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Special Report of the Society for Maternal- Fetal Medicine Placenta Accreta Spectrum Ultrasound Marker Task Force: Consensus on denition of markers and approach to the ultrasound examination in pregnancies at risk for placenta accreta spectrum Scott A. Shainker, DO, MS; Beverly Coleman, MD, FACR; Ilan E. Timor, MD; Amarnath Bhide, MRCOG, MD; Bryann Bromley, MD; Alison G. Cahill, MD, MSCI; Manisha Gandhi, MD; Jonathan L. Hecht, MD, PhD; Katherine M. Johnson, MD; Deborah Levine, MD; Joan Mastrobattista, MD; Jennifer Philips, MD; Lawrence J. Platt, MD; Alireza A. Shamshirsaz, MD; Thomas D. Shipp, MD; Robert M. Silver, MD; Lynn L. Simpson, MD; Joshua A. Copel, MD; Alfred Abuhamad, MD; On behalf of the Society for Maternal-Fetal Medicine The Society for Maternal Fetal Medicine (SMFM), American Institute of Ultrasound in Medicine (AIUM), American College of Radiologists (ACR), and Gottesfeld Hohler Memorial Society (GOHO) endorse this document. The American College of Obstetricians and Gynecologists (ACOG) and International Society of Ultrasound In Obstetrics and Gynecology (ISUOG) support this document. The Society of Radiologists in Ultrasound (SRU) approves this document. Placenta accreta spectrum includes the full range of abnormal placental attachment to the uterus or other structures, encompassing placenta accreta, placenta increta, placenta percreta, morbidly adherent placenta, and invasive placentation. The incidence of placenta accreta spectrum has increased in recent years, largely driven by increasing rates of cesarean delivery. Prenatal detection of placenta accreta spectrum is primarily made by ultrasound and is important to reduce maternal morbidity associated with the condition. Despite a large body of research on various placenta accreta spectrum ultrasound markers and their screening performance, inconsistencies in the literature persist. In response to the need for stan- dardizing the denitions of placenta accreta spectrum markers and the approach to the ultrasound ex- amination, the Society for Maternal-Fetal Medicine convened a task force with representatives from the American Institute of Ultrasound in Medicine, the American College of Obstetricians and Gynecologists, the American College of Radiology, the International Society of Ultrasound in Obstetrics and Gynecology, the Society for Radiologists in Ultrasound, the American Registry for Diagnostic Medical Sonography, and the Gottesfeld-Hohler Memorial Ultrasound Foundation. The goals of the task force were to assess placenta accreta spectrum sonographic markers on the basis of available data and expert consensus, provide a standardized approach to the prenatal ultrasound evaluation of the uterus and placenta in pregnancies at risk of placenta accreta spectrum, and identify research gaps in the eld. This manuscript provides infor- mation on the Placenta Accreta Spectrum Task Force process and ndings. Key words: accreta, cesarean, increta, maternal morbidity, maternal mortality, placenta accreta spectrum, percreta, previa Introduction Placenta accreta spectrum (PAS), encompassing the terms placenta accreta, placenta increta, placenta percreta, morbidly adherent placenta, and invasive placentation, in- cludes the full range of abnormal placental attachment to the uterus or other structures. There has been a dramatic rise in the incidence of PAS over recent years. 1 This rise is most notably driven by increasing rates of cesarean delivery. The risk is highest in the presence of placenta previa and previous cesarean deliveries. 1,2 Corresponding author: Society for Maternal-Fetal Medicine, Publications Committee. [email protected] B2 JANUARY 2021 SMFM Special Report smfm.org

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Page 1: SMFM Special Report

SMFM Special Report

smfm.org

Special Report of the Society for Maternal-

Fetal Medicine Placenta Accreta Spectrum Ultrasound Marker Task Force: Consensus ondefinition of markers and approach to theultrasound examination in pregnancies at risk forplacenta accreta spectrum Scott A. Shainker, DO, MS; Beverly Coleman, MD, FACR; Ilan E. Timor, MD; Amarnath Bhide, MRCOG, MD;Bryann Bromley, MD; Alison G. Cahill, MD, MSCI; Manisha Gandhi, MD; Jonathan L. Hecht, MD, PhD;Katherine M. Johnson, MD; Deborah Levine, MD; Joan Mastrobattista, MD; Jennifer Philips, MD; Lawrence J. Platt, MD;Alireza A. Shamshirsaz, MD; Thomas D. Shipp, MD; Robert M. Silver, MD; Lynn L. Simpson, MD; Joshua A. Copel, MD;Alfred Abuhamad, MD; On behalf of the Society for Maternal-Fetal Medicine

CoCo

B2

The Society for Maternal Fetal Medicine (SMFM), American Institute of Ultrasound in Medicine (AIUM), American College ofRadiologists (ACR), and Gottesfeld Hohler Memorial Society (GOHO) endorse this document. The American College ofObstetricians and Gynecologists (ACOG) and International Society of Ultrasound In Obstetrics and Gynecology (ISUOG)support this document. The Society of Radiologists in Ultrasound (SRU) approves this document.

rrespondinmmittee. p

JANUARY

Placenta accreta spectrum includes the full range of abnormal placental attachment to the uterus or other

structures, encompassing placenta accreta, placenta increta, placenta percreta, morbidly adherentplacenta, and invasive placentation. The incidence of placenta accreta spectrum has increased in recentyears, largely driven by increasing rates of cesarean delivery. Prenatal detection of placenta accretaspectrum is primarilymade by ultrasound and is important to reducematernalmorbidity associatedwith thecondition. Despite a large body of research on various placenta accreta spectrum ultrasound markers andtheir screening performance, inconsistencies in the literature persist. In response to the need for stan-dardizing the definitions of placenta accreta spectrum markers and the approach to the ultrasound ex-amination, the Society for Maternal-Fetal Medicine convened a task force with representatives from theAmerican Institute of Ultrasound inMedicine, the AmericanCollege of Obstetricians andGynecologists, theAmerican College of Radiology, the International Society of Ultrasound in Obstetrics and Gynecology, theSociety for Radiologists in Ultrasound, the American Registry for Diagnostic Medical Sonography, and theGottesfeld-Hohler Memorial Ultrasound Foundation. The goals of the task force were to assess placentaaccreta spectrum sonographic markers on the basis of available data and expert consensus, provide astandardized approach to the prenatal ultrasound evaluation of the uterus and placenta in pregnancies atrisk of placenta accreta spectrum, and identify research gaps in the field. This manuscript provides infor-mation on the Placenta Accreta Spectrum Task Force process and findings.

Key words: accreta, cesarean, increta, maternal morbidity, maternal mortality, placenta accretaspectrum, percreta, previa

Introduction morbidly adherent placenta, and invasive placentation, in-

Placenta accreta spectrum (PAS), encompassing the termsplacenta accreta, placenta increta, placenta percreta,

g author: Society for Maternal-Fetal Medicine, [email protected]

2021

cludes the full range of abnormal placental attachment to theuterus or other structures. There has been a dramatic rise inthe incidence of PAS over recent years.1 This rise is mostnotably driven by increasing rates of cesarean delivery. Therisk is highest in the presence of placenta previa and previouscesarean deliveries.1,2

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TABLE 1Task force participating members and societies

Alfred Abuhamad SMFM, Co-Chair

Scott A. Shainker SMFM, Co-Chair

Beverly Coleman ACR

Ilan E. Timor GOHO

Amarnath Bhide ISUOG

Bryann Bromley AIUM

Alison G. Cahill ACOG

Joshua A. Copel GOHO

Manisha Ghandi ACOG

Jonathan L. Hechta

Katherine M. Johnson SMFM

Deborah Levine SRU

Joan Mastrobattista AIUM

Jennifer Philips SMFM

Lawrence J. Platt GOHO

Alireza A. Shamshirsaz GOHO

Thomas D. Shipp ARDMS

Robert M. Silver SMFM

Lynn L. Simpson SMFM

ACOG, American College of Obstetricians and Gynecologists; ACR, American College ofRadiologists; AIUM, American Institute of Ultrasound in Medicine; ARDMS, American Reg-istry for Diagnostic Medical Sonography; GOHO, Gottesfeld-Hohler Memorial Society; ISUOG,International Society of Ultrasound in Obstetrics and Gynecology; SMFM, Society forMaternal-Fetal Medicine; SRU, Society of Radiologists in Ultrasound.

a Pathology consultant, Department of Pathology, Beth Israel Deaconess Medical Center andHarvard Medical School, Boston, MA.

Shainker. Special Report of the SMFM: Definition of markers and ultrasound ex-amination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

smfm.org SMFM Special Report

PAS is associated with a marked increase in maternalmorbidity and mortality. The morbidity is primarily related tomassive hemorrhage with associated organ damage, ce-sarean hysterectomy, and need for critical care re-sources.1,2 Prenatal detection of PAS allows formobilizationof multidisciplinary care teams and surgical planning, whichreduces maternal morbidity.3e8 Furthermore, the ability tocorrectly stratify the risk of PAS, including decreasing therisk with a “normal” ultrasound, reduces the possibility ofiatrogenic complications associated with planned prema-ture delivery, preoperative invasive procedures, and patientand provider anxiety.The prenatal detection and risk stratification for PAS are

primarily made by ultrasound. However, ultrasound is anoperator-dependent imaging modality with substantialvariability in image quality among providers. Furthermore,placental location and challenging imaging conditions,including elevated body mass index (BMI) or posteriorplacentation, may impede the sonographic detection ofPAS markers. There has been limited consensus on theoptimal approach to the ultrasound evaluation of patients atrisk of PAS, such as the appropriate timing of screening,need for transvaginal ultrasound (TVUS) imaging, use ofcolor and pulsedDoppler, angle of placental insonation, andequipment settings.Despite a large body of literature on various PAS ultra-

sound markers and their screening performance, importantinconsistencies in screening results persist. This is primarilybecause of the retrospective design of most studies, lack ofstandardized definitions of PAS markers, lack of agreementon the optimal gestational age for assessment, and in-consistencies in the approach to the ultrasound evaluationof the placenta.9 Furthermore, patients’ a priori risks have asignificant influence on the positive predictive value (PPV) ofPAS markers. Recent data have shown that these markersare frequently present in women at low risk for PAS.10

In response to the need for standardizing the defini-tions of PAS markers and the approach to the ultra-sound examination, the Society for Maternal-FetalMedicine (SMFM) convened a task force with the goalsof assessing PAS sonographic markers on the basis ofavailable data and expert consensus, providing a stan-dardized approach to the prenatal ultrasound evaluationof the uterus and placenta in pregnancies at risk ofPAS, and identifying research gaps in the field. Thismanuscript provides information on the PAS Task Forceprocess and outcomes.

ProcedureSMFM invited representatives from theAmerican Institute ofUltrasound in Medicine (AIUM), American College of Ob-stetricians and Gynecologists (ACOG), American College ofRadiology (ACR), International Society of Ultrasound inObstetrics and Gynecology (ISUOG), Society for Radiolo-gists in Ultrasound (SRU), American Registry for DiagnosticMedical Sonography (ARDMS), and Gottesfeld-Hohler

Memorial Ultrasound Foundation (GOHO) to the PAS TaskForce (Table 1). The PAS Task Force was organized into 4subcommittees: first-trimester markers, placental lacunae,uteroplacental interface, and uterovesical interface, whichalso included miscellaneous markers (cervical invasion,placental bulge, and exophytic mass). Each subcommitteewas chaired by a PAS Task Force member and included atleast 2 additional members. The authors S.A.S. and A.A.participated on all 4 subcommittees. Each subcommitteeperformed a detailed literature review of respectivemarkers.This included the definitions of each marker, indication forthe examination, reported diagnostic accuracy of eachmarker, gestational age at assessment, and optimal ultra-sound approach for evaluation.6,7,11e42 The task force helda face-to-face meeting in December 2018 in Boston, MA, toreview each subcommittee’s findings and recommenda-tions. Expert consensus opinion was obtained when avail-able data could not provide clear definitions for each PASmarker and/or the optimal approach for screening. In addi-tion, research gaps were noted.

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FIGURE 1Placenta lacunae

Grayscale imaging of placenta lacunae (asterisk) in the setting of placenta previa with placenta accreta spectrum. A, Transvaginal midline sagittal image.B, Transabdominal midline sagittal image.Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

SMFM Special Report smfm.org

Literature ReviewAs outlined in a recent Obstetrics Care Consensus, ultra-sound is the primary screening modality for PAS.7 Ultra-sound markers of PAS can be seen early in the firsttrimester, although historically screening is predominantlyperformed in the second and third trimesters of pregnancy.The ultrasound marker with the strongest association withPAS is a persistent placenta previa at the time of delivery, inthe setting of a previous cesarean delivery.5,43 Other classicsonographic markers of PAS include the presence ofplacental lacunae (Figure 1), loss of the retroplacentalhypoechoic zone (Figure 2), thinning of the retroplacentalmyometrium (Figure 3), hypervascularity of the uterovesicleor retroplacental space (Figure 4), extension of placentaltissue into the uterus and/or bladder, and placental bridgingvessels (Figures 5 and 6).11,39e41,44e46 The presence ofexcessive color Doppler flow in the retroplacental spacealong with abnormal placental bridging vessels has alsobeen associated with PAS (Figure 6).6,7,46,47

FIGURE 2Retroplacental hypoechoic zone

Transvaginal midline sagittal grayscale imaging of placenta previa. A, Normalthe retroplacental hypoechoic zone (arrows) in placenta accreta spectrum.

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Task force members identified several significant limita-tions to the current literature on this subject. Most studiesare retrospective in design, lack control “low-risk” com-parison groups, and do not provide clear definitions of thePAS markers being studied, which limits the ability to makecomparisons among studies and combines many of thereported diagnostic performance statistics.9 It is importantto note that most studies were designed to highlight asso-ciations between ultrasoundmarkers and PAS; thus, resultscannot be inferred to reflect on the diagnostic and predictiveaccuracy of these markers. Furthermore, most of thestudies included cases with surgically or histologicallyconfirmed placenta accreta, making it difficult to extrapolateinformation regarding the validity of PASmarkers in the first-trimester ultrasound.

First TrimesterSeveral PAS ultrasoundmarkers have been described in thefirst trimester. The prevalence and type of markers of PAS in

-appearing retroplacental hypoechoic zone (arrows). B, Abnormal or loss of

regnancies at risk of PAS. Am J Obstet Gynecol 2021.

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FIGURE 3Myometrial thinning

Transabdominal midline sagittal grayscale imaging from a patient withfocal placenta accreta spectrum. The area with normal myometrialthickness (asterisks) is compared to areas with myometrial thinning(arrows).

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination inpregnancies at risk of PAS. Am J Obstet Gynecol 2021.

smfm.org SMFM Special Report

the first trimester vary between the early first trimester ofpregnancy (6e9 weeks of gestation) and the later firsttrimester of pregnancy (11e14 weeks of gestation).11

In a patient with a previous cesarean delivery, implanta-tion of a gestational sac in the lower uterine segment onultrasound early in the first trimester is one of the mostcommon markers for PAS in the first trimester. A cesareanscar pregnancy (CSP), defined as a gestational sacimplanted in the lower uterine segment within or in closeproximity to the cesarean scar, markedly increases the riskof PAS (Figures 7 and 8).11,48,49 When a gestational sac isimplanted within a cesarean scar “niche,” extrauterine

FIGURE 4Hypervascularity of the uterovesical space

Transabdominal midline sagittal ultrasound in grayscale imaging (A) andhypervascularity of the uterovesical space. Note the presence of a large blo

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in p

extension of placental tissue and the need for hysterectomyis substantially increased.50 Histopathologically, a CSP isnot distinguishable from that of second trimester PAS,suggesting that they represent a continuum in the patho-genesis of the disease.51 In 1 study of 68 patients withprenatally identified PAS confirmed at delivery and a tech-nically adequate ultrasound examination between 6 and 9weeks of gestation, all were noted to have a low implanta-tion of the gestational sac.11

In the late first trimester, a low implantation of the gesta-tional sac is identified in approximately 28% of patients withPAS (Figure 9).11 This is explained by the growth of thegestational sac toward the fundal portion of the endome-triumas the pregnancy progresses. If the placenta is anteriorand under the cesarean scar, it can remain anchored to thecesarean scar significantly raising the risk of PAS.In a recent systematic review and meta-analysis evalu-

ating the first-trimester detection of PAS in high-riskwomen, a gestational sac implanted in close proximity to auterine scar was identified in 82.4% of women (95% confi-dence interval [CI], 85.8e95.7) with confirmed PAS.52

However, the sensitivity of this finding in the same anal-ysis was found to only be 44% (95% CI, 21.5e69.2), high-lighting the limitations of assessing the risk in the firsttrimester.52

Other markers that have traditionally been described inthe second and third trimesters have also been identified inthe late first trimester and are variably associated withPAS.52 The definitions of the individual markers have beeninconsistent but include the presence of placental lacunae,an abnormal bladder interface, uterovesicular hyper-vascularity, and loss of the retroplacental clearzone.11,16,28,53 This last marker is particularly helpful in

color Doppler imaging (B) of placenta accreta spectrum demonstratingod clot (asterisk) in the lower uterine segment.

regnancies at risk of PAS. Am J Obstet Gynecol 2021.

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FIGURE 5Uteroplacental interface

Transvaginal midline sagittal imaging of placenta previa with placenta accreta spectrum. A, Grayscale imaging demonstrating irregularities along theuteroplacental interface (arrows) and bulging of the lower uterine segment into the bladder (asterisk). B, Color Doppler imaging highlighting hyper-vascularity within the uteroplacental interface.

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

SMFM Special Report smfm.org

determining the extent of PAS, carrying a sensitivity of84.3% and diagnostic odds ratio (DOR) of 23.8 (95% CI,10.6e57.2).53 For cases that were ultimately determined tobe placenta percreta at the time of delivery, the sensitivity ofthis marker was 92.1% with a DOR of 20.4 (95% CI,6.0e108.7). Placental lacunae and posterior bladder wallinterruption or abnormalities were also noted in the late firsttrimester in cases of percreta, each with sensitivities be-tween 80% and 90%.53 Anterior placentation at the first-trimester sonographic evaluation is more common inwomen with PAS at delivery.11,16,28 Similar to findings in thesecond and third trimesters, the presence of multiple PASmarkers in the first trimester increased the diagnosticaccuracy.52e54

Second and Third Trimesters

Placental lacunae The presence of placental lacunae has been commonly re-ported in association with PAS.39,55,56 Often described asnumerous, large, and irregular echolucencies within theparenchyma of the placenta, placental lacunae should raisethe concern for underlying PAS.55,56 Previous studies inPAS differ substantially in the definition of lacunae with re-gard to the required size, number, and presence of bloodflow in lacunae. Lacunar blood flow has been described aslow-velocity flow in some reports, although others reportturbulent high-velocity flow.9,26,34,57 Finberg andWilliams,55

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in their 1992 seminal work on ultrasound markers of PAS,proposed a placental lacunae vascular space grading sys-tem, with grade 0 indicating no placental lacunae, grade 1þincluding placentas with 1 to 3 small lacunae, grade 2þcontaining 4 to 6 larger and irregular lacunae, and grade 3þdescribing a placenta with many large and “bizarre-appearing” lacunae throughout (Figure 1). Grade 3þ shouldraise a high degree of concern for PAS. Yang et al38 inves-tigated the association of lacunae with maternal complica-tions in 51 pregnancies at risk of PAS, with previouscesarean delivery and persistent placenta previa. The au-thors found that the need for cesarean hysterectomy andmaternal complications positively correlated with the num-ber of lacunae.38 Furthermore, the absence of lacunae inpregnancies with placenta previa and previous cesareandelivery is a reassuring sign with negative predictive values(NPV) ranging from 88% to 100% for PAS.9,38,55

Abnormal uteroplacental interface

Abnormal uteroplacental interface has been described asloss of the retroplacental hypoechoic zone, myometrialthinning, and increased vascularity on color Doppler.6,10,46

There is substantial variation in the definition and statisti-cal performance of the loss of the retroplacental hypoechoiczone for predicting PAS.9,13,39,46 The classic definition ofmyometrial thinning is a retroplacental myometrial thicknessof <1 mm. However, only 50% of cohort studies of PAS

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FIGURE 6Abnormal uterine contour and bridging vessel

Transabdominal midline sagittal ultrasound image of placenta previa with placenta accreta spectrum. A, Grayscale imaging of an abnormal uterinecontour with bulging of the lower uterine segment (small arrows) into the posterior bladder wall and interruption of the bladder wall (large arrow). B, ColorDoppler imaging demonstrating bridging vessel at the site of the bladder wall interruption (large arrow).

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

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provided a working definition of this marker.46,47 In addition,myometrial thinning is often seen in advancing gestationand can be more pronounced in women with previous ce-sarean delivery.58 This marker can be iatrogenically pro-duced and/or exaggerated with undue transducer pressure,

FIGURE 7Cesarean scar pregnancy

Transvaginal midline sagittal ultrasound in grayscale imaging demon-strating a cesarean scar pregnancy. Note the teardrop shape of thegestational sac (A) in close proximity to an empty bladder (B) and touchingthe internal cervical os (arrow) of the cervix (C).

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination inpregnancies at risk of PAS. Am J Obstet Gynecol 2021.

highlighting the need to minimize transducer pressure onthe abdomen when examining the placenta.41,46

Uterovesical interface

Uterovesical interface markers include bridging vessels,increased vascularity between the uterus and bladder, andinterruption of the bladder wall. Bridging vessels representneovascularity atop the uterine serosa and frequently withinthe uterovesical interface, depending on placental posi-tion.42,47,59 The color Doppler finding of neovascularity isfound in most cases of PAS and reflects the engorgedmyometrial vessels in the area of placentation. The hyper-vascular uterovesicle interface also reflects the dilation ofthe uteroplacental vasculature and the chaotic vasculargrowth and flow within this space.46 Sensitivity and speci-ficity of hypervascular uterovesical interface are variablyreported as ranging from 11% to 100% and 36% to 100%,respectively.24,37,60e64 Bladder varicosities are often seen inthe absence of PAS and in the setting of placenta pre-via.42,59 In addition, hypervascularity of the lower uterinesegment and/or cervix can be seen in placenta previawithout PAS, highlighting the difficulty in assessing thismarker. Interruption of the echogenic bladder wall, espe-cially with placental tissue, is a clear marker of PAS as itrepresents an extension of placental tissue beyond theuterus (Figure 6). Engorged vessels in the uterovesical

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FIGURE 8Ultrasound markers commonly seen in cesarean scar pregnancy

Transvaginal ultrasound in grayscale imaging (A) and color Doppler imaging (B) of a cesarean scar implantation (arrow) and bulging of the bladder line(arrowheads).

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

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interface may result in ultrasound echo dropout, thusmimicking placental extension into the uteroplacentalinterface.47

Miscellaneous markers

There are numerous other miscellaneous markers for PASthat have been described. Of these, placental bulge, exo-phytic placental mass, and cervical vascular extension werereviewed by the committee. The placental bulge isdescribed as a deviation of the uterine serosa, away fromthe expected planes, changing the uterine contour(Figures 5, 6, and 10).13,23,47 In a small study comparingultrasound and magnetic resonance imaging (MRI) featuresthat may predict placental invasion, the placental bulge wasfound to have a specificity of 88%, highlighting this markeras a reassuring sign when absent.23 An exophytic massrepresents a protrusion of placental tissue outside theuterus and is diagnostic of placenta percreta when seen.Similarly, the absence of this finding is reassuring, as itcarries an 80% to 100% specificity, albeit with a maximal

FIGURE 9Low implantation pregnancy

A, TVUS at 11 weeks of gestation in grayscale imaging in a pregnancy with lointernal os (arrow) of the cervix (C). B, TVUS at 11 weeks of gestation in color DNote the presence of an extensive vascularity extending into the cervix (C).TVUS, transvaginal ultrasound.

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sensitivity of 42%.23,34,61 In 1 systematic review of PAS,only cases of placenta increta and placenta percreta had aplacental bulge or an exophytic mass, highlighting theirrelative rarity in clinical practice.46 Vascular cervical exten-sion is defined by placental extension into the cervixinvolving at least the inner one-third, best seen on TVUS.This marker performs poorly, however, as it was identified ingreater than 50% of the time in a low-risk cohort withoutPAS.10

Combined markers

When ultrasound markers are combined, their performanceimproves substantially, yielding a sensitivity of 81.1% (95%CI, 69e94), specificity of 98.9% (95% CI, 98e100), PPV of90.9% (95% CI, 82e100), and NPV of 97.5 (95% CI,96e99).18 Thinning of the myometrium and loss of the ret-roplacental clear zone seem to have the highest interob-server agreements.13 Most data regarding the predictabilityof PAS ultrasound markers have been derived in singlecenters with a relatively high volume of PAS cases. The true

w implantation of the gestational sac. Note that the placenta is covering theoppler imaging in a pregnancy with low implantation of the gestational sac.

regnancies at risk of PAS. Am J Obstet Gynecol 2021.

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FIGURE 10Abnormal uterine contour

Transabdominal midline sagittal ultrasound imaging with an extended viewof a pregnancy with placenta accreta spectrum. Note the presence of aplacental bulge and thickening in the lower uterine segment (arrows) andinto the bladder (B). Double arrows indicate the difference in the placentalthickness in the upper and lower segments of the uterus.

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination inpregnancies at risk of PAS. Am J Obstet Gynecol 2021.

TABLE 2Definitions of placenta accreta spectrummarkers in the first trimester of pregnancy

Marker Definition

Cesarean scarpregnancy

Gestational sac implantation in part or totally withinthe cesarean scar.

Gestational sac may have a teardrop or triangularshape.

Low implantationpregnancy

Gestational sac located close to the internal cervicalos (up to 8 6/7 weeks of gestation) and/or placentalimplantation located posterior to a partially filledmaternal bladder (up to 13 6/7 weeks of gestation).

Shainker. Special Report of the SMFM: Definition of markers and ultrasound ex-amination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

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sensitivity of these markers in the community setting re-mains unknown.

Existing Consensus GuidelinesThe European Working Group on Abnormally InvasivePlacenta (EW-AIP) and the International Federation of Gy-necology and Obstetrics (FIGO) developed language out-lining various PAS ultrasound markers and suggestedstandardized definitions for each.40,41 The EW-AIP estab-lished a list of 11 PAS ultrasound markers (6 in 2-dimensional [2D] grayscale, 4 in 2D color Doppler, and 1 in3-dimensional [3D] power Doppler). This was derived fromthe analysis of 23 manuscripts reviewed by an expert panel.The panel placed importance on defining each PAS markerwithout ambiguity but did not report on their predictivevalues.41 The recent FIGO consensus guidelines for PASprenatal screening and diagnosis listed the EW-AIP 11markers along with their definitions. These guidelines didnot recommend using certain markers over others, andacknowledged that none carries 100% sensitivity andspecificity. The FIGO consensus guidelines also com-mented on the role of a CSP as the first-trimester precursorto PAS.40 Taking these published definitions into account,we reviewed the general utility of each ultrasound markerand utilized the these published definitions when possibleand appropriate. We also attempted to consolidate someultrasound PAS markers to simplify language and stream-line definitions.

Ultrasound Approach and Definitions ofPlacenta Accreta Spectrum Markers

General considerations We recommend starting the assessment with trans-abdominal imaging to obtain an overview of placental

location and start assessing the regions of concern. TVUS isstrongly recommended for the assessment of PAS. Trans-vaginal imaging optimizes resolution and allows for adetailed assessment of the lower uterine segment, posteriorbladder wall, and cervix. The bladder should be partially full.Color Doppler should be utilized to assess for vascularityand placental extension into the uterine wall and sur-rounding structures. The transducer should be adjusted tooperate at the highest clinically appropriate frequency,realizing that there is a trade-off between resolution andbeam penetration.65 Ultrasound image magnificationshould be performed to enhance the visualization of targetregions. When assessing the retroplacental region,perpendicular orientation of the angle of insonation andapplying minimal transducer pressure are recommended.Given the continuumof disease fromCSP to PAS, screeningfor PAS should begin early in the first trimester and continuethroughout the pregnancy until practitioners haveconcluded whether there is sonographic concern for PAS.

First trimester

In the first trimester, a detailed evaluation of the uterus isnecessary to determine the location of the gestational sacor placenta (depending on gestational age) in reference tothe bladder, internal os, and cesarean scar. When per-forming TVUS, the maternal bladder should be partiallyfilled, enough to allow for a sonographic window, withoutoverfilling, which can result in distortion of the uteroves-ical interface. The target area should be magnified tooccupy at least one-half of the ultrasound image, andfocal zones should be appropriately placed. After 10weeks of gestation, color Doppler can be used to assessfor the presence of hypervascularity and lacunae; whenpossible, color Doppler should be limited to the placentalregion and not overlap the fetus. The definition of first-trimester PAS markers and the proposed ultrasoundapproach are presented in Table 2 and Box 1,respectively.

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BOX 1Approach to ultrasound examination in the first trimester of pregnancy

� Transvaginal ultrasound is recommended in early pregnancy, and transabdominal ultrasound may be performed when appropriate.� Detailed evaluation of the uterus in the midsagittal plane to document the gestational sac (up to 8 6/7 weeks of gestation) and/or the placental location(up to 13 6/7 weeks of gestation).

� Documentation should include reference to the position of the sac and/or placenta relative to the bladder, cesarean scar (if present), and internalcervical os.

� Color Doppler imaging using a low-velocity scale, low wall filter and high gain to maximize detection of flow (adjusting as needed for body habitus andother clinical factors).a

� Evaluate shape of gestational sac (up to 8 6/7 weeks of gestation).� Imaging should be performed with a partially filled maternal bladder.— The area of interest should be magnified so that it occupies at least half of the ultrasound image with the focal zone at an appropriate depth.

a Color Doppler should be limited to the areas of interest and avoid the embryo or fetus whenever possible.

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

SMFM Special Report smfm.org

Second and third trimesters

The antenatal diagnosis of PAS is most often made in thesecond and third trimesters of pregnancy. Classic sono-graphic markers of PAS are typically described in womenwith anterior placentae previa and previous cesareandeliveries.6,7

Table 3 lists the proposed definitions of PAS ultrasoundmarkers in the second and third trimesters of pregnancy.Other than placenta previa, placenta lacunae arefrequently described as classic ultrasound markers ofPAS. Lacunae can often be found in low-risk non-PASpregnancies; however, when present in women with riskfactors, they carry the highest sensitivity of all 2D gray-scale markers.10,66 When lacunae are large, numerous,and with irregular borders, their association with PAS isincreased.55 Lacunae tend to congregate near the area ofplacental invasion; thus, the presence of lacunae bloodflow on grayscale and color Doppler is also associatedwith PAS.Sonographic assessment of the uteroplacental inter-

face includes evaluation of the loss of the retroplacentalhypoechoic zone and thinning of the retroplacentalmyometrium.6,9,13,39,46,47 The uteroplacental interface isoften inferior to the posterior bladder wall. Similar toother PAS markers in women with an anterior placentaand previous cesarean delivery, the uteroplacentalinterface is best seen utilizing a combination of trans-abdominal and transvaginal imaging with a partially fil-led bladder.The uterine contour is optimally evaluated when the

placenta is anterior, utilizing a partially filled bladder as theacoustic window. This marker, often referred to as the“placental bulge,” can be seen on both transabdominal andtransvaginal imaging. The bulge does not always reflect a“through-and-through” defect of the uterine wall; rather, ithighlights the area of scar dehiscence and thinning of themyometrium in areas of PAS.12,46,67 Although this findinghas not been correlated specifically with increasedmorbidity or mortality, its presence raises the concern forextrauterine placental extension (placenta percreta). Color

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Doppler is often helpful to determine the extent of vascularinvasion.Bridging vessels are defined as vessels, identified on

color Doppler, that extend from the placenta across themyometrium and/or beyond the uterine serosa. This hasbeen considered as one of the “classic markers” of PASover the years but has lacked consistency in its defi-nition.6,9 Typically seen running perpendicular to thelong axis of the uterus, bridging vessels are oftenassociated with the presence of a placental bulge withplacental tissue extending beyond the uterine serosa.41

Unlike other markers that can often be seen in caseswithout PAS, this marker is rarely seen in cases withoutPAS.10

It is important to note that the placenta is a 3Dstructure, and thus, comprehensive sonographicassessment is required in pregnancies at risk of PAS.This is best performed by obtaining several parasagittaland transverse planes of the placenta during the ultra-sound examination. Special attention should be given tothe retroplacental area and the lower segment and cer-vical regions. This is best achieved with a combinedtransabdominal and transvaginal approach. Table 4presents the sonographic approach in the second andthird trimesters of pregnancy.

DiscussionThis document, endorsed by AIUM, SMFM, ACR, andGOHO, supported by ACOG and ISUOG, and approvedby SRU, with ARDMS participating in the developmentand production of the document, presents aconsensus-based approach to ultrasound examinationand assessment of PAS. Pregnancies with PAS are at asignificantly increased risk of maternal and fetal mor-bidities and mortalities. Prenatal detection of PAS re-duces pregnancy complications and improvesoutcomes.3,7,8,43 Several PAS markers have beenidentified and studied. There has been an effort tostandardize the definitions of PAS markers, with theultimate goal of improving risk stratification by

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TABLE 3Definitions of PAS markers in the second andthird trimesters of pregnancy

Marker Definition

Placental lacunae Irregular, hypoechoic spaces within theplacenta containing vascular flow (which can beseen on grayscale and/or color Dopplerimaging).

The following lacunae findings are associatedwith high risk of PAS:Multiple (often defined as �3)� Large size� Irregular borders� High velocitya and/or turbulent flow within

Abnormaluteroplacentalinterface

Loss of the retroplacental hypoechoic zonebetween the placenta and myometrium.b

This marker is often located along the posteriorbladder wall resulting in partial or completeinterruption or irregularities of the uterovesicalinterface.

Thinning of the retroplacental myometrium(previously described as myometrial thicknessof <1 mm).

Abnormal uterinecontour (placentalbulge)

Placental tissue distorting the uterine contourresulting in a bulge-like appearance.

Exophytic mass Placental tissue extruding beyond the uterineserosa.

Bridging vessel Vessel that extends from the placenta across themyometrium and beyond the uterine serosa.

PAS, placenta accreta spectrum.

a Some studies suggest a velocity of >15 cm/s as the threshold for high peak systolicvelocity; b This space represents the uterine decidua and has been described as the “clearzone.”

Shainker. Special Report of the SMFM: Definition of markers and ultrasound ex-amination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

TABLE 4Approach to ultrasound examination in thesecond and third trimesters of pregnancy

Marker Approaches

Lacunae Detailed evaluation of the entire placenta inorthogonal planes.

Lacunae should be evaluated using grayscaleand color Doppler imaging.

Doppler assessment should generally beperformed with a low-velocity scale, low wallfilters, and high gain to maximize detection offlowa (adjusting as needed for body habitusand other clinical factors).

Abnormal uteroplacentalinterface

Evaluation of the uteroplacental interface isoptimized by perpendicular orientation of thetransducer to the area of interest withminimal transducer pressure.

Transvaginal ultrasound is recommended inthe setting of an anterior, low-lying placentaor placenta previa.

Imaging should be performed with a partiallyfilled maternal bladder.

Optimization of gain settings to helpdifferentiate between placental andmyometrial tissues.

The area of interest should be magnified sothat it occupies at least half of the ultrasoundimage with the focal zone at appropriatedepth.

Myometrial measurement should be madeperpendicular to the long axis of the uterusand measured at the thinnest site (commonlyalong the uterine scar).

Abnormal uterinecontour (placental bulge)

Placental tissue distorting the uterine contourresulting in a bulge-like appearance (this isbest appreciated in a midsagittal plane of theuterus).

Exophytic mass Placental tissue visualized beyond the uterineserosa.

Bridging vessel Doppler assessment of vessels extendingfrom the placenta across the myometriumand beyond the uterine serosa.b

a Some studies suggest a velocity of >15 cm/s as the threshold for high peak systolicvelocity; b Bridging vessels need to be differentiated from bladder varicosities, which arenot placental in origin and do not increase risk of placenta accreta spectrum.

Shainker. Special Report of the SMFM: Definition of markers and ultrasound ex-amination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

smfm.org SMFM Special Report

ultrasound resulting in improved prenatal detection andthus positively impacting pregnancy outcomes. Thistask force, assembled by SMFM with representationfrom multiple societies and organizations, providesdefinitions for PAS markers along with a standardizedapproach to the ultrasound examination in pregnanciesat risk of PAS.It is important to recognize that the proposed definitions

of PAS markers are based on the current literature, alongwith expert opinion when data are lacking. As ultrasoundtechnology advances with improved tools, the detection ofabnormal placental invasion and vasculature should begreatly enhanced. Advancement in ultrasound technologymay render the definitions of some existing PAS markersobsolete. An example is the current definition of abnormalplacental vasculature. Emerging ultrasound technology hasresulted in significant improvements in the sonographic

detection of low-velocity vascular flow. Accordingly, thismay result in difficulty differentiating normal from abnormalplacental flow.It is also important to note that many of the markers pre-

sented in this document have been studied in women withprevious cesarean deliveries and placenta previa. In womenwithout these risk factors, however, the markers are seenoften and typically in the absence of PAS.10 As such, the

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BOX 2PAS ultrasound marker research gaps

� What is the utility of transvaginal ultrasound screening in the first trimester of pregnancy in all women with previous cesarean delivery?� What is the appropriate timing of screening in the first trimester of pregnancy in women with previous cesarean delivery?� Does location, size, and number of lacunae predict extent of invasion?� How to define “high” peak systolic velocity in lacunae?� Are the vessels resulting in uterovesicular hypervascularity placental or maternal in origin?� What is the significance of increased placental thickness?� Does the role of vascular imaging change with newer techologies?� What is the role of 3D ultrasound when assessing placental volume, exophytic masses, and bridging vessels?� How to define and assess cervical hypervascularity?� How do PAS ultrasound markers correlate with maternal biomarkers?� How do placental ultrasound markers progress with advancing gestational age?� What is the role of MRI in the evaluation of PAS?

3D, 3-dimensional; MRI, magnetic resonance imaging; PAS, placenta accreta spectrum.

Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

SMFM Special Report smfm.org

recommended ultrasound approach to women withoutthese risk factors remains largely unknown and is an area ofgreat interest.There are several limitations of ultrasound in

detecting PAS. Ultrasound is an operator-dependentimaging modality and, thus, is highly dependent onthe skills of the examiner performing the ultrasound.The detection rates will depend on placental locationand maternal imaging conditions that impact sono-graphic visualization of markers. A standardizedapproach to the performance of the ultrasound ex-amination along with consensus-based definitions ofPAS markers will result in more consistency in diag-nosis and allows for the evaluation of markers acrosscenters to improve diagnostic performance. Despiteoptimizing a systematic approach to ultrasound ex-amination for PAS markers, inherent limitations of ul-trasound may diminish detection rates. These includeposterior placentation, with limited sound penetrationand resolution; elevated maternal BMI; and uterineleiomyomata. The task force also identified researchgaps for sonographic markers of PAS (Box 2). Wehope that future research will use the definitionshereby provided along with a standardized approachto the ultrasound examination to facilitate datacomparison. In addition, although the scope of thistask force was focused on ultrasound examination, wehope similar efforts are made in the future to provideguidance on the use of MRI for the evaluation of PAS.As PAS has become more prevalent, the need for agree-

ment on the definitions of ultrasound markers and sono-graphic approach to the patient at risk of PAS is crucial. Thisdocument provides necessary steps toward consistency inthe definitions of PAS markers and the approach to diag-nosis. Accurate antenatal diagnosis is paramount in opti-mizing maternal and fetal outcomes. Further work will beneeded to measure the impact of the proposed

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standardized definitions, along with the approach to ultra-sound examination. n

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This document has undergone an internal peer review through amultilevel committee process within SMFM. This review involvescritique and feedback from the SMFM Publications and DocumentReview Committees and final approval by the SMFM Executive Com-mittee. SMFM accepts sole responsibility for the document content.SMFM publications do not undergo editorial and peer review by theAmerican Journal of Obstetrics & Gynecology. The SMFMPublicationsCommittee reviews publications every 18 to 24 months and issuesupdates as needed. Further details regarding SMFM publications canbe found at www.smfm.org/publications.

SMFM has adopted the use of the word “woman” (and the pronouns“she” and “her”) to apply to individuals who are assigned female sex atbirth, including individuals who identify as men and nonbinary in-dividuals who identify as both genders or neither gender. As gender-neutral language continues to evolve in the scientific and medicalcommunities, SMFM will reassess this usage and make appropriateadjustments, as necessary.

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