A hypothesis for the pathogenesis and natural history of proximal tubal blockage

Spyros Papaioannou

Consultant Obstetrician and Gynaecologist, Birmingham Heartlands and Solihull NHS Trust, Bordesley Green East Birmingham B9 5SS, UK.Correspondence should be addressed to: 142 Harbonre Park Road, Birmingham B17 0BS, UK. e-mail: spyrospap{at}talk21.com


    Abstract
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 Abstract
 Introduction
 Anatomy
 Physiology
 Pathology
 An hypothesis for the...
 Conclusions
 References
 
This paper reviews the literature on the proximal Fallopian tube and attempts to synthesize the available information into an hypothesis to elucidate the pathogenesis and natural history of proximal tubal blockage (PTB). There is evidence that the unique anatomy and physiology of the proximal Fallopian tube may predispose this tubal segment to a ‘physiological’ blockage, by tubal secretions and/or material back flowing from the uterine cavity, during the estrogen-dominant phase of the menstrual cycle. This would normally be reversed during the subsequent progesterone-dominant phase. However, if this reversal process is defective, organization of this material can occur, which can lead to initially incomplete and then complete tubal obstruction. Tubal wall damage does not normally exist in these cases. This sequence of events is supported by our experience in transcervical tubal cannulation. Flushing and/or guide-wiring the tubes can re-establish tubal patency and fertility. The tubal perfusion pressure, assessed during transcervical tubal cannulation procedures, can serve as a marker of the severity of PTB and the success of recanalization.

Key words: proximal tubal blockage/selective salpingography/tubal catheterization/tubal perfusion pressures


    Introduction
 Top
 Abstract
 Introduction
 Anatomy
 Physiology
 Pathology
 An hypothesis for the...
 Conclusions
 References
 
The diagnosis of proximal tubal blockage (PTB), in most clinical settings, is still seen as an indication for either IVF treatment or tubal surgery. This is despite the substantial body of evidence that exists for the effectiveness of selective salpingography and tubal catheterization (SS/TC) in recanalizing the proximally occluded oviduct and restoring fertility for women diagnosed with PTB (Thurmond and Rosch, 1990Go; Gleicher et al., 1992Go; Woolcott et al., 1995Go; Lang and Dunaway, 1996Go). The endorsement of SS/TC by influential professional bodies (American Fertility Society, 1993Go; Royal College of Obstetricians and Gynaecologists, 1998Go) has yet to make an impact in routine clinical practice.

The incidence of PTB is believed to be in the range of 10–25% of the total number of infertile women with tubal disease (Sulak et al., 1987Go; Thurmond, 1991Go; Honore et al., 1999Go). This relatively low incidence may partly explain the reluctance of many clinicians to invest time and money in acquiring the skills necessary to perform SS/TC and developing a relevant service. Safety considerations, in relation to the irradiation of the ovaries of reproductive age women when fluoroscopic guidance is used, as well as the perception of SS/TC as a technically difficult procedure, may also limit the attractiveness of the technique to a wider clinical body. These issues have been addressed by our group in previous publications, with reassuring results (Papaioannou et al., 2002aGo; dGo).

In addition, PTB is a poorly understood clinical and pathological entity. The fact that in many cases PTB is caused by plugs of amorphous material that occlude the tubal lumen without the presence of any tubal wall damage (Sulak et al., 1987Go) has not been fully appreciated. The mechanisms of formation, as well as the natural history of such plugs, are unknown. In this paper, the anatomy, physiology and pathology of the intramural segment of the Fallopian tube are briefly reviewed. Based on evidence from these disciplines, an hypothesis to explain the pathogenesis and describe the natural history of PTB caused by plugs of amorphous material is proposed. Other conditions (e.g. infection, polyps) that can cause PTB are either not discussed, or are mentioned only in relation to the proposed hypothesis (e.g. endometriosis, salpingitis isthmica nodosa).


    Anatomy
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 Introduction
 Anatomy
 Physiology
 Pathology
 An hypothesis for the...
 Conclusions
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For a long time, the course of the intramural fallopian tube has been a contentious issue. Lisa et al. (1954)Go, based on the study of fixed hysterectomy specimens, suggested that the intramural segment is straight, with a length of 1 cm or less in almost all cases. This view was universally accepted until Sweeney (1962)Go described the course of the intramural tube in 50 uteruses (100 tubes) that were dissected after hysterectomy but before fixation. He found it to be tortuous in the majority of cases, with a length of between 1 and 3.5 cm, depending on the exact course of the intramural segment. Sweeney concluded that, given its tortuous course, probing or catheterizing the proximal tube was practically impossible and potentially damaging, a view that remained authoritative for a number of years. The intramural tubal lumen caliber has been reported to be as narrow as 0.1 mm (Rocker, 1964Go). Even after the first successful attempts at transcervical tubal catheterization had been published (Platia and Krudy, 1985Go; Confino et al., 1986Go), Sweeney’s pessimism was still conveyed in a critical editorial, in which over-enthusiastic investigators are cautioned about the narrow and tortuous nature of the intramural oviduct and the harm that transcervical cannulation procedures might cause (DeCherney, 1987Go).

However, work with Falloposcopy has since shown that in the majority of cases the course of the intramural segment in vivo is, at least for instrumentation purposes, gently curved or straight. A cannula of 1–1.2 mm in diameter can be accommodated, without causing any damage (Kerin et al., 1990Go). The tortuous course and narrow diameter described in ex vivo specimens were artifacts created by myometrial contraction.

In addition to its course, the presence or absence in the intramural segment of a sphincteric mechanism, which would regulate its conflicting functions, has also been the subject of controversy (Andersen, 1928Go; Ueno, 1933Go; Lisa et al., 1954Go). On one hand, the sphincter would isolate the tubal lumen from the uterine cavity, thus protecting the peritoneal cavity from contamination ascending from the vagina. On the other hand, it would permit or even encourage the passage of the fertilized ovum in the direction of the uterus and the passage of spermatozoa in the opposite direction. However, it is clear today that a sphincteric mechanism analogous to those present elsewhere in the body (e.g. anal, urethral sphincter), marked by true circumferential muscle fibres with a dedicated nerve supply, does not exist in the Fallopian tube (Hershlag et al., 1989Go). Although close apposition between myosaplingeal fibres has been shown, cell-to-cell contacts fulfilling the criteria of ‘gap junctions’ (the electrical synapses between muscle cells that allow them to contract in coordination) have not been demonstrated (Lindblom and Norstrom, 1986Go).


    Physiology
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 Anatomy
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 An hypothesis for the...
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Changes in the concentrations of estrogen and progesterone induce motility changes of the uterotubal junction (UTJ) mediated by adrenergic nerve activity (Hershlag et al., 1989Go). A differential distribution of alpha and beta adrenoreceptors has been found in the musculature of the human UTJ. The submucosal and middle muscle layers express mainly beta receptors, while the subperitoneal layer expresses predominantly alpha receptors (Wilhelmsson and Lindblom, 1980Go). In the rabbit model, estrogen activates the alpha adrenergic receptors, reducing transisthmic flow, whereas beta adrenoreceptor stimulation by progesterone markedly increases transisthmic flow (Strom et al., 1983Go). Hence, stimulation of the outer layers of the UTJ during the phase of estogenic dominance can cause muscle spasm, while the inhibitory response of progesterone at 4–6 days after ovulation may relax the tubal musculature (Korenaga and Kadota, 1981Go).

Cilial activity in the Fallopian tube is also influenced by the hormonal changes of the menstrual cycle. During the proliferative phase, the cilia beat less frequently than following ovulation (Critoph and Dennis, 1977Go; Lyons et al., 2002Go). Furthermore, there is a decrease of the proportion of ciliated cells along the tube, the lowest being in the intramural region (Hershlag, 1989Go; Crow et al., 1994Go). The direction of tubal cilial movement is believed to be towards the peritoneal cavity in the follicular/periovulatory phase and towards the uterus in the luteal phase, although this is still the subject of debate (Gaddum-Rose et al., 1973Go; Westrom et al., 1977Go). In addition, during the late proliferative phase and for a short period after ovulation, a column of tenacious mucus in the isthmic lumen has been described (Jansen, 1980Go). It is thought that this mucus column provides a medium for sperm transport, at the same time protecting the sperm from ciliary activity that might hinder its progression towards the ampulla.


    Pathology
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 Anatomy
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 Pathology
 An hypothesis for the...
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The not uncommon inability to demonstrate histologically the occlusion in tubal segments excised because of PTB, despite blockage being confirmed more than once before surgery, has been described as frustrating for both patients and surgeons (Siegler and Hellman, 1963Go; Grant, 1971Go; Rock et al., 1979Go). A possible explanation of this phenomenon was offered by Sulak et al. (1987)Go. They reported the identification of amorphous material forming a cast in the tubal lumen in 33% of women that underwent segmental tubal resection because of PTB. All of these had the diagnosis made preoperatively by both hysterosalpingography (HSG) and laparoscopy, and dye test, and the blockage was further confirmed during surgery. The existence of such intraluminal debri was later confirmed by Falloposcopy (Kerin et al., 1991Go).

The significance of this concept of PTB, being, in a significant number of cases, not the consequence of structural tubal damage but rather the result of intraluminal tubal plugs, cannot be over-emphasized. For the first time it offered a possible explanation for the lack of any demonstrable pathology in many tubal segments resected because of PTB, as such plugs may easily be dislodged and missed at the time of pathological examination. It also suggested that tubal resection itself in such cases, far from representing over-treatment, might even convert a ‘normal’ oviduct into a scarred one.

An important consideration in a discussion about PTB is its intermittent presence. In some cases, PTB, despite being present on an initial tubal patency test, cannot be demonstrated on the next. Tubal spasm is considered by most to be an expression of normal UTJ function or a physiological response to uterine distention during diagnostic procedures. However, evidence to the contrary was provided by Gleicher and colleagues. Women who had PTB confirmed on both an HSG and laparoscopy, and dye test, but who were later found to have patent Fallopian tubes on a subsequent HSG or SS were prospectively followed up. No infertility treatment was administered, as the initial diagnosis of PTB was attributed to tubal spasm. The pregnancy rate in this group of women was poor (Gleicher et al., 1993Go). Furthermore, tubal perfusion pressures measured during SS in women diagnosed with tubal spasm were found, with few exceptions, to be elevated. There is therefore a possibility that intermittent tubal blockage, in the absence of technical failure, is not a normal physiological variation (Gleicher and Karande, 1996Go).


    An hypothesis for the pathogenesis and natural history of PTB
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 Abstract
 Introduction
 Anatomy
 Physiology
 Pathology
 An hypothesis for the...
 Conclusions
 References
 
The absence of a sphincteric mechanism in the intramural tubal segment, in combination with its straight course, mean that backflow of material from the uterus into the tube is possible. Retrograde menstruation has been documented as a physiological event in menstruating women with patent tubes (Halme et al., 1984Go). Indeed, it has been one of the theories proposed to explain the pathogenesis of peritoneal endometriosis. It is also possible that uterine cavity contents could backflow into the Fallopian tubes during other phases of the menstrual cycle.

During the estrogen-dominant phase of the cycle, increased muscle tone, reduced ciliary activity and increased tubal secretions at the UTJ, and to a certain extent the isthmus, can result in stasis of the tubal luminal contents and functional obstruction of the proximal tube. The biological purpose of this event may be the delay of the zygote in the ampulla for the first few days post-conception, where the environment is optimal for its nutrition and development. This functional proximal tube obstruction should normally be reversed during the progesterone-dominant phase of the menstrual cycle, as there is then relaxation of the UTJ musculature, increased cilial activity and a reduction in tubal secretions. As the progesterone concentration increases towards its peak a few days following ovulation, the zygote can enter the isthmus and the uterine cavity at a time when the hormonal circumstances for its progression, implantation and growth are favourable. If for some reason the functional obstruction is not reversed, prolonged stasis of uterine material and tubal secretions at this site would result. This, especially if repetitive, could in turn result in organization of this material, and, therefore, initially partial and then, given time, complete anatomical obstruction of the narrow intramural tubal lumen. Calcification of the obstructing material can follow (Kerin et al., 1991Go). Finally, fibrosis occurs, which represents a non-specific final response of the intramural tube to chronic injury (Fortier and Haney, 1985Go), following which tubal damage has become irreversible.

Endometriosis or salpingitis isthmica nodosa might predispose to the development of this process in the first place and/or to its faster progression. Tubal endometriosis has been demonstrated histologically in 14.3% of tubal segments that were resected because of PTB, and can be present even without laparoscopically visible peritoneal disease (Fortier and Haney, 1985Go). The cyclical swelling of endometriosis deposits inside the proximal tube in response to the cyclical estrogen and progesterone changes, if not sufficient to cause obstruction on its own, may make the resolution of the physiological functional obstruction described above lengthier. Elevated tubal perfusion pressures during SS/TC have been shown to be highly suggestive of tubal endometriosis (Karande et al., 1995Go). They may signify partial (proximal) tubal obstruction, a condition that at the moment is hypothetical as measurement of tubal perfusion pressure (TPP) is an underutilized diagnostic tool. Salpingitis isthmica nodosa has been identified in 7–25% of patients seeking treatment for PTB (Fortier and Haney, 1985Go; Thurmond et al., 1988Go).

With currently used diagnostic tests (HSG and laparoscopy, and dye), the observation of tubal spasm may be the first clinically detectable sign of the process described here. PTB at this stage is still partial or not established, and is only sometimes demonstrable. This would depend on the degree of the obstruction, the quality of the obstructing material, the condition of the contralateral tube and on technical factors (adequacy of cervical seal, level of intrauterine pressure achieved). At an early stage, PTB may be curable by simply flushing the Fallopian tubes with contrast medium or dye. Hence, the failure to demonstrate the condition during a tubal patency test when PTB has been observed before might only be due to the fact that the second test itself was therapeutic. The observation that the natural conception rate following HSG is higher than the ‘spontaneous cure rate’ of infertility (at least when oil-soluble media are used) would lend support to this view (Vanderckhove et al., 2001Go). It can be argued that the direct injection of contrast medium into the Fallopian tube itself, as is the case during SS, would be a more specific diagnostic/therapeutic approach. Guide-wire tubal catheterization can be used when persistent blockage or high TPPs are encountered. This intervention, when successful in recanalizing the tube and lowering the TPP, can be expected to improve pregnancy rates, at least for some women. In addition, the degree of TPP reduction in these cases would quantify the treatment effect in the form of a variable with prognostic significance (Papaioannou et al., 2002bGo).

The pathophysiological mechanisms that produce PTB in the first place probably predispose these women to its reoccurrence following successful anatomical (unblocking of tubes with PTB) or functional (reduction of elevated TPPs) recanalization. Nevertheless, conception rates during the first 4 years follow-up following SS/TC are not significantly affected (Papaioannou et al., 2002cGo). If, however, proximal tubal blockage does reoccur, a repeat SS/TC can be successfully attempted (Thurmond and Rosch, 1990Go; Lang and Dunaway, 1996Go), and spontaneous conceptions and live births have been documented for these woman after each procedure (Motta et al., 1995Go).

The observation that GnRH analogue treatment can be beneficial in the management of PTB lends further support to the suggested chain of events. Women diagnosed with PTB and treated with GnRH analogues showed, in a small, prospective, randomized, placebo-controlled trial, a trend toward higher post-therapy patency rates in comparison with a control group of women that did not receive GnRH treatment (Surrey et al., 2000Go). Women with PTB show a marked improvement in the ease of passage of the Falloposcopy catheter following GnRH therapy (Wiedemann et al., 1996Go). Of course, suppression of intratubal endometriosis could be an explanation of this finding. Another explanation may be that the suppression by GnRH analogues of the cyclical changes of estrogen and progesterone would give time to the inherent proximal tube clearing mechanisms to clear its lumen from any obstructing material, where this has not yet been organized.

Further research is necessary to test the accuracy of the proposed hypothesis. If the cycle of tubal functional obstruction and then reversal, in synchronicity with ovarian steroid production as described, reflects a reproductive reality then the TPPs during the phase of estrogen dominance should on average be higher than measurements during the phase of progesterone dominance. In addition, if disruption of this cyclicity represents a source of reproductive delay, then TPPs of fertile women, or women who experience infertility due to male factor, should on average be lower than those of women with unexplained (or not yet explained) infertility. Where waiting lists for treatment exist, comparing the rates of spontaneous conceptions in infertile women with PTB while on the waiting list for assisted reproduction following SS/TC or without it, will offer more insight into the place of this procedure in the management of these patients. Clearly the ethics and practicalities of these need to be thoroughly thought through.


    Conclusions
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 Abstract
 Introduction
 Anatomy
 Physiology
 Pathology
 An hypothesis for the...
 Conclusions
 References
 
As is the case with other body functions (e.g. inflammation, immune reaction), it is possible that the complex mechanisms that are in place to facilitate tubal function can, if a delicate balance of conflicting influences is disrupted, work against their biological purpose. In the case of proximal tubal blockage, anatomical or functional obstruction can be the result of chronic stasis inside the narrow proximal tubal segment. As there is initially no structural damage, this can be relieved by the use of SS/TC. For the purposes of fertility treatment this is adequate in many cases, especially as the length of this process before it becomes irreversible seems to spread over many years.


    References
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Submitted on July 25, 2003; accepted on November 12, 2003.





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