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The number of deliveries by Cesarean section has been increasing steadily worldwide in recent decades. Although it is often assumed that Cesarean section improves neonatal outcomes, there is no hard scientific evidence to support this view1. The safety of Cesarean section, however, has increased owing to improvements in surgical and anesthetic techniques, increased safety of blood transfusion and routine use of antibiotics and thromboprophylaxis2, 3. Cesarean section is also associated with long-term risks such as postoperative pelvic adhesions, uterine scar rupture, and placental complications such as placenta previa and accreta4–6. The latter two complications are likely to be associated with the poor uterine scar healing following Cesarean sections.
Uterine scar dehiscence may present as an acute event in the antenatal or intrapartum period, leading to significant fetal and maternal morbidity7, 8. The frequency of uterine rupture is estimated at 0.2–3.8% and that of uterine dehiscence is between 0.6 and 3.8%9–11.
Gilliam et al. identified an increased risk of placenta previa with a history of Cesarean section5. The consequences of abnormally adherent placenta are particularly severe, and they are responsible for 41–64% of all obstetric hysterectomies; 65% of these cases have a history of previous Cesarean section7, 8. 80% of maternal deaths associated with placenta previa in the UK over the last 12 years occurred in women with a history of previous Cesarean section and abnormally adherent placenta.
In recent years the first-trimester diagnosis of early pregnancy implantation into a deficient Cesarean section scar has been described9, 10. The term ‘Cesarean scar pregnancy’ has been used to describe this condition, which often leads to serious maternal morbidity due to severe hemorrhage. There is also evidence that viable Cesarean scar pregnancies have the potential to develop into placenta previa or accreta at term9, 10. Routine surveillance of Cesarean section scars by ultrasonography during pregnancy has been proposed by some authors, in an attempt to identify ‘silent’ or asymptomatic scar dehiscence11, 12. Several studies have attempted to assess scar integrity during pregnancy, but the sonographic detection of uterine scars is easiest in the non-pregnant state13. Scar integrity has also been assessed by saline contrast sonohysterography, in order to delineate scar deficiency more accurately14. However this method of assessment is not without risks and therefore is limited in its practical application.
The purpose of this study was to describe morphological features of transverse lower-segment uterine Cesarean section scars on non-enhanced B-mode transvaginal ultrasound scans in a large group of non-pregnant women. The morphological appearances of the scars were compared to the demographic data and obstetric history in an attempt to identify factors associated with deficient Cesarean section scars.
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Non-pregnant, premenopausal women with a history of previous transverse lower-segment Cesarean section, who were referred to our early pregnancy and gynecology assessment unit for a variety of gynecological indications, were invited to join this study. A full medical history was taken in each case including a detailed obstetric and gynecological history, the number of previous Cesarean sections, the gestational age at the time of the operation and the indication for the operation. Women were included only if the Cesarean section had been performed more than 3 months prior to the assessment. Women who underwent classical Cesarean sections, open myomectomy and those who underwent a hysterectomy following a Cesarean section were excluded from the study. All the women underwent a transvaginal ultrasound scan, which was performed by gynecologists with expertise in transvaginal scanning using high-frequency transducers of 5–7.5 MHz (Aloka SSD-5000, Aloka Co., Tokyo, Japan).
On ultrasound scan, the uterus was examined in the longitudinal plane and the internal os was identified as the point of junction between the endometrial cavity and the cervical canal. The uterine flexion was determined by assessing the angle between the longitudinal axis of the uterus and the longitudinal axis of the cervix. Uterine anteflexion was diagnosed when the long axis of the uterine body was deviating anteriorly in relation to the long axis of the cervix, while posterior deviation was classified as retroflexion. An attempt was then made to ascertain the location of a Cesarean section scar within the anterior uterine wall. In cases of multiple previous Cesareans, the number of all visible scars was recorded. In all the women, the distance between the uterine Cesarean section scar and the top of the uterine cavity (a) was measured in the longitudinal plane (Figure 1). The ‘height ratio’ of the uterine Cesarean scar was defined as the ratio of this distance (a) to the whole length of the uterine cavity measured from the internal os to the top (b). A value of 1 corresponds to the scar being located at the level of the internal os, while a value < 1 indicates that the scar is above the level of the internal os. In cases of multiple Cesarean sections, the scar closest to the fundus was taken as representative for the particular case.
Figure 1. A longitudinal view of the uterus illustrating the assessment of Cesarean section scar position (S) in relation to the internal os (O). Distances from the scar to the uterine fundus (a) and from the internal os to the fundus (b) are measured as shown, and the height ratio is expressed as a/b.
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Scars were described as deficient if there was detectable myometrial thinning at the site (Figure 2). The degree of thinning was expressed as the ratio of the myometrial thickness at the depth of the scar (c) to the thickness of the adjacent normal myometrium measured in the longitudinal section (d) (‘deficiency ratio’). The loss of more than 50% of myometrial mantle at the scar level was classified as severe deficiency.
Figure 2. A longitudinal view of a uterus with a deficient Cesarean section scar. The severity of scar deficiency was assessed by measuring the myometrial thickness at the depth of the scar (c) and the thickness of the adjacent unaffected myometruium (d). The degree of deficiency is expressed as the ratio c/d.
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The study was approved by the local ethics committee and all patients gave consent to take part in it. All clinical findings were stored in a clinical database that facilitated data entry and retrieval (PIA-Fetal Database, Viewpoint Bildverabeitung GmbH, Wessling, Germany). Statistical evaluation was by univariate and multivariate analysis. Univariate analysis involved comparing different variables in the two main groups, i.e. those women with deficient and those with non-deficient scars. The continuous variables were compared using two-sample t-test or Mann–Whitney test where indicated, while the categorical variables were compared using the Pearson chi-square or Fisher's exact test as appropriate. A multiple logistic regression model was used to see the concurrent effects of all the potential prognostic factors, paying special attention to interactions. The variable Cesarean section was fitted in two ways, one according to the total number of scars visualized, the other by differentiating full-term and preterm Cesareans. Term gestations were defined as pregnancies that were completed at 37 weeks' gestation or more. In addition, logistic function was used in a discriminant analysis to provide a risk classification for these patients. Multivariate analysis involved constructing multiple logistic regression models for all variables to identify which retained statistical significance, and a value of P < 0.05 was considered to be statistically significant.
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In a period of 18 months a total of 354 women with histories of previous transverse lower-segment Cesarean sections were examined by transvaginal ultrasound. Thirty (8.5%) data sets were incomplete and these women were excluded from further analysis. The remaining 324 (91.5%) women, who were included in the data analysis, had undergone a total of 471 Cesarean sections. Two hundred and eleven (65.1%, 95% CI 61–69) women had had one Cesarean section, 84 (25.9%, 95% CI 22–30) had had two Cesarean sections, 24 (7.4%, 95% CI 5–10) had had three, and five (1.5%, 95% CI 0–2.6) had had four Cesarean sections.
There was no statistically significant difference in the mean gestational age at the time of surgery or in the type of Cesarean section (emergency or elective) between women who underwent single or multiple Cesareans (Table 1). However, women who had had three or more Cesarean sections were younger at the time of their first Cesarean compared to those who had had fewer Cesarean sections (Table 1).
Table 1. Demographic data and scar morphology in women with single and multiple Cesarean sections (CS)
|Parameter||Single CS (n = 211)||Two CS (n = 84)||Three or more CS (n = 29)||P|
|Maternal age at time of first CS (years, mean (range))||29.4 (14–44)||30.8 (20–41)||25.7 (18–31)||0.01|
|Gestational age at CS (weeks, mean (range))||38.0 (24–42)||38.6 (26–43)||38.4 (28–42)||NS|
|First CS by emergency (n (%))||154/211 (73.0)||78/168 (46.4)||34/92 (37.0)||NS|
|Women with deficient scars (n (%))||32/211 (15.2)||20/84 (23.8)||11/29 (37.9)||0.01|
|Visualized scars (n (%))|
| 0||1 (0.5)||1 (1.2)||1 (3.4)||0.0001|
| 1||210 (99.5)||43 (51.2)||19 (65.5)|| |
| 2||—||40 (47.6)||6 (20.7)|| |
| 3||—||—||3 (10.3)|| |
Cesarean section scars were visible on ultrasound scan in 321/324 (99.1%, 95% CI 98.0–100) women. However, it was not always possible to identify individual scars in women with histories of multiple Cesarean sections. The total number of visible individual scars decreased from 210/211 (99.5%, 95% CI 97.4–99.9) in women with a single previous section to 123/168 (73.2%, 95% CI 66.0–79.3) in women with two previous operations and 40/92 (43.5%, 95% CI 39.7–53.7) in those with three or more operations (P < 0.0001) (Table 1).
The majority of scars were located close to the internal os but 14/321 (4.4%, 95% CI 2.2–6.6) women had evidence of corporal scars (Table 2). A total of 63/324 (19.4%, 95% CI 15.1–23.8) women had evidence of myometrial thinning at the Cesarean section site as previously defined. In 32/324 (9.9%, 95% CI 7.1–13.4) women the defects were severe, involving ≥ 50% of the myometrium (Table 2). The distribution of myometrial thickness measurement is shown in Figure 3. On univariate analysis there were significant differences between women with deficient and non-deficient scars in the number of previous Cesarean sections and uterine flexion (Table 3). Using multivariate analysis, the history of multiple Cesarean sections, uterine retroflexion and the inability to visualize all Cesarean scars in women with previous multiple Cesarean sections were all significantly associated with deficient scars (Table 4). The odds ratios (OR) for deficient scars nearly doubled for each additional Cesarean section (OR = 1.9, 95% CI 1.3–2.9).
Figure 3. Distribution of myometrial thickness at the Cesarean section site in women with evidence of scar deficiency (n = 63).
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Table 2. Distribution of height and myometrial deficiency ratios (n = 321)
|Height ratio (a/b) (n (%))||307 (95.6)||11 (3.4)||3 (0.9)||—|
|Deficiency ratio (c/d) (n (%))||271 (84.4)||18 (5.6)||28 (8.7)||4 (1.2)|
Table 3. Univariate analysis of women with deficient and non-deficient Cesarean section (CS) scars
|Parameter||Non-deficient (n = 261)||Deficient (n = 63)||P|
|Age (years, mean (95% CI))||41 (39.5–41.6)||40 (38–43)||NS|
|Parity (median (range))||2 (1–12)||2 (1–4)||NS|
|Number of CSs (median (range))||1 (1–4)||1 (1–3)||0.01|
|Indication for CS* (n (%))|| || || |
| Elective||67 (27)||19 (33)||NS|
| Emergency||179 (73)||38 (67)|| |
|Proportion of preterm CS (n (%))|| || || |
| Term||222 (85.1)||54 (85.7)||NS|
| Preterm||39 (14.9)||9 (14.3)|| |
|Number of vaginal births in addition to CS (median (range))||0 (0–10)||0 (0–3)||NS|
|Number of visible scars (median (range))||1 (0–3)||1 (1–2)||NS|
|Height ratio of Cesarean scar above internal os (a/b) (median (range))||1 (0.25–1)||1 (0.46–1)||NS|
|Uterine position (n (%))|| || || |
| Anteflexed||226 (87)||45 (71.4)||0.005|
| Retroflexed||35 (13)||18 (28.6)|| |
Table 4. Multiple logistic regression analysis of deficient versus non-deficient Cesarean section scars
|Variable||Coeffi-cient||Odds ratio (95% CI)||P|
|Position of uterus||0.89||2.4 (1.3–4.8)||0.01|
|Number of scars visualized||− 1.15||0.31 (0.13–0.75)||0.01|
|Number of Cesarean sections||0.69||1.9 (1.3–2.9)||0.001|
|Constant||− 2.23|| || |
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Our study showed that lower-segment uterine Cesarean section scars can be identified on standard B-mode transvaginal ultrasound scan in almost all women with a history of previous Cesarean sections. In women with a history of multiple Cesarean sections it was often impossible to identify all previous scars individually, and the number of detectable individual scars was lower with increasing number of previous Cesarean sections. This may be explained by the fact that some uterine incisions are made at exactly the same site as the previous scar. In addition there was a tendency for uterine scars to become deficient in cases of multiple sections, which also interferes with the ability to visualize individual scars on the ultrasound scan.
We found that nearly 20% of women had detectable myometrial thinning at the site of a previous Cesarean section. In half of these women the defects were large, involving more than 50% of the myometrial thickness. There were only three variables that were associated with deficient scars: history of multiple Cesarean sections; uterine retroflexion; and the inability to visualize all uterine scars in cases of multiple sections.
A relationship between multiple previous Cesarean sections and scar deficiency has also been reported by Regnard et al.15. Our study has confirmed this observation, and we showed that the odds of a scar becoming deficient increase with the number of previous sections. An analogy to this observation is where repeated trauma to a wound can disrupt the normal healing process16. Furthermore, this can be extrapolated from the final stage of wound healing in the skin, whereby the highly vascular granulation tissue is replaced by avascular scar tissue17. Thus, further injury to the scar tissue, an area with poor vascular perfusion, will compromise the pathways involved in healing18.
There was also an association between scar deficiency and inability to identify all the scars in women with multiple Cesarean sections. However, this finding is more likely to be a consequence, rather than the cause, of scar deficiency. Deficient scars tend to occupy larger areas of the lower uterine segment, which hampers visualization of individual scars. As expected, the ability to see individual scars decreased with increasing number of previous Cesarean sections.
Uterine retroflexion was another variable that was associated with deficient scars. The chance of a woman with a retroflexed uterus having a deficient scar was more than twice that of a woman with an anteflexed uterus. The flexion point of the uterus is at the level of the internal os. In a retroflexed uterus the lower segment of the uterus is therefore under a degree of tension, which may compromise healing of a Cesarean section scar. This could be the result of mechanical traction to the scar or reduced vascular perfusion caused by stretching of the lower uterine segment. Impaired tissue perfusion results in reduced wound oxygen tension, which has been reported to delay wound healing by slowing the production of collagen16.
The clinical significance of these findings is uncertain. Uterine rupture in women with previous Cesarean section is a rare event that occurs in 12 per 10 000 with elective repeat sections and up to 35 per 10 000 with vaginal births after Cesarean section19. Therefore a high level of observed scar deficiency, as seen in our study, is unlikely to be helpful in identifying women at risk of scar rupture. Even with evidence of severe deficiency of more than 50% of myometrial thickness the risk of scar rupture would still be less than 5%. The results of the study may also be important for patients undergoing endometrial ablation. There have been cases of thermal injury to the bowel following microwave endometrial ablation in patients who had undergone Cesarean deliveries as a result of the microwave energy passing through the thin myometrial layer and affecting the bowel20.
Detection of severe scar deficiency may be helpful in identifying women at risk of Cesarean scar ectopic pregnancy in the future. This is also a rare complication of Cesarean sections that occurs in approximately 1 in 1800 pregnancies9. However, scar implantation is a severe complication, which is associated with significant maternal morbidity. There is some evidence from the literature that scar implantations tend to occur only in women with severe deficient scars and that the risk of scar implantation may be proportional to the size of the myometrial defect. The treatment of scar pregnancies is simple and highly effective when the diagnosis is made in the first trimester, but the risk of severe complications increases with increasing gestational age. In view of the observed association between multiple Cesarean sections and scar deficiency it may be feasible to offer all women with two or more previous sections an early scan to rule out scar implantation. In our hospital, with approximately 5000 deliveries/year and a Cesarean section rate of 22%, the percentage of women booking for antenatal care with a history of two or more previous Cesarean sections was 1.5–1.8%. If all these women attended for ultrasound screening of scar pregnancy an additional 70–90 scans/year would need to be performed in order to detect 50% of all scar implantations.
In conclusion deficient Cesarean scars are a frequent finding in a population of women who had had previous Cesarean sections. A policy of routine scar assessment by ultrasonography in order to prevent uterine rupture is unlikely to be practical or helpful. However, a small number of women with multiple previous sections may benefit from an early scan at 6–7 weeks' gestation to identify and treat scar ectopic pregnancies.