of HGSC often made the precise origin difficult to determine, most HGSCs occurring in the adnexa were presumed to arise from the ovary.

2.3 Emerging role of the fallopian tube ovarian carcinogenesis

2.31 Discovery of the Breast Cancer susceptibility gene (BRCA)

In 1995 specific heritable mutations in BRCA genes were described and subsequent genetic testing testing of patients showed that approximately 20% of HGSCs were linked to an inherited or germline mutation in one of the BRCA genes.[7] Subsequently, screening for the presence of these mutations in women without HGSC made it possible to identify women who were at increased risk for developing the disease and who would benefit from preventive surgery [see BRCA mutation].

2.32 Prevention of ovarian cancer in women with mutations in BRCA1 and BRCA2 by risk reduction salpingo-oophorectomy (RRSO)

Women with either a strong family history of breast and ovarian cancer or a documented inherited (germline) mutation in a BRCA gene were encouraged to consider risk reduction salpingo-oophorectomy (RRSO). The surgery was ideally conducted prior to the time that the risk of developing HGSC became too great to defer the procedure, which was age 35 for women with BRCA1 and 45 for BRCA2 mutations. Initially the primary target of the procedure was the ovaries. However removal of both tubes and ovaries reduced the risk of subsequent HGSC by 85% [see BRCA mutation].[8]

2.33 Discovery of early fallopian tube cancers in women with BRCA mutations

Beginning in 2000, case reports described early and often non-invasive malignancies in the fallopian tubes which were called serous tubal intraepithelial carcinomas or STICs.[9][10][11][12] These studies were conducted on ovaries and fallopian tubes from asymptomatic women with germline BRCA mutations who underwent RRSO.

3 Introduction of the SEE-FIM protocol

3.1 Conception

Prior to 2000, pathologic examination of the fallopian tubes in women with ovarian cancer usually entailed a random sampling technique in which only a portion of the ampulla and fimbria was submitted for pathologic examination.[13] The discovery of tubal cancers in healthy women was an uncommon occurrence. However, the emerging data linking the fallopian tube to some HGSCs focused more attention on the fallopian tubes removed from high risk women.[14] In January 2005, the SEE-FIM protocol was conceived and introduced in the Division of Women’s and Perinatal Pathology at Brigham and Women's Hospital in Boston, Massachusetts. This protocol required processing all of the fallopian tube in each case for examination. In addition, it specified the handling and sectioning of the distal one-third (infundibulum and fimbria).[1] The protocol was initially applied to fallopian tubes removed from women with germ line BRCA mutations who were undergoing RRSO. The use of this and similar dissection protocols would coincide with a shift in attention from the ovary to the distal fallopian tube as an origin of HGSC.[15][16]

3.2 Method

The SEE-FIM protocol introduced a modification of standard fallopian tube dissection protocols that ensured complete examination of the distal one third including the fimbria. The proximal portions of the tube were sectioned across the short axis (transverse or cross-sections, similar to cutting a loaf of bread), like prior sectioning protocols. The change in procedure entailed longitudinal or sagittal sectioning of the fimbria (cutting parallel to the long axis). This exposed a greater amount of epithelial surface in the fimbria, intended to maximize the odds of locating small cancers in this region.[1]

The SEE-FIM protocol consists of five steps (See Figure):

  1. The tube is fixed for at least 2 hours in laboratory fixative.
  2. The distal one third is amputated.
  3. The distal one third is sectioned in the longitudinal (sagittal) plane as thinly as possible and submitted for processing.
  4. The remainder of the tube is sectioned in the transverse (cross section) plane every 1-2 millimeters and submitted for processing.
  5. Sections are stained with hematoxylin and eosin and are examined by the pathologist with attention to the epithelial cells and the presence of any evidence of a malignancy or precancerous condition.[1]

4 Application to pathology practice

4.1 Use and validation

Following its introduction in 2005 and published description in 2006,[1] the SEE-FIM protocol was incorporated into many pathology practices that processed risk reduction specimens or gynecologic cancers. This was followed by a rise in the number of cases in which early cancers or cancer precursors were detected in the fimbria. In a recent review published in 2018, the SEE-FIM protocol was being used by 85% of academic pathology practices and 65% of private practices in the United States.[15] Multiple publications have subsequently described this technique in detecting early cancers in the fallopian tube and the protocol is in use throughout the United States and elsewhere in the World.[17][18][19][20]

4.2 Acceptance by societies and use in large studies.

With greater use in routine practice and research, the SEE-FIM protocol has highlighted the distal fallopian tube as an important site of origin for HGSC.

Routine use of the SEE-FIM protocol has been recommended by the College of American Pathologists and the International Society of Gynecologic Pathologists when processing fallopian tubes in risk reduction surgeries, and cases of ovarian and uterine serous cancer.[21][22] It is also recommended in the reporting guidelines for gynecologic cancer sponsored by the British Gynecologic Cancer Society.[23] It is also part of routine protocols in academic institutions and was employed to ascertain the frequency of STIC in a large population-based study.[24][25]

4.3 Variation in SEE-FIM or similar protocols

Currently, most institutions employ either the SEE-FIM or a similar protocol (one that completely examines the tube including fimbria but does not specify the SEE-FIM procedure) in evaluating fallopian tubes from risk reduction specimens or women with HGSC. The most important aspect of the protocol is thorough examination of the distal one third, where more than 80% of the early cancers are found. The taking of additional microscopic sections through the fimbria tissue block (analogous to taking multiple thin sections in a deli slicer) is an approach that will increase the detection frequency of small lesions.[14] In one study of HGSC approximately 10% of fallopian tubes initially interpreted as normal were found to contain a STIC after thorough sectioning of the entire fimbria.[26] However, in most practices, care is taken to produce thin sections (1-3 mm thick) of the fimbria during gross exam and additional sections from the tissue block are not taken if no abnormality is seen on microscopic exam.[14]

5. Discoveries

The SEE-FIM protocol standardized the approach to detecting early cancers and precancers in pathologic specimens of the fallopian tube. Because it was designed to optimize inspection, when it or similar protocols were adopted and used consistently, credible data could be accumulated regarding the frequency of either cancers or precancers in the fallopian tube.[27][28]

5.1 Shifting focus to the distal tube in serous carcinogenesis

5.11 Early detection of STICs or early HGSC in RRSOs in the fimbria of women with BRCA mutations

The SEE-FIM protocol initially was used for the evaluation of risk reduction salpingectomy specimens from women with germline BRCA mutations. Multiple studies using this protocol or a comparable protocol that processes the entire fallopian tube have detected precancers and early cancers in asymptomatic women at a frequency of up to 3.2%. Many of the latter tumors are limited to the epithelium (serous tubal intraepithelial carcinomas or STICs).[29][30][31] One study of 347 women using the SEE-FIM protocol identified neoplasia in over 5% with STIC in 4%.[32] Another study with rigorous evaluation of the fallopian tubes and ovaries disclosed a detection rate of 9.1%.[33] In all of these studies neoplasia was more likely to be detected in women with BRCA1 (versus BRCA2) mutations.

5.12 Linking the fallopian tube to advanced cases of HGSC

A study published in 2007 using the SEE-FIM protocol on specimens with advanced HGSC, identified STIC in nearly one half of cases, providing further evidence that the origin of these tumors could be traced to the distal fallopian tube.[27] This was eventually followed by recommendations to reclassify many HGSCS as tubal rather than ovarian in origin in practice.[34] A literature survey reported the frequency of associated STIC in cases of HGSC to range from 11-61%.[35] One study of women with HGSC found a STIC in 15 of 39 cases using the SEE-FIM protocol versus 1 of 113 cases using traditional (and limited) sampling techniques.[17] In another, conventional criteria for classifying site of origin (based largely on the distribution of the tumor seen on gross or macroscopic exam) classified 13% of HGSCs as tubal in origin, but 64% were eventually linked to the fallopian tube after careful microscopic analysis of the fallopian tube and fimbria.[36]

5.13 Discovery of and characterization of a serous carcinogenic “sequence” in the fimbria

Mutations in the tumor suppressor gene TP53 are consistently found in HGSCs. Small benign epithelial alterations containing the same mutations and termed “p53 signatures” have been described in the distal fallopian tube in both women with BRCA mutations and those in the general population.[37][38] Careful inspection of the distal tube with the SEE-FIM protocol revealed that tubes from up to 70% of women with BRCA mutations and 50% of women in general harbored p53 signatures.[39] Much less common are proliferations containing TP53 mutations that display changes intermediate between the p53 signature and STIC that were termed serous tubal intraepithelial lesions (STIL).[40] Together this continuum of epithelial changes in the fimbria linked to TP53 mutations further connected the fallopian tube to the development of HGSC.[41]

5.14 Complementary clinical studies confirming the link between the distal fallopian tube and HGSC

5.141 Determining the prevalence of early cancers (STICs) in the general population

Clinically derived population-based studies using the SEE-FIM protocol were conducted to determine the frequency of STICs in women who were not considered at high risk for HGSC. The estimated prevalence of STIC in these populations has been computed at 1.2 and 0.85 per 1000 women.[25][42] For comparison, the lifetime risk of ovarian cancer is approximately 13 per 1000 women.

5.142 Applications of SEE-FIM to ascertain recurrence risk in patient care.

For women in whom very early cancers (STICs) were discovered, earlier studies placed the risk of later relapse and disseminated HGSC at approximately 5-10%.[28][43][44] A more recent study analyzing multiple studies (meta-analysis) estimated the recurrence risks at 5 and 10 years to be 10% and 27% respectively. Consequently, thorough examination of the fallopian tubes has been recommended to ascertain the risk of a later recurrence.[45] Conversely, if no malignancy was found at risk reduction salpingectomy, the likelihood of a later HGSC is reported to be less than 1%. As a result, the SEE-FIM or comparable protocols have been endorsed to ascertain the likelihood of an early cancer in the distal tube and either alert the patient and their physician to the risk of recurrence or reassure them when no abnormality was found.[45][46]

5 Protocol contribution to the field of ovarian cancer pathogenesis and prevention

5.1 Prevention of HGSC by salpingectomy

5.11 Prevention of HGSC in women at low risk

Retrospective studies suggest that preemptive salpingectomy will reduce the incidence of later ovarian cancer by approximately 50%. Professional societies in the USA and throughout the world have issued statements addressing "opportunistic salpingectomy" (salpingectomy at the time of hysterectomy for benign conditions, other intra-abdominal procedures, or sterilization) as a potential means for reducing HGSC risk.[47][48][49][50] A recent study updating data that were accumulated over 10 years failed to identify a case of HGSC in over 25,000 women who had undergone opportunistic salpingectomy [see Prophylactic salpingectomy].[51] Studies such as this rely on the SEE-FIM or a comparable protocol to ensure that the normal appearing fallopian tubes in these patients do not harbor an occult malignancy.

5.12 Prevention of HGSC in high risk women by risk reduction salpingectomy (RRS)

Currently, preventing HGSC in women with germ-line BRCA mutations entails removal of both the ovaries and fallopian tubes. However, because so many HGSCs appear to have their origin in the fallopian tube, clinical trials are ongoing that offer salpingectomy alone for selected women with BRCA mutations who strongly desire a longer interval of preservation of ovarian function. These trials also rely on the the SEE-FIM or a comparable protocol to exclude the presence of occult HGSC and are in progress.[52]

7 See also

High grade serous carcinoma, BRCA mutation, Fallopian tube cancer, Ovarian cancer, Ovarian Cancer Research Alliance, Prophylactic salpingectomy

8 Abbreviations

BRCA – Breast cancer associated tumor suppressor genes, including BRCA1 and BRCA2. Inherited (germline) loss of a BRCA gene imposes an increased risk of breast and ovarian cancer.

TP53 – A tumor suppressor gene that is mutated in High grade serous carcinoma.

RRSO – Risk reduction salpingo-oophorectomy, traditionally employed to reduce the risk of future HGSCs in women with BRCA1 or BRCA2 germ-line mutations or women otherwise presumed to be at increased risk for this tumor.

RRS – Risk reduction salpingectomy, intended to reduce the risk of future HGSCs without removal of the ovaries.

HGSC – Extrauterine high grade serous carcinoma, historically the most common and most lethal “ovarian” carcinoma.

STIC – Serous tubal intraepithelial carcinoma, a non-invasive precursor to high grade serous carcinoma

References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 Medeiros, Fabiola; Muto, Michael G.; Lee, Yonghee; Elvin, Julia A.; Callahan, Michael J.; Feltmate, Colleen; Garber, Judy E.; Cramer, Daniel W.; Crum, Christopher P. (February 2006). "The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome". The American Journal of Surgical Pathology. 30 (2): 230–236. doi:10.1097/01.pas.0000180854.28831.77. ISSN 0147-5185. PMID 16434898. Unknown parameter |s2cid= ignored (help)
  2. ↑ Cass, Ilana; Holschneider, Christine; Datta, Nandini; Barbuto, Denise; Walts, Ann E.; Karlan, Beth Y. (December 2005). "BRCA-mutation-associated fallopian tube carcinoma: a distinct clinical phenotype?". Obstetrics and Gynecology. 106 (6): 1327–1334. doi:10.1097/01.AOG.0000187892.78392.3f. ISSN 0029-7844. PMID 16319259. Unknown parameter |s2cid= ignored (help)
  3. ↑ Cannistra, S. A. (1993-11-18). "Cancer of the ovary". The New England Journal of Medicine. 329 (21): 1550–1559. doi:10.1056/NEJM199311183292108. ISSN 0028-4793. PMID 8155119.
  4. ↑ Scully, RE; Young, RH; Clement, PB (1998). Tumors of the maldeveloped gonads, fallopian tube, and broad ligament. Atlas of Tumor Pathology (Third Series, Fascicle 23 ed.). Armed Forces Institute of Pathology. pp. 464–465. Search this book on
  5. ↑ Benedet, JL; Miller, DM (1992). "Tumors of the fallopian tube: clinical features, staging and management.". In Coppleson, M. Gynecologic Oncology (2nd ed.). Churchill Livingstone. pp. 853–860. Search this book on
  6. ↑ Woolas, R.; Jacobs, I.; Davies, A. Prys; Leake, J.; Brown, C.; Grudzinskas, J. G.; Oram, D. (November 1994). "What is the true incidence of primary fallopian tube carcinoma?". International Journal of Gynecological Cancer. 4 (6): 384–388. doi:10.1046/j.1525-1438.1994.04060384.x. ISSN 1525-1438. PMID 11578438. Unknown parameter |s2cid= ignored (help)
  7. ↑ Schubert, E. L.; Lee, M. K.; Mefford, H. C.; Argonza, R. H.; Morrow, J. E.; Hull, J.; Dann, J. L.; King, M. C. (May 1997). "BRCA2 in American families with four or more cases of breast or ovarian cancer: recurrent and novel mutations, variable expression, penetrance, and the possibility of families whose cancer is not attributable to BRCA1 or BRCA2". American Journal of Human Genetics. 60 (5): 1031–1040. ISSN 0002-9297. PMC 1712449. PMID 9150150.
  8. ↑ Rebbeck, Timothy R.; Lynch, Henry T.; Neuhausen, Susan L.; Narod, Steven A.; Van't Veer, Laura; Garber, Judy E.; Evans, Gareth; Isaacs, Claudine; Daly, Mary B.; Matloff, Ellen; Olopade, Olufunmilayo I.; Weber, Barbara L.; Prevention and Observation of Surgical End Points Study Group (2002-05-23). "Prophylactic oophorectomy in carriers of BRCA1 or BRCA2 mutations". The New England Journal of Medicine. 346 (21): 1616–1622. doi:10.1056/NEJMoa012158. ISSN 1533-4406. PMID 12023993.
  9. ↑ Zweemer, R. P.; van Diest, P. J.; Verheijen, R. H.; Ryan, A.; Gille, J. J.; Sijmons, R. H.; Jacobs, I. J.; Menko, F. H.; Kenemans, P. (January 2000). "Molecular evidence linking primary cancer of the fallopian tube to BRCA1 germline mutations". Gynecologic Oncology. 76 (1): 45–50. doi:10.1006/gyno.1999.5623. ISSN 0090-8258. PMID 10620440.
  10. ↑ Rose, P. G.; Shrigley, R.; Wiesner, G. L. (May 2000). "Germline BRCA2 mutation in a patient with fallopian tube carcinoma: a case report". Gynecologic Oncology. 77 (2): 319–320. doi:10.1006/gyno.2000.5740. ISSN 0090-8258. PMID 10785486.
  11. ↑ Paley, P. J.; Swisher, E. M.; Garcia, R. L.; Agoff, S. N.; Greer, B. E.; Peters, K. L.; Goff, B. A. (February 2001). "Occult cancer of the fallopian tube in BRCA-1 germline mutation carriers at prophylactic oophorectomy: a case for recommending hysterectomy at surgical prophylaxis". Gynecologic Oncology. 80 (2): 176–180. doi:10.1006/gyno.2000.6071. ISSN 0090-8258. PMID 11161856.
  12. ↑ Colgan, T. J.; Murphy, J.; Cole, D. E.; Narod, S.; Rosen, B. (October 2001). "Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status". The American Journal of Surgical Pathology. 25 (10): 1283–1289. doi:10.1097/00000478-200110000-00009. ISSN 0147-5185. PMID 11688463. Unknown parameter |s2cid= ignored (help)
  13. ↑ Rosai and Ackerman's Surgical Pathology. Elsevier. 2011. Search this book on
  14. ↑ 14.0 14.1 14.2 Powell, C. Bethan; Kenley, Eric; Chen, Lee-May; Crawford, Beth; McLennan, Jane; Zaloudek, Charles; Komaromy, Miriam; Beattie, Mary; Ziegler, John (2005-01-01). "Risk-reducing salpingo-oophorectomy in BRCA mutation carriers: role of serial sectioning in the detection of occult malignancy". Journal of Clinical Oncology. 23 (1): 127–132. doi:10.1200/JCO.2005.04.109. ISSN 0732-183X. PMID 15625367.
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  16. ↑ Kurman, Robert J.; Shih, Ie-Ming (July 2011). "Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer--shifting the paradigm". Human Pathology. 42 (7): 918–931. doi:10.1016/j.humpath.2011.03.003. ISSN 1532-8392. PMC 3148026. PMID 21683865.
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  18. ↑ Minig, L.; Cabrera, S.; Oliver, R.; Couso, A.; Rubio, M. J.; Iacoponi, S.; Martin-Salamanca, M. B.; Carballo-Rastrilla, S.; Cádenas-Rebollo, J. M.; García-Garcia, A.; Gil-Ibáñez, B.; Juan-Fita, M. J.; Patrono, M. G. (October 2018). "Pathology findings and clinical outcomes after risk reduction salpingo-oophorectomy in BRCA mutation carriers: a multicenter Spanish study". Clinical & Translational Oncology. 20 (10): 1337–1344. doi:10.1007/s12094-018-1865-9. ISSN 1699-3055. PMID 29623583. Unknown parameter |s2cid= ignored (help)
  19. ↑ Zhao, R. J.; Wang, Y. Y.; Li, Z.; Wu, K. Y.; Kong, L. F.; Zheng, W. X. (2017-08-08). "[Morphologic features of fallopian tubal epithelium in pelvic high-grade serous carcinoma]". Zhonghua Bing Li Xue Za Zhi = Chinese Journal of Pathology. 46 (8): 542–547. doi:10.3760/cma.j.issn.0529-5807.2017.08.005. ISSN 0529-5807. PMID 28810294.
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  22. ↑ Malpica, Anais; Euscher, Elizabeth D.; Hecht, Jonathan L.; Ali-Fehmi, Rouba; Quick, Charles M.; Singh, Naveena; Horn, Lars-Christian; Alvarado-Cabrero, Isabel; Matias-Guiu, Xavier; Hirschowitz, Lynn; Duggan, Máire; Ordi, Jaume; Parkash, Vinita; Mikami, Yoshiki; Ruhul Quddus, M. (January 2019). "Endometrial Carcinoma, Grossing and Processing Issues: Recommendations of the International Society of Gynecologic Pathologists". International Journal of Gynecological Pathology. 38 (1 Suppl 1): S9–S24. doi:10.1097/PGP.0000000000000552. ISSN 1538-7151. PMC 6296844. PMID 30550481.
  23. ↑ "Ovary, Fallopian Tube and Primary Peritoneal Carcinoma Histopathology Reporting Guide" (PDF). May 2019.
  24. ↑ "Gynecologic Pathology Grossing Guidelines Specimen Type" (PDF). April 2023.
  25. ↑ 25.0 25.1 Samimi, Goli; Trabert, Britton; Geczik, Ashley M.; Duggan, Máire A.; Sherman, Mark E. (October 2018). "Population Frequency of Serous Tubal Intraepithelial Carcinoma (STIC) in Clinical Practice Using SEE-Fim Protocol". JNCI Cancer Spectrum. 2 (4): pky061. doi:10.1093/jncics/pky061. ISSN 2515-5091. PMC 6649708 Check |pmc= value (help). PMID 31360879.
  26. ↑ Soong, Thing Rinda; Howitt, Brooke E.; Miron, Alexander; Horowitz, Neil S.; Campbell, Frank; Feltmate, Colleen M.; Muto, Michael G.; Berkowitz, Ross S.; Nucci, Marisa R.; Xian, Wa; Crum, Christopher P. (November 2018). "Evidence for lineage continuity between early serous proliferations (ESPs) in the Fallopian tube and disseminated high-grade serous carcinomas". The Journal of Pathology. 246 (3): 344–351. doi:10.1002/path.5145. ISSN 1096-9896. PMID 30043522. Unknown parameter |s2cid= ignored (help)
  27. ↑ 27.0 27.1 Kindelberger, David W.; Lee, Yonghee; Miron, Alexander; Hirsch, Michelle S.; Feltmate, Colleen; Medeiros, Fabiola; Callahan, Michael J.; Garner, Elizabeth O.; Gordon, Robert W.; Birch, Chandler; Berkowitz, Ross S.; Muto, Michael G.; Crum, Christopher P. (February 2007). "Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship". The American Journal of Surgical Pathology. 31 (2): 161–169. doi:10.1097/01.pas.0000213335.40358.47. ISSN 0147-5185. PMID 17255760. Unknown parameter |s2cid= ignored (help)
  28. ↑ 28.0 28.1 Stewart, Martha E.; Knisely, Anne T.; Sullivan, Mackenzie W.; Ring, Kari L.; Modesitt, Susan C. (May 2019). "Evaluation of screening and risk-reducing surgery for women followed in a high-risk breast/ovarian cancer clinic: it is all about the tubes in BRCA mutation carriers". Gynecologic Oncology Reports. 28: 18–22. doi:10.1016/j.gore.2019.01.010. ISSN 2352-5789. PMC 6365389. PMID 30775416.
  29. ↑ Bogaerts, Joep M. A.; Steenbeek, Miranda P.; van Bommel, Majke H. D.; Bulten, Johan; van der Laak, Jeroen A. W. M.; de Hullu, Joanne A.; Simons, Michiel (April 2022). "Recommendations for diagnosing STIC: a systematic review and meta-analysis". Virchows Archiv: An International Journal of Pathology. 480 (4): 725–737. doi:10.1007/s00428-021-03244-w. ISSN 1432-2307. PMC 9023413 Check |pmc= value (help). PMID 34850262 Check |pmid= value (help).
  30. ↑ Stroot, Iris A. S.; Brouwer, Jan; Bart, Joost; Hollema, Harry; Stommel-Jenner, Denise J.; Wagner, Marise M.; van Doorn, Helena C.; de Hullu, Joanne A.; Gaarenstroom, Katja N.; Beurden, Marc; van Lonkhuijzen, Luc R. C. W.; Slangen, Brigitte F. M.; Zweemer, Ronald P.; Gómez Garcia, Encarna B.; Ausems, Margreet G. E. M. (2023-02-21). "High-Grade Serous Carcinoma at Risk-Reducing Salpingo-Oophorectomy in Asymptomatic Carriers of BRCA1/2 Pathogenic Variants: Prevalence and Clinical Factors". Journal of Clinical Oncology: JCO2201237. doi:10.1200/JCO.22.01237. ISSN 1527-7755. PMID 36809028 Check |pmid= value (help). Unknown parameter |s2cid= ignored (help)
  31. ↑ Blok, F.; Dasgupta, S.; Dinjens, W. N. M.; Roes, E. M.; van Beekhuizen, H. J.; Ewing-Graham, P. C. (May 2019). "Retrospective study of a 16 year cohort of BRCA1 and BRCA2 carriers presenting for RRSO: Prevalence of invasive and in-situ carcinoma, with follow-up". Gynecologic Oncology. 153 (2): 326–334. doi:10.1016/j.ygyno.2019.03.003. ISSN 1095-6859. PMID 30894273. Unknown parameter |s2cid= ignored (help)
  32. ↑ Conner, James R.; Meserve, Emily; Pizer, Ellen; Garber, Judy; Roh, Michael; Urban, Nicole; Drescher, Charles; Quade, Bradley J.; Muto, Michael; Howitt, Brooke E.; Pearlman, Mark D.; Berkowitz, Ross S.; Horowitz, Neil; Crum, Christopher P.; Feltmate, Colleen (February 2014). "Outcome of unexpected adnexal neoplasia discovered during risk reduction salpingo-oophorectomy in women with germ-line BRCA1 or BRCA2 mutations". Gynecologic Oncology. 132 (2): 280–286. doi:10.1016/j.ygyno.2013.12.009. ISSN 1095-6859. PMC 3932113. PMID 24333842.
  33. ↑ Powell, C. Bethan; Chen, Lee-may; McLennan, Jane; Crawford, Beth; Zaloudek, Charles; Rabban, Joseph T.; Moore, Dan H.; Ziegler, John (July 2011). "Risk-reducing salpingo-oophorectomy (RRSO) in BRCA mutation carriers: experience with a consecutive series of 111 patients using a standardized surgical-pathological protocol". International Journal of Gynecological Cancer. 21 (5): 846–851. doi:10.1097/IGC.0b013e31821bc7e3. ISSN 1525-1438. PMID 21670699. Unknown parameter |s2cid= ignored (help)
  34. ↑ Singh, Naveena; Gilks, C. Blake; Hirschowitz, Lynn; Kehoe, Sean; McNeish, Iain A.; Miller, Dianne; Naik, Raj; Wilkinson, Nafisa; McCluggage, W. Glenn (May 2016). "Primary site assignment in tubo-ovarian high-grade serous carcinoma: Consensus statement on unifying practice worldwide". Gynecologic Oncology. 141 (2): 195–198. doi:10.1016/j.ygyno.2015.10.022. ISSN 1095-6859. PMID 26827965.
  35. ↑ Chen, F.; Gaitskell, K.; Garcia, M. J.; Albukhari, A.; Tsaltas, J.; Ahmed, A. A. (May 2017). "Serous tubal intraepithelial carcinomas associated with high-grade serous ovarian carcinomas: a systematic review". BJOG: An International Journal of Obstetrics and Gynaecology. 124 (6): 872–878. doi:10.1111/1471-0528.14543. ISSN 1471-0528. PMID 28218502. Unknown parameter |s2cid= ignored (help)
  36. ↑ Przybycin, Christopher G.; Kurman, Robert J.; Ronnett, Brigitte M.; Shih, Ie-Ming; Vang, Russell (October 2010). "Are all pelvic (nonuterine) serous carcinomas of tubal origin?". The American Journal of Surgical Pathology. 34 (10): 1407–1416. doi:10.1097/PAS.0b013e3181ef7b16. ISSN 1532-0979. PMID 20861711. Unknown parameter |s2cid= ignored (help)
  37. ↑ Piek, J. M.; van Diest, P. J.; Zweemer, R. P.; Jansen, J. W.; Poort-Keesom, R. J.; Menko, F. H.; Gille, J. J.; Jongsma, A. P.; Pals, G.; Kenemans, P.; Verheijen, R. H. (November 2001). "Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer". The Journal of Pathology. 195 (4): 451–456. doi:10.1002/path.1000. ISSN 0022-3417. PMID 11745677. Unknown parameter |s2cid= ignored (help)
  38. ↑ Lee, Y.; Miron, A.; Drapkin, R.; Nucci, M. R.; Medeiros, F.; Saleemuddin, A.; Garber, J.; Birch, C.; Mou, H.; Gordon, R. W.; Cramer, D. W.; McKeon, F. D.; Crum, C. P. (January 2007). "A candidate precursor to serous carcinoma that originates in the distal fallopian tube". The Journal of Pathology. 211 (1): 26–35. doi:10.1002/path.2091. ISSN 0022-3417. PMID 17117391. Unknown parameter |s2cid= ignored (help)
  39. ↑ Mehra, Karishma K.; Chang, Martin C.; Folkins, Ann K.; Raho, Caroline J.; Lima, Joema F.; Yuan, Liping; Mehrad, Mitra; Tworoger, Shelley S.; Crum, Christopher P.; Saleemuddin, Aasia (January 2011). "The impact of tissue block sampling on the detection of p53 signatures in fallopian tubes from women with BRCA 1 or 2 mutations (BRCA+) and controls". Modern Pathology. 24 (1): 152–156. doi:10.1038/modpathol.2010.171. ISSN 1530-0285. PMID 20871594. Unknown parameter |s2cid= ignored (help)
  40. ↑ Vang, Russell; Visvanathan, Kala; Gross, Amy; Maambo, Emily; Gupta, Mamta; Kuhn, Elisabetta; Li, Rose Fanghong; Ronnett, Brigitte M.; Seidman, Jeffrey D.; Yemelyanova, Anna; Shih, Ie-Ming; Shaw, Patricia A.; Soslow, Robert A.; Kurman, Robert J. (May 2012). "Validation of an algorithm for the diagnosis of serous tubal intraepithelial carcinoma". International Journal of Gynecological Pathology. 31 (3): 243–253. doi:10.1097/PGP.0b013e31823b8831. ISSN 1538-7151. PMC 3366037. PMID 22498942.
  41. ↑ Jarboe, Elke; Folkins, Ann; Nucci, Marisa R.; Kindelberger, David; Drapkin, Ronny; Miron, Alexander; Lee, Yonghee; Crum, Christopher P. (January 2008). "Serous carcinogenesis in the fallopian tube: a descriptive classification". International Journal of Gynecological Pathology. 27 (1): 1–9. doi:10.1097/pgp.0b013e31814b191f. ISSN 0277-1691. PMID 18156967. Unknown parameter |s2cid= ignored (help)
  42. ↑ Meserve, Emily E. K.; Mirkovic, Jelena; Conner, James R.; Yang, Eric; Muto, Michael G.; Horowitz, Neil; Strickland, Kyle C.; Howitt, Brooke E.; Crum, Christopher P. (July 2017). "Frequency of "incidental" serous tubal intraepithelial carcinoma (STIC) in women without a history of or genetic risk factor for high-grade serous carcinoma: A six-year study". Gynecologic Oncology. 146 (1): 69–73. doi:10.1016/j.ygyno.2017.04.015. hdl:10161/15044. ISSN 1095-6859. PMID 28479065.
  43. ↑ Powell, C. B.; Swisher, E. M.; Cass, I.; McLennan, J.; Norquist, B.; Garcia, R. L.; Lester, J.; Karlan, B. Y.; Chen, L. (May 2013). "Long term follow up of BRCA1 and BRCA2 mutation carriers with unsuspected neoplasia identified at risk reducing salpingo-oophorectomy". Gynecologic Oncology. 129 (2): 364–371. doi:10.1016/j.ygyno.2013.01.029. ISSN 1095-6859. PMC 6853713 Check |pmc= value (help). PMID 23391663.
  44. ↑ Patrono, Maria Guadalupe; Iniesta, Maria D.; Malpica, Anais; Lu, Karen H.; Fernandez, Rodrigo Orozco; Salvo, Gloria; Ramirez, Pedro T. (December 2015). "Clinical outcomes in patients with isolated serous tubal intraepithelial carcinoma (STIC): A comprehensive review". Gynecologic Oncology. 139 (3): 568–572. doi:10.1016/j.ygyno.2015.09.018. ISSN 1095-6859. PMID 26407480.
  45. ↑ 45.0 45.1 Steenbeek, Miranda P.; van Bommel, Majke H. D.; Bulten, Johan; Hulsmann, Julia A.; Bogaerts, Joep; Garcia, Christine; Cun, Han T.; Lu, Karen H.; van Beekhuizen, Heleen J.; Minig, Lucas; Gaarenstroom, Katja N.; Nobbenhuis, Marielle; Krajc, Mateja; Rudaitis, Vilius; Norquist, Barbara M. (2022-06-10). "Risk of Peritoneal Carcinomatosis After Risk-Reducing Salpingo-Oophorectomy: A Systematic Review and Individual Patient Data Meta-Analysis". Journal of Clinical Oncology. 40 (17): 1879–1891. doi:10.1200/JCO.21.02016. ISSN 1527-7755. PMC 9851686 Check |pmc= value (help). PMID 35302882 Check |pmid= value (help). Unknown parameter |pmc-embargo-date= ignored (help)
  46. ↑ Phillips, Kelly-Anne; Friedlander, Michael L. (2022-06-10). "Risk of Peritoneal Cancer After Risk-Reducing Bilateral Salpingo-Oophorectomy for Women With Germline BRCA Pathogenic Variants: A Cause for Concern or Potentially Avoidable?". Journal of Clinical Oncology. 40 (17): 1850–1852. doi:10.1200/JCO.22.00325. ISSN 1527-7755. PMID 35333598 Check |pmid= value (help). Unknown parameter |s2cid= ignored (help)
  47. ↑ Falconer, Henrik; Yin, Li; Grönberg, Henrik; Altman, Daniel (February 2015). "Ovarian cancer risk after salpingectomy: a nationwide population-based study". Journal of the National Cancer Institute. 107 (2): dju410. doi:10.1093/jnci/dju410. ISSN 1460-2105. PMID 25628372.
  48. ↑ ACOG (January 2008). "ACOG Practice Bulletin No. 89. Elective and risk-reducing salpingo-oophorectomy". Obstetrics and Gynecology. 111 (1): 231–241. doi:10.1097/01.AOG.0000291580.39618.cb. ISSN 0029-7844. PMID 18165419.
  49. ↑ Ntoumanoglou-Schuiki, Angelika; Tomasch, Gordana; Laky, Rene; Taumberger, Nadja; Bjelic-Radisic, Vesna; Tamussino, Karl (June 2018). "Opportunistic prophylactic salpingectomy for prevention of ovarian cancer: What do national societies advise?". European Journal of Obstetrics, Gynecology, and Reproductive Biology. 225: 110–112. doi:10.1016/j.ejogrb.2018.03.043. ISSN 1872-7654. PMID 29704813. Unknown parameter |s2cid= ignored (help)
  50. ↑ Walker, Joan L.; Powell, C. Bethan; Chen, Lee-May; Carter, Jeanne; Bae Jump, Victoria L.; Parker, Lynn P.; Borowsky, Mark E.; Gibb, Randall K. (2015-07-01). "Society of Gynecologic Oncology recommendations for the prevention of ovarian cancer". Cancer. 121 (13): 2108–2120. doi:10.1002/cncr.29321. ISSN 1097-0142. PMID 25820366. Unknown parameter |s2cid= ignored (help)
  51. ↑ Hanley, Gillian E.; Niu, Jin; Han, Jihee; Fung, Sharon; Bryant, Heather; Kwon, Janice S.; Huntsman, David G.; Finlayson, Sarah J.; McAlpine, Jessica N.; Miller, Dianne; Earle, Craig C. (2022). "Opportunistic salpingectomy between 2011 and 2016: a descriptive analysis". CMAJ Open. 10 (2): E466–E475. doi:10.9778/cmajo.20210219. ISSN 2291-0026. PMC 9177200 Check |pmc= value (help). PMID 35640988 Check |pmid= value (help).
  52. ↑ Nebgen, Denise R.; Hurteau, Jean; Holman, Laura L.; Bradford, Andrea; Munsell, Mark F.; Soletsky, Beth R.; Sun, Charlotte C.; Chisholm, Gary B.; Lu, Karen H. (July 2018). "Bilateral salpingectomy with delayed oophorectomy for ovarian cancer risk reduction: A pilot study in women with BRCA1/2 mutations". Gynecologic Oncology. 150 (1): 79–84. doi:10.1016/j.ygyno.2018.04.564. ISSN 1095-6859. PMID 29735278. Unknown parameter |s2cid= ignored (help)



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