The Origin of Pelvic Low-Grade Serous Proliferative Lesions
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1 The Origin of Pelvic Low-Grade Serous Proliferative Lesions Ovarian Atypical Proliferative (Borderline) Serous Tumors, Noninvasive Implants and Endosalpingiosis Robert J. Kurman, M.D. Kurman RJ, Vang R, Junge J Gerd Hannibal C, Kjaer SK, Shih I-M AJSP 2011;35:
2 The Birth of Borderline Officially established as a distinct category by FIGO in 1971 and WHO in 1973 Since then controversy has surrounded terminology and behavior Little attention directed towards determining origin
3 Tubal Hyperplasia Tubal hyperplasia significantly associated with SBTs Robey and Silva tubal hyperplasia in 69% of SBTs compared to 26% of controls (p<0.01) Tubal hyperplasia not significantly associated with SBTs Yanai-Inbar et al no significant difference between SBTs and controls Different criteria for Dx of tubal hyperplasia used in the two studies Robey, Silva. Int J Gynecol Pathol 1989;8: Yanai-Inbar et al Int J GynecolPathol 1995;14:
4 Current Study Case Selection (n=29) Population-based SBT study Denmark Approximately, 950 SBTs collected over 20 yrs with 32 yr FU, no losses to FU 22 cases with tubal implants selected because adjacent tubal tissue was available for review Consult cases from JHH 7 cases in patients - no ovarian tumor
5 Definition of Tubal Hyperplasia in Current Study Papillary tufting, detached clusters of epithelial cells (secretory and ciliated) and papillae composed of bland epithelium with or without associated psammoma bodies Papillary tubal hyperplasia (PTH)
6
7 Papillary Tubal Hyperplasia
8 Findings in Danish Study Age of patients yrs; mean 42 yrs 10 yrs younger than cohort; no other differences PTH in 20 (91%) of 22 Psammoma bodies in 50% Chronic salpingitis in 36% Evidence of prior PID in 36% Noninvasive implants in omentum and/or uterine serosa in 14% Endosalpingiosis on tube or in omentum in 27%
9 Findings in JHH Study Age of patients yrs; mean 46 yrs Psammoma bodies in 57% Chronic inflammation in 42% Evidence of prior PID in 57% Noninvasive implants in 14% Endosalpingiosis in 29%
10 Proposed Evolution of Tubal Hyperplasia Focal epithelial stratification
11 Proposed Evolution of Tubal Hyperplasia Formation of tuft that expands, forming rounded papillae
12 Proposed Evolution of Tubal Hyperplasia Papillae are pinched off and extruded into lumen
13 Papillary Tubal Hyperplasia
14 Proposed Evolution of Tubal Hyperplasia Expulsion of papillae/clusters from tube with implantation on ovary and peritoneal surfaces with development of Cystadenoma and SBT Endosalpingiosis Noninvasive implants Spectrum of serous proliferations
15 Proposed Evolution of Psammoma Bodies Develop in epithelium and when papillae form they are in the central core (salpingoliths) Seidman et al. Int J Gynecol Pathol 2002;21: Salpingolith
16 Proposed Evolution of Psammoma Bodies If epithelium invaginates psammoma bodies are deposited in the lamina propria
17 Proposed Evolution of Psammoma Bodies Expulsion from tube with implantation on ovary and peritoneum Degeneration of epithelium that surrounds the psammoma bodies results in naked psammoma bodies Naked psammoma bodies appear to act as an irritant in the peritoneal cavity leading to fibrosis which can in turn lead to adhesions and possibly bowel obstruction
18
19 Endosalpingiosis and Noninvasive Implants?Progression Various studies (and personal experience) suggest that endosalpingiosis and noninvasive implants can undergo malignant transformation resulting in the development of low-grade serous carcinoma
20 Three Possible Mechanisms to Explain Association of Tubal Hyperplasia and SBT (APST)s The tubal and ovarian lesions arise independently, so-called field effect Ovarian tumor is primary and tubal hyperplasia is secondary Tubal hyperplasia is primary and SBT (APST), noninvasive implants and endosalpingiosis are secondary
21 Problems with Independent Development of Tubal Hyperplasia and SBT (APST) (Field Effect) One field but different embryological origins Ovaries develop from the genital ridge not from the müllerian ducts Fallopian tubes develop from the müllerian ducts
22 Problems with Independent Development of Tubal Hyperplasia and SBT (APST) (Field Effect) SBT (APST)s have a müllerian phenotype but the ovarian surface epithelium (OSE) from which it is postulated SBT (APST)s are derived from, is mesothelial
23 Problems with the Field Effect Psammoma bodies are an integral part of PTH but are only rarely associated with mesothelial proliferations Morphology, immunohistochemistry and gene expression profiles link SBT (APST)s to fallopian tube epithelium not to the OSE Marquez RT, et al. Clin Cancer Res 2005;11: SBT (APST)s, noninvasive implants and endosalpingiosis, for all practical purposes, do not occur in males
24 Origin of Some SBT (APST)s from Cortical Inclusion Cysts A distinct possibility
25 Tube and Ovary at Ovulation
26 Formation of Cortical Inclusion Cyst
27 Implantation of FTE on Ovary OSE OSE FTE FTE CIC CIC Calretinin PAX 8
28 Two Types of Ovarian Cortical Inclusions Cysts (CICs) CICs lined by flat epithelium represent invagination of ovarian surface epithelium CICs lined by columnar epithelium are of tubal origin An interpretation also recently proposed by Li J. et al Mod Pathol 2011;24:
29 Fallopian Tube Ovary - CIC CD 45
30 CICs Cellular composition of FTE and CICs (columnar epithelial type) is identical OSE does not contain lymphocytes Aneuploidy in CICs Pothuri B, et al PLoS One 2010, 5e10358 CICs may account for the origin of some SBT (APST)s but they develop from tubal epithelium not from OSE
31 Papillary Tubal Hyperplasia
32 Papillary Tubal Hyperplasia Atypical Proliferative Tumor
33 CD3 + T and NKp44 + NK cells in Tubal Epithelium CD3=Pink NKp44=Brown Courtesy Dr W.Vermi and Dr F.Facchetti
34 APST (SBT) CD68R L Ardghiri et al CD8
35 Endosalpingiosis in a Lymph Node CD 45 CD 45
36 Intraepithelial Leukocytes (IELs) Fallopian tube epithelium (FTE), CICs and APSTs contain the same population of cells of the immune system Most are cytotoxic T-cells (CD8+) and macrophages (CD68R+) In addition, NKp44 + NK cells have been identified in FTE. This subset of NK cells secretes IL-22, a cytokine known for providing mucosal protection Conclusions Subpopulations of leukocytes, primarily involved in immune mucosal protection, may, through inflammation, play a role in neoplastic development
37 Model for the Origin and Development of all Low-grade Pelvic Serous Proliferations Chronic inflammation induces proliferation of tubal epithelium In some cases the proliferation progresses to PTH with shedding of papillae and epithelial clusters that implant on ovarian and peritoneal surfaces On ovary lesion is a cortical inclusion cyst On peritoneum it is endosalpingiosis
38 Origin and Development of all Lowgrade Pelvic Serous Proliferations Cortical inclusion cysts (tubal type) can develop into a serous cystadenoma Mutation of KRAS or BRAF results in the development of a SBT(APST)
39 Small SBT(APST) arising in Cystadenoma Borderline tumor Cyst Before After Cheng EJ, et al Lab Invest 2004; 84:
40 Mutations of KRAS and BRAF Precede the Development of a SBT(APST) 3 mm Serous cystadenoma adjacent to SBT(APST) SBT(APST) in Serous cystadenoma BRAF mutation Codon 600, T1796A BRAF mutation Codon 600, T1796A Cheng EJ, et al Lab Invest 2004; 84:
41 PTH - Primary or Secondary? PTH is the primary event Seven cases of PTH in this study in the absence of an ovarian tumor PTH is morphologically identical in patients with or without an ovarian tumor
42 Origin and Development of all Lowgrade Pelvic Serous Proliferations Model not only explains development of ovarian SBT(APST)s But also primary peritoneal SBT(APST)s and noninvasive implants in the absence of an ovarian tumor In conclusion, all pelvic serous proliferations, benign and malignant, develop from the fallopian tube epithelium
43 The era of indifference to the fallopian tube has passed Woodruff JD, Pauerstein CJ The Fallopian Tube Structure, Function, Pathology and Management Williams and Wilkins Co; 1969 Finally
NIH Public Access Author Manuscript Am J Surg Pathol. Author manuscript; available in PMC 2012 November 1.
NIH Public Access Author Manuscript Published in final edited form as: Am J Surg Pathol. 2011 November ; 35(11): 1605 1614. doi:10.1097/pas.0b013e318229449f. Papillary Tubal Hyperplasia. The Putative Precursor
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