Open Access

Classification of intra-abdominal adhesions after cesarean delivery

Gynecological SurgeryEndoscopic Imaging and Allied Techniques201210:765

https://doi.org/10.1007/s10397-012-0765-1

Received: 5 July 2012

Accepted: 16 August 2012

Published: 2 September 2012

Abstract

The objective of the study was to develop a standard classification for adhesions after cesarean delivery. We searched the Medline, Pubmed, EMBASE, and the Cochrane database of systematic reviews from 1996 through 2011 for all articles pertaining to adhesion scoring after a cesarean delivery. We performed the search using the keywords “cesarean, adhesions, repeat cesarean, intra-abdominal adhesions, adhesion scoring system, and adhesion classification.” Most published adhesion scoring systems were non-site-specific or unclearly described. The most comprehensive adhesion scoring systems were described in three prospective studies that came from two institutions. The scoring systems were similar, site-specific, involving over four sites, and assessing the severity and consistency of adhesions. We combined the two scoring systems to develop a standardized classification of adhesions after cesarean delivery. To date, there are no uniform classifications of intra-abdominal adhesions after cesarean delivery. We hereby outline the first standardized classification of adhesions after cesarean delivery.

Keywords

Adhesion Cesarean Classification Scoring system

Background

Cesarean delivery is one of the most common operations performed on women, and its rate keeps increasing. The rates of cesarean in the USA in 1996 and 2009 were 20.7 and 32.9 % respectively, an increase of over 50 % [1, 2]. In the states of Louisiana and New Jersey, the rates were close to 40 %. The increasing rate of cesarean deliveries can be attributed to many factors including an increased repeat cesarean delivery rate. The repeat cesarean delivery rate among all live births was 6.7 % in 1996 and 14.8 % in 2001, representing an increase of over 120 %. [3]. Martin et al. reported that the repeat cesarean delivery rate increased from 69.8 in 1996 to 88.7 in 2003 per 100 births among low-risk women with a previous cesarean [2].

Adhesions develop frequently following cesarean delivery, with estimates of adhesions following the first cesarean ranging from 24.4 % overall [4] to 73 % when the parietal peritoneum is left open [5]. Several studies have demonstrated that adhesions develop more frequently and with greater density with each repeat cesarean and are associated with increasing maternal morbidity [4, 68].

In studies of post-cesarean adhesions, however, each institution has used a different adhesion-grading system and approach, which may explain the significant variation in reporting. In the field of infertility, the classification of adnexal adhesions of the American Society for Reproductive Medicine has been widely used clinically and for research purposes [9]. Yet, to date, there has been no standardization of adhesions after cesarean delivery. Indeed, there is a paucity of information about adhesions in obstetric settings, and its consequences have been underappreciated [10].

The purpose of our literature review is to develop a standard classification for adhesions after cesarean delivery.

Materials and methods

We searched Medline, EMBASE, Pubmed, and the Cochrane database of systematic reviews from 1996 through 2011for all articles pertaining to adhesion scoring after a cesarean delivery. We performed the search using the keywords “cesarean, adhesions, repeat cesarean, intra-abdominal adhesions, adhesion scoring system, and adhesion classification”. We reviewed reference lists from any identified article including reviews to find other publications.

Study selection

We examined all articles that studied adhesions after cesarean deliveries and the outcome. Those with adhesion scoring systems or classifications of adhesions were evaluated for whether scoring was performed prospectively and whether it was site-specific. We included studies where the adhesions were evaluated prospectively with site-specific adhesion scoring systems (Table 1) [5, 11, 12]. Studies with unclear evaluation of adhesions (Table 2) [1318] and retrospective studies (Tables 3 and 4) [1925] were excluded.
Table 1

Prospective studies with site-specific adhesion scoring system

Authors

Type of study

Main outcome measures

Number of patients analyzed

Number of adhesion sites

Results

Lyell et al. [5]

Prospective cohort

Effect of parietal peritoneal closure

173

Over 4 sites

Parietal peritoneal closure is associated with reduced adhesion formation

Tulandi et al. [11]

Prospective cohort

Prevalence of adhesions with or without keloids

429

Over 4 sites

Women with keloids have increased adhesions between the uterus and the bladder or the abdominal wall

Tulandi et al. [12]

Prospective cohort

Prevalence and extent of adhesions after repeated cesareans

1,026

Over 4 sites

Adhesion are mainly between the uterus and the bladder or the anterior abdominal wall

Table 2

Randomized and prospective studies with unclear evaluation of adhesions

Authors

Type of study

Main outcome measures

Number of patients analyzed

Results

Comments

Roset et al. [13]

Randomized clinical trial

Effect of combined parietal and visceral peritoneum closure

29

No difference in long-term morbidity between closure and non-closure of peritoneum

Outcomes were evaluated by patient report

Weerawetwat et al. [14]

Randomized clinical trial

Effect of parietal and visceral peritoneum closure

65

No difference in adhesion formation between closure and non-closure of peritoneum

Adhesion score (no, mild, moderate and severe) based on the width of the adhesion bands; lack of detailed description of site-specific adhesions

Komoto et al. [15]

Prospective cohort

Effect of combined parietal and visceral peritoneum closure

50

Increased adhesion formation with parietal and visceral peritoneum closure

Frequency of adhesions was evaluated, and severity was based on whether adhesiolysis was performed

Salim et al. [16]

Prospective cohort

Relationship between abdominal scar characteristics and adhesions

107

Depressed previous scar is associated with increased adhesions.

Adhesion severity: light filmy or dense vascular

Malvasi et al. [17]

Prospective cohort

Effect of visceral peritoneum closure

112

Increased adhesions with visceral peritoneum closure

Evaluation of mainly adhesions between the bladder and the uterus. Severity of adhesions was graded using the American Fertility Society classification for adnexal adhesions

Zareian et al. [18]

Randomized clinical trial

Effect of combined parietal and visceral peritoneum closure

31

Parietal and visceral peritoneum closure may decrease adhesion formation

Adhesion score based on the ease of removal of adhesion bands between the uterus and omentum or rectus muscle. Small number of cases

Table 3

Retrospective studies with site-specific adhesion scoring system

Authors

Type of study

Main outcome measures

Number of patients analyzed

Results

Morales et al. [6]

Retrospective cohort

Prevalence of adhesions after cesareans

542

Cesareans result in adhesion formation. Site-specific locations available only if described in operative notes

Tulandi et al. [4]

Retrospective cohort

Prevalence of adhesion after repeat cesareans

1,283

Increased adhesion with each subsequent cesarean. Site-specific locations available only if described in operative notes. Scores assigned based on severity of adhesion

Table 4

Retrospective studies with no or unclear description of site-specific adhesions

Authors

Type of study

Main outcome measures

Number of patients analyzed

Results

Myers and Bennett [19]

Retrospective study

Effect of combined parietal and visceral peritoneum closure

191

Combined parietal and visceral peritoneum closure was associated with decreased adhesion formation

Phipps et al. [20]

Case control study

Identification of risk factor of bladder injury

126

Adhesions from prior cesarean is a risk factor for bladder injury at repeat cesarean

Zhu et al. [21]

Retrospective cohort

Effect of parietal peritoneum closure

612

Non-closure of parietal peritoneum is associated with increased visceral adhesions

Nisenblat et al. [22]

Retrospective cohort

Complications after repeated cesareans

768

Increased complications and dense adhesion with cesarean number. Dense adhesions were defined as multiple adhesions between the uterus and surrounding organs

Hamel [23]

Retrospective cohort

Incidence and severity of adhesions

62

Decreased adhesions with closure of the rectus muscle or the parietal peritoneum.

Fatusic and Hudic [24]

Retrospective study

Prevalence of adhesions

400

Decreased adhesions after MisgavLadach cesarean. Adhesion scores based on Bristow and Montz scoring system

Chapa et al. [25]

Retrospective cohort

Effect of adhesion barriers at cesarean

112

An adhesion barrier and parietal peritoneum closure reduced adhesion formation

Findings

Besides studies listed on Table 1, all adhesion scoring systems were non-site-specific or unclearly described [1318]. There were three randomized studies (Table 2). Roset et al. evaluated a subgroup of patients involved in a previous randomized trial; adhesions were evaluated retrospectively [13]. Weerawetwat et al. used an adhesion scoring system (no adhesions, mild, moderate, and severe adhesions) based on the width of the adhesion bands and described whether the adhesions involved the uterus, bladder, omentum, or abdominal wall [14]. The study lacks detailed description of site-specific adhesions. Another randomized study [18] used a different grading of adhesions based on the ease of removal of adhesion bands between the uterus and omentum or rectus muscle. The study involved a small number of cases.

Of three prospective non-randomized studies, Salim et al. used a site-specific adhesion scoring system, and severity of adhesions was divided into light filmy or dense vascular adhesions [16]. However, detailed description of site-specific adhesions was not provided. Komoto et al. evaluated the frequency of adhesions but not the severity [15]. Malvasi et al. evaluated adhesions in limited locations, primarily between the bladder and the uterus, and severity of adhesions was graded as none, mild, or severe [17].

The most comprehensive adhesion scoring systems were described in three prospective studies (Table 1). Although they came from two institutions, the scoring systems were similar, site-specific involving over four sites, and assessed the severity and consistency of adhesions. The validity of the two scoring systems was evaluated by each institution, with inter-rater reliability of 0.85 and 0.84, respectively. As a result, we combined the two scoring systems (Table 5). In this new classification, we use a point system, and the scores from multiple sites are additive. The area of incision covered by adhesions is divided into <3 cm, 3–6 cm, and >6 cm. This is based on the estimate that in general, the length of incision for cesarean delivery is approximately 10 cm. Three centimeters is about one third of the incision length and 6 cm is approximately two third of the length.
Table 5

Proposed classification of intra-abdominal adhesions after cesarean delivery

Adhesions

Consistency of the adhesions

<3 cm

3–6 cm

>6 cm

Between uterus and bladder

Filmy

1

2

4

Dense

4

8

16

Between uterus and abdominal fascia

Filmy

1

2

4

Dense

4

8

16

Between uterus and omentum

Filmy

1

2

4

Dense

4

8

16

Between omentum and abdominal fascia

Filmy

2

Dense

8

Adhesions to other pelvic structure that interfere with the delivery

Filmy

4

Dense

8

Comment

There have been many studies evaluating adhesion formation after cesarean delivery, mainly comparing the effects of peritoneal closure and non-closure. Due to the increasing number of repeat cesarean deliveries, several authors have started to examine the effects of repeated cesareans on adhesion formation.

To date, there has never been a uniform classification of intra-abdominal adhesions after cesarean delivery. Previous studies have used either no adhesion scoring system or a non-site-specific scoring system [1925]. For example, Chapa et al. graded the adhesions as no adhesions (grade 0), minimal or filmy adhesions (grade 1), moderate/thick adhesions (grade 2), and absence of free space between the uterus and anterior abdominal wall/viscera [25]. The system does not indicate which viscera are involved in most of the adhesions. Others used the Bristow and Montz scoring system [26], a non-site-specific scoring system that has been used to evaluate adhesions after oncologic surgery as well as in an animal model. It consists of no adhesions (0 point), avascular adhesions (1 point), vascular adhesions (3 points), and thick adhesions (5 points). Some studies have not reported overall adhesions; rather, they stratified adhesions into minor or dense adhesions.

The need for a standardized adhesion classification is obvious. It will allow investigators and readers to evaluate and compare results from different studies. Routine use of a standardized adhesion classification might also enable future investigators to conduct more reproducible retrospective studies. More importantly, knowledge of the presence and severity of adhesions will prepare the obstetrician for future repeat cesarean deliveries. We and others found that rates of dense adhesion after one cesarean was greater than 20 % and after two cesareans, greater than 40 % [4, 27].

We propose a classification of intra-abdominal adhesions after cesarean delivery. Our proposed classification is based on our previous prospective studies of adhesions after cesareans, site-specific, and assessed the severity and consistency of adhesions. We also use a point system (Table 5). Because vascularity especially at the time of repeat cesarean delivery is difficult to evaluate, we did not include it in our classification system. The application and results of using this classification system remain to be seen.

The characteristics of the previous incision scar might provide an idea about the severity of intra-abdominal adhesions [11, 28]. In a study, the authors reported that elevated scars are associated with increased dense adhesions [28]. In another study, women with keloids on the cesarean scar have increased adhesions between the uterus and the bladder, and between the uterus and the abdominal wall [11]. A uniform reporting of adhesions at the time of previous cesareans will be very useful.

Indeed, adhesions after a cesarean delivery are common, and their extent and density increase with repeated cesarean deliveries. The presence of adhesions increases time to delivery of the fetus and time of the procedure [4, 11, 29]. Greenberg et al. reported that the mean interval of incision to delivery in women with severe adhesions (19.8 min) was significantly longer than in those with less severe adhesions (15.6 min). In addition, more women with severe adhesions remained undelivered at 30 min after incision [29]. Maternal morbidities can also increase with each subsequent cesarean delivery. This includes increased bowel and bladder injury, uterine and wound dehiscence, hysterectomy, post-partum hemorrhage, and pulmonary emboli [4, 30, 31].

Conclusion

We hereby outlined the first standardized classification of adhesions after cesarean delivery. It is site-specific and evaluates the prevalence and severity of adhesions. We encourage clinicians and investigators to adopt this classification into a standard practice.

Declarations

Acknowledgments

Togas Tulandi received a travel grant as advisor for Genzyme for adhesion related research.

Authors’ Affiliations

(1)
Department of Obstetrics and Gynecology, McGill University
(2)
Department of Obstetrics and Gynecology, Stanford University

References

  1. Hamilton BE, Ventura SJ, Osterman MJK, Kirmeyer S, Mathews TJ, Wilson E (2011) Births: final data for 2009. Nat Vital Stat Rep 60:1–35Google Scholar
  2. Martin JA, Hamilton BE, Ventura SJ et al. Births: Final data for 2003. National vital statistics reports; vol 54 no 2. Hyattsville, MD. National Center for Health Statistics. 2005. http://www.cdc.gov/nchs/births.htm
  3. Barber EL, Lundsberg LS, Belanger K, Pettker CM, Funai EF, Illuzzi JL (2011) Indications contributing to the increasing cesarean delivery rate. Obstet Gynecol 118:29–38PubMedView ArticleGoogle Scholar
  4. Tulandi T, Agdi M, Zarei A, Miner L, Sikirica V (2009) Adhesion formation and morbidity after repeat cesarean delivery. Am J Obstet Gynecol 201:56.e.1–56.e.16View ArticleGoogle Scholar
  5. Lyell DJ, Caughey AB, Hu E, Daniels K (2005) Peritoneal closure at primary cesarean delivery and adhesions. Obstet Gynecol 106:275–280PubMedView ArticleGoogle Scholar
  6. Morales KJ, Gordon MC, Bates GW Jr (2007) Postcesarean delivery adhesions associated with delayed delivery of infant. Am J Obstet Gynecol 196:461.e1–461.e16.8View ArticleGoogle Scholar
  7. Nisenblat V, Barak S, Griness OB, Degani S, Ohel G, Gonen R (2006) Maternal complications associated with multiple cesarean deliveries. Obstet Gynecol 108:21–26PubMedView ArticleGoogle Scholar
  8. Makoha FW, Felimban HM, Fathuddien MA, Roomi F, Ghabra T (2004) Multiple cesarean section morbidity. Int J Gynecol Obstet 87:227–232View ArticleGoogle Scholar
  9. American Fertility Society (1988) The American Fertility Society classifications of adnexal adhesions, distal tubal occlusion, tubal occlusion secondary to tubal ligation, tubal pregnancies, müllerian anomalies and intrauterine adhesions. Fertil Steril 49:944–955Google Scholar
  10. Diamond MP (2011) Postoperative adhesions: an underappreciated complication of cesarean deliveries. Am J Obstet Gynecol 205(6 Suppl):S1PubMedView ArticleGoogle Scholar
  11. Tulandi T, Al-Sannan B, Akbar G, Ziegler C, Miner L (2011) Prospective study of intraabdominal adhesions among women of different races with or without keloids. Am J Obstet Gynecol 204:132.e1–132.e14View ArticleGoogle Scholar
  12. Tulandi T, Al-Sannan B, Akbar G, Miner L, Ziegler C, Sikirica V (2011) Clinical Relevance of intra-abdominal adhesions in cesarean delivery. Gynecol Surg 8(4):399–403View ArticleGoogle Scholar
  13. Roset E, Boulvain M, Irion O (2003) Nonclosure of the peritoneum during caesarean section: long-term follow-up of a randomised controlled trial. Eur J Obstet Gynecol Reprod Biol 108:40–44PubMedView ArticleGoogle Scholar
  14. Weerawetwat W, Buranawanich S, Kanawong M (2004) Closure vs. non-closure of the visceral and parietal peritoneum at cesarean delivery: 16 year study. J Med Assoc Thail 87:1007–1011Google Scholar
  15. Komoto Y, Shimoya K, Shimizu T, Kimura T, Hayashi S, Temma-Asano K, Kanagawa T, Fukuda H, Murata Y (2006) Prospective study of non-closure or closure of the peritoneum at cesarean delivery in 124 women: impact of prior peritoneal closure at primary cesarean on the interval time between first cesarean section and the next pregnancy and significant adhesion at second cesarean. J Obstet Gynaecol Res 32:396–402PubMedView ArticleGoogle Scholar
  16. Salim R, Kadan Y, Nachum Z, Edelstein S, Shalev E (2008) Abdominal scar characteristics as a predictor of intra-abdominal adhesions at repeat cesarean delivery. Fertil Steril 90:2324–2327PubMedView ArticleGoogle Scholar
  17. Malvasi A, Tinelli A, Farine D, Rahimi S, Cavallotti C, Vergara D, Martignago R, Stark M (2009) Effects of visceral peritoneal closure on scar formation at cesarean delivery. Int J Gynaecol Obstet 105:131–135PubMedView ArticleGoogle Scholar
  18. Zareian Z, Zareian P (2006) Non-closure versus closure of peritoneum during cesarean section: a randomized study. Eur J Obstet Gynecol Reprod Biol 128:267–269PubMedView ArticleGoogle Scholar
  19. Myers SA, Bennett TL (2005) Incidence of significant adhesions at repeat cesarean section and the relationship to method of prior peritoneal closure. J Reprod Med 50:659–662PubMedGoogle Scholar
  20. Phipps MG, Watabe B, Clemons JL, Weitzen S, Myers DL (2005) Risk factors for bladder injury during cesarean delivery. Obstet Gynecol 105:156–160PubMedView ArticleGoogle Scholar
  21. Zhu Y, Cai Q, Wu W (2006) Closure vs. nonclosure of the peritoneum at cesarean delivery. Int J Gynaecol Obstet 94:103–107View ArticleGoogle Scholar
  22. Nisenblat V, Barak S, Griness OB, Degani S, Ohel G, Gonen R (2006) Maternal complications associated with multiple cesarean deliveries. Obstet Gynecol 108:21–26PubMedView ArticleGoogle Scholar
  23. Hamel KJ (2007) Incidence of adhesions at repeat cesarean delivery. Am J Obstet Gynecol 196:e31–e32PubMedView ArticleGoogle Scholar
  24. Fatusic Z, Hudic I (2009) Incidence of post-operative adhesions following Misgav-Ladach cesarean section—a comparative study. J Matern Fetal Neonatal Med 22:157–160PubMedView ArticleGoogle Scholar
  25. Chapa HO, Venegas G, Vanduyne CP, Antonetti AG, Sandate JP, Silver L (2011) Peritoneal adhesion prevention at cesarean section: an analysis of the effectiveness of an absorbable adhesion barrier. J Reprod Med 56:103–109PubMedGoogle Scholar
  26. Bristow RE, Montz FJ (2005) Prevention of adhesions formation after radical oophorectomy using a sodium hyaluronate-carboxymethylcellulose (HA-CMC) barrier. Gynecol Oncol 99:301–308PubMedView ArticleGoogle Scholar
  27. Soltan MH (1996) Al Nuaim L, Khashoggi T, Chowdhury N, Kangave D, Adelusi B. Sequelae of repeat cesarean sections. Int J Gynaecol Obstet 52:127–132PubMedView ArticleGoogle Scholar
  28. Dogan NU, Haktankacmaz SA, Dogan S, Ozkan O, Celik H, Eryilmaz OG, Doganay M, Gulerman C (2011) A reliable way to predict intraabdominal adhesions at repeat cesarean delivery: scar characteristics. Acta Obstet Gynecol Scand 90:531–534PubMedView ArticleGoogle Scholar
  29. Greenberg MB, Daniels K, Blumenfeld YJ, Caughey AB, Lyell DJ (2011) Do adhesions at repeat cesarean delay delivery of the newborn? Am J Obstet Gynecol 205:380.e1–380.e15View ArticleGoogle Scholar
  30. Silver RM, Landon MB, Rouse DJ, Leveno KJ, Spong CY, Thom EA, Moawad AH (2006) Caritiset al. Maternal morbidity associated with multiple repeat cesarean deliveries. Obstet Gynecol 107:1226–1232PubMedView ArticleGoogle Scholar
  31. Andolf E, Thorsell M, Kallen K (2010) Cesarean delivery and risk for postoperative adhesions and intestinal obstruction: a nested case–control study of the Swedish Medical Birth Registry. Am J Obstet Gynecol 203:406.e1–406.e16View ArticleGoogle Scholar

Copyright

© Springer-Verlag 2012

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