Abstract
The objective of this article is to provide a comprehensive review of the occurrence and consequences of postoperative adhesions following cesarean delivery (CD), and an overview of the published clinical data on prevention in this setting using adhesion barriers. Adhesions occur frequently after CD and the incidence increases with each subsequent CD. Repeat CDs are complicated by adhesions, which increase operating time, time to delivery and risk of bladder injury. Clinical data on the efficacy of adhesion prevention strategies specific to the setting of CD are limited. Two small, nonrandomized studies found that the use of absorbable anti-adhesion barriers was associated with a significant reduction in adhesion formation and a shorter time to delivery at repeat CD, compared with no barrier use. Implications for practice and research are discussed. There is a significant need for well-controlled, randomized clinical studies investigating adhesion prevention in the labor and delivery setting.
Keywords
Cesarean delivery (CD) is one of the most common obstetric surgeries. The number of CDs performed has increased in the past decade, with a current rate of approximately 33% of all births in the USA [101] and 26% in Africa, Asia and Latin America [1]. Observational studies show an increase in complications as the number of subsequent CDs increases, including elevated risk for placenta accreta, hysterectomy, blood transfusion, intensive care unit admission and a significant increase in operation time and hospital stay [2,3]. Postoperative adhesions are a common complication of major abdominal surgery, including CD. Adhesions form during healing and consist of fibrous scar tissue that often abnormally connects internal organs or structures. There is limited information in the literature on the management of adhesions relating to CD and no practice guidelines specific to the labor and delivery setting. The aim of this review is to summarize the clinical evidence on the occurrence and consequences of adhesions, and the efficacy of anti-adhesion barriers in CD for an interdisciplinary labor and delivery healthcare team, and to consider the potential role of labor and delivery nurses in managing adhesions in this setting.
Adhesion formation
Adhesions form as a result of abnormal wound healing [4–7]. During tissue healing, a fibrin clot is formed by the aggregation of blood cells, platelets and clotting and growth factors. During the normal healing process, fibrinolytic activity prevents the formation of fibrin deposits and abnormal tissue attachments. However, if fibrinolysis is suppressed (e.g., by tissue ischemia and hypoxia), then fibrin deposits may persist and develop into adhesions. The physical trauma of surgery and the resulting tissue ischemia is a key factor in the formation of adhesions. Others include residual blood, postoperative infection, inflammation and foreign bodies (e.g., sutures) [8,9]. Adhesions are often described as filmy or dense. Filmy adhesions tend to be weak and stringy, with few blood vessels, and are generally easy to cut or remove. Dense adhesions tightly connect tissues, which makes this type of adhesion difficult to remove. They may contain blood vessels and are more likely to recur after removal. However, adhesions can be categorized or scored in a number of ways (
Adhesion classification.
Copyright © Springer-Verlag (2012); reproduced with permission from Springer Science+Business Media.
Copyright © American Medical Association (1974). All rights reserved.
Copyright © The American Fertility Society (1988).
Copyright © The CV Mosby Co. (1978).
CD: Cesarean delivery.
Following a CD, the size of the uterus prevents direct contact between the incision site and the intestines in the first few days. Therefore, most adhesions related to CDs are found in the lower abdomen between the uterus, bladder and omentum [14]. The pathology behind the formation of adhesions following CD may differ from other surgeries owing to the substerile operative area, increased blood loss, the type of incision and the altered physiological and anatomical state of pregnancy [7,14]. Amniotic fluid has fibrinolytic activity and may play a role in the prevention of adhesions [15].
Consequences of adhesions
Abdominal adhesions are associated with significant morbidity and can result in bowel obstruction, chronic pelvic pain, secondary infertility (by distorting anatomy and/or causing tubal blockage) and a need for repeat surgery [6]. The only treatment is surgical lysis (adhesiolysis), but this often results in the formation of further adhesions. The presence of adhesions complicates subsequent surgery due to the additional tissue separation required, which increases operation time, the risk of bleeding and injury to organs, such as the bladder. A review of the literature indicates that adhesions develop following an estimated 93–100% of upper abdominal laparotomies and 67–93% of lower abdominal laparotomies [16]; consequently the prevention of adhesions is a major unmet medical need.
Adhesions also increase healthcare utilization and costs. A retrospective analysis of data from the 2005 Healthcare Cost and Utilization Project's Nationwide Inpatient Sample found that adhesiolysis-related procedures were associated with 967,332 days of inpatient care and costs of US$2.25 billion [17]. Of the secondary adhesiolysis procedures recorded in 2005, CD-related adhesiolysis accounted for healthcare costs of US$18 million [17].
Adhesion prevention
Modification of surgical technique is beneficial, but not sufficient alone to prevent adhesion formation [6]. A variety of adhesion-prevention treatments have been investigated and are summarized in
Methods of adhesion prevention.
CD: Cesarean delivery.
Review of the literature: adhesions & CD
For this narrative review, English language publications reporting human studies that were published between July 2001 and May 2013 were retrieved from the MEDLINE/PubMed online database using relevant multiple search terms including adhesion(s), C-section, cesarean, barrier(s), adhesion-related disorder, Interceed, oxidized regenerated cellulose, Seprafilm, sodium hyaluronate carboxymethylcellulose, Adept® (Baxter Healthcare, IL, USA) and icodextrin. Abstracts were reviewed to identify articles relating to adhesions in the setting of CD; 71 were selected for full review. Of these, 45 met the only inclusion criterion of original research reporting the frequency, consequences or prevention of adhesions in CD, and all are included in this synthesis. Case studies, reviews and letters were excluded. As data on adhesion barriers in CD are extremely limited, the section on safety was supplemented with information regarding safety in other gynecological surgeries (obtained outside of the literature search described above).
Frequency of adhesions after CD
In published prospective and retrospective studies investigating adhesions after primary CD, the occurrence rate varied widely, with 24–73% of women affected [7,8,10,12,18,19]. This variation in incidence may, in part, be due to differing surgical techniques and the adhesion-scoring methods used. A number of different surgical techniques are used in CD that may affect the rate of adhesion occurrence, in particular closure or nonclosure of the peritoneum following delivery. The rate may also differ depending on the type of uterine incision used [20] and the technique used for hysterotomy closure [21]. This remains controversial as conflicting results have been seen in different studies. The majority of studies appear to support a lower adhesion rate following closure of the peritoneum, although the surgical techniques were not standardized and other contributing factors may be involved [7,10,22–28]. By contrast, other studies have supported a lower adhesion rate with nonclosure [29–33] or have observed no difference in overall adhesion occurrence with closure versus non-closure [9,34,35]. A secondary analysis of data from one study found reduced adhesion occurrence following closure of the rectus muscles, whereas closure of the visceral peritoneum appeared to increase adhesions [36]. Long-term follow-up from the CAESAR study – a factorial, randomized controlled trial assessing different surgical techniques for CD – may assist in clarifying the effects of closure/nonclosure [37], although it is not known when these data might be available.
Regardless of the surgical method used, it is clear that adhesions frequently occur after CD and that the incidence increases with each subsequent CD, as shown by many clinical studies [7,8,11,12,18,19,38–47].
Consequences of adhesions in CD
Clinical data describing the effects of adhesions specifically for repeat CDs are summarized in
Summary of clinical studies reporting the effects of adhesions at repeat cesarean delivery.
Copyright © Mosby, Inc. (2009), reproduced with permission from Elsevier.
CD: Cesarean delivery; OR: Odds ratio; SEM: Standard error of the mean.
Other complications may also occur as a result of post-CD adhesions. A retrospective case review of CDs that were followed by exploratory relaparotomy found a bowel obstruction, caused by adhesions, in one out of 28 (3.6%) cases assessed [52]. Adhesions between the anterior lower uterine segment and the anterior abdominal wall may also result in technical limitations for pelvic ultrasound imaging [53]. Surprisingly, in a prospective study of 50 women undergoing a second CD, there was no correlation between the presence of adhesions and abdominal pain, chronic constipation, dyspareunia or dysmenorrhea, and no correlation between the severity and quantity of adhesions and symptom severity, leading the authors to suggest that adhesions after CD may differ from those after other types of abdominal surgery [14]. However, the authors acknowledge that this was a small pilot study and that further research is needed. Other studies have indicated that the number of complications increases with an increasing number of repeat CDs, which may be associated with the higher incidence of adhesions in these patients [19,31,41,45,46]. By contrast, a case–control study of 602 women found no significant increase in surgery time in patients with two or more previous CDs compared with those having only one, even though the occurrence of adhesions was significantly higher in the group with two or more [43].
Adhesion prevention in CD: adhesion barriers
Published clinical data on the efficacy of adhesion barriers specifically in CD are very limited, with only two studies identified for this review. A retrospective cohort analysis study of 112 women evaluated the efficacy of ORC in reducing the incidence of adhesion formation and severity at primary CD compared with a control group (no barrier used) [28]. Placement of the adhesion barrier was one strip over the closed hysterotomy and another perpendicular to the first, over the anterior uterine serosa, to form an inverted T shape. At repeat CD, the proportion of women with no adhesions was significantly higher in the barrier group versus the no-barrier group and there were no grade 3 adhesions in the barrier group (

A cohort study evaluated the efficacy of HA/CMC in preventing adhesions at repeat CD [54]. The proportion of patients with adhesions was significantly lower in the barrier group versus the control group (

Although these two studies provided positive data on the reduction in adhesion occurrence with the use of adhesion barriers in CDs, they are both small, nonrandomized studies; hence the level of evidence is low. Large, high-quality, randomized studies are therefore needed to confirm these limited data on adhesion prevention in CD. Two ongoing clinical trials are assessing the effectiveness of HA/CMC versus no barrier in reducing adhesion formation in CDs; one is a multicenter, randomized, controlled, single-blind study and the other a randomized, double-blind trial.
Data from studies of other types of gynecological surgery have provided evidence for the efficacy of adhesion barriers; however, this cannot be extrapolated to the setting of CD, particularly as the formation of adhesions may differ following CDs compared with other surgeries, based on the surgical environment. No studies assessing other adhesion-prevention strategies in CD were identified in the literature search.
Safety of absorbable adhesion barriers
No adverse effects associated with the use of absorbable adhesion barriers were reported in the two clinical trials evaluating their efficacy in CD surgery. In addition, there were no adverse effects reported in studies of barriers in gynecological surgery [55,56]. If there is a risk of ongoing bleeding from the surgical site, ORC should not be used as it may increase the risk of adhesions in this situation [57]. Concerns were previously raised as to whether HA/CMC could promote tumor growth because it contains hyaluronan, which is known to promote cell migration, differentiation and proliferation. However, in a retrospective case review of 202 women, HA/CMC did not increase the rate of early postoperative complications following surgery for gynecological cancer, and did not adversely affect disease-free survival or overall survival in these patients [58]. One retrospective study of HA/CMC in patients undergoing laparotomy for ovarian, fallopian tube or primary peritoneal cancers suggested an increase in postoperative intra-abdominal fluid collections in the HA/CMC group versus the control group. However, this patient population represents a group undergoing extensive surgery for malignancy, with the majority undergoing debulking procedures and most of the fluid collections occurring in those having large bowel resections. The authors noted that the data therefore should not be extrapolated to other patient populations [59].
Implications for practice & research
Prevention of adhesions following CD may reduce the risk of complications during future pelvic/abdominal surgeries, including repeat CD, and could reduce the risk of secondary infertility, bowel obstruction, and, potentially, chronic pelvic pain. In the context of repeat CD, it may assist in keeping delivery times to a minimum, which is especially important if fetal distress is present, and minimize anesthesia time for both mother and baby. It could be speculated that a reduced need for manipulation without the complication of adhesions may decrease the need for blood transfusion and potentially lower the risk of infection, allowing many women to leave hospital sooner after a CD. Adhesion prevention is important in CDs because this procedure cannot be replaced with minimally invasive laparoscopic methods; open surgery remains essential [14]. The rate of CDs has been increasing throughout the past decade, so the number of women likely to be affected by adhesions has increased and may continue to do so if the trend for an increase in CD rate is maintained. The rate of repeat CD is also increasing, accompanied by a decline in the rate of vaginal birth after cesarean. Although there are no published data on the consequences of adhesions in women having a vaginal birth after cesarean, the presence of adhesions may increase delivery time regardless of delivery method, which increases the potential for complications for mother and baby.
A secondary benefit of adhesion reduction is reduced healthcare utilization, together with its related costs. A cost–effectiveness analysis indicated that an adhesion-prevention strategy utilizing an adhesion barrier (HA/CMC) was more cost effective than routine care without an adhesion-prevention measure in patients undergoing radical hysterectomy and pelvic lymph-adenectomy for stage IB cervical cancer [60]. However, as discussed previously, the pathology behind the formation of adhesions following CD may differ from other surgeries; therefore, cost–benefit analyses in the CD setting are needed to confirm the potential healthcare utilization and cost benefits. A medical database analysis found that healthcare costs, length of hospital stay, operating time and overall complication rates were significantly greater in women undergoing adhesiolysis at the time of repeat CD than in those not undergoing adhesiolysis in a matched control group [61].
The role of the labor and delivery nurse in the prevention and management of adhesions currently centers on raising awareness within the interdisciplinary healthcare team regarding the high rate of adhesion occurrence after CD and the potential consequences. Repeat surgery for adhesiolysis is likely to be carried out by a general surgeon and therefore the gynecology/obstetric healthcare team may not be fully aware of the extent of complications due to adhesions in patients who have previously been in their care. There is a significant need for research and well-controlled, randomized clinical studies investigating methods of adhesion prevention in the labor and delivery setting. Substantial gaps exist in the currently published data regarding the efficacy of barriers in reducing adhesions after CD, and the effects on clinical outcomes such as length of hospital stay, reduction in complication rate, and healthcare utilization and costs. As clinical trial data on the efficacy of adhesion barriers in CD are presently very limited, the expected benefits are mostly extrapolated from clinical studies of other gynecologic/pelvic surgery. Once stronger evidence is reported on their efficacy in the CD setting, the role of labor and delivery nurses could also extend to ensuring the availability of adhesion barriers on the unit as, if barriers are available to use, surgeons are more likely to consider using them as part of the CD procedure. All labor and delivery units would benefit from having an adhesion risk reduction/aversion strategy to prevent adhesions at primary CD rather than waiting until adhesions are already present to tackle the problem.
Conclusion & future perspective
Adhesions are common after CD and their incidence increases with each subsequent procedure. Abdominal adhesions are associated with significant morbidity including bowel obstruction, secondary infertility, chronic pelvic pain and a need for repeat surgery. However, data on the occurrence of these complications following CD are limited. Clinical studies show that adhesions complicate subsequent CD surgery, with an increased operating time and time to delivery, which may increase the risk of adverse outcomes. Adhesions are also associated with an increased risk of bladder injury. Therefore, prevention of adhesion formation following CD is an unmet medical need. Data on adhesion prevention specific to CDs are scarce, but two small, nonrandomized studies support a reduction in adhesion formation and time to delivery at repeat CD with absorbable adhesion barriers [28,54]. The use of anti-adhesion agents should be an adjunct to good surgical technique rather than a replacement. Labor and delivery nurses could aid the prevention and management of adhesions by raising awareness within the healthcare team regarding the high rate of adhesion occurrence after CDs, and the potential consequences. Data from ongoing randomized clinical trials of adhesion barriers will likely play a key role in determining whether their use in CD becomes widely accepted. Adhesion prevention in the labor and delivery setting should be a key area for future research.
Financial & competing interests disclosure
This review includes discussion of the sodium hyaluronate/carboxymethylcellulose (Seprafilm®) adhesion barrier, manufactured by Genzyme Biosurgery. The author has no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.
Medical writing assistance was provided by H Varley (Envision Custom Solutions, Horsham, UK) and was supported by Sanofi Biosurgery (formerly Genzyme Biosurgery).
Executive summary
Cesarean delivery (CD) is one of the most common obstetric surgeries.
Postoperative adhesions are a common complication of abdominal surgery and can cause bowel obstruction, chronic pelvic pain, secondary infertility and complications during subsequent surgery.
The only treatment is surgical lysis, but this often perpetuates adhesion formation.
Good surgical technique is beneficial but not sufficient to prevent adhesions. Several adhesion-prevention strategies have been investigated; the most widely used in the labor and delivery setting are absorbable anti-adhesion barriers.
Adhesions frequently form after CD and their incidence increases with each subsequent CD.
Adhesions may complicate subsequent CDs by delaying entry into the uterine cavity, increasing time to delivery and total operation time.
Adhesions are also associated with a greater risk of bladder injury.
Clinical data on the efficacy of adhesion barriers in CD are very limited.
Two cohort studies have shown that absorbable adhesion barriers significantly reduced adhesion formation following CD compared with a control group (no barrier used).
Time to delivery was also significantly reduced with barrier use versus no barrier.
No adverse effects were reported in studies of adhesion barriers in CD and other gynecological surgeries.
Prevention of adhesions following CD may reduce the risk of secondary infertility, bowel obstruction and complications during future surgeries, and could help minimize delivery time for repeat CDs.
Potential reductions in healthcare utilization and costs are a secondary benefit of adhesion reduction.
Labor and delivery nurses could aid adhesion prevention and management by raising awareness of adhesions and their consequences within the healthcare team.
Combined with good surgical technique, adhesion barriers may reduce adhesion formation following CD, thus preventing adhesion-related complications at repeat CD.
Adhesion prevention in the labor and delivery setting should be a key area for future research.
