Department of Obstetrics and Gynaecology, Catholic University of the Sacred Heart, Largo F.Vito, 1, Rome 00168, Italy
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: laparoscopy/salpingoscopy/tubal surgery
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Modern refinements of laparoscopic instrumentation and techniques allow laparotomy to be avoided for tubal reconstructive surgery in most instances, and the advent of salpingoscopy, a new endoscopic technique, has allowed improved selection of patients who are candidates for tubal surgery.
The aim of the present study was to evaluate in a prospective manner the reproductive outcome after reconstructive surgery by laparoscopy, comparing the prognostic value of salpingoscopy versus the American Fertility Society (AFS) classification (The American Fertility Society, 1988) in patients with adnexal adhesions or distal tubal occlusion (DTO).
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Infertility was primary in 30 patients and secondary in 21 patients. The mean duration of infertility prior to operative laparoscopy was 47 months (range 12143). In all patients included in this study, tubal infertility was due to previous pelvic inflammatory disease (PID). No patients had been previously submitted to pelvic surgery, nor had been previously treated medically or surgically for endometriosis; no evidence of endometriosis was present at the time of operative laparoscopy.
Preoperative work-up included partner's semen analysis, HSG and ovulation studies. The presence of a severe male factor was considered a contraindication for surgery. This was defined as a sperm concentration 5x106/ml, as below this limit a decrease in the percentage of pregnancies is seen in clinical practice (Brinsden and Rainsbury, 1992
).
Salpingo-ovariolysis and salpingoneostomy were defined according to the classification by Gomel (Gomel, 1980). Laparoscopy was performed using a four-puncture technique with a transumbilical 11 mm laser laparoscope adapted to a video camera with a high-resolution monitor and three 5 mm trocars for ancillary instruments. Salpingo-ovariolysis was performed according to accepted techniques (Gomel et al., 1986
; Nezhat et al., 1995
). A combination of bipolar coagulation and fine scissors was used to divide the adhesions. For salpingoneostomy, the Bruhat technique (Bruhat et al., 1979
) was followed, using, instead of a CO2 laser, microscissors for neostomy incision and bipolar forceps at low power electrical energy for fimbrial eversion (Gomel and Taylor, 1995
).
For salpingoscopy, a 2.8 mm rigid salpingoscope that allows a detailed vision of the tubal ampullary mucosa was used. The salpingoscope was introduced into the abdominal cavity through the operating channel of the laser laparoscope. The details of this technique (originally described by Brosens et al., 1987) as performed by our group have been previously described (Marana et al., 1991
).
Patients with asymmetrical tubal lesions were classified according to the least affected adnexa. In the salpingo-ovariolysis group, 13 patients had bilateral adnexal adhesions, six patients had adnexal adhesions involving the only remaining tube, and five patients had unilateral adnexal adhesions and contralateral hydrosalpinx. In the salpingoneostomy group, hydrosalpinx was bilateral in 24 patients, and unilateral (of the only remaining tube) in three patients. At the time of surgery, the senior author evaluated the adnexal adhesions or the DTO according to the AFS classification, and, at the same time, assessed the status of the tubal mucosa by salpingoscopy according to the Puttemans' classification (Puttemans et al., 1987) as follows: grade I, normal mucosal folds are seen; grade II, the major folds are separated, flattened, but otherwise normal (in fact, this might be considered a grade I tube distended by an increased intraluminal hydrostatic pressure and therefore considered as normal); grade III, focal adhesions between the mucosal folds are seen; grade IV, extensive adhesions between the mucosal folds and/or disseminated flat areas are present; grade V, there is a complete loss of the mucosal fold pattern. The salpingoscopic findings, as well as clinical history, description of surgical procedures, and all useful information for patients' follow-up, were recorded on forms specially designed for the study.
All patients were contacted periodically by telephone to find out their reproductive outcome. No patient was lost to follow-up. The mean duration of follow-up was 33 months (range 1467).
Statistical analysis was performed with the Fisher's exact test for categorical variables and with Spearman's rank correlation test to compare the salpingoscopic grade and the AFS class. Life-table analysis and log-rank correlation were used for the calculation and comparison of cumulative pregnancy rates. A P value of <0.05 was considered statistically significant.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The correlation between the salpingoscopic grade of the tubal mucosa and the AFS score for every single tube was calculated for the 24 patients undergoing salpingo-ovariolysis and the 27 patients undergoing salpingoneostomy. In the salpingo-ovariolysis group there were 37 tubes available for comparison: 26 tubes from 13 patients with bilateral adnexal adhesions, six tubes from patients who had only one tube and five tubes from patients with a contralateral hydrosalpinx. In the salpingoneostomy group there were 54 tubes available for comparison: 44 tubes from 22 patients with bilateral hydrosalpinx; three patients had only one tube; in two patients with bilateral hydrosalpinx only one tube could be cannulated; included in this group, only for comparison purposes, were five hydrosalpinges found in patients belonging to the salpingo-ovariolysis group.
Statistical analysis demonstrated a lack of correlation between salpingoscopic grades and the AFS classification for both the salpingo-ovariolysis (r = 0.029; not significant) and the salpingoneostomy (r = 0.056; not significant) groups.
Twenty-five pregnancies occurred in the 51 patients. Nineteen patients spontaneously conceived an intrauterine pregnancy (IUP) and carried it to term. Two patients had a second term pregnancy and in one patient the term pregnancy was preceded by a spontaneous abortion. Three extrauterine pregnancies occurred, one in a patient with a class III mucosa in the salpingo-ovariolysis group and two in two patients with a class IV mucosa in the salpingoneostomy group.
In the salpingo-ovariolysis group of patients, the crude term pregnancy rate was 50% (12/24), whereas for the subgroup of patients with a normal tubal mucosa (classes I and II), this rate was 71% (12/17).
In the salpingoneostomy group of patients, the crude term pregnancy rate was 26% (7/27), whereas for the subgroup of patients with a normal tubal mucosa it was 64% (7/11).
In this study, no IUP was observed in patients with class III, IV or V ampullary mucosa.
In Figures 1 and 2, life-table analysis calculating term pregnancy rate is presented for both the salpingo-ovariolysis and salpingoneostomy groups. Log-rank correlation demonstrated a significant difference in estimated cumulative pregnancy rate over time between patients with classes I and II versus classes III to V ampullary mucosa for both the salpingo-ovariolysis (P = 0.0025) and the salpingoneostomy (P = 0.0003) groups.
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Since the first report on the value of salpingoscopy at the time of tubal microsurgery (Henry-Suchet et al., 1985), there has been increasing interest in the salpingoscopic technique to detect intraluminal lesions, which may be inversely correlated with pregnancy outcome.
In a series of 22 patients with bilateral hydrosalpinx (De Bruyne et al., 1989), a 59% (10/17) intrauterine pregnancy rate was obtained following microsurgery when mucosal adhesions were absent at preoperative salpingoscopy. One ectopic pregnancy occurred in one of the five patients with intraluminal adhesions. The authors stated that `there was no correlation between the presence or extent of pelvic adhesions and the presence or extent of intraluminal adhesions'.
In a retrospective study (Dubuisson et al., 1994), the fertility outcome of a series of 81 patients who underwent laparoscopic salpingoneostomy or, in some cases, fimbrioplasty, was reported. Salpingoscopy was not performed in this study and the status of tubal mucosa was only evaluated at gross inspection at the infundibulum after neostomy. This author reported a correlation between the mucosal appearance at the neostomy site as evaluated using criteria previously proposed (Boer-Meisel et al., 1986
) and pregnancy outcome (44% intrauterine pregnancy rate for groups I and II, i.e. normal mucosa and/or moderate attenuation of the mucosal folds, versus 0% for group III, i.e. no folds or honeycomb appearance). There was no correlation with the adhesion stage. In fact, intrauterine pregnancy rates in patients without adhesions (29%) were not significantly different from those in patients with adhesions (32%). According to Dubuisson et al. (1994), laparoscopic assessment of the tubal mucosa at neostomy site performed just as well as Mage's distal tube score (Mage et al., 1986
) in providing a prognosis.
Another study (Vasquez et al., 1995a) examined the correlation between the presence and extent of peritubal adhesions, scored according to the AFS classification (The American Fertility Society, 1988
), and the presence and extent of mucosal adhesions, evaluated at salpingoscopy, in 46 patients with bilateral hydrosalpinges and 14 with a hydrosalpinx of the single tube. Peritubal adhesions were absent in seven, mild in 46, moderate in 28 and severe in nine hydrosalpinges. Of seven hydrosalpinges without peritubal adhesions, one showed intratubal adhesion; in 83 hydrosalpinges with peritubal adhesions, including 37 cases with moderate or severe degrees of peritubal adhesions, mucosal adhesions were absent in 31 (37%). The correlation between the extent of peritubal and mucosal adhesions was not statistically significant. In this series, no information in terms of subsequent reproductive outcome was provided. The same authors (Vasquez et al., 1995b
), in another prospective study relating tubal lesions to pregnancy outcome in hydrosalpinges, demonstrated that thick-walled hydrosalpinges with wall fibrosis exclude intrauterine pregnancies, and that amongst the different lesions of thin-walled hydrosalpinges, mucosal adhesions are the most important factor in determining fertility outcome. Thin-walled hydrosalpinges with normal or flattened ampullary mucosal folds, without adhesions, were associated with a 58% intrauterine pregnancy rate and no case of tubal pregnancy.
In a recent prospective study (Marana et al., 1995a) the prognostic value of salpingoscopy was compared with the AFS scoring systems for adnexal adhesions and DTO in patients with tubal infertility undergoing reconstructive tubal surgery, mostly by microsurgery. In the salpingo-ovariolysis group of patients, the term pregnancy rate was 66% (19/29), whereas, for those patients with a normal ampullary mucosa (salpingoscopic grades I and II), this rate was 86% (19/22). In the salpingoneostomy group of patients, the term pregnancy rate was 31% (8/26), whereas, for those patients with a normal ampullary mucosa, it was 73% (8/11). At statistical analysis, there was a significant correlation between salpingoscopic grade (grades I and II versus grades III to V) and the achievement of a term pregnancy for both the salpingo-ovariolysis (P < 0.001) and the salpingoneostomy (P < 0.001) groups of patients. There was no significant correlation between the AFS scores and the achievement of a term pregnancy for both groups of patients: minimalmild (12/19: 63%) versus moderatesevere (7/10: 70%) scores for the salpingo-ovariolysis group, and mild (6/18: 33%) versus moderatesevere (2/8: 25%) scores for the salpingoneostomy group.
The prognostic value of routine salpingoscopy during diagnostic laparoscopy for infertility has also been discussed (Heylen et al., 1995). A total of 157 patients were evaluated. Cumulative pregnancy rates in patients with at least one normal tube at salpingoscopy after respectively 12, 24 and 48 months, were 43, 63 and 71%. In the intermediate group (class III, n = 18), the cumulative pregnancy rate was 38% at 48 months. No spontaneous intrauterine pregnancies were observed in classes IV and V, which included 20 patients. Only three ectopic pregnancies were observed: one occurred in the combined class III, one in the class III, and one in the combined class IVV.
In a recent, prospective study (De Bruyne et al., 1997), the prognostic value of salpingoscopy was evaluated in patients undergoing salpingo-ovariolysis (n = 130) or salpingoneostomy (n = 96) by microsurgical laparotomy for post-PIDtubal disease. There were no other causes of infertility in these patients. The authors found a significant difference when the cumulative intrauterine pregnancy rates for salpingoscopic classes III versus IIIV were compared both in the salpingo-ovariolysis (P = 0.015) and salpingoneostomy groups (P = 0.004).
The best prognostic indicator in terms of reproductive outcome was evaluated according to which type of abnormalities were detected at Falloposcopy (Dunphy and Green, 1995). Sixty-two infertile women were examined by Falloposcopy in-office using the linear everting catheter. All women were subsequently examined by hysteroscopy and laparoscopy. No patient required surgery to correct DTO. Epithelial abnormalities, adhesions, vascular abnormalities and abnormalities of luminal diameter were recorded as present or absent, and as minor or major, according to a classification (Kerin et al., 1992). When evaluating the reproductive outcome at follow-up, the authors concluded that, although four or five descriptive variables, including dilatation and vascularity, had been included in the Falloposcopic scoring system, a much simpler visual assessment was possible indicating whether the epithelium is normal and/or whether adhesions are present. A recent report showed similar findings (Marconi and Quintana, 1998
), i.e. the frequency of mucosal flattening and vascular alterations was not different between pregnant and non-pregnant patients, whereas the presence of intraluminal adhesions and nuclear staining with methylene blue was negatively correlated with the occurrence of subsequent pregnancies.
In the present study, we evaluated in a prospective manner the prognostic value of salpingoscopy in a group of 51 patients with infertility undergoing salpingo-ovariolysis or salpingoneostomy by operative laparoscopy. When comparing intraluminal findings at salpingoscopy with the AFS classification based on the pelvic external appearance, no correlation existed between the internal and external findings. There was a statistically significant correlation between the term cumulative pregnancy rate and the salpingoscopic classes but not with AFS classification, for both the salpingo-ovariolysis and salpingoneostomy groups.
When taking into consideration the results reported by other groups using the same salpingoscopic classification, we observed an agreement in the intrauterine pregnancy rate for patients with class III disease. Discrepancies were noted for class III when comparing our results with those of Heylen et al. (1995) and De Bruyne et al. (1989, 1997). However, when pooling our data on patients with class III disease, we can comment on a total of 16 patients. In these patients we observed one intrauterine pregnancy and three ectopic pregnancies. For classes IV and V, our present and previous findings are in agreement with those of Heylen et al. (1995) who did not observe any intrauterine pregnancy in this class of patients, while De Bruyne et al. (1997) reported 10 intrauterine pregnancies out of 58 patients with class IV and no intrauterine pregnancies out of five patients with class V disease (Heylen et al., 1995; Marana et al., 1995a
, b
; De Bruyne et al., 1997
). This inconsistency may possibly be due to different classification criteria, such as the inclusion of polyps, strictures, aspecifical mucosal deposits (De Bruyne et al., 1997
), as compared to only adhesions (present study; Heylen et al., 1995
). It is of note that in the population described by De Bruyne et al. (1997), only seven out of 73 patients with hydrosalpinx were in class III, compared with 3542% in our and the Brosens (1996) studies (Brosens, 1996
; De Bruyne et al., 1997
; Marana et al., 1997
), possibly reflecting the fact that some class III tubes were scored in higher stages by De Bruyne et al. (1997), e.g. in class III or more, by inclusion of polyps, strictures or aspecifical deposits.
The use of salpingoscopy may modify the management of patients with tubal infertility, since accurate evaluation of the endosalpinx allows us to identify the patients with a normal tubal mucosa (7680% of cases of periadnexal adhesions and 3542% of cases of hydrosalpinx) who may benefit the most from tubal reconstructive surgery (Brosens, 1996; Marana et al., 1997
). In these patients an intrauterine pregnancy rate equal to or higher than 70% may be expected following salpingo-ovariolysis and 60% following salpingoneostomy (Brosens, 1996
; Marana et al., 1997
).
In the present study we evaluated the prognostic role of salpingoscopy during reproductive surgery by operative laparoscopy and obtained the same results as previously reported for microsurgery by laparotomy (Marana et al., 1995a).
It should be considered that, unlike in the USA, in Italy, as in other European countries, operative laparoscopy, even for infertility, is fully subsidised by the government health service when performed in a public hospital. On the contrary, IVF and embryo transfer is mainly performed in private centres and is not reimbursed either by the Government or private insurances.
The cumulative pregnancy rate in this study showed that in the presence of a normal tubal mucosa all patients after salpingo-ovariolysis obtained the conception of a term pregnancy within 12 months from surgery, and the salpingoneostomy group of patients within 15 months, for cumulative term pregnancy rates of 71 and 64% respectively.
Based on these results, we strongly advise that young patients be offered laparoscopy, using salpingoscopy to select patients who may benefit from tubal surgery. In the presence of hydrosalpinges a small incision (35 mm) can be performed in the avascular central point of the distended distal portion of the tube with a monopolar needle to allow the introduction of the salpingoscopic sheath and then the salpingoscope into the tube for evaluation of the tubal mucosa.
Patients with normal tubal mucosa should undergo salpingo-ovariolysis and salpingoneostomy. If no pregnancy occurs within 1 year from surgery in patients with a normal tubal mucosa, assisted reproductive technologies may be considered.
Patients with abnormal tubal mucosa and especially classes IVV should not undergo salpingoneostomy, but should be immediately referred to assisted reproductive technologies after the diagnostic laparoscopy with salpingoscopy. Recent reports suggest that surgical correction of the hydrosalpinx may improve the outcome of IVFembryo transfer. Further studies are needed to verify if this subgroup of patients could benefit from salpingectomy (Andersen et al., 1996; Puttemans and Brosens, 1996
; Aboulghar et al., 1998
).
Although larger series may be needed, our data support previous evidence from the literature, and confirm the importance of salpingoscopy in patients with tubal factor infertility.
![]() |
Notes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
American Fertility Society (1988) The American Fertility Society classifications of adnexal adhesions, distal tubal occlusion, tubal occlusion secondary to tubal ligation, tubal pregnancies, Mullerian anomalies and intrauterine adhesions. Fertil. Steril., 49, 944955.[ISI][Medline]
Andersen, A.N., Lindhard, A., Loft, A. et al. (1996) The infertile patient with hydrosalpinges IVF with or without salpingectomy? Hum. Reprod., 11, 20812084.[ISI][Medline]
Boer-Meisel, M.E., te Velde, E.R., Habbema, J.D.F. et al. (1986) Predicting the pregnancy outcome in patients treated for hydrosalpinx: a prospective study. Fertil. Steril., 45, 2328.[ISI][Medline]
Brinsden, P.R. and Rainsbury, P.A. (eds) (1992) A Textbook of In-vitro Fertilization and Assisted Reproduction. Parthenon, Canforth, pp. 3972.
Brosens, I.A. (1996) The value of salpingoscopy in tubal infertility. Reprod. Med. Review., 5, 19.
Brosens, I.A., Boeckx, W., Delattin, P. et al. (1987) Salpingoscopy: a new preoperative diagnostic tool in tubal infertility. J. Obstet. Gynaecol., 94, 768773.
Bruhat, M.A., Mage, G. and Manhes, H. (1979) Use of the CO2 laser via laparoscopy. In Kaplan, I. (ed.), Laser Surgery III. International Society for Laser Surgery, Tel Aviv, pp. 274276.
De Bruyne, F., Puttemans, P., Boeckx, W. et al. (1989) The clinical value of salpingoscopy in tubal infertility. Fertil. Steril., 51, 339340.[ISI][Medline]
De Bruyne, F., Hucke, J. and Willers R. (1997) The prognostic value of salpingoscopy. Hum. Reprod., 12, 266271.[Abstract]
Dubuisson, J.B., Chapron, C., Morice, P. et al. (1994) Laparoscopic salpingostomy: fertility results according to the tubal mucosa appearance. Hum. Reprod., 9, 334339.[Abstract]
Dunphy, B.C. and Greene, C.A. (1995) Falloposcopic cannulation, oviductal appearances and prediction of treatment independent intrauterine pregnancy. Hum. Reprod., 10, 33133316[Abstract]
Gomel, V. (1980) Classification of operations for tubal and peritoneal factors causing infertility. Clin. Obstet. Gynecol., 23, 12591260.[Medline]
Gomel, V. and Taylor, P.J. (eds) (1995) Diagnostic and Operative Gynecologic Laparoscopy. Mosby, St Louis.
Gomel, V., Taylor, P., Yuzpe, A.A. et al. (eds) (1986) Laparoscopy and Hysteroscopy in Gynecologic Practice. Year Book Medical Publishers, Chicago, p. 252.
Henry-Suchet, J., Loffredo, V., Tesquier, L. et al. (1985) Endoscopy of the tube (=tuboscopy): its prognostic value for tubo-plasties. Acta Eur. Fertil., 16, 139145.[Medline]
Heylen, S.M., Brosens, I.A. and Puttemans, P.J. (1995) Clinical value and cumulative pregnancy rates following rigid salpingoscopy during laparoscopy for infertility. Hum. Reprod., 10, 29132916.[Abstract]
Hulka, J.F. (1982) Adnexal adhesions: a prognostic staging and classification system based on a five-year survey of fertility surgery results at Chapel Hill, North Carolina. Am. J. Obstet. Gynecol., 144, 141148.[ISI][Medline]
Kerin, J.F., Williams, D.B., San Roman, G.A. et al. (1992) Falloposcopic classification and treatment of fallopian tube lumen disease. Fertil. Steril., 57, 731741.[ISI][Medline]
Mage, G., Pouly, J.L., de Joliniere, J.B. et al. (1986) A preoperative classification to predict the intrauterine and ectopic pregnancy rate after distal tubal microsurgery. Fertil. Steril., 46, 807810.[ISI][Medline]
Marana, R., Muzii, L., Rizzi, M. et al. (1991) Salpingoscopy in patients with contralateral ectopic pregnancy. Fertil. Steril., 55, 838840.[ISI][Medline]
Marana, R., Rizzi, M., Muzii, L. et al. (1995a) Correlation between the American Fertility Society classification of adnexal adhesions and distal tubal occlusion, salpingoscopy, and reproductive outcome in tubal surgery. Fertil. Steril., 64, 924929.[ISI][Medline]
Marana, R., Muzii, L., Rizzi, M. et al. (1995b) Prognostic role of laparoscopic salpingoscopy of the only remaining tube after contralateral ectopic pregnancy. Fertil. Steril., 63, 303306.[ISI][Medline]
Marana, R., Catalano, G.F., Caruana, P. et al. (1997) The role of salpingoscopy in tubal reconstructive surgery. In Gomel, V. and Leung, P.C.K. (eds), Proceedings of the 10th World Congress of In vitro Fertilization and Assisted Reproduction. Monduzzi Editore, Bologna, Italy, pp. 10511057.
Marconi, G. and Quintana, R. (1998) Methylene blue dyeing of cellular nuclei during salpingoscopy, a new in-vivo method to evaluate vitality of tubal epithelium. Hum. Reprod., 13, 34143417.[Abstract]
Nezhat, C.R., Nezhat, F.R., Luciano, A.A. et al. (eds) (1995) Operative Gynecologic Laparoscopy. Principles and Techniques. McGraw-Hill, New York.
Puttemans, P.J. and Brosens, I.A. (1996) Preventive salpingectomy of hydrosalpinx prior to IVF. Salpingectomy improves in-vitro fertilization outcome in patients with a hydrosalpinx: blind victimization of the Fallopian tube? Hum. Reprod., 11, 20792081.[ISI][Medline]
Puttemans, P.J., Brosens, I.A., Delattin, P.H. et al. (1987) Salpingoscopy versus hysterosalpingography in hydrosalpinges. Hum. Reprod., 2, 535540.[Abstract]
Rock, J.A., Katayama, K.P., Martin, E.J. et al. (1978) Factors influencing the success of salpingostomy techniques for distal fimbrial occlusion. Obstet. Gynecol., 52, 591596.[Abstract]
Vasquez, G., Boeckx, W. and Brosens, I. (1995a) No correlation between peritubal and mucosal adhesions in hydrosalpinges. Fertil. Steril., 64, 10321033.[ISI][Medline]
Vasquez, G., Boeckx, W. and Brosens, I. (1995b) Prospective study of tubal mucosal lesions and fertility in hydrosalpinges. Hum. Reprod., 10, 10751078.[Abstract]
Submitted on January 28, 1999; accepted on August 28, 1999.