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Postcesarean delivery adhesions associated with delayed delivery of infant
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OBSTETRICS
Postcesarean delivery adhesions associated with delayed delivery of infant Kelly J. Morales, MD; Michael C. Gordon, MD; G. Wright Bates, Jr, MD OBJECTIVE: The purpose of this study was to estimate the incidence of adhesions after cesarean deliveries and to determine their impact on delivery and infant well-being. STUDY DESIGN: This was a retrospective cohort analysis with chart review. The charts of 542 women who had undergone primary (265 women) or repeat cesarean (277 women) deliveries were reviewed. The incidence, severity, and locations of adhesions; delivery time; cord blood pH, and Apgar scores were noted.
fourth cesarean delivery had formed pelvic adhesive disease. Compared with primary cesarean section, delivery of the infant was delayed 5.6 minutes (52%) with 1 previous cesarean birth, 8.5 minutes (79%) after 2 cesarean birth, and 18.1 (169%) during the fourth cesarean birth (P ⬍ 0.001 for all comparisons).
RESULTS: After the first cesarean delivery, 100 of 217 women (46%)
CONCLUSION: A high percentage of cesarean deliveries result in adhesive disease, which delays repeat cesarean delivery of the fetus. The potential for adhesive disease should be included in counseling regarding primary elective cesarean births.
had pelvic adhesive disease; 48 of 64 women (75%) who underwent a third cesarean delivery and 5 of 6 women (83%) who underwent a
Key words: adhesion, cesarean delivery, complication, pregnancy
Cite this article as: Morales KJ, Gordon MC, Bates GW Jr. Postcesarean delivery adhesions associated with delayed delivery of infant. Am J Obstet Gynecol 2007;196:461.e1-461.e6.
C
esarean deliveries in the United States reached a record high in 2004 and represented 29% of all births. The higher incidence, in part, was due to an 8% increase in primary procedures and a 13% decrease in the rate of vaginal birth after a cesarean delivery.1,2 The decline
From the San Antonio Uniformed Services Health Education Consortium, Wilford Hall Medical Center, Lackland AFB, San Antonio, TX, and Brooke Army Medical Center, Fort Sam Houston, TX. Presented in part at the Armed Forces District Annual Meeting of the American College of Obstetricians and Gynecologists, Seattle, WA, Oct. 31-Nov. 4, 2005. The opinions expressed in this article are those of the authors and are not meant to be construed as official or as reflecting the opinions of the United States Air Force, the United States Army, or the Department of Defense. Received May 2006; accepted Dec. 12, 2006. Reprints: G. Wright Bates, Jr, MD, Atlanta Center for Reproductive Medicine, 100 Stone Forest Dr, Suite 300, Woodstock, GA 30189; [email protected] 0002-9378/$32.00 © 2007 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2006.12.017
of operative vaginal deliveries and vaginal deliveries of breech or multiple gestations also contributed to the increased cesarean section rate. In addition, primary elective cesarean births may be on the rise, with considerable national debate focused on the role of cesarean deliveries in the prevention of pelvic relaxation and the potential negative impact of vaginal deliveries on long-term maternal health.3-5 Cesarean deliveries also may impact maternal health negatively, with resultant difficulty in conceiving or delivering a healthy infant.6,7 A recent study has demonstrated an increased risk of unexplained stillbirth in subsequent pregnancies after cesarean delivery.8 In addition, delivery by cesarean may have an immediate impact on fetal well-being. The risk of neonatal respiratory distress that necessitates resuscitation with oxygen therapy is increased when the mode of delivery is cesarean.9 Multiple causes likely play a role in the negative effects of cesarean delivery. Postoperative adhesions are a well-known complication of other major abdominal surgeries and may be negative sequelae of cesarean deliveries. Reports indicate that adhesions form in most women who un-
dergo abdominal surgeries, surpassing 90% in some series.10 Cesarean deliveries represent a subset of laparotomies. Conventional wisdom is that repeat cesarean deliveries are often more difficult because of adhesions that involve the lower uterine segment and that delay entry into the uterine cavity and delivery of the infant. However, a Medline search of the English language literature (cesarean, adhesions, pregnancy, pH, Apgar) failed to identify studies that specifically examined the scope of pelvic adhesive disease after each successive cesarean delivery and the impact on delivery or well-being of the infant. Because the debate over elective primary cesarean delivery continues, it is important to study all facets that may contribute to both maternal and fetal morbidity. Likewise, optimal intrapartum management and counseling should reflect the potential delay of infant delivery and its impact on fetal health. Therefore, the goal of this study was to describe the incidence of adhesions that were encountered at repeat cesarean deliveries. Furthermore, we wanted to quantify the impact of the adhesions on the delivery of the infant and fetal well-being.
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TABLE 1
Indications for cesarean delivery Indication Nonreassuring fetal heart rate tracing
Primary cesarean delivery (n) 68*
Repeat cesarean delivery (n) 22*
..............................................................................................................................................................................................................................................
Abruption
8*
3*
Uterine rupture
0
2*
Severe preeclampsia remote from delivery
2
4
Cord prolapse
0
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
1*
..............................................................................................................................................................................................................................................
Placenta previa
3
1
Arrest disorder
99
31
4
1
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
Failed operative vaginal delivery
..............................................................................................................................................................................................................................................
Malpresentation
56
16
Maternal medical condition†
4
1
History of shoulder dystocia
2
Maternal herpes simplex virus on examination
9
Suspected macrosomia
3
1
Previous classic cesarean delivery or history of rupture
0
16
Elective repeat cesarean
N/A
172
Repeat cesarean delivery with advanced preterm labor
N/A
2
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
0
..............................................................................................................................................................................................................................................
1
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Not otherwise specified
7
3
..............................................................................................................................................................................................................................................
N/A, not available. * Classified as emergent indications. †
Maternal cardiac or other medical condition, with labor contraindication.
M ATERIALS AND M ETHODS We performed a retrospective cohort analysis of women who had had a cesarean delivery at Wilford Hall Medical Center. After Institutional Board Review approval was obtained, the Wilford Hall labor and delivery database was queried to obtain the list of the first 285 consecutive women who had undergone a repeat cesarean delivery from the years 2000-2003 and the first 285 consecutive women with a primary cesarean delivery in that same time frame. Their medical records were reviewed to identify potential subjects who met the inclusion requirements and to compile the study data. Candidates were excluded (n ⫽ 26 461.e2
women ) if it was noted that they had a history of a pelvic infection (pelvic inflammatory disease noted in the prenatal records or admission history and physical) or abdominal surgery other than cesarean deliveries. Participants were included only once in the study, with the chart from their first cesarean delivery in that timeframe reviewed, and any subsequent deliveries were excluded (n ⫽ 2 deliveries) from analysis. Infants with a high risk of fetal compromise that included infants with major anomalies and infants who were ⬍30 weeks of gestational age or 1000 g were excluded from analysis of fetal well-being. Emergent cesarean deliveries were analyzed indepen-
American Journal of Obstetrics & Gynecology MAY 2007
dently from nonurgent births for infant well-being because of the high likelihood of compromised fetal acid/base status that was unrelated to intraoperative factors. Sample size calculation indicated that at least 250 study subjects were needed in each group to detect a 25% difference in the incidence of adhesions and time required to deliver the infant. Demographic information included maternal age, gestational age, and infant gender and weight. Number of cesarean deliveries, indications for surgery, and complications were included in the surgical parameters. The time from the skin incision to delivery of the infant was calculated from Operating Department records. Adhesions were scored as severe, if the operative summary contained the words severe, extensive, or dense. Adhesions were categorized as mild, if operative notes used words such as present, mild, few, or some. The Apgar scores, cord blood gases, and infant resuscitation served as surrogate markers of infant well-being. Data were analyzed with SPSS statistical software (SPSS Inc, Chicago, IL). The normally distributed data (demographic variables and time to delivery) was presented as mean with SD after visual assessment of a frequency plot, with the determination of significance accomplished by the Fisher exact probability test. Nonparametric data (Apgar score, pH) were analyzed with the Mann Whitney test. The determination of significance for the incidence of adhesions and low pH was performed with a Pearson chi-square test and were expressed as odds ratios (OR) with 95% CI. Correlation was assessed with simple linear regression for the determination of Pearson’s product-moment correlation coefficient (r) and coefficient of determination (r2). A probability value of ⬍.05 was considered significant. We also reviewed the records to identify operative complications.
R ESULTS The study had 542 women who met the inclusion requirements, with 265 subjects having a primary cesarean delivery and 277 subjects having a second, third, or fourth cesarean delivery. Of those
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TABLE 2
Demographics of the primary and repeat cesarean delivery groups Cesarean delivery Demographic
Primary delivery (n ⴝ 265)
Second delivery (n ⴝ 207)
Third delivery (n ⴝ 64)
Fourth delivery (n ⴝ 6)
Maternal age (y)*
27.8 ⫾ 5.9
29.7 ⫾ 5.3
30.9 ⫾ 4.9
33.0 ⫾ 3.3
................................................................................................................................................................................................................................................................................................................................................................................
Gestational age (wk)*
38.3 ⫾ 3.6
38.9 ⫾ 2.0
38.3 ⫾ 2.2
37.9 ⫾ 1.8
Fetal weight (g)*
3237 ⫾ 82
3541 ⫾ 525
3445 ⫾ 658
3291 ⫾ 431
Gender
128/108
106/109
30/34
3/3
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ † ................................................................................................................................................................................................................................................................................................................................................................................
* Values are means ⫾ SD. †
Data are expressed as male/female.
women with primary cesarean deliveries, 76 women had emergent cesarean deliveries for indications that included nonreassuring fetal heart rate status, cord prolapse, and abruptio placentae remote from delivery; the remaining procedures had nonurgent indications. There were 28 emergent repeat cesarean deliveries; 249 of 277 women underwent elective repeat cesarean delivery or had other nonurgent indications (Table 1). All 277 women in the repeat cesarean group who were included in the analysis had undergone a low-transverse cesarean delivery. There were 3 patients in the primary cesarean delivery group who underwent a classic cesarean delivery. These patients were not excluded from analysis. Four patients in the primary cesarean group had general anesthesia, although all of the patients who had repeat cesarean deliveries had regional (spinal or epidural) anesthesia. The gestational age, infant
weight, and gender for the primary and repeat cesarean groups were not statistically different. The maternal age was compared in each group with the mean age of study subjects per cesarean delivery, which rose in an expected linear fashion with each successive cesarean delivery (r ⫽ 0.22, r2 ⫽ 0.05; P ⬍ .001; Table 2). Interns served as the primary surgeon for 46% of the primary and for only 6% of the repeat cesarean deliveries. Eleven women (4%) who underwent primary cesarean section had adhesions that were documented, although 153 (53%) of the women who underwent repeat cesarean delivery had adhesions (OR, 27; 95% CI, 13.2-47.9; P ⬍ .001). Forty-six percent of second cesarean deliveries (OR, 19.5; 95% CI, 10.6-39.7), 75% of the third cesarean deliveries (OR, 44.3; 95% CI, 31.5-164.6), and 83% of the fourth cesarean deliveries had documentation of adhesive disease (Table 3).
Fifty-four percent of the adhesions were classified as severe. Seven percent of all adhesions involved only the uterus and bladder. Adhesions that involved the anterior abdominal wall were noted in 77% of the individuals with repeat cesarean deliveries. Other sites that were documented included the uterus, bladder, adnexa, omentum, and small bowel. However, more than one half of the cases did not have information regarding the location of the adhesions documented. In addition, none of the charts documented the presence or absence of tissue distortion or scar formation that involved the subcuticular space, rectus muscles, or fascia. A statistically significant increase in the time from skin incision to delivery was found when repeat procedures were compared with primary procedures (Figure). Delivery of the infant was delayed 5.6 minutes (52%) with 1 previous
TABLE 3
Incidence and severity of adhesions documented Cesarean delivery Variable
First delivery
All repeat deliveries (n ⴝ 265)
Second delivery (n ⴝ 207)
Third delivery (n ⴝ 64)
Patients with adhesions (n)
11
153
100
48
Fourth delivery (n ⴝ 6) 5
................................................................................................................................................................................................................................................................................................................................................................................ † †
Patients with adhesions in each group (%)
4
Severe adhesions (n)
2
53*
46*
75*
83*
................................................................................................................................................................................................................................................................................................................................................................................
84*
55*
26*
3*
................................................................................................................................................................................................................................................................................................................................................................................
Mild adhesions (n)
9
16
11
5
0
No severity documented (n)
1
47
29
16
2
................................................................................................................................................................................................................................................................................................................................................................................
................................................................................................................................................................................................................................................................................................................................................................................
* P ⬍ .05, compared with primary cesarean deliveries. †
P ⬍ .05, for third and fourth cesarean deliveries, compared with second cesarean delivery (first repeat).
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FIGURE
Time from skin incision to delivery of infant during 1st, 2nd, 3rd, and 4th cesarean delivery 70 60 50 40
Time required to deliver infant (minutes)
30 20 10 0 1st
2nd
3rd
4th
Number of cesarean deliveries
The boxplot represents the standard deviation. The thickline is the mean. The whiskers denote the maximum and minimum values.
cesarean delivery, 8.5 minutes (79%) after 2 cesarean deliveries, and 18.1 minutes (169%) during the fourth cesarean birth, compared with primary cases (P ⬍ .001 for all comparisons). The time from skin incision to removal of the infant was still slower by 4.2 minutes (59%) and 8.8 minutes (124%) for emergent indications after 1 or 2 previous cesarean births. Nonurgent cases demonstrated a 4.8- (39%) and 7.3- (60%) minute delay during the second and third cesarean de-
liveries (P ⬍ .05 for all 4 comparisons). The length of time that was required to deliver the infant also correlated with the presence or absence and severity of adhesion. Repeat cases in women who had any adhesions demonstrated a 7.5minute delay after 1 previous procedure, with the delivery occurring 9.6 minutes slower with 2 previous cesarean deliveries (P ⬍ .001 for both). Severe adhesions increased the delivery time during the second cesarean delivery by 79% (8.4
minutes) and by 117% (12.6 minutes) during the third cesarean delivery (P ⬍ .001 for both; Table IV). Likewise, the level of the resident who performed the primary cesarean correlated with the time to deliver the infant (r ⫽ 0.48, r2 ⫽ 0.23; P ⬍ .001). If interns were the primary surgeon, the time to delivery of the baby was 13.2 ⫾ 4.8 minutes; if the interns were second-year residents, the time to delivery was 9.7 ⫾ 3.7 minutes; if the interns were third-year residents, the time to delivery was 7.1 ⫾ 6.1 minutes, and if the interns were fourth-year residents, the time to delivery was 4.7 ⫾ 1.9 minutes. A linear correlation between level of resident and time to delivery of the infant was not seen with repeat cesarean deliveries. However, second-year residents required 3.8 additional minutes on average to deliver the infant during a repeat cesarean delivery, when compared with upper level residents (18.1 ⫾ 8.2 minutes vs 14.3 ⫾ 6.8 minutes; P ⫽ .01). There were no missing data on skin incision or delivery time in the Operating Department records. Cord blood gases were available for 81% of primary cesarean deliveries and 73% of repeat cesarean deliveries; Apgar scores were assigned to all infants. An emergent indication was more likely to result in an umbilical cord pH of ⬍7.2, when compared with nonurgent indication for primary cesarean procedure (OR, 4.4; 95% CI, 1.9-10.1; P ⫽ .002). Infants who were delivered during a
TABLE 4
Time from skin incision to delivery of the infant (minutes) Cesarean delivery Variable (min)
Primary delivery (n ⴝ 265)
Second delivery (n ⴝ 207)
Third delivery (n ⴝ 64)
Fourth delivery (n ⴝ 6)
Overall
10.7 ⫾ 6.0
16.3 ⫾ 7.7
19.2 ⫾ 10.4
28.8 ⫾ 11.1
Not urgent
12.2 ⫾ 5.8
17.0 ⫾ 7.6
19.5 ⫾ 10.4
28.8 ⫾ 11.1*
Emergent
7.1 ⫾ 5.2
11.3 ⫾ 6.8
15.8 ⫾ 11.7
*
No adhesions
14.8 ⫾ 6.9
15.8 ⫾ 6.3
12
Any adhesions
18.2 ⫾ 8.1
20.3 ⫾ 13.0
27.5 ⫾ 11.8
Severe adhesions
19.1 ⫾ 8.1
23.3 ⫾ 13.0
32.2 ⫾ 8.3
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ † ................................................................................................................................................................................................................................................................................................................................................................................ ‡ ................................................................................................................................................................................................................................................................................................................................................................................ ‡ ................................................................................................................................................................................................................................................................................................................................................................................
Values are means ⫾ SD. Repeat times compared with primary are significant (P ⬍ .05), unless otherwise indicated. * All of the fourth cesarean deliveries were scheduled or nonurgent procedures. †
Only 1 of the fourth cesarean deliveries was adhesion free, with no significant difference noted.
‡
The small number of cases precluded subgroup analysis.
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www.AJOG.org nonurgent cesarean delivery were twice as likely to have a low pH when repeat cesarean births were compared with primary cases (OR, 2.3; 95% CI, 1.1-4.5; P ⫽ .017). No significant difference in pH values was detected after emergent primary, compared with emergent repeat procedures. No correlation between time that was required to deliver the infant and pH was noted (r ⫽ 0.003, r2 ⫽ 0; P ⫽ .48). There was a significant correlation between pH value and the 1-minute Apgar score (r ⫽ 0.45, r2 ⫽ 0.20; P ⬍ .001). The 1-minute Apgar score also correlated with the time that was required for delivery of the infant (r ⫽ 0.21, r2 ⫽ 0.04; P ⬍ .001). The 1-minute Apgar scores were significantly lower for emergent cesarean deliveries, compared with nonurgent or scheduled cases (median, 8; interquartile range, 5-9; vs median, 8; interquartile range, 7-8; P ⫽ .005). However, infants who were delivered by nonurgent repeat cesarean procedures had a lower 1-minute Apgar score than did infants who were delivered by nonurgent primary cases (median, 8; interquartile range, 7-9; vs median, 8; interquartile range, 8-9; P ⫽ .005) No difference was noted in emergent cases. No statistically significant difference was detected in 5-minute Apgar scores between the primary and repeat cesarean deliveries. Operative complications were documented infrequently in our cohort. Two episodes of incidental cystotomy and 1 bowel injury were noted in each group; the only cervical laceration was documented in the primary cohort. Asymptomatic uterine dehiscence and uterine rupture occurred in 5.1% of repeat procedures, but only 2 cases (0.7%) resulted in emergent cesarean deliveries.
C OMMENT Cesarean deliveries are the most commonly performed abdominal surgeries in the United States. These procedures represent a subset of laparotomies and frequently are associated with factors that are known to induce adhesions (such as residual blood, postoperative infections, tissue desiccation, and foreign bodies). A recent prospective cohort
analysis indicated that adhesions occur frequently after cesarean deliveries without parietal peritoneal closures (73% after no closure vs 52% after closure).11 The general surgery literature has reported an incidence of intraperitoneal adhesions that range from 67%-93% with intraabdominal surgeries.12 From the first report ⬎100 years ago by Bryant13 to present day, adhesions have been held responsible for a multitude of postoperative and intraoperative complications.14 However, little attention has been focused on the potential negative impact of adhesions that occur after a cesarean delivery. Our study has confirmed that adhesions commonly form after a cesarean delivery and that this incidence increases with each subsequent cesarean birth. However, the retrospective cohort study design, with reliance on medical records, may introduce recall bias and underreporting of the true incidence and severity of pelvic adhesive disease. This fact may account for the lower incidence of adhesions after 1 cesarean delivery that we observed, compared with the ⬎70% adhesion formation rate that was published recently.11 Underreporting in our chart review may be also suggested by the infant delivery data. Although there was a correlation between the severity of adhesive disease and the length of time that was necessary to deliver the infant, repeat cesarean delivery with no documented adhesions also required a longer interval for successful delivery. These would seem to correct for the possibility that adhesions would be noted as “severe” in dictated operation reports just because the cesarean delivery took a long time. Distortion of tissue planes between the skin and peritoneal cavity or suprafascial scar tissue may account for some of the added time. Maternal weight and truncal obesity, which were not documented, could also be confounding factors. Nonetheless, each additional cesarean delivery, with the associated increase in the severity of pelvic adhesive disease, delays delivery of the infant and may compromise fetal health. In addition, during the study period, peritoneal closure was not performed routinely at our institution and was not documented in
Research
any of the operative reports. However, the underreporting of this practice may have biased our results and resulted in an underestimation of the true incidence of adhesions. Delivery of the infant took longer with each subsequent cesarean delivery. Likewise, the presence of adhesions increased the time from skin incision to delivery of the infant. Several factors may have played a role in this delay. The timing of infant delivery may be affected by the varying degrees of skill that each obstetric surgeon possesses. However, interns served as the primary surgeons for many of the primary cesarean deliveries, and most of the repeat cesarean deliveries were performed by residents with more surgical experience. Likewise, a staff physician is present at all cases, but repeat cases more often warrant active staff participation. If procedures with an intern as the primary surgeon were excluded from analysis, the overall delay in delivery of the infant increased by 2.1 minutes when primary cesarean deliveries were compared with repeat cesarean deliveries. These facts confound our results, and it is probable that the delay in infant delivery with subsequent cesarean surgeries would be even more dramatic if the more experienced surgeons had also performed the primary procedures. In addition, although statistical significance was achieved, the low number of third and fourth repeat cesarean deliveries is reflected in the wide confidence intervals and may hinder interpretation of the data. However, the time to deliver the infant was shorter in primary cesarean deliveries that were performed under emergent conditions, and by comparison, emergent repeat cesarean deliveries had a greater delay in the delivery of the infant than did nonurgent cases. The presence of adhesions also had the greatest impact on the time that was required to deliver the infant during repeat emergent cases, which further increases the potential negative impact on an infant who already may be compromised. During nonurgent cesarean births, the infants in our study were more likely to have a low pH value (⬍7.2) when delivered by repeat procedures, compared with primary cesarean cases. A signifi-
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cant linear correlation was also seen between the 1-minute Apgar score and the number of previous cesarean deliveries It could be suggested that both findings were due to longer exposure to the effects of anesthesia. In multiple studies, regional anesthesia has been shown to result in lower pH values at the time of cesarean births.15 Maternal hypotension from regional anesthesia may compromise fetal well-being to a greater degree if the delivery of the infant is delayed by adhesions or distorted tissue planes from previous cesarean deliveries. Maternal hypoventilation because of narcotic administration in labor or induction of general anesthesia may also result in lower pH values.16 Preexisting fetal compromise may also play a role. We specifically analyzed emergent indications separate from scheduled and nonurgent repeat cases. As one would expect, a higher percentage of infants had a low pH after emergent primary cases, compared with nonurgent procedures. However, no correlation between the number of previous cesarean procedures or the indication for a repeat cesarean delivery and the pH was detected. Likewise, no correlation was seen between the Apgar score and the presence of adhesions. The small decline in Apgar score and an increased incidence of umbilical cord pH ⬍7.0 may not reflect clinically significant deficits. The combination of pH, Apgar score, and base excess with insight
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www.AJOG.org into the resuscitation required by the infant would represent a complete picture of fetal well-being. However, only a small fraction of the available blood gases contained a recording of base excess, and the documentation of fetal resuscitation was lacking or inconsistent. We have confirmed earlier reports of the high incidence of pelvic adhesive disease after cesarean delivery and elucidated the severity and location of those adhesions. Our data quantified the difficulty of performing repeat cesarean deliveries and have demonstrated a potential detriment to fetal health with the resultant delayed delivery time. This information is valuable for the necessary preprocedure counseling that must occur with primary elective cesarean deliveries and may affect intrapartum treatment of patients with a history of a previous cesarean delivery. f REFERENCES 1. United States Center for Disease Control, National Center for Health Statistics. 2004 Hospital Discharge Advance Data No. 359. July 8, 2005. 2. Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2003. Natl Vital Stat Rep 2005;54:1-116. 3. Dietz HP, Bennett MJ. The effect of childbirth on pelvic organ mobility. Obstet Gynecol 2003;102:223-8. 4. Hemminki E. Long term maternal health effects of caesarean section. J Epidemiol Comm Health 1991;45:24-8. 5. Hall MH, Bewley S. Maternal mortality and mode of delivery. Lancet 1999;354:776.
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6. Murphy DJ, Stirrat GM, Heron J. The relationship between cesarean section and subfertility in a population-based sample of 14,541 pregnancies. Hum Reprod 2002;17:1914-7. 7. Sheiner E, Shoham-Vardi I, Hershkovitz R, Katz M, Mazor M. Infertility treatment is an independent risk factor for cesarean delivery among nulliparous women aged 40 and above. Am J Obstet Gynecol 2001;185:888-92. 8. Smith GCS, Pell JP, Dobble R. Caesarean section and risk of unexplained stillbirth in subsequent pregnancy. Lancet 2003;362: 1779-84. 9. Morrison JJ, Rennie JM, Milton PJ. Neonatal respiratory morbidity and mode of delivery at term: influence of timing of elective caesarean section. BJOG 1995;102:101-6. 10. Becker JM, Dayton MT, Fazio VW, et al. Prevention of postoperative abdominal adhesions by a sodium hyaluronate-based bioresorbable membrane: a prospective, randomized, double-blind multicenter study. J Am Coll Surg 1996;183:297-306. 11. Lyell DJ, Caughey AB, Hu E, Daniels K. Peritoneal closure at primary cesarean delivery and adhesions. Obstet Gynecol 2005;106:275-80. 12. Weibel MA, Manjo G. Peritoneal adhesions and their relation to abdominal surgery. Am J Surg 1973;126:345-53. 13. Bryant T. Clinical lectures on intestinal obstruction. Med Times Gazette 1872;1:363. 14. Menzies D, Ellis H. Intestinal obstruction from adhesions: How big is the problem? Ann R Coll Surg Engl 1990;72:60-3. 15. Mueller MD, Bruhwiler H, Schupfer GK, et al. Higher rate of fetal acidemia after regional anesthesia for elective cesarean delivery. Obstet Gynecol 1997;90:131-4. 16. Thorp JA, Rushing RS. Antepartum and intrapartum assessment: umbilical cord blood gas analysis. Obstet Gynecol Clin 1999;354: 776.
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OBSTETRICS
Postcesarean delivery adhesions associated with delayed delivery of infant Kelly J. Morales, MD; Michael C. Gordon, MD; G. Wright Bates, Jr, MD OBJECTIVE: The purpose of this study was to estimate the incidence of adhesions after cesarean deliveries and to determine their impact on delivery and infant well-being. STUDY DESIGN: This was a retrospective cohort analysis with chart review. The charts of 542 women who had undergone primary (265 women) or repeat cesarean (277 women) deliveries were reviewed. The incidence, severity, and locations of adhesions; delivery time; cord blood pH, and Apgar scores were noted.
fourth cesarean delivery had formed pelvic adhesive disease. Compared with primary cesarean section, delivery of the infant was delayed 5.6 minutes (52%) with 1 previous cesarean birth, 8.5 minutes (79%) after 2 cesarean birth, and 18.1 (169%) during the fourth cesarean birth (P ⬍ 0.001 for all comparisons).
RESULTS: After the first cesarean delivery, 100 of 217 women (46%)
CONCLUSION: A high percentage of cesarean deliveries result in adhesive disease, which delays repeat cesarean delivery of the fetus. The potential for adhesive disease should be included in counseling regarding primary elective cesarean births.
had pelvic adhesive disease; 48 of 64 women (75%) who underwent a third cesarean delivery and 5 of 6 women (83%) who underwent a
Key words: adhesion, cesarean delivery, complication, pregnancy
Cite this article as: Morales KJ, Gordon MC, Bates GW Jr. Postcesarean delivery adhesions associated with delayed delivery of infant. Am J Obstet Gynecol 2007;196:461.e1-461.e6.
C
esarean deliveries in the United States reached a record high in 2004 and represented 29% of all births. The higher incidence, in part, was due to an 8% increase in primary procedures and a 13% decrease in the rate of vaginal birth after a cesarean delivery.1,2 The decline
From the San Antonio Uniformed Services Health Education Consortium, Wilford Hall Medical Center, Lackland AFB, San Antonio, TX, and Brooke Army Medical Center, Fort Sam Houston, TX. Presented in part at the Armed Forces District Annual Meeting of the American College of Obstetricians and Gynecologists, Seattle, WA, Oct. 31-Nov. 4, 2005. The opinions expressed in this article are those of the authors and are not meant to be construed as official or as reflecting the opinions of the United States Air Force, the United States Army, or the Department of Defense. Received May 2006; accepted Dec. 12, 2006. Reprints: G. Wright Bates, Jr, MD, Atlanta Center for Reproductive Medicine, 100 Stone Forest Dr, Suite 300, Woodstock, GA 30189; [email protected] 0002-9378/$32.00 © 2007 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2006.12.017
of operative vaginal deliveries and vaginal deliveries of breech or multiple gestations also contributed to the increased cesarean section rate. In addition, primary elective cesarean births may be on the rise, with considerable national debate focused on the role of cesarean deliveries in the prevention of pelvic relaxation and the potential negative impact of vaginal deliveries on long-term maternal health.3-5 Cesarean deliveries also may impact maternal health negatively, with resultant difficulty in conceiving or delivering a healthy infant.6,7 A recent study has demonstrated an increased risk of unexplained stillbirth in subsequent pregnancies after cesarean delivery.8 In addition, delivery by cesarean may have an immediate impact on fetal well-being. The risk of neonatal respiratory distress that necessitates resuscitation with oxygen therapy is increased when the mode of delivery is cesarean.9 Multiple causes likely play a role in the negative effects of cesarean delivery. Postoperative adhesions are a well-known complication of other major abdominal surgeries and may be negative sequelae of cesarean deliveries. Reports indicate that adhesions form in most women who un-
dergo abdominal surgeries, surpassing 90% in some series.10 Cesarean deliveries represent a subset of laparotomies. Conventional wisdom is that repeat cesarean deliveries are often more difficult because of adhesions that involve the lower uterine segment and that delay entry into the uterine cavity and delivery of the infant. However, a Medline search of the English language literature (cesarean, adhesions, pregnancy, pH, Apgar) failed to identify studies that specifically examined the scope of pelvic adhesive disease after each successive cesarean delivery and the impact on delivery or well-being of the infant. Because the debate over elective primary cesarean delivery continues, it is important to study all facets that may contribute to both maternal and fetal morbidity. Likewise, optimal intrapartum management and counseling should reflect the potential delay of infant delivery and its impact on fetal health. Therefore, the goal of this study was to describe the incidence of adhesions that were encountered at repeat cesarean deliveries. Furthermore, we wanted to quantify the impact of the adhesions on the delivery of the infant and fetal well-being.
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TABLE 1
Indications for cesarean delivery Indication Nonreassuring fetal heart rate tracing
Primary cesarean delivery (n) 68*
Repeat cesarean delivery (n) 22*
..............................................................................................................................................................................................................................................
Abruption
8*
3*
Uterine rupture
0
2*
Severe preeclampsia remote from delivery
2
4
Cord prolapse
0
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
1*
..............................................................................................................................................................................................................................................
Placenta previa
3
1
Arrest disorder
99
31
4
1
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
Failed operative vaginal delivery
..............................................................................................................................................................................................................................................
Malpresentation
56
16
Maternal medical condition†
4
1
History of shoulder dystocia
2
Maternal herpes simplex virus on examination
9
Suspected macrosomia
3
1
Previous classic cesarean delivery or history of rupture
0
16
Elective repeat cesarean
N/A
172
Repeat cesarean delivery with advanced preterm labor
N/A
2
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
0
..............................................................................................................................................................................................................................................
1
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
.............................................................................................................................................................................................................................................. ..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Not otherwise specified
7
3
..............................................................................................................................................................................................................................................
N/A, not available. * Classified as emergent indications. †
Maternal cardiac or other medical condition, with labor contraindication.
M ATERIALS AND M ETHODS We performed a retrospective cohort analysis of women who had had a cesarean delivery at Wilford Hall Medical Center. After Institutional Board Review approval was obtained, the Wilford Hall labor and delivery database was queried to obtain the list of the first 285 consecutive women who had undergone a repeat cesarean delivery from the years 2000-2003 and the first 285 consecutive women with a primary cesarean delivery in that same time frame. Their medical records were reviewed to identify potential subjects who met the inclusion requirements and to compile the study data. Candidates were excluded (n ⫽ 26 461.e2
women ) if it was noted that they had a history of a pelvic infection (pelvic inflammatory disease noted in the prenatal records or admission history and physical) or abdominal surgery other than cesarean deliveries. Participants were included only once in the study, with the chart from their first cesarean delivery in that timeframe reviewed, and any subsequent deliveries were excluded (n ⫽ 2 deliveries) from analysis. Infants with a high risk of fetal compromise that included infants with major anomalies and infants who were ⬍30 weeks of gestational age or 1000 g were excluded from analysis of fetal well-being. Emergent cesarean deliveries were analyzed indepen-
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dently from nonurgent births for infant well-being because of the high likelihood of compromised fetal acid/base status that was unrelated to intraoperative factors. Sample size calculation indicated that at least 250 study subjects were needed in each group to detect a 25% difference in the incidence of adhesions and time required to deliver the infant. Demographic information included maternal age, gestational age, and infant gender and weight. Number of cesarean deliveries, indications for surgery, and complications were included in the surgical parameters. The time from the skin incision to delivery of the infant was calculated from Operating Department records. Adhesions were scored as severe, if the operative summary contained the words severe, extensive, or dense. Adhesions were categorized as mild, if operative notes used words such as present, mild, few, or some. The Apgar scores, cord blood gases, and infant resuscitation served as surrogate markers of infant well-being. Data were analyzed with SPSS statistical software (SPSS Inc, Chicago, IL). The normally distributed data (demographic variables and time to delivery) was presented as mean with SD after visual assessment of a frequency plot, with the determination of significance accomplished by the Fisher exact probability test. Nonparametric data (Apgar score, pH) were analyzed with the Mann Whitney test. The determination of significance for the incidence of adhesions and low pH was performed with a Pearson chi-square test and were expressed as odds ratios (OR) with 95% CI. Correlation was assessed with simple linear regression for the determination of Pearson’s product-moment correlation coefficient (r) and coefficient of determination (r2). A probability value of ⬍.05 was considered significant. We also reviewed the records to identify operative complications.
R ESULTS The study had 542 women who met the inclusion requirements, with 265 subjects having a primary cesarean delivery and 277 subjects having a second, third, or fourth cesarean delivery. Of those
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TABLE 2
Demographics of the primary and repeat cesarean delivery groups Cesarean delivery Demographic
Primary delivery (n ⴝ 265)
Second delivery (n ⴝ 207)
Third delivery (n ⴝ 64)
Fourth delivery (n ⴝ 6)
Maternal age (y)*
27.8 ⫾ 5.9
29.7 ⫾ 5.3
30.9 ⫾ 4.9
33.0 ⫾ 3.3
................................................................................................................................................................................................................................................................................................................................................................................
Gestational age (wk)*
38.3 ⫾ 3.6
38.9 ⫾ 2.0
38.3 ⫾ 2.2
37.9 ⫾ 1.8
Fetal weight (g)*
3237 ⫾ 82
3541 ⫾ 525
3445 ⫾ 658
3291 ⫾ 431
Gender
128/108
106/109
30/34
3/3
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ † ................................................................................................................................................................................................................................................................................................................................................................................
* Values are means ⫾ SD. †
Data are expressed as male/female.
women with primary cesarean deliveries, 76 women had emergent cesarean deliveries for indications that included nonreassuring fetal heart rate status, cord prolapse, and abruptio placentae remote from delivery; the remaining procedures had nonurgent indications. There were 28 emergent repeat cesarean deliveries; 249 of 277 women underwent elective repeat cesarean delivery or had other nonurgent indications (Table 1). All 277 women in the repeat cesarean group who were included in the analysis had undergone a low-transverse cesarean delivery. There were 3 patients in the primary cesarean delivery group who underwent a classic cesarean delivery. These patients were not excluded from analysis. Four patients in the primary cesarean group had general anesthesia, although all of the patients who had repeat cesarean deliveries had regional (spinal or epidural) anesthesia. The gestational age, infant
weight, and gender for the primary and repeat cesarean groups were not statistically different. The maternal age was compared in each group with the mean age of study subjects per cesarean delivery, which rose in an expected linear fashion with each successive cesarean delivery (r ⫽ 0.22, r2 ⫽ 0.05; P ⬍ .001; Table 2). Interns served as the primary surgeon for 46% of the primary and for only 6% of the repeat cesarean deliveries. Eleven women (4%) who underwent primary cesarean section had adhesions that were documented, although 153 (53%) of the women who underwent repeat cesarean delivery had adhesions (OR, 27; 95% CI, 13.2-47.9; P ⬍ .001). Forty-six percent of second cesarean deliveries (OR, 19.5; 95% CI, 10.6-39.7), 75% of the third cesarean deliveries (OR, 44.3; 95% CI, 31.5-164.6), and 83% of the fourth cesarean deliveries had documentation of adhesive disease (Table 3).
Fifty-four percent of the adhesions were classified as severe. Seven percent of all adhesions involved only the uterus and bladder. Adhesions that involved the anterior abdominal wall were noted in 77% of the individuals with repeat cesarean deliveries. Other sites that were documented included the uterus, bladder, adnexa, omentum, and small bowel. However, more than one half of the cases did not have information regarding the location of the adhesions documented. In addition, none of the charts documented the presence or absence of tissue distortion or scar formation that involved the subcuticular space, rectus muscles, or fascia. A statistically significant increase in the time from skin incision to delivery was found when repeat procedures were compared with primary procedures (Figure). Delivery of the infant was delayed 5.6 minutes (52%) with 1 previous
TABLE 3
Incidence and severity of adhesions documented Cesarean delivery Variable
First delivery
All repeat deliveries (n ⴝ 265)
Second delivery (n ⴝ 207)
Third delivery (n ⴝ 64)
Patients with adhesions (n)
11
153
100
48
Fourth delivery (n ⴝ 6) 5
................................................................................................................................................................................................................................................................................................................................................................................ † †
Patients with adhesions in each group (%)
4
Severe adhesions (n)
2
53*
46*
75*
83*
................................................................................................................................................................................................................................................................................................................................................................................
84*
55*
26*
3*
................................................................................................................................................................................................................................................................................................................................................................................
Mild adhesions (n)
9
16
11
5
0
No severity documented (n)
1
47
29
16
2
................................................................................................................................................................................................................................................................................................................................................................................
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* P ⬍ .05, compared with primary cesarean deliveries. †
P ⬍ .05, for third and fourth cesarean deliveries, compared with second cesarean delivery (first repeat).
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FIGURE
Time from skin incision to delivery of infant during 1st, 2nd, 3rd, and 4th cesarean delivery 70 60 50 40
Time required to deliver infant (minutes)
30 20 10 0 1st
2nd
3rd
4th
Number of cesarean deliveries
The boxplot represents the standard deviation. The thickline is the mean. The whiskers denote the maximum and minimum values.
cesarean delivery, 8.5 minutes (79%) after 2 cesarean deliveries, and 18.1 minutes (169%) during the fourth cesarean birth, compared with primary cases (P ⬍ .001 for all comparisons). The time from skin incision to removal of the infant was still slower by 4.2 minutes (59%) and 8.8 minutes (124%) for emergent indications after 1 or 2 previous cesarean births. Nonurgent cases demonstrated a 4.8- (39%) and 7.3- (60%) minute delay during the second and third cesarean de-
liveries (P ⬍ .05 for all 4 comparisons). The length of time that was required to deliver the infant also correlated with the presence or absence and severity of adhesion. Repeat cases in women who had any adhesions demonstrated a 7.5minute delay after 1 previous procedure, with the delivery occurring 9.6 minutes slower with 2 previous cesarean deliveries (P ⬍ .001 for both). Severe adhesions increased the delivery time during the second cesarean delivery by 79% (8.4
minutes) and by 117% (12.6 minutes) during the third cesarean delivery (P ⬍ .001 for both; Table IV). Likewise, the level of the resident who performed the primary cesarean correlated with the time to deliver the infant (r ⫽ 0.48, r2 ⫽ 0.23; P ⬍ .001). If interns were the primary surgeon, the time to delivery of the baby was 13.2 ⫾ 4.8 minutes; if the interns were second-year residents, the time to delivery was 9.7 ⫾ 3.7 minutes; if the interns were third-year residents, the time to delivery was 7.1 ⫾ 6.1 minutes, and if the interns were fourth-year residents, the time to delivery was 4.7 ⫾ 1.9 minutes. A linear correlation between level of resident and time to delivery of the infant was not seen with repeat cesarean deliveries. However, second-year residents required 3.8 additional minutes on average to deliver the infant during a repeat cesarean delivery, when compared with upper level residents (18.1 ⫾ 8.2 minutes vs 14.3 ⫾ 6.8 minutes; P ⫽ .01). There were no missing data on skin incision or delivery time in the Operating Department records. Cord blood gases were available for 81% of primary cesarean deliveries and 73% of repeat cesarean deliveries; Apgar scores were assigned to all infants. An emergent indication was more likely to result in an umbilical cord pH of ⬍7.2, when compared with nonurgent indication for primary cesarean procedure (OR, 4.4; 95% CI, 1.9-10.1; P ⫽ .002). Infants who were delivered during a
TABLE 4
Time from skin incision to delivery of the infant (minutes) Cesarean delivery Variable (min)
Primary delivery (n ⴝ 265)
Second delivery (n ⴝ 207)
Third delivery (n ⴝ 64)
Fourth delivery (n ⴝ 6)
Overall
10.7 ⫾ 6.0
16.3 ⫾ 7.7
19.2 ⫾ 10.4
28.8 ⫾ 11.1
Not urgent
12.2 ⫾ 5.8
17.0 ⫾ 7.6
19.5 ⫾ 10.4
28.8 ⫾ 11.1*
Emergent
7.1 ⫾ 5.2
11.3 ⫾ 6.8
15.8 ⫾ 11.7
*
No adhesions
14.8 ⫾ 6.9
15.8 ⫾ 6.3
12
Any adhesions
18.2 ⫾ 8.1
20.3 ⫾ 13.0
27.5 ⫾ 11.8
Severe adhesions
19.1 ⫾ 8.1
23.3 ⫾ 13.0
32.2 ⫾ 8.3
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ † ................................................................................................................................................................................................................................................................................................................................................................................ ‡ ................................................................................................................................................................................................................................................................................................................................................................................ ‡ ................................................................................................................................................................................................................................................................................................................................................................................
Values are means ⫾ SD. Repeat times compared with primary are significant (P ⬍ .05), unless otherwise indicated. * All of the fourth cesarean deliveries were scheduled or nonurgent procedures. †
Only 1 of the fourth cesarean deliveries was adhesion free, with no significant difference noted.
‡
The small number of cases precluded subgroup analysis.
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www.AJOG.org nonurgent cesarean delivery were twice as likely to have a low pH when repeat cesarean births were compared with primary cases (OR, 2.3; 95% CI, 1.1-4.5; P ⫽ .017). No significant difference in pH values was detected after emergent primary, compared with emergent repeat procedures. No correlation between time that was required to deliver the infant and pH was noted (r ⫽ 0.003, r2 ⫽ 0; P ⫽ .48). There was a significant correlation between pH value and the 1-minute Apgar score (r ⫽ 0.45, r2 ⫽ 0.20; P ⬍ .001). The 1-minute Apgar score also correlated with the time that was required for delivery of the infant (r ⫽ 0.21, r2 ⫽ 0.04; P ⬍ .001). The 1-minute Apgar scores were significantly lower for emergent cesarean deliveries, compared with nonurgent or scheduled cases (median, 8; interquartile range, 5-9; vs median, 8; interquartile range, 7-8; P ⫽ .005). However, infants who were delivered by nonurgent repeat cesarean procedures had a lower 1-minute Apgar score than did infants who were delivered by nonurgent primary cases (median, 8; interquartile range, 7-9; vs median, 8; interquartile range, 8-9; P ⫽ .005) No difference was noted in emergent cases. No statistically significant difference was detected in 5-minute Apgar scores between the primary and repeat cesarean deliveries. Operative complications were documented infrequently in our cohort. Two episodes of incidental cystotomy and 1 bowel injury were noted in each group; the only cervical laceration was documented in the primary cohort. Asymptomatic uterine dehiscence and uterine rupture occurred in 5.1% of repeat procedures, but only 2 cases (0.7%) resulted in emergent cesarean deliveries.
C OMMENT Cesarean deliveries are the most commonly performed abdominal surgeries in the United States. These procedures represent a subset of laparotomies and frequently are associated with factors that are known to induce adhesions (such as residual blood, postoperative infections, tissue desiccation, and foreign bodies). A recent prospective cohort
analysis indicated that adhesions occur frequently after cesarean deliveries without parietal peritoneal closures (73% after no closure vs 52% after closure).11 The general surgery literature has reported an incidence of intraperitoneal adhesions that range from 67%-93% with intraabdominal surgeries.12 From the first report ⬎100 years ago by Bryant13 to present day, adhesions have been held responsible for a multitude of postoperative and intraoperative complications.14 However, little attention has been focused on the potential negative impact of adhesions that occur after a cesarean delivery. Our study has confirmed that adhesions commonly form after a cesarean delivery and that this incidence increases with each subsequent cesarean birth. However, the retrospective cohort study design, with reliance on medical records, may introduce recall bias and underreporting of the true incidence and severity of pelvic adhesive disease. This fact may account for the lower incidence of adhesions after 1 cesarean delivery that we observed, compared with the ⬎70% adhesion formation rate that was published recently.11 Underreporting in our chart review may be also suggested by the infant delivery data. Although there was a correlation between the severity of adhesive disease and the length of time that was necessary to deliver the infant, repeat cesarean delivery with no documented adhesions also required a longer interval for successful delivery. These would seem to correct for the possibility that adhesions would be noted as “severe” in dictated operation reports just because the cesarean delivery took a long time. Distortion of tissue planes between the skin and peritoneal cavity or suprafascial scar tissue may account for some of the added time. Maternal weight and truncal obesity, which were not documented, could also be confounding factors. Nonetheless, each additional cesarean delivery, with the associated increase in the severity of pelvic adhesive disease, delays delivery of the infant and may compromise fetal health. In addition, during the study period, peritoneal closure was not performed routinely at our institution and was not documented in
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any of the operative reports. However, the underreporting of this practice may have biased our results and resulted in an underestimation of the true incidence of adhesions. Delivery of the infant took longer with each subsequent cesarean delivery. Likewise, the presence of adhesions increased the time from skin incision to delivery of the infant. Several factors may have played a role in this delay. The timing of infant delivery may be affected by the varying degrees of skill that each obstetric surgeon possesses. However, interns served as the primary surgeons for many of the primary cesarean deliveries, and most of the repeat cesarean deliveries were performed by residents with more surgical experience. Likewise, a staff physician is present at all cases, but repeat cases more often warrant active staff participation. If procedures with an intern as the primary surgeon were excluded from analysis, the overall delay in delivery of the infant increased by 2.1 minutes when primary cesarean deliveries were compared with repeat cesarean deliveries. These facts confound our results, and it is probable that the delay in infant delivery with subsequent cesarean surgeries would be even more dramatic if the more experienced surgeons had also performed the primary procedures. In addition, although statistical significance was achieved, the low number of third and fourth repeat cesarean deliveries is reflected in the wide confidence intervals and may hinder interpretation of the data. However, the time to deliver the infant was shorter in primary cesarean deliveries that were performed under emergent conditions, and by comparison, emergent repeat cesarean deliveries had a greater delay in the delivery of the infant than did nonurgent cases. The presence of adhesions also had the greatest impact on the time that was required to deliver the infant during repeat emergent cases, which further increases the potential negative impact on an infant who already may be compromised. During nonurgent cesarean births, the infants in our study were more likely to have a low pH value (⬍7.2) when delivered by repeat procedures, compared with primary cesarean cases. A signifi-
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cant linear correlation was also seen between the 1-minute Apgar score and the number of previous cesarean deliveries It could be suggested that both findings were due to longer exposure to the effects of anesthesia. In multiple studies, regional anesthesia has been shown to result in lower pH values at the time of cesarean births.15 Maternal hypotension from regional anesthesia may compromise fetal well-being to a greater degree if the delivery of the infant is delayed by adhesions or distorted tissue planes from previous cesarean deliveries. Maternal hypoventilation because of narcotic administration in labor or induction of general anesthesia may also result in lower pH values.16 Preexisting fetal compromise may also play a role. We specifically analyzed emergent indications separate from scheduled and nonurgent repeat cases. As one would expect, a higher percentage of infants had a low pH after emergent primary cases, compared with nonurgent procedures. However, no correlation between the number of previous cesarean procedures or the indication for a repeat cesarean delivery and the pH was detected. Likewise, no correlation was seen between the Apgar score and the presence of adhesions. The small decline in Apgar score and an increased incidence of umbilical cord pH ⬍7.0 may not reflect clinically significant deficits. The combination of pH, Apgar score, and base excess with insight
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www.AJOG.org into the resuscitation required by the infant would represent a complete picture of fetal well-being. However, only a small fraction of the available blood gases contained a recording of base excess, and the documentation of fetal resuscitation was lacking or inconsistent. We have confirmed earlier reports of the high incidence of pelvic adhesive disease after cesarean delivery and elucidated the severity and location of those adhesions. Our data quantified the difficulty of performing repeat cesarean deliveries and have demonstrated a potential detriment to fetal health with the resultant delayed delivery time. This information is valuable for the necessary preprocedure counseling that must occur with primary elective cesarean deliveries and may affect intrapartum treatment of patients with a history of a previous cesarean delivery. f REFERENCES 1. United States Center for Disease Control, National Center for Health Statistics. 2004 Hospital Discharge Advance Data No. 359. July 8, 2005. 2. Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2003. Natl Vital Stat Rep 2005;54:1-116. 3. Dietz HP, Bennett MJ. The effect of childbirth on pelvic organ mobility. Obstet Gynecol 2003;102:223-8. 4. Hemminki E. Long term maternal health effects of caesarean section. J Epidemiol Comm Health 1991;45:24-8. 5. Hall MH, Bewley S. Maternal mortality and mode of delivery. Lancet 1999;354:776.
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6. Murphy DJ, Stirrat GM, Heron J. The relationship between cesarean section and subfertility in a population-based sample of 14,541 pregnancies. Hum Reprod 2002;17:1914-7. 7. Sheiner E, Shoham-Vardi I, Hershkovitz R, Katz M, Mazor M. Infertility treatment is an independent risk factor for cesarean delivery among nulliparous women aged 40 and above. Am J Obstet Gynecol 2001;185:888-92. 8. Smith GCS, Pell JP, Dobble R. Caesarean section and risk of unexplained stillbirth in subsequent pregnancy. Lancet 2003;362: 1779-84. 9. Morrison JJ, Rennie JM, Milton PJ. Neonatal respiratory morbidity and mode of delivery at term: influence of timing of elective caesarean section. BJOG 1995;102:101-6. 10. Becker JM, Dayton MT, Fazio VW, et al. Prevention of postoperative abdominal adhesions by a sodium hyaluronate-based bioresorbable membrane: a prospective, randomized, double-blind multicenter study. J Am Coll Surg 1996;183:297-306. 11. Lyell DJ, Caughey AB, Hu E, Daniels K. Peritoneal closure at primary cesarean delivery and adhesions. Obstet Gynecol 2005;106:275-80. 12. Weibel MA, Manjo G. Peritoneal adhesions and their relation to abdominal surgery. Am J Surg 1973;126:345-53. 13. Bryant T. Clinical lectures on intestinal obstruction. Med Times Gazette 1872;1:363. 14. Menzies D, Ellis H. Intestinal obstruction from adhesions: How big is the problem? Ann R Coll Surg Engl 1990;72:60-3. 15. Mueller MD, Bruhwiler H, Schupfer GK, et al. Higher rate of fetal acidemia after regional anesthesia for elective cesarean delivery. Obstet Gynecol 1997;90:131-4. 16. Thorp JA, Rushing RS. Antepartum and intrapartum assessment: umbilical cord blood gas analysis. Obstet Gynecol Clin 1999;354: 776.