The potential value of tubal perfusion pressures measured during selective salpingography in predicting fertility

Spyros Papaioannou1,5, Masoud Afnan1, Alan J. Girling4, Aravinthan Coomarasamy2, Josephine M. McHugo3 and Khaldoun Sharif1

1 Assisted Conception Unit, 2 Education Resource Center and 3 Department of Radiology, Birmingham Women’s Hospital, Metchley Park Road, Birmingham B15 2TG and 4 School of Mathematics and Statistics, University of Birmingham, Birmingham B15 2TT, UK

5 To whom correspondence should be addressed: 142, Harborne Park Road, Harborne, Birmingham B17 0BS, UK. e-mail:spyrospap{at}talk21.com


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
BACKGROUND: The value of tubal perfusion pressures assessed during selective salpingography and tubal catheterization in predicting fertility has not been investigated. METHODS: A total of 325 infertile women underwent selective salpingography and tubal catheterization. Pregnancy information was collected in 256 (78.7%). The 50th (300 mmHg) and 90th (500 mmHg) centiles of the tubal perfusion pressure distribution in women with normal tubes on selective salpingography were used as thresholds. Women were divided into three tubal perfusion pressure groups: good (both tubes <300, or one tube <300 and the other 300–500 mmHg), mediocre (both tubes 300–500, or one tube <300 and the other >500 mmHg) and poor (both tubes >500, or one tube > 500 and the other 300–500 mmHg). RESULTS: The pregnancy rate in the good perfusion pressure group was significantly higher than that in the poor perfusion pressure group, both when all non-IVF/ICSI first conceptions (P = 0.001) as well as when spontaneous first conceptions only were considered (P = 0.010). The pregnancy rate in the mediocre group lay between the good and the poor groups, though none of the comparisons reached statistical significance. CONCLUSIONS: Selective salpingography can provide additional diagnostic information in comparison with other tubal assessment tests. Tubal perfusion pressures may be predictive of future fertility.

Key words: infertility/selective salpingography/tubal catheterization/tubal perfusion pressures


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Fallopian tube assessment with hysterosalpingography (HSG) or laparoscopy and dye is still synonymous with patency testing. If the tubes were found to be blocked, IVF or tubal surgery would be recommended. If they were patent, intrauterine insemination (IUI) or ovulation induction or even a period of expectant management would be considered. However, the diagnostic accuracy and fertility predictive value of HSG have been criticized (Swart et al., 1995Go; Mol et al., 1999Go). Even laparoscopy, which is considered the optimum method for assessing tubal patency (World Health Organization, 1986), may not determine whether a visualized blockage is due to a temporary cause (e.g. tubal spasm) or whether true anatomical occlusion exists (Flood and Grow, 1993Go; Mol et al., 1999Go).

Selective salpingography and tubal catheterization under fluoroscopic guidance (SS/TC) have been successfully used in the diagnosis and treatment of proximal tubal blockage (Thurmond and Rosch, 1990Go; Capitanio et al., 1991Go; Ferraiolo et al., 1995Go; Lang and Dunaway, 1996Go). With SS/TC, individual Fallopian tubes are assessed and the tubal perfusion pressure (TPP) can be recorded. Patent Fallopian tubes with normal compliance (and therefore normal perfusion pressure) can be differentiated from patent but non-compliant Fallopian tubes (with high perfusion pressure) (Gleicher and Karande, 1996Go).

In a previous paper (Papaioannou et al., 2002aGo) we have shown that in a group of women with high TPP at selective salpingography, TPP reductions achieved by guide-wire tubal catheterization result in an improved fertility prognosis. In the present paper we examine the value of TPP recorded at the end of SS/TC in predicting fertility in a group of unselected infertile women.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Patients
In the 3 year period starting April 1996, TPP measurements were recorded during 325 SS/TC. The mean age at SS/TC (± SD) of the women studied was 32.4 (± 5.2) years. Median duration of infertility at the time of the procedure was 3.25 years (range 0.4–23.4 years). Of these women, 42.6% presented with primary and 57.4% with secondary infertility. In 219 (67.4%) of the cases, SS/TC was performed because of proximal tubal blockage (PTB) previously diagnosed by HSG (32.3%), laparoscopy and dye (15.4%) or both (19.7%). In the remaining 106 (32.6%), the procedure was performed as a first line tubal assessment test, without an HSG or laparoscopy and dye having taken place before. Approval of the local ethics committee was obtained.

Amongst this latter group of 106 women, there were 40 who had normal tubes (as judged by the opacification pattern after SS) and for whom complete TPP data were also available. In this ‘normal tubal status’ group of infertile women, the mean age at SS/TC (± SD) was 32.7 (± 5.2) years, the median duration of infertility was 2.4 years (range 1.1–12.4 years), and 19 (47.5%) presented with primary and 21 (52.5%) with secondary infertility. The 50th (median) and 90th percentiles of the distribution of TPP for this group of women were used as thresholds in a TPP based classification of Fallopian tubes for the whole population studied.

Equipment and technique used
The method used has been described elsewhere (Papaioannou et al., 2002aGo,b,c). In brief, the Fallopotorque (Cook UK, Letchworth, UK) SS/TC catheter system was used. The fluoroscopic unit employed was the mobile Phillips Optimus BV29 with a C-arm system (Phillips Corporation, The Netherlands). SS/TC was performed during the follicular phase of the menstrual cycle. The distal end of the selective salpingography catheter was connected by polyethylene tubing to a syringe pump (KMAR-400; Cook UK) and by means of a three-way stopcock to a pressure-sensitive transducer, which conveyed information to a computer. The pump was activated to flush the catheter with contrast medium and the encountered resistance was displayed as a pressure curve on the computer screen while a hard copy printout could be obtained. Water-soluble contrast medium (Hexabrix 320; Mallinckrodt Medical, Round Spinney, UK) at a constant flow rate of 10 ml/min was used.

Data collection
TPP data were extracted from computer-stored TPP curves (Papaioannou et al., 2002aGo). The final TPP (after SS or after TC if that was performed) for each Fallopian tube was recorded. The maximum TPP value (minus the system background pressure) for each Fallopian tube was used in the analysis. Reproductive outcome was assessed with semi-structured questionnaires sent to women along with pre-paid reply envelopes in August 2000. In January 2001, a second mail-shot was sent to women who had not responded. Subsequently we telephoned those women whose responses were unclear or incomplete as well as non-responders. If the telephone numbers in the patient’s case-notes were inaccurate, their family doctor or the health authority was contacted to identify the patient’s current phone number.

Statistical methods
In the ‘normal tubal status’ group of infertile women, the 10th, 50th (median) and the 90th percentiles of the distribution of TPP were 120, 300 and 500 mmHg respectively. Using the median and 90th centiles from this group as threshold values, Fallopian tubes were classified as follows. L = low pressure if TPP <300 mmHg; I = intermediate pressure if TPP >=300–500 mmHg; H = high pressure if TPP >500 mmHg or absent Fallopian tube (unilateral salpingectomy had been performed in 11 cases). Each subject was then placed, on the basis of the combination of the TPP values from both Fallopian tubes, in one of the following six TPP categories: LL, LI, LH, II, HI and HH. These categories were then combined into three groups: good (categories LL and LI), mediocre (categories LH and II) or poor (categories HI and HH). The three groups were not significantly different in terms of age, duration and type of infertility (primary/secondary), male factor, anovulation and indication for SS/TC (Table I).


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Table I. Patient characteristics in the different tubal perfusion pressure groups
 
Proportional hazards survival analysis was used to evaluate the prognostic significance of TPP, age at SS/TC, duration of infertility at SS/TC, type of infertility (primary or secondary) and presence of male factor, on the time to first conception after SS/TC. Only the woman’s first conception during the study period was considered. Both the Cox model and parametric Weibull model were fitted. Parameter estimates from the Weibull model are presented because of their convenient interpretation as multiplicative factors operating directly on the time to conception (Collett, 1994Go).

At first, only spontaneous conceptions were counted as successes. Conceptions arising after medical intervention were considered as censored at the time of conception. Cases for whom no conception was reported were censored at the time of the mail or telephone follow-up. In a supplementary analysis, the definition of success was extended to include all first conceptions except those arising from IVF or ICSI treatments. Thus, in the supplementary analysis, conceptions resulting from clomiphene citrate, IUI, ovulation induction or donor insemination treatments were also counted as successes.

For the data summary in Table II, total waiting time (TWT) was defined as the total time before success or censoring, summed over all subjects in a group. Average spontaneous conception hazard rate (ASCHR) was defined as the number of successes per year of waiting time with approximate SE—assuming constant within-groups hazard rate—given by ASCHR/v(number of successes). StatView version 5 software (SAS Institute, Inc., 1998) was used for statistical analysis.


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Table II. Unadjusted effect of covariates in the time to first conception after selective salpingography and tubal catheterization (SS/TC)
 

    Results
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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Questionnaires were returned by 225 women while pregnancy information was obtained by telephone interviews in 31 additional cases (total response rate 256 out of 325 women, 78.7%). TPP data were available for 198 (77.3%) of the responders. In the remaining cases, TPP had either not been recorded or not been measured. In total, during the study period, there were 65 spontaneous conceptions, six conceptions resulting from clomiphene citrate treatment, two from ovulation induction, 10 from IUI and two resulting from donor insemination.

Table II summarizes the (unadjusted) effect of the TPP categories, as well as of the other covariates, on time to first conception after SS/TC. The P-values were generated by separate survival analyses of spontaneous conceptions for each covariate. Only TPP category (P = 0.019) and age at SS/TC (P = 0.011) showed statistically significant effects.

The age-adjusted cumulative conception rates for the three TPP groups are shown in Figure 1. The pregnancy rate in the good TPP status group of women was significantly higher than the pregnancy rate in the poor TPP status group, both when all non-IVF/ICSI first conceptions (P = 0.001) as well as when first spontaneous-only conceptions were considered (P = 0.010). The pregnancy rate in the mediocre TPP status group lay between the good and the poor TPP status groups, though none of the comparisons reached statistical significance (mediocre against poor: P = 0.060 and P = 0.124; mediocre against good; P = 0.126 and P = 0.325 respectively). The remaining covariates (duration of infertility at SS/TC, type of infertility and male factor) did not contribute significantly to the model.



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Figure 1. Age-adjusted cumulative conception rates. Solid lines are estimates from the Cox model, dotted lines from the Weibull model, showing good agreement between the two. Estimates are adjusted to the age category <30 years. (A) Survival analysis with only spontaneous conceptions counted as successes. (B) Survival analysis with all but IVF/ICSI first conceptions counted as successes.

 
The numerical effects of changes in TPP status and age groups to the time to first conception are illustrated by the multiplicative factors shown in Table III. These are applicable to the time to first conception of an ideal case, i.e. a woman in the good TPP status group of <30 years of age. For example, a woman <30 years of age but in the poor TPP status group would take on average 3.64 times longer to achieve a spontaneous pregnancy in comparison with the ideal case.


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Table III. Multiplicative factors applicable to time to first conception after selective salpingography and tubal catheterization of a woman in the good tubal perfusion pressure (TPP) group aged <=30 years
 

    Discussion
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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Pressure measurements during uterine insufflation were recorded for the first time (as kymographic traces) by Rubin (1947Go), who used gas (O2 or CO2) insufflation, to test for tubal patency. As HSG became more popular than Rubin’s test, the concept of pressure measurement during Fallopian tube patency testing was neglected for many years.

Perfusion pressures recorded during HSG (using a standardized contrast medium injection system) were found to be a reflection of the Fallopian tube of lesser resistance and therefore of limited value. Normal pressures (<350 mmHg) during HSG could occur despite significant uterine and/or unilateral tubal pathology (Gleicher et al., 1992Go). A possible useful application of such measurements could be to check the technical sufficiency of uterine perfusion during Fallopian tube patency testing. In women with normal tubes, no spill of dye occurs during laparoscopy and dye studies at uterine perfusion pressures of <70 mmHg (Baker and Adamson, 1995Go). Sufficient uterine perfusion pressures are not achieved by all cannula techniques in use (Jessup et al., 1993Go).

In contrast, perfusion pressures recorded during selective salpingography are reflective of the investigated tube only. Fallopian tubes judged to be normal by opacification pattern exhibit a range of TPP, which is significantly lower than that of abnormally appearing oviduct (Gleicher et al., 1992Go). Nevertheless, in many cases, Fallopian tubes judged to be normal on the basis of their opacification patterns alone, have been found by other authors to have high TPP (Gleicher et al., 1992Go; Hilgers and Yeung, 1999Go). This has been our experience as well. Furthermore, in most of these cases the external appearance of the proximal tube at laparoscopy is normal (Hilgers and Yeung, 1999Go). TPP measurement therefore may provide diagnostic information, which cannot be replaced by other tubal assessment tools. High TPP values might indicate intramural abnormalities not detectable with HSG, laparoscopy and dye or selective salpingography alone.

Gleicher et al. (1992Go) felt that normal TPP during selective salpingography lie in the 40–350 mmHg range. Using a different TPP measurement set-up, and in some cases laparoscopy, Hilgers and Yeung found that, in freely patent tubes, the mean (± SD) TPP was 403 ± 46 mmHg (Hilgers and Yeung, 1999Go). Both groups used fluoroscopic guidance, as was the case in our study. Using a TPP measurement set-up similar to that proposed by Gleicher et al., we reached a similar conclusion. We based our conclusion on TPP measured only in infertile women without any evidence of tubal disease. It can be argued that the ‘ideal’ normal reference range would be obtained by measuring TPP in fertile women. However, apart from the ethical concerns that such a study would raise, SS/TC is, at the moment, an investigation confined to the service of infertile women. Therefore in terms of routine clinical practice, our conclusion, which is supported by the work of previous authors, would be, although admittedly based on a small number of cases, the most useful estimate of normality.

Different results were presented in abstract form by Kaseki et al. (1991Go) During hysteroscopic selective salpingography and using indigo-carmine instead of water-soluble radiopaque medium, they recorded systolic and diastolic TPP (mean ± SD) of 84.8 ± 41.6 and 72.3 ± 9.6 mmHg respectively. When carbon dioxide was used the respective values were 103.1 ± 15.2 and 86.6 ± 2 mmHg. The different technique used as well as the small number of their patients (n = 16) and the absence of any information about their background make meaningful comparisons with results of other authors difficult. It would be plausible to assume that different TPP reference ranges apply when different selective salpingography techniques are used. Further research would be necessary to clarify the issue, and also establish the clinical usefulness of the differentiation of systolic and diastolic TPP made by the authors, which is not replicated elsewhere in the literature (Kaseki et al., 1991Go).

The only available information about the predictive value of TPP measurements in terms of fertility potential we are aware of comes from the prospective study by Karande et al. (1995Go). This demonstrated a significantly higher pregnancy rate in a group of women with normal TPP in comparison with a group of patients with elevated TPP. All 47 women studied underwent ovarian stimulation using either gonadotrophins or clomiphene citrate, while average follow-up was 8 months.

Our study offers a practical tool for the interpretation of such measurements in everyday clinical practice. Using the same TPP classification system as before (Papaioannou et al., 2002aGo), we found that infertile women can be classified, on the basis of TPP after SS/TC values, in groups which have different prognosis in terms of spontaneous future fertility. The observed differences were more pronounced when all non-IVF or ICSI first conceptions were considered. This second scenario is probably closer to real life clinical practice. There is no reason why anovulation should not be treated, donor insemination should not be used in couples with azoospermia or why clomiphene citrate or IUI should not by offered to suitable couples, once Fallopian tube patency has been confirmed or re-established, especially when TPP are low.

More importantly, the demonstration of tubal patency alone is shown to be an inaccurate predictor of future fertility. It becomes a more accurate method once combined with TPP measurements. Women with patent Fallopian tubes who belong in the poor tubal TPP status group should be counselled realistically about their chances of a spontaneous conception. The success rates anticipated through treatments whose success depends on tubal function, such as clomiphene citrate, IUI, ovulation induction and donor insemination, should be adjusted accordingly. Earlier resort to IVF may be indicated after taking into account the specifics of each case.

Although the population of women who underwent SS/TC was consecutive, the same was impossible to achieve for the women who were included in the final analysis. This was the case because both TPP and pregnancy data were necessary for a subject to qualify for inclusion. Loss to follow-up is not an uncommon shortcoming of retrospective studies. However, there is evidence that the quantitative effects of non-consecutive inclusion of patients or indeed retrospective data collection on estimates of diagnostic accuracy are not significant (Lijmer et al., 1999Go)

Furthermore, as can be deduced from Table II, the group of women for whom pregnancy data were collected but for whom no TPP data were available, was a relatively fertile group. In some cases, TPP measurements had not been performed because of equipment malfunction. In others, as stated in the relevant reports, TPP were not assessed at all. It would be plausible to assume, and certainly this is our recollection, that if no significant resistance was felt during SS/TC and everything looked normal, then the operator would be more inclined to defer TPP measurements. In other words, women in the good TPP tubal status group are probably over-represented in this good prognosis group. Therefore the reported fertility differences between the TPP status groups may, if anything, be underestimates of reality.

The population studied consisted of infertile women who either had been diagnosed with PTB before undergoing SS/TC or underwent the procedure as their first tubal assessment test. This heterogeneity is justified by our intention to use the final TPP, irrespective of any pre-existing diagnosis, as the variable of interest and to study its association with the possibility of future fertility. This decision was dictated by the need to raise sufficient numbers in order to uncover possible associations, in a subject area that has not been investigated before. Ideally, however, the two populations should be studied separately, a line that we adopted in other publications (Papaioannou et al., 2002dGo,e). Encouraged by the results of the present study, our intention is to differentiate between the two groups in future research into the association of TPP at the completion of SS/TC and subsequent fertility.

These results should be seen in the context of the methodology used. Prospective studies would be required to confirm our findings. Further research should also be directed towards a number of questions in relation to further practical application of TPP. There is some evidence that SS can benefit pregnancy rates even in infertile women with patent, Fallopian tubes as judged by HSG (Kamiyama et al., 2000Go). Perhaps TPP measurements can serve as a quantifiable variable, which can be useful in discriminating between good and bad prognosis cases in this context as well, and this should be investigated further. There is no information about the possible influence of advancing age to background TPP values. We do not know if the length of infertility is reflected in TPP measurements. In other words, if longer periods of infertility are to a certain extent the logical consequence of poor tubal status from the beginning, that could have been detected by measuring TPP from the start. If positive associations exist then one might even wonder whether TPP measurements could serve, in a similar way as early follicular FSH values are used to describe ‘ovarian reserve’, as markers of ‘tubal reserve’. Then it would be possible to hypothesize that, as far as the Fallopian tube is concerned, many other prognostic factors (age, length of infertility, possible infections, tubal surgery) can be condensed in a single measurement which is of prognostic significance for fertility. This would be a categorical, as used in this study, or even perhaps a continuous variable, which could describe tubal status more accurately than the dichotomous patency question currently used by most.

In conclusion, we present evidence that TPP values, as assessed at the completion of an SS/TC procedure, may be predictive of future spontaneous as well as non-IVF/ICSI assisted fertility. If our results are replicated in larger prospective studies, TPP assessment would have the potential to become a useful adjunct to other diagnostic information provided by SS/TC and to aid treatment decision-making in assisted reproduction.


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Baker, V.L. and Adamson, G.D. (1995) Threshold intrauterine perfusion pressures for intraperitoneal spill during hydrotubation and correlation with tubal adhesive disease. Fertil. Steril., 64, 1066–1069.[ISI][Medline]

Capitanio, G.L., Ferraiolo, A., Croce, S., Gazzo, R., Anserini, P. and de Cecco, L. (1991) Transcervical selective salpingography: a diagnostic and therapeutic approach to cases of proximal tubal injection failure. Fertil. Steril., 55, 1045–1050.[ISI][Medline]

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Papaioannou, S., Afnan, M., Girling, A.J., Coomarasamy, A., Ola, B., Olufowobi, O., McHugo, J.M., Hammadieh, N. and Sharif, K. (2002a) The effect in pregnancy rates of tubal perfusion pressure reductions achieved by guide-wire tubal catheterization. Hum. Reprod., 17, 2174–2179.[Abstract/Free Full Text]

Papaioannou, S., Afnan, M., Girling, A.J., Ola, B., Hammadieh, N., Coomarasamy, A. and Sharif, K. (2002b) The learning curve of selective salpingography and tubal catheterisation. Fertil. Steril., 77, 1049–1052.[CrossRef][ISI][Medline]

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Papaioannou, S., Afnan, M., Girling, A.J., Ola, B., Olufowobi, O., Coomarasamy, A.K. and Sharif, K. (2002e) Diagnostic and therapeutic value of selective salpingography and tubal catheterization in an unselected infertile population. Fertil. Steril. (in press).

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Submitted on August 7, 2002; resubmitted on September 20, 2002; accepted on October 1, 2002.





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