Cesarean scar pregnancy is a precursor of morbidly adherent placenta Timor-Tritsch I.E.,1 Monteagudo A.,1 Cali G.,2 Vintzileos A.,3 Viscarello R.,4 Al-Khan A.,5 Zamudio S.,5 Mayberry P.,4 Cordoba MM,1 Dar P.6 1
NYU School of Medicine, Department of Obstetrics and Gynecology, Division of Maternal Fetal Medicine, New York, NY 2 Department of Obstetrics and Gynecology, Arnas Civico Hospital, Palermo, Italy 3 Winthrop University Hospital, Department of Obstetrics and Gynecology, Division of Maternal Fetal Medicine and Surgery, Mineola, NY 4 Maternal Fetal Care PC, Stamford, CT 5 Hackensack University Medical Center, Department of Obstetrics and Gynecology, Hackensack, NJ 6 Albert Einstein College of Medicine, Department of Obstetrics and Gynecology and Women’s Health, Bronx, NY
Keywords: Cesarean scar pregnancy, morbidly adherent placenta, CSP, MAP, cesarean pregnancy Corresponding Author: Ilan E. Timor-Tritsch, MD Professor of Obstetrics and Gynecology NYU School of Medicine Department of Ob/Gyn 550 First Avenue, NBV-9N1 New York, NY 10016 Tel: 212.263.7952 Fax: 212.263.7890 [email protected]
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Abstract Goal: To provide futher sonographic, clinical and histologic evidence that cesarean scar pregnancy (CSP) is a precursor and an early form of second and third trimester morbidly adherent placenta (MAP). Materials and Methods: We identified 10 cases of CSP fulfilling published ultrasound criteria. Nine patients, had counseling and offered early termination, but decided to continue the pregnancy to achieve live born neonates. The possibility of significant pregnancy complications and, possible hysterectomy were emphasized. Patients were followed with ultrasound scans and customary pregnancy surveillance. The plan was to reach near term or term and undergo elective cesarean delivery and if necessary: hysterectomy. Charts, ultrasound images, operative reports and histo-pathological examinations of the placentas were reviewed. Results: The ultrasound diagnosis of CSP was made before 10 weeks. By the second trimester all patients exhibited sonographic signs of MAP. Nine of the 10 patients delivered live born neonates between 32 to 36 weeks. Three patients had antepartum complications. Progressive shortening of the cervix and intractable vaginal bleeding prompted termination of one pregnancy having hysterectomy at 20 weeks. All patients underwent hysterectomy. Blood loss ranged from 300 to 6000 ml. Placenta percreta was the histopathologic diagnosis in all 10 cases. Conclusion: The cases in this series provide validation to the hypothesis that CSP is a precursor of MAP, both sharing the same histopathology. Our findings provide evidence that can be used to counsel patients with proven CSP who can now make an informed
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decision between first trimester termination and continuation of the pregnancy risking premature delivery, loss of the uterus and further fertility.
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Introduction The rate of cesarean deliveries (CD), cesarean scar pregnancies (CSP) and the different degrees (accreta, increta and percreta) of morbidly adherent placenta (MAP), also known as placental attachment disorders (PAD), have increased in a parallel fashion in the last decade (1-11). Even though there was a leveling-off in the number of the CDs in the USA in 2012 (3), a similar trend has yet to materialized and be evaluated regarding the CSP and the MAP. The current literature documents that if expectant management of CSP is selected, some gestations will encounter severe maternal morbidity such as massive intra/postpartum hemorrhage, shock, intra-abdominal bleeding, massive transfusions, uterine rupture with fetal loss, and in most cases, if not all, leading to hysterectomy. (10) In addition, some gestations diagnosed as CSP in the first trimester have been reported to go on to late preterm or early term and result in live offspring; however, in all published cases hysterectomy with permanent loss of fertility, as the result of a MAP has been the endresult.(12-17) In 2012, Sinha and Mishra (16) reported on two CSP cases which had contrasting outcomes. The first had a complicated 1st trimester course requiring two D&C’s, laparoscopy as well as IM methotrexate; while the second case continued the pregnancy and at 37 weeks underwent an elective CD for placenta previa with suspected accreta. The CD was complicated by a MAP, massive postpartum hemorrhage and followed by hysterectomy. The histology of the placenta was consistent with placenta increta. Therefore, based upon their reading of the literature and the above two cases, they hypothesized that CSP and MAP are not a separate entities but “rather a continuum of the same condition”. In another recent articleBallas et al (15) reported that in 10 cases with gestational ages between 8 and
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14 weeks the sacs were located in the lower uterine segment and fulfilled the diagnostic criteria of CSP. These women went on to deliver live offspring at the expense of losing their uteri due to MAP. If CSP is managed expectantly in the 1st trimester and the pregnancy “survives” the 2nd trimester, most likely it evolves into MAP leading to an almost unavoidable peripartum hysterectomy. In 5 additional case reports described in the published literature (12,14-17) the sonographic diagnosis of CSP was made, but the pregnancy continued reaching near term and, had similar outcome to the cases described by Sinha (16) and Ballas (15). Comstock et al (18) showed that when 1st trimester scans of patients, who had 2nd and 3rd trimester MAP, were retrospectively examined, there were US findings consistent with early accreta termed by them: “scar pregnancy”. In our recently published article, based upon histopathologic evaluation of cases of CSP and early placenta accreta in the late 1st and early 2nd trimesters, our pathologists confirmed that the CSP and the MAP have identical histopathologic features indistinguishable from each other. (19) We propose that there is a continuum, or spectrum, of PAD , starting as CSP, progressing to early placenta accreta and eventually resulting in MAP classically seen in the late 2nd and 3rd trimester. While cases may have different clinical presentation, they all share the same histology.(19) It should be clear, that not all patients diagnosed with MAP have to necessarily loose their uteri. Leaving the placenta inplace after cutting the cord at itrs placental insertion was described in the literature as a possible management in patients desiring future fertility. (20) Chanddraharan et al (21) also describe theit uterus sparing procedure termed “The Triple P procedure”.
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In this paper, we present 10 patients in which 1st trimester diagnosis of CSP was well documented and established, and who, after extensive counseling elected to continue the pregnancy. We detail the diagnostic process, present their sonographic ‘history’, their clinical course, delivery and obstetric outcome. Our goal is to provide further proof to the hypothesis that CSP is a precursor of the MAP and that CSP is the initial event in the continuum of the MAP from the 1st, to the 2nd and throughout the 3rd trimester of the pregnancy.
Materials and methods The authors identified 10 patients with CSPs during two years to our 2 centers, who expressed their desire to continue their pregnancies and to deliver live offspring. These 10 patients constituted 24% of the patients presented to the 2 centers with CSP demonstrating fetal heart activity ( 13 patients out of 62, however 3 of these patients who later suffered uterine ruptures during the 2nd trimester). The US diagnosis of a CSP was established upon our previously described sonographic features (14). These were as follows: 1. Visualization of an empty uterine cavity as well as an empty endocervical canal . 2. Detection of the placenta and/or a gestational sac embedded in/on the hysterotomy scar. 3. In early gestations (8 postmenstrual weeks this shape may become rounded or even oval. 4. A thin (1-3 mm) or absent myometrial layer between the gestational sac and the bladder. 5. A closed and empty cervical canal. 6. The presence of embryonic/fetal pole and/or yolk sac with or without heart activity. 7. The presence of a prominent and at times
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rich vascular pattern at or in the area of a CD scar in the presence of a positive pregnancy test. All, but one patient, were extensively counseled about the diagnosis and were offered early termination of the pregnancy by one of the following methods: local intra-gestational and/or systemic injection of methotrexate, uterine artery embolization, aspiration of the gestational sac or a combination of the above. These patients instead chose close US based monitoring of the pregnancy in a hope to achieve a viable late preterm or early term delivery by repeat cesarean section, understanding the possibility of eventual hysterectomy, if needed. They were closely followed at their obstetricians’ offices with serial US scans at 2-4 week intervals, and in some cases with MRI, as well as the customary pregnancy surveillance. The plan in each case was to reach late preterm or early term and undergo elective CD with an option to proceed to cesarean hysterectomy. All patients agreed to the above management plan. Charts, serial US images, operative reports and histo-pathological examinations of the 10 patients were prospectively collected and retrospectively reviewed for this article. This research was approved by the institutional review Board as an exempt study (strudy number S12-3237; 31 August 20120 because it involved the collection of existing data, documents records and pathological/diagnostic specimens that are publicly available. Also the information was recorded by the investigators in such a manner that subjects could not be identified either directly or indirectly.
Results
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Table 1 details demographic, clinical data, outcomes as well as the histopathologic results of the 10 patients. The US diagnosis of CSP was made as early as 5 weeks and 4 days and in all but one case, prior to 12 weeks. The first US examination ranged from week 5 and 4 days to 9 week and 2 days. In one patient (#8) the diagnosis of CSP was made retrospectively by evaluating her scans performed at 6, 8,11 and 15 weeks, after the diagnosis of placenta accreta was made prospectively at 23 weeks. By the 2nd trimester all patients exhibited most or all of the well documented sonographic signs of MAP, namely: placenta previa, loss of the normal hypoechoic zone, interruption or alteration of the bladder line, placental lacunae, thinning of the myometrium at the uterine/bladder interface and finally an increased vascularity by 2D/3D color/power Doppler of the placenta. (22,23) The average age of the patients was 35.5 (27-44). 70% (7 of 10) patients had only 1 prior CD; and 30% (3 of 10) had two or 3 prior cesarean deliveries. The average time between the last CD and the present pregnancy was 27 months (range 12 - 141 months). Patients #1 to #5 were managed by the same provider. The rest of the women (#6 to #10) were treated by different maternal fetal medicine specialists in different institutions. Nine of the 10 cases resulted in a live born neonate. The gestational age at delivery among live born infants ranged from 32 to 36 weeks. Only 3 patients had complications during the antepartum course. Patient #5 had bleeding at 33 postmenopausal weeks and was delivered at 34 weeks; Patient # 9 had contractions at 33 postmenopausal weeks and was delivered at 34 weeks. In case #6 at 19 week’s US detected a significant collection of blood and blood
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clots in the uterine cavity with progressive shortening of the cervix. As a response to the intractable blood loss with progressive cervical shortening at 20 weeks gestation a total abdominal hysterectomy was performed after umbilical artery embolization and intracardiac KCL. At laparotomy the paper thin anterior uterine wall spontaneously ruptured and the cord was partially extruded. All patients had hysterectomy, with preoperative placement of prophylactic hypogastric artery balloons in all but 2 patients (#8 and #10). The mean blood loss was 1560ml (range 300-6000ml) despite the preventive insertion of preoperative, bilateral balloon catheters into the hypogastric arteries by interventional radiology as well as the prior knowledge of the expected diagnosis and planned surgical management. In almost all cases the reason for the bleeding was due to neovascularization and significant pelvic adhesions, the surgical separation of the uterus from the bladder; and parametrial involvement. Two patients (#7 and #9) received large amounts of blood and blood products. Only one bladder injury was reported. Placenta percreta was the histologic finding in all 10 cases. The successive and representative US images of each patient as well a picture of their removed uteri are presented in Figures 1 to 10. .Discussion This as a report of 10 patients with CSP early in pregnancy who chose to continue their pregnancies; nine of them reached preterm or near term resulting in viable offspring. All 10 patients had cesarean hysterectomies, most with a significant blood loss, and in all cases the histological report was consistent with placenta percreta. One patient had intractable blood loss, cervical shortening of the cervix leading to pregnancy loss and hysterectomy at 20 weeks. It is important to stress that similar cases with unforeseen emergencies were This article is protected by copyright. All rights reserved
described in the literature. In our in-depth review of CSP (9) we identified 46 articles with 47 cases of MAP in the early 2nd trimester, in which the diagnosis of CSP or MAP was established early in pregnancy. To distinguish these from the ‘classical’ 3rd trimester MAP, we used the term “Early Placenta Accreta” when their description matched the sonographic definition of CSP. All, but 9, of those 47 patients had previous CDs and most of the 9 patient without a proven CD had pre-pregnancy intrauterine surgical procedure. Of the 46 articles 29 were published after the year 2000 reflecting the increasing trend of CSP leading to MAP. Spontaneous uterine rupture was seen in 15 of the 47 pregnancies, most were “silent”, followed by bleeding, shock, hemoperitoneum ending in hysterectomy. Uterine artery embolization (UAE) to curb bleeding was performed in 5 patients. Thirty seven patients had laparotomies with 35 hysterectomies; one of them had an arterio-venous malformation. In 10 of the above 46 above articles, with patients diagnosed with uterine ruptures in the 1st or 2nd trimester, the clinical descriptions were identical for an early placenta accreta or for a CSP. By the descriptions, it is evident, that the rupture occurred due to and at the site of the CD scar. Obvious similarities make these cases hard to classify as typical MAP or, for that matter, typical cases of CSP. This may be a compelling reason to believe in a hypothesis of their common pathogenesis. These cases as well as similar and previously reported, mostly sporadic cases solidify the clinical fact that CSP is a precursor of MAP. Patients in this study were managed by different practitioners at different institutions and slightly different management protocols. Their common denominator was the conservative but proactive approach with close clinical and sonographic surveillance. All 10 patients sacrificed their uteri to achieve a live neonate.
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This paper provides important information useful for patient counseling. In all but one patient in this cohort the diagnosis of CSP was made in the 1st trimester. All patients were followed with serial US and all demonstrated progression from the 1st trimester CSP to the typical sonographic findings of 2nd/3rd trimester MAP. All, but one patient (#6), delivered late preterm or early term. Blood loss was significant at the time of the CD. In all cases the histology confirmed the diagnosis of MAP. The literature describes pregnancies implanted low and anteriorly, “on the scar”, termed “true scar pregnancy”, differentiating them from gestations found entirely surrounded by myometrium and “in the scar”, or in the niche of scar, with a thin or no myometrium between the gestation and the bladder. (23, 24) In our cases #1 to 3 and #5 the sac was clearly “on the scar”, while the rest demonstrated that the implantations were “in the niche of the scar”. The question whether a previous CD scar has to have a defect (niche) for invasive placental penetration to take place may remain unanswered based upon these series. Klinman’s theory (25), that the trophoblast has a special propensity to adhere to denuded scar tissue may provide some explanation to the above question. One fact seems to gain increasing weight in the above discussion: the post CD uterine niche appears to be a recognized risk factor for a CSP. (26) Regardless of the exact site of the placental implantation (“on” the scar or “in” the niche), this implantation will remain unchanged invading the available thin myometrium or the scar tissue penetrating to the level of the uterine serosa or the bladder. In a continuing pregnancy placental location and its insertion are not likely to change during the entire pregnancy being firmly “anchored” in/on the scar. Moreover, the argument of “in” or “on” the scar/niche may lose its importance at around 7-9 weeks as at this time the
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gestational/chorionic sac exceeds the size of the “niche” and “rolls”, at first, towards the lower part of the previously empty uterine cavity and later during the 2nd trimester progressively into the available space filling the entire uterine cavity. The presently available literature (27) as well as our observation suggests that during the 2nd and 3rd trimesters, the evolving histologic picture staring with a CSP is that of an unmistakable MAP. Our opinion is, that until more data is available describing the natural history of either kind of placental implantation, the discussion of “on” or “in” the scar has to be a postponed, since management or treatment of this faulty placental implantation is dictated by the evolving clinical picture and not so much by its initial location.
A short time interval between the last CD and the subsequent conception may increase the risk for MAP or for that matter a CSP (28), however our small number of cases and lack of a control group does not allow us to comment on this issue. Based upon this case series and the recent literature on the progression of CSP to MAP, we firmly believe that every patient who had a previous CD diagnosed with an early pregnancy should have a 1st trimester transvaginal US scan to ascertain location of the gestational sac and placental insertion. The issue of routine scan in the above situation was explored and published, (28, 29) however needs further clinical proof.
Summary and conclusions.
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In summary, all the cases diagnosed in this series as CSP early in pregnancy, ended up with histologically proven placenta accrete at delivery. It is therefore reasonable to establish the practice that all women with a prior CDs who present with subsequent early, 1st trimester pregnancy should have a transvaginal scan to rule-out a CSP. If an anteriorly attached, low lying early gestation (with or without heart activity) is identified by ultrasound in a woman with previous CD: it should be considered a CSP until proven otherwise by ruling out a cervical pregnancy and an abortion in progress. If a CSP is diagnosed, the patient can be given the option to electively terminate or continue the pregnancy; If choosing the latter, they should be advised that their chances to achieve the desired delivery (usually premature) of a live offspring should be weighed against the significantly high risks of premature delivery, hysterectomy and permanent loss of fertility, but even more so, to uterine rupture massive blood loss, shock, even death, before the patient even reaches the emergency room. A final thought. Our personal impression is that there is very low and limited awareness in the community of obstetrical and gynecological practitioners as to the early and correct identification of CSP. Our case #8 illustrates this fact. It was only at the 2nd trimester scan and following an episode of vaginal bleeding that the placental pathology was identified. Reviewing the 1st trimester US images the diagnosis of CSP was made. It is not known if this patient would have considered an intervention at the time of the 1st trimester. However it is clear, that by not establishing the correct early diagnosis of CSP and its possible consequences, the patient was denied her management options.
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In conclusion, we believe that the cases in this series provide further validation to the hypothesis that CSP is one of, and the most common precursor of MAP sharing the same histopathology. LEGENDS Figure 1. Case #1. Gray scale images of the CSP at 6 weeks and 3 days and at 7 weeks are shown with the arrows pointing to the implantation of the placenta. At 23 weeks as well as two color Doppler images at 30 and 34 weeks are consistent with a MAP. The specimen of the removed uterus performed at 35 weeks with the area of the placental insertion (arrow) is shown. Figure 2. Case #2. Ultrasound image of the CSP at 9 weeks and 2 days (gray scale) with 2 arrows pointing to the implantation of the placenta. At 23 and 34 weeks (color Doppler) the US images are consistent with a MAP. After the cesarean delivery the removed uterus at 36 weeks is shown with the area of the placental implantation (arrow). Figure 3. Case #3. Ultrasound image at 7 weeks and 4 days (gray and color Doppler) of the CSP with the arrows pointing to the implantation of the placenta. At 22 weeks (color Doppler) is consistent with a MAP. The removed uterus at 36 weels, the time of the cesarean delivery showes the site of the placenta (arrow). Figure 4. Case #4. Gray scale image of the CSP at 8 weeks and 3 color Doppler images at 12 weeks and 5 days with the arrows pointing to the implantation of the placenta. The diagnosis of MAP was established at 23 weeks and 5 days and confirmed at 33 weeks. The uterus removed at 36 weeks. The placental implantation site is marked (arrow).
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Figure 5. Case #5. The gray scale image of the s CSP at 8 weeks and 4 days with the arrows pointing to the implantation of the placenta. At 16 weeks, at 26 weeks and 4 days the images of the developing MAP. A color Dopler picture at 33 weeks alongside with the removed uterus at 34 weeks are shown. The placental invasion site is marked by an arrow. (Bl: bladder) Figure 6. Case #6. Three color Doppler images of the CSP at 9 weeks and 2 days (with the arrows pointing to the implantation of the placenta), at 15 weeks and 2 days as well as the image of the MAP at 17 weeks and 2 days. The patient’s clinical presentation (intractible bleeding and cervical shortening) at 19 weeks lead to hysterectomy at 20 weeks. The removed uterus is shown. The area of placental invasion rendered the anteriot lower uterine segment paper thin. During the surgery, while handling the uterus, it ruptured extruding the cord and part of the placenta (arrow). Figure 7 Case #7. Color Doppler imaging depicting features of placental invasion of the uterine wall below the bladder of a CSP at 6 weeks (the arrow pointing to the implantation of the placenta) and and 18 weeks The sonographic evidence of the MAP at 21, 24 and 28 weeks respectively follow . The uterus shown was removed after the cesarean delivery at 37 weeks . The arrow points to the area of the penetrating placental site. Figure 8 Case #8. Serial transvaginal images of the scar pregnancy (at 8 weeks and 2 days and 10 weeks and 4 days with the arrows pointing to the implantation of the placenta.) as well as the Color Doppler sonograms at 13, 14 weks and 4 days, 15 weeks and 6 days are shown followed by the ultrasound image of the MAP and 23 weeks 3 days. The uterus was removed at 37 weeks after the cesarean delivery. The site of placental invasion is marked by an arrow.
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Figure 9. Case #9. Gray scale images at 8 weeks and 3 days, 11 weeks and 5 days (the arrows pointing to the implantation of the placenta) and at 15 weeks 1 day attest to a low, anterior placental implantation below the bladder consistent with a cesarean scar pregnancy. At 23 weeks and 5 days the diagnosis of MAP was made. At 32 weeks uncontrollable uterine contractions lead to cesarean delivery and hysterectomy. The placental invasion site is marked by an arrow. Figure 10 Case #10. The serial gray scale and color Doppler images at 7 weeks and 5 days ( the arrows pointing to the implantation of the placenta.), 13 weeks, 17 weeks, 28 weeks and 4 days, 29 weeks and 2 days and at 31 weeks and 3 days demonstrate the anterior and low implantation of the placenta, the lacunar nature of it and its vascularity. The uterus was removed at the time of the CD at 34 weeks and 1 day. The placental invasion is marked by an arrow.
Table 1 #
#
Age
Time
Dx @
Antepartum
Delivery
Use of
Repeat C/D
Weight
Bleeding
of
interval
(week)
Complication
(week)
preventive
resulting in
(g.)
(ml)
P
between
placement
live
CS
last and
of
offspring
index
hypogastric
pregnancy
artery
(months)
balloons
Hysterectomy
Histology
1
1
41
59
6w3d
None
35w
+
+
2580
800
+
Percreta
2
1
27
38
9w2d
None
35w
+
+
2450
1100
+
Percreta
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3
1
37
21
5w4d
None
36w
+
+
2850
900
+
Percreta
4
1
37
26
6w4d
None
34w
+
+
2600
1300
+
Percreta
5
2
44
52
6w4d
Bleeding
34w1d
+
+
2650
1300
+
Percreta
At 19 w
At 20w
+
Θ
266
300
+
Percreta
severe
UAE
at 33 w 6
1
32
25
6w1d
bleeding, short cx
TAH
Intracardiac KCl
7
2
35
141
6w5d
Lost for
32w
+
+
2120
6000
+
Percreta
f/u until 18w 8
1
37
14
7w2d
None
34w2d
-
+
3300
300
+
Percreta
9
1
40
48
6w5d
Contractions
32w
+
+
1920
3000
+
Percreta
*
at 32 w
8w5d
None
34w1d
-
+
2120
600
+
Percreta
10
1
27
12
w: week; d: day; PCS: previous cesarean section; Dx: diagnosis; RC/D: repeat cesarean delivery; TAH:
total abdominal hysterectomy; UAE: uterine artery embolization; Cx: cervix; f/u follow up
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22. Cali G, Giambanco L, Puccio G, Forlani F. Morbidly adherent placenta: evaluation of ultrasound diagnostic criteria and differentiation of placenta accreta from percreta. Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology 2013;41:406-12. 23. Comstock CH, Bronsteen RA. The antenatal diagnosis of placenta accreta. BJOG : an international journal of obstetrics and gynaecology 2014;121:171-81; discussion 81-2. 24. Sadeghi H, Rutherford T, Rackow BW, Campbell KH, Duzyj CM, Guess MK, Kodaman PH, Norwitz ER. Cesarean scar ectopic pregnancy: case series and review of the literature. American journal of perinatology 2010;27:111-20.
25. Kliman HJ, Feinberg RF, Haimowitz JE. Human trophoblast-endometrial interactions in an in vitro suspension culture system. Placenta. 1990;11(4):349-67. 26. Bij de Vaate AJ, van der Voet LF, Naji O, Witmer M, Veersema S, Brölmann HA, Bourne T, Huirne JA. Prevalence, potential risk factors for development and symptoms related to the presence of uterine niches following Cesarean section: systematic review. Ultrasound Obstet Gynecol. 2014 Apr;43(4):372-82. doi: 10.1002/uog.13199. 27. Jurkovic D. Cesarean scar pregnancy and placenta accreta. Ultrasound Obstet Gynecol. 2014 Apr;43(4):361-2. doi: 10.1002/uog.13346. No abstract available. PMID:24692219 [PubMed - in process] 28. Wax JR, Seiler A, Horowitz S, Ingardia CJ. Interpregnancy interval as a risk factor for placenta accreta. Connecticut medicine 2000;64:659-61. 29. Stirnemann JJ, Chalouhi GE, Forner S, Saidji Y, Salomon LJ, Bernard JP, Ville Y. First-trimester uterine scar assessment by transvaginal ultrasound. American journal of obstetrics and gynecology 2011;205:551 e1-6. 30. Stirnemann JJ, Mousty E, Chalouhi G, Salomon LJ, Bernard JP, Ville Y. Screening for placenta accreta at 11-14 weeks of gestation. American journal of obstetrics and gynecology 2011;205:547 e1-6.
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NYU School of Medicine, Department of Obstetrics and Gynecology, Division of Maternal Fetal Medicine, New York, NY 2 Department of Obstetrics and Gynecology, Arnas Civico Hospital, Palermo, Italy 3 Winthrop University Hospital, Department of Obstetrics and Gynecology, Division of Maternal Fetal Medicine and Surgery, Mineola, NY 4 Maternal Fetal Care PC, Stamford, CT 5 Hackensack University Medical Center, Department of Obstetrics and Gynecology, Hackensack, NJ 6 Albert Einstein College of Medicine, Department of Obstetrics and Gynecology and Women’s Health, Bronx, NY
Keywords: Cesarean scar pregnancy, morbidly adherent placenta, CSP, MAP, cesarean pregnancy Corresponding Author: Ilan E. Timor-Tritsch, MD Professor of Obstetrics and Gynecology NYU School of Medicine Department of Ob/Gyn 550 First Avenue, NBV-9N1 New York, NY 10016 Tel: 212.263.7952 Fax: 212.263.7890 [email protected]
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1002/uog.13426 This article is protected by copyright. All rights reserved
Abstract Goal: To provide futher sonographic, clinical and histologic evidence that cesarean scar pregnancy (CSP) is a precursor and an early form of second and third trimester morbidly adherent placenta (MAP). Materials and Methods: We identified 10 cases of CSP fulfilling published ultrasound criteria. Nine patients, had counseling and offered early termination, but decided to continue the pregnancy to achieve live born neonates. The possibility of significant pregnancy complications and, possible hysterectomy were emphasized. Patients were followed with ultrasound scans and customary pregnancy surveillance. The plan was to reach near term or term and undergo elective cesarean delivery and if necessary: hysterectomy. Charts, ultrasound images, operative reports and histo-pathological examinations of the placentas were reviewed. Results: The ultrasound diagnosis of CSP was made before 10 weeks. By the second trimester all patients exhibited sonographic signs of MAP. Nine of the 10 patients delivered live born neonates between 32 to 36 weeks. Three patients had antepartum complications. Progressive shortening of the cervix and intractable vaginal bleeding prompted termination of one pregnancy having hysterectomy at 20 weeks. All patients underwent hysterectomy. Blood loss ranged from 300 to 6000 ml. Placenta percreta was the histopathologic diagnosis in all 10 cases. Conclusion: The cases in this series provide validation to the hypothesis that CSP is a precursor of MAP, both sharing the same histopathology. Our findings provide evidence that can be used to counsel patients with proven CSP who can now make an informed
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decision between first trimester termination and continuation of the pregnancy risking premature delivery, loss of the uterus and further fertility.
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Introduction The rate of cesarean deliveries (CD), cesarean scar pregnancies (CSP) and the different degrees (accreta, increta and percreta) of morbidly adherent placenta (MAP), also known as placental attachment disorders (PAD), have increased in a parallel fashion in the last decade (1-11). Even though there was a leveling-off in the number of the CDs in the USA in 2012 (3), a similar trend has yet to materialized and be evaluated regarding the CSP and the MAP. The current literature documents that if expectant management of CSP is selected, some gestations will encounter severe maternal morbidity such as massive intra/postpartum hemorrhage, shock, intra-abdominal bleeding, massive transfusions, uterine rupture with fetal loss, and in most cases, if not all, leading to hysterectomy. (10) In addition, some gestations diagnosed as CSP in the first trimester have been reported to go on to late preterm or early term and result in live offspring; however, in all published cases hysterectomy with permanent loss of fertility, as the result of a MAP has been the endresult.(12-17) In 2012, Sinha and Mishra (16) reported on two CSP cases which had contrasting outcomes. The first had a complicated 1st trimester course requiring two D&C’s, laparoscopy as well as IM methotrexate; while the second case continued the pregnancy and at 37 weeks underwent an elective CD for placenta previa with suspected accreta. The CD was complicated by a MAP, massive postpartum hemorrhage and followed by hysterectomy. The histology of the placenta was consistent with placenta increta. Therefore, based upon their reading of the literature and the above two cases, they hypothesized that CSP and MAP are not a separate entities but “rather a continuum of the same condition”. In another recent articleBallas et al (15) reported that in 10 cases with gestational ages between 8 and
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14 weeks the sacs were located in the lower uterine segment and fulfilled the diagnostic criteria of CSP. These women went on to deliver live offspring at the expense of losing their uteri due to MAP. If CSP is managed expectantly in the 1st trimester and the pregnancy “survives” the 2nd trimester, most likely it evolves into MAP leading to an almost unavoidable peripartum hysterectomy. In 5 additional case reports described in the published literature (12,14-17) the sonographic diagnosis of CSP was made, but the pregnancy continued reaching near term and, had similar outcome to the cases described by Sinha (16) and Ballas (15). Comstock et al (18) showed that when 1st trimester scans of patients, who had 2nd and 3rd trimester MAP, were retrospectively examined, there were US findings consistent with early accreta termed by them: “scar pregnancy”. In our recently published article, based upon histopathologic evaluation of cases of CSP and early placenta accreta in the late 1st and early 2nd trimesters, our pathologists confirmed that the CSP and the MAP have identical histopathologic features indistinguishable from each other. (19) We propose that there is a continuum, or spectrum, of PAD , starting as CSP, progressing to early placenta accreta and eventually resulting in MAP classically seen in the late 2nd and 3rd trimester. While cases may have different clinical presentation, they all share the same histology.(19) It should be clear, that not all patients diagnosed with MAP have to necessarily loose their uteri. Leaving the placenta inplace after cutting the cord at itrs placental insertion was described in the literature as a possible management in patients desiring future fertility. (20) Chanddraharan et al (21) also describe theit uterus sparing procedure termed “The Triple P procedure”.
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In this paper, we present 10 patients in which 1st trimester diagnosis of CSP was well documented and established, and who, after extensive counseling elected to continue the pregnancy. We detail the diagnostic process, present their sonographic ‘history’, their clinical course, delivery and obstetric outcome. Our goal is to provide further proof to the hypothesis that CSP is a precursor of the MAP and that CSP is the initial event in the continuum of the MAP from the 1st, to the 2nd and throughout the 3rd trimester of the pregnancy.
Materials and methods The authors identified 10 patients with CSPs during two years to our 2 centers, who expressed their desire to continue their pregnancies and to deliver live offspring. These 10 patients constituted 24% of the patients presented to the 2 centers with CSP demonstrating fetal heart activity ( 13 patients out of 62, however 3 of these patients who later suffered uterine ruptures during the 2nd trimester). The US diagnosis of a CSP was established upon our previously described sonographic features (14). These were as follows: 1. Visualization of an empty uterine cavity as well as an empty endocervical canal . 2. Detection of the placenta and/or a gestational sac embedded in/on the hysterotomy scar. 3. In early gestations (8 postmenstrual weeks this shape may become rounded or even oval. 4. A thin (1-3 mm) or absent myometrial layer between the gestational sac and the bladder. 5. A closed and empty cervical canal. 6. The presence of embryonic/fetal pole and/or yolk sac with or without heart activity. 7. The presence of a prominent and at times
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rich vascular pattern at or in the area of a CD scar in the presence of a positive pregnancy test. All, but one patient, were extensively counseled about the diagnosis and were offered early termination of the pregnancy by one of the following methods: local intra-gestational and/or systemic injection of methotrexate, uterine artery embolization, aspiration of the gestational sac or a combination of the above. These patients instead chose close US based monitoring of the pregnancy in a hope to achieve a viable late preterm or early term delivery by repeat cesarean section, understanding the possibility of eventual hysterectomy, if needed. They were closely followed at their obstetricians’ offices with serial US scans at 2-4 week intervals, and in some cases with MRI, as well as the customary pregnancy surveillance. The plan in each case was to reach late preterm or early term and undergo elective CD with an option to proceed to cesarean hysterectomy. All patients agreed to the above management plan. Charts, serial US images, operative reports and histo-pathological examinations of the 10 patients were prospectively collected and retrospectively reviewed for this article. This research was approved by the institutional review Board as an exempt study (strudy number S12-3237; 31 August 20120 because it involved the collection of existing data, documents records and pathological/diagnostic specimens that are publicly available. Also the information was recorded by the investigators in such a manner that subjects could not be identified either directly or indirectly.
Results
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Table 1 details demographic, clinical data, outcomes as well as the histopathologic results of the 10 patients. The US diagnosis of CSP was made as early as 5 weeks and 4 days and in all but one case, prior to 12 weeks. The first US examination ranged from week 5 and 4 days to 9 week and 2 days. In one patient (#8) the diagnosis of CSP was made retrospectively by evaluating her scans performed at 6, 8,11 and 15 weeks, after the diagnosis of placenta accreta was made prospectively at 23 weeks. By the 2nd trimester all patients exhibited most or all of the well documented sonographic signs of MAP, namely: placenta previa, loss of the normal hypoechoic zone, interruption or alteration of the bladder line, placental lacunae, thinning of the myometrium at the uterine/bladder interface and finally an increased vascularity by 2D/3D color/power Doppler of the placenta. (22,23) The average age of the patients was 35.5 (27-44). 70% (7 of 10) patients had only 1 prior CD; and 30% (3 of 10) had two or 3 prior cesarean deliveries. The average time between the last CD and the present pregnancy was 27 months (range 12 - 141 months). Patients #1 to #5 were managed by the same provider. The rest of the women (#6 to #10) were treated by different maternal fetal medicine specialists in different institutions. Nine of the 10 cases resulted in a live born neonate. The gestational age at delivery among live born infants ranged from 32 to 36 weeks. Only 3 patients had complications during the antepartum course. Patient #5 had bleeding at 33 postmenopausal weeks and was delivered at 34 weeks; Patient # 9 had contractions at 33 postmenopausal weeks and was delivered at 34 weeks. In case #6 at 19 week’s US detected a significant collection of blood and blood
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clots in the uterine cavity with progressive shortening of the cervix. As a response to the intractable blood loss with progressive cervical shortening at 20 weeks gestation a total abdominal hysterectomy was performed after umbilical artery embolization and intracardiac KCL. At laparotomy the paper thin anterior uterine wall spontaneously ruptured and the cord was partially extruded. All patients had hysterectomy, with preoperative placement of prophylactic hypogastric artery balloons in all but 2 patients (#8 and #10). The mean blood loss was 1560ml (range 300-6000ml) despite the preventive insertion of preoperative, bilateral balloon catheters into the hypogastric arteries by interventional radiology as well as the prior knowledge of the expected diagnosis and planned surgical management. In almost all cases the reason for the bleeding was due to neovascularization and significant pelvic adhesions, the surgical separation of the uterus from the bladder; and parametrial involvement. Two patients (#7 and #9) received large amounts of blood and blood products. Only one bladder injury was reported. Placenta percreta was the histologic finding in all 10 cases. The successive and representative US images of each patient as well a picture of their removed uteri are presented in Figures 1 to 10. .Discussion This as a report of 10 patients with CSP early in pregnancy who chose to continue their pregnancies; nine of them reached preterm or near term resulting in viable offspring. All 10 patients had cesarean hysterectomies, most with a significant blood loss, and in all cases the histological report was consistent with placenta percreta. One patient had intractable blood loss, cervical shortening of the cervix leading to pregnancy loss and hysterectomy at 20 weeks. It is important to stress that similar cases with unforeseen emergencies were This article is protected by copyright. All rights reserved
described in the literature. In our in-depth review of CSP (9) we identified 46 articles with 47 cases of MAP in the early 2nd trimester, in which the diagnosis of CSP or MAP was established early in pregnancy. To distinguish these from the ‘classical’ 3rd trimester MAP, we used the term “Early Placenta Accreta” when their description matched the sonographic definition of CSP. All, but 9, of those 47 patients had previous CDs and most of the 9 patient without a proven CD had pre-pregnancy intrauterine surgical procedure. Of the 46 articles 29 were published after the year 2000 reflecting the increasing trend of CSP leading to MAP. Spontaneous uterine rupture was seen in 15 of the 47 pregnancies, most were “silent”, followed by bleeding, shock, hemoperitoneum ending in hysterectomy. Uterine artery embolization (UAE) to curb bleeding was performed in 5 patients. Thirty seven patients had laparotomies with 35 hysterectomies; one of them had an arterio-venous malformation. In 10 of the above 46 above articles, with patients diagnosed with uterine ruptures in the 1st or 2nd trimester, the clinical descriptions were identical for an early placenta accreta or for a CSP. By the descriptions, it is evident, that the rupture occurred due to and at the site of the CD scar. Obvious similarities make these cases hard to classify as typical MAP or, for that matter, typical cases of CSP. This may be a compelling reason to believe in a hypothesis of their common pathogenesis. These cases as well as similar and previously reported, mostly sporadic cases solidify the clinical fact that CSP is a precursor of MAP. Patients in this study were managed by different practitioners at different institutions and slightly different management protocols. Their common denominator was the conservative but proactive approach with close clinical and sonographic surveillance. All 10 patients sacrificed their uteri to achieve a live neonate.
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This paper provides important information useful for patient counseling. In all but one patient in this cohort the diagnosis of CSP was made in the 1st trimester. All patients were followed with serial US and all demonstrated progression from the 1st trimester CSP to the typical sonographic findings of 2nd/3rd trimester MAP. All, but one patient (#6), delivered late preterm or early term. Blood loss was significant at the time of the CD. In all cases the histology confirmed the diagnosis of MAP. The literature describes pregnancies implanted low and anteriorly, “on the scar”, termed “true scar pregnancy”, differentiating them from gestations found entirely surrounded by myometrium and “in the scar”, or in the niche of scar, with a thin or no myometrium between the gestation and the bladder. (23, 24) In our cases #1 to 3 and #5 the sac was clearly “on the scar”, while the rest demonstrated that the implantations were “in the niche of the scar”. The question whether a previous CD scar has to have a defect (niche) for invasive placental penetration to take place may remain unanswered based upon these series. Klinman’s theory (25), that the trophoblast has a special propensity to adhere to denuded scar tissue may provide some explanation to the above question. One fact seems to gain increasing weight in the above discussion: the post CD uterine niche appears to be a recognized risk factor for a CSP. (26) Regardless of the exact site of the placental implantation (“on” the scar or “in” the niche), this implantation will remain unchanged invading the available thin myometrium or the scar tissue penetrating to the level of the uterine serosa or the bladder. In a continuing pregnancy placental location and its insertion are not likely to change during the entire pregnancy being firmly “anchored” in/on the scar. Moreover, the argument of “in” or “on” the scar/niche may lose its importance at around 7-9 weeks as at this time the
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gestational/chorionic sac exceeds the size of the “niche” and “rolls”, at first, towards the lower part of the previously empty uterine cavity and later during the 2nd trimester progressively into the available space filling the entire uterine cavity. The presently available literature (27) as well as our observation suggests that during the 2nd and 3rd trimesters, the evolving histologic picture staring with a CSP is that of an unmistakable MAP. Our opinion is, that until more data is available describing the natural history of either kind of placental implantation, the discussion of “on” or “in” the scar has to be a postponed, since management or treatment of this faulty placental implantation is dictated by the evolving clinical picture and not so much by its initial location.
A short time interval between the last CD and the subsequent conception may increase the risk for MAP or for that matter a CSP (28), however our small number of cases and lack of a control group does not allow us to comment on this issue. Based upon this case series and the recent literature on the progression of CSP to MAP, we firmly believe that every patient who had a previous CD diagnosed with an early pregnancy should have a 1st trimester transvaginal US scan to ascertain location of the gestational sac and placental insertion. The issue of routine scan in the above situation was explored and published, (28, 29) however needs further clinical proof.
Summary and conclusions.
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In summary, all the cases diagnosed in this series as CSP early in pregnancy, ended up with histologically proven placenta accrete at delivery. It is therefore reasonable to establish the practice that all women with a prior CDs who present with subsequent early, 1st trimester pregnancy should have a transvaginal scan to rule-out a CSP. If an anteriorly attached, low lying early gestation (with or without heart activity) is identified by ultrasound in a woman with previous CD: it should be considered a CSP until proven otherwise by ruling out a cervical pregnancy and an abortion in progress. If a CSP is diagnosed, the patient can be given the option to electively terminate or continue the pregnancy; If choosing the latter, they should be advised that their chances to achieve the desired delivery (usually premature) of a live offspring should be weighed against the significantly high risks of premature delivery, hysterectomy and permanent loss of fertility, but even more so, to uterine rupture massive blood loss, shock, even death, before the patient even reaches the emergency room. A final thought. Our personal impression is that there is very low and limited awareness in the community of obstetrical and gynecological practitioners as to the early and correct identification of CSP. Our case #8 illustrates this fact. It was only at the 2nd trimester scan and following an episode of vaginal bleeding that the placental pathology was identified. Reviewing the 1st trimester US images the diagnosis of CSP was made. It is not known if this patient would have considered an intervention at the time of the 1st trimester. However it is clear, that by not establishing the correct early diagnosis of CSP and its possible consequences, the patient was denied her management options.
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In conclusion, we believe that the cases in this series provide further validation to the hypothesis that CSP is one of, and the most common precursor of MAP sharing the same histopathology. LEGENDS Figure 1. Case #1. Gray scale images of the CSP at 6 weeks and 3 days and at 7 weeks are shown with the arrows pointing to the implantation of the placenta. At 23 weeks as well as two color Doppler images at 30 and 34 weeks are consistent with a MAP. The specimen of the removed uterus performed at 35 weeks with the area of the placental insertion (arrow) is shown. Figure 2. Case #2. Ultrasound image of the CSP at 9 weeks and 2 days (gray scale) with 2 arrows pointing to the implantation of the placenta. At 23 and 34 weeks (color Doppler) the US images are consistent with a MAP. After the cesarean delivery the removed uterus at 36 weeks is shown with the area of the placental implantation (arrow). Figure 3. Case #3. Ultrasound image at 7 weeks and 4 days (gray and color Doppler) of the CSP with the arrows pointing to the implantation of the placenta. At 22 weeks (color Doppler) is consistent with a MAP. The removed uterus at 36 weels, the time of the cesarean delivery showes the site of the placenta (arrow). Figure 4. Case #4. Gray scale image of the CSP at 8 weeks and 3 color Doppler images at 12 weeks and 5 days with the arrows pointing to the implantation of the placenta. The diagnosis of MAP was established at 23 weeks and 5 days and confirmed at 33 weeks. The uterus removed at 36 weeks. The placental implantation site is marked (arrow).
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Figure 5. Case #5. The gray scale image of the s CSP at 8 weeks and 4 days with the arrows pointing to the implantation of the placenta. At 16 weeks, at 26 weeks and 4 days the images of the developing MAP. A color Dopler picture at 33 weeks alongside with the removed uterus at 34 weeks are shown. The placental invasion site is marked by an arrow. (Bl: bladder) Figure 6. Case #6. Three color Doppler images of the CSP at 9 weeks and 2 days (with the arrows pointing to the implantation of the placenta), at 15 weeks and 2 days as well as the image of the MAP at 17 weeks and 2 days. The patient’s clinical presentation (intractible bleeding and cervical shortening) at 19 weeks lead to hysterectomy at 20 weeks. The removed uterus is shown. The area of placental invasion rendered the anteriot lower uterine segment paper thin. During the surgery, while handling the uterus, it ruptured extruding the cord and part of the placenta (arrow). Figure 7 Case #7. Color Doppler imaging depicting features of placental invasion of the uterine wall below the bladder of a CSP at 6 weeks (the arrow pointing to the implantation of the placenta) and and 18 weeks The sonographic evidence of the MAP at 21, 24 and 28 weeks respectively follow . The uterus shown was removed after the cesarean delivery at 37 weeks . The arrow points to the area of the penetrating placental site. Figure 8 Case #8. Serial transvaginal images of the scar pregnancy (at 8 weeks and 2 days and 10 weeks and 4 days with the arrows pointing to the implantation of the placenta.) as well as the Color Doppler sonograms at 13, 14 weks and 4 days, 15 weeks and 6 days are shown followed by the ultrasound image of the MAP and 23 weeks 3 days. The uterus was removed at 37 weeks after the cesarean delivery. The site of placental invasion is marked by an arrow.
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Figure 9. Case #9. Gray scale images at 8 weeks and 3 days, 11 weeks and 5 days (the arrows pointing to the implantation of the placenta) and at 15 weeks 1 day attest to a low, anterior placental implantation below the bladder consistent with a cesarean scar pregnancy. At 23 weeks and 5 days the diagnosis of MAP was made. At 32 weeks uncontrollable uterine contractions lead to cesarean delivery and hysterectomy. The placental invasion site is marked by an arrow. Figure 10 Case #10. The serial gray scale and color Doppler images at 7 weeks and 5 days ( the arrows pointing to the implantation of the placenta.), 13 weeks, 17 weeks, 28 weeks and 4 days, 29 weeks and 2 days and at 31 weeks and 3 days demonstrate the anterior and low implantation of the placenta, the lacunar nature of it and its vascularity. The uterus was removed at the time of the CD at 34 weeks and 1 day. The placental invasion is marked by an arrow.
Table 1 #
#
Age
Time
Dx @
Antepartum
Delivery
Use of
Repeat C/D
Weight
Bleeding
of
interval
(week)
Complication
(week)
preventive
resulting in
(g.)
(ml)
P
between
placement
live
CS
last and
of
offspring
index
hypogastric
pregnancy
artery
(months)
balloons
Hysterectomy
Histology
1
1
41
59
6w3d
None
35w
+
+
2580
800
+
Percreta
2
1
27
38
9w2d
None
35w
+
+
2450
1100
+
Percreta
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3
1
37
21
5w4d
None
36w
+
+
2850
900
+
Percreta
4
1
37
26
6w4d
None
34w
+
+
2600
1300
+
Percreta
5
2
44
52
6w4d
Bleeding
34w1d
+
+
2650
1300
+
Percreta
At 19 w
At 20w
+
Θ
266
300
+
Percreta
severe
UAE
at 33 w 6
1
32
25
6w1d
bleeding, short cx
TAH
Intracardiac KCl
7
2
35
141
6w5d
Lost for
32w
+
+
2120
6000
+
Percreta
f/u until 18w 8
1
37
14
7w2d
None
34w2d
-
+
3300
300
+
Percreta
9
1
40
48
6w5d
Contractions
32w
+
+
1920
3000
+
Percreta
*
at 32 w
8w5d
None
34w1d
-
+
2120
600
+
Percreta
10
1
27
12
w: week; d: day; PCS: previous cesarean section; Dx: diagnosis; RC/D: repeat cesarean delivery; TAH:
total abdominal hysterectomy; UAE: uterine artery embolization; Cx: cervix; f/u follow up
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