You are here

The place of reconstructive tubal surgery in the era of assisted reproductive techniques

Reproductive BioMedicine Online, Volume 31, Issue 6, December 2015, Pages 722 - 731

Abstract

Assisted reproductive techniques yield high rates of success for women with tubal factor infertility. Because they are potentially effective for all categories of infertility, for two decades, clinical and basic research in infertility has been focused on IVF techniques and outcomes, rather than developing surgical techniques or training infertility subspecialists in tubal microsurgery. Nonetheless, in comparison with IVF, reconstructive tubal surgery is inexpensive and offers multiple opportunities to attempt conception. Performing laparoscopic salpingostomy prior to IVF in women with good prognosis tubal disease may improve the outcome of subsequent IVF, while offering the potential for spontaneous conception. Tubo-tubal anastomosis for reversal of tubal ligation, performed either by a microsurgical technique through a mini-laparotomy or by laparoscopy, is preferable to IVF in younger women with no other fertility factors, because it offers potentially higher cumulative pregnancy rates. Surgery is the only alternative for women with tubal factor infertility who for personal or other reasons are unable to undergo assisted reproductive techniques. Tubal reconstructive surgery and assisted reproductive techniques must be considered complementary forms of treatment for women with tubal factor infertility, and training in tubal reconstructive surgery should be an integral part of subspecialty training in reproductive endocrinology and infertility.

Keywords: assisted reproductive techniques, IVF, reproductive surgery, tubal microsurgery.

Introduction

Until the mid-1980s, reconstructive surgery was the only therapeutic option for infertility caused by tubal and peritoneal factors. Because traditional surgical techniques yielded poor outcomes, often as a result of extensive postoperative adhesions, gynaecologic microsurgery was introduced in the early 1970s (Gomel, 1974, Gomel, 1977a, Gomel, 1983a, and Swolin, 1975). This new approach offered significantly improved outcomes, especially in tubal anastomosis (Gomel, 1980a). Simultaneously laparoscopic access was explored for tubal reconstruction, especially in distal tubal disease, by applying the same microsurgical tenets (Gomel, 1975, Gomel, 1977b, Gomel, 1977c, and Gomel, 1978a). Laparoscopic access provided the advantages that are now well recognized: less postoperative discomfort and analgesic requirement, shorter hospital stay and period of convalescence, frequently reduced costs and superior cosmesis (Gomel, 1978b).

Most of the laparoscopic procedures became ambulatory, performed on a day-care basis. It also became evident that this route of access yielded results that were not dissimilar to those obtained via laparotomy, provided of course that the technique used was the same (Gomel, 1983b). Experience with laparoscopy enabled surgical modifications for more complex cases, such as tubo-cornual anastomosis and uterine myomectomy; a small mini-laparotomy incision replaced a formal laparotomy, permitting such procedures also to be performed on an ambulatory basis (James and Gomel, 1990).

Human life normally originates in the proximal ampulla, near the ampullary-isthmic junction of the Fallopian tube, with subsequent transport to the uterus. IVF followed by embryo transfer was designed to duplicate this function. The initial results were at best very modest. The first international survey by Seppälä in 1984 included 10,028 initiated cycles, which resulted in 523 births (5.2%) (Seppälä, 1985). The birth rate per initiated cycle reported by Norfolk for 1981–1983 was 11.5%, our own in Vancouver for 1984 and 1985 was 10.3% and the overall results in the USA for 1985 and 1986 were 6.6% and 6.4%, respectively.

The IVF results significantly improved during the 1990s; in the USA they progressed from 12.3% of births per initiated cycle in 1990 (SART, 1992) to 25.4% in 1999 (SART, 2004). They have reached a plateau around 28–30% since 2002 (CDC, 2003, CDC, 2006, and CDC, 2011). Another very significant progress during the 1990s was the introduction of intracytoplasmic sperm injection (ICSI), which proved to be a panacea in the treatment of male infertility (Palermo et al., 1992).

In concert with the improvement in the outcomes of assisted reproductive techniques, a significant decline in the use and teaching of reconstructive surgery occurred. Increasingly IVF began to be offered as the primary treatment option in cases of tubal factor infertility. Surprisingly, this change occurred despite the acceptance of laparoscopic access to perform many of the reconstructive tubal operations and the use of access by mini-laparotomy for more complex procedures, both of which had become day-care procedures (Gomel, 1989). Being concerned with this trend, we emphasized as early as 1992 that both therapeutic options had a place, that treatment should be individualized based on the clinical findings and circumstances of the couple, and that these two options were not competitive but rather complementary (Gomel and Taylor, 1992). It has been gratifying to find support for the opinions we have expressed about the role of reproductive surgery since the early 1990s in the American Society of Reproductive Medicine's (ASRM) ‘Committee opinion: role of tubal surgery in the era of assisted reproductive technology’, published in March 2012 (ASRM, 2012).

In Vancouver the university department has for many years had a very active surgical programme, with a significant number of patients who provide us with a realistic and accurate accounting of the efficacies of these different surgical interventions. Furthermore, there has been substantial constancy in our surgical techniques. Our treatment population is largely permanent, and this has permitted thorough long-term follow up. However, we would caution against simple extrapolation of our statistics to other populations and other surgeons. In particular, we have learnt that extensive training in microsurgical principles is key to successful outcome (Gomel and McComb, 2006).

The purpose of this paper is not to review the surgical techniques of various surgical procedures, which have been described in detail elsewhere (Gomel, 1983a, Gomel, 2010, and Gomel, Taylor, 2008). The discussion will be limited to the procedures used for infertility associated with tubal and peritoneal factors and outcomes yielded by the use of proper microsurgical techniques in carefully selected patients, and a brief discussion on the relative places of reconstructive microsurgery and IVF.

Fertility-promoting procedures

The goal of fertility-promoting surgery is to restore the anatomic and functional integrity of the reproductive organs. Restoration of the anatomic integrity does not equate with the restoration of functional integrity since the latter is dependent upon of the extent of damage (fibrosis, intra-tubal adhesions, damage to the ciliated cells and fimbriae) that existed prior to the surgery. This is why proper selection of cases is an important factor in the outcome. The significant improvement of results with assisted reproductive techniques offers the reproductive surgeon of today the luxury of operating on cases with a more favourable prognosis, which results in improved success rate for a given procedure.

Reconstructive surgery for distal tubal disease

Procedures for distal tubal disease include salpingo-ovariolysis, fimbrioplasty and salpingostomy. These are some of the first procedures performed by laparoscopic access in the early phase of operative laparoscopy; they were performed with a monocular view, with assistants unable to view the operative field (Gomel, 1975, Gomel, 1977b, Gomel, 1977c, Gomel, 1978b, Gomel, 2010, and Gomel, Taylor, 2008). Indeed, they are all amenable to being performed by laparoscopic access, which has been our approach from the beginning. They should be undertaken as part of any diagnostic laparoscopy performed for infertility investigation.

Salpingo-ovariolysis and fimbrioplasty

Periadnexal adhesive disease may be the only apparent lesion or may be associated with tubal occlusion. If periadnexal adhesions are the sole lesion, laparoscopic salpingo-ovariolysis, using a microsurgical approach, may be performed by laparoscopy, preferably as part of the initial diagnostic procedure. For patients who had undergone this procedure, a cumulative intrauterine pregnancy rate (CPR) of 62% and a live birth rate of 59% were reported in the early 1980s (Gomel, 1983c). Intrauterine pregnancy rates ranging from 51% to 62%, and ectopic pregnancy rates from 5% to 8% were reported from centres in Europe and North America.

Agglutination of the fimbriae (fimbrial phimosis) necessitates a fimbrioplasty; this condition often coexists with periadnexal adhesions, which are dealt with first. The reported cumulative intrauterine pregnancy rates after laparoscopic fimbrioplasty range from 40% to 48%, and the ectopic pregnancy rates range from 5% to 6% (Gomel, 1983b and James, Gomel, 1990).

Salpingostomy

As opposed to cornual tubal occlusion, which may spare the rest of the tube from the effects of infection, the inflammation associated with a hydrosalpinx extends along the entire length of the tube. This results in varying degrees of damage to the ciliary mucosa, scarring of the myosalpinx and serosa, and occlusion of the distal end of the tube. Extension to the peritoneal cavity may also result in varying degrees of periadnexal and pelvic adhesions.

When present, adhesions are dealt with first. A salpingostomy can also be performed by laparoscopy using a microsurgical approach (Gomel, 1977c). In the case of distal occlusion the outcome is obviously dependent upon the surgical technique, but also largely on the condition (extent of damage) of the tube.

Work from our department and others have shown that certain factors in a woman's history predict the outcome of salpingostomy (Taylor et al., 2001). Rates of CPR of 25%−30% are attainable with liberal use of salpingostomy. While salpingostomy results in poor intrauterine pregnancy and high tubal pregnancy rates in tubes with extensive damage, the results in those with mild to moderate damage are very encouraging. Intrauterine pregnancy rates up to 70% have been reported with mild cases (Gomel and Erenus, 1990). The status of the Fallopian tubes can be assessed with a well-performed hysterosalpingography (HSG), or by direct visualization at laparoscopy, during which a ‘tuboscopy’ may also be undertaken to inspect the endothelium of the ampullary portion of the tube. (Boer-Meisel et al, 1986, Marana et al, 1999, and te Velde et al, 1989). Prognosis is indeed poor in the presence of intratubal adhesions, absence of mucosal folds with flattened patches of scarred mucosa (tuboscopy stage 3 and 4). The same applies to rigid, thick walled hydrosalpinges, which are usually not enlarged. In such cases a salpingostomy is not indicated.

The existence of a credible alternative treatment in the form of IVF gives us the opportunity to select for surgery cases with a good prognosis, and the luxury to perform the procedure by laparoscopy as part of a diagnostic laparoscopy. Laparoscopic access offers similar outcomes to open access provided a proper technique is used; this emphasizes the need for proper investigation of the couple and individualization of treatment (Canis et al, 1991, Dubuisson et al, 1994, Kosasa, Hale, 1988, Larsson, 1982, Lilford, Watson, 1990, Oh, 1996, Schlaff et al, 1990, Tulandi, Vilos, 1985, and Verhoeven et al, 1983).

IVF in the presence of hydrosalpinges

The deleterious effect of hydrosalpinx on the outcome of IVF treatment has been recognized (Strandell et al, 1994 and Strandell et al, 1998). This is evident with large hydrosalpinges, visible at sonography. Significant improvement of outcomes with salpingectomy and proximal occlusion of the tube before IVF in such cases has also been demonstrated (Strandell et al, 2001 and Zouves et al, 1991). It also became evident that the detrimental effect is due to a ‘wash-out’ effect owing to the passage of the collected tubal fluid to the uterine cavity at the time, or soon after transfer of the embryos (McComb, Taylor, 2001 and Van Voorhis et al, 1998). A study from our department demonstrated that performing a salpingostomy in the terminally occluded Fallopian tube of women with a unilateral hydrosalpinx and a contralateral patent tube significantly improved rates of implantation (McComb and Taylor, 2001). The beneficial effect of salpingostomy in IVF was demonstrated earlier in a small number of cases (Murray et al., 1998). Obviously salpingostomy, in addition, offers the woman the potential of achieving a pregnancy naturally. This and other evidence suggest that there may well be a place for laparoscopic salpingostomy using a microsurgical technique, instead of salpingectomy, when factors contraindicating this approach are absent. ASRM's committee opinion (ASRM, 2012) in this regard is as follows: ‘Although IVF is preferred over salpingostomy for mild hydrosalpinges in older women and for those with male factor or other infertility factors, salpingostomy before IVF may improve the subsequent likelihood of success of IVF while still giving the patient the option to attempt spontaneous conception… Patients with poor-prognosis hydrosalpinges are better served by salpingectomy followed by IVF.’ And further on in the text: ‘Intuitively, it makes sense that laparoscopic neo-salpingostomy before IVF should improve the pregnancy rate, but there are still no confirmatory studies.’

Tubal anastomosis

Microsurgery finds its ultimate application in tubo-tubal anastomosis. The precision afforded by this technique allows total excision of occluded or diseased portions, proper alignment, and accurate apposition of each layer of the proximal and distal tubal segments. Tubal anastomosis may be undertaken to overcome an occlusion located anywhere along the tube; an occlusion caused by a disease process, congenital or iatrogenic; and/or to excise a non-occluding tubal lesion.

Tubal anastomosis for reversal of sterilization

In the vast majority of cases of reversal of tubal sterilization the available tubal segments are normal. The procedure is an exercise in which exquisitely precise surgery applies the full advantage of microsurgical principles, including magnification, to direct careful excision of tissue and accurate approximation of the tubal segments with non-reactive micro-sutures. The outcome is an anatomically and physiologically normal, albeit shortened, Fallopian tube (Gomel, 1977a, Gomel, 1978b, Gomel, 1980a, and Gomel, 2010).

Based on our experience at the University of British Columbia, in the absence of a male factor the major factors that affect outcome are: (i) the age of the woman, which plays a paramount role on fertility, irrespective of the mode of treatment; (ii) the length of the available tubal segments; (iii) the quality of the microsurgical technique; and (iv) selection of patients. Therefore, the outcome depends on the degree of rigour in surgical technique and selection criteria.

The age at the time of reversal is paramount. Those women who have normal ovarian function and a fertile male partner, and who are 35 years of age or younger at the time of reversal, can anticipate a cumulative live birth rate of about 70%, with most pregnancies occurring within 12 months after surgery. Those 35 years of age or older can anticipate a cumulative live birth rate of 50%, and with a good technique an ectopic pregnancy rate as low as 2% (Gomel, 1980a, Gomel, 1989, and Rouzi et al, 1995).

The effect of advancing age on fertility has long been known. IVF has proven this scientifically and demonstrated this to be principally associated with changes due to ageing of oocytes. This is also evident in the outcomes of reproductive surgery including reversal of sterilization (Gomel, 1980a, Gomel, 1983d, Gomel, 2010, Gomel, McComb, 2006, Gomel, Taylor, 2008, Rouzi et al, 1995, Schlösser et al, 1993, and Winston, 1980). However, it must be noted that the pregnancy and birth rates obtained with microsurgical tubal anastomosis in patients of older reproductive age is not negligible. In 1990 Trimbos-Kemper (Trimbos-Kemper, 1990) carried out a multicentre survey in the Netherlands, and evaluated the outcome of 78 women aged 40 or older who underwent reversal of sterilization. The reconstructed tubal length in each case was more than 4 cm. The birth rate, after a minimum period of 1-year follow-up, was 44%. Spontaneous abortion occurred in 26% of those with intrauterine pregnancies, which is expected in this age group. Recent publications support this evidence, although some refer to pregnancies rather than live births (Caillet et al, 2010 and Gordts et al, 2009).

Tubal length is also an important factor; ideally the reconstructed tube should be not less than 5 cm long. Proper function requires the presence of an ampullary-infundibular segment of some 3 cm and an isthmic segment of approximately 2 cm to enable oocyte capture and retention.

An inverse relationship between the total length of the reconstructed oviduct and the interval between surgery and the occurrence of pregnancy has been reported (Gomel, 1980a and Gomel, 1983d). With oviducts longer than 6 cm, most of the pregnancies occurred within five cycles following the reconstructive surgery. Among the 36 patients whose longest or only oviduct measured 4 cm or less, there was a significantly greater time lapse (mean: 19.1 months) between the surgery and occurrence of pregnancy, compared with 10.2 months in the whole series. In the early days of microsurgical surgery, before less destructive tubal sterilization techniques gained acceptance, reversals were often performed with markedly shorter tubal segments (Gomel, 1980a and Winston, 1980). The importance of tubal length, as a factor for successful outcome, has been corroborated by many authors (Henderson, 1984 and Silber, Cohen, 1984).

Use of a precise microsurgical technique is essential to achieve good outcomes. There are great variations in the outcomes reported in major published series of open microsurgical procedures: live birth rates vary between 50% and 81% (Boeckx et al, 1986, Caillet et al, 2010, Gomel, 1978b, Gomel, 1983d, Gordts et al, 2009, Henderson, 1984, Paterson, 1985, Putman et al, 1990, Rock et al, 1987, Schepens et al, 2011, Schlösser et al, 1993, Silber, Cohen, 1984, Spivak et al, 1986, Trimbos-Kemper, 1990, te Velde et al, 1990, Winston, 1980, and Xue, Fa, 1989). The ectopic pregnancy rates should normally be low since the anastomosed tubal segments are usually healthy. In an early series of 118 women, 96 (81.4%) had one or more intrauterine pregnancies and 93 (78.8%) one or more births; two (1.7%) had ectopic pregnancies (Gomel, 1983b). Xue and Fa (1989), from Shanghai, with whose work the author was familiar, in a series of 117 women reported intrauterine pregnancy, term delivery and ectopic pregnancy rates of 83.8%, 81.2% and 1.7%, respectively. The low ectopic pregnancy and the high birth rates reflect the use of a precise technique; and proper selection since the majority of these women had a reversal due to loss of a child, in the same marital relationship with proven prior fertility.

In series of tubo-tubal anastomosis reporting average or poor intrauterine pregnancy rates, invariably one finds an elevated rate of ectopic pregnancy. This may be associated with technique and/or patient selection. There are several recent publications from Hanover (Germany) on retrospective studies of reconstructive tubal microsurgery, by mini-laparotomy for infertility (Schippert et al, 2010a, Schippert et al, 2010b, and Schippert et al, 2012). Of 127 women submitted to tubal anastomosis for reversal of sterilization 38 were lost to follow-up; the outcomes were reported on the remaining 89 women, whose mean age was 35.5 years (age range 26–42). Of these 89 patients 45 (50.6%) had live births and six (6.7%) tubal pregnancies. A study from Belgium (Gordts et al., 2009), reported on 261 women who had tubal anastomosis for reversal of sterilization, performed over a span of 20 years. Of these, 89 (34%) were lost to follow-up, and an additional eight were excluded from the analysis. On the remaining 164, the live birth rate was 60% and the ectopic pregnancy rate 7.7%.

Precise microsurgical technique and rigour in patient selection criteria are crucial to achieve excellent results. This is corroborated by relatively recent reports on sterilization reversal, which include two large series from Korea (Kim et al, 1997a and Kim et al, 1997b). It is interesting to note the significant differences in the outcome of these two studies. Both series had around 10% loss to follow-up, which were excluded from the analysis. The first, which included 359 patients, had birth and ectopic gestation rates of 82% and 2%, respectively, as opposed to the other, which included 922 patients with a birth rate of only 40% and an ectopic gestation rate of 5%.

Tubo-tubal anastomosis can be performed by laparoscopic access, and this access route is used in many centres. The reported outcomes with this approach are inferior in comparison to open access (Bisonette et al, 1999, Dubuisson, Chapron, 1998, Dubuisson, Swolin, 1995, Ribeiro et al, 2004, and Wiegerinck et al, 2005). This is largely due to modification of the proven microsurgical technique (Gomel, 1980a, Gomel, 2010, and Gomel, Taylor, 2008), in order to make the laparoscopic procedure easier to perform. The few who employed a truly microsurgical, two-layer anastomosis technique by laparoscopic access report results that are not too dissimilar to those obtained by open access (Cha et al, 2001 and Yoon et al, 1999); this confirms the importance of good surgical technique, irrespective of the mode of surgical access.

Laparoscopic access for microsurgical tubal anastomosis was tried in the mid-1980s in Vancouver. It was concluded at the time that the mechanical disadvantages inherent in laparoscopic surgery lead to less precision than that readily attainable by microsurgery using an operating microscope through a mini-laparotomy incision. Because hospital stay and incapacity were similar for both forms of surgical access, it was decided to continue to use microsurgery by mini-laparotomy for reversal surgery, which also applies to anastomotic surgery for proximal (cornual) tubal disease (Gomel, McComb, 2006 and Gomel, Taylor, 2008).

Several groups have explored robot-assisted tubal anastomosis. Initial reports of small series by Falcone et al. (2000) and Degueldre et al. (2000), both of whom were proficient in microsurgery, used a two-layer microsurgical anastomosis. They reported the use of robot-facilitated suturing but increased the length of the procedure. Both groups have published more recent reports with a greater number of cases. The first group compared outcomes between the robot-assisted tubal anastomosis to those performed by outpatient mini-laparotomy (Rodgers et al., 2007). They found that both surgical and anaesthesia mean times were greater with the robotic approach, which also incurred a mean cost increase of US $1446.00 per case. The authors' conclusion was: ‘Overall, there do not seem to be any advantages of robotic surgery compared with outpatient mini-laparotomy.’

The second group (Caillet et al., 2010) reported ‘a retrospective study on all consecutive patients who underwent robotically assisted laparoscopic tubal re-anastomosis between February 1999 and June 2007’, all performed with laparoscopic assistance and by the same surgeon and assistant. The study was performed on 97 of 160 women undergoing surgery, due to 47 lost to follow-up and others for various reasons. ‘Sixty six of the 97 women became pregnant at least once; and 58 gave birth at least once’, representing a pregnancy rate of 68% and a birth rate of 60%. Ectopic pregnancy rates were not provided. The authors stressed the fact that the use of the robot was associated with prolonged operating times and increased costs.

Tubo-tubal anastomosis is a relatively simple operation for a physician skilled in microsurgery. Based on the outcomes and limitations mentioned earlier, it is difficult at this stage to justify the routine use of a robot for such cases, and its use would better serve more complex surgical procedures.

Proper preliminary investigation, including of the male partner, will enable proper selection of treatment for the patient: surgery or IVF (Gomel, 2007). Investigation should include obtaining the surgical report of the prior sterilization, which should provide information about the status of the pelvic organs at the time, and suggest the length of tubal segments that remain. In addition, undertaking a well-performed hysterosalpingogram (HSG) will provide useful information about the cervical canal and uterine cavity, and outline the remaining proximal tubal segments; and reveal any pathologic findings such as salpingitis isthmica nodosa (SIN), tubal endometriosis, fibrosis, etc. Proper preliminary investigation will enable proper selection of patients and improve the outcome.

A retrospective cohort study (Boeckxstaens et al., 2007), published in 2007, analysed the delivery rates of 163 patients, 79 of whom had IVF treatment and 84 who had surgical reversal. Patient characteristics were similar in both groups. The cumulative delivery rate during 72 months was 52% in the IVF group and 59.5% in the reversal group. The cumulative delivery rates for those aged <37 years was 52.4% after IVF and 72.2% after reversal (P = 0.012). The average cost per delivery was 11,707 euros for IVF and 6015 euros for surgical reversal.

The ASRM committee opinion in regard to sterilization reversal supports the position held for more than three decades and reads as follows: ‘There is good evidence to support the recommendation for microsurgical anastomosis for tubal ligation reversal… it can be accomplished by mini-laparotomy as an outpatient procedure.’ Comparable results may be obtained by laparoscopy if the procedure is performed ‘in an identical fashion to open microsurgical tubal anastomosis… Operating times are prolonged.’ ‘Only surgeons who are very facile with laparoscopic suturing and who have extensive training in conventional tubal microsurgery should attempt this procedure’ (ASRM, 2012).

Tubo-cornual resection and anastomosis by microsurgery

Tubo-cornual resection and anastomosis (TCA) by microsurgery for occlusion of the proximal Fallopian tube is an effective treatment for restoration of fertility. Lesions of the proximal tube most associated with occlusion are inflammatory in origin due to ascending trans-mucosal infection through the cervix and uterus. The continued ascent of the infection is frequently impeded by the very occlusion it produces, with a consequent sparing of the distal oviduct and ovary from the effects of the inflammatory process (Gomel and McComb, 2006). Thus, the satisfactory intrauterine and live birth rates yielded by the use of proper microsurgical technique reflect the preservation of relatively healthy distal oviducts (Madelenat et al, 1977 and McComb, Gomel, 1980).

The single HSG finding of cornual occlusion is not sufficient to recommend the procedure. It is imperative to distinguish between true pathologic occlusion and cornual spasm (which can occur during HSG), accumulation of mucous debris forming a plug, or simple synechiae. It has been reported that tubal spasm or transient occlusion by mucus plugs occurs in up to 40% of cases (Allahbadia and Merchant, 2010). This led to the introduction of selective salpingography and tubal cannulation (catheterization) for both diagnostic and therapeutic measures, since these procedures restore tubal patency in most such cases. (Thurmond, 1991).

Selective salpingography and tubal cannulation

The association of HSG with false-positive results in regard to cornual occlusion is largely due to the lack of preparation of the patient for the procedure and use of a poor technique. This was clearly demonstrated by Lang and Dunaway (1996). In 400 cases diagnosed as having cornual occlusion with a prior HSG elsewhere, simple premedication with aspirin before repeat HSG demonstrated tubal patency in one or both tubes in 82 of the 400 cases. The use of selective salpingography in the others revealed tubal patency in one or both tubes in 131 of 318 cases. The remaining 187 women were submitted to tubal cannulation; this procedure was successful, in one or both tubes, in 145 and failed in 42.

Tubal catheterization can also be carried out by hysteroscopy under laparoscopic guidance. Both have a place. Radiographic selective salpingography and if required cannulation should be performed when the HSG demonstrates cornual occlusion and preferably in the same setting. This approach, in addition to overcoming the occlusion by dislodging the debris or lysing the synechiae, may also outline a healthy tube that is distally patent; or, not infrequently, a diseased distal tube that is inoperable. Such findings are important in directing subsequent treatment. Selective salpingography and cannulation may also be performed under ultrasonic guidance. While this approach is relatively simple and inexpensive, its diagnostic accuracy is considered inferior. Only few investigators have used this approach.

Hysteroscopic cannulation provides the opportunity to catheterize a tube while performing a laparoscopy, when the dye test suggests cornual occlusion. Laparoscopy-guided hysteroscopic cannulation has the advantages of permitting thorough examination of the abdomen and pelvis, providing information about the distal tube and any underlying disease; and in addition not having radiation exposure. The disadvantages are being more invasive and expensive, and the requirement of general anaesthesia.

A review demonstrated that the mean successful cannulation rate is 70%, with a pregnancy rate of 33% and a live birth rate of 26%. The results vary greatly in various series and in many did not report birth rates (Hou et al., 2014). The preceding clearly demonstrates the role and benefit of selective salpingography and cannulation, and the importance of its use before recommending reconstructive surgery or IVF.

The inflammatory causes of cornual disease include chronic salpingitis, follicular salpingitis, obliterative fibrosis and SIN. The latter may be progressive and is associated with ectopic pregnancy, if the affected oviduct is open distally. SIN is found in about 35% of cases (Madelenat et al., 1977). It is considered to be of inflammatory aetiology since other stigmata of previous peritoneal/pelvic infection such as perihepatic adhesions and adnexal adhesions frequently co-exist. The diagnosis is readily made by HSG. Radiologic contrast will be noted within diverticula that extend from the intramural and/or isthmic lumens. A proximal tubal nodule with superficial adhesions is characteristic when observed laparoscopically. The nodular tissue is firm to touch, belying the histological findings of myosalpingeal hyperplasia and fibrosis that encase the diverticula that are composed of tubal epithelium (Gomel and McComb, 2006). Selective salpingography and/or tubal cannulation cannot correct SIN and the other inflammatory occluding lesions.

The management strategy in proximal tubal occlusion must take into account other variables, including the condition of the distal tube, the extent and nature of pelvic adhesions, the presence of associated pelvic disease, and the status of other fertility parameters, especially male factor infertility. This strategy must also respect the following principles: simplicity, reproducibility and cost-effectiveness. The selection of treatment must be individualized according to the investigative findings, the wishes of the couple, the expertise of the surgeon and the results achieved by the centre in which the couple will be managed (Gomel, 2010 and McComb, Gomel, 1980). An irrefutable diagnosis of cornual disease and absence of distal disease must be reached, as described above, before recommending surgery.

Tubo-cornual anastomosis became possible after the introduction of microsurgery. This procedure replaced the traditional technique of tubo-cornual implantation. Compared with tubo-uterine implantation, microsurgical tubo-cornual anastomosis offers several advantages: it largely maintains the integrity of the uterine cornu; it preserves a longer tube; it obviates the need for a Caesarean section, except for obstetric reasons; and it yields better results. The technique and the advantages of microsurgical tubo-cornual anastomosis for pathologic cornual occlusion were first reported at the 8th IFFS World Congress on Fertility and Infertility held in Buenos Aires in 1974 (Gomel, 1974), and by subsequent publication in January 1977 (Gomel, 1977a). In this article, data on 14 such cases were presented, with an intrauterine pregnancy rate of 53.8%. In a subsequent report (McComb and Gomel, 1980) data on 38 cases were provided and subsequently data on 48 cases (Gomel, 1983d). Of these 48 patients, 27 achieved term births (56.3%); of the three women who had ectopic pregnancies, one had a term pregnancy; and of the three who experienced spontaneous abortions, two also had viable births; 18 did not conceive.

Published series describe live birth rates ranging from 33% to 56% (Awartani, McComb, 2003, Donnez, Casanas-Roux, 1986, Gillett, Herbison, 1989, Gomel, 1977a, Gomel, 1978b, Gomel, 1980a, Gomel, 1983b, Gomel, 1983e, McComb, 1986, Patton et al, 1987, and Tomazevic et al, 1996). Most of these studies were published before 1990; there is a paucity of recent publications, which implies decreased utilization of this procedure. Recent reports from Schippert et al., referred to under reversal of sterilization, also included a series on tubo-cornual anastomosis performed between 1990 and 2001 (Schippert et al, 2010a, Schippert et al, 2010b, and Schippert et al, 2012). Of the patients contacted for the review, only 63% responded (loss to follow up rate 37%). Among the 68 patients who responded, 38 became pregnant (crude pregnancy rate 55.9%), nine aborted, seven had an ectopic pregnancy (10.3%) and 22 delivered (32.4%).

The outcomes after tubo-cornual anastomosis depend on almost the same parameters (in the absence of a male factor) as tubo-tubal anastomosis for reversal of sterilization or mid tubal pathological conditions: (i) the age of the woman; (ii) the status of the distal tube; (iii) the quality of the microsurgical technique employed; and (iv) selection of patients. The outcome is clearly dependent largely on the degree of rigour in surgical technique and selection criteria.

The ASRM committee opinion in regard to microsurgical tubo-cornual anastomosis for pathologic cornual occlusion states: ‘Unless the proximal blockage on HSG is clearly due to SIN, selective salpingography or tubal cannulation can be attempted… Before performing this procedure, there should be confirmation of normal distal tubal anatomy’ (ASRM, 2012). Further, it states: ‘IVF is preferred to resection and microsurgical anastomosis… Microsurgery may be considered after failed tubal cannulation if IVF is not an option for the patient, but it should be attempted only by those with appropriate training.’

IVF versus reconstructive tubal surgery?

For the infertile woman with tubal damage there are only two realistic options to achieve a pregnancy: reconstructive surgery or IVF/assisted reproductive techniques. The presence of a credible alternative, in assisted reproductive techniques, permits the reproductive surgeon to operate on cases with a better prognosis, which was not the case before the end of the 1980s. We have known for a long time that one of the important factors influencing surgical outcome was the degree of tubal damage, which led to the development of various classifications (Boer-Meisel et al, 1986, Gomel, 1980b, Gomel, 1983f, Gomel, Erenus, 1990, and The American Fertility Society, 1998). Operating on patients with a better prognosis will translate into superior outcomes, as has been well demonstrated.

Assisted reproduction has revolutionized reproductive medicine, and it has dramatically changed treatment of infertility for the good. It has permitted streamlining of the investigation of the couple presenting with infertility. It has offered couples the opportunity to attempt conception with a new therapeutic modality and, with the development of ICSI, with an effective way to overcome most types of male infertility (Palermo et al., 1992).

The success rate of assisted reproductive techniques significantly improved during the 1990s, reaching a plateau of 28–30% of births per initiated cycle since 2002 in the USA (CDC, 2003, CDC, 2006, CDC, 2011, SART, Society for Assisted Reproductive Technology; The American Fertility Society, 1992, and SART, Society for Assisted Reproductive Technology; American Society for Reproductive Medicine, 2004). The rate in Europe is much lower (21%), related largely to the fact that legislation in most countries limits the number of embryos to be transferred. This limitation in turn results in a lower proportion of multiple births (22.3%) (CDC, 2011 and Karlström, Bergh, 2007).

Multiple pregnancies frequently result in preterm birth, associated with increased perinatal mortality and morbidity including cerebral palsy (Bergh et al., 1999). The rates of preterm birth for singleton pregnancies, singletons from multiple fetuses, twins, triplets and higher order multiples are 12.5%, 18.3%, 63.3% and 95.3%, respectively. The perinatal mortality is 1.9% in the IVF group of births, a rate that is almost double that of controls. The large proportion of multiple births, with the associated increased obstetric complications, neonatal complications and neonatal deaths, also causes great societal costs and significant financial and emotional burden for parents.

Another aspect of assisted reproductive techniques that must be considered is the following: based on the current US outcomes of a birth rate of 28.5% per initiated cycle, the cumulative probability of live birth after three cycles of treatment would be approximately 54%. However, several studies have shown conclusively that a large proportion of couples do not wish to undergo three cycles of IVF, even when these are subsidized (Land et al, 1997 and Olivius et al, 2004). Others will refuse to undergo IVF for religious or ethical reasons, and to many the cost of IVF is prohibitive; the procedure is not covered by health insurance in many jurisdictions or countries, while surgical treatment is usually covered (as is the case in British Columbia).

Assisted reproductive techniques and reconstructive microsurgery are complementary. This is clearly demonstrated in an early study, performed when IVF results were relatively modest and published in 1996. In this study (Tomazevic et al., 1996) 59 women with occlusive proximal disease underwent microsurgical tubo-cornual anastomosis; 27 (45.8%) had live births, and three had ectopic pregnancies. Of the 32 women who failed to have a child within 2 years, 21 agreed to undergo IVF. The 66 cycles of IVF resulted in live births for 12 of women, increasing the number of women with live births to 39 (66.1%).

The choice of primary treatment and any subsequent treatment should be dependent on careful investigation of the patient and consideration of both technical and non-technical factors that affect the couple. These must be individualized for each case (Gomel and Taylor, 1992). Non-technical considerations include age. As discussed earlier, the age of the female partner is very important in the outcome, irrespective of the treatment selected. In women in the later reproductive years, it is prudent to attempt IVF first, since the result is immediate. The other considerations are costs and the wishes of the couple. Health insurance coverage and the cost of the procedure, depending on the jurisdiction and the resources of the couple, play important roles in the decision-making process. Another often underestimated factor is the economic impact for a couple of a multiple pregnancy, which occurs much more frequently with IVF. Active involvement of the couple in the decision-making process is more likely to result in resolution of the conflict of infertility should treatment prove unsuccessful.

Technical considerations result from proper investigation of the couple. For example, ICSI within the IVF setting is the only realistic treatment option in the presence of severe male factor infertility. IVF clearly represents the only therapeutic option for those with inoperable tubal damage and for those with tubal disease coincident with another important infertility factor. For others whose sole cause of infertility is a tubal factor that is amenable to surgery, successful surgery will offer multiple cycles in which to achieve conception and the opportunity to have more than one pregnancy without further cost or risk (Gomel and Taylor, 1992). The overall risks of reconstructive tubal surgery are small and include the recognized complications of anaesthesia and surgery. The miscarriage rate subsequent to reconstructive tubal surgery is not increased over that of the general population.

Microsurgical reconstruction is also effective in complex anatomic situations. One such case was a woman with a left unicornuate uterus devoid of adjacent adnexa but with a tube and ovary on the contralateral side. This necessitated microsurgical tubo-ovarian transposition and a left tubo-cornual anastomosis. Subsequently the woman had three pregnancies resulting in three live births (Gomel and McComb, 1985).

The preface of the book Microsurgery in Female Infertility (Gomel, 1983a) contains the following statement: ‘Further developments are also occurring in the area of in-vitro fertilization and embryo transfer (IVF and ET), which will undoubtedly produce improved results. Nonetheless, I do not consider the techniques of microsurgery on the one hand and IVF and ET on the other as competitive; on the contrary, I see them as complementary, enabling us to achieve a greater success rate among those patients presenting with complex fertility problems.’ This concept is still valid today.

The teaching and practice of microsurgical techniques and principles offers opportunities beyond infertility. It makes the gynaecological surgeon much more conscious of avoiding peritoneal trauma and more careful in tissue handling and tissue care. It requires the surgeon to become more conscious of conservation and overall a better surgeon (Gomel, 1980c), skills that may well be lost without instruction in reconstructive microsurgery. Such skills are necessary to obtain better outcomes in other reproductive surgical procedures, such as myomectomy, ovarian cystectomy, removal of ectopic pregnancy and repair of congenital defects. Reproductive surgery encompasses much more than simply procedures designed to improve fertility. In fact, it includes all surgical procedures performed on the pelvic organs of female children, adolescents and women of childbearing age. It is useful to be reminded that ‘female infertility is frequently caused by misdiagnosis or delayed diagnosis and treatment of acute conditions in young and/or reproductive age women, such as pelvic inflammatory disease, ectopic pregnancy, appendicitis, etc. It is also caused by surgical procedures that are unnecessary, unnecessarily extensive and/or traumatic, resulting in damage to or loss of normal reproductive organs and development of post-operative adhesions’ (Gomel, 2005). The ASRM (ASRM, 2012), with its last ‘Committee opinion: role of tubal surgery in the era of assisted reproductive technology has recognized the important role reconstructive microsurgery continues to have in the treatment of infertility. In turn it is important for university and other training programmes to continue to teach these skills and encourage their practice.

References

  • Allahbadia, Merchant, 2010 G.N. Allahbadia, R. Merchant. Fallopian tube recanalization: lessons learnt and future challenges. Womens Health. 2010;4:531-548
  • ASRM, 2012 ASRM. Committee opinion: role of tubal surgery in the era of assisted reproductive technology. Fertil. Steril. 2012;97:539-545
  • Awartani, McComb, 2003 K. Awartani, P.F. McComb. Microsurgical resection of nonocclusive salpingitis isthmica nodosa is beneficial. Fertil. Steril. 2003;79:1199-1203 Crossref
  • Bergh et al, 1999 T. Bergh, A. Ericson, T. Hillensjo, K.G. Nygren, U.B. Wennerholm. Deliveries and children born after in-vitro fertilization in Sweden 1982–1995: a retrospective cohort study. Lancet. 1999;354:1579-1585 Crossref
  • Bisonette et al, 1999 F. Bisonette, L. Lapensee, R. Bouzayen. Outpatient laparoscopic tubal anastomosis and subsequent fertility. Fertil. Steril. 1999;72:549-552
  • Boeckx et al, 1986 W. Boeckx, S. Gordts, K. Buysse, I. Brosens. Reversibility after female sterilization. Br. J. Obstet. Gynaecol. 1986;93:839-842 Crossref
  • Boeckxstaens et al, 2007 A. Boeckxstaens, P. Devroey, J. Collins, H. Tournaye. Getting pregnant after tubal sterilization: surgical reversal or IVF?. Hum. Reprod. 2007;22:2660-2664 Crossref
  • Boer-Meisel et al, 1986 M.E. Boer-Meisel, E.R. te Velde, J.D. Habbema, J.W. Kardaun. Predicting the pregnancy outcome in patients treated for hydrosalpinx: a prospective study. Fertil. Steril. 1986;45:23-29
  • Caillet et al, 2010 M. Caillet, J. Vandromme, S. Rozenberg, M. Paesmans, O. Germay, M. Degueldre. Robotically assisted laparoscopic microsurgical tubal reanastomosis: a retrospective study. Fertil. Steril. 2010;94:1844-1847 Crossref
  • Canis et al, 1991 M. Canis, G. Mage, J.L. Pouly, H. Manhes, A. Wattiez, M.A. Bruhat. Laparoscopic distal tuboplasty: report of 87 cases and a 4-year experience. Fertil. Steril. 1991;56:616-621
  • CDC, 2003 CDC. Reproductive Health. www.cdc.gov/ART/ART (2003)
  • CDC, 2006 CDC. Reproductive Health. www.cdc.gov/ART/ART (2006)
  • CDC, 2011 CDC. Reproductive Health. www.cdc.gov/ART/ART (2011)
  • Cha et al, 2001 S.H. Cha, M.H. Lee, J.H. Kim, C.N. Lee, T.K. Yoon, K.Y. Cha. Fertility outcome after tubal anastomosis by laparoscopy and laparotomy. J. Am. Assoc. Gynecol. Laparosc. 2001;8:348-352 Crossref
  • Degueldre et al, 2000 M. Degueldre, J. Vandromme, P.T. Huong, G.B. Cadiere. Robotically assisted laparoscopic microsurgical tubal reanastomosis: a feasibility study. Fertil. Steril. 2000;74:1020-1023 Crossref
  • Donnez, Casanas-Roux, 1986 J. Donnez, F. Casanas-Roux. Prognostic factors influencing the pregnancy rate after microsurgical cornual anastomosis. Fertil. Steril. 1986;46:1089-1092
  • Dubuisson, Chapron, 1998 J.B. Dubuisson, C. Chapron. Single suture laparoscopic tubal re-anastomosis. Curr. Opin. Obstet. Gynecol. 1998;10:307-313 Crossref
  • Dubuisson et al, 1994 J.B. Dubuisson, C. Chapron, P. Morice, F.X. Aubriot, H. Foulot, J. Bouquet de Jolinière. Laparoscopic salpingostomy: fertility results according to the tubal mucosal appearance. Hum. Reprod. 1994;9:334-339
  • Dubuisson, Swolin, 1995 J.B. Dubuisson, K. Swolin. Laparoscopic tubal anastomosis (the one stich technique) preliminary results. Hum. Reprod. 1995;10:2044-2046
  • Falcone et al, 2000 T. Falcone, J.M. Goldberg, H. Margossian, L. Stevens. Robotic-assisted laparoscopic microsurgical tubal anastomosis: a human pilot study. Fertil. Steril. 2000;73:1040-1042 Crossref
  • Gillett, Herbison, 1989 W.R. Gillett, G.P. Herbison. Tubocornual anastomosis: surgical considerations and coexistent infertility factors in determining the prognosis. Fertil. Steril. 1989;51:241-246
  • Gomel, 1974 V. Gomel. Tubal reconstruction by microsurgery. (, 1974) Presented at; the Eighth World Congress on Fertility and Sterility (IFFS) Buenos Aires, Argentina. 3–9 November 1974; Abstract No. 391
  • Gomel, 1975 V. Gomel. Laparoscopic tubal surgery in infertility. Obstet. Gynecol. 1975;46:47-49
  • Gomel, 1977a V. Gomel. Tubal reanastomosis by microsurgery. Fertil. Steril. 1977;28:59-65
  • Gomel, 1977b V. Gomel. Reconstructive surgery of the oviduct. J. Reprod. Med. 1977;18:181-190
  • Gomel, 1977c V. Gomel. Salpingostomy by laparoscopy. J. Reprod. Med. 1977;18:26-28
  • Gomel, 1978a V. Gomel. Salpingostomy by microsurgery. Fertil. Steril. 1978;29:380-387
  • Gomel, 1978b V. Gomel. Recent advances in surgical correction of tubal disease producing infertility. Curr. Probl. Obstet. Gynecol. 1978;1:1-60
  • Gomel, 1980a V. Gomel. Microsurgical reversal of sterilization: a reappraisal. Fertil. Steril. 1980;33:587-597
  • Gomel, 1980b V. Gomel. Causes of failure of reconstructive infertility microsurgery. J. Reprod. Med. 1980;24:239-243
  • Gomel, 1980c V. Gomel. The impact of microsurgery in gynecology. Clin. Obstet. Gynecol. 1980;23:1301-1310 Crossref
  • Gomel, 1983a V. Gomel. Microsurgery in Female Infertility. (Little, Brown and Company, Boston, 1983) 100
  • Gomel, 1983b V. Gomel. An odyssey through the oviduct. Fertil. Steril. 1983;39:144-156
  • Gomel, 1983c V. Gomel. Salpingo-ovariolysis by laparoscopy in infertility. Fertil. Steril. 1983;34:607-611
  • Gomel, 1983d V. Gomel. Microsurgery in Female Infertility. (Little, Brown and Company, Boston, 1983) 225-244
  • Gomel, 1983e V. Gomel. Microsurgery in Female Infertility. (Little, Brown and Company, Boston, 1983) 171-181
  • Gomel, 1983f V. Gomel. Microsurgery in Female Infertility. (Little, Brown and Company, Boston, 1983) 245-251
  • Gomel, 1989 V. Gomel. Operative laparoscopy: time for acceptance. Fertil. Steril. 1989;52:1-11
  • Gomel, 2005 V. Gomel. Reproductive surgery. Minerva Ginecol. 2005;57:21-28
  • Gomel, 2007 V. Gomel. Reversal of tubal sterilization versus IVF in the era of assisted reproductive technology: a clinical dilemma. Reprod. Biomed. Online. 2007;15:403-407 Crossref
  • Gomel, 2010 V. Gomel. Reproductive surgery. V. Gomel, A.I. Brill (Eds.) Reconstructive and Reproductive Surgery in Gynecology (Informa Health, London, UK, 2010) 259-280 Crossref
  • Gomel, Erenus, 1990 V. Gomel, M. Erenus. Salpingostomy by microsurgery. The American Fertility Society, 46th Annual Meeting. (, 1990) Program Supplement. P-097, S-106 (abstract)
  • Gomel, McComb, 1985 V. Gomel, P.F. McComb. Microsurgical transposition of the human fallopian tube and ovary with subsequent intrauterine pregnancy. Fertil. Steril. 1985;43:804-808
  • Gomel, McComb, 2006 V. Gomel, P.F. McComb. Microsurgery for tubal infertility. J. Reprod. Med. 2006;51:177-184
  • Gomel, Taylor, 2008 V. Gomel, E. Taylor. Reconstructive tubal surgery. H.A. Rock, H.W. Jones III (Eds.) Te Linde's Operative Gynecology tenth ed. (Lippincott Williams and Wilkins, Philadelphia, 2008) 403-437
  • Gomel, Taylor, 1992 V. Gomel, P.J. Taylor. In vitro fertilization versus reconstructive tubal surgery. J. Assist. Reprod. Genet. 1992;9:306-312
  • Gordts et al, 2009 S. Gordts, R. Campo, P. Puttemans, S. Gordts. Clinical factors determining pregnancy outcome after microsurgical tubal reanastomosis. Fertil. Steril. 2009;92:1198-1202 Crossref
  • Henderson, 1984 S.R. Henderson. The reversibility of female sterilization with the use of microsurgery: a report on 102 patients with more than one year of follow-up. Am. J. Obstet. Gynecol. 1984;149:57-61
  • Hou et al, 2014 Hou H.Y., Chen Y.Q., Li T.C., Hu C.X., Chen X., Yang Z.H. Outcome of laparoscopy-guided hysteroscopic tubal catheterization for infertility due to proximal tubal obstruction. J. Minim. Invasive Gynecol. 2014;21:272-278 Crossref
  • James, Gomel, 1990 C. James, V. Gomel. Surgical management of tubal factor infertility. Curr. Opin. Obstet. Gynecol. 1990;2:200-206
  • Karlström, Bergh, 2007 P.O. Karlström, C. Bergh. Reducing the number of embryos transferred in Sweden-impact on delivery and multiple birth rates. Hum. Reprod. 2007;22:2202-2207
  • Kim et al, 1997a J.D. Kim, K.S. Kim, J.K. Doo, C.H. Rhyeu. A report on 387 cases of microsurgical tubal reversals. Fertil. Steril. 1997;68:875-880 Crossref
  • Kim et al, 1997b S.H. Kim, C.J. Shin, J.G. Kim, S.Y. Moon, J.Y. Lee, Chang Y.S. Microsurgical reversal of tubal sterilization: a report on 1118 cases. Fertil. Steril. 1997;68:865-870 Crossref
  • Kosasa, Hale, 1988 T.S. Kosasa, R.W. Hale. Treatment of hydrosalpinx using a single incision eversion procedure. Int. J. Fertil. 1988;33:319-323
  • Land et al, 1997 J.A. Land, D.A. Courtar, J.L. Evers. Patient dropout in an assisted reproductive technology program: implications for pregnancy rates. Fertil. Steril. 1997;68:278-281 Crossref
  • Lang, Dunaway, 1996 Lang E.K., H.H. Dunaway. Recanalization of obstructed fallopian tube by selective salpingography and transvaginal bougie dilatation: outcome and cost analysis. Fertil. Steril. 1996;66:210-215
  • Larsson, 1982 B. Larsson. Late results of salpingostomy combined with salpingolysis and ovariolysis by electromicrosurgery in 54 women. Fertil. Steril. 1982;37:156-160
  • Lilford, Watson, 1990 R.J. Lilford, A.J. Watson. Has in vitro fertilization made salpingostomy obsolete?. Br. J. Obstet. Gynaecol. 1990;97:557-560 Crossref
  • Madelenat et al, 1977 P. Madelenat, J. DeBrux, R. Palmer. L'etiologie des obstructions tubaires proximales et son róle dans le prognostic des implantations. Gynecologie. 1977;28:47-53
  • Marana et al, 1999 R. Marana, G.F. Catalano, L. Muzii, P. Caruana, F. Margutti, S. Mancuso. The prognostic role of salpingoscopy in laparoscopic tubal surgery. Hum. Reprod. 1999;14:2991-2995 Crossref
  • McComb, 1986 P.F. McComb. Microsurgical tubocornual anastomosis for occlusive cornual disease: reproducible results without the need for tubouterine implantation. Fertil. Steril. 1986;46:571-577
  • McComb, Gomel, 1980 P.F. McComb, V. Gomel. Cornual occlusion and its microsurgical reconstruction. Clin. Obstet. Gynecol. 1980;23:1229-1241
  • McComb, Taylor, 2001 P.F. McComb, R.C. Taylor. Pregnancy outcome after unilateral salpingostomy with a contralateral patent oviduct. Fertil. Steril. 2001;76:1278-1279 Crossref
  • Murray et al, 1998 D.L. Murray, A.W. Sagoskin, E.A. Widra, M.J. Levy. The adverse effect of hydrosalpinges on in vitro fertilization pregnancy rates and the benefit of surgical correction. Fertil. Steril. 1998;69:41-45 Crossref
  • Oh, 1996 S.T. Oh. Tubal patency and conception rates with three methods of laparoscopic terminal salpingostomy. J. Am. Assoc. Gynecol. Laparosc. 1996;3:519-523 Crossref
  • Olivius et al, 2004 C. Olivius, B. Friden, G. Borg, C. Bergh. Why do couples discontinue in vitro fertilization treatment? A cohort study. Fertil. Steril. 2004;81:258-261 Crossref
  • Palermo et al, 1992 G. Palermo, H. Joris, P. Devroey, A. Van Steirteghem. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet. 1992;340:17-18 Crossref
  • Paterson, 1985 P.J. Paterson. Factors influencing success of microsurgical tuboplasty for sterilization reversal. Clin. Reprod. Fertil. 1985;3:57-64
  • Patton et al, 1987 P.E. Patton, T.J. Williams, C.B. Coulam. Microsurgical reconstruction of the proximal oviduct. Fertil. Steril. 1987;47:35-39
  • Putman et al, 1990 J.M. Putman, A.E. Holden, D.L. Olive. Pregnancy rates following tubal anastomosis: Pomeroy partial salpingectomy versus electrocautery. J. Gynecol. Surg. 1990;6:173-178 Crossref
  • Ribeiro et al, 2004 S.C. Ribeiro, R.A. Tormena, C.G. Giribela, C.R. Izzo, N.C. Santos, J.A. Pinotti. Laparoscopic tubal anastomosis. Int. J. Gynaecol. Obstet. 2004;84:142-146 Crossref
  • Rock et al, 1987 J.A. Rock, D.S. Guzick, E. Katz, H.A. Zacur, T.M. King. Tubal anastomosis: pregnancy success following the reversal of Falope ring or monopolar cautery sterilization. Fertil. Steril. 1987;48:13-17
  • Rodgers et al, 2007 A.K. Rodgers, J.M. Goldberg, J.P. Hammel, T. Falcone. Tubal anastomosis by robotic compared with outpatient minilaparotomy. Obstet. Gynecol. 2007;109:1375-1380 Crossref
  • Rouzi et al, 1995 A.A. Rouzi, M. Mackinnon, P.F. McComb. Predictors of success of reversal of sterilization. Fertil. Steril. 1995;64:29-36
  • SART, Society for Assisted Reproductive Technology; The American Fertility Society, 1992 SART, Society for Assisted Reproductive Technology; The American Fertility Society. In vitro fertilization-embryo transfer (IVF-ET) in the United States: 1990 results generated from the IVF-ET Registry. Fertil. Steril. 1992;57:15-24
  • SART, Society for Assisted Reproductive Technology; American Society for Reproductive Medicine, 2004 SART, Society for Assisted Reproductive Technology; American Society for Reproductive Medicine. Assisted reproductive technology in the United States: 2000 results generated from the American Society for Reproductive Medicine Registry. Fertil. Steril. 2004;1:207-220
  • Schepens et al, 2011 J.J. Schepens, B.W. Mol, M.A. Wiegerinck, S. Houterman, C.A. Koks. Pregnancy outcomes and prognostic factors from tubal sterilization reversal by suturless laparoscopical re-anastomosis: a retrospective cohort study. Hum. Reprod. 2011;26:354-359 Crossref
  • Schippert et al, 2010a C. Schippert, C. Bassler, P. Soergel, U. Hille, B. Hollwitz, G.J. Garcia-Rocha. Reconstructive, organ preserving microsurgery in tubal infertility: still an alternative to in vitro fertilization. Fertil. Steril. 2010;93:1359-1361 Crossref
  • Schippert et al, 2010b C. Schippert, U. Hille, C. Bassler, P. Soergel, B. Hollwitz, G.J. Garcia-Rocha. Organ-preserving and reconstructive microsurgery of Fallopian tubes in tubal infertility: still an alternative to in vitro fertilization (IVF). J. Reconstr. Microsurg. 2010;26:317-332
  • Schippert et al, 2012 C. Schippert, P. Soergel, I. Staboulidou, C. Bassler, S. Gagalick, P. Hillemanns, K. Buchler, G.J. Garcia-Rocha. The risk of ectopic pregnancy following tubal reconstructive microsurgery and assisted reproductive technology procedures. Arch. Gynecol. Obstet. 2012;285:863-871 Crossref
  • Schlaff et al, 1990 W.D. Schlaff, D.K. Hassiakos, M.D. Damewood, J.A. Rock. Neosalpingostomy and distal tubal obstruction: prognostic factors and impact of surgical technique. Fertil. Steril. 1990;54:984-990
  • Schlösser et al, 1993 H.W. Schlösser, C. Frantzen, N. Mansour, H.C. Verhoeven. Sterilisation Refertilisierung. Erfahrungen und Ergebnisse bei 119 microchirurgisch refertilisierten Frauen. Geburtshilfe Frauenheilkd. 1993;43:213-216
  • Seppälä, 1985 M. Seppälä. The world collaborative report on in vitro fertilization and embryo replacement: current state of the art in January 1984. Ann. N. Y. Acad. Sci. 1985;442:558-562
  • Silber, Cohen, 1984 S.J. Silber, R. Cohen. Microsurgical reversal of tubal sterilization: factors affecting pregnancy rate, with long-term follow-up. Obstet. Gynecol. 1984;64:67-82
  • Spivak et al, 1986 M.M. Spivak, C.L. Librach, D.M. Rosenthal. Microsurgical reversal of sterilization: a six-year study. Am. J. Obstet. Gynecol. 1986;154:355-361 Crossref
  • Strandell et al, 1994 A. Strandell, U. Waldenström, L. Nilsson, L. Hamberger. Hydrosalpinx reduces in-vitro fertilization/embryo transfer pregnancy rates. Hum. Reprod. 1994;9:861-863
  • Strandell et al, 1998 A. Strandell, A. Sjögren, U. Bentin-Ley, J. Thorburn, L. Hamberger, M. Brännström. Hydrosalpinx fluid does not adversely affect the normal development of human embryos and implantation in vitro. Hum. Reprod. 1998;13:2921-2925 Crossref
  • Strandell et al, 2001 A. Strandell, A. Lindhard, U. Waldenström, J. Thorburn. Hydrosalpinx and IVF outcome: cumulative results after salpingectomy in a randomized, controlled trial. Hum. Reprod. 2001;16:2403-2410
  • Swolin, 1975 K. Swolin. Electro microsurgery and salpingostomy: long-term results. Am. J. Obstet. Gynecol. 1975;121:418-419
  • Taylor et al, 2001 R.C. Taylor, J. Berkowitz, P.F. McComb. Role of salpingostomy in the treatment of hydrosalpinx. Fertil. Steril. 2001;75:594-600 Crossref
  • te Velde et al, 1989 E.R. te Velde, M.E. Boer-Meisel, J. Meisner, J. Schoemaker, J.D.F. Habbema. The significance of preoperative hysterosalpingography and laparoscopy for predicting the pregnancy outcome in patients with a bilateral hydrosalpinx. Eur. J. Obstet. Gynecol. Reprod. Biol. 1989;31:33-45 Crossref
  • te Velde et al, 1990 E.R. te Velde, M.E. Boer-Meisel, C.W.N. Looman, J.D.F. Habbama. Factors influencing success or failure after reversal of sterilization: a multivariate approach. Fertil. Steril. 1990;54:270-277
  • The American Fertility Society, 1998 The American Fertility Society. The 1988 American Fertility Society classifications of adnexal adhesions, distal tubal occlusion, tubal occlusion secondary to tubal ligation. Fertil. Steril. 1998;49:944-954
  • Thurmond, 1991 A.S. Thurmond. Selective salpingography and fallopian tube recanalization. AJR Am. J. Roentgenol. 1991;156:33-38 Crossref
  • Tomazevic et al, 1996 T. Tomazevic, M. Ribic-Pucelj, A. Omahen, B. Colja. Microsurgery and in-vitro fertilization and embryo transfer for infertility resulting from pathological proximal tubal blockage. Hum. Reprod. 1996;11:2613-2617 Crossref
  • Trimbos-Kemper, 1990 T.C. Trimbos-Kemper. Reversal of sterilization in women over 40 years of age: a multicenter survey in the Netherlands. Fertil. Steril. 1990;53:575-577
  • Tulandi, Vilos, 1985 T. Tulandi, G.A. Vilos. A comparison between laser surgery and electrosurgery for bilateral hydrosalpinx: a two year followup. Fertil. Steril. 1985;44:846-848
  • Van Voorhis et al, 1998 B.J. Van Voorhis, A.E. Sparks, C.H. Syrop, D.W. Stowall. Ultrasound guided aspiration of hydrosalpinges is associated with improved pregnancy and implantation rates after in-vitro fertilization cycles. Hum. Reprod. 1998;13:736-739 Crossref
  • Verhoeven et al, 1983 H.C. Verhoeven, H. Berry, C. Frantzen, H.W. Schlösser. Surgical treatment for distal tubal occlusion: a review of 167 cases. J. Reprod. Med. 1983;28:293-304
  • Wiegerinck et al, 2005 M.A. Wiegerinck, M. Roukema, P.H. van Kessel, B.W. Mol. Suturless re-anastomosis by laparoscopy versus microsurgical reanastomosis by laparotomy for sterilization reversal. Hum. Reprod. 2005;20:2355-2358 Crossref
  • Winston, 1980 R.M.L. Winston. Reversal of sterilization. Clin. Obstet. Gynecol. 1980;23:1261-1265
  • Xue, Fa, 1989 Xue P., Fa Y.Y. Microsurgical reversal of female sterilization. J. Reprod. Med. 1989;34:451-455
  • Yoon et al, 1999 T.K. Yoon, H.R. Sung, Kang H.G., S.H. Cha, C.N. Lee, K.Y. Cha. Laparoscopic tubal anastomosis: fertility outcome in 202 cases. Fertil. Steril. 1999;72:1121-1126 Crossref
  • Zouves et al, 1991 C. Zouves, M. Erenus, V. Gomel. Tubal ectopic pregnancy after in vitro fertilization and embryo transfer: a role for proximal occlusion or salpingectomy after failed distal tubal surgery?. Fertil. Steril. 1991;56:691-695
rbmo1445-fig-5001

Victor Gomel, Professor Emeritus and former Head in the Department of Obstetrics and Gynecology, University of British Columbia, is internationally known for his pioneering work in both gynecologic microsurgery and operative laparoscopy. His in-vitro fertilization program conceived Canada's first IVF baby, born in 1983. He has published extensively, received honorary memberships and awards of excellence from numerous international scientific societies and universities, in recognition of his pioneering work. He received several prestigious awards, including the Chevalier de la Légion d'Honneur from France; Doctor of Science, Honoris causa, and the Jacques Salat-Baroux reproduction prize, from the French National Academy of Medicine.

Footnotes

Department of Obstetrics and Gynecology, University of British Columbia, Vancouver, BC, Canada