risk factors for abnormally invasive placenta: a

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

KEYWORDSAbnormally invasiveplacenta; cesarean section;placenta; risk factors;systematic review andmeta-analysis

Introduction

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

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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].

472 A. IACOVELLI ET AL.

https://doi.org/10.1080/14767058.2018.1493453

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

20 8 12

Pilloni [21] 2016 Italy Prospective 2011–2014 Placenta previa(26 weeksof gestation)

314 37 277

Thiravit [22] 2016 Thailand Retrospective 2005–2014 Women with ultra-sound suspicionof AIP

21 12 9

Collins [23] 2015 UK/USA Prospective 2012–2014 Clinical and/or ultra-sound suspicionof AIP

89 42 47

Lyell [24] 2015 USA Retrospective 2009–2010 AIP andmatched controls

736 37 699

Miller [25] 2015 USA Retrospective 2008–2013 AIP andmatched controls

125 25 100

Parra-Herran [26] 2015 Canada Retrospective 2002–2015 Women undergoingpostpartumhysterectomy

61 44 17

Thurn [27] 2015 Denmark,Finland, Iceland,Norway,and Sweden

Prospective 2009–2012 Women affected byAIP versus gen-eral population

605,567 205 605,362

Alchalabi [28] 2014 Jordan Retrospective 2003–2012 Women who had CSfor AIP or pla-centa previa

81 23 58

Bour [29] 2014 France Retrospective 2006–2012 Clinical and/or US sus-picion of AIP

32 16 16

Rac [10] 2014 USA Retrospective 1997–2011 Placenta previa/lowlying þ> 1 CS184

54 130

Zhou [30] 2014 China Retrospective 2011–2013 Women with prior CS 68 12 56Noda [31] 2014 Japan/USA Retrospective 2011–2013 Women with suspicion

of AIP28 7 21

Asıcıoglu [32] 2014 Turkey Retrospective 2005–2010 placenta previa 364 46 318Laban [33] 2014 Egypt Retrospective 2012–2013 AIP and

matched controls76 26 50

Bowman [34] 2013 USA Retrospective 1999–2002 Women affected ornonaffected by AIPwith a prior CS

2749 196 2553

Cali [35] 2013 Italy Prospective 2004–2012 Placenta previa andprior uter-ine surgery

187 41 146

Ueno [36] 2013 Japan Retrospective 2009–2013 Women undergoingMRI for the suspi-cion of AIP

65 15 50

Weiniger [37] 2013 Israel Prospective 2002–2011 Placenta previa and/orat least one CS sus-pected of AIP on US

92 52 40

Eshkoli [38] 2013 Israel Retrospective 1988–2011 AIP andmatched controls

34,869 139 34.730

Kamara [39] 2013 Australia Prospective 1993–2008 Placenta previaþ p-rior CS

167 65 102

Klar [40] 2013 Germany Retrospective 2000–2007 AIP andunmatched controls

483 161 322

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)

El Behery [49] 2010 Egypt Prospective 2007–2009 Clinical risk factorsfor AIP

35 7 28

Hasegawa [50] 2009 Japan Retrospective 2000–2007 Placenta previa 127 5 122Morita [51] 2009 Japan Retrospective 2008 Women undergoing

MRI for the suspi-cion of AIP

7 3 4

Dwyer [52] 2008 USA Retrospective 2001–2016 Clinical or imaging sus-picion of AIP

32 15 17

Wong [53] 2008 New Zealand Prospective 2004–2006 Clinical risk factorsfor AIP

66 9 57

Tantbirojn [54] 2008 USA Retrospective 2002–2007 Cases of post-partumhysterectomy

49 38 11

Mok [55] 2008 UK prospective 2002–2007 Women with ultra-sound suspicion ofAIP undergoinginterventionalradiology

13 5 8

Japaraj [56] 2007 Malaysia Prospective 2002–2005 Placenta previaþ p-rior CS

20 7 13

Wong [57] 2007 New Zealand retrospective 2004–2005 Clinical and/or ultra-sound suspicionof AIP

36 5 31

Bencaiova [58] 2007 Switzerland retrospective 1999–2003 AIP andmatched controls

8839 31 8808

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


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.


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

Millischer [20] 2017 ? ? ? ? ?Pilloni [21] 2016 ? ? ? ? ?Thiravit [22] 2016 ? ? ? ? ?Collins [23] 2015 ? ? ? ? ?Lyell [24] 2015 ? ? ? ? ?Miller [25] 2015 ? ? ? ? ?Parra-Herran [26] 2015 ? ? ? ?Thurn [27] 2015 ? ? ? ? ? ?Alchalabi [28] 2014 ? ? ? ? ?Bour [29] 2014 ? ? ? ? ?Rac [10] 2014 ? ? ? ?Zhou [30] 2014 ? ? ? ? ? ?Noda [31] 2014 ? ? ? ? ?Asıcıoglu [32] 2014 ? ? ? ? ?Laban [33] 2014 ? ? ? ? ?Bowman [34] 2013 ? ? ? ? ? ?Cal�ı [35] 2013 ? ? ? ?Ueno [36] 2013 ? ? ? ? ?Weiniger [37] 2013 ? ? ? ? ?Eshkoli [38] 2013 ? ? ? ? ? ?Kamara [39] 2013 ? ? ? ? ?Klar [40] 2013 ? ? ? ? ?Upson [41] 2013 ? ? ? ? ? ?Fitzpatrick [42] 2012 ? ? ? ? ? ?Hannon [43] 2012 ? ? ? ? ?Chantraine [44] 2012 ? ? ? ?Lim [45] 2011 ? ? ? ? ?Sadashivaiah [46] 2011 ? ? ? ? ?Esh-Broder [47] 2011 ? ? ? ? ?Derman [48] 2011 ? ? ? ?El Behery [49] 2010 ? ? ? ?Hasegawa [50] 2009 ? ? ? ? ? ?Morita [51] 2009 ? ? ? ? ?Dwyer [52] 2008 ? ? ? ? ?Wong [53] 2008 ? ? ? ? ?Tantbirojn [54] 2008 ? ? ? ? ?Mok [55] 2008 ? ? ? ? ?Japaraj [56] 2007 ? ? ? ?Wong [57] 2007 ? ? ? ? ?Bencaiova [58] 2007 ? ? ? ? ? ?Warshak [59] 2006 ? ? ? ? ?Wu [60] 2005 ? ? ? ? ? ?Usta [61] 2005 ? ? ? ? ? ?Gielchinsky [62] 2004 ? ? ? ? ? ?Chou [63] 2000 ? ? ? ? ?Twickler [64] 2000 ? ? ? ? ?

A maximum of two stars can be given for Comparability.


Table

3.Results

ofthe

head-to-head

meta-analyses

comparin

gthe

risk

ofabno

rmally

invasive

placenta

(AIP)foreach

catego

rical

potentialpredictor(see

also

online

Figu

resS1–S32).

Predictors

Nstud

ies

References

Totalw

omen

OR

pI2,%

Sensitivity

Specificity

(sam

ple)

(n/N

versus

n/N)a

(95%

CI)

(95%

CI)

(95%

CI)

Obesity

5[24,27,36,38,42]

74/66,469versus

442/487,637

1.37

(1.04–1.81)

.02

014.3

(11.4–17.7)

88.0

(87.8–88.1)

(554,106)

Maternal

age>35

years

17[20,24,27,28,36,38,41,42,

45,46,50,54,55,58–61]

499/138,158versus

653/916,688

3.13

(1.40–6.97)

.005

9648.7

(38.0–59.6)

77.0

(67.3–84.6)

(1,055,206)

Currentsm

oking

11[24,27,34,36,38–42,45,61]

209/130,136versus

1130/918,844

1.13

(0.88–1.47)

.34

388.60

(3.40–20.0)

90.8

(83.3–95.2)

(1,048,980)

Multip

arity

20(1,022,675)

[23–28,34,39,41,42,

45,46,51,54,55,58,59,

61,62]

621/46,403

versus

938/976,362

2.49

(1.71–3.61)

<.001

7640.5

(27.9–54.5)

79.1

(65.9–88.1)

Placenta

previa

24[22,23,25–27,

29–31,34,37,38,41–43,

45,48,49,51,52,54,

57–59,62]

644/5256

versus

1050/1,051,966

11.0

(4.71–25.8)

<.001

9669.0

(51.9–82.2)

84.7

(64.5–94.4)

(1,057,222)

Placenta

previaþ

previous

CS12

[23,27,29,32,35,45,46,50–52,59,61]

200/912versus

131/428,095

12.0

(1.64–88.0)

.01

9787.2

(67.7–95.9)

54.1

(14.5–89.1)

(429,007)

�1previous

CS33

[22–29,31–36,38,40,42–46,

49–51,54–59,61–63]

925/80,458

versus

737/575,710

4.66

(3.02–7.18)

<.001

8285.1

(71.7–92.8)

53.5

(39.4–67.0)

(656,168)

Previous

electiveCS

3[27,32,39]

169/43,982

versus

337/649,742

3.73

(0.50–27.7)

.20

9887.2

(66.7–95.9)

54.1

(14.5–89.1)

(606,098)

Previous

emer-

gencyCS

3[27,32,39]

127/62,219

versus

189/543,879

1.17

(0.21–6.65)

.997

40.2

(34.7–45.8)

89.8

(89.7–89.8)

(606,098)

Previous

uter-

inesurgery

34[21–29,31–33,35,36,38,40–46,

49–52,54,55,57–59,

61–63]

893/116,082versus

976/941,281

4.42

(2.96–6.59)

<.001

8284.4

(70.7–92.4)

55.4

(41.9–68.1)

(1,057,363)

Previous

abortio

n6

[26,28,38–40,60]

179/3019

versus

364/33,092

1.36

(0.84–2.20)

.21

6225.6

(6.88–61.5)

72.4

(51.4-59.4-82.4)

(36,111)

Previous

curettage

16[22,23,25,26,32,35,37,40,44,45,

49,54,56–58,60]

232/1099

versus

412/9787

1.87

(0.96–3.64)

.06

8231.5

(19.0–47.3)

78.8

(66.5–87.4)

(10,886)

IVF

7[23,27,36,38,40,42,47]

51/14,402versus

598/474,495

2.80

(1.16–6.76)

.02

828.84

(5.02–15.1)

96.5

(92.2–98.4)

(488,897)

Shortintervalb

betweenprevi-

ousCS

andsub-

sequ

ent

pregnancy

2[24,42]

62/195

versus

81/625

1.81

(0.72–4.58)

.21

6843.4

(35.1–51.9)

80.4

(77.2–83.3)

(820)

CS:C

aesarean

section;

IVF:in

vitrofertilizatio

n;OR:

Odd

sRatio

;CI:confidence

interval.

a The

first“n/N”refersto

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https://doi.org/10.1080/14767058.2018.1493453

(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.

Pooled % of AIP Pooled % of AIP(95% CI) (95% CI)

Predictors A B

Maternal age >35 years 16.9 (11.9–22.4) 0.8 (0.4–1.3)Obesity 3.3 (0.0–12.3) 5.5 (3.2–8.2)Current smoking 0.8 (0.0–2.3) 6.1 (4.9–6.5)Multiparity 27.7 (17.4–39.0) 5.5 (4.4–6.7)Diagnosis of placenta previa 50.9 (37.2–64.5) 1.7 (0.9–2.8)Placenta previaþ previous CS 40.9 (27.2–55.3) 5.7 (0.5–14.3)� 1 previous CS 35.2 (29.2–41.4) 5.0 (2.5–8.1)Previous elective CS 16.8 (0.1–50.7) 5.2 (0.0–19.9)Previous emergency CS 10.3 (0.0–40.3) 16.0 (0.0–52.2)Previous myomectomy 25.5 (0.0–71.1) 43.3 (29.2–58.0)Previous uterine surgery 30.7 (26.6–34.9) 1.3 (0.6–2.2)Previous abortion 32.9 (5.2–69.6) 26.1 (5.6–54.6)Previous curettage 38.0 (21.6–55.6) 32.8 (16.0–52.2)IVF 3.5 (0.4–8.57) 9.7 (6.8–12.9)Short intervala between previous CS and subsequent pregnancy 28.6 (22.5–35.2) 8.8 (6.7–11.2)Manual extraction of the placenta 15.8 (0.0–93.8) 31.9 (9.30–59.8)Uterine incision 100.0 (20.6–100.0) 75.5 (67.8–81.9)Endometrial ablation 100.0 (20.7–100.0) 46.6 (36.5–56.9)

CS: Cesarean section; IVF: in vitro fertilization; CI: Confidence Interval; AIP: abnormally invasive placenta.a<23 months


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.

Disclosure statement

The authors report no conflict of interest.

ORCID

Danilo Buca http://orcid.org/0000-0001-6880-7407Alessandra Familiari http://orcid.org/0000-0002-6353-9383

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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


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


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


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


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


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


Pongrojpaw 2014 Prenatal Diagnosis of Placenta Accreta by Colour Doppler Ultrasonography: 5-Year Review


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


Riteau 2014 Accuracy of Ultrasonography and Magnetic Resonance Imaging in the Diagnosis of Placenta Accreta


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


Chantraine 2013 Prenatal diagnosis of abnormally invasive placenta reduces maternal peripartumhemorrhage and morbidity


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


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


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


Peker 2013 Assessment of total placenta previa by magnetic resonance imaging and ultrasonography to detect placenta accreta and its variants


Samuel 2013 Fraction of cell-free fetal DNA in the maternal serum as a predictor of abnormal placental invasion-a pilot study


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


Wong 2012 Antenatal ultrasound assessment of placental⁄myometrial involvement in morbidly adherent placenta


Eller 2011 Maternal Morbidity in Cases of Placenta Accreta Managed by a Multidisciplinary Care Team Compared With Standard Obstetric Care


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


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


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


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


Robinson 2010 Effectiveness of Timing Strategies for Delivery of Individuals With Placenta Previa and Accreta


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


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


Sivan 2010 Prophylactic Pelvic Artery Catheterization and Embolization in Women with Placenta

Accreta: Can It Prevent Cesarean Hysterectomy?


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


Sofiah 2009 Placenta Accreta: Clinical Risk Factors, Accuracy of Antenatal Diagnosis and Effect on Pregnancy Outcome


Shih 2009 Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale

and color Doppler techniques


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


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


Rosen 2008 Placenta Accreta and Cesarean Scar

Pregnancy: Overlooked Costs of the Rising

Cesarean Section Rate


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


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


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


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


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


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


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


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


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


Lam 2002 usa of magnetic resonance imaging and ultrasound in the antenatal diagnosis of placenta accreta


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).

Study or Subgroup

Gielchinski 2004Kim 2004Usta 2005Warshak 2006Bencaiova 2007Tantbirojn 2008Wong 2008Mok 2008El Behery 2010Lim 2011Sadashivaiah 2011Chantraine 2012Hannon 2012Kamara 2013Peker 2013Bowman 2013Klar 2013Weiniger 2013Laban 2014Tanimura 2014Zhou 2014Asicioglu 2014Bour 2014Alchalabi 2014Miller 2015Parra-Herran 2015Thiravit 2016Millischer 2017

Total (95% CI)

Heterogeneity: Tau² = 3.11; Chi² = 126.69, df = 27 (P < 0.00001); I² = 79%Test for overall effect: Z = 3.50 (P = 0.0005)

Mean

30.732.332.635.2

3036.333.3

3633.432.436.536.534.5

3234.232.832.534.630.535.332.329.336.134.735.7

3536

37.2

SD

4.54.34.83.85.55.55.61.55.63.5

33.52.95.54.45.65.44.11.83.82.65.24.55.36.16.5

43.2

Total

31034229

313895794

13126520

196161522615124616232544128

1224

Mean

30.631.7

3031.4

2933.833.931.533.835.229.426.735.5

3336

28.931.4

3529.4

3333

29.231.431.133.334.435.235.3

SD

43.55.84.56.36.15.73.35.82.8

45.71.3

55.56.75.84.62.75.8

45.6

54.75.55.85.24.2

Total

31022

32516

880811578

284994

10220

255332240504356

3181658

100179

12

13327

Weight

5.3%4.1%4.0%2.9%4.2%2.4%2.4%3.5%2.0%2.7%2.4%2.2%4.1%4.5%3.1%5.2%5.1%4.3%5.1%3.5%4.3%4.5%2.9%3.6%3.5%2.8%2.3%2.9%

100.0%

IV, Random, 95% CI

0.10 [-0.57, 0.77]0.60 [-1.46, 2.66]2.60 [0.50, 4.70]3.80 [0.48, 7.12]

1.00 [-0.94, 2.94]2.50 [-1.51, 6.51]

-0.60 [-4.55, 3.35]4.50 [1.86, 7.14]

-0.40 [-5.07, 4.27]-2.80 [-6.37, 0.77]7.10 [3.17, 11.03]9.80 [5.62, 13.98]-1.00 [-3.08, 1.08]-1.00 [-2.65, 0.65]-1.80 [-4.89, 1.29]

3.90 [3.07, 4.73]1.10 [0.05, 2.15]

-0.40 [-2.21, 1.41]1.10 [0.08, 2.12]

2.30 [-0.29, 4.89]-0.70 [-2.51, 1.11]0.10 [-1.52, 1.72]4.70 [1.40, 8.00]3.60 [1.12, 6.08]

2.40 [-0.22, 5.02]0.60 [-2.76, 3.96]0.80 [-3.28, 4.88]1.90 [-1.35, 5.15]

1.45 [0.64, 2.26]

Year

2004200420052006200720082008200820102011201120122012201320132013201320132014201420142014201420142015201520162017

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).

Study or Subgroup

Usta 2005Warshak 2006Bencaiova 2007Wong 2008Tantbirojn 2008Mok 2008Morita 2009El Behery 2010Sadashivaiah 2011Lim 2011Hannon 2012Chantraine 2012Weiniger 2013Bowman 2013Klar 2013Peker 2013Tanimura 2014Asicioglu 2014Bour 2014Laban 2014

Total (95% CI)

Heterogeneity: Tau² = 0.28; Chi² = 87.21, df = 19 (P < 0.00001); I² = 78%Test for overall effect: Z = 4.00 (P < 0.0001)

Mean

3.31.1

22.4

222

2.41.32.1

42.8

53.51.71.32.21.73.42.9

SD

2.41

1.21.11.50.50.51.10.50.5

20.9

31.51.10.81.50.92.70.6

Total

229

319

3853749

12135255

1612015461626

553

Mean

2.52.11.71.31.11.40.31.3

21.5

52.84.8

21.80.7

01.32.12.7

SD

2.51.80.91.31.20.50.31.31.50.82.52.13.32.51.20.80.81.41.50.5

Total

32516

8808571184

289449

4056

3222043

3181650

10148

Weight

4.1%3.9%7.0%5.1%4.9%6.3%5.9%4.5%3.9%4.9%1.1%2.7%3.2%5.3%7.8%6.6%5.1%7.5%2.6%7.6%

100.0%

IV, Random, 95% CI

0.80 [-0.24, 1.84]-1.00 [-2.10, 0.10]0.30 [-0.12, 0.72]1.10 [0.31, 1.89]0.90 [0.05, 1.75]0.60 [0.04, 1.16]1.70 [1.06, 2.34]1.10 [0.15, 2.05]

-0.70 [-1.80, 0.40]0.60 [-0.25, 1.45]

-1.00 [-3.70, 1.70]0.00 [-1.46, 1.46]0.20 [-1.11, 1.51]1.50 [0.73, 2.27]

-0.10 [-0.31, 0.11]0.60 [0.10, 1.10]2.20 [1.40, 3.00]0.40 [0.10, 0.70]

1.30 [-0.21, 2.81]0.20 [-0.07, 0.47]

0.60 [0.31, 0.90]

Year

20052006200720082008200820092010201120112012201220132013201320132014201420142014



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).

Study or Subgroup

Lim 2011Mok 2008Morita 2009Peker 2013Sadashivaiah 2011Tanimura 2014Warshak 2006Weiniger 2013Zhou 2014

Total (95% CI)

Heterogeneity: Tau² = 0.31; Chi² = 47.27, df = 8 (P < 0.00001); I² = 83%Test for overall effect: Z = 1.40 (P = 0.16)

Mean

1.32

0.331.05

11.80.82.51.3

SD

0.80.50.30.60.51.5

11.50.3

Total

953

204

159

5212

129

Mean

1.51

0.50.71.7

01.21.61.3

SD

0.80.30.50.8

10.50.51.30.3

Total

684

209

43164056

202

Weight

9.2%12.1%11.2%12.5%

9.3%9.7%

10.3%11.4%14.1%

100.0%

IV, Random, 95% CI

-0.20 [-1.03, 0.63]1.00 [0.51, 1.49]

-0.17 [-0.77, 0.43]0.35 [-0.09, 0.79]

-0.70 [-1.52, 0.12]1.80 [1.03, 2.57]

-0.40 [-1.10, 0.30]0.90 [0.33, 1.47]

0.00 [-0.19, 0.19]

0.30 [-0.12, 0.71]



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).

Study or Subgroup

Bowman 2013Collins 2015

Total (95% CI)

Heterogeneity: Tau² = 0.82; Chi² = 1.45, df = 1 (P = 0.23); I² = 31%Test for overall effect: Z = 1.35 (P = 0.18)

Mean

2926.1

SD

9.15.3

Total

5542

97

Mean

31.926.7

SD

6.95.4

Total

5647

103

Weight

39.9%60.1%

100.0%

IV, Random, 95% CI

-2.90 [-5.91, 0.11]-0.60 [-2.83, 1.63]

-1.52 [-3.73, 0.69]

Year

20132015



5

Figure S5. Results of the meta-analysis comparing the likelihood of AIP in women >35 years versus women ≤35 years.

Study or Subgroup

Usta 2005Wu 2005Warshak 2006Bencaiova 2007Tantbirojn 2008Mok 2008Hasegawa 2009Lim 2011Sadashivaiah 2011Fitzpatrick 2012Ueno 2013Eshkoli 2013Upson 2013Alchalabi 2014Thurn 2015Lyell 2015Millischer 2017

Total (95% CI)

Total eventsHeterogeneity: Tau² = 2.39; Chi² = 402.88, df = 16 (P < 0.00001); I² = 96%Test for overall effect: Z = 2.79 (P = 0.005)

Events

1136

57

263343

777

17011132493

6

499

Total

8170

91759

315

4665

13828

103282685

26355

12293313

138518

Events

1175

42412

2251

578

187128

1013

1122

653

Total

266380

167080

188

8178

25237

39327432184

55381

4826347

916688

Weight

6.5%6.8%5.3%6.5%5.8%4.3%5.1%4.4%3.8%6.9%6.1%7.0%6.7%6.3%6.7%7.0%4.9%

100.0%

M-H, Random, 95% CI

3.64 [1.52, 8.75]4.31 [2.53, 7.33]

3.75 [0.66, 21.25]1.17 [0.51, 2.73]

2.60 [0.66, 10.23]4.50 [0.41, 49.63]2.76 [0.44, 17.13]

0.80 [0.08, 8.47]10.50 [0.67, 165.11]

4.32 [2.76, 6.75]1.21 [0.38, 3.85]

35.18 [28.55, 43.34]1.03 [0.56, 1.91]

4.50 [1.61, 12.60]2.05 [1.03, 4.10]3.26 [2.48, 4.29]

2.14 [0.30, 15.35]

3.13 [1.40, 6.97]

Year

20052005200620072008200820092011201120122013201320132014201520152017

Age >35y Age <35y Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [Age >35y] Favours [Age <35y]

6

Figure S6. Results of the meta-analysis comparing the likelihood of AIP in obese versus non obese women.

Study or Subgroup

Fitzpatrick 2012Eshkoli 2013Ueno 2013Thurn 2015Lyell 2015

Total (95% CI)

Total eventsHeterogeneity: Tau² = 0.00; Chi² = 3.21, df = 4 (P = 0.52); I² = 0%Test for overall effect: Z = 2.25 (P = 0.02)

Events

2921

348

74

Total

78870

265426

93

66469

Events

102137

14162

27

442

Total

30233999

63452681

592

487637

Weight

28.4%3.9%0.9%

55.5%11.3%

100.0%

M-H, Random, 95% CI

1.16 [0.69, 1.95]0.57 [0.14, 2.30]

3.50 [0.21, 59.59]1.45 [1.00, 2.10]1.97 [0.87, 4.48]

1.37 [1.04, 1.81]

Year

20122013201320152015

Obese Non obese Odds Ratio Odds RatioM-H, Random, 95% CI

0.02 0.1 1 10 50Favours [Obese] Favours [Non obese]

7

Figure S7. Results of the meta- comparing the likelihood of AIP in smokers versus non smokers women.

Study or Subgroup

Usta 2005Lim 2011Fitzpatrick 2012Eshkoli 2013Ueno 2013Upson 2013Klar 2013Bowman 2013Kamara 2013Thurn 2015Lyell 2015

Total (95% CI)


Events

90

2621

8021352312

0

209

Total

741

65558

366969

67445

5861889

7

130136

Events

139

108137

14277140160

42193

37

1130

Total

27312

32534311

62336633

4162299

109543678

726

918844

Weight

6.5%0.6%

12.6%3.0%1.0%

23.2%12.4%18.0%10.2%11.7%0.8%

100.0%

M-H, Random, 95% CI

2.77 [1.13, 6.76]0.12 [0.00, 3.78]1.34 [0.77, 2.32]0.90 [0.22, 3.63]

1.71 [0.14, 20.33]1.45 [1.13, 1.86]0.90 [0.52, 1.57]1.14 [0.78, 1.67]1.05 [0.55, 2.01]0.55 [0.30, 0.98]

1.23 [0.07, 21.87]

1.13 [0.88, 1.47]

Year

20052011201220132013201320132013201320152015

Smokers Non smokers Odds Ratio Odds RatioM-H, Random, 95% CI

0.01 0.1 1 10 100Favours [Smokers] Favours [Non smokers]

8

Figure S8. Results of the meta- comparing the likelihood of AIP in multiparous versus primiparous women.

Study or Subgroup

Gielchinski 2004Usta 2005Warshak 2006Bencaiova 2007Mok 2008Tantbirojn 2008Morita 2009Sadashivaiah 2011Lim 2011Fitzpatrick 2012Kamara 2013Upson 2013Bowman 2013Alchalabi 2014Parra-Herran 2015Miller 2015Lyell 2015Collins 2015Thurn 2015

Total (95% CI)

Total eventsHeterogeneity: Tau² = 0.37; Chi² = 73.76, df = 18 (P < 0.00001); I² = 76%Test for overall effect: Z = 4.79 (P < 0.00001)

Events

23162

182

11103

8328

7832031

8301542

621

Total

46254

63977

312

134

14980

1632558433529

47023

38862

46403

Events

7916

713

327

246

5137

350113

31317

727

163

938

Total

158293

194134

10376

109

24187

4019702191

382696

26666

566705

976362

Weight

8.9%5.8%2.7%7.1%1.5%2.3%1.0%1.2%1.6%8.5%7.6%6.9%9.1%4.4%4.5%5.8%6.5%5.8%8.9%

100.0%

M-H, Random, 95% CI

1.00 [0.70, 1.44]2.16 [0.81, 5.81]0.86 [0.12, 5.94]1.44 [0.71, 2.95]

4.67 [0.30, 73.38]4.07 [0.46, 35.75]

5.40 [0.15, 188.83]0.21 [0.01, 5.05]

1.50 [0.11, 21.31]4.69 [3.00, 7.33]0.73 [0.39, 1.36]

4.94 [2.34, 10.46]3.21 [2.38, 4.34]

10.14 [2.70, 38.08]7.75 [2.12, 28.28]1.77 [0.67, 4.66]2.52 [1.09, 5.83]2.71 [1.01, 7.28]3.76 [2.68, 5.28]

2.49 [1.71, 3.61]

Year

2004200520062007200820082009201120112012201320132013201420152015201520152015

Multiparous Primiparous Odds Ratio Odds RatioM-H, Random, 95% CI

0.01 0.1 1 10 100Favours [Multiparous] Favours [Primiparous]

9

Figure S9. Results of the meta- comparing the likelihood of AIP in women with versus women without a diagnosis of placenta previa.

Study or Subgroup

Gielchinski 2004Warshak 2006Bencaiova 2007Wong 2007Tantbirojn 2008Dwyer 2008Morita 2009El Behery 2010Lim 2011Derman 2011Fitzpatrick 2012Hannon 2012Upson 2013Weiniger 2013Bowman 2013Eshkoli 2013Noda 2014Zhou 2014Bour 2014Collins 2015Miller 2015Thurn 2015Parra-Herran 2015Thiravit 2016

Total (95% CI)


Events

7553

19113293

869

464691737

12163911

1003110

644

Total

714

109332021

59

118

8911

199052

1411045

2233196314

14893318

5256

Events

3034

262

1940501

473

311289466

0003

1410513

2

1050

Total

61311

87303

2911

226

29

3005

40161240

244933824

6351326

111604078

283

1051966

Weight

3.3%4.4%5.0%3.5%4.0%4.6%2.8%4.2%2.9%3.6%4.8%3.8%5.3%4.9%5.3%5.3%3.2%3.3%3.2%4.7%4.7%5.3%4.5%3.6%

100.0%

M-H, Random, 95% CI

15.35 [0.87, 269.87]0.97 [0.19, 5.03]

16.09 [6.06, 42.73]0.05 [0.00, 0.73]

10.00 [1.16, 86.00]1.93 [0.43, 8.61]

7.00 [0.22, 218.95]1.20 [0.19, 7.63]

19.00 [0.67, 536.55]4.80 [0.38, 59.89]

154.31 [46.83, 508.51]3.00 [0.28, 31.63]

30.53 [22.33, 41.75]3.29 [1.11, 9.74]

45.60 [30.51, 68.15]38.41 [27.37, 53.91]6.29 [0.31, 127.06]

41.28 [2.32, 733.15]127.29 [6.03, 2685.63]

12.46 [3.37, 46.00]25.40 [6.30, 102.42]

414.12 [313.34, 547.32]17.88 [3.57, 89.59]

0.63 [0.05, 8.20]

11.03 [4.71, 25.83]

Year

200420062007200720082008200920102011201120122012201320132013201320142014201420152015201520152016

Placenta previa No placenta previa Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [Placenta previa] Favours [Normal placenta]

10

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.

Study or Subgroup

Usta 2005Warshak 2006Dwyer 2008Hasegawa 2009Morita 2009Lim 2011Sadashivaiah 2011Cali 2013Asicioglu 2014Bour 2014Thurn 2015Collins 2015

Total (95% CI)


Events

173

103183

4134163430

200

Total

819

151019

1111817719

42141

912

Events

56522110

120

8512

131

Total

2661617

117642

6918713

42735048

428095

Weight

9.0%8.6%8.8%8.5%7.1%7.6%7.6%7.8%9.1%7.6%9.2%9.0%

100.0%

M-H, Random, 95% CI

13.87 [4.93, 38.99]0.83 [0.15, 4.64]

4.80 [1.07, 21.45]24.64 [3.52, 172.36]5.40 [0.15, 188.83]

24.00 [1.11, 518.58]0.38 [0.02, 8.10]

74.43 [4.49, 1232.85]3.47 [1.73, 6.94]

127.29 [6.03, 2685.63]441.62 [293.07, 665.45]

8.18 [3.16, 21.17]

12.02 [1.64, 87.99]

Year

200520062008200920092011201120132014201420152015

Placenta previa+CS No placenta previa+CS Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [Previa+CS] Favours [No previa+CS]

11

Figure S11. Results of the meta- comparing the likelihood of AIP in women with versus women without ≥1 previous cesarean section.

Study or Subgroup

Chou 2000Gielchinski 2004Usta 2005Warshak 2006Japarai 2007Bencaiova 2007Wong 2007Mok 2008Tantbirojn 2008Hasegawa 2009Morita 2009El Behery 2010Sadashivaiah 2011Lim 2011Fitzpatrick 2012Hannon 2012Chantraine 2012Eshkoli 2013Cali 2013Klar 2013Bowman 2013Ueno 2013Bour 2014Asicioglu 2014Laban 2014Alchalabi 2014Noda 2014Parra-Herran 2015Lyell 2015Collins 2015Thurn 2015Miller 2015Thiravit 2016

Total (95% CI)


Events

71517

67645

2731338

1131112

1044119

1691116342623

5332540

1041512

925

Total

4030811720

153712122910

2161111

1501317

15211118

601581

1926

17753441041

21777

607346319

80458

Events

7295

530

2510

1122411

2111

350

14226

40

12002

1112

2101

100

737

Total

40590266

80

730224

120

1175

1922

23935

1965869

4231152

466

18723371820

51912

54483362

2

575710

Weight

3.9%4.7%4.1%2.9%

4.4%2.1%1.3%3.0%2.6%1.3%3.0%1.4%1.4%4.9%1.6%2.0%5.2%1.6%4.9%5.2%3.5%1.5%4.8%1.6%1.6%2.6%3.9%4.7%3.1%5.3%4.4%1.4%

100.0%

M-H, Random, 95% CI

1.00 [0.32, 3.17]1.00 [0.48, 2.08]

13.87 [4.93, 38.99]0.91 [0.16, 5.20]

Not estimable1.14 [0.47, 2.79]

11.50 [1.11, 118.71]2.20 [0.07, 64.90]

11.05 [2.05, 59.56]24.64 [3.52, 172.36]

1.50 [0.06, 40.63]0.87 [0.16, 4.60]0.38 [0.02, 8.10]

2.67 [0.12, 57.62]31.70 [17.72, 56.72]11.00 [0.65, 187.17]

9.60 [0.85, 108.72]3.86 [2.63, 5.66]

74.43 [4.49, 1232.85]0.92 [0.51, 1.64]5.18 [3.40, 7.89]

14.44 [3.66, 56.91]20.43 [1.04, 401.67]

3.47 [1.73, 6.94]45.29 [2.62, 784.15]

81.98 [4.74, 1418.44]8.00 [1.17, 54.72]3.38 [1.05, 10.89]5.50 [2.71, 11.17]5.41 [1.11, 26.31]9.25 [7.03, 12.17]

1.63 [0.67, 3.96]8.33 [0.35, 198.09]

4.66 [3.02, 7.18]

Year

200020042005200620072007200720082008200920092010201120112012201220122013201320132013201320142014201420142014201520152015201520152016

≥1 previous CS No previous CS Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [ ≥1 previous CS] Favours [No previous CS]

12

Figure S12. Results of the meta- comparing the likelihood of AIP in women with versus women without ≥1 previous elective cesarean section.

Study or Subgroup

Kamara 2013Asicioglu 2014Thurn 2015

Total (95% CI)


Events

3025

114

169

Total

49213

43720

43982

Events

35211

91

337

Total

156527

649059

649742

Weight

33.1%33.4%33.5%

100.0%

M-H, Random, 95% CI

5.46 [2.75, 10.85]0.20 [0.13, 0.31]

18.64 [14.15, 24.56]

2.73 [0.09, 80.27]

Year

201320142015

Elective CS No elective CS Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [Elective CS] Favours [No elective CS]

13

Figure S13. Results of the meta- comparing the likelihood of AIP in women with versus women without ≥1 previous emergency cesarean section.

Study or Subgroup

Kamara 2013Asicioglu 2014Thurn 2015

Total (95% CI)


Events

352171

127

Total

118151

61950

62219

Events

3025

134

189

Total

49213

543617

543879

Weight

32.7%33.1%34.2%

100.0%

M-H, Random, 95% CI

0.27 [0.13, 0.54]1.21 [0.65, 2.26]4.65 [3.49, 6.21]

1.17 [0.21, 6.65]

Year

201320142015

Emergency CS No emergency CS Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [Emergency CS] Favours [No emergency CS]

14

Figure S14. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous myomectomy.

Study or Subgroup

Wu 2005Warshak 2006Japarai 2007Wong 2007Tantbirojn 2008Cali 2013Parra-Herran 2015Collins 2015Thiravit 2016

Total (95% CI)


Events

010020221

8

Total

41112

46353

66

Events

111875

3641424011

301

Total

44624193547

141588418

872

Weight

10.0%8.2%8.1%8.1%9.1%

10.8%13.2%20.2%12.3%

100.0%

M-H, Random, 95% CI

0.33 [0.02, 6.26]5.82 [0.21, 158.82]

0.56 [0.02, 15.46]1.85 [0.07, 51.48]1.58 [0.07, 35.25]0.03 [0.00, 0.43]0.76 [0.06, 8.99]0.73 [0.12, 4.62]0.32 [0.02, 4.20]

0.57 [0.21, 1.59]

Year

200520062007200720082013201520152016

Myomectomy No myomectomy Odds Ratio Odds RatioM-H, Random, 95% CI

0.005 0.1 1 10 200Favours [Myomectomy] Favours [No myomectomy]

15

Figure S15. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous uterine surgery.

Study or Subgroup

Chou 2000Gielchinski 2004Usta 2005Warshak 2006Bencaiova 2007Wong 2007Dwyer 2008Tantbirojn 2008Mok 2008Hasegawa 2009Morita 2009El Behery 2010Lim 2011Sadashivaiah 2011Chantraine 2012Hannon 2012Fitzpatrick 2012Cali 2013Klar 2013Upson 2013Eshkoli 2013Ueno 2013Asicioglu 2014Bour 2014Alchalabi 2014Noda 2014Laban 2014Thurn 2015Lyell 2015Collins 2015Parra-Herran 2015Miller 2015Thiravit 2016Pilloni 2016

Total (95% CI)


Events

71517764

1230531383

1212

113411994

104113416235

26104254239151225

893

Total

40308118

153712263212102

1611111714

15011860

3701915211

1917726441053

6073421782506319

161

116082

Events

7295

52

2513802241110

210

142263354

120020

1011205

100

12

976

Total

40590266

77302

246

171

1175

192252

23969

42336658319658

46187

6371823

544833519

711622

153

941281

Weight

3.7%4.6%4.0%2.4%4.3%1.9%2.6%2.7%1.1%2.4%1.2%2.8%1.3%1.3%1.8%1.1%4.8%1.5%4.8%5.3%5.1%3.3%4.6%1.4%1.4%2.4%1.4%5.3%4.6%1.4%3.3%4.3%1.2%4.6%

100.0%

M-H, Random, 95% CI

1.00 [0.32, 3.17]1.00 [0.48, 2.08]

13.87 [4.93, 38.99]1.59 [0.24, 10.57]1.14 [0.47, 2.79]

11.50 [1.11, 118.71]0.86 [0.15, 5.06]

16.88 [3.02, 94.17]2.20 [0.07, 64.90]

24.64 [3.52, 172.36]1.50 [0.06, 40.63]0.87 [0.16, 4.60]

2.67 [0.12, 57.62]0.38 [0.02, 8.10]

9.60 [0.85, 108.72]25.00 [0.90, 695.79]31.70 [17.72, 56.72]

74.43 [4.49, 1232.85]0.92 [0.51, 1.64]3.55 [2.80, 4.49]3.86 [2.63, 5.66]

14.44 [3.66, 56.91]3.47 [1.73, 6.94]

20.43 [1.04, 401.67]81.98 [4.74, 1418.44]

8.00 [1.17, 54.72]45.29 [2.62, 784.15]

9.25 [7.03, 12.17]5.50 [2.71, 11.17]

15.74 [0.87, 284.61]4.25 [1.09, 16.62]1.63 [0.67, 3.96]

8.33 [0.35, 198.09]2.16 [1.04, 4.47]

4.42 [2.96, 6.59]

Year

2000200420052006200720072008200820082009200920102011201120122012201220132013201320132013201420142014201420142015201520152015201520162016

Uterine surgery No uterine surgery Odds Ratio Odds RatioM-H, Random, 95% CI

0.002 0.1 1 10 500Favours [Uterine surgery] Favours [No uterine surgery]

16

Figure S16. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous abortion.

Study or Subgroup

Wu 2005Eshkoli 2013Kamara 2013Klar 2013Alchalabi 2014Parra-Herran 2015

Total (95% CI)


Events

520

23711122

179

Total

1762550

651742628

3019

Events

5913942901222

364

Total

27432319

1023095533

33092

Weight

25.6%2.7%

20.5%26.6%13.4%11.2%

100.0%

M-H, Random, 95% CI

1.53 [0.99, 2.36]0.05 [0.00, 0.73]0.78 [0.41, 1.49]1.68 [1.14, 2.48]2.63 [0.96, 7.20]1.83 [0.58, 5.83]

1.36 [0.84, 2.20]

Year

200520132013201320142015

Abortion No Abortion Odds Ratio Odds RatioM-H, Random, 95% CI

0.01 0.1 1 10 100Favours [Abortion] Favours [No abortion]

17

Figure S17. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous curettage.

Study or Subgroup

Wu 2005Bencaiova 2007Japarai 2007Wong 2007Tantbirojn 2008El Behery 2010Lim 2011Chantraine 2012Cali 2013Klar 2013Weiniger 2013Asicioglu 2014Miller 2015Collins 2015Parra-Herran 2015Thiravit 2016

Total (95% CI)


Events

271440

151190

593238111353

232

Total

138374111916

419

2314653

2482322

75

1099

Events

841735

23684

41102

208

1429399

412

Total

3128465

91733311213

16433739

116102675416

9787

Weight

9.4%8.9%5.6%3.3%4.9%4.3%2.8%3.2%3.6%9.6%8.6%8.7%8.1%8.2%5.9%5.1%

100.0%

M-H, Random, 95% CI

0.66 [0.40, 1.08]19.33 [9.45, 39.51]

1.14 [0.18, 7.28]0.06 [0.00, 1.15]

6.52 [0.76, 56.33]1.39 [0.12, 15.81]1.59 [0.05, 47.52]

40.11 [1.89, 852.92]0.06 [0.00, 1.07]1.56 [1.04, 2.34]1.45 [0.63, 3.34]2.44 [1.10, 5.42]

5.76 [2.13, 15.56]1.89 [0.71, 5.03]0.96 [0.17, 5.50]1.17 [0.15, 9.01]

1.87 [0.96, 3.64]

Year

2005200720072007200820102011201220132013201320142015201520152016

Curettage No curettage Odds Ratio Odds RatioM-H, Random, 95% CI

0.01 0.1 1 10 100Favours [Curettage] Favours [No curettage]

18

Figure S18. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous IVF.

Study or Subgroup

Esh-Broder 2011Fitzpatrick 2012Ueno 2013Eshkoli 2013Klar 2013Thurn 2015Collins 2015

Total (95% CI)


Events

12538

10103

51

Total

7646

151433

2712153

4

14402

Events

3012612

13115110939

598

Total

24471379

5033436

456415618

85

474495

Weight

17.6%9.0%

13.0%17.4%16.9%17.7%8.4%

100.0%

M-H, Random, 95% CI

13.00 [6.63, 25.49]10.04 [1.16, 86.85]

0.79 [0.19, 3.28]1.43 [0.70, 2.92]1.19 [0.53, 2.66]3.14 [1.64, 6.00]

3.54 [0.35, 35.40]

2.80 [1.16, 6.76]

Year

2011201220132013201320152015

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)


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

0.01 0.1 1 10 100Favours [<23 months] Favours [≥23 months]

20

Figure S20. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous manual extraction of the placenta.

Study or Subgroup

Wong 2007Hannon 2012Miller 2015

Total (95% CI)


Events

010

1

Total

113

5

Events

51125

41

Total

3515

122

172

Weight

31.2%30.2%38.5%

100.0%

M-H, Random, 95% CI

1.85 [0.07, 51.48]1.17 [0.04, 34.52]0.55 [0.03, 10.92]

1.01 [0.16, 6.47]

Year

200720122015

Manual extraction No manual extraction Odds Ratio Odds RatioM-H, Random, 95% CI

0.002 0.1 1 10 500Favours [Manual extraction] Favours [No Manual extraction]

21

Figure S21. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous uterine incision.

Study or Subgroup

Fitzpatrick 2012

Total (95% CI)

Total eventsHeterogeneity: Not applicableTest for overall effect: Z = 0.01 (P = 0.99)

Events

1

1

Total

1

1

Events

105

105

Total

139

139

Weight

100.0%

100.0%

M-H, Random, 95% CI

0.98 [0.04, 24.64]

0.98 [0.04, 24.64]

Year

2012

Uterine incision No uterine incision Odds Ratio Odds RatioM-H, Random, 95% CI

0.001 0.1 1 10 1000Favours [Uterine incision] Favours [No Uterine incision]

22

Figure S22. Results of the meta- comparing the likelihood of AIP in women with versus women without a previous endometrial ablation.

Study or Subgroup

Collins 2015

Total (95% CI)

Total eventsHeterogeneity: Not applicableTest for overall effect: Z = 0.75 (P = 0.45)

Events

1

1

Total

1

1

Events

41

41

Total

88

88

Weight

100.0%

100.0%

M-H, Random, 95% CI

3.43 [0.14, 86.59]

3.43 [0.14, 86.59]

Year

2015

Ablation No ablation Odds Ratio Odds RatioM-H, Random, 95% CI

0.001 0.1 1 10 1000Favours [Ablation] Favours [No ablation]

23

Figure S23. Funnel plot of the effect estimates vs their standard errors (outcome: maternal age).

-50 0 50 10025

20

15

10

5

0

Effect size

Standard error

Bias assessment plot

Egger: bias = 0.667937 (95% CI = -0.804926 to 2.140799) P = 0.3598

24

Figure S24. Funnel plot of the effect estimates vs their standard errors (outcome: parity).

-40 -20 0 20 4012,5

10,0

7,5

5,0

2,5

0,0

Effect size

Standard error


Egger: bias = 1.478759 (95% CI = -0.342425 to 3.299942) P = 0.1052

25

Figure S25. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: maternal age >35 years).

-2 0 2 4 61,5

1,0

0,5

0,0

Log(Odds ratio)

Standard error


Egger: bias = -3.633327 (95% CI = -6.890699 to -0.375956) P = 0.0312

26

Figure S26. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: current smoking).

Egger: bias = -0.676657 (95% CI = -2.111194 to 0.757879) P = 0.3137

27

Figure S27. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: multiparity).

Egger: bias = -0.108188 (95% CI = -1.800274 to 1.583897) P = 0.8943

28

Figure S28. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: diagnosis of placenta previa).

-3,0 -0,5 2,0 4,5 7,0 9,52,5

2,0

1,5

1,0

0,5

0,0

Log(Odds ratio)

Standard error


Egger: bias = -2.971904 (95% CI = -5.011173 to -0.932634) P = 0.0063

29

Figure S29. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor:≥1 previous CS).

-5,0 -2,5 0,0 2,5 5,0 7,52,5

2,0

1,5

1,0

0,5

0,0

Log(Odds ratio)

Standard error


Egger: bias = -0.288971 (95% CI = -1.598341 to 1.020398) P = 0.6554

30

Figure S30. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: previous uterine surgery).

-5,0 -2,5 0,0 2,5 5,0 7,52,5

2,0

1,5

1,0

0,5

0,0

Log(Odds ratio)


Egger: bias = -0.010543 (95% CI = -1.206695 to 1.185609) P = 0.9858

31

Figure S31. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: previous placenta previa + cesarean section).

-3 0 3 6 92,4

2,0

1,6

1,2

0,8

0,4

0,0

Log(Odds ratio)

Standard error


Egger: bias = -3.593153 (95% CI = -7.787928 to 0.601622) P = 0.0854

32

Figure S32. Funnel plot of the logarithm of the odds ratios vs their standard errors (predictor: previous curettage).

-6,0 -3,5 -1,0 1,5 4,0 6,53

2

1

0

Log(Odds ratio)


Egger: bias = 0.222797 (95% CI = -1.869905 to 2.3155) P = 0.8227

risk factors for abnormally invasive placenta: a

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