Tubal assessment tests: still have not found what we are looking for

RBMOnline - Vol 15. No 4. 2007 376-382 Reproductive BioMedicine Online; www.rbmonline.com/Article/2792 on web 29 May 2007

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!BSTRACT Interest in tubal assessment is as old as interest in fertility and infertility. The Fallopian tube is a particularly complex structure and, as such, an ideal method for its clinical assessment is very difficult to obtain. As a result, a number of different methods have been suggested. Some of these methods are more complementary to each other rather than potential substitutes for one another. Some have been used for many years with a clear evidence base for their performance as diagnostic tests. For other, relatively new tests, very little evidence about their performance is available. Research is moving from a purely anatomical approach (are the tubes open or blocked?) to encompassing functional enquiry (are the open tubes functional and, if not, are there interventions with which fertility performance can be improved?). The available evidence, or lack thereof, for the most commonly used tubal assessment tests is reviewed in this paper. Many questions remain, which, despite the increasing success of IVF, will continue to challenge and stimulate specialists and the public, who are interested in ways to maximize spontaneous as opposed to assisted fertility. Keywords: dye test, Fallopian tube, hysterosalpingogram, laparoscopy, selective salpingography, tubal assessment

)NTRODUCTION



The Fallopian tube, far from being a passive conduit for gametes and early embryos, plays an important role in many reproductive functions such as sperm transport and capacitation, ova retrieval and transport, fertilization, embryo storage, nourishment and transport. Complex and co-ordinated neuromuscular activity, cilial action and endocrine secretions are required for successful tubal function. It is now known that hydrosalpinges halve IVF treatment success, a reversible effect if excised (Ozmen et al., 2007).

The first reference to the Fallopian tube is recorded in Hindu scriptures of the 9th century BC. Herophilus, Soranus and Galen, 600–1000 years later, began to study anatomy systematically with dissections. They believed however, that the anatomy of the female was analogous with male anatomy and that the Fallopian tubes therefore ended up in the urinary system and did not participate in reproduction. These views remained authoritative for more than 1000 years until Gabrielle Fallopius, at the University of Padua, Italy, recorded the first accurate description of the cradle

© 2007 Published by Reproductive Healthcare Ltd, Duck End Farm, Dry Drayton, Cambridge CB3 8DB, UK

Symposium - Tubal assessment tests - S Papaioannou et al.

of fertilization and gave his name to it forever. It would be another few hundred years before the first attempt to access the Fallopian tube was made with a view to studying or treating infertility. In the quest for the ideal Fallopian tube assessment test, numerous methods have been described (Table 1). The number of different proposals means that none meets all the criteria for the ideal diagnostic test as summarized in Table 2. The performance of the common tubal assessment test against these criteria is examined by presenting the evidence where available. It is important to note that many of these tests are complementary to each other, rather than alternatives to one another, and also that there are significant differences in the evidence base and experience behind them, so the tests should not be seen as equal each other in those terms.

(YSTEROSALPINGOGRAPHY Hysterosalpingography (HSG) is the most common Fallopian tube assessment test. It is performed today in a way almost identical to that described by Carey (1914), a rare survivor in modern medical practice. Oil-soluble contrast media were initially used but they were associated with an increased risk of complications, such as granulomatous changes and fibrosis on the peritoneal surfaces, and have been almost completely replaced by water-soluble radio-opaque dyes. More recent oilsoluble media have been suggested to be as safe; nevertheless, water-based contrast media are still by far the most popular. The safety and low cost of HSG are amongst its attractions. The evidence, in terms of reliability, is also reassuring. A study where four expert observers evaluated the results of 143 HSG

Table 1. Fallopian tube assessment tests. Method of assessment

Reference

Transcervical whalebone tubal catheterisation Laparoscopy Hysterosalpingogram Rubin’s test: tubal perfusion pressures Oxygen Carbon dioxide Dye injections with culdoscentecis Injection of phenolsulphonphthalein which, having been absorbed by the peritoneum if the Fallopian tubes were patent, could then be detected in the urine Injection of radiolabelled xenon solution with gamma-camera screening Selective salpingography and tubal catheterisation Salpingoscopy Falloposcopy Hystercontrast sonography Fertiloscopy

Smith (1849) Jacobaeus (1910), Palmer (1947) Carey (1914) Rubin (1920) Rubin (1952) Decker (1952) Speck (1970)

Pertynski et al. (1977) Corfman and Taylor (1966) Brosens et al. (1987) Kerin et al. (1990a) Deichert (1993) Watrelot et al. (1999)

Table 2. Characteristics of the ideal Fallopian tube assessment test. Characteristic

Definition

Safety Accuracy

The incidence of any short- or long-term complications Extent to which the test measures what is supposed to measure (but what is the ‘gold standard’?) The degree to which repeated use of the test by the same or different examiners on the same patient produces the same result Ability to improve pregnancy rates Ability to inform about the possibility of a post-test pregnancy The total cost of the procedure expressed either in monetary terms or in terms of money per live birth, where such information is available

Reliability (reproducability) Effectiveness (therapeutic potential) Prognostic ability Cost

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Symposium - Tubal assessment tests - S Papaioannou et al.

procedures twice reported that, for the same observer (intraobserver reliability), there was almost perfect agreement for proximal obstruction and substantial agreement for distal obstruction, hydrosalpinx and peritubal adhesions. Between different observers (inter-observer reliability), there was almost perfect agreement for proximal tubal blockage, substantial agreement for distal obstruction and hydrosalpinx and moderate agreement for peritubal adhesions (Mol et al., 1996). Therefore HSG is a reliable test, giving consistent results. But is it accurate? Does it give the right result? In a meta-analysis that included 4000 women, HSG results were compared with the findings of laparoscopy and dye, the accepted gold standard. The results show that HSG is far from a perfect test (Swart et al., 1995). With a sensitivity of 65%, it uncovers tubal pathology in two-thirds of the cases where it exists. But with a specificity of 83%, it is reassuring that if tubal pathology is absent, the HSG will be normal in five out of six women. Therefore, with likelihood ratios for a positive test (sensitivity/1–specificity) of 3.8 and for a negative test (1–sensitivity/specificity) of 0.42, HSG is classified as only a moderately useful test (Richardson et al., 1999). Effectiveness is an important advantage of HSG. A Cochrane review has identified the following improvements in fertility post-HSG with the use of different contrast media: (i) oilsoluble media versus no intervention: statistically significant increase in the odds of live birth (odds ratio (OR) 2.98, 95% CI 1.40–6.37) and pregnancy (OR 3.30, 95% CI 2.00–5.43); (ii) oil-soluble media versus water-soluble media: statistically significant increase in the odds of live birth (OR 1.49, 95% CI 1.05–2.11) and pregnancy (OR 1.24, 95% CI 0.97–1.57); or (iii) water-soluble plus oil-soluble media versus water-soluble media alone, no increase in the odds of live birth (OR 1.06, 95% CI 0.64–1.77) or pregnancy (OR 1.18, 95% CI 0.82–1.70). There are no randomized controlled trial data to assess Fallopian tube flushing with water-soluble media versus no intervention (Johnson et al., 2005). Prognosis is described in terms of adjusted fecundity rate ratios (FRR). These express the spontaneous pregnancy probability for women with a specific feature relative to those without it. When the result of the HSG is one-sided pathology, with a FRR of 0.81 (95% CI 0.47–1.4), the confidence interval (CI) crosses unity and the impact in future fertility is uncertain. If bilateral tubal pathology is identified however, with a FRR of 0.30 (95% CI 0.13–0.71), the result is statistically significant with future fertility predicted to be a third compared with fertility following a normal HSG result. Therefore the demonstration of one-sided pathology at HSG is of uncertain prognostic value (Mol et al., 1997).

(YSTEROSALPINGO CONTRAST SONOGRAPHY



Hysterosalpingo-contrast-sonography (HyCoSy) is a transvaginal ultrasound technique in which a solution of galactose and 1% palmitic acid (Echovist) or a mixture of air and saline is infused into the uterine cavity and observed to flow along the Fallopian tubes to assess tubal patency. The bright echoes generated by the HyCoSy solution make tubal visualisation possible. Results can be further improved by the use of colour Doppler imaging or 3D technology.

HyCoSy is accepted as a safe outpatient procedure with relatively small cost. The accuracy of HyCoSy has been assessed in a meta-analysis, which compared the results of HyCoSy and laparoscopy and dye tests in 428 infertile women. Sensitivity was 93.3% and specificity 89.7%. Therefore likelihood ratios would be nine for a positive HyCoSy (sensitivity/1–specificity) and 0.07 for a negative HyCoSy (1–sensitivity/specificity), making the test moderately useful and very useful, respectively (Holz et al., 1997). As regards HyCoSy reliability, data are only available for agreement between different examiners. Substantial interobserver agreement was found for bilateral and right tubal patency and occlusion, although for left tubal patency and occlusion, inter-observer agreement was found to be only fair. Investigators have postulated that this could have been due to: (i) a true difference in the prevalence in tubal occlusion between right and left in the population examined; (ii) an investigation beginning on the right side and then moving to the left side, with limited time available for the left-side examination; and (iii) right-handedness of the investigator possibly having an effect on the performance of the test (Tekay et al., 1997).

,APAROSCOPYANDDYETEST Laparoscopy and dye (lap and dye) test is used as the gold standard in Fallopian tube testing. In addition to patency testing, the gross external appearance of the Fallopian tube and the fimbrial mucosa can be assessed. The presence, nature and exact position of adhesions can be identified and the peritoneal surfaces can be inspected for evidence of endometriosis. The incidence of such abnormalities in the infertile female population is not negligible. Significant laparoscopic findings have been reported in 60% of women with unexplained infertility (Peterson and Behrman, 1970) and in 38.7% of women attending an infertility clinic (Templeton et al., 1977). Furthermore, when abnormalities are encountered during laparoscopy, treatment during the same procedure is possible. A randomized controlled trial reported that laparoscopic ablation or resection of minimal or mild endometriosis enhances fecundity in infertile women (Marcoux et al., 1997). As the lap and dye test has been used as the gold standard Fallopian tube evaluation test, its evidence base is necessarily deficient. There are no studies to describe its accuracy: what do you compare it with? Nor can its reliability be studied: in other words, you cannot repeat a laparoscopy, other than to measure its intra- and inter-observer reproducibility. Furthermore, women with Fallopian tubes that appear normal on lap and dye and have no other infertility factors may still not conceive, while women with severely damaged Fallopian tubes, for whom IVF treatment is advised, sometimes leave the IVF waiting list and queue for the antenatal clinic. In terms of safety and costs, lap and dye is significantly more risky and expensive than many of the alternatives. The prognostic value of lap and dye is significantly better than that of HSG. Adjusted FRR are, for unilateral tubal occlusion 0.65 (95% CI 0.40–0.85), meaning that future fertility is reduced by a third, and for bilateral tubal occlusion 0.2 (95% CI 0.10- 0.35), a reduction of four-fifths. The observation of hydrosalpinges at lap and dye has a slightly better fertility

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Symposium - Tubal assessment tests - S Papaioannou et al.

prognosis than the observation of tubal occlusion with adjusted FRR of 0.46 (95% CI 0.28–0.60) and 0.32 (95% CI 0.20– 0.53) for unilateral and bilateral hydrosalpinx respectively. Surprisingly, the presence of peritubal adhesions was not found to influence future fertility (Mol et al., 1999). It is noteworthy that most of the work on the performance of HSG and lap and dye has been done by the same group in Holland. The group has taken a particular interest in this subject and their work has only been published within the last 12 years, although these methods have been used for a lot longer: a witness to the difficulties in the study of the performance of diagnostic tests.

3ELECTIVESALPINGOGRAPHYANDTUBAL CATHETERISATION There are a number of reasons why the proximal Fallopian tube should be considered as a different organ than the distal Fallopian tube (Table 3). Selective salpingography and tubal catheterisation (SSTC) is a transvaginal outpatient procedure, recommended specifically for the diagnosis and treatment of proximal tubal blockage (National Institute for Health and Clinical Excellence, 2004). There is no technical reason however, and there may be some advantages, in using the method as a first-line screening tubal test that also provides the opportunity to treat proximal tubal blockage at the same time (Papaioannou et al., 2003a). Selective salpingography performs well regarding safety. The most common complication is tubal perforation, reported in about 5% of cases. However no treatment is necessary. An ectopic pregnancy has been reported in 5% of the cases. Infection is very rare if screening or routine prophylaxis are implemented (Thurmond et al., 2000). One might understandably be concerned about the longer irradiation of the ovaries and the probable long-term risks of carcinogenesis and hereditary disorders. However the available data are reassuring (Papaioannou et al., 2002a). The only randomized controlled trial that reported on the accuracy of SSTC, by comparing the findings of selective salpingography and lap and dye, concluded in a draw. It found that SSTC was a better test for the ascertainment of proximal tubal blockage. There was no difference between the two tests as regards distal tubal occlusion. Lap and dye was better for the

detection of peritubal adhesions, results that would have been expected (Woolcott et al., 1999). There are no data concerning the reliability of the method. SSTC provides the examiner with the opportunity to measure tubal perfusion pressures, which have been found by lifetable analysis to be prognostic of future spontaneous fertility (Papaioannou et al., 2002b, 2003b). There are data about the relative cost of SSTC as a proximal tubal blockage treatment procedure. The cost per live birth is less with SSTC (US$6400) compared to IVF (US$12,000) or tubal surgery (US$17,000) (Lang and Dunaway, 1996). Tubal spasm has been considered by many as the only basis of proximal tubal blockage, a physiological variation of proximal tube function. The available evidence would be against these assumptions however. There is a group of infertile women for whom proximal tubal blockage is consistently demonstrated in successive tubal assessment tests. In some cases, partial tubal atresia has been documented (Nawroth et al., 2006). The pregnancy rates of women diagnosed with tubal spasm and followed up prospectively without receiving any treatment are much lower than would be expected for fertile women and as documented for women with proximal tubal blockage treated with SSTC (Confino et al., 1990; Gleicher et al., 1994).

3ALPINGOSCOPY Salpingoscopy was originally performed during laparotomy for reconstructive tubal surgery to assess the mucosa of the infundibulum and ampulla. A flexible bronchoscope was initially used with improved images obtained by the introduction of a dedicated rigid salpingoscope. Atraumatic grasping forceps are applied just behind the fimbriae to hold the tubal wall against the sheath of the salpingoscope, while an infusion of distending medium is instilled to open up the potential space of the tubal lumen. Prediction of fertility outcome by laparoscopy can be improved by the concomitant performance of salpingoscopy (Marchino et al., 2001). The two tests probably complement rather substitute one another. There is no information about accuracy, reliability, prognosis and effectiveness. Special equipment and expertise are required, making salpingoscopy an expensive proposition. As it is performed during laparoscopy, its risk profile is comparable.

Table 3. Differences between proximal and distal Fallopian tubes. Proximal

Distal

Short Narrow lumen (1 mm) Can be tortuous Muscular Few ciliated and many secretory epithelial cells Prone to amorphous material, salpingitis isthmica nodosa, endometriosis, polyps

Long Wide lumen (1 cm) Straight Not muscular Many ciliated and few secretory epithelial cells Prone to infection

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Salpingoscopy was the first tubal assessment test that disclosed a new world of detailed in-vivo images of the actual site of human fertilization. It can clearly demonstrate the presence or absence of anatomical distortions, especially adhesions between and destruction of mucosal folds on a micro-endoscopic, i.e. mucosal, level. Its proponents argued that salpingoscopy could and should direct the infertility investigation and treatment care pathway, either towards reconstructive (micro)surgery or towards assisted reproduction technologies. Lesions of the infundibulum and ampullary segment have been detected in patients with apparently normal tubes on HSG and laparoscopy (Puttemans et al., 1987). However, although the presence of ampullary mucosal adhesions has been reported to negatively affect fertility and increase the risk of an ectopic pregnancy, mucosal adhesions are not incompatible with normal fertility (Maguiness and Djahanbakhch, 1992) and, unless the damage is severe, there is poor correlation with histological assessment (Hershlag et al., 1991). Therefore, not enough is known about these lesions and salpingoscopy remains a research tool. As an alternative to salpingoscopy performed during laparoscopy, salpingoscopy performed during transvaginal hydrolaparoscopy, as an office procedure, has been described as part of fertiloscopy.

&ALLOPOSCOPY Falloposcopy is defined as microendoscopy of the oviductal lumen from the uterotubal ostium to the fimbriae by a transcervical approach (Kerin et al., 1990b). At first, the technique involved the passage into the tubal lumen, under hysteroscopic vision, of a flexible cannula, into which the falloposcope was introduced. The procedure is carried out with the help of continuous fluid irrigation through the flexible cannula (coaxial delivery system). More recently a miniature tubular balloon system has been described that is rolled out, along the Fallopian tube lumen, by the use of hydraulic pressure, carrying at the same time the falloposcope forward (linear eversion system). This can be used without the aid of hysteroscopy in the non-anaesthetised woman with little or no sedation. However the instruments used are expensive and sensitive. As with salpingoscopy, there is no information about accuracy, reliability, prognosis and effectiveness. Despite initial enthusiasm, falloposcopy has not come into widespread usage. Even in expert hands, technical difficulties are not uncommon with falloposcopy. In the multicentre study reported by Rimbach, 43% of women examined did not receive a complete falloposcopic assessment due to instrument damage or light reflections that obscure visibility (Rimbach et al., 2001). As with salpingoscopy, falloposcopy findings have been associated with fertility prognosis (Kerin et al., 1992). Again there is uncertainty about the exact significance of these findings and whether such findings are present in fertile women. Another difficulty with these results is that they are being generated from dedicated units. It is not known if the same results would be reproduced from non-experts in these methods. Falloposcopy has to be described as a research tool abandoned by many due to the poor quality of images obtained.

4RANSVAGINALHYDROLAPAROSCOPY FERTILOSCOPY Fertiloscopy, performed under local anaesthesia or sedation, is an all in one outpatient assessment of the female reproductive system. Its advocates would add that is complete. Two introducers are used: one, into the pouch of Douglas, is fitted with a balloon that, once it is inflated, prevents the introducer escaping from the pelvic cavity. Prewarmed Ringer’s lactate is used as a distension medium. This enables transvaginal hydrolaparoscopy (telescope up to 4 mm diameter), salpingoscopy (same telescope) as well as therapeutic procedures via the operating channel (5 French). The other introducer is inserted into the uterine cavity and permits dyetesting and hysteroscopy (telescope up to 2.9 mm diameter). Microsalpingoscopy is routinely performed. Using the enlargement lens of the telescope, it allows the cells of the tubal mucosa to be examined following the dye test. Staining of the tubal cell nuclei provides a means of assessing the functional capacity of the Fallopian tubes: the more coloured the nuclei, the less functioning is the mucosa (Watrelot et al., 2002). As the transvaginal route offers easy access to the tubes, ovaries and fossa ovarica, some operative procedures are possible. However, in the absence of a panoramic view, these will be limited to minor interventions (Gordts et al., 2005). Fertiloscopy accuracy was assessed in a multicentre study of 92 infertile women who underwent fertiloscopy first, followed by lap and dye. The sensitivity of fertiloscopy was 86%. Agreement between the two methods was almost complete. The authors commented that fertiloscopy could replace laparoscopy as a routine procedure in such women (Watrelot et al., 2003). In terms of reliability, the inter-observer (between observers) agreement for tubo-ovarian adhesions at transvaginal hydrolaparoscopy has been reported at 95%, comparable to that of standard laparoscopy (Campo et al., 1999). The prognostic value of the method was assessed in a series of 272 infertile women. The adjusted fecundity rate ratios for one-sided tubal pathology, two-sided tubal pathology and adhesions/endometriosis were 0.59, 0 and 0.80, respectively: numbers comparable with the ones for lap and dye (van Tetering et al., 2007). Complications occurred in 2% of cases. The visual analogue scale scores showed pain to be limited and the procedure to be acceptable in terms of safety.

#ONCLUSIONS In an ideal world, the answer to the question about the optimum tubal assessment test would be the result of simply filling in the boxes in a table similar to Table 4. After agreeing about the relative weight, safety, accuracy, effectiveness and so on that each test should have, there would be a visible objective result to go by. However, most of the boxes are still unfilled. The evidence base is good for the older tests, HSG and lap and dye, which is why these are recommended by the UK National Institute for Health and Clinical Excellence (NICE) (2004). Even given the numbers required for conclusive randomized studies to be performed, and the ethical uncertainties that such research would arouse, it would be surprising if the next edition of the NICE guideline would be much different from the current one.

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Symposium - Tubal assessment tests - S Papaioannou et al.

Table 4. Characteristics of currently available tubal assessment tests. Test

HSG Laparoscopy and dye test HyCoSy SSTC Salpingoscopy Falloposcopy Fertiloscopy

Characteristic Safety Accuracy Reliability Effectiveness

Prognostic Low ability cost

+ –

– +

+ ?

+ ?

– +

+ –

+ + ? ? ?

+ + ? ? ?

+ ? ? ? ?

? ? ? ? ?

? + ? ? ?

+ + ? ? ?

+ = positive; – = negative; ? = unknown. HSG = hysterosalpingography; HyCoSy = hysterosalpingo-contrast-sonography; SSTC = selective salpingography and tubal catheterisation.

In assessing the tubal assessment tests, the complexities of tubal function and the fact that these are not adequately described by flushing liquids through the tubes, should be taken into account. In a sense, simple patency of the tube might give false reassurance for women with tubes that might be open, as simple pipes that conduct fluid, but not necessarily functional as far as eggs and sperm are concerned. There is little evidence to support this, nevertheless, it needs to be accepted that there is a lot more to Fallopian tube assessment than HSG and lap and dye tests. The fact that these are the methods mainly prescribed in guidelines should not make us think they are perfect. On the contrary, the evidence of their imperfections is significant.

2EFERENCES Brosens I, Boeckx W, Delattin P et al. 1987 Salpingoscopy: a new pre-operative diagnostic tool in tubal infertility. British Journal of Obstetrics and Gynaecology 94, 768–773. Campo R, Gordts S, Rombauts L, Brosens I 1999 Diagnostic accuracy of transvaginal hydrolaparoscopy in infertility. Fertility and Sterility 71, 1157–1169. Carey WH 1914 Note on the determination of patency of fallopian tubes by the use of Cillargol and X-ray shadow. American Journal of Obstetric Diseases in Women and Children 69, 462. Confino E, Tur-Kaspa I, DeCherney A et al. 1990 Transcervical balloon tuboplasty. A multicenter study. Journal of the American Medical Association 264, 2079–2082. Corfman PA, Taylor HC Jr 1966 An instrument for transcervical treatment of the oviducts and uterine cornua. Obstetrics and Gynecology 27, 880–884. Decker A 1952 Culdoscopy. WB Saunders Co, Philadelphia. Deichert U 1993 [Contrast hysterosalpingography (or HyCoSy)]. Contraception, Fertilité, Sexualité 21, 213–216. Gleicher N, Karande V, Rabin D, Pratt D 1994 ‘Benign’ tubal spasm? Fertility and Sterility 62, 427–428. Gordts S, Puttemans P, Gordts S et al. 2005 Transvaginal laparoscopy. Best Practice and Research in Clinical Obstetrics and Gynaecology 19, 757–767. Hershlag A, Seifer DB, Carcangiu ML et al. 1991 Salpingoscopy: light microscopic and electron microscopic correlations. Obstetrics and Gynecology 77, 399–405. Holz K, Becker R, Schurmann R 1997 Ultrasound in the investigation of tubal patency. A meta-analysis of three comparative studies of

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