Updates on laparoscopic cervical cerclage: obstetric outcomes and surgical techniques

Aim: Preterm birth is a worldwide health problem. After unsuccessful transvaginal cerclage, the transabdominal isthmo-cervical cerclage can be indicated. A laparoscopic approach has been described. Methods: A search was performed including the combination of: “((cerclage) AND (laparoscopy)) AND (pregnancy)”. A systematic review was performed to compare indications, outcomes, techniques, and safety. Results & discussion: 42 articles were found through database search. 30 articles were included for review. By reviewing the literature, the transabdominal cervico-isthmic laparoscopic cerclage is highly effective in selected patients with a history of refractory cervical insufficiency. This technique has a high neonatal survival rate when placed in preconceptional or post conceptional patients. Moreover, laparoscopic cervical cerclage is a safe procedure when laparoscopic expertise is present.


Strategy of research
The research was performed using the PubMed database. Filters applied: in the last 5 years. A search was performed including the combination of the following words: "((cerclage) AND (laparoscopy)) AND (pregnancy)". The search and selection criteria were restricted to the English language.

Selection of articles
The selection procedure followed the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) principles and is presented using a PRISMA flow chart ( Figure 1). Recent articles were prioritized. Evidence included human, animal and cadaver data. Each article's title, abstract and text were reviewed for their appropriateness and their relevance. Full text analysis of eligible studies was performed. The initial list of selected papers was enriched by individual suggestions of the authors of the present review. Articles concerning robot-assisted transabdominal cerclage for the prevention of preterm birth were excluded. Reference lists from relevant papers were hand-searched for additional reports. The risk of bias and data synthesis was taken into consideration. Selective outcomes reporting bias was minimized by choosing the common outcomes in several studies. Confounding and publication bias was diminished by the adoption of standardized stricter inclusion and exclusion criteria.

Extraction of data
The collection of data was done. Data were grouped depending on the type of clinical studies. Obstetrical outcomes and the differences in the surgical techniques were all reviewed. Inclusion criteria were hospitalized high risk women who underwent a laparoscopic cerclage preconceptionally or post conceptionally.
The operative technique and characteristics were as follows: -Gestational age at the moment of the cerclage.
-Type of the tape.
-Gestational age at the delivery.

Results
Thirty studies were included in our review. The PRISMA flow chart is presented in Figure 1. All these studies have reported the indications, surgical techniques, complications, and obstetrical and postnatal outcomes. The authors suggested four articles due to their relevant historical findings.
Lesser et al. [3] and Scibetta et al. [4] were the first authors who described the laparoscopic cervical cerclage. Since the publication of these two manuscripts, several case series have been reported in order to discuss the experience in their institution, the surgical and obstetrical outcomes and complications pre-and post-operative. The most common primary outcome was neonatal survival, and the secondary outcome was delivery ≥34 weeks of gestation. All the obstetrical outcomes are resumed in Table 1.
Time of the procedure & outcomes Ades et al. had an important experience in laparoscopic cervical cerclage. They shared the outcomes of 121 pregnancies after a pre-pregnancy laparoscopic cervical cerclage in women at high risk for pre-term from 2007 to 2017 [14]. The perinatal survival rate was 98.5% with a mean gestational age at delivery of 35.2 weeks. Moreover, Ades et al. published a paper concerning their experience in laparoscopic transabdominal cerclage in 19 pregnant women at 6-11 weeks of gestation [9]. The perinatal survival rate was 100% with an average gestational age at delivery of 37.1 weeks. Furthermore, Ades et al. reported the obstetric outcomes of subsequent pregnancies in women who had a laparoscopic transabdominal cerclage left in situ [6]. Of 22 women, the neonatal survival rate was 95% in the second pregnancy and 86% of women delivered after 34 weeks of gestation. On the other hand, the neonatal survival rate was 100% (3/3) in the third pregnancies, and 100% (3/3) of women delivered after 34 weeks of gestation.

Modified LCC
The largest case series was reported by Chung et al. who underwent a retrospective observational cohort study of patients operated on modified laparoscopic transabdominal cervical cerclage from 2003 to 2018 with a sample size of 299 pregnant women with a mean gestational age of 12.5 weeks [19]. There were 176 of 205 successful deliveries via cesarean section with a fetal survival rate of 85.9%. This technique is described first by Shin et al. in 2015, and it differs from the conventional laparoscopic cervical cerclage by the origin of the insertion of the tape -laterally to uterine vessels and above the uterosacral ligament. The different surgical techniques are detailed in Table 2.

LCC in twin pregnancy
However, there are few articles introducing the efficiency of laparoscopic cervical cerclage in twin pregnancy. The largest sample of twin pregnancy undergoing laparoscopic cervical cerclage was studied by Huang et al. in 2019: 24 women delivered by cesarean section, with 16/24 after 34 weeks and 21/24 women producing live births [5].

Emergency LCC
However, the outcomes of emergency laparoscopic cervical cerclage were introduced in one case series of 5 patients by Kavallaris et al. in 2021 [13]. Patients, who underwent cervical cerclage in a mean gestational age of 14.4 weeks due to cervical insufficiency and dilation, delivered by cesarean section at 38.1 weeks with a 100% survival rate.
Moawad et al. thoroughly studied the safety and beneficence of laparoscopic transabdominal cervical cerclage in their systematic review with meta-analysis [25], where they compared 25 studies (1116 patients) on transabdominal cerclage placed by laparotomy to 15 studies (728 patients) on transabdominal cerclage performed by laparoscopy. They reported a higher neonatal survival rate in the laparoscopic group without a difference in peroperative complications between the two approaches. The time of surgery was longer in laparoscopic cases, but the length of stay in the hospital was significantly shorter.

Discussion
Laparoscopic cervical cerclage is a surgical approach suggested to prevent premature labor in high-risk women with a history of failed transvaginal cerclage, trachelectomy, or absent vaginal cervix. Hulshoff et al. [26] compared indirectly the laparotomy to the laparoscopic approach in transabdominal cerclage. They concluded that there is no Table 1. Indications and outcomes of laparoscopic cervical cerclage across different included studies.

Efficacy of LCC in twin pregnancy
Huang et al.

2019
Women with cervical incompetence associated with (i) one or more previous mid-trimester loss; (ii) a previously failed TVC; or (iii) a short cervix not amenable to TVC. All treated with prophylactic LCC in preconception (21)  Transabdominal laparoscopic "needle-free" cerclage is a safe and effective treatment option for a well-selected group of women at high risk of cervical incompetence. [15] Efficiency and safety of the new approach of laparoscopic cerclage  [27] showed that LCC seems to be safe in comparison with the transabdominal approach in the management of cervical insufficiency with a statistically significant lower incidence of fetal loss, blood loss, and rate of hemorrhage. In our case, this systematic review evaluates the different indications and surgical techniques of LCC, and obstetrical outcomes without any direct comparison. The summary of results and comparison with other literature are discussed as follows: Indications of laparoscopic cervical cerclage A select cohort of women, with a history of second-trimester abortions or early preterm labor due to cervical insufficiency, should benefit from periconceptional counseling for laparoscopic cervical cerclage [28]. These women must have previous unsuccessful vaginal cerclage or failure of vaginal insertion of cerclage because of congenitally short cervix, cervical conization, or cervical scarring. The minimal number of second trimester abortions, or the number of previous unsuccessful transvaginal cerclage considered in the inclusion criteria are not identical in several reviewed case series. Although clear recommendations concerning abdominal cerclage are provided, no evidence is proven as to the preferred approach between laparotomy, laparoscopy, and the vaginal route. The MAVRIC study [29] is a multicenter randomized controlled trial where patients were assigned randomly (1  [25].

Time of the surgery: before or after conception
The laparoscopic cervical cerclage can be provided before conception or after conception, most commonly during the first trimester of pregnancy. There is no cohort study dealing with the difference between the preconceptional and postconceptional laparoscopic cervical cerclage. A systematic review undergone by Tulandi et al. [30], evaluated the efficacy of abdominal cerclage via laparoscopy before versus after conception, and did not find any significant difference in the live birth rates when abdominal cerclage was performed before or during pregnancy. Although no difference in obstetrical primary outcomes is shown between the two groups, there is a risk of perioperative pregnancy loss among gravid women reported in some manuscripts. Whittle et al. [22] studied the effect of timing for cerclage on pregnancy outcome in their case series. The mean gestational age for delivery was 32.9 weeks and 34.5 weeks when cerclage was placed in gravid and non-gravid women respectively. Additionally, they reported seven pregnancy failures when cerclage was placed in pregnancy, while two failures were noted when the cerclage was done on non-gravid women. Of concern, they concluded that the timing of cerclage placement did not influence the gestational age at delivery, but cerclage failure did occur more often when the cerclage was placed during that pregnancy. However, multiple anatomical changes that occurred during the first trimester of pregnancy should be considered during the surgery and can modify the surgical technique. The difficulty of uterine manipulation, developing the uterine windows, and the uterine vessels engorgement among gravid women can affect the uterine artery skeletonization and the placement of the knot during the operation. Of note, the conversion to laparotomy did occur more frequently when the patient was pregnant in Whittle et al. case series. On the other hand, the disadvantage of preconception cerclage is that pregnancy may either never occur or result in an early loss unrelated to cervical incompetence.

Surgical technique Uterine manipulation
In the case of gravid women, using a uterine manipulator during laparoscopic cervical cerclage is not possible. In the modified LCC, four trocars were used with atraumatic forceps for uterine manipulation [21]. Sponge on ring forceps placed into the vaginal fornix was used for pregnant women in Whipple et al. experience [22]. In preconceptional laparoscopic cerclage, tenaculum and dilator of 6 or 8 mm or a transcervical uterine manipulator are commonly used during this surgery [4].

Type of the tape
Two types of tapes are described in the reviewed studies: The conventional Mersilene Tape and Prolene suture. Whittle et al. [22] were the first who decided to use Prolene instead of Mersilene, inspired by the choice of Rust et al. [31] in choosing of suture material for a vaginal cerclage. Ades et al. used Prolene n 1 in their laparoscopic cerclage (5-7). Shin et al. [21] used Mersilene tape in their case series of postconceptional laparoscopic cerclage, and had an average gestational age at delivery of 36.2 weeks with a fetal survival rate of 95% without reported complications. On the other hand, we found a case series by Whittle et al. [22] where Prolene n • 1 was used, six cases of laparotomy conversion, and an average gestational age at delivery of 32.9 ± 8.8 weeks. However, Ades et al. [9] used Prolene in 19 gravid women before 11 weeks, and found that all patients delivered with an average gestational age of 37.1 weeks without any reported complications. Of concern, no cohort study dealing with the comparison between the two types of tape was found in the literature. However, Mersilene tape is more likely resistant to uterine contractions during labor, but it causes fibrosis around and within the braided fibers. Thus, Prolene known as mono-filament non-braided suture with minimal tissue reactivity and durability, are easier to insert and remove, but it may be more likely to cut through the uterine tissue.

Method of tape insertion
Traditional laparoscopic cervical cerclage is based on a three-port laparoscopic approach with a fourth suprapubic assistant port. Four ports are preferable in gravid women to facilitate uterine manipulation. An incision is performed at the level of the utero-vesical fold in the visceral peritoneum and extended laterally to the broad ligaments. It is not necessary to carry out the bladder reflection systematically, while it is preferable in the case of previous cesarean sections. Most surgeons dissected the uterovesical and paravesical spaces and made a broad ligament window after identification of the ureters and uterine arteries. Although the suture may be inserted in either direction, there was no evidence that placing the suture from anterior to posterior has advantages more than the opposite direction. Some authors preferred the anterior to posterior direction for better visualization, and reduced risk of bowel injury and bladder erosions. Straight or straightened needles can be used during this procedure because they presented a more accurate direction of the suture. Furthermore, the suture is then passed at the level of the uterine isthmus medial to the uterine vessels. However, the tape is inserted laterally to the uterine vessels and above the ureters at the level of the uterine isthmus, above the uterosacral ligament in the modified laparoscopic cervical cerclage [21]. This technique reduced the operation time and blood loss and improved the recovery time in comparison with a traditional laparoscopic cervical cerclage. This modified method did not completely block blood flow to the uterus, and the development of existing collateral circulation did not affect fetal growth. However, Shaltout et al. [16] described their technique where after insertion of the needle bilaterally with an anterior to posterior direction, both needles were passed through the cervical tissue medial to uterosacral ligaments toward the posterior vaginal fornix, and the tape was tied behind the intravaginal segment of the cervix. On the other hand, Wang et al. [11] also described a different technique where a Transvaginal Mersilene Needle was inserted at the 4 o'clock position of the posterior fornix until its tip appeared down the vesico-uterine peritoneum, then a transvaginal penetration of the Endopath Ultra Veress insufflation needle was punctured at 7 o'clock position to slip the tape into the vagina after surrounding the cervical isthmus, to finish with transvaginal knotting.

Location of the knot & cerclage removal
Three different locations of the knot were described: anterior, posterior, and intravaginal knot. Anterior knots have the advantage of avoiding the risk of adhesions in the Douglas pouch, and can be easily removed in laparoscopy, but may increase the risk of erosion into the bladder. On the other hand, posterior knots can be removed via posterior colpotomy in case of pregnancy failure in the second trimester and this allows vaginal delivery. To avoid the unindicated cesarean section at term for removing the intracorporal cerclage knots, some authors described the intravaginal knot method to simplify knot removal [16]. To sum up, the knot is preferably placed anteriorly in post conceptional cerclage to simplify the difficulty in accessing the posterior cul de sac, while the posterior knot is preferable in preconceptional cerclage. To simplify the cerclage removal, Ades et al. [6] conducted a case series describing the outcomes of subsequent pregnancies when the laparoscopic cervical cerclage was left in situ and concluded a high neonatal survival rate after 34 weeks of gestation even in third pregnancies.

Safety & complications
Multiple complications are described by reviewing the literature. Some complications were related to the laparoscopic surgery and others to the transabdominal cervical cerclage procedure. Although Moawad et al. [25] reported a rate of 1% of peroperative complications in their meta-analysis, some reports described a higher complication rate. Specific complications such as bleeding from uterine vessels and loss of pregnancy when cerclage was performed in gravid women are the most reported. The overall complications rate reported was 1.3% in the Ades et al. case series of 121 interval cerclage [14]. There was one post-operative wound infection, and one intra-operative bladder injury and one uterine fundal perforation, both laparoscopically sutured. On the other hand, the case series of Whittle et al. [22] was the first largest study that reported a serious rate of complications, especially in the non-interval procedure. It included 31 cerclages during pregnancy and 34 preconceptional cerclage, there were two fetal losses (2/31) and seven conversions to laparotomy (7/65) due to bleeding from the uterine vessels (5), or impaired visibility (2). Six of the seven patients who required conversion to laparotomy were pregnant. Ades et al. [9] did not report any serious complications in their case series where cerclage was placed in 19 pregnant women before 11 weeks of gestation. Chung et al. [19] published recently the outcomes of the modified laparoscopic cervical cerclage when placed in gravid women with a mean gestational age of 12.5 weeks with the largest sample size (299). The operative complications rate was 0%. To sum up, we can consider that the operative complications seem uncommon in these procedures and depend directly on the operators' skills and expertise.

Obstetrical outcomes
Moawad et al. [25] reported in their meta-analysis improved obstetric outcomes associated with the laparoscopic approach in comparison with laparotomy and robotic surgery.  [19]. Furthermore, the neonatal survival rate was 93.8%, with mean gestational age at delivery 36.9 in Clark et al. study [20], where 124 preconceptional women and 13 pregnant women, with a history of recurrent pregnancy loss underwent laparoscopic cervical cerclage.

Strengths & limitations
To our knowledge, this is a large and new systematic review exploring the surgical technique of the laparoscopic approach of abdominal cerclage with obstetrical outcomes. On the other hand, the small sample size in some of the included studies, their retrospective design, and the lack of standardized criteria for the technique, and timing of the operation represent the major limitations of this systematic review, thus making it difficult to conclude any convincing evidence on the management strategies. We also included case reports and case series, thus facing a higher risk of publication bias and decreasing the level of the evidence of our findings. Moreover, indications for delivery are not discussed in any study: patients with an indicated preterm labor (for placental disease for example) should be excluded.

Future work
Future randomized cohort studies with a larger sample size are required to evaluate the best technique (medial or lateral to the uterine artery, posterior-to-anterior direction or the opposite), the most efficient type of tape (Mersilene or Prolene), and the best timing for this procedure (preconception or first trimester) to have better obstetrical outcomes. However, these studies need significant statistical power. Furthermore, the beneficial outcomes of laparoscopic cervical cerclage may be a reason for medical laboratories and manufacturers to invest more in the production of resorbable tape based on native tissue. Moreover, further studies are needed to evaluate the efficiency of laparoscopic cervical cerclage in multiple pregnancies.

Conclusion
Although the United Kingdom National Institute for Health and Care Excellence (NICE) classified laparoscopic cerclage as a procedure with limited evidence for success, multiple studies showed that transabdominal cervico-isthmic laparoscopic cerclage is highly effective in selected patients with a history of refractory cervical insufficiency. This technique has a high neonatal survival rate when placed in preconceptional or post conceptional patients. Moreover, laparoscopic cervical cerclage seems to be a safe procedure when the correct skill and laparoscopic expertise are present.

Summary points
• After unsuccessful transvaginal cerclage, the transabdominal isthmo-cervical cerclage can be indicated in a selected high-risk patient. A laparoscopic approach has been described. • The transabdominal cervico-isthmic laparoscopic cerclage is highly effective in selected patients with a history of refractory cervical insufficiency. • This technique has a high neonatal survival rate when placed in preconceptional or post conceptional patients.
• Laparoscopic cervical cerclage is a safe procedure when laparoscopic expertise is present.
Financial & competing interests disclosure