Evelien M. Sandberg1, Jon I. Einarsson1 and Thomas F. McElrath1
Brigham and women’s Hospital, Boston, MA, USA
Jon I. Einarsson
15.2 Methods to Prevent Preterm Loss Associated with Cervical Insufficiency
Preterm delivery is the most common cause of neonatal morbidity and mortality, with reported preterm birth rates in Europe and other developed countries around 5–11 % of all deliveries (Lawn et al. 2010). Cervical insufficiency contributes to both preterm delivery and second-trimester fetal loss. It has been conservatively reported that cervical insufficiency complicates approximately 0.1–1 % of all pregnancies, and estimates suggest that 8 % of women with repeated second or early third-trimester losses may be affected (Ludmir 1988; Scarantino et al. 2000). In a normal pregnancy, the cervix stays both closed, with substantial length (>3 cm) and only toward the end of term the cervix starts to progressively shorten, become effaced in preparation for normal labor and delivery. In some cases, however, the cervix starts to shorten and dilates pathologically early in gestation (Alfirevic et al. 2012). This condition has been described as early as the seventeenth century by Riverius and was formerly termed ‘cervical incompetence’. While this term has largely given way to the less pejorative, ‘cervical insufficiency’ they both refer to a condition where the cervix fails to maintain an intrauterine pregnancy until term (Ludmir 1988). Cervical insufficiency is characterized by painless dilation of the cervix followed by either the premature rupture or prolapse of the fetal membranes but without uterine contractions.
The pathogenesis of the cervical insufficiency has never been well understood. It has been thought to be possibly associated with everything from congenital weakness or previous cervical trauma, such as prior cone biopsy, improperly performed pregnancy terminations, or precipitous vaginal delivery. However, several recent studies have suggested that maternal and fetal inflammations are more likely key factors contributing to premature cervical effacement and dilatation (Harger 2002; Warren et al. 2009; Rust et al. 2001; McElrath et al. 2008). Work has suggested that specific cytokines present in the maternal and fetal milieu are directly correlated to premature labor causes and more specifically to cervical insufficiency (McElrath et al. 2011; Faupel-Badger et al. 2011). Moreover, the contribution of this background of biochemical, inflammatory, and immunological stimuli could explain why the ability of the cervix to remain closed varies from pregnancy to pregnancy. It is likely that cervical insufficiency is not an independent condition but one portion of a spectrum of conditions leading to spontaneous preterm birth (Lawn et al. 2010).
Nonetheless, cervical insufficiency is associated with dramatic consequences which may contribute to further morbidity including intraamniotic infection, preterm premature rupture of the fetal membranes (PPROM) and preterm labor and delivery (PTD), and fetal loss (www.uptodate.org).
To prevent the adverse effects caused by cervical insufficiency, a variety of therapies have been proposed and will be discussed briefly in this chapter. More specifically will be discussed the laparoscopic transabdominal cerclage.
15.2 Methods to Prevent Preterm Loss Associated with Cervical Insufficiency
When cervical insufficiency is suspected, a variety of diagnostic and treatment options can be considered:
· Fetal fibronectin: The fetal fibronectin test is a test performed between 24 and 35 weeks gestation and measures the fibronectin protein that leaks into the vagina. If higher concentrations are noted, the risk of preterm delivery is increased. A negative test is reassuring as the possibility of preterm labor within the next 7–10 days is diminished. However, the test has a high false-positive rate. Despite this disadvantage, there is now substantial evidence that the fibronectin test is a reasonable test to reassure pregnant women (Duhig et al. 2009; Honest et al. 2009).
· Progesterone: Administration of progesterone either intramuscularly or vaginally in the second and third trimester of pregnancy, depending on the indication, has been demonstrated to reduce the risk of primary or recurrent preterm birth (Berghella et al. 2010). Intramuscular progesterone has been specifically demonstrated to reduce the risk of recurrent preterm birth in women with prior history of premature birth (Berghella et al. 2010). Therefore in this group of women, it is appropriate to conduct progesterone prophylaxis between 16 weeks and 36 weeks gestation. More research is needed in terms of efficacy and the long-term consequences of progesterone use (Arisoy and Yayla 2012).
· Pessary: A pessary is a silicone device that is inserted through the vagina and provides support to the cervix. It is a noninvasive, easy to apply, and cost-effective method and has been used over the past 50 years to prevent preterm birth, without gaining much popularity though. In a recent randomized control trial, however, a significant difference was found in the prolongation of pregnancy between women with cervical shortening treated with pessary and those managed expectantly. The authors concluded that the pessary is an affordable and safe alternative in a population of appropriately selected at-risk pregnant women with a cervical length of 25 mm or less (Goya et al. 2012). Pessary presents an interesting new option in the management of cervical insufficiency.
Considered generally, the placement of a cervical cerclage involves the circumferential suturing of the uterine cervix or lower uterine segment. The aim is to give mechanical support and thereby maintain the cervical length and integrity. Cerclage can be placed either transvaginally or transabdominally. In 1957, Lash and Lash (1950), Shirodkar (1955), and McDonald (1957) first reported outcomes on cerclage placed transvaginally. In 1965, Benson and Durfee described the first transabdominal approach for women in whom a vaginal approach was not possible or had previously failed (Benson and Durfee 1965). More than 30 years later, in 1998, the first laparoscopically performed transabdominal cerclage was reported (Burger et al. 2011). It is currently estimated that, in the United States, cerclage is performed at a rate of 1 per every 300 pregnancies (Menacker and Martin 2008). Elsewhere in the world, cerclage placement has been reported to be higher, up to 1 per every 100 pregnancies (Al-Azemi et al. 2003). In multiple pregnancies, placement of cerclage occurs more often, up to 10 % for triplets.
15.3.1 Indication for Cerclage Placement
Historically, the indications for cerclage placement (either transabdominally or transvaginally) have been diverse and include factors such as poor obstetric history, uterine anomalies, cervical trauma, and cervical shortening seen on ultrasound examination. More recently, the Cochrane review (Alfirevic et al. 2012) divided the indications of cerclage into the following categories:
· History indicated cerclage: this type of cerclage is placed because of a perceived increased risk related to a woman’s obstetric or gynecological history. The history indicated cerclage is preferably placed at 12–14 weeks of gestation, after assessment of viability and chromosomal risk. Multiple authors suggest that a history-indicated cerclage might be considered for women meeting the following three criteria (MRC/RCOG 1993; Buckingham et al. 1965; Leppert et al. 1987; Rechberger et al. 1988): (1) Two or more consecutive prior second trimester pregnancy losses or three or more early (<34 weeks) preterm births. (2) Risk factors for cervical insufficiency are present (history of cervical trauma and/or short labors or progressively earlier deliveries in successive pregnancies). (3) Other causes of preterm birth (e.g., infection, placental bleeding, multiple gestation) have been excluded.
· Ultrasound-indicated cerclage: if the cervical length decreases to less than 25 mm on screening prior to 24 weeks, placement of a transvaginal cerclage could be considered (Committee opinion no. 522: 2012; Society for Maternal-Fetal Medicine Publications Committee 2012). The efficacy of this cerclage is limited to women with a prior preterm birth who are not found to have a cervical length <2.5 cm. In a randomized control trial comparing Shirodkar cerclage to expectant management in women with short cervix, no significant differences were found with regard to perinatal or maternal morbidity (To et al. 2004).
· Exam indicated cerclage is a rare procedure in which a cervical suture is placed in women who are incidentally found to have a dilated cervix with or without prolapsed membranes. In order to perform this type of cerclage, the patient must not be in labor and not have heavy vaginal bleeding or infection (Liddiard et al. 2011). The complication rate, mainly due to the membrane ruptures, as well as the loss rate was higher than in other types of cerclage placement (Liddiard et al. 2011).
As elsewhere transvaginal cervical is the initial procedure of choice in our institution. However, for those with who have failed prior prophylactic methods designed to prevent recurrent spontaneous preterm birth, we reserve consideration of a transabdominal cerclage.
15.3.2 Transvaginal Cerclage
The transvaginal approach, which is most commonly used, has two primary placement techniques:
15.3.3 Transabdominal Cerclage
The transabdominal cerclage involves a Mersilene band (or other nonabsorbable suture material) passed around the cervicouterine isthmus at the level of the uterosacral ligament insertions with either an anterior or posterior tying of the ligature (Mingione et al. 2003). This procedure is typically reserved for patients who have failed one or more prior prophylactic techniques to prevent preterm birth (Reid et al. 2008).
Advantages of transabdominal over transvaginal cerclage are the more proximal placement of stitches (at the level of the internal os) and the ability to leave the suture in place for future pregnancies (Carter and Soper 2005). A disadvantage of this approach is the need for two surgeries during pregnancy (one to place the cerclage and a cesarean section for the delivery of the infant). Additionally, there is the possibility that additional surgery may be required in case of miscarriage or fetal demise (Lesser et al. 1998; Davis et al. 2000). In a systematic review, transabdominal cerclage was associated with a lower likelihood of perinatal death or delivery before 24 weeks of gestation (6 versus 12.5 % with repeat transvaginal cerclage), but a higher rate of serious operative complications, such as need for transfusion or organ injury (3 versus 0 %) compared with transvaginal cerclage (Zaveri et al. 2002). Subsequent studies have reported similar findings (Debbs et al. 2007). It has been suggested that the reason for the improved outcomes associated with abdominal cerclage is that the position of the cerclage at the level of the internal os (House and Socrate 2006).
The question whether cerclage should be placed via laparotomy or laparoscopy is still up for debate. In a recent systematic review comparing the effectiveness of abdominal cerclage placed via laparotomy or laparoscopy, the authors concluded that the outcomes of both methods of cerclage were excellent, with mean fetal survival rate (defined as total number of live born infants who survived the neonatal period, which is 6 weeks after delivery, divided by total number of pregnancies) between 80.9 and 90.8 %. The perioperative complication rates for both procedures were low and not significantly different, however in favor of the laparoscopic group (Burger et al. 2011).
Despite the limited available data, the present results seem to indicate that both approaches are safe and associated with good perinatal outcomes in patients with a poor obstetrical history. Therefore, it has been suggested that when possible, the abdominal cerclage should be done via laparoscopy, as this is associated with lower cost and the traditional benefits of minimally invasive surgery, such as fewer adhesions, less postoperative pain, no required hospitalization, and more timely recovery (Burger et al. 2011). However, more research with sufficient power needs to be done to define if one method is superior to the other.
15.3.4 Timing of Placement
Transabdominal cerclage placement can be performed prior to conception or, as stated by the American College of Obstetricians and Gynecologists’ guideline on cervical insufficiency (2003), during early pregnancy (11–14 weeks), after ultrasound evaluation (American College of Obstetricians and Gynecologists 2003). The preconceptional approach is associated with less blood loss and avoids the risk of pregnancy-associated complications (e.g., rupture of the fetal membranes). It is also much easier to place the cerclage in a nonpregnant patient, which shortens operating time.
Placement of an abdominal cerclage late or after the first trimester is not possible since the large size of the uterus makes the procedure difficult if not impossible and is therefore associated with higher risk. At our institution, we prefer placing the cerclage prior to conception due to the greater ease of placement and the reduced risk of complications. A laparoscopic approach is also associated with minimal morbidity and therefore seems justifiable, even in the rare cases where patients are not able to conceive after the cerclage placement.
15.3.5 Contraindication of Cerclage Placement
Not all women are appropriate candidates for consideration of cerclage placement. The major contraindications are fetal anomaly incompatible with life, intrauterine infection, active uterine bleeding, uterine activity, preterm premature rupture of membranes, and fetal demise. Another relative contraindication is the presence of prolapsing fetal membranes through the external cervical os given that the risk of iatrogenic rupture of the membranes is extremely high, up to 50 % (Harger 2002; American College of Obstetricians and Gynecologists 2003). Frequently, the membranes can be reduced with maternal positioning (intraoperative Trendelenburg), back-filling the maternal bladder, decompression amniocentesis.
There is evidence that suggests that performing a cerclage in multiple pregnancies may be detrimental and is associated with an increase in preterm delivery and pregnancy loss. One randomized control trial on this subject has been published so far, comparing the effect of a cerclage versus no treatment for multiple gestations and the authors concluded that no significant additional benefit was to be found in the cerclage group (Dor et al. 1982). However, the number of study patients was limited. In a meta-analysis, outcomes were found to be even worse in the subgroup of women carrying twins, with a doubling of delivery before 35 weeks, compared to the group with expectant management (Jorgensen et al. 2007).
15.3.6 Laparoscopic Cerclage Operation Technique
In this section is presented the laparoscopic technique for cerclage placement as it is done at our institution. However, many variations of this operation have been described over time.
The placement of cerclage via laparoscopic approach is performed under general endotracheal anesthesia. After placing the patient in the modified dorsal lithotomy position, the patient is prepped and draped in the usual fashion for abdominal/vaginal procedure. A Foley catheter is inserted in the bladder and for nonpregnant women, a uterine manipulator is placed in the uterus. Then, as per author’s preference, a 10 mm umbilical trocar is inserted with 5 mm accessory trocars in bilateral lower quadrants and left upper quadrant.
With the Harmonic Ace (Ethicon, Cincinnati, OH) the vesicouterine peritoneum is opened and dissected off the lower uterine segment, in order to view anteriorly on both side the uterine vessels and to expose the avascular window between the uterine artery and the uterus. A 5-mm nonabsorbable Mersilene (Ethicon Inc., Somerville, NJ) polyester suture, with adjacent straightened blunt needles to allow passage through the trocar, is then introduced into the abdominal cavity. The stitch is placed by passing each needle medial to the uterine vessels from posterior to anterior, at the level of the internal cervical os bilaterally. The uterosacral ligaments are used as reference point; a distance of 1.5 cm superior and 1 cm lateral to the insertion of the uterosacral ligament on the posterior uterus is a good initial guide for needle placement. After placing the stitch, the two needles are cut off and removed, and the Mersilene suture is then tied tightly around the cervix with six knots using intracorporeal knot tying. The ends of the stitch are trimmed and a silk suture is used to secure the knot to the lower uterine segment in an effort to minimize protrusion of the knot. Then the visceral peritoneum is closed over the cerclage with a running 2–0 Monocryl (Ethicon Inc., Somerville, NJ) suture that is tied intracorporeally.
The patient is observed in the recovery room for 3–4 h until she can tolerate oral pain medication, void spontaneously, and has adequate pain control. The patient may then be discharged home.
The major intraoperative complication of cerclage placement is bleeding from inadvertent damage to adjacent vessels. We feel the risk of bleeding can be minimized if the cerclage is placed prior to conception, when the pelvic vessels are smaller. Other adverse events described in case reports and case series include fetal death (defined as fetal loss during surgery or 2 weeks later) and intrauterine growth restriction (from inadvertent ligation of the uterine arteries), suture migration, infection, premature labor, premature rupture of membranes, uterine rupture, rectovaginal fistula, and maternal discomfort (www.uptodate.org). In a systematic review (Burger et al. 2011), a comparison of perioperative complications was made between women with laparotomy cerclage and laparoscopic cerclage. The conclusion of the authors was that the perioperative complications were low and not significantly different between the two groups.
For women with a transabdominal cerclage in place, elective cesarean delivery at 37 weeks of gestation is advised at our institution. We prefer not to wait until 39 weeks since this may increase the risk of active labor with the cerclage in place. In our experience, laboring against an abdominal cerclage has been associated with tearing of the lower uterine segment and uterine dehiscence. The Mersilene band can then be removed or left in place if future pregnancies are planned. Successful repeated pregnancies are routine at our institution.
In cases of a miscarriage or a fetal demise, the cervix can be dilated to accommodate the uterine evacuation and pregnancies up to 20 weeks have been successfully evacuated by appropriately trained personnel in this manner. If fetal demise occurs in the late second trimester, the cerclage may need to be taken down either transvaginally or laparoscopically in order to allow the vaginal delivery of the pregnancy and to avoid the need for a hysterotomy.
15.3.9 Outcome and Efficacy
Unfortunately the efficacy of cerclage placement for prevention of premature delivery remains uncertain, and according to the literature, the reported outcomes vary widely. Smaller observational studies have suggested that transvaginal cerclage reduces preterm birth (MacNaughton et al. 1993). More rigorous studies have been less optimistic but there does seem to be a positive effect for women with a history of prior preterm birth and newly diagnosed cervical shortening (Daskalakis 2009). Abdominal cerclage outcomes have not been rigorously tested but success rates have been reported between 85 and 90 % (Novy 1991; Witt et al. 2009) for cerclages placed via laparotomy and between 79 and 100 % for the cerclage placed laparoscopically (Al-Fadhli and Tulandi 2004; Carter et al. 2009; Whittle et al. 2009).
Although these numbers suggest very optimistic results, the use of cerclage and its efficacy still remains uncertain. At our institution, we reserve placement of an abdominal cerclage for situations where a patient has both had multiple prior preterm losses despite the concurrent use of medically indicated conventional prophylactic therapy. Given that the efficacy of abdominal cerclage has not yet been rigorously demonstrated, we hesitate to offer this as a primary prophylactic therapy to patients who have not already failed more standard treatment.
While the available literature on transabdominal cerclage is limited and clinical outcomes of cerclage placement remains uncertain, current experience indicates that laparoscopic cerclage is a safe and effective procedure. Studies indicate that it is comparable with the laparotomy approach or even superior in terms of surgical outcomes, cost, and postoperative morbidity (Fick et al. 2007). Furthermore, laparoscopic cerclage placement has been associated with excellent perinatal outcomes, even in patients with a poor obstetrical history (Fick et al. 2007). Further research with larger patient populations needs to be done to adequately define the appropriate indications for cerclage placement as well as the optimal choice of mode of access, i.e., vaginal vs. laparoscopic vs. abdominal, as well as the potential combination with alternative techniques.
· Maternal and fetal inflammation may be a key factor contributing to the pathogenesis of cervical insufficiency.
· Cerclage can be placed either transvaginally or transabdominally.
· When the standard and conventional therapy fails, it has been our practice to attempt transabdominal placement.
· Laparoscopic cerclage seems to be a safe and effective procedure, comparable with the laparotomy approach or even superior in terms of surgical outcomes, cost, and postoperative morbidity.
· Further research with larger patient populations needs to be done to adequately define the appropriate indications for cerclage placement as well as the optimal choice of mode of access.
Al-Azemi M, Al-Qattan F, Omu A, Taher S, Al-Busiri N, Abdulaziz A (2003) Changing trends in the obstetric indications for cervical cerclage. J Obstet Gynaecol 23:507–511PubMedCrossRef
Al-Fadhli R, Tulandi T (2004) Laparoscopic abdominal cerclage. Obstet Gynecol Clin North Am 31:497–504PubMedCrossRef
Alfirevic Z, Stampalija T, Roberts D, Jorgensen AL (2012) Cervical stitch (cerclage) for preventing preterm birth in singleton pregnancy. Cochrane Database Syst Rev 4:CD008991PubMed
American College of Obstetricians and Gynecologists (2003) ACOG practice bulletin. Cervical insufficiency. Obstet Gynecol 102:1091CrossRef
Arisoy R, Yayla M (2012) Transvaginal sonographic evaluation of the cervix in asymptomatic singleton pregnancy and management options in short cervix. J Pregnancy 4:1–10CrossRef
Benson RC, Durfee RB (1965) Transabdominal cervicouterine cerclage during pregnancy for treatment of cervical incompetency. Obstet Gynecol 25:145–155PubMed
Berghella V, Mackeen AD (2011) Cervical length screening with ultrasound-indicated cerclage compared with history-indicated cerclage for prevention of preterm birth: a meta-analysis. Obstet Gynecol 118(1):148–155PubMedCrossRef
Berghella V, Figueroa D, Szychowski JM, Owen J, Hankins GD, Iams JD, Sheffield JS, Perez-Delboy A, Wing DA, Guzman ER (2010) Vaginal ultrasound trial 17-alpha-hydroxyprogesterone caproate for the prevention of preterm birth in women with prior preterm birth and a short cervical length. Am J Obstet Gynecol 202(4):351PubMedCentralPubMedCrossRef
Buckingham JC, Buethe RA Jr, Danforth DN (1965) Collagen-muscle ratio in clinically normal and clinically incompetent cervices. Am J Obstet Gynecol 91:232PubMed
Burger NB, Brolmann HA, Einarsson JI, Langebrekke A, Huirne JA (2011) Effectiveness of abdominal cerclage placed via laparotomy or laparoscopy: systematic review. J Minim Invasive Gynecol 18:696–704PubMedCrossRef
Carter JF, Soper DE (2005) Laparoscopic abdominal cerclage. JSLS 9(4):491–493PubMedCentralPubMed
Carter JF, Soper DE, Goetzl LM, Van Dorsten JP (2009) Abdominal cerclage for the treatment of recurrent cervical insufficiency: laparoscopy or laparotomy? Am J Obstet Gynecol 201:111.e1–111.e4CrossRef
Committee opinion no. 522: incidentally detected short cervical length. Obstet Gynecol 2012. 119:679
Daskalakis GJ (2009) Prematurity prevention: the role of cerclage. Curr Opin Obstet Gynecol 21(2):148–152, ReviewPubMedCrossRef
Davis G, Berghella V, Talucci M, Wapner RJ (2000) Patients with a prior failed transvaginal cerclage: a comparison of obstetric outcomes with either transabdominal or transvaginal cerclage. Am J Obstet Gynecol 183:836–839PubMedCrossRef
Debbs RH, DeLa Vega GA, Pearson S, Sehdev H, Marchiano D, Ludmir J (2007) Transabdominal cerclage after comprehensive evaluation of women with previous unsuccessful transvaginal cerclage. Am J Obstet Gynecol 197(3):317PubMedCrossRef
Dor J, Shalev J, Mashiach S, Blankstein J, Serr DM (1982) Elective cervical suture of twin pregnancies diagnosed ultrasonically in the first trimester following induced ovulation. Gynecol Obstet Invest 13:55–60PubMedCrossRef
Duhig KE, Chandiramani M, Seed PT, Kenyon AP, Shennan AH (2009) Fetal fibronectin as a predictor of spontaneous preterm labour in asymptomatic women with a cervical cerclage. Br J Obstet Gynaecol 116(6):799–803CrossRef
Faupel-Badger JM, Fichorova RN, Allred EN, Hecht JL, Dammann O, Leviton A, McElrath TF (2011) Cluster analysis of placental inflammatory proteins can distinguish preeclampsia from preterm labor and premature membrane rupture in singleton deliveries less than 28 weeks of gestation. Am J Reprod Immunol 66(6):488–494. doi:10.1111/j.1600-0897.2011.01023.xPubMedCentralPubMedCrossRef
Fick AL, Caughey AB, Parer JT (2007) Transabdominal cerclage: can we predict who fails? J Matern Fetal Neonatal Med 20(1):63–67PubMedCrossRef
Final report of the Medical Research Council/Royal College of Obstetricians and Gynaecologists multicentre randomised trial of cervical cerclage. MRC/RCOG working party on cervical cerclage. Br J Obstet Gynaecol 1993. 100:516–23
Goya M, Pratcorona L, Merced C, Rodó C, Valle L, Romero A, Juan M, Rodríguez A, Muñoz B, Santacruz B, Bello-Muñoz JC, Llurba E, Higueras T, Cabero L, Carreras E, Pesario Cervical para Evitar Prematuridad (PECEP) Trial Group (2012) Cervical pessary in pregnant women with a short cervix (PECEP): an open-label randomised controlled trial. Lancet 379(9828):1800–1806PubMedCrossRef
Harger JH (2002) Cerclage and cervical insufficiency: an evidence-based analysis. Obstet Gynecol 100:1313–1327PubMedCrossRef
Honest H, Forbes CA, Durée KH, Norman G, Duffy SB, Tsourapas A, Roberts TE, Barton PM, Jowett SM, Hyde CJ, Khan KS (2009) Screening to prevent spontaneous preterm birth: systematic reviews of accuracy and effectiveness literature with economic modelling. Health Technol Assess 13(43):1–627PubMedCrossRef
House M, Socrate S (2006) The cervix as a biomechanical structure. Ultrasound Obstet Gynecol 28(6):745–749PubMedCrossRef
Jorgensen AL, Alfirevic Z, Tudur Smith C, Williamson PR, Cerclage IPD Meta-analysis Group (2007) Cervical stitch (cerclage) for preventing pregnancy loss: individual patient data meta-analysis. BJOG 114(12):1460–1476PubMedCrossRef
Lash AF, Lash SR (1950) Habitual abortion: the incompetent internal os of the cervix. Am J Obstet Gynecol 59:68–76PubMed
Lawn JE, Gravett MG, Nunes TM, Rubens CE, Stanton C, GAPPS Review Group (2010) Global report on preterm birth and stillbirth (1 of 7): definitions, description of the burden and opportunities to improve data. BMC Pregnancy Childbirth 10(Suppl 1):S1PubMedCentralPubMedCrossRef
Leppert PC, Yu SY, Keller S et al (1987) Decreased elastic fibers and desmosine content in incompetent cervix. Am J Obstet Gynecol 157:1134PubMedCrossRef
Lesser KB, Childers JM, Surwit EA (1998) Transabdominal cerclage: a laparoscopic approach. Obstet Gynecol 91:855–856PubMedCrossRef
Liddiard A, Bhattacharya S, Crichton L (2011) Elective and emergency cervical cerclage and immediate pregnancy outcomes: a retrospective observational study. JRSM Short Rep 2(11):91, Epub 28 Nov 2011PubMedCentralPubMedCrossRef
Ludmir J (1988) Sonographic detection of cervical incompetence. Clin Obstet Gynecol 31:101–109PubMedCrossRef
MacNaughton MC, Chalmers JG, Dubowitz V et al (1993) Final report of the Medical Research Council/Royal College of Obstetrics and Gynaecology multicentre randomized trial of cervical cerclage. Br J Obstet Gynaecol 100:516–523CrossRef
Mcdonald IA (1957) Suture of the cervix for inevitable miscarriage. J Obstet Gynaecol Br Emp 64:346PubMedCrossRef
McElrath TF, Hecht JL, Dammann O, Boggess K, Onderdonk A, Markenson G, Harper M, Delpapa E, Allred EN, Leviton A (2008) Pregnancy disorders that lead to delivery before the 28th week of gestation: an epidemiologic approach to classification. Am J Epidemiol 168(9):980–989PubMedCentralPubMedCrossRef
McElrath TF, Fichorova RN, Allred EN, Hecht JL, Ismail MA, Yuan H, Leviton A, ELGAN Study Investigators (2011) Blood protein profiles of infants born before 28 weeks differ by pregnancy complication. Am J Obstet Gynecol 204(5):418.e1–418.e12CrossRef
Menacker F, Martin JA (2008) Expanded health data from the new birth certificate, 2005. Natl Vital Stat Rep 56(13):1–24, J Obstet Gynaecol 2003;23:507–511PubMed
Mingione MJ, Scibetta JJ, Sanko SR, Phipps WR (2003) Clinical outcomes following interval laparoscopic transabdominal cervico-isthmic cerclage placement: case series. Hum Reprod 18(8):1716–1719PubMedCrossRef
Norwitz ER, Lee DM, Goldstein DP (1997) Transabdominal cervicoisthmic cerclage: placing the stitch before conception. J Gynecol Tech 3:53
Novy MJ (1991) Transabdominal cervicoisthmic cerclage: a reappraisal 25 years after its introduction. Am J Obstet Gynecol 164:1635–1641PubMedCrossRef
Rechberger T, Uldbjerg N, Oxlund H (1988) Connective tissue changes in the cervix during normal pregnancy and pregnancy complicated by cervical incompetence. Obstet Gynecol 71:563PubMed
Reid GD, Wills HJ, Shukla A, Hammill P (2008) Laparoscopic transabdominal cervico-isthmic cerclage: a minimally invasive approach. Aust N Z J Obstet Gynaecol 48(2):185–188PubMedCrossRef
Rust OA, Atlas RO, Reed J, van Gaalen J, Balducci J (2001) Revisiting the short cervix found by transvaginal ultrasound in the second trimester: why cerclage therapy may not help. Am J Obstet Gynecol 185:1098–1105PubMedCrossRef
Scarantino SE, Reilly JG, Moretti ML, Pillari VT (2000) Laparoscopic removal of a transabdominal cervical cerclage. Am J Obstet Gynecol 182:1086–1088PubMedCrossRef
Shirodkar VN (1955) A new method of operative treatment for habitual abortion in the second trimester of pregnancy. Antiseptic 52:299
Society for Maternal-Fetal Medicine Publications Committee, with the assistance of Vincenzo Berghella, MD (2012) Progesterone and preterm birth prevention: translating clinical trials data into clinical practice. Am J Obstet Gynecol 206:376
To MS, Alfirevic Z, Heath VC, Cicero S, Cacho AM, Williamson PR, Nicolaides KH, Fetal Medicine Foundation Second Trimester Screening Group et al (2004) Cervical cerclage for prevention of preterm delivery in women with short cervix: randomised controlled trial. Lancet 363(9424):1849–1853PubMedCrossRef
Warren JE, Nelson LM, Stoddard GJ, Esplin MS, Varner MW, Silver RM (2009) Polymorphisms in the promoter region of the interleukin-10 (IL-10) gene in women with cervical insufficiency. Am J Obstet Gynecol 201(4):372.e1-5PubMedCrossRef
Whittle WL, Singh SS, Allen L et al (2009) Laparoscopic cervico-isthmic cerclage: surgical technique and obstetric outcomes. Am J Obstet Gynecol 201:364.e1–364.e7CrossRef
Witt MU, Joy SD, Clark J, Herring A, Bowes WA, Thorp JM (2009) Cervicoisthmic cerclage: transabdominal vs transvaginal approach. Am J Obstet Gynecol 201:105.e1–105.e4CrossRef
www.uptodate.org (Topic cerclage, June 2012)
Zaveri V, Aghajafari F, Amankwah K, Hannah M (2002) Abdominal versus vaginal cerclage after a failed transvaginal cerclage: a systematic review. Am J Obstet Gynecol 187(4):868–872PubMedCrossRef