REVIEW ARTICLE Risk factors for abnormally invasive placenta: a systematic review and meta-analysis Antonia Iacovelli a , Marco Liberati a , Asma Khalil b , Ilan Timor-Trisch c , Martina Leombroni a , Danilo Buca a , Michela Milani a , Maria Elena Flacco d , Lamberto Manzoli e , Francesco Fanfani a , Giuseppe Cal ı f , Alessandra Familiari g , Giovanni Scambia g and Francesco D’Antonio h,i a Department of Obstetrics and Gynaecology, University of Chieti, Chieti, Italy; b Fetal medicine Unit, Division of Developmental Sciences, St. George’s University of London, London, United Kingdom; c Department of Obstetrics and Gynaecology, Division of Maternal-Fetal Medicine, New York, NY, USA; d Local Health Unit of Pescara, Pescara, Italy; e Department of Medical Sciences, University of Ferrara, Ferrara, Italy; f Department of Obstetrics and Gynaecology, Arnas Civico Hospital, Palermo, Italy; g Catholic University of the Sacred Heart, Rome, Italy; h Women s Health and Perinatology Research Group, Department of Clinical Medicine, Faculty of Health Sciences, UiT-The Arctic University of Norway, Tromsø, Norway; i Department of Obstetrics and Gynaecology, University Hospital of Northern Norway, Tromsø, Norway ABSTRACT Purpose of the article. To explore the strength of association between different maternal and pregnancy characteristics and the occurrence of abnormally invasive placenta (AIP). Materials and methods: Pubmed, Embase, CINAHL databases were searched. The risk factors for AIP explored were: obesity, age >35 years, smoking before or during pregnancy, placenta previa, prior cesarean section (CS), placenta previa and prior CS, prior uterine surgery, abortion and uter- ine curettage, in vitro fertilization (IVF) pregnancy and interval between a previous CS, and a sub- sequent pregnancy. Random-effect head-to-head meta-analyses were used to analyze the data. Results: Forty-six were included in the systematic review. Maternal obesity (Odd ratio, OR: 1.4, 95% CI 1.0–1.8), advanced maternal age (OR: 3.1, 95% CI 1.4–7.0) and parity (OR: 2.5, 95% CI 1.7–3.6), but not smoking were associated with a higher risk of AIP. The presence of placenta previa in women with at least a prior CS was associated with a higher risk of AIP compared to controls, with an OR of 12.0, 95% CI 1.6–88.0. Furthermore, the risk of AIP increased with the number of prior CS (OR of 2.6, 95% CI 1.6–4.4 and 5.4, 95% CI 1.7–17.4 for two and three prior CS respectively). Finally, IVF pregnancies were associated with a high risk of AIP, with an OR of 2.8 (95% CI 1.2–6.8). Conclusion: A prior CS and placenta previa are among the strongest risk factors for the occur- rence of AIP. ARTICLE HISTORY Received 22 May 2018 Accepted 22 June 2018 KEYWORDS Abnormally invasive placenta; cesarean section; placenta; risk factors; systematic review and meta-analysis Introduction Abnormally invasive placenta (AIP) encompasses a het- erogeneous group of anomalies characterized by dif- ferent degrees of invasion of chorionic villi through the myometrium and uterine serosa [1]. Women affected by AIP require a tailored surgical management which is commonly accomplished by fundal hysterotomy, followed by delivery of the fetus and subsequent elective hysterectomy, although recent evidences suggest that an appropriate hemo- static control can be achieved by conservative techni- ques aiming at preserving the uterus [2,3]. Such surgical approaches require an accurate pre- natal identification of women affected by AIP, which has been shown to reduce the burden of surgical complications associated with these anomalies, such as massive hemorrhage, damage to adjacent organs, and admission to intensive care unit by allowing a pre-planned management of these conditions [4,5]. Prenatal diagnosis of AIP is usually accomplished by ultrasound, whereas fetal magnetic resonance imaging (MRI) is commonly used to confirm the diagnosis and to delineate the topography of placental invasion. Overall, prenatal imaging has been shown to reliably identify these disorders and to predict their sever- ity [6–9]. Recent studies suggested that prenatal diagnosis of AIP may improve when combining imaging signs with CONTACT Francesco D’Antonio [email protected]Department of Clinical Medicine, Faculty of Health Sciences, UiT - The Arctic University of Norway Hansine Hansens, veg 18, Tromsø, Norway Supplemental data for this article can be accessed here. ß 2018 Informa UK Limited, trading as Taylor & Francis Group THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 2020, VOL. 33, NO. 3, 471–481 https://doi.org/10.1080/14767058.2018.1493453
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REVIEW ARTICLE
Risk factors for abnormally invasive placenta: a systematic review andmeta-analysis
Antonia Iacovellia, Marco Liberatia, Asma Khalilb, Ilan Timor-Trischc, Martina Leombronia, Danilo Bucaa ,Michela Milania, Maria Elena Flaccod, Lamberto Manzolie, Francesco Fanfania, Giuseppe Cal�ıf,Alessandra Familiarig , Giovanni Scambiag and Francesco D’Antonioh,i
aDepartment of Obstetrics and Gynaecology, University of Chieti, Chieti, Italy; bFetal medicine Unit, Division of DevelopmentalSciences, St. George’s University of London, London, United Kingdom; cDepartment of Obstetrics and Gynaecology, Division ofMaternal-Fetal Medicine, New York, NY, USA; dLocal Health Unit of Pescara, Pescara, Italy; eDepartment of Medical Sciences,University of Ferrara, Ferrara, Italy; fDepartment of Obstetrics and Gynaecology, Arnas Civico Hospital, Palermo, Italy; gCatholicUniversity of the Sacred Heart, Rome, Italy; hWomen�s Health and Perinatology Research Group, Department of Clinical Medicine,Faculty of Health Sciences, UiT-The Arctic University of Norway, Tromsø, Norway; iDepartment of Obstetrics and Gynaecology,University Hospital of Northern Norway, Tromsø, Norway
ABSTRACTPurpose of the article. To explore the strength of association between different maternal andpregnancy characteristics and the occurrence of abnormally invasive placenta (AIP).Materials and methods: Pubmed, Embase, CINAHL databases were searched. The risk factors forAIP explored were: obesity, age >35 years, smoking before or during pregnancy, placenta previa,prior cesarean section (CS), placenta previa and prior CS, prior uterine surgery, abortion and uter-ine curettage, in vitro fertilization (IVF) pregnancy and interval between a previous CS, and a sub-sequent pregnancy. Random-effect head-to-head meta-analyses were used to analyze the data.Results: Forty-six were included in the systematic review. Maternal obesity (Odd ratio, OR: 1.4,95% CI 1.0–1.8), advanced maternal age (OR: 3.1, 95% CI 1.4–7.0) and parity (OR: 2.5, 95% CI1.7–3.6), but not smoking were associated with a higher risk of AIP. The presence of placentaprevia in women with at least a prior CS was associated with a higher risk of AIP compared tocontrols, with an OR of 12.0, 95% CI 1.6–88.0. Furthermore, the risk of AIP increased with thenumber of prior CS (OR of 2.6, 95% CI 1.6–4.4 and 5.4, 95% CI 1.7–17.4 for two and three priorCS respectively). Finally, IVF pregnancies were associated with a high risk of AIP, with an OR of2.8 (95% CI 1.2–6.8).Conclusion: A prior CS and placenta previa are among the strongest risk factors for the occur-rence of AIP.
ARTICLE HISTORYReceived 22 May 2018Accepted 22 June 2018
Abnormally invasive placenta (AIP) encompasses a het-erogeneous group of anomalies characterized by dif-ferent degrees of invasion of chorionic villi throughthe myometrium and uterine serosa [1].
Women affected by AIP require a tailored surgicalmanagement which is commonly accomplished byfundal hysterotomy, followed by delivery of the fetusand subsequent elective hysterectomy, althoughrecent evidences suggest that an appropriate hemo-static control can be achieved by conservative techni-ques aiming at preserving the uterus [2,3].
Such surgical approaches require an accurate pre-natal identification of women affected by AIP, which
has been shown to reduce the burden of surgicalcomplications associated with these anomalies, suchas massive hemorrhage, damage to adjacent organs,and admission to intensive care unit by allowing apre-planned management of these conditions [4,5].
Prenatal diagnosis of AIP is usually accomplished byultrasound, whereas fetal magnetic resonance imaging(MRI) is commonly used to confirm the diagnosis andto delineate the topography of placental invasion.Overall, prenatal imaging has been shown to reliablyidentify these disorders and to predict their sever-ity [6–9].
Recent studies suggested that prenatal diagnosis ofAIP may improve when combining imaging signs with
CONTACT Francesco D’Antonio [email protected] Department of Clinical Medicine, Faculty of Health Sciences, UiT - The Arctic Universityof Norway Hansine Hansens, veg 18, Tromsø, Norway
Supplemental data for this article can be accessed here.
� 2018 Informa UK Limited, trading as Taylor & Francis Group
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE2020, VOL. 33, NO. 3, 471–481https://doi.org/10.1080/14767058.2018.1493453
maternal or pregnancy characteristics, such as parity,age or number of prior cesarean section (CS) [10].
The aim of this systematic review was to explorethe strength of association between different maternaland pregnancy characteristics and the occurrenceof AIP.
Materials and methods
Data sources
This review was performed according to an a prioridesigned protocol and recommended for systematicreviews and meta-analysis [11–13]. Medline, Embase,and CINAHL were searched electronically on 23February 2017 and utilizing combinations of the rele-vant medical subject heading (MeSH) terms, keywords, and word variants for “abnormal invasiveplacenta,” “morbidly adherent placenta,” and“outcome” (Supplementary Table 1). The search andselection criteria were restricted to English language.Reference lists of relevant articles and reviews werehand searched for additional reports. Prisma guide-lines were followed [14]. This study was registeredwith the Prospero database (registration number:CRD42018083510).
Main outcomes and measures
We aim to ascertain the strength of associationbetween several maternal and pregnancy risk factorsand the occurrence of AIP. The risk factors for AIPexplored were:
� Maternal obesity� Maternal age >35 years� Smoking before or during pregnancy� Placenta previa� Prior CS� Placenta previa and prior CS� Prior uterine surgery, including either CS
or myomectomy� Prior abortion� Prior uterine curettage for abortion� In vitro fertilization (IVF) pregnancy� Interval between a previous CS and a subse-
quent pregnancy� Prior manual extraction of the placenta
For the assessment of the association between aprior CS and the occurrence of AIP, we aimed to
stratify the analysis according to the number (one,two, and three previous CS) and type (elective versusemergency) CS.
Eligibility criteria, study selection, anddata collection
Only studies reporting the prevalence of a given riskfactor in women affected compared to those notaffected by AIP were considered eligible for the inclu-sion. Studies not reporting a control group and thosewithout a clear confirmation of AIP were excluded.Studies published before 2000 were excluded, as weconsidered that improvements in the diagnosis anddefinition of AIP make these less relevant. We plannedto perform a sensitivity analysis including only casesaffected by placenta percreta.
Prospective and retrospective case-control studies,case reports, and case series were analyzed. Opinions,cases series with less than four cases of AIP, and casereports were also excluded in order to avoid publica-tion bias.
Two reviewers (AI, ML) independently extracteddata. Inconsistencies were discussed among thereviewers and consensus reached. For those articles inwhich targeted information was not reported but themethodology was such that the information mighthave been recorded initially, the authors were con-tacted requesting the data. Histopathological findingsand/or surgical notes were used as a gold standard.
Quality assessment of the included studies was per-formed using the Newcastle-Ottawa scale (NOS) forcase-control studies; according to NOS, each study isjudged on three broad perspectives: the selection ofthe study groups; the comparability of the groups;and the ascertainment outcome of interest [15].Assessment of the selection of a study includes theevaluation of the representativeness of the exposedcohort, selection of the nonexposed cohort, ascertain-ment of exposure, and the demonstration that out-come of interest was not present at start of study.Assessment of the comparability of the study includesthe evaluation of the comparability of cohorts basedon the design or analysis. Finally, the ascertainment ofthe outcome of interest includes the evaluation of thetype of the assessment of the outcome of interest,length, and adequacy of follow-up. According to NOS,a study can be awarded a maximum of one star foreach numbered item within the Selection andOutcome categories. A maximum of two stars can begiven for Comparability [15].
Table 1. General characteristics of the included studies.Author Year Country Study design Period analyzed Inclusion criteria Pregnancies (n) AIP (n) Controls (n)
Millischer [20] 2017 France Retrospective 2009–2012 Placenta previaþ priorCS and US suspicionof AIP
Upson [41] 2013 Ireland Retrospective 2005–2010 All deliveries 403,602 357 403,245Fitzpatrick [42] 2012 UK Retrospective 2010–2011 All women with AIP
versus all womenwith no AIP
390 134 256
Hannon [43] 2012 UK Retrospective NS Cases of post-partumhysterectomy
16 12 4
Chantraine [44] 2012 Argentina–Germ-any-Belgium
Retrospective NS Women with pla-centa increta
22 13 9
Lim [45] 2011 USA Retrospective 2009–2010 Clinical and/or US riskfactors for AIP
13 9 4
Sadashivaiah[46]
2011 UK Retrospective 2004–2008 Women undergoinginterventional radi-ology for AIP
13 4 9
Esh-Broder [47] 2011 Israel Retrospective 2004–2009 All deliveries 25,235 42 25,193Derman [48] 2011 USA Retrospective NS Women with ultra-
sound suspicionof AIP
17 4 13
(continued)
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 473
Statistical analysis
We evaluated the association between 17 potentialpredictors and the presence of abnormally invasiveplacenta (AIP) among pregnant women. Four out of22 potential predictors were continuous (maternalage, parity, number of previous cesarean sections –CS, and BMI); 18 were categorical (maternal age >35years, obesity, current smoking, multiparity, diagnosisof placenta previa, diagnosis of placenta previa withprevious CS, previous CS, previous elective CS, previ-ous emergency CS, previous uterine surgery, previousabortion, previous curettage, in vitro fertilization – IVF,short interval [<23 months] between previous CS andsubsequent pregnancy, manual extraction of the pla-centa, uterine incision, endometrial ablation).
We first used random-effect head-to-head meta-analyses, expressing the results as summary odds ratio(OR) or mean difference (and relative 95% confidenceinterval – CI) for categorical or continuous predictors,respectively. When single study results were reportedas median and ranges, we used the method describedby Hozo et al. to obtain the corresponding means andstandard deviations (SD), and when interquartileranges (IQR) rather than ranges were reported, they
were divided by 1.35 to obtain the equivalent SD[16,17]. In all meta-analyses, the statistical heterogen-eity was quantified using the I2 metric.
Some of the comparisons involving the categoricalpredictors showed a marked imbalance in the successrate between the groups being compared. Besidesthe computational issues, in such cases the oddsratios may be of limited interest and sensitivity andspecificity could be more informative. We thus calcu-lated the overall sensitivity and specificity (andrelated 95% CIs) for each comparison using the effi-cient-score method (corrected for continuity)described by Newcombe [18]. Finally, we performedrandom-effect meta-analyses of proportions to esti-mate the pooled rates of AIP by each categoricalpotential predictor.
We were able to assess publication bias graphically,through funnel plots, and formally, through Egger’sregression asymmetry test, only in 10 out of 22 meta-analyses, because the formal tests for funnel plotasymmetry cannot be used when the total number ofpublications included for each outcome is <10 (thepower is too low to distinguish chance from realasymmetry) [17,19]. RevMan 5.3 (The Cochrane
Table 1. Continued.Author Year Country Study design Period analyzed Inclusion criteria Pregnancies (n) AIP (n) Controls (n)
Warshak [59] 2006 USA Retrospective 2000–2005 US diagnosis or suspi-cion of AIP
28 12 16
Wu [60] 2005 USA Retrospective 1982–2002 AIP andmatched controls
450 111 339
Usta [61] 2005 Lebanon Retrospective 1983–2003 Placenta previa 347 22 325Gielchinsk [62] 2004 Israel Retrospective 1990–2000 AIP and
matched controls620 310 310
Chou [63] 2000 Taiwan Retrospective 1994–1998 Women with persistentplacenta previa
80 14 66
Twickler [64] 2000 USA Retrospective NS Women with placentaprevia and prior CS
20 9 11
474 A. IACOVELLI ET AL.
Collaboration, 2014) and Stata, version 13.1 (StataCorp, College Station, TX, 2013) were used to analyzethe data.
Results
General characteristics
A total of 969 articles were identified. After screeningthe abstracts, 182 full text articles were assessed withrespect to their eligibility for inclusion (SupplementalTable 2) and 46 studies were included in the system-atic review (Table 1, Figure 1) [10,20–64]. The studiesby Rac, Bowman, and Wu [10,34,60], those byWeininger and Esh-Broder [37,47], and those by Wong[53,57] were carried out in the same time periods andinstitutions; however, because they looked at differentpotential predictors of AIP, were kept in the systematicreview (Table 1). These studies included 1,085,693women (2219 AIP and 1,083,474 controls).
Quality assessment based on NOS guidelines isshown in Table 2. Most of the studies were of highquality, and there was a low risk of bias and low con-cern regarding the applicability of the studies. Thesmall number of cases in some of the included
studies, different definitions of the risk factors ana-lyzed, dissimilarity of the populations, and lack ofstratification according to the severity of AIP representtheir major weaknesses.
Synthesis of the results
Five studies (554,106 pregnancies) explored the associ-ation between maternal obesity and the occurrence ofAIP, reported a higher risk of such disorders in obeseversus nonobese women with an OR of 1.4 (95% CI1.0–1.8) (Table 3). Likewise, advanced maternal age(OR: 3.1, 95% CI 1.4–7.0) and parity (OR: 2.5, 95% CI1.7–3.6), but not smoking were associated with ahigher risk of AIP (Table 3).
Twenty-six (1.057.222 pregnancies) and 33 (656,168pregnancies) studies respectively, reported thestrength of association between placenta previa andCS and AIP (Table 3). Overall, the presence of placentaprevia was associated with a higher risk of AIP com-pared to controls, with and OR of 11.0 (5% CI4.7–25.8) and 4.7 (95% CI 3.0–7.2) (Table 3). Moreimportantly, the risk of AIP increased with the numberof prior CS (OR of 2.6, 95% CI 1.6–4.4 and 5.4, 95% CI
Records identified through database searching
(n = 951)
Scre
enin
g In
clu
ded
E
ligib
ility
Id
enti
fica
tion
Additional records identified through other sources
(n = 18)
Records after duplicates removed (n = 969)
Records screened (n = 969)
Records excluded (n =787)
Full-text articles assessed for eligibility
(n = 182)
Full-text articles excluded, with reasons
(n = 136)
Studies included in qualitative synthesis
(n = 46)
Studies included in quantitative synthesis
(meta-analysis) (n = 46)
Figure 1. Systematic review flowchart.
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 475
1.7–17.4 for two and three prior CS respectively)(Table 3). When stratifying the analysis according tothe type of AIP, there was no difference in the preva-lence of such disorders in women undergoing electiveversus emergency CS. Finally, there was no associationbetween a short interval between the prior CS and asubsequent pregnancy and the occurrence of AIP,although the two studies included in this analysis dif-fered as regard as the definition of such interval(Table 3).
The presence of placenta previa in women with atleast a prior CS (12 studies, 429.007 pregnancies) wasassociated with a higher risk of AIP compared to con-trols, with an OR of 12.0, 95% CI 1.6–88.0 (Table 3).
Thirty-four studies explored the associationbetween a prior uterine surgery, defined as CS, myo-mectomy or any other procedure involving an hyster-otomy, and the occurrence of AIP, reporting a higherrisk of these disorders in women with a prior uterinesurgery (OR: 4.4, 95% CI 3.0–6.6) (Table 3).
A prior abortion was not associated with a higherrisk of AIP, irrespective of the fact that uterine curet-tage was performed. Finally, IVF pregnancies wereassociated with a high risk of AIP, with an OR of 2.8(95% CI 1.2–6.8).
Pooled proportions for the different risk factorsexplored in the present systematic review in pregnan-cies affected compared to those not affected by AIPare reported in Table 4.
When considering only cases with a histopatho-logical diagnosis of AIP, either maternal age >35 years(OR: 3.9, 95% CI 2.6–5.9, I2: 0%), multiparity (OR: 3.5,95% CI 2.4–5.3, I2: 7.8%), placenta previa (OR: 14.5,95% CI 5.4–39.3, I2: 63.5%), a prior CS (OR: 6.8, 95% CI2.6–17.6, I2: 74.8%), prior uterine surgery (OR: 7.4, 95%CI 2.9–18.4, I2: 77.2%), placenta previa and prior CS(OR: 10.6, 95% CI 2.2–52.6, I2: 63.9%), IVF pregnancy(OR: 11.6, 95% CI 6.2–21.5, I2: 0%) were associatedwith the occurrence of AIP, while prior uterine curet-tage for abortion (OR: 2.5, 95% CI 0.9–6.6, I2: 51.9%),smoking (OR: 0.92, 95% CI 0.2–4.2, I2: 32.9%) and man-ual extraction of the placenta (OR: 0.8, 95% CI0.03–17.3, I2: 0%) did not show any degree of associ-ation with such anomalies.
Discussion
Main findings
The findings from this systematic review showed thatadvanced maternal age, obesity, parity, prior CS, pla-centa previa, and IVF are associated with a significanthigh risk of AIP. A prior CS and placenta previa areamong the strongest risk factors for the occurrence ofAIP, with such risk increasing with the number of priorCS or when placenta previa and CS coexist.
Strengths and limitations
The small number of cases in some of the includedstudies, their retrospective nonrandomized design, dif-ferent definitions of the risk factors analyzed amongthe included studies and dissimilarity of the popula-tions (due to various inclusion criteria) represent themajor limitations of this systematic review. Assessmentof the potential publication bias was also problematicbecause of the nature of the outcome evaluated
Table 2. Quality assessment of the included studies accordingto Newcastle-Ottawa scale (NOS) a study can be awarded amaximum of one star for each numbered item within theSelection and Outcome categories.Author Year Selection Comparability Outcome
(outcome rates, with the left-side limited to a value ofzero), which limits the reliability of funnel plots, andbecause of the scarce number of individual studies,which strongly limits the reliability of formal tests. Notall the included studies were case-control seriesreporting matched populations and it might beentirely possible that the presence and degree ofassociation between some of the risk factors exploredand AIP might have been affected by other severalmaternal or pregnancy characteristics which were notbalanced between cases affected and not affected byAIP. Furthermore, we could not completely ascertainthe possible association between some of theexplored potential predictors, such as the type of CS,uterine incision and interval between CS and followingpregnancy, and AIP in view of the very small numberof included studies and the different cut-offs adoptedin the included studies [65].
Despite these limitations, the present review repre-sents the most comprehensive published estimate ofthe investigated outcomes in twin pregnanciesaffected by discordant growth.
Implications for clinical practice
Accurate prediction of AIP is fundamental in order toimprove the surgical outcome of these anomalies [5].Recent studies suggested that predictive models inte-grating maternal characteristics and imaging signs canimprove the diagnostic accuracy of prenatal imagingin detecting AIP [10,66].
In the present systematic review, the presence ofboth placenta previa and a prior CS was not unsurpris-ingly associated with the highest risk of AIP.Furthermore, the risk of AIP increased with increasingthe number of prior CS. These findings suggest thatevery woman presenting with placenta previa and atleast one prior CS should be considered to be poten-tially affected by AIP and referred to centers with highexpertise in diagnosis and management in order torule out these anomalies.
Fetal MRI should be considered because it may adduseful information on the depth and topography ofplacental invasion which may modify surgical manage-ment. Serial follow-up scans should be also arrangedbecause signs of AIP can be evident only later on ingestation. Despite this, it should be stressed thatabout 10% of women affected by the most severetypes of AIP remained undiagnosed until birth, thushighlighting the need for developing more accuratepredictive models for detecting these anomalies.
In the present review, we found a significant associ-ation between IVF pregnancies and AIP. Althoughcommonly reported, such association is difficult toexplain. It might be entirely possible that the reportedassociation between AIP and IVF might have beenaffected by the presence of other risk factors such asadvanced maternal age or BMI. Alternatively, it mightbe hypothesized that IVF per se increase the risk ofAIP. Although controlled ovarian stimulation allows toretrieve a considerable number of oocytes thusincreasing the success rate of IVF cycles, it has alsobeen shown to alter endometrial receptivity and
Table 4. Proportion meta-analysis: pooled rates of abnormally invasive placenta (AIP) in womenwith (A) and without (B) each categorical potential predictor.
structure by inducing abnormal levels of estradiol[67–69], which affect placental implantation.
Prenatal diagnosis of AIP is commonly performedduring the second and third trimester of pregnancy,while there is no robust data on first trimester diagno-sis, with most of the studies including only casesaffected by these anomalies. Despite this, it has still tobe ascertained when to scan women at risk of AIP.One of the most relevant issues when trying to diag-nose AIP is which subset of women should be referredfor an early detailed assessment in order to rule outAIP. The major risk factors for AIP are placenta previaand previous caesarean section. However, AIP canoccur even in women with no classical risk factors forthese conditions. In a recent large cohort study, Bailitet al. reported that 18% of women with AIP were nul-liparous and that 37% had no prior CS, thus challeng-ing the theory that AIP can occur almost exclusively inmultiparous women [65].
Despite this, it is authors’ collective opinion thatevery woman with at least one prior CS should bescanned early in pregnancy (between 5 and 9 weeksof gestation) in order to assess the gestational sacposition, relationship with prior CS and anterior uter-ine wall and to stratify the risk of AIP [70–72].
Further large studies are need in order to build reli-able predictive models for AIP tailored upon maternalcharacteristics, ultrasound, and MRI signs observed inorder to improve the diagnostic accuracy of prenatalimaging in detecting AIP.
[1] Oyelese Y, Smulian JC. Placenta previa, placentaaccreta, and vasa previa. Obstet Gynecol. 2006;107(4):927–941.
[2] Chandraharan E, Rao S, Belli AM, et al. The Triple-Pprocedure as a conservative surgical alternative toperipartum hysterectomy for placenta percreta. Int JGynecol Obstet. 2012;117(2):191–194.
[3] Palacios Jaraquemada JM, Pesaresi M, Nassif JC, et al.Anterior placenta percreta: surgical approach, hemo-stasis and uterine repair. Acta Obstet Gynecol Scand.2004;83(8):738–744.
[4] Eller AG, Porter TF, Soisson P, et al. Optimal manage-ment strategies for placenta accreta. BJOG. 2009;116(5):648–654.
[5] Tikkanen M, Paavonen J, Loukovaara M, et al.Antenatal diagnosis of placenta accreta leads toreduced blood loss. Acta Obstet Gynecol Scand.2011;90(10):1140–1146.
[6] D’Antonio F, Iacovella C, Bhide A. Prenatal identifica-tion of invasive placentation using ultrasound: sys-tematic review and meta-analysis. Ultrasound ObstetGynecol. 2013;42(5):509–517.
[8] Pagani G, Cal�ı G, Acharya G, et al. Diagnostic accuracyof ultrasound in detecting the severity of abnormallyinvasive placentation: a systematic review and meta-analysis. Acta Obstet Gynecol Scand. 2018;97(1):25–37.
[9] Familiari A, Liberati M, Lim P, et al. Diagnostic accur-acy of magnetic resonance imaging in detecting theseverity of abnormal invasive placenta: a systematicreview and meta-analysis. Acta Obstet Gynecol Scand.2018;97(5):507–520.
[10] Rac MW, Dashe JS, Wells CE, et al. Ultrasound predic-tors of placental invasion: the placenta accreta Index.Am J Obstet Gynecol. 2015;212(3):343.e1–343.e7.
[11] Henderson LK, Craig JC, Willis NS, et al. How to writea Cochrane systematic review. Nephrology (Carlton).2010;15(6):617–624.
[12] NHS Centre for Reviews and Dissemination. Systematicreviews: CRD’s guidance for undertaking reviews inhealth care. York (UK). University of York; 2009.
[13] Leeflang MM, Deeks JJ, Gatsonis C, et al. Systematicreviews of diagnostic test accuracy. Ann Intern Med.2008;149(12):889–897.
[14] Prisma statement; [cited 2017 Mar 10]. Available fromhttp://www.prisma-statement.org
[15] Newcastle-Ottawa Scale for assessing the quality ofnonrandomised studies in meta-analyses; [cited 2017Jun 1]. Available from http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
[16] Hozo SP, Djulbegovic B, Hozo I. Estimating the meanand variance from the median, range, and the size ofa sample. BMC Med Res Methodol. 2005;5:13.
[17] Higgins JPT, Green S. Cochrane handbook for system-atic reviews of interventions: the CochraneCollaboration; 2011 [cited 2017 June]. Available fromwww.cochrane-handbook.org
[18] Newcombe RG. Two-sided confidence intervals forthe single proportion: comparison of seven methods.Stat Med. 1998;17(8):857–872.
[19] Egger M, Davey Smith G, Schneider M, et al. Bias inmeta-analysis detected by a simple, graphical test.BMJ. 1997;315(7109):629–634.
[20] Millischer AE, Salomon LJ, Porcher R, et al. Magneticresonance imaging for abnormally invasive placenta:the added value of intravenous gadolinium injection.BJOG. 2017;124(1):88–95.
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 479
[21] Pilloni E, Alemanno MG, Gaglioti P, et al. Accuracy ofultrasound in antenatal diagnosis of placental attach-ment disorders. Ultrasound Obstet Gynecol. 2016;47(3):302–307.
[22] Thiravit S, Lapatikarn S, Muangsomboon K, et al. MRIof placenta percreta: differentiation from other enti-ties of placental adhesive disorder. Radiol Med.2017;122(1):61–68.
[23] Collins SL, Stevenson GN, Al-Khan A, et al. Three-dimensional power Doppler ultrasonography for diag-nosing abnormally invasive placenta and quantifyingthe risk. Obstet Gynecol. 2015;126(3):645–653.
[24] Lyell DJ, Faucett AM, Baer RJ, et al. Maternal serummarkers, characteristics and morbidly adherent pla-centa in women with previa. J Perinatol. 2015;35(8):570–574.
[25] Miller ES, Linn RL, Ernst LM. Does the presence of pla-cental basal plate myometrial fibres increase the riskof subsequent morbidly adherent placenta: a case-control study. BJOG. 2016;123(13):2140–2145.
[26] Parra-Herran C, Djordjevic B. Histopathology of pla-centa creta: chorionic villi intrusion into myometrialvascular spaces and extravillous trophoblast prolifer-ation are frequent and specific findings with implica-tions for diagnosis and pathogenesis. Int J GynecolPathol. 2016;35(6):497–508.
[27] Thurn L, Lindqvist PG, Jakobsson M, et al. Abnormallyinvasive placenta – prevalence, risk factors and ante-natal suspicion: results from a large population-basedpregnancy cohort study in the Nordic countries.BJOG. 2016;123(8):1348–1355.
[28] Alchalabi H, Lataifeh I, Obeidat B, et al. Morbidlyadherent placenta previa in current practice: predic-tion and maternal morbidity in a series of 23 womenwho underwent hysterectomy. J Matern FetalNeonatal Med. 2014;27(17):1734–1737.
[29] Bour L, Plac�e V, Bendavid S, et al. Suspected invasiveplacenta: evaluation with magnetic resonance imag-ing. Eur Radiol. 2014;24(12):3150–3160.
[30] Zhou J, Li J, Yan P, et al. Maternal plasma levels ofcell-free b-HCG mRNA as a prenatal diagnostic indica-tor of placenta accrete. Placenta. 2014;35(9):691–695.
[31] Noda Y, Kanematsu M, Goshima S, et al. Prenatal MRimaging diagnosis of placental invasion. AbdomImaging. 2015;40(5):1273–1278.
[32] Asıcıoglu O, Sahbaz A, G€ung€ord€uk K, et al. Maternaland perinatal outcomes in women with placentapraevia and accreta in teaching hospitals in WesternTurkey. J Obstet Gynaecol. 2014;34(6):462–466.
[33] Laban M, Ibrahim EA, Elsafty MS, et al. Placentaaccreta is associated with decreased decidual naturalkiller (dNK) cells population: a comparative pilotstudy. Eur J Obstet Gynecol Reprod Biol. 2014;181:284–288.
[34] Bowman ZS, Eller AG, Kennedy AM, et al. Accuracy ofultrasound for the prediction of placenta accreta. AmJ Obstet Gynecol. 2014;211(2):177.e1–177.e7.
[35] Cal�ı G, Giambanco L, Puccio G, et al. Morbidly adher-ent placenta: evaluation of ultrasound diagnostic cri-teria and differentiation of placenta accreta frompercreta. Ultrasound Obstet Gynecol. 2013;41(4):406–412.
[36] Ueno Y, Kitajima K, Kawakami F, et al. Novel MRI find-ing for diagnosis of invasive placenta praevia: evalu-ation of findings for 65 patients using clinical andhistopathological correlations. Eur Radiol. 2014;24(4):881–888.
[37] Weiniger CF, Einav S, Deutsch L, et al. Outcomes ofprospectively-collected consecutive cases of ante-natal-suspected placenta accreta. Int J Obstet Anesth.2013;22(4):273–279.
[38] Eshkoli T, Weintraub AY, Sergienko R, et al. Placentaaccreta: risk factors, perinatal outcomes, and conse-quences for subsequent births. Am J Obstet Gynecol.2013;208(3):219.e1–219.e7.
[39] Kamara M, Henderson JJ, Doherty DA, et al. The riskof placenta accreta following primary elective caesar-ean delivery: a case-control study. BJOG. 2013;120(7):879–886.
[40] Klar M, Laub M, Schulte-Moenting J, et al. Clinical riskfactors for complete and partial placental retention –a case-control study. J Perinat Med. 2013;41(5):529–534.
[41] Upson K, Silver RM, Greene R, et al. Placenta accretaand maternal morbidity in the Republic of Ireland,2005-2010. J Matern Fetal Neonatal Med.2014;27(1):24–29.
[42] Fitzpatrick KE, Sellers S, Spark P, et al. Incidence andrisk factors for placenta accreta/increta/percreta inthe UK: a national case-control study. PLoS One.2012;7(12):e52893.
[43] Hannon T, Innes BA, Lash GE, et al. Effects of localdecidua on trophoblast invasion and spiral arteryremodeling in focal placenta creta – an immunohisto-chemical study. Placenta. 2012;33(12):998–1004.
[44] Chantraine F, Blacher S, Berndt S, et al. Abnormal vas-cular architecture at the placental-maternal interfacein placenta increta. Am J Obstet Gynecol.2012;207(3):188.e1–188.e9.
[45] Lim PS, Greenberg M, Edelson MI, et al. Utility ofultrasound and MRI in prenatal diagnosis of placentaaccreta: a pilot study. Am J Roentgenol.2011;197(6):1506–1513.
[46] Sadashivaiah J, Wilson R, Thein A, et al. Role ofprophylactic uterine artery balloon catheters in themanagement of women with suspected placentaaccreta. Int J Obstet Anesth. 2011;20(4):282–287.
[47] Esh-Broder E, Ariel I, Abas-Bashir N, et al. Placentaaccreta is associated with IVF pregnancies: a retro-spective chart review. BJOG. 2011;118(9):1084–1089.
[48] Derman AY, Nikac V, Haberman S, et al. MRI of pla-centa accreta: a new imaging perspective. Am JRoentgenol. 2011;197(6):1514–1521.
[49] El Behery MM, Rasha L E, El Alfy Y. Cell-free placentalmRNA in maternal plasma to predict placental inva-sion in patients with placenta accreta. Int J GynecolObstet. 2010;109(1):30–33.
[50] Hasegawa J, Matsuoka R, Ichizuka K, et al.Predisposing factors for massive hemorrhage duringcesarean section in patients with placenta previa.Ultrasound Obstet Gynecol. 2009;34(1):80–84.
[51] Morita S, Ueno E, Fujimura M, et al. Feasibility of dif-fusion-weighted MRI for defining placental invasion. JMagn Reson Imaging. 2009;30(3):666–671.
480 A. IACOVELLI ET AL.
[52] Dwyer BK, Belogolovkin V, Tran L, et al. Prenatal diag-nosis of placenta accreta: sonography or magneticresonance imaging? J Ultrasound Med. 2008;27(9):1275–1281.
[53] Wong HS, Cheung YK, Zuccollo J, et al. Evaluation ofsonographic diagnostic criteria for placenta accreta.J Clin Ultrasound. 2008;36(9):551–559.
[54] Tantbirojn P, Crum CP, Parast MM. Pathophysiologyof placenta creta: the role of decidua and extravilloustrophoblast. Placenta. 2008;29(7):639–645.
[55] Mok M, Heidemann B, Dundas K, et al. Interventionalradiology in women with suspected placenta accretaundergoing caesarean section. Int J Obstet Anesth.2008;17(3):255–261.
[56] Japaraj RP, Mimin TS, Mukudan K. Antenatal diagnosisof placenta previa accreta in patients with previouscesarean scar. J Obstet Gynaecol Res. 2007;33(4):431–437.
[57] Wong HS, Cheung YK, Strand L, et al. Specific sono-graphic features of placenta accreta: tissue interfacedisruption on gray-scale imaging and evidence of ves-sels crossing interface-disruption sites on Dopplerimaging. Ultrasound Obstet Gynecol. 2007; 29(2):239–240.
[58] Bencaiova G, Burkhardt T, Beinder E. Abnormal pla-cental invasion experience at 1 center. J Reprod Med.2007;52(8):709–714.
[59] Warshak CR, Eskander R, Hull AD, et al. Accuracy ofultrasonography and magnetic resonance imaging inthe diagnosis of placenta accreta. Obstet Gynecol.2006;108(3 Pt 1):573–581.
[60] Wu S, Kocherginsky M, Hibbard JU. Abnormal placen-tation: twenty-year analysis. Am J Obstet Gynecol.2005;192(5):1458–1461.
[61] Usta IM, Hobeika EM, Musa AA, et al. Placenta previa-accreta: risk factors and complications. Am J ObstetGynecol. 2005;193(3 Pt 2):1045–1049.
[62] Gielchinsky Y, Mankuta D, Rojansky N, et al. Perinataloutcome of pregnancies complicated by placentaaccreta. Obstet Gynecol. 2004;104(3):527–530.
[63] Chou MM, Ho ES, Lee YH. Prenatal diagnosis of pla-centa previa accreta by transabdominal color Dopplerultrasound. Ultrasound Obstet Gynecol. 2000;15(1):28–35.
[64] Twickler DM, Lucas MJ, Balis AB, et al. Color flowmapping for myometrial invasion in women with aprior cesarean delivery. J Matern Fetal Med.2000;9(6):330–335.
[65] Bailit JL, Grobman WA, Rice MM, et al. Morbidlyadherent placenta treatments and outcomes. ObstetGynecol. 2015;125(3):683–689.
[66] Tovbin J, Melcer Y, Shor S, et al. Prediction of mor-bidly adherent placenta using a scoring system.Ultrasound Obstet Gynecol. 2016;48(4):504–510.
[67] Evans GE, Phillipson GT, Sin IL, et al. Gene expressionconfirms a potentially receptive endometrium identi-fied by histology in fertile women. Hum Reprod.2012;27(9):2747–2755.
[68] Horcajadas JA, Riesewijk A, Polman J, et al. Effect ofcontrolled ovarian hyperstimulation in IVF on endo-metrial gene expression profiles. Mol Hum Reprod.2005;11(3):195–205.
[69] Kolibianakis E, Bourgain C, Albano C, et al. Effect ofovarian stimulation with recombinant follicle-stimulat-ing hormone, gonadotropin releasing hormone antag-onists, and human chorionic gonadotropin onendometrial maturation on the day of oocyte pick-up.Fertil Steril. 2002;78(5):1025–1029.
[72] Cal�ı G, Forlani F, Minneci G, et al. First-trimester pre-diction of surgical outcome in abnormally invasiveplacenta using the cross-over sign. Ultrasound ObstetGynecol. 2018;51(2):184–188.
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 481
Supporting information 1: Search strategy. EMBASE ---------------------------------------------------------- 1 exp Placenta Accreta/ (3080) 2 (placenta* adj5 accreta*).tw. (1988) 3 (placenta* adj5 increta*).tw. (470) 4 (placenta* adj5 percreta*).tw. (907) 5 (invas* adj5 placenta*).tw. (1714) 6 (infiltrat* adj5 placenta*).tw. (230) 7 (placenta* adj5 adhes*).tw. (270) 8 (adhere* adj5 placenta*).tw. (692) 9 "myometrial invasion*".tw. (2876) 10 (myometri* adj5 (invad* or invasion*)).tw. (3408) 11 "Morbidly adherent placenta".tw. (213) 12 (Morbid* adhere* adj5 placenta*).tw. (260) 13 "Abnormal invasive placenta".tw. (5) 14 (Abnorm* adj5 invasi* adj5 placenta*).tw. (177) 15 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 or 9 or 10 or 11 or 12 or 13 or 14 (8930) 16 exp Ultrasonography/ (633694) 17 (ultrasound* or ultrasonograph*).tw. (382563) 18 endosonograph*.tw. (3473) 19 sonograph*.tw. (64372) 20 MRI*.tw. (305042) 21 exp Magnetic Resonance Imaging/ (748839) 22 "magnetic resonance imag*".tw. (222840) 23 (image* or imaging).tw. (1176661) 24 exp Diagnostic Imaging/ (139764) 25 (echoplanar adj5 imag*).tw. (446) 26 ("echo planar" adj5 imag*).tw. (3732) 27 ("echo-planar" adj5 imag*).tw. (3732) 28 (doppler or USS).tw. (129906) 29 echograph*.tw. (11634) 30 screen*.tw. (791632) 31 exp Mass Screening/ (204355) 32 16 or 17 or 18 or 19 or 20 or 21 or 22 or 23 or 24 or 25 or 26 or 27 or 28 or 29 or 30 or 31 (2998350) 33 exp Prenatal Diagnosis/ (95324) 34 (antenatal* or "ante natal*").tw. (41149) 35 (prenatal* or "pre natal*").tw. (104498) 36 ((before or prior or preced*) adj5 (birth* or born or labour or labor or parturi*)).tw. (22412) 37 33 or 34 or 35 or 36 (213157) 38 15 and 32 and 37 (534) 39 limit 38 to english language (496)
MEDLINE ------------------------------------------------------------ 1 exp Placenta Accreta/ (1704) 2 (placenta* adj5 accreta*).tw. (1413) 3 (placenta* adj5 increta*).tw. (307) 4 (placenta* adj5 percreta*).tw. (610) 5 (invas* adj5 placenta*).tw. (1110) 6 (infiltrat* adj5 placenta*).tw. (170) 7 (placenta* adj5 adhes*).tw. (204) 8 (adhere* adj5 placenta*).tw. (420) 9 "myometrial invasion*".tw. (1983) 10 (myometri* adj5 (invad* or invasion*)).tw. (2345) 11 "Morbidly adherent placenta".tw. (107) 12 (Morbid* adhere* adj5 placenta*).tw. (131) 13 "Abnormal invasive placenta".tw. (1) 14 (Abnorm* adj5 invasi* adj5 placenta*).tw. (107) 15 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 or 9 or 10 or 11 or 12 or 13 or 14 (6038) 16 exp Ultrasonography/ (379729) 17 (ultrasound* or ultrasonograph*).tw. (263531) 18 endosonograph*.tw. (2376) 19 sonograph*.tw. (48240) 20 MRI*.tw. (180780) 21 exp Magnetic Resonance Imaging/ (365559) 22 "magnetic resonance imag*".tw. (177248) 23 (image* or imaging).tw. (880455) 24 exp Diagnostic Imaging/ (2331532) 25 (echoplanar adj5 imag*).tw. (317) 26 ("echo planar" adj5 imag*).tw. (3016) 27 ("echo-planar" adj5 imag*).tw. (3016) 28 (doppler or USS).tw. (91665) 29 echograph*.tw. (9061) 30 screen*.tw. (574359) 31 exp Mass Screening/ (111739) 32 16 or 17 or 18 or 19 or 20 or 21 or 22 or 23 or 24 or 25 or 26 or 27 or 28 or 29 or 30 or 31 (3348031) 33 exp Prenatal Diagnosis/ (66466) 34 (antenatal* or "ante natal*").tw. (30102) 35 (prenatal* or "pre natal*").tw. (83174) 36 ((before or prior or preced*) adj5 (birth* or born or labour or labor or parturi*)).tw. (17934) 37 33 or 34 or 35 or 36 (161379) 38 15 and 32 and 37 (366) 39 limit 38 to english language (328)
CINAHL -------------------------------------------------- 1. CINAHL; PLACENTA ACCRETA/; 3. CINAHL; (placenta* N5 accreta*).ti,ab; 4. CINAHL; (placenta* N5 increta*).ti,ab; 5. CINAHL; (placenta* N5 percreta*).ti,ab; 6. CINAHL; (invas* N5 placenta*).ti,ab; 7. CINAHL; (infiltrat* N5 placenta*).ti,ab;. 8. CINAHL; (adhere* N5 placenta*).ti,ab; 9. CINAHL; (Morbid* adhere* adj5 placenta*).ti, ab; 10. CINAHL; (Abnorm* adj5 invasi* adj5 placenta). ti, ab; 11. CINAHL; "myometrial invasion*".ti,ab;. 12. CINAHL; (myometri* N5 (invad* OR invasion*)).ti,ab;. 13. CINAHL; 1 OR 3 OR 4 OR 5 OR 6 OR 7 OR 8 OR 9 OR 10; 14. CINAHL; exp ULTRASONOGRAPHY/; 15. CINAHL; (ultrasound* OR ultrasonograph*).ti,ab; 16. CINAHL; endosonograph*.ti,ab; 17. CINAHL; sonograph*.ti,ab; 18. CINAHL; MRI*.ti,ab; 8960 results. 19. CINAHL; exp MAGNETIC RESONANCE IMAGING/; 20. CINAHL; "magnetic resonance imag*".ti,ab; 21. CINAHL; (image* OR imaging).ti,ab; 22. CINAHL; exp DIAGNOSTIC IMAGING/; 23. CINAHL; (echoplanar N5 imag*).ti,ab; 24. CINAHL; ("echo planar" N5 imag*).ti,ab; 25. CINAHL; ("echo-planar" N5 imag*).ti,ab; 26. CINAHL; (doppler OR USS).ti,ab; 27. CINAHL; echograph*.ti,ab; 28. CINAHL; screen*.ti,ab; 29. CINAHL; 12 OR 13 OR 14 OR 15 OR 16 OR 17 OR 18 OR 19 OR 20 OR 21 OR 22 OR 23 OR 24 OR 25 OR 26; 30. CINAHL; exp PRENATAL DIAGNOSIS/; 31. CINAHL; (antenatal* OR "ante natal*").ti,ab; 31. CINAHL; (prenatal* OR "pre natal*").ti,ab; 33. CINAHL; ((before OR prior OR preced*) adj5 (birth* OR born OR labour OR labor OR parturi*)).ti,ab; 34. CINAHL; 28 OR 29 OR 30 OR 31; 35. CINAHL; 11 AND 27 AND 32; 36. CINAHL; 33 [Limit to: Publication Year 1990-2013 and (Language English)];
Cochrane ---------------------------------------------------- #1 MeSH descriptor: [Placenta Accreta] 13 #2 placenta* near/5 accreta*:ti,ab,kw 40 #3 placenta* near/5 (increta* or percreta*):ti,ab,kw 9 #4 invas* near/5 placenta*:ti,ab,kw 15 #5 infiltrat* near/5 placenta*:ti,ab,kw 4 #6 Morbid* adhere* near/5 placenta*:ti,ab,kw 5 #7 Abnorm* near/5 invasi* near/5 placenta*:ti,ab,kw 1 #8 placenta* near/5 adhes*:ti,ab,kw 5 #9 adhere* near/5 placenta*:ti,ab,kw 13 #10 "myometrial invasion*":ti,ab,kw 59 #11 (myometri* near/5 (invad* or invasion*)):ti,ab,kw 61 #12 #1 or #2 or #3 or #4 or #5 or #6 or #7 or #8 or #9 or #10 or #11 127
Supporting Information 2. Excluded studies and reason for the exclusion.
Author Year Title Reason for the exclusion
Ayad 2017 The role of three-dimensional power Doppler ultrasound in diagnosis of abnormally invasive placenta
It was not entirely clear whether all women in the study group haAIP.
Millischer 2017 Dynamic contrast enhanced MRI of the placenta: A tool for prenatal diagnosis of placenta accreta?
This study shares cases with that of Millischer et al. Which was included in the present systematic review
Aitken 2016 MRI Significantly Improves Disease Staging to Direct Surgical Planning for Abnormal Invasive Placentation: A Single Centre Experience
No control group included
Balcacer 2016 Magnetic Resonance Imaging and Sonography in the Diagnosis of
Placental Invasion
No data on risk factors
Khalid 2016 Diagnostic Accuracy of Color Doppler Ultrasound in Antenatal Diagnosis of Morbidly Adherent placenta, taking Operative Findings of Caesarean Section as Gold Standard
No data on risk factors
Ishan Kumar 2016 Invasive placental disorders: a prospective US and MRI comparative analysis No data on risk factors
Lim 2016 Correlation of probability scores of placenta accreta on magnetic resonance imaging with
hemorrhagic morbidity
No data on risk factors
Sengupta 2016 Interventions for improving pregnancy outcomes in antenatally diagnosed or suspected morbidly adherent placenta
Review article
Ueno 2016 Evaluation of Interobserver Variability and Diagnostic Performance of Developed MRI-Based Radiological Scoring System for Invasive Placenta Previa
No data on risk factors
Haidar 2016 Can 3D power doppler analysis of a potentially morbidly adherent placenta improve the prenatal diagnosis of this condition?
Conference abstract
Goh 2015 Placenta accreta: Diagnosis, management and the molecular biology of the morbidly adherent placenta.
Review article
Hashem 2015 Role of MRI versus ultrasound in the assessment of placental abnormalities and diseases It was not possible to extrapolate data on cases affected compared those not affected by AIP
Horowitz 2015 When Timing Is Everything:Are Placental MRI Examinations Performed Before 24 Weeks’ Gestational Age Reliable?
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Kelekci 2015 A Comprehensive Surgical Procedure in Conservative Management of Placenta Accreta Only women affected by AIP were included in this study
Ishan Kumar 2015 Chemical Shift Artifact on Steady-State MRI Sequences for Detection of Vesical Wall Invasion in placenta Percreta
Only cases affected by AIPincluded in this study
Polat 2015 Shorter the cervix, more difficult the placenta percreta operations
No control group included
Rheinboldt 2015 Sonography of placental abnormalities: a pictorial review It was not possible to extrapolate data on cases affected compared those not affected by AIP
Salim 2015 Precesarean Prophylactic Balloon Catheters for Suspected Placenta Accreta A Randomized Controlled Trial
no data on risk factors for AIP, patients at risk for placenta accretand with a prenatal diagnosis for placenta accreta were randomly
assigned to intervention group or control group
Shamshirsaz 2015 Maternal Morbidity in Patients With Morbidly Adherent Placenta Treated
With and Without a Standardized Multidisciplinary Approach
Only cases affected by AIP included
Mahesh 2015 Morbidly AdherentPlacenta:Ultrasound Assessment andSupplementalRole of Magnetic Resonance Imaging
no data on risk factors
Tovbin 2015 Predicting of morbidly adherent placenta using a scoring system: A prospective study It was not possible to extrapolate data on cases affected compared those not affected by AIP
Wang 2015 Reproductive outcomes after previous cesarean scar pregnancy: Follow up of 189 women No data on the outcomes explored in this ssytematic review
Creanga 2015 Morbidity associated with cesarean delivery in the United States: Is placenta accreta an increasingly important contributor?
In the present study AIP was confirmedaccording to 1) radiologicevidence; 2) a presumptive clinical diagnosis made surgically durincaesarean section or laparotomy post-vaginal delivery; 3) pathologreport, or 4) a description in the patient discharge summary writteby the obstetrician. However, in the present systematic review, wincluded only women with a histopathological, clinical or surgicaconfirmation of AIP. In view of the different reference standardsadopted thisstudy was not considered suitable for the inclusion
Tanimura 2015 Prediction of adherent placenta in pregnancy with placenta previa using ultrasonography and magnetic resonance imaging
Data were reported only as continuous variables
Algebally 2014 The Value of Ultrasound and Magnetic Resonance Imaging in Diagnostics and Prediction of Morbidity in
No data on risk factors for AIP
Bowman 2014 Risk factors for unscheduled delivery in patients with placenta accreta Another study from the same research group was included in thepresent systematic review
Bowman 2014 Interobserver Variability of Sonography for Prediction of Placenta Accreta Another study from the same research group was included in thepresent systematic review
Gilboa 2014 A Novel Sonographic Scoring System for Antenatal Risk Assessment of
Obstetric Complications in Suspected Morbidly Adherent Placenta
No crude number for different risk factors explored in this retrospective study could be extrapolate for the group of AIP and
normal placentation
Hafeez 2014 Placenta Previa; Prevalence, Risk Factor and Outcome Only cases with placenta previa included in this series; no information of AIP
Hall 2014 Prenatal Sonographic Diagnosis of Placenta Accreta—Impact on Maternal and Neonatal
Outcomes
Only cases affected by AIP included
D’Antonio 2014 Prenatal identification of invasive placentation using magnetic resonance imaging: systematic review
and meta-analysis
Systematic review, no original data reported
Pather 2014 Maternal outcome after conservative management of placenta percreta at caesarean section: A report of three cases and a review of the
literature
Only cases affected by AIP included
Pongrojpaw 2014 Prenatal Diagnosis of Placenta Accreta by Colour Doppler Ultrasonography: 5-Year Review
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Quant 2014 Transabdominal Ultrasonography as a Screening Test for Second-Trimester
Placenta Previa
No data on AIP
Rahimi-Sharbaf 2014 Ultrasound detection of placenta accreta in the first trimester of pregnancy It was not possible to extrapolate data on cases affected compared those not affected by AIP
Rezk 2014 Grey-scale and colour Doppler ultrasound versus magnetic resonance imaging for the prenatal diagnosis of placenta accreta
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Riteau 2014 Accuracy of Ultrasonography and Magnetic Resonance Imaging in the Diagnosis of Placenta Accreta
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Silver 2014 Center of excellence for placenta accreta It was not possible to extrapolate data on cases affected compared those not affected by AIP
Desai 2014 Elevated first trimester PAPP-A is associated with increased risk of placenta accreta It was not possible to extrapolate data on cases affected compared those not affected by AIP
Young 2014 Does previa location matter? Surgical morbidity associated with location of a placenta previa
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Chantraine 2013 Prenatal diagnosis of abnormally invasive placenta reduces maternal peripartumhemorrhage and morbidity
No control group included
Elhawary 2013 Diagnostic value of ultrasonography and magnetic resonance imaging in pregnant women at risk for placenta accreta
It was not possible to extrapolate data for cases affected and not affected by AIP
Fitzpatrick 2013 The management and outcomes of placenta accreta, increta, and percreta in the UK: a population-based descriptive study
No data on risk factors
Chalubinsky 2013 Prenatal sonography can predict degree of placental invasion no crude number for different risk factors explored in this retrospective study could be extrapolate for the group of AIP and
normal placentation
Ebrahim 2013 Clinical and ultrasound assessment in patients with placenta It was not possible to extrapolate the data regarding the prevalencethe different risk factors explored in women with compared to tho
without AIP
Higgins 2013 Real increasing incidence of hysterectomy for placenta accreta following previous caesarean section
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Maher 2013 Diagnostic accuracy of ultrasound and MRI in the prenatal diagnosis of placenta accreta No data could be extrapolated for women not affected by AIP
Pereira 2013 Placenta membranacea with placenta accreta: radiologic diagnosis and clinical implications
Case report
Salomon 2013 MRI and ultrasound fusion imaging for prenatal diagnosis No data on risk factors
D’Antonio 2013 Prenatal identification of invasive placentation using ultrasound: systematic review and meta-analysis
Systematic review, no original data reported
Varghese 2013 Magnetic resonance imaging of placenta accreta Review article
Walker 2013 Multidisciplinary Management of Invasive Placenta Previa It was not possible to extrapolate data on cases affected compared those not affected by AIP
Guleria 2013 Abnormally invasive placenta: changing trends in diagnosis and management No control group included
Morlando 2013 Placenta accreta: incidence and risk factors in an area with a particularly high rate of cesarean section
Only cases affected by AIP included
Peker 2013 Assessment of total placenta previa by magnetic resonance imaging and ultrasonography to detect placenta accreta and its variants
Data were reported only as continuous variables
Samuel 2013 Fraction of cell-free fetal DNA in the maternal serum as a predictor of abnormal placental invasion-a pilot study
Data were reported only as continuous variables
Chantraine 2012 Individual decisions in placenta increta and percreta: a case series No control group included
Dreux 2012 Second-trimester maternal serum markers and placenta accreta No control group included
Fukushima 2012 Cervical length predicts placental adherence and massive hemorrhage in placenta previa No crude number for the different risk factors explored in the presereview could be extrapolated
Gouhar 2012 Role of transperineal sonography in diagnosis of placenta previa/accreta: A prospective study
It was not possible to extrapolate the data regarding the prevalencethe different risk factors explored in women with compared to tho
without AIP
Gyamfi-Bannerman 2012 Risk of Uterine Rupture and Placenta Accreta With Prior Uterine Surgery Outside of the Lower Segment
This study explored the occurrence of AIP in women with specifirisk factors. Furthermore, the study used the same database of another publication included in the present systematic review
PALACIOS-JARAQUEMADA1,2,
2012 MRI in the diagnosis and surgical management of abnormal placentation No data on risk factors
Benedetti Panici 2012 Intraoperative aorta balloon occlusion: fertility preservation in patients with placenta previa accreta/increta
Only cases of AIP included in this study
Rao 2012 Abnormal Placentation: Evidence-Based Diagnosis and Management of Placenta
Previa, Placenta Accreta, and Vasa Previa
Review article
Shweel 2012 Placenta accreta in women with prior uterine surgery: Diagnostic accuracy of Doppler ultrasonography and MRI
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Wong 2012 Antenatal ultrasound assessment of placental⁄myometrial involvement in morbidly adherent placenta
Only cases affected by AIP included
Eller 2011 Maternal Morbidity in Cases of Placenta Accreta Managed by a Multidisciplinary Care Team Compared With Standard Obstetric Care
No control group included
Esakoff 2011 Diagnosis and morbidity of placenta accreta No data on risk factors
Carnevale 2011 Perioperative Temporary Occlusion of the Internal Iliac Arteries No data on risk factor and no control group
Hamada 2011 Ultrasonographic findings of placenta lacunae and a lack of a clear zone in cases with placenta previa and normal placenta
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Mansour 2011 Placenta previa – accreta: Do we need MR imaging? No data on risk factors
Marshall 2011 Impact of multiple cesarean deliveries on maternal morbidity: a systematic review Systematic review, no original data reported
McLean 2011 Assessing the Role of Magnetic Resonance Imaging in the
Management of Gravid Patients at Risk for Placenta Accreta
It was not possible to extrapolate data on cases affected compared those not affected by AIP separately
Morotti 2011 Defective placental adhesion in voluntary termination of second-trimester pregnancy and risk of recurrence in subsequent pregnancies
No data on control group
Tikkanen 2011 Antenatal diagnosis of placenta accreta leads to reduced blood loss Only cases affected by AIP included
Wright 2011 Predictors of massive blood loss in women with placenta accreta Only cases affected by AIP included
Wehrum 2011 Accreta complicating complete placenta previa is characterized by reduced systemic levels of vascular
endothelial growth factor and by epithelial-to-mesenchymal transition of the invasive trophoblast
It was not possible to extrapolate data on the risk factors observed the present systematic review in women affected compared to thos
non-affected by AIP
Soyer 2011 Value of pelvic embolization in the management of severe postpartum hemorrhage due to placenta accreta, increta or percreta
Only cases affected by AIP included in this study
Fishman 2011 Risk factors for emergent preterm delivery in women with placenta previa and ultrasound findings suspicious for placenta accreta
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Rosenberg 2011 Critical analysis of risk factors and outcome of placenta previa This study explored the occurrence of AIP in women with specifirisk factors. Furthermore, in view of the very large sample size
especially in the group of women not affect by placenta previa, it wnot possible to extrapolate the raw number of AIP in this populatio
Dueñas-Garcia 2010 Utility of the pulsatility index of the uterine arteries and human chorionic gonadotropin in a series of cases of
placenta accreta
Only cases affected by AIP included
Lau 2010 Prenatal diagnosis of morbidly adherent placenta Editorial, no original data included
Woodring 2010 Prediction of placenta accreta by ultrasonography and colordoppler imaging It was not possible to extrapolate data on cases affected compared those not affected by AIP
Rao 2010 Role of interventional radiology in the management of morbidly adherent placenta
Only cases affected by AIP included
Robinson 2010 Effectiveness of Timing Strategies for Delivery of Individuals With Placenta Previa and Accreta
No data on risk factors
Diop 2010 Placenta Accreta: Management with Uterine Artery Embolization in 17 Cases Only cases of AIP included in this study
Iwata 2010 Limitations of internal iliac artery ligation for the reduction of intraoperative hemorrhage during cesarean hysterectomy in cases of placenta previa accreta
Only cases affected by AIP included
Provansal 2010 Fertility and obstetric outcome after conservative management of placenta accreta Only cases affected by AIP included
Angstman 2010 Surgical management of placenta accreta: a cohort series and suggested approach Only cases affected by AIP included
Lone 2010 Risk factors and management patterns for emergency obstetric hysterectomy over 2 decades
No data on risk factors
Sivan 2010 Prophylactic Pelvic Artery Catheterization and Embolization in Women with Placenta
Accreta: Can It Prevent Cesarean Hysterectomy?
No data on risk factors
Chou 2009 PRENATAL DETECTION OF BLADDER WALL INVOLVEMENT IN INVASIVE PLACENTATION WITH SEQUENTIAL TWO-DIMENSIONAL AND ADJUNCTIVE
THREE-DIMENSIONAL ULTRASONOGRAPHY
no data on risk factor for normal placentation
Mazouni 2009 Differences in the management of suspected cases of placenta accreta in France and Argentina
No data on risk factors
Sofiah 2009 Placenta Accreta: Clinical Risk Factors, Accuracy of Antenatal Diagnosis and Effect on Pregnancy Outcome
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Shih 2009 Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale
and color Doppler techniques
No data on risk factors
Teo 2009 Use of magnetic resonance imaging in evaluation of placental invasion No data on risk factors
Chou 2009 PRENATAL DETECTION OF BLADDER WALL INVOLVEMENT IN INVASIVE PLACENTATION WITH SEQUENTIAL TWO-DIMENSIONAL AND ADJUNCTIVE
THREE-DIMENSIONAL ULTRASONOGRAPHY
Only cases affected by AIP included in this study
Maselli 2008 Magnetic resonance imaging in the evaluation of placental adhesive disorders: correlation with color Doppler ultrasound
No data on risk factors for AIP
Miura 2008 Increased level of cell-free placental mRNA in a subgroup of placenta previa that needs hysterectomy
No data on risk factors
Rosen 2008 Placenta Accreta and Cesarean Scar
Pregnancy: Overlooked Costs of the Rising
Cesarean Section Rate
No data on risk factors
Lax 2007 The value of specific MRI features in the evaluation of suspected placental invasion No data on risk factors
Rani 2007 Comparative study of transperineal and transabdominal sonography in the diagnosis of placenta previa
No data on AIP
Sumigama 2007 Placenta previa increta/percreta in Japan: A retrospective study of ultrasound findings, management and clinical course
It was not possible to extrapolate data on cases affected compared those not affected by AIP for the outcomes explored in the presen
systematic review
Stanek 2007 Occult Placenta Accreta: The Missing Link in the Diagnosis of Abnormal Placentation This study included women with occult placenta accreta, a conditiocharacterized by basal plate myometrial fibers without intervenindecidua in spontaneously delivered placentas. Althought this entitmay share several characteristics with the classical types of AIP, ihas been not clearly defined yet and therefore this study was not
considered suitable for the inclusion.
Tan 2007 Perioperative Endovascular Internal Iliac Artery Occlusion Balloon Placement in Management of Placenta Accreta
Only cases affected by AIP included
Knight 2007 Peripartum hysterectomy in the UK: management and outcomes of the associated haemorrhage
It was not possible to extrapolate data on the risk factors observed the present systematic review in women affected compared to thos
non affected by AIP
Shrivastava 2007 Case-control comparison of cesarean hysterectomy with and without prophylactic placement of intravascular balloon catheters for placenta accreta
Only cases affected by AIP included in this study
Grobman 2007 Pregnancy Outcomes for Women With Placenta Previa in Relation to the Number of Prior Cesarean Deliveries
This study uses the same databse of that by Bowman et al, which wconsidered most representative of the clinical condition and the
outcomes observed in the present systematic review
Alchalabi 2007 Does the number of previous cesarean delivery affects maternal outcome and complication rates
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Yap 2007 Manual removal of suspected placenta accreta at cesarean hysterectomy It was not possible to extrapolate data on cases affected compared those not affected by AIP
Blaicher 2006 Magnetic resonance imaging of the normal placenta No data on risk factors for AIP
Mazouni 2006 Placenta Accreta: A Review of Current Advances in Prenatal Diagnosis Review article
Lax 2006 The value of specific MRI features in the evaluation of suspected placental invasion No data on rcontrol groups
Yang 2006 Sonographic findings of placental lacunae and the prediction of adherent placenta in women with placenta previa totalis and prior Cesarean section
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Silver 2006 Maternal Morbidity Associated With Multiple Repeat Cesarean Deliveries This study uses the same databse of that by Bowman et al, which wconsidered most representative of the clinical condition and the
outcomes observed in the present systematic review
Palacio-Jaraquemada 2005 Magnetic resonance imaging in 300 cases of placenta accreta: surgical correlation of new findings
No control group included
Armstrong 2004 Is placenta accreta catching up with us? No controls group included
Comstock 2004 Sonographic detection of placenta accreta in the second and third trimesters of pregnancy No data on risk factors
KIM 2004 Magnetic Resonance Imaging with True Fast Imaging with Steady- State Precession and Half-Fourier Acquisition Single-Shot Turbo
Spin-Echo Sequences in Cases of Suspected Placenta Accreta
no data on risk factors
Moodley 2004 Imaging techniques to identify morbidly adherent placenta praevia: a prospective study
No data on risk factors
Landon 2004 Maternal and Perinatal Outcomes Associated with a Trial of Labor after Prior Cesarean Delivery
no data on risk for AIP, this study focus on VBAC and its complications
Predanic 2004 A Sonographic Assessment of Different Patterns of Placenta Previa “Migration”
in the Third Trimester of Pregnancy
No data on risk factors
Taipale 2004 Prenatal Diagnosis of Placenta Accreta and Percreta With Ultrasonography, Color Doppler, and Magnetic Resonance Imaging
Only two acses of AIP included in this study
Kayem 2004 Conservative Versus Extirpative Management in Cases of Placenta Accreta Only cases affected by AIP included in this study
Makoha 2004 Multiple cesarean section morbidity This study explored the occurrence of AIP in women with specifirisk factors (CS).
Kim 2004 Magnetic Resonance Imaging with True Fast Imaging with SteadyState Precession and Half-Fourier Acquisition Single-Shot Turbo Spin-Echo Sequences in Cases of Suspected
Placenta Accreta
Data were reported only as continuous variables
Chou 2003 Internal Iliac Artery Embolization before Hysterectomy for Placenta Accreta Only cases affected by Aip included in this study
Chou 2002 The application of three-dimensional color power Doppler ultrasound in the depiction of abnormal uteroplacentalangioarchitecture in placenta previa percreta
It was not stated when the cases included in this study were recruiteBecause this study might share cases with the others from the sam
author, we did not considered it eligibel for the inclusion
Gilliam 2002 The Likelihood of Placenta Previa With Greater Number of Cesarean Deliveries and Higher Parity
It was not possible to extrapolate data on cases affected compared those not affected by AIP
Lam 2002 usa of magnetic resonance imaging and ultrasound in the antenatal diagnosis of placenta accreta
No control group included
Gielchinsky 2002 Placenta Accreta—Summary of 10 Years: A Survey of 310 Cases Only acses affected by AIP included in this study
Lam 2002 Use of Magnetic Resonance Imaging and Ultrasound in the Antenatal Diagnosis of Placenta Accreta
Only one case not affected by AIP included
Ghourab 2001 BOlraicgkinwaellAlSrtciicelnece, Ltd Third-trimester transvaginal ultrasonography in placenta
previa: does the shape of the lower placental edge predict clinical outcome?
No rdata on isk factors for AIP
Patel 2000 A CRITICAL EVALUATION OF TRANSPERINEAL SONOGRAPHY (TPS) IN THE DIAGNOSIS OF PLACENTA
PREVIA
Conference abstract
Russ 2000 Pelvic Varices Mimicking
Placenta Percreta at Sonography
Case report
Sentilhes Long-term psychological impact of severe postpartum hemorrhage No data on risk factors
1
Figure S1. Results of the meta-analysis comparing the maternal age in women with versus women without a diagnosis of abnormally invasive placenta (AIP).
AIP No AIP Mean Difference Mean DifferenceIV, Random, 95% CI
-10 -5 0 5 10Favours [AIP] Favours [No AIP]
2
Figure S2. Results of the meta-analysis comparing the parity status in women with versus women without a diagnosis of abnormally invasive placenta (AIP).
AIP No AIP Mean Difference Mean DifferenceIV, Random, 95% CI
-4 -2 0 2 4Favours [AIP] Favours [No AIP]
3
Figure S3. Results of the meta-analysis comparing the number of previous cesarean sections in women with versus women without a diagnosis of abnormally invasive placenta (AIP).
AIP No AIP Mean Difference Mean DifferenceIV, Random, 95% CI
-2 -1 0 1 2Favours [AIP] Favours [No AIP]
4
Figure S4. Results of the meta-analysis comparing the Body Mass Index in women with versus women without a diagnosis of abnormally invasive placenta (AIP).
Figure S10. Results of the meta- comparing the likelihood of AIP in women with versus women without a diagnosis of placenta previa and a previous cesarean section.
IVF No IVF Odds Ratio Odds RatioM-H, Random, 95% CI
0.01 0.1 1 10 100Favours [IVF] Favours [No IVF]
19
Figure S19. Results of the meta- comparing the likelihood of AIP in women reporting versus women not reporting a short interval (<23 months) between previous CS and subsequent pregnancy.
Study or Subgroup
Fitzpatrick 2012Lyell 2015
Total (95% CI)
Total eventsHeterogeneity: Tau² = 0.30; Chi² = 3.10, df = 1 (P = 0.08); I² = 68%Test for overall effect: Z = 1.26 (P = 0.21)
Events
4913
62
Total
64131
195
Events
6120
81
Total
82543
625
Weight
49.2%50.8%
100.0%
M-H, Random, 95% CI
1.12 [0.52, 2.41]2.88 [1.39, 5.96]
1.81 [0.72, 4.58]
Year
20122015
<23 months ≥23 months Odds Ratio Odds RatioM-H, Random, 95% CI