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	Congenital ampullary atresia of the fallopian tube and the embryology of fimbrial and ovarian epithelium.

Niamh Tallona MB,BCh, BAO, FRCSC. 
Ghadeer Akbara  MD, FRCSC.
Peter McComba  MB,BS, FRCSC.
a Division of  Reproductive Endocrinology and Infertility, 
Department of Obstetrics and Gynaecology, 
University of British Columbia, 
Vancouver,
British Columbia, 
Canada
nmtallon@gmail.com
 HYPERLINK "mailto:ghadeer.akbar@mail.mcgill.ca" ghadeer.akbar@mail.mcgill.ca
pmccomb@mail.ubc.ca
Corresponding author: Dr. Peter McComb
Postal Address:
a Division of Reproductive Endocrinology and Infertility, 
UBC Department of Obstetrics and Gynecology, 
D409-4500 Oak Street, 
Vancouver, 
BC Canada, V6H 3N1. 
Phone: 1-604-2288112.
Abstract:
Three cases of congenital ampullary atresia are reported.  This augments our earlier series from 5 to 8 cases.  Despite the atresia of the ampulla, in each case there was preservation of the fimbria, suggesting that the embryologic origin of the fimbria is distinct from the remainder of the ampulla.  This observation concurs with the recent hypothesis that both fimbrial tissue and the ovarian surface epithelium are derived from celomic mesoderm and that each may give rise to epithelial malignancy.  All 8 cases presented to our tertiary care centre for infertility evaluation over the years 1987-2012.  Participants underwent hysterosalpingography and laparoscopy to yield the definitive diagnosis.  Surgical intervention by laparoscopic salpingostomy and fimbrial approximation resulted in at least one child for 5 of 8 women. 
Key words: congenital partial segmental ampullary tubal atresia











Background:
This paper addresses the diagnosis and therapy of congenital ampullary atresia (CAA).  It also complements our knowledge of the common embryologic origin of the fimbria and ovarian surface epithelium (OSE), as well as the propensity of each tissue to develop epithelial malignancies.  
Congenital ampullary atresia of the fallopian tube is a rare finding with an unknown prevalence in the general population (2). Those affected can be asymptomatic or misclassified, because the findings of an absence of a segment of the ampulla of the fallopian tube at laparoscopy are often subtle and can be misinterpreted as being an ampullary obstruction of infectious etiology. We have previously reported a series of 5 cases of CAA in 2003.  All presented with infertility.  This publication now adds to these cases.  Fertility outcomes after corrective surgery are also reported. 
At initial hysterosalpingography (HSG) ampullary obstruction due to the CAA is identified.  However, the definitive diagnosis of CAA is made at laparoscopy with the pathognomonic finding of a fallopian tube that is obstructed at the mid-ampullary region to form a hydrosalpinx. In the absence of the distal ampulla, the occluded mid-ampulla is connected by a 2-3 centimetre band of mesosalpinx to the  outlying fimbrial tissue. To improve fertility potential, surgical treatment consists of laparoscopic salpingostomy of the terminus of the occluded ampulla with approximation of the fimbria with microsuture (3).  The fimbria is attached so that a cumulus oophorus retrieved by the fimbria will have access to the ampullary lumen.
Objective:
To report the novel observation that fimbrial tissue is always present ipsilateral to the CAA.  This finding supports the concept that the fimbria has an embryologic origin that is distinct from the remainder of the fallopian tube.  It also is in accordance with the notion that �ovarian� epithelial malignancies may arise from the fimbria as well as the ovary.

Materials and Methods:
The health data from women referred for infertility to an individual consultant were gathered prospectively at the time of initial assessment at our tertiary care centre over the years of 2003 � 2012.   The assessment included HSG and laparoscopy. Those afflicted with CAA underwent corrective surgery at the same laparoscopy. The diagnosis of CAA was entered postoperatively into an ongoing administrative database system, dBase III (Ashton-Tate, Culver City, Ca). The cases are collated here for review. This series augments 5 cases reported by one of us previously.  That series derived from the years 1987 - 2002 (1).
Results:
Congenital ampullary atresia was identified in an additional 3 cases, to bring the total combined with our previous series, to 8 such women (Table 1).  Of particular interest, we document healthy fimbrial tissue to be physically adjacent to the ipsilateral ovary in each of the cases.  After the reconstructive surgery, 5 women have delivered at least one healthy infant each; another has experienced a pregnancy of inconclusive site.
These 8 cases represent 3.9% of all laparoscopic salpingostomies performed for distal tubal obstruction over a 25 year period.  This includes distal occlusions of infectious causation, but excludes iatrogenic occlusions such as fimbriectomy, segmental sterilization or excision of ectopic pregnancy.  
At the time of referral, for all but one case, the diagnosis by the referring gynecologist was distal hydrosalpinx, or hydrosalpinges, of infectious etiology.  This was so, irrespective of whether a laparoscopy had been performed.  In the single case where the etiology of CAA was correctly identified at referral, that gynecologist had previously attended a case of CAA.








Discussion:
Congenital ampullary atresia is a rare finding that is likely under-reported due to the diagnostic subtleties associated with the condition.  
Alternate mechanisms by which segmental tubal deletions may occur include environmental factors, acquired infectious obstruction, or they may be secondary to vascular torsion. In all of the cases reviewed in this series, there was no history of acute undiagnosed pelvic pain suggesting acute torsion. Of the eight cases of CAA identified, three had positive chlamydial cervical cultures. However, the pathognomonic findings of CAA at laparoscopy and a total lack of intra-peritoneal infectious stigmata, as well as the high degree of fecundity achieved after salpingostomy with approximation of the fimbria, point to a true congenital etiology.  Occlusion sustained after pelvic infection is usually associated with damage to the ciliary mucosa and thus poor pregnancies rates after terminal salpingostomy.
In the literature, both unilateral and bilateral tubal atresias have been described, either involving the isthmic, ampullary or distal portions of the tube (4, 5). These are isolated findings in 30% of cases. The other 70% are associated with Mullerian anomalies (6). When the abnormality is an isolated partial absence of the tube, it has not been associated with a renal tract abnormality (7). 
The fallopian tubes, uterus, cervix and upper vagina all derive from the paramesonephric (Mullerian) system; the pair of ducts that originates from the coelomic epithelium of the urogential ridge between 8-16 weeks gestational age. The adjacent mesonephric (Wolfian) system acts as a developmental guide, directing normal paramesonephric fusion and canalization (8,9). The fallopian tubes derive, embryologically, from the unfused cranial aspect of the paramesonephric ducts. 
The master regulatory genes involved in development are known as the homeobox genes. These are highly conserved and are expressed in a co-linear fashion, leading to very controlled and ordered gene expression from the 3� to the 5� end of the gene. The HOXA genes are associated with the Mullerian system in the female human; HOXA9 expression is highest in the fallopian tube, with HOXA10 and HOXA11 activity being found in the uterus (10). 
A recent study has documented that fimbrial tissue develops at a later stage than previously thought - after 20 weeks� gestation (11). Along these lines, Garrett and coworkers hypothesize that the embryologic origin of the fimbria is distinct from the remainder of the oviduct (12). This is based upon the finding of fimbrial tissue juxtaposed with the ovary in females affected by Mayer Rokitanszki Kauster Hauser (MRKH) syndrome, despite absence of the remainder of the fallopian tubes (and also the vagina and uterus).
Despite a lack of an established genetic role in CAA, there is a 12 fold increased risk for Mullerian anomalies amongst affected family members who have segmental oviductal atresias.  Given the phenotypic differences amongst those families affected, the underlying aetiology is thought to be polygenic or multifactorial (13).  
Our documentation that fimbrial tissue is always juxtaposed with the ovary, despite the absolute deficiency in the adjacent distal ampulla, is further evidence that the fimbria and the OSE derive, in part, from a single embryologic heritage.  This fundamental shift in embryologic theory is also supported by work by Auersperg from our Department (14).  She has quantified the immunohistochemical staining for mesenchymal differentiation markers of OSE, as well as for epithelial markers and Pax8 that characterize fimbrial and ampullary tissues. She has shown that the OSE and fimbrial markers overlap.  This is consistent with the hypothesis that the OSE and fimbria are parts of a transitional epithelium of common origin. The results support the hypothesis that, rather than there being 2 independent sources of ovarian cancer, instead the immature, incompletely determined phenotype of both the fimbria and the OSE, contributes to their joint propensity to neoplastic transformation.
Moreover, this common fimbrial - ovarian embryologic origin provides further explanation of �ovarian� epithelial carcinogenesis that is documented to arise in the fallopian tube by Salvador and coworkers (15). 
We conclude that our finding of consistent presence of the fimbria in all 8 cases of CAA, supports the concept proposed by Garrett that the fimbria may have a unique embryologic origin that is distinct from the remainder of the fallopian tube.  This also accords with the notion that ovarian carcinogenesis, specifically epithelial malignancies, may arise from fimbrial tissues as well as from the OSE.
 
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Taylor RC, Berkowitz J, McComb PF (2001) Role of laparoscopic salpingostomy in the treatment of hydrosalpinx. Fertil Steril 75: 594�600.   
Nawroth F, Nugent W, Ludwig M (2006) Congenital partial atresia of the Fallopian tube. Reprod BioMed Online 12: 205-8.
McBean JH, Brumsted JR (1994) Pregnancy after laparoscopic neosalpingostomy in a patient with atresia of the distal fallopian tubes. Fertil Steril ( 61: 1163 4. 
Nicosia SV (1985) Pathology of the oviducts and embryonal remnants. Obstet Gynecol Annu 14: 382 410.
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Braun P, Grau FV, Pons RM, Enguix DP (2005) Is hysterosalpingography able to diagnose all uterine malformations correctly? A retrospective study. Eur J Radiol 53: 274�9.
Taylor HS, Vanden Heuvel GB, Igarashi P (1997) A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes.  Biol Reprod 57: 1338-45.
Sulak O, Malas MA, Esen K, Cetin E, Ungor B, Tagil SM (2005) Uterine tube-ovary relationship and fimbrial development during the fetal period. Saudi Med J 26: 1080-4.
Garrett LA, Vargas SO, Drapkin R, Laufer MR (2008) Does the fimbria have an embryologic origin distinct from that of the rest of the fallopian tube? Fertil Steril 90: e5-8. 
Hammoud AO, Gibson M, Peterson CM, Kerber RA, Mineau GP, Hatasaka H (2008) Quantification of the familial contribution to mullerian anomalies. Obstet Gynecol 111: 378�84. 
Auersperg N (2011) The origin of ovarian carcinomas: a unifying hypothesis.  Int J Gynecol Pathol 30: 12-21.
Salvador S, Gilks B, Kobel M, Huntsman D, Rosen B, Miller D (2009) Int J Gynecol Cancer  19: 58-64. 

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Youez - 2016 - github.com/yon3zu
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