The mechanism of hydrosalpinx in embryo implantation

Osnat Eytan1,4, Fuad Azem2, Ilan Gull1, Igal Wolman1, David Elad3 and Ariel J. Jaffa1

1 Ultrasound Unit in Obstetrics and Gynecology, Lis Maternity Hospital, Tel-Aviv Sourasky Medical Center, Tel-Aviv 64239, 2 Sara Racine IVF Unit, Lis Maternity Hospital, Tel-Aviv Sourasky Medical Center, Tel-Aviv 64239 and 3 Department of Biomedical Engineering, Faculty of Engineering, Tel-Aviv University, Tel-Aviv 69978, Israel


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
BACKGROUND: Hydrosalpinx adversely affects embryo implantation and contributes to poor implantation rates post embryo transfer. Embryo transport depends on concomitant intrauterine fluid motion induced by uterine wall motility, the result of spontaneous myometrial contractions towards the fundus. METHODS AND RESULTS: The uterine dynamics of five patients with hydrosalpinx were recorded and analysed by image-processing techniques: the frequency was higher while the amplitudes and passive widths were lower compared with healthy volunteers. The existing peristaltic activity should have induced intrauterine fluid flow; however, the recordings failed to show the expected transport of fluid bolus. This observation was supported by mathematical simulations based on the hypothesis that fluid accumulation in the Fallopian tube of a patient with hydrosalpinx increases tubal pressure and thereby induces a pressure gradient between the fundus and the cervix. This pressure gradient acts adversely to the cervix-to-fundus intrauterine peristalsis and generates reflux currents that may thrust embryos away from the implantation site. CONCLUSIONS: The reflux phenomenon could explain the reduced implantation rate associated with hydrosalpinx. Resolution of the issue of whether the removal of a Fallopian tube with hydrosalpinx should be undertaken for improving IVF pregnancy rates should be accompanied by prospective randomized clinical trials.

Key words: hydrosalpinx/pressure/reflux/simulation/uterine contractions


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
In-vitro fertilization (IVF) was originally developed to overcome the impediment created by tubal obstruction that prevents spermatozoa–oocyte mating in vivo. Hydrosalpinx is a tubal pathology in which oviductal fluid is accumulated in the ampullar lumen as a result of occlusion of the infundibulum (Harper, 1994Go). It results in a lower rate of embryo implantation after embryo transfer compared with other tubal diseases (Anderson et al., 1994; Strandell et al., 1994Go; Fleming and Hull, 1996Go; Katz et al., 1996Go; De Wit et al., 1998Go), and bilateral hydrosalpinx yields about one-half the rate of implantation of the unilateral form (Wainer et al., 1997Go). The more extensive the hydrosalpinx, the lower the implantation rates (De Wit et al., 1998Go). Aspiration of the hydrosalpinx fluid prior to an IVF procedure slightly increased implantation rates (Sowter et al., 1997Go) even though the hydrosalpinx fluid itself does not have a toxic effect on the embryo (Sawin et al., 1997; Granot et al., 1998Go; Strandell et al., 1998Go; Spandorfer et al., 1999Go). Indeed, implantation rates were improved after surgical treatment, and were significantly better after salpingectomy (Kassabji et al., 1994Go; Sharara and McClamrock, 1997Go; Dechaud et al., 1998Go; Murray et al., 1998Go; Bredkjaer et al., 1999Go; Strandell et al., 1999Go).

The hypothesis of the current study is that accumulation of tubal fluid in the Fallopian tube of a patient with hydrosalpinx increases tubal pressure and thereby induces a pressure gradient between the utero–tubal junction and the uterine os. This pressure is in a direction opposite to cervix-to-fundus myometrial contractions which normally induce intrauterine peristaltic fluid motions that push the embryo to a fundal implantation site (Fanchin et al., 1998Go; Ijland et al., 1999Go). This adverse pressure gradient may induce fluid reflux (Shapiro et al., 1969Go) and create a mechanical obstacle to pre-implantation embryo motion towards the site of implantation in patients with hydrosalpinx.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
To explore the above hypothesis and its ability to explain the low rate of embryo implantation of patients with hydrosalpinx, we examined several features of the uterine activity in these patients by means of transvaginal ultrasound (TVUS) imaging and conducted mathematical simulations of these phenomena.

In-vivo uterine motility
Patients
Five patients with hydrosalpinx (mean age 29.6 years, range 26–35) on days 10–17 of their menstrual cycle participated in the study. The hydrosalpinx was diagnosed and documented by hysterosalpingography, laparoscopy, and ultrasonography. Four patients had unilateral hydrosalpinx and one had bilateral hydrosalpinx. In this study only patients without fluid accumulation in the uterine cavity were included. The findings of this group were compared with a group of 25 healthy women who were evaluated in an earlier study (Eytan et al., 2001Go).

Data acquisition
TVUS images of sagittal cross-sections of a non-pregnant uterus were recorded with a digital ultrasound system (Sonoline Elegra, Siemens, Seattle, WA, USA). The sagittal cross-section near the fundus revealed a length of 3–4 cm from the fundus towards the cervix (Figure 1aGo). The images were recorded for 5 min while the patient was lying in a supine position and with the operator holding the probe steady. The images were digitized 1 s apart. The diameter of the Fallopian tube with the hydrosalpinx and the size of the follicles were measured prior to the recording.



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Figure 1. (a) Transvaginal ultrasound image from the recording of the sagittal cross-section of the uterus of a patient with hydrosalpinx. (b) The detected intrauterine fluid-wall interface (FWI) marked on the transvaginal ultrasound images. The arrows indicate the changing width of the uterine cavity at a fixed distance from the fundus at different times.

 
The analysis of uterine motility was performed in two stages. First, the intrauterine fluid-wall interface (FWI) was detected from each TVUS image by an edge-detecting technique (Figure 1bGo). Then, the dynamics of uterine motility (i.e. frequency and amplitude of the intrauterine FWI) were analysed from the variation of the geometry of the intrauterine FWI with time, as observed in consecutive images (Eytan et al., 1999Go,2001Go).

Data analysis
The boundaries of the intrauterine cavity in the sagittal cross-section were analysed by a custom-designed edge-detecting image processing technique (Eytan et al., 1999Go,2001Go). The analysis was performed only in the region containing the uterine cavity, where the borders of the uterine cavity were detected in each image (Figure 1bGo). The borders of the uterine cavity appeared as a narrow channel which changed over time due to myometrial motility. In order to analyse the characteristics of uterine peristalsis, we processed the geometry of the uterine cavity from all the images to evaluate the time variation of the width of the uterine cavity at fixed distances from the fundus.

The dynamic parameters of uterine activity were analysed from the time variations of the width (Figure 2Go). The geometry of the passive intrauterine cavity (i.e. absence of contractions) in the sagittal cross-section was computed by an arithmetic average of the time variations of the width of the uterine cavity at each fixed distance from the fundus. The amplitude was defined by the difference between the peaks and the passive width. The frequency of uterine wall motility at fixed distances from the fundus was derived by means of a fast Fourier transform.



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Figure 2. An example of the time variation of the width of the uterine cavity that was analysed from the fluid-wall interface of all processed images (Figure 1bGo) at a distance of 4 mm from the fundus. The amplitude and the ‘passive’ width are demonstrated.

 
Mathematical Simulation
The intrauterine fluid motion in patients with hydrosalpinx was simulated by the pulsatile two-dimensional (2D) model developed by our group and described in detail elsewhere (Eytan and Elad, 1999Go). The dynamic geometry of the uterine cavity is simulated by a finite, uniform 2D channel (Figure 3Go). Fluid motion within the channel is induced by two rhythmic wall displacements that were simulated by an infinite train of sinusoidal waves that propagated along the channel walls. Thus, the time-dependent geometry of the FWI is defined as follows:


Here, 2a is the non-perturbed width of the channel, b is the wave amplitude, {lambda} is the wavelength, t is the time and T is the wave period. Utilization of these boundary conditions along with the fluid conservation equations in a model with parameters suitable for a human uterus provides the intrauterine flow field (Eytan and Elad, 1999Go). We could also compute possible trajectories of massless particles in order to simulate the pre-implantation transport of embryo transport within the uterus.



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Figure 3. (a) Schematic description of a uniform two-dimensional channel with oscillating walls. (b) Schematic description of pressures within the uterus.

 

    Results
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
In-vivo measurements
The dynamic parameters of the intrauterine FWI from TVUS images of patients with hydrosalpinx yielded apparently higher frequencies and lower passive widths and amplitudes compared with healthy women (Table IGo). The results of both groups were not compared with a non-parametric test since the groups were too small to show any differences. The intrauterine fluid flow in the healthy women was demonstrated by changes in the distribution of the echogenic fluid as depicted by white boluses (Figure 4Go). The spatial distribution of the echogenic fluid in patients with hydrosalpinx revealed relatively minor changes in the boluses' position, indicating the likelihood that no intrauterine fluid flow was present. The extent of dilatation of the Fallopian tube due to the accumulation of hydrosalpinx fluid in four patients was 3–5 mm while it was 10.5 mm in one patient (no hydrosalpinx fluid accumulation, however, was detected within the uterine cavity of the latter patient). The diameter of the measured follicles reached 21.3 mm.


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Table I. Dynamics of the studied parameters of the intrauterine fluid-wall interface of spontaneous cycles
 


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Figure 4. Ultrasound of an image of the sagittal cross-section of the uterine cavity. The intrauterine fluid appears white, and the dashed circles illustrate fluid boluses.

 
Intrauterine fluid transport
The transport characteristics of intrauterine fluid were simulated by using the following parameters in a computational model: a = 0.5 mm, b = 0.15 mm, {lambda} = 50 mm and T = 20 s (Eytan and Elad, 1999Go). In order to examine the possible pre-implantation pathways of embryos, we followed the trajectories of massless particles at different sites within the intrauterine fluid. In a normal healthy uterus, we assumed P1–P2 = 0 (Figure 3bGo). Moreover, as a result of wall motility, the particles travelled along curly paths but covered a net axial distance in the direction of the propagated contractions (Figure 5aGo). When an adverse external pressure was developed (P1<P2), the particles still went along curly paths, but some of them were transported in the opposite direction of contraction propagation (Figure 5bGo). As the pressure difference between P2 and P1 exceeded the pressure created by the peristaltic contractions, all the particles were transported against the direction of the contractions (Figure 5cGo). This outcome is similar to a reflux phenomenon wherein the net displacement of a particle per cycle is against the direction of the travelling wave (Shapiro et al., 1969Go) and it starts near the walls and increases as P2–P1 increases (Pozrikidis, 1987Go).



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Figure 5. Trajectories of fluid particles during one period (T) during symmetric contractions when (a) P2–P1 = 2.6 mmHg, (b) P2–P1 = 3.1 mmHg, (c) P2–P1 = 3.38 mmHg. Open/closed circles are initial/final location of the particles.

 
In order to understand the transport of a mass of fluid (assembly of particles) as seen in the TVUS recording, we followed the transport of eight particles that formed an imaginary circular bolus at t = 0 (Figure 6aGo, circles). After the completion of one cycle of contraction (t = 20 s), the bolus was slightly distorted (Figure 6aGo, squares). After two cycles (t = 40 s), the bolus spread over a length of one half of a wavelength (Figure 6aGo, triangles). When the adverse pressure increased slightly (i.e. 3.1 mmHg), the distortion of the bolus decreased (Figure 6bGo) and it remained essentially immobile. It should be noted that the particles are transported over a limited space only, creating an illusion that the bolus is stationary. When the adverse pressure exceeded 3.38 mmHg all the particles within the intrauterine fluid model were transported against the direction of the contractions (Figure 6cGo) and, as a result, the ‘embryo’ would not reach the fundal site for implantation.



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Figure 6. The dynamic expansion of a bolus after a few contractions cycles. (a) A small adverse pressure (2.6 mmHg): the bolus still moves in the direction of the contractions. (b) Increased adverse pressure (3.1 mmHg): the bolus appears to remain in place. (c) When the adverse pressure exceeds the pressure generated by the peristaltic pump (3.38 mmHg), the bolus moves in a direction opposite to that of the contractions. Dots indicate the initial position; squares describe the position after one cycle; triangles describe the position after two cycles.

 

    Discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
This study attempted to theoretically verify the hypothesis that hydrosalpinx induces an increased pressure gradient within the Fallopian tube, thereby creating an adverse pressure gradient between the fundus and the cervix. This adverse pressure difference was in opposition to the peristaltic uterine activity and appeared to create a mechanical effect of reflux which would tend to push embryos towards the cervix and prevent their implantation. The phenomena that involve peristaltic motion, fluid flow and particles are well documented in fluid mechanics (Shapiro et al., 1969Go). Applying them to intrauterine embryo transport sheds light on how this mechanism behaves in the uterus.

During myometrial contraction, the geometry of the uterine cavity changes and induces intrauterine flow. This flow may be visualized in the TVUS recordings of the sagittal cross-section of healthy women by the movements of fluid boluses. The movement of a fluid bolus was barely observable in the TVUS recording of patients with hydrosalpinx, although the uterine dynamics existed. These results mean that the absence of changes in spatial distribution of the echogenic fluid does not necessarily imply that uterine peristalsis is absent. The computational model demonstrates that visualization of a stationary fluid bolus is feasible under peristaltic contractions. It does not imply an impaired peristaltic motion, but rather the presence of adverse pressure. Hence, the paucity of bolus motion in patients with hydrosalpinx could be explained by the presence of adverse pressure having been applied on the uterine cavity.

It may be assumed that the baseline pressure within the uterine cavity and within the Fallopian tubes of healthy women is fairly constant, and that no flow is present in the absence of uterine or oviductal peristaltic activity, thus, P1 = P2 = P3 = P4 (Figure 3bGo). In this case, the intrauterine fluid flow is visible in a TVUS recording, and embryos would be pushed toward the site of implantation at the fundal area when they are transferred into the uterine cavity by IVF.

We postulated that in both unilateral and bilateral hydrosalpinx the pressure in the Fallopian tube (P3 and/or P4) is larger than the intrauterine pressure (P1 = P2). For example, in unilateral hydrosalpinx P1 = P2 = P3 < P4. This adverse pressure is in the opposite direction to that of the peristaltic pumping and may cause reflux (Figure 5Go,b and c). Thus, the boluses of fluid containing the embryos that are transferred into the uterus by an IVF procedure will not be conveyed toward the fundus in the direction of contractions, but will instead be pushed toward the cervix and implantation will not occur. The calculated values of the adverse pressure which ‘hold’ the bolus in place (3–4 mmHg) should be higher within the uterus since the embryo has weight and volume. Nevertheless, the calculated adverse pressure is of the order of the pressure found in the uterine cavity (5–25 mmHg) during the proliferative and secretory phases (Hendricks, 1966Go).

The hypothesis that hydrosalpinx induces internal pressure within the Fallopian tube and thus affects the normal pressure within the uterus can explain the reported observations in the literature. The reflux phenomenon would satisfactorily explain the associated reduced implantation rate (Andersen et al., 1994Go; Strandell et al., 1994Go; Fleming and Hull, 1996Go; Katz et al., 1996Go; Sharara et al., 1996Go; Wainer et al., 1997Go; De Wit et al., 1998Go; Strandell et al., 1999Go) since the embryos would be pushed towards the cervix. The increasing size and extent (unilateral or bilateral) of hydrosalpinx are inversely correlated to the implantation rate (Wainer et al., 1997Go; De Wit et al., 1998Go; Nackley and Muasher, 1998Go): we contend that they probably increase the adverse pressure gradient and thereby increase the refluxed volume of the intrauterine fluid. In cases where the adverse pressure exceeds the pressure created by the uterine peristaltic pump, peristaltic pumping is not effective (Eytan and Elad, 1999Go). This finding may explain the direction of the flow of hydrosalpinx fluid from the Fallopian tube to the uterus and the accumulation of fluid within the uterine cavity during ovarian stimulation and hydrorrhea (Andersen et al., 1996Go; Sharara and McClamrock, 1997Go; Sawin, 1998Go; Strandell et al., 1998Go; Sharara, 1999Go).

The mathematical model used in the current study illustrates that deletion of the adverse pressure removes reflux. Thus, it would be reasonable that the performance of salpingectomy in patients with bilateral hydrosalpinx yielded double the implantation rates of those patients who had no surgical intervention (Strandell et al., 1999Go). Temporary removal of the pressure by surgical fluid drainage prior to IVF was only slightly beneficial to implantation (Sowter et al., 1997Go), probably due to the re-accumulation of the fluid since the pathology remained unchanged. The mechanical effects of hydrosalpinx on implantation warrant further investigation to refine our understanding of them and thus contribute valuable lines of evidence for both resolving the controversial issue of whether to surgically remove Fallopian tubes with hydrosalpinx and for providing new directions in enhancing IVF/embryo transfer pregnancy rates.


    Acknowledgements
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
We thank Mrs Gali Barkan for her assistance in recruiting the patients.


    Notes
 
4 To whom correspondence should be addressed at: Ultrasound Unit in Obstetrics and Gynecology, Lis Maternity Hospital, Tel-Aviv Sourasky Medical Center, 6 Weizmann Street, Tel-Aviv 64239, Israel. E-mail: osnate{at}post.tau.ac.il Back


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
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Submitted on April 26, 2001; accepted on September 6, 2001.