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Role of reproductive surgery in the era of assisted reproductive technology
Best Practice & Research Clinical Obstetrics & Gynaecology, 6, 26, pages 747 - 755
Reproductive surgery could be divided into surgery as a primary treatment for infertility, surgery to enhance in-vitro fertilisation outcome, and surgery for fertility preservation. A shift has occurred away from surgery as a primary treatment of infertility to surgery playing a crucial part in enhancing in-vitro fertilisation outcome and for fertility preservation. A normal uterine cavity is a prerequisite for implantation, and hysteroscopic correction of intrauterine pathology, including polypectomy, myomectomy and metroplasty, increases the chances of having a successful pregnancy. Management of hydrosalpinx before in-vitro fertilisation treatment by laparoscopic salpingectomy or proximal tubal occlusion increases the in-vitro fertilisation delivery rate. Finally, surgery plays an important role in preservation of fertility. This includes laparoscopic ovarian transposition, ovarian tissue removal for cryopreservation and ovarian transplantation.
Keywords: assisted reproductive technology, endometrial polyp, endometriosis, fertility preservation, hysteroscopy, infertility, infertility surgery, in-vitro fertilization, laparoscopy, myoma, reproductive surgery.
Traditionally, infertility caused by tubal diseases, periadnexal adhesions or endometriosis has been treated surgically. The initial approach to reproductive surgery was by laparotomy, and was then followed by laparoscopy and hysteroscopy. The place of laparotomy in infertility has become limited. With the advancement of in-vitro fertilisation (IVF) treatment, even the role of reproductive surgery by minimally invasive techniques has been questioned. In this review, we evaluate the evolution and the place of reproductive surgery in the era of assisted reproductive technology.
Investigations of peritoneal and tubal factors
Transvaginal ultrasound examination is an important diagnostic tool in the investigation of infertility. It provides information about the uterus and the ovaries, including antral follicle count and a possible ovarian cyst. As tubal factors account for 30–40% of female infertility, evaluation of the cause of infertility should include hysterosalpingography examination. 1 Checking the patency of the fallopian tubes is not necessary if there is another indication for IVF, such as severe male factors, although assessment of the uterine cavity may still be necessary. Transvaginal ultrasound examination provides information about tubal patency as well as the uterine cavity. Sonohysterography is an alternative diagnostic tool. 2
If endometrioma is suspected, magnetic resonance imaging (MRI) examination is advocated. Magnetic resonance imaging sensitivity (71%) and specificity (82%) to diagnose endometriosis with cystic structures are higher than those of ultrasound. 2 Its sensitivity for diagnosing endometriotic implants is only 13%. In addition, MRI is costly. Using MRI in the investigation of infertility is not cost-effective.
The presence of endometriosis can be established by laparoscopy examination. In addition, laparoscopic treatment of stage I and II endometriosis is associated with an increased pregnancy rate. 3 The pregnancy rate at 36 weeks after surgery, however, was only 30.7%. In addition, a meta-analysis showed that laparoscopic ablation of endometriosis enhances fecundity only slightly (odds ratio 1.66). 4 The effects are, therefore, minimal. In women with unexplained infertility, a randomised-controlled trial 5 showed that laparoscopy did not increase the pregnancy rate. As a result, we do not include laparoscopy in our work-up for infertility.
Investigations of the uterine cavity
Besides evaluation of tubal patency, hysterosonography and hysterosalpingography examination provides information about the uterine cavity. Hysteroscopy is not routinely carried out in the investigation of infertility except when an intrauterine lesion is suspected.
Surgical treatment of infertility
Surgical treatment for infertility can be divided into hysteroscopy and laparoscopy.
Today, it is clear that the presence of intrauterine pathology is associated with decreased fertility.
In a randomised-controlled trial of 215 women with endometrial polyp who were scheduled to undergo intrauterine insemination up to four treatment cycles started 3 months after surgery, the investigators allocated participants into hysteroscopic polypectomy (n = 107) or endometrial biopsy only (n = 109). 6 The pregnancy rate in the polypectomy group (51.4%) was significantly higher than in the control group (25.4%). Furthermore, more than one-half of women in the polypectomy group conceived spontaneously within 3 months after surgery. This was independent of the size of the polyp.
In addition to endometrial polyp, submucous myoma also decreases fertility. A meta-analysis showed that submucous fibroids or intramural fibroids with a submucosal component decreased clinical pregnancy (RR 0.36, 95% CI 0.18 to 0.74) and implantation rates (RR 0.28, CI 0.12 to 0.65). 7 Casini et al. 8 conducted a randomised-controlled trial of 52 women, and reported that removal of submucous myoma led to a significant increase in pregnancy rate (from 27.2 to 43.3%) and a decrease in miscarriage rate (from 50% to 38.5%). Shokeir et al. 9 conducted another randomised-controlled study among women with submucous myoma and unexplained infertility, and found that the pregnancy rate in the myomectomy group was 63.4% and in the control group was 28.2% (RR 2.1; 95% CI 1.5 to 2.9).
No randomised-controlled trial has been conducted among women with uterine septum. In a prospective study, however, an association was found between hysteroscopic removal of uterine septum (hysteroscopic metroplasty) and a higher pregnancy rate than in women with unexplained infertility. 10 The live birth rate was also higher in the metroplasty group than in the group with idiopathic infertility (34.1% and 18.9%, respectively).
Hysteroscopic lysis of adhesions
As with uterine septum, the association between infertility, miscarriage and intrauterine adhesions derived mainly from observational studies.11, 12, 13, and 14Roy et al. 14 evaluated 89 women with infertility and reported that the pregnancy rate after hysteroscopic lysis of mild adhesions (58%) was higher than that of moderate adhesions (30%) and severe adhesions (33.3%). Fernandez et al. 13 studied 64 women with severe adhesions. Hysteroscopic removal of the adhesions led to a live birth rate of 32.8%. 13 In a retrospective study of 43 women, we found an overall pregnancy rate of 51.2% and a live birth rate of 32.6% after removal of the adhesions. 15
The benefit of diagnostic laparoscopy in women with no risk factors for intra-abdominal adhesions is small. In addition, treatment of stage I or II endometriosis leads to a small increase in pregnancy rate. Accordingly, the use of laparoscopy as a diagnostic tool in infertility has diminished markedly. Furthermore, today, alternative treatments of infertility are available, including superovulation and intrauterine insemination, and IVF.
On the other hand, laparoscopy is a surgical approach of choice for those who are found to have pelvic pathology on imaging. Most laparoscopic-promoting procedures should be carried out by laparoscopy and not by laparotomy.
Laparoscopic tubal surgery
The results of tubal surgery are inferior compared with IVF treatment. In addition, surgery is associated with delayed conception and increased ectopic pregnancy rate. The incidence of ectopic pregnancy after IVF is 1.8 %, 16 which is similar to that in the general population. The IVF ectopic rate, however, doubles in those with tubal factor. The pregnancy rate per cycle after IVF treatment is 40.6%. This compares favourably with the pregnancy rate 12 months after laparoscopic tuboplasty.
In a randomised-controlled study, 17 the rates of pregnancy and ectopic pregnancy 24 months after salpingostomy for hydrosalpinx by laparotomy were 43.7% and 5.0%, and after laparoscopic salpingostomy were 41.6%, and 3.9%, respectively. 17 The results of a meta-analysis also showed similar overall pregnancy rates between laparoscopy and laparotomy. 18 The overall intrauterine pregnancy rates in women with mild hydrosalpinx were 32.8% after laparotomy and 39.5% after laparoscopic neo-salpingostomy.
For fimbrial phimosis, laparoscopic fimbrioplasty is associated with cumulative pregnancy rates of 35% and 58% at 12 and 24 months, respectively. 19
The most successful tubal surgery is reversal of tubal sterilisation. In general, tubal anastomosis is used in fertile women who have undergone tubal sterilisation. In a strict sense, they are not quite infertile. The cumulative pregnancy rates after laparoscopic tubal anastomosis were 60.3% and 79.4% at 6 and 12 months after surgery, respectively. The ectopic pregnancy rate was 3.2%. 20
Besides tubal anastomosis, other reconstructive tubal operations are associated with inferior pregnancy results compared with IVF. It also takes many months for conception to occur. The place of tubal surgery is therefore limited.
Laparoscopic treatment of ovarian endometrioma
In our practice, instead of relying on laparoscopy for diagnosis, we identify adnexal mass from diagnostic imaging. Laparoscopy is carried out for treatment purposes. For example, we identify ovarian endometrioma on transvaginal ultrasound and laparoscopy is carried out to remove the endometriotic cyst.
Ovarian endometrioma can be treated by fenestration and ablation or by excision or stripping the ovarian cyst wall. With fenestration, the ovarian cyst wall is leftin situ. The 12- and 24-month cumulative pregnancy rates after excision were 50% and 66.7%, and after fenestration were about 15% and 23.5%, respectively. 21 Compared with the fenestration technique, excision of the endometrioma is associated with a higher pregnancy rate and a lower recurrence rate.21, 22, 23, and 24
In-vitro fertilisation outcome-enhancing surgery
Surgery plays an important role in enhancing IVF outcome.
Hysteroscopy should be carried out at least after one failed IVF treatment. Fatemi et al. 25 studied 678 asymptomatic infertile women undergoing a first IVF treatment. They found endometrial polyps in 6% and submucous myomas in 1% of cases. Other findings were intrauterine adhesions (2%) and uterine septum (2%). The overall prevalence of intrauterine abnormalities among these women was 11%. Karayalcin et al. 26 evaluated 2500 women before IVF treatment, and found intrauterine pathology in 22.9% of cases. 26 These included endometrial polyps (7.7%), submucous myoma (3.8%), intrauterine adhesions (1.1%) and uterine septum (2.9%). The presence of those lesions decreases fertility.
Tomaževič et al. 27 evaluated the effect of uterine septum on IVF outcome among 2481 embryo transfers in IVF and intracytoplasmic sperm injection cycles. 27 The study group consisted of 289 women undergoing embryo transfers before and 538 women undergoing embryo transfers after hysteroscopic metroplasty. It was then compared with two consecutive embryo transfers in the control group. The live birth rate in women with a large septum was 2.7% before surgery, 15.6% after surgery and 20.9% in the control group. In women with a small septum, the live birth rate was 2.8% before surgery, 18.6% after surgery, and 21.9% in the control group.
Hysteroscopic proximal tubal occlusion
The presence of hydrosalpinx impairs IVF outcomes by decreasing the implantation and pregnancy rates. 28 This could be caused by the possible toxicity of hydrosalpinx fluid to the embryo or by the mechanical effect of the fluid impairing implantation. A relatively new application of hysteroscopy in women with hydrosalpinx before IVF treatment is placement of a device occluding the proximal part of the fallopian tube. 29 The most common device used for this purpose is Essure®(Conceptus Inc, Scottsdale, AZ).30, 31, and 32In a small study, 32 the procedure led to a 40% ongoing pregnancy rate and 20% live birth rate after one IVF cycle.
Yet, this procedure should still be considered experimental. The number of published cases is small, and the effects of the device on the pregnancy still need to be evaluated in a large number of cases. Today, the procedure should be limited to women at risk of laparoscopy, including those with previous multiple laparotomies or bowel resection.
If laparoscopic surgery as the main treatment of infertility has fallen into disfavor, it plays an important role in enhancing IVF outcome.
Owing to the experimental nature of hysteroscopic proximal tubal occlusion for hydrosalpinx, laparoscopic removal of the hydrosalpinx (salpingectomy) before IVF is the procedure of choice. Randomised-controlled trials have shown that pre-IVF salpingectomy leads to higher IVF-pregnancy and delivery rates.33, 34, 35, and 36For example, Strandell et al. 34 reported that the delivery rate in the salpingectomy group (28.6%) was significantly higher than in the control group (16.3%). Kontoravdis et al. 35 found that the implantation and on-going pregnancy rates were 10.4% and 34.2% in the salpingectomy group and 4.6% and 18.7% in the control non-intervention group. Because of the possible decreased ovarian function after salpingectomy, it is important to excise the hydrosalpinx close to the tube to avoid compromising the blood supply to the ovary. 37
Laparoscopic proximal tubal occlusion
In women in whom the distal fallopian tube is buried in dense and severe adhesions, occluding the tube proximally close to the uterus is preferable. In a randomised-controlled trial, the investigators compared laparoscopic salpingectomy, proximal tubal occlusion and no intervention. 35 The ongoing IVF pregnancy rates after salpingectomy or proximal tubal occlusion were similar. The resulting blocked tube proximally and distally, however, traps the hydrosalpinx fluid and the tube might become dilated.
Repeat surgery for advanced endometriosis
In one study, 38 the cumulative pregnancy rates in women with stage 3 and 4 endometriosis were 33.3% after initial surgery and 24% after reoperation. The cumulative pregnancy rate after a second cycle of IVF and in-vivo transfer of the embryo to the uterus was 69.6%. This study suggests that, compared with the initial surgery, the results of repeat surgery in women with advanced endometriosis are inferior to those of IVF and in-vivo transfer of the embryo to the uterus. 38 Others supported their findings. 39
Surgical management of ovarian endometrioma before in-vitro fertilisation
Results of studies evaluating the effect of endometrioma on IVF outcome have been mixed.40, 41, 42, 43, 44, 45, and 46It seems that small endometriomas of 4 cm or less do not influence IVF outcome. Almog et al. 47 found no differences in the number of oocyte retrieved from the ovary that contained endometrioma (6 ± 0.4) and from the healthy ovary (6.1 ± 0.5). The embryo quality and the clinical pregnancy rate were also similar.40, 43, 44, and 45
Large endometrioma that interferes with oocyte retrieval needs to be operated. As previously discussed, this could be carried out by excision (stripping) or by fenestration and ablation. It seems that excision of ovarian endometrioma is associated with reduced ovarian reserve.47, 48, 49, and 50We recently compared the response of operated and non-operated ovaries to gonadotropin stimulation in 38 women with ovarian endometrioma. 47 The antral follicle count, number of dominant follicles, and number of oocytes collected in the operated ovary were significantly lower than in the non-operated ovary (4.5 ± 3.8v7.4 ± 5.2; 4.7 ± 3.9v7.6 ± 4.7, 4.3 ± 3.9v7.4 ± 4.8, respectively). This could be caused by an inadvertent excision of healthy ovarian tissue, or from vascular injury and ischaemia secondary to electrocoagulation. In contrast, fenestration and ablation of endometrioma does not seem to impair ovarian response to gonadotropins. 50
Tsoumpou et al. 51 conducted a meta-analysis involving five studies and compared the outcome of IVF between women who had surgical treatment of endometrioma and untreated women. 51 No difference was found in the pregnancy rate per cycle (OR 0.92, 95% CI 0.61 to 1.38) between the two groups. Similarly, the IVF clinical pregnancy rate between the treated and the non-treated groups was comparable.
It seems that the best surgical treatment of ovarian endometrioma remains excision.21 and 23In the presence of poor surgical plane between the ‘cyst wall’ and the surrounding ovarian tissue, fenestration and selective ablation of the wall of the endometrioma should be considered. Recurrence rate of the endometrioma with the ablation technique is indeed increased, but the presence of endometrioma does not impair the IVF outcome. The purpose of surgery in infertile women is to improve fertility and not to eradicate the disease, such as for women with chronic pelvic pain.
The effect of intramural myoma on IVF outcome remains unclear. In a randomised-controlled trial, intramural myoma with submucous component was found to be associated with decreased pregnancy rates. 8 In a meta-analysis of 19 studies, no significant difference was found in IVF live birth rate in women with and without intramural myoma. 52
Surgery for fertility preservation
Laparoscopy plays an important role in fertility preservation, especially in women undergoing pelvic radiation. Laparoscopy is also a tool for obtaining ovarian tissue for ovarian preservation and for transplantation.
Laparoscopic ovarian transposition
Women with haematologic, neurologic, genitourinary, or low intestinal malignancies are often treated with pelvic irradiation. In order to protect the ovaries from the radiation, laparoscopic ovarian transposition (ovarian suspension, ovariopexy, or oophoropexy) could be carried out.53, 54, 55, 56, and 57In women younger than 40 years old, the procedure is associated with preservation of ovarian function in 88.6% of cases. 55 Among women with early cervical cancer who underwent laparoscopic ovarian suspension before radiation, normal ovarian function was found in 50–63.6%.56 and 57
During surgery, ovarian tissue could be excised for ovarian cryopreservation and for possible transplantation in the future. Because of the high rate of ovarian failure, ovarian transposition is not recommended in women over 40 years old.
Ovarian tissue transplantation
The best method for fertility preservation is embryo cryopreservation, followed by oocyte and then ovarian cryopreservation. For prepubertal females, ovarian cryopreservation is the only alternative for fertility preservation. 58 In women who wish to conceive, the current and proven method is to graft the frozen-thawed ovarian tissue into the ovarian fossa or into the remaining and irradiated ovary.
In a review, 59 eight out of 25 women conceived after ovarian tissue transplantation. The tissue becomes functional 3–4 months after transplantation.60, 61, and 62The graft might last up to 3 years, depending on the amount of ovarian tissue transplanted. Accordingly, ovarian transplantation should be carried out only when the patient is ready to conceive. Today, at least 12 live births have resulted from transplantation of frozen-thawed ovarian tissue.61, 62, 63, 64, 65, 66, 67, and 68
Reproductive surgery could be divided into surgery as a primary treatment of infertility, surgery to enhance IVF outcome, and surgery for fertility preservation. The role of surgery as a primary treatment of infertility has changed and, today, surgery plays a crucial part in enhancing IVF outcome and in fertility preservation. A normal uterine cavity is a prerequisite for implantation, and hysteroscopic correction of intrauterine pathology, including polypectomy, myomectomy and metroplasty, increases the chances of having a successful pregnancy. Management of hydrosalpinx before IVF treatment by laparoscopic salpingectomy or proximal tubal occlusion increases the IVF delivery rate. Finally, surgery plays an important role in preserving fertility. This includes laparoscopic ovarian transposition, ovarian tissue removal for cryopreservation and ovarian transplantation.
- The role of reproductive surgery as primary treatment of infertility is limited.
- Laparotomy for treatment of infertility has been replaced by laparoscopy and hysteroscopy.
- Surgery plays a crucial role in enhancing IVF outcome and for fertility preservation.
- Hysteroscopy correction of intrauterine abnormality, including polyp, submucous myoma, intrauterine adhesions and uterine septum, enhances pregnancy and delivery rates.
- Small endometriomas do not have to be removed before IVF treatment.
- Removal of hydrosalpinx increases IVF delivery rate.
- Laparoscopic ovarian suspension before radiation preserves menstrual functions in most cases.
- Fertility preservation should be offered to young women undergoing treatment with gonadotoxic agent.
- Effects of the Essure®device on IVF pregnancy and delivery rates and on the obstetrical outcome.
- Effects of uterine septum as well as intrauterine adhesions on delivery rates.
- Developing oocytes from frozen-thawed ovarian tissue.
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Department of Obstetrics and Gynecology, McGill University, Montreal, QC, Canada
∗ Corresponding author. McGill University Health Center, Women's Pavilion, 687 Pine Ave. West, Montreal, QC, H3A 1A1, Canada. Fax: +1 514 843 1448.
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