To determine the risk factors related to recurrent caesarean section (C.S) morbidity and to suggest a morbidity scoring system based on these risk factors which can help in the prediction of C.S. morbidity.
Based on individual risk factors, a scoring system was developed to predict the cesarean section morbidity.
Objective: To determine the risk factors related to recurrent caesarean section (C.S) morbidity and to suggest a morbidity scoring system based on these risk factors which can help in the prediction of C.S. morbidity.
Patients & Methods: This prospective study included 1000 women undergoing Caesarean Section (C.S) under general anaesthesia, divided into two groups: Group (1): Control Group,500 patients, who underwent C.S for the first time. Group (2): Study Group, 500 patients who had one or more previous C.S. Simple scoring system was developed to record the possible risk factors related to C.S morbidity.
Results: There were 6 significant pre-operative risk factors. These are: high parity, preterm delivery, placenta praevia, antepartum haemorrhage, medical disorders and bad general condition. There were 5 highly significant risk factors related to intra-operative morbidity which were: high parity, placenta praevia, intra-peritoneal adhesions, low experienced surgeon (P<0.001) and preterm gestational age (P<0.01) and 5 risk factors related to previous C.S operation these were: previous 3 or more C.S (P<0.01), previous C.S at rural hospital or private clinic (P<0.001), previous upper segment C.S (P<0.05), previous complicated C.S (P<0.05) and tender previous scar (P<0.01). Eleven factors related to post-operative morbidity were more significant in the repeated C.S. group. The incidence of overall morbidities were significantly more in the repeated C.S group. Total post-operative morbidity was highly significant starting from previous 4 or more C.S Risk factors related to intra-operative morbidity were used to develop a morbidity scoring system.
Conclusion: Based on a summation of logistic coefficient corresponding to individual risk factor, a scoring system was suggested which can help in the prediction of C.S. morbidity. Further prospective evaluation of this scoring system would be helpful to confirm the usefulness and practicality of this system.
Key words :caesarean section, repeated caesarean, maternal morbidity, risk factors, scoring system.
Tables will open in new windows for easy reference.Introduction & Aim of Work
The Caesarean Section (C.S) rate has increased at an accelerated pace over the past two decades from 5% to 25% in the United States and some other countries (1), with repeat C.S accounting for as much as 35% to 50% of the increased abdominal deliveries(2). A post-partum history of four or more previous caesarean sections is a clear risk factor for intra-operative complications (3).There is objective evidence to support the widely held view that multiple C.S predispose to an increased risk of uterine rupture, severe intraperitoneal adhesions, significant haemorrhage, placenta praevia, placenta acreta, bladder injury and hysterectomy, etc. (3)(4)(5)(6)(7)(8)(9).
The rapid increase in C.S rate (2) may lead to a higher number of women facing multiple C.S. Despite their need for information regarding the safety of additional C.S, little data are available (5). The rapidly increasing number of diagnostic and therapeutic options, the quality demands of patients and the public, and the emphasis on cost containment all contribute to the need for more explicit clinical reasoning and decision making (11).
This study has been done to determine the risk factors associated with recurrent C.S morbidity (intra- and/or post-operative) and to develop a scoring system, which can help in the prediction of C.S. morbidity and may affect the decision for the current and future pregnancy.
Subjects & Methods
This prospective study was performed on 1000 women undergoing C.S delivery, under general anaesthesia, at Al-Azhar University Hospitals, Cairo, Egypt, during a 16 month period from December 1999 to April 2001.
The patients were classified into two groups. The first group included 500 patients who underwent C.S for the first time (control group). The second included 500 patients who had one or more previous C.S. (study group) or (repeated C.S group). All patients in the control group (with no previous uterine scar) or in the study group (with previous uterine scar) were admitted to the hospital for C.S operation.
A detailed history and general, abdominal and pelvic examination were done for each patient. An intra-venous line was connected and a blood sample was taken for haemoglobin (Hb) estimate and cross-matching for a blood transfusion if needed. Ultrasonography was done for patients who had no previous sonographic report or not requiring an urgent C.S. All pre-operative data were recorded in a simplified form designed by the research workers.
All patients underwent C.S. under general anaesthesia in the same operation room for emergency C.S. (connected with the delivery department). All data of intra-operative findings, operative procedures, morbidities and assessment of the newborn data was recorded in a simple data record.
As the estimate of intra-operative blood loss is subjective and can be inaccurate, comparison of preoperative and postoperative haemoglobin for all patients in both groups provided more objective measures to estimate this finding. Also, patients who needed the transfusion of one or more units of blood during their C.S. operation were recorded so as to determine whether their intra-operative bleeding was moderate or severe.
All patients were observed post-operatively for at least 5-7 days for early detection of any post-operative complication and its management. Follow-up of the newborns and the premature babies who were admitted to the pre-mature baby center and their data were also recorded.
Several risk factors can contribute to C.S. morbidity (3)(4)(5)(6)(7)(8)(9)(10).To decide about these risk factors, a scoring system was developed to record the possible risk factors and the different morbidities. Data was recorded for all patients in a manner of a simplified scoring system composed of 0,1,2 for both the pre-operative and intra-operative risk factors on one hand; and the intra-operative and post-operative morbidities on the other hand. The definition of this scoring system was :
For The Risk Factors:
0: No risk factor
1: The risk factor may be a cause of morbidity
2: The risk factor is a cause of morbidity
For The Morbidity:
No = 0 : No abnormality detected
Yes = 1: Mild or moderate degree of morbidity
2 : Severe degree of morbidity
Statistical analysis by one way analysis of variance (ANOVA) was done between the control and repeated C.S. groups to determine the significant risk factors.
Each morbidity was statistically analysed and compared to that of the control group. The study group was statistically evaluated to correlate between the number of previous C.S and morbidity. Total scores of risk factors which are included in cases with either intra and/or postoperative morbidity were compared in both groups to evaluate which factor lead to morbidity.
Multivariate logistic regression analysis of pre and intraoperative risk factors was done as separate variables, then the strongest risk factors related to each morbidity were included in logistic regression analysis for the study group to determine the risk factors that dependently and significantly influence or lead to specific morbidity.
Multi-variate analysis allows each variable to be weighted according to its importance (strength of correlation) and variables with no correlation being omitted. Computer package (Epi-info-ver.5) was used to correlate the regression coefficient for each pair of variables, then the regression coefficient of all possible combinations of variables was calculated. (12)(13)
Each variable was evaluated one at a time (forward selection procedure) until no additional variables made a significant contribution. Backward elimination was also used; the results were identical.
Odds ratio, Mean, B-coefficient, 95% confidence intervals, Standard error, F-test and P-value were estimated for risk factor which was statistically and strongly related to a specific morbidity in the final analysis.
The risk factors were then evaluated with multiple logistic regression to identify which factors were independently associated with C.S. morbidity. Logistic coefficients were averaged to determine a mean coefficient for all risk factors.
Cesarean deliveries accounted for 14.3% of the 7000 deliveries performed during the study period.
Preoperative risk factors:
According to the C.S morbidity scoring system there were 12 pre-operative risk factors of significant importance for developing C.S. morbidity; 6 factors were significant in the control and another 6 were significant in the study group (Table 1).
Among the cases of repeated C.S Group, 5 possible pre-operative risk factors specifically related to the previous uterine scar (s) were selected. These are the number of previous C.S (total score 641), place of previous C.S (total score 335), type of previous uterine incisions (total score 123), complications of previous C.S (total score 133), and pre-operative assessment of the integrity of the previous uterine scar (s) (total score 162).
Intraoperative risk factors:
Specific to intraoperative risk factors there were 5 significant factors for the study group and only one significant factor in the control group which was limited experience of the surgeon who performed the C.S operation. (Table 2).
On studying the frequency of intra-operative morbidity in relation to the number of previous C.S (Table 3)., three or more previously performed C.S 's were significantly associated with severe bleeding with or without bilateral extension of a uterine incision (P<0.01). Rupture of previous uterine scar and cesarean hysterectomy, were highly significant starting from previous four C.S. (P<0.01). The incidence of overall intra-operative morbidity was significantly more in the repeated C.S. group (P<0.05). In the repeated C.S. group, the frequency of dehiscence of the previous uterine scar was 21.4% and rupture of the previous uterine scar was 6.4% According to the number of previous C.S 's it was found that the incidence of dehiscence was increased with the increasing number of C.S, reaching to 33.3% among cases with 6 or more operations. Also, the incidence of rupture of previous uterine scar or scars started to be significant after the previous two C.S, and after a previous hysterotomy while it became highly significant after previous four C.S (P<0.01)The extension of the uterine incisions, when associated with moderate or severe bleeding, were more significant in the repeated C-S group than in the Control Group (P- <0.001). Bilateral extension of the uterine incision started to increase with the increasing number of C.S 's reaching 33.3% after previous four C.S 's, and this was associated with severe bleeding in 16.6% of the cases. Injury of the urinary bladder during the C.S. procedure occurred more in the repeated C.S. group (2.2%) than in the Control Group (0.6%).The difference was statistically significant (P<0.05) The incidence of intra-operative bladder injury in the repeated C.S Group was found to increase with increasing number of previous C.S 's from the fourth or more, and with a previous hysterotomy.
Subtotal abdominal hysterectomy was observed to be more frequent in the repeated C.S Group (2.2%) compared with the Control Group (0.8%).This was more frequent among the repeated C.S. group especially after the previous 4 or more C.S. ( P-<0.001). (Table 3).
The incidence of overall intra-operative morbidity in the repeated C.S Group was 55.4% compared with 46.6% in the Control Group (P<0.05).The overall intra-operative morbidity was increased significantly during the fourth or more C.S 's procedure.
In the repeated C.S. group, most of maternal post-operative complications shows no relation to the number of previous C.S. However, there was a significant increase in the incidence of post-operative haemorrhage after number four or more previous C.S. and after previous hysterotomy. (Table 4).The overall post-operative morbidity in the repeated C.S. group started to increase from the fourth C.S operation. Regarding neonatal morbidity, neonatal asphyxia (determined by Apgar's score), was significantly higher in the Study Group.
On studying the scores of the risk factors which related to intra-operative morbidity,10 factors were more significant among the cases with repeated C.S when compared to that of the control cases. Of these factors, 5 were highly significant, these were: high parity, placenta praevia, intraperitoneal adhesions, a surgeon with limited experience (P<001), and preterm gestational age (P<0.01). The other 5 significant factors were severe pre-eclampsia or uncontrolled diabetes, dystocia, ante-partum haemorrhage, upper segment uterine incision and difficult delivery of the fetus (P<0.05). Also 11 risk factors related to post-operative morbidity were more significant among the cases with repeated C.S when compared with that of the control cases. These were: high parity, severe pre-eclampsia or uncontrolled diabetes, preterm gestational age, bad general condition of the patient, low experience surgeon, intra-peritoneal adhesions (P<0.001), placenta praevia, vaginal bleeding, upper segment uterine incision (P<0.01), dystocia, repair of irregular uterine edges (P<0.05). Another 5 risk factors related to previous C.S operation and were associated with increased intra-operative more than post-operative morbidity which were previous 3 or more C.S (P<0.01), previous C.S at rural hospital or private clinic (P<0,001), previous upper segment uterine scar (P<0.05), previous complicated C.S (P<0.05) and tender previous uterine scar (P<0.01).
Table 5 summarize risk factors which lead to C.S morbidity in the repeated C.S Group. Using the data set estimation of the logistic model (by a method of estimation called maximum likelihood) yielded results of significant risk factors that were arranged according to their B-coefficient values, which means their close relation to the occurrence of the morbidities.
After exclusion of less significant risk factors, it has been tried to reach a scoring system using the highly significant and most relevant risk factors. (Table 6)Discussion
Analyses of cesarean deliveries have identified several factors associated with the operation. These include: demographic factors (14), intrapartum factors (15), nonclinical factors (16) and site of care (17). However, no system combines the factors associated with cesarean delivery. So that patient could be stratified based on their risk of cesarean delivery. Risk stratification is an important strategy in obstetrics.(10).The scoring system that help to identify patients at high risk for adverse outcomes, allow intensive obstetric services to be concentrated for those patients who are most likely to need them (18).The application of intensive services to high-risk women helps assure that necessary services are available and delivered in a cost-efficient manner (10).
Preoperative risk factors:
In the present study, there were 6 pre-operative risk factors of significant importance for developing morbidity in patients who had a previous C.S, and underwent a repeated C.S. procedure. These factors were high parity, pre-term delivery, placenta praevia, associated active vaginal bleeding, medical disorders and bad general condition.
High parity, associated with complications such as anaemia, prolonged labour and malpresentation, can lower the resistance, encouraging infection in the postoperative period. (19). Birth weight is also associated with parity. Grand multiparas deliver much larger ones.(20)
In term of the gestational age, the number of cases that were less than 34 weeks of gestational age was more in the repeated C.S. Group compared with the Control Group. There is increased maternal morbidity associated with C.S at very early gestational ages compared to C.S at term.(21)
Cases associated with moderate or severe gestational or medical disorders in the repeated C.S. Group were 18.0% & 30% respectively, more than those in the Control Group 14.6% & 25.0%. Most of the cases in this series were multipara with all the associated hazards of multiparity. Also, this may reflect that medical disorders during pregnancy, by themselves, may indicate to deliver by C.S. In gestational diabetes, increased newborn fat was associated in-independably with an increased risk for C.S in labor.(22)
The incidence of placenta praevia or lower uterine segment anterior placenta was 20.0 % among those with a previous Caesarean Section Group which is much higher when compared with 13.8% in the Control Group. The difference is, statistically, highly significant (P <0.001). Women with a history of cesarean delivery are 50% more likely to have a subsequent birth complicated by placenta praevia than those without such a history.(4)(20)(21)(22)(23).Cases presented by antepartum haemorrhage, with active vaginal bleeding, were noticed to be more in the repeated C.S Group (14.2%) compared with 8.4% in the Control Group. These results confirmed previous studies.(20)
Among the cases of repeated C.S. Group, 5 possible pre-operative risk factors specifically related to the previous uterine scar (s) were selected. These were:1-the number of previous C.S. Seidman et al 1994 (24) noted increase in the percent of uterine ruptures with numbers of prior C.S,. However, in primary preterm C.S, the risk of postoperative maternal morbidity and uterine rupture or dehiscence in subsequent pregnancies were increased (25) Hanley et al 1996 (26) reported that there is little objective evidence to support the widely held view that multiple C.S predispose to an increased risk of uterine rupture in subsequent pregnancy., 2-place of the previous procedure, Richards and Richards 1982 (27), reported a significant increase in the number of positive cultures and use of antibiotics during C.S in rural hospitals when compared with urban hospitals and they reported little difference in maternal and neonatal morbidity rates between urban and rural hospitals (27).,3-type of previous uterine incisions, as a lower uterine incision has a much lower risk of scar rupture than a classical incision (28)(29).,4-complications of the previous C.S. and 5-pre-operative assessment of the integrity of the previous uterine scar (s). The fear of uterine rupture remains the main indication for repeat C.S.(30)
Intraoperative risk factors:
The possible intra-operative risk factors (Table 2), which could lead to intra-operative or post operative morbidities are:1-the level of the surgeon who performs the C.S operation. In the present study the, level of training among the surgeons was equal for both groups over the study period but surgeons with a high level of experience or consultant level in the Control Group were 17% compared with 35.8% in the repeated C.S Group. It is noted that C.S should only be performed by well trained personnel who are appropriately skilled (31).Only superficial wound separation due to haematoma in patients operated on by assistant medical officers was slightly more than in patients operated on by specialists in obstetrics (32).2-presence of adhesions during dissection, as adhesion formation remains a major concern after surgery (33).,3-type of uterine incision. vertical incisions are used less frequently because of greater surgical risks, blood loss, infections, and uterine rupture in subsequent pregnancies (34).,4-difficulty in fetal delivery. Sonographic determination of the position of the fetus and location of the placenta are vital in deciding the surgical approach and maneuver for delivery of the fetus (35)(36).,5-mode of placental delivery. Manual extraction of the placenta is associated with a greater risk of post-cesarean endometritis than that observed with assisted spontaneous placental delivery.(37).,and 6-the condition of repair of the edges of uterine incision. The character of the scar has been suggested to be altered by some defective procedures, such as inclusion of decidua in suture line, use of too much catgut to repair irregular uterine edges and, too much tightening of the suture line by continuous suturing and unequal thickness of uterine edges.(34).
In the present study, intraoperative complications were analyzed (table 3).The results of this analysis confirmed previous studies.(6)(8)(38) Regarding post-operative morbidity (Table 4) , post-operative haemorrhage either in the form of, intraperitoneal bleeding or excessive vaginal bleeding was more in the repeated C.S. Group (5.4%) than the Control Group (2.0%). Yao (1990) (39) reported 5.87% incidence of post-partum haemorrhage after C.S.
There was an increased poor perinatal outcome in the repeat C.S. Group reaching 28.4% compared with 21.8% in the Control Group (P-<0.05). Wrakusumah in 1995 (7) studied the perinatal outcome in C.S. deliveries and reported 15.5 – 18.7 % of poor outcome (Apgar’s score 1-6) and 68.6-78.6% of good outcome (Apgar’s score 7 or more). There was no specific statistically significant effect of increasing the number of C.S. (7).Although Infant born by elective repeat caesarean section are at increased risk of developing respiratory problems (40).
Although respiratory distress has been claimed to be higher for repeat C.S than for vaginal delivery, it is unlikely that there is a significant difference when gestational ages of the fetuses are identical and, fetal hypoxia and acidosis are avoided (9).
In the present study the results of regression analysis support the findings of total score analysis and they are important in a number of respects, including :
Intra-operative C.S. morbidity increased especially in the fourth C.S. or the previous complicated one
Post-operative morbidity significantly increased especially in those cases with a history of complicated previous C.S.. or in anaemic patients, patients with a bad general condition, no use of prophylactic antibiotics, manual separation and delivery of the placenta during C.S., and repair of irregular uterine edges with multiple sutures
High risk factors lead to intra-operative morbidity in repeated C.S. Group are pre-term gestational age, previous 3 C.S. or more, associated severe pre-eclampsia or uncontrolled diabetes, placenta praevia, tender previous uterine scar, and the presence of a surgeon with limited experience.
Clinical risk factors associated with intra-operative C.S. morbidity were used to develop a morbidity scoring system based on a summation of logistic coefficient corresponding to individual risk factor. Such a scoring system may be recommended (table 6), including 5 factors to predict the occurrence of intra-operative morbidity this might be useful to low-experienced or junior level surgeons who perform C.S. while making arrangements for consultation by or from a more experienced surgeon. Statistically, the cut-off point of this score in our study was equal to 3, i.e. surgeon who perform C.S. with limited or little experience=<3; and surgeon who have more or high- experience=>3.
A further prospective evaluation of this scoring system would be helpful to confirm the usefulness and practicality of this system in prediction of intra-operative C.S. morbidity and to determine the ease of use
In conclusion: The high risk factors associated with intra-operative C.S. morbidity were used to develop a morbidity scoring system based on a summation of logistic coefficient corresponding to individual risk factor. Such a scoring system may be recommended to predict the occurrence of intra-operative morbidity and might be useful to limited-experienced surgeon who perform C.S. while making arrangements for consultation of a more experienced surgeon.
Table 1: Distribution of cases according to the C.S. morbidity scoring system - Preoperative Risk Factors
Table 2: Frequency and scoring of possible intra-operative risk factors
Table 3: Frequency of intra-operative morbidity in relation to the number of previous C.S. in the study group compared with the control group
Study Group (Repeated C.S. Group)
Table 4: Frequency of post-operative morbidity in relation to the number of previous C.S. In the study group compared with the control group
Study Group (Repeated C.S. Group)
Table 5: Logistic regression analysis of risk factors which are commonly associated with intra and post-operative C.S. morbidity in Repeated C.S. Group (Study Group)
Table 6: Suggested Score
1. Cepicky P, Stembera Z, Zema V, Lomickova T, Mandys F. When is it possible to meet the wish of a women to terminate her labour by Cesarean Section ? Europ J Obstet Gynecol Reprod Biol 1991; 38(2):109 â 12.
2. Shiono PH, Mc Nellis D, Rhoads GG :Reasons for the rising cesarean delivery rates:1978-1984.Obstet Gynecol 1987;69:696-700.
3. Hanley ML, Smulian JC, Lake MF, McLean DA, Vintzileos AM. Analysis of repeat cesarean delivery indications : Implications of heterogeneity. Am J Obstet Gynecol 1996;175 : 883 â 888.
4. Taylor VM, Kramer MD, Vaughan TL, Peacock S. Placenta Previa and Prior Cesarean Delivery : How Strong is the Association ?. Obstet Gynecol 1994; 84 : 55 â 57.
5. Kirkinen P:Multiple cesarean sections: outcomes and complications. Br J Obstet Gynecol 1988;95:777-782.
6. Caughey AB, Shipp TD, Repke JT, Zelop CM ,Cohen A, Lieberman E : Rate of uterine rupture during a trial of labour in women with one or two prior cesarean deliveries. Am. J Obstet Gynecol.1999; 181 (4) : 872 â 6.
7. Wirakusumah FF.): Maternal and Perinatal Mortality / Morbidity Associated with Cesarean Section in Indonesia. J Obstet Gynecol.1995; 21(5) : 475 â 481.
8. Rajasekar D,Hall M : Urinary Tract injuries during obstetric intervention. Br J Obstet Gynecol.1997;104 (6) : 731 â 4.
9. Morrison JJ, Rennie JM, Milton PJ: Neonatal respiratory morbidity and mode of delivery at term : influences of timing of elective cesarean section. British Journal of Obstetrics and Gynaecology, 1995;102 : 101 â 106.
10. Hueston WJ. Development of a cesarean delivery risk score. Obstet Gynecol 1994;84(6):965-68
11. Steyerberg E: Clinical decision sciences. Available at: http://www.eur.nl/fgg/mgz/clusters/cluster2.html. Accessed 20 April 2002.
12. Silver RK, Minogue J. When does a statistical fact become an ethical imperative?. Am J Obstet Gynecol 1987:157:229-233.
13. Hirsch RP, Riegelman RK. Basic principles and methods of analysis, In statistical operations: Analysis of health research data. eds, Hirsch RP, Riegelman RK, Blackwell Science, Inc. USA p 23,338.
14. Peipert JF, Bracken MB. Maternal age: An independent risk factor for cesarean delivery. Obstet Gynecol 1993;81:200-5
15. Thorp JA,Hu DH, Albin RM, et al. The effect of intrapartum epidural analgesia on nulliparous labor: A randomized controlled, prospective trial.Am J Obstet Gynecol 1993;169:851-8
16. Gould JB, Davey B, Stafford RS. Socioeconomic differences in rates of cesarean section. N Engl J Med 1989;321:231-9
17. de Regt RH, Minkoff HL, Feldman J, Schwarz RH. Relation of private or clinic care to cesarean birth rate. N Engl J Med 1986;315:619-24.
18. Sokol RJ, Rosen MG, Stojkov J, Chik L. Clinical application of high-risk screening on an obstetric service. Am J Obstet Gynecol 1979;135:1051-6.
19. Younis MN, Abd El Moneim S, Serour G, Hamed AF, El Massry G, Sultan M, et al. Factors affecting the occurrence of post-caesarean section febrile morbidity. Population Sciences, Journal of the International Islamic Center, Al Azhar University Cairo,1985; 6 : 139.
20. Ajayi RA, Soothill PW, Campbell S, Nicolaides KH. Antenatal testing to predict outcome in pregnancies with unexplained antepartum haemorrhage. Br J Obstet Gynecol 1992;99:122-125.
21. Evans LC, Combs CA. Increased maternal morbidity after caesarean section before 28 weeks of gestation. Int J Gynecol Obstet 1993;40:227-233.
22. Bernstein IR, Catalano PM. Examination of factors contributing to the risk of caesarean delivery in women with gestational diabetes.Obstet Gynecol 1994;83:462-465.
23. Crane JM, Van den Hof MC, Dodds L, Armson BA, Liston R. Maternal complications with placenta previa. Am J Perinatol 2000; 17 (2) : 101 â 5.
24. Seidman DS, Paz I, Nadu A, Dollberg S, Stevenson DK, Gale R, Mashiach S, Barkai G. Are multiple cesarean sections safe?. Eur J Obstet Gynecol and Reprod Biol 1994;57:7-12.
25. Halperin ME, Moore DC, Hannah WJ.: Classical versus low-segment transverse incision for preterm caesarean section : maternal complications and outcome of subsequent pregnancies. Br J Obst Gynaecol.1988; 95 : 990 â 996.
26. Hanley ML, Smulian JC, Lake MF, McLean DA, Vintzileos AM.: Analysis of repeat cesarean delivery indications : Implications of heterogeneity. Am. J. Obstet. Gynecol., 1996;175 : 883 â 888.
27. Richards TA, Richards JL. A comparison of cesarean section morbidity in urban and rural hospitals. Am J Obstet Gynecol 1982;144:270-275.
28. Abuhamad A, O’Sullivan MJ. Operative Techniques For Cesarean Section, In Surgical Obstetrics, ed. Plauche WC, W B Saunders Co. Philadelphia 1992;pp 417-429.
29. Hammad MMA, Seleha SH, Nayel MAB, Wahby MO. The silent rupture of the lower segment cesarean section scar. J Of Egyptian Society Of Obstet Gynecol 1990;16:63-69.
30. Meehan FP, Burke G, Kehoe JT. Update on delivery following prior cesarean section: a 15 years review 1972-1987.Int J Gynecol Obstet 1989;30:205-212.
31. Longombe AO, Wood PB, Dix R. Cesarean section: Indications and risks in rural Zaire. Int J Gynecol Obstet 1990;33:199-202.
32. Pereira C, Bugalho A, Bergstrom S,Vaz F, Cotiro M.A comparative study of cesarean deliveries by assistant medical officers and obstetricians in Mozambiuque. Br J Obstet Gynecol 1996;103:508-512.
33. Younis MN, Serour G, Hamed AF, El Tabbakh MN. Effect of antiprostaglandin, corticosteroids, and anticoagulants on postoperative adhesions after tubal surgery. III World Conference on, Fallopian Tube In Health and Disease July 3-6, Kiel, W Germany, 1990.
34. Hauth JC, Owen J, Davis RO. Transverse uterine incision closure: One versus two layers. Am J Obstet Gynecol 1992;167:1108-1111.
35. Hassan A, Zarewych B, Evans TN. Cesarean section: A 15 years review of changing incidence, indications and risks. Am J Obstet Gynecol 1981;140:81-90.
36. Raimer KA, O’Sullivan MJ. Cesarean section: history, incidence, and indications. Surgical Obstetrics ,ed, Plauche WC, W B Saunders Co, Philadelphia,1992;pp405-415.
37. Atkinson MW, Owen J, Wren A, Hauth JC. The effect of manual removal of the placenta on post-cesarean section endometritis. Obstet Gynecol 1996;87:99-102.
38. Nielsen TF.: Caesarean section : A Controversial feature of modern obstetric practice. Gynecol Obstet Invest. 1986;21 (2) : 57 â 63.
39. Yao XY : Sequelae in 4122 cases of cesarean section. Zhonghua Fu Chan Ke Za Zhi 1990 Jan; 25 (1) : 15 â 7, 61.
40. Hook B, Kiwi R, Amini S B, Fanaroff A, Hack M. : Neonatal morbidity after elective repeat cesarean section and trial of labour. Pediatrics. 1997;100(3 Pt 1) : 348 â 53.