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Special Report of the Society for Maternal-Fetal Medicine Placenta Accreta Spectrum Ultrasound Marker Task Force: Consensus on definition of markers and approach to the ultrasound examination in pregnancies at risk for placenta accreta spectrum

      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 standardizing the definitions of placenta accreta spectrum markers and the approach to the ultrasound examination, 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 field. This manuscript provides information on the Placenta Accreta Spectrum Task Force process and findings.

      Key words

      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.

      Introduction

      Placenta accreta spectrum (PAS), encompassing the terms placenta accreta, placenta increta, placenta percreta, morbidly adherent placenta, and invasive placentation, includes 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.
      • Creanga A.A.
      • Bateman B.T.
      • Butwick A.J.
      • et al.
      Morbidity associated with cesarean delivery in the United States: is placenta accreta an increasingly important contributor?.
      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.
      • Creanga A.A.
      • Bateman B.T.
      • Butwick A.J.
      • et al.
      Morbidity associated with cesarean delivery in the United States: is placenta accreta an increasingly important contributor?.
      ,
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      PAS is associated with a marked increase in maternal morbidity and mortality. The morbidity is primarily related to massive hemorrhage with associated organ damage, cesarean hysterectomy, and need for critical care resources.
      • Creanga A.A.
      • Bateman B.T.
      • Butwick A.J.
      • et al.
      Morbidity associated with cesarean delivery in the United States: is placenta accreta an increasingly important contributor?.
      ,
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      Prenatal detection of PAS allows for mobilization of multidisciplinary care teams and surgical planning, which reduces maternal morbidity.
      • Shamshirsaz A.A.
      • Fox K.A.
      • Salmanian B.
      • et al.
      Maternal morbidity in patients with morbidly adherent placenta treated with and without a standardized multidisciplinary approach.
      • Shamshirsaz A.A.
      • Fox K.A.
      • Erfani H.
      • et al.
      Multidisciplinary team learning in the management of the morbidly adherent placenta: outcome improvements over time.
      • Warshak C.R.
      • Ramos G.A.
      • Eskander R.
      • et al.
      Effect of predelivery diagnosis in 99 consecutive cases of placenta accreta.
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine
      Obstetrics Care Consensus No. 7: placenta accreta spectrum.
      • Erfani H.
      • Fox K.A.
      • Clark S.L.
      • et al.
      Maternal outcomes in unexpected placenta accreta spectrum disorders: single-center experience with a multidisciplinary team.
      Furthermore, the ability to correctly stratify the risk of PAS, including decreasing the risk with a “normal” ultrasound, reduces the possibility of iatrogenic complications associated with planned premature delivery, preoperative invasive procedures, and patient and provider anxiety.
      The prenatal detection and risk stratification for PAS are primarily made by ultrasound. However, ultrasound is an operator-dependent imaging modality with substantial variability in image quality among providers. Furthermore, placental location and challenging imaging conditions, including elevated body mass index (BMI) or posterior placentation, may impede the sonographic detection of PAS markers. There has been limited consensus on the optimal approach to the ultrasound evaluation of patients at risk of PAS, such as the appropriate timing of screening, need for transvaginal ultrasound (TVUS) imaging, use of color and pulsed Doppler, angle of placental insonation, and equipment settings.
      Despite a large body of literature on various PAS ultrasound markers and their screening performance, important inconsistencies in screening results persist. This is primarily because of the retrospective design of most studies, lack of standardized definitions of PAS markers, lack of agreement on the optimal gestational age for assessment, and inconsistencies in the approach to the ultrasound evaluation of the placenta.
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      Furthermore, patients’ a priori risks have a significant influence on the positive predictive value (PPV) of PAS markers. Recent data have shown that these markers are frequently present in women at low risk for PAS.
      • Philips J.
      • Gurganus M.
      • DeShields S.
      • et al.
      Prevalence of sonographic markers of placenta accreta spectrum in low-risk pregnancies.
      In response to the need for standardizing the definitions of PAS markers and the approach to the ultrasound examination, the Society for Maternal-Fetal Medicine (SMFM) convened a task force with the goals of assessing PAS sonographic markers on the basis of available data and expert consensus, providing a standardized approach to the prenatal ultrasound evaluation of the uterus and placenta in pregnancies at risk of PAS, and identifying research gaps in the field. This manuscript provides information on the PAS Task Force process and outcomes.

      Procedure

      SMFM invited representatives from the American Institute of Ultrasound in Medicine (AIUM), American College of Obstetricians and Gynecologists (ACOG), American College of Radiology (ACR), International Society of Ultrasound in Obstetrics and Gynecology (ISUOG), Society for Radiologists in Ultrasound (SRU), American Registry for Diagnostic Medical Sonography (ARDMS), and Gottesfeld-Hohler Memorial Ultrasound Foundation (GOHO) to the PAS Task Force (Table 1). The PAS Task Force was organized into 4 subcommittees: first-trimester markers, placental lacunae, uteroplacental interface, and uterovesical interface, which also included miscellaneous markers (cervical invasion, placental bulge, and exophytic mass). Each subcommittee was chaired by a PAS Task Force member and included at least 2 additional members. The authors S.A.S. and A.A. participated on all 4 subcommittees. Each subcommittee performed a detailed literature review of respective markers. This included the definitions of each marker, indication for the examination, reported diagnostic accuracy of each marker, gestational age at assessment, and optimal ultrasound approach for evaluation.
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      ,
      American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine
      Obstetrics Care Consensus No. 7: placenta accreta spectrum.
      ,
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      • Hubinont C.
      • Mhallem M.
      • Baldin P.
      • Debieve F.
      • Bernard P.
      • Jauniaux E.
      A clinico-pathologic study of placenta percreta.
      • Zosmer N.
      • Jauniaux E.
      • Bunce C.
      • Panaiotova J.
      • Shaikh H.
      • Nicholaides K.H.
      Interobserver agreement on standardized ultrasound and histopathologic signs for the prenatal diagnosis of placenta accreta spectrum disorders.
      • Calì G.
      • D’Antonio F.
      • Forlani F.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.M.
      Ultrasound detection of bladder-uterovaginal anastomoses in morbidly adherent placenta.
      • Fujisaki M.
      • Furukawa S.
      • Maki Y.
      • Oohashi M.
      • Doi K.
      • Sameshima H.
      Maternal morbidity in women with placenta previa managed with prediction of morbidly adherent placenta by ultrasonography.
      • Rac M.W.
      • Moschos E.
      • Wells C.E.
      • McIntire D.D.
      • Dashe J.S.
      • Twickler D.M.
      Sonographic findings of morbidly adherent placenta in the first trimester.
      • Tovbin J.
      • Melcer Y.
      • Shor S.
      • et al.
      Prediction of morbidly adherent placenta using a scoring system.
      • Pilloni E.
      • Alemanno M.G.
      • Gaglioti P.
      • et al.
      Accuracy of ultrasound in antenatal diagnosis of placental attachment disorders.
      • Cho H.Y.
      • Hwang H.S.
      • Jung I.
      • Park Y.W.
      • Kwon J.Y.
      • Kim Y.H.
      Diagnosis of placenta accreta by uterine artery Doppler velocimetry in patients with placenta previa.
      • Gilboa Y.
      • Spira M.
      • Mazaki-Tovi S.
      • Schiff E.
      • Sivan E.
      • Achiron R.
      A novel sonographic scoring system for antenatal risk assessment of obstetric complications in suspected morbidly adherent placenta.
      • Rac M.W.
      • Dashe J.S.
      • Wells C.E.
      • Moschos E.
      • McIntire D.D.
      • Twickler D.M.
      Ultrasound predictors of placental invasion: the placenta accreta index.
      • Collins S.L.
      • Stevenson G.N.
      • Al-Khan A.
      • et al.
      Three-dimensional power Doppler ultrasonography for diagnosing abnormally invasive placenta and quantifying the risk.
      • Riteau A.S.
      • Tassin M.
      • Chambon G.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      • Bowman Z.S.
      • Eller A.G.
      • Kennedy A.M.
      • et al.
      Accuracy of ultrasound for the prediction of placenta accreta.
      • Maher M.A.
      • Abdelaziz A.
      • Bazeed M.F.
      Diagnostic accuracy of ultrasound and MRI in the prenatal diagnosis of placenta accreta.
      • Calì G.
      • Giambanco L.
      • Puccio G.
      • Forlani F.
      Morbidly adherent placenta: evaluation of ultrasound diagnostic criteria and differentiation of placenta accreta from percreta.
      • Peker N.
      • Turan V.
      • Ergenoglu M.
      • et al.
      Assessment of total placenta previa by magnetic resonance imaging and ultrasonography to detect placenta accreta and its variants.
      • Ballas J.
      • Pretorius D.
      • Hull A.D.
      • Resnik R.
      • Ramos G.A.
      Identifying sonographic markers for placenta accreta in the first trimester.
      • Wong H.S.
      • Cheung Y.K.
      • Williams E.
      Antenatal ultrasound assessment of placental/myometrial involvement in morbidly adherent placenta.
      • Lim P.S.
      • Greenberg M.
      • Edelson M.I.
      • Bell K.A.
      • Edmonds P.R.
      • Mackey A.M.
      Utility of ultrasound and MRI in prenatal diagnosis of placenta accreta: a pilot study.
      • Stirnemann J.J.
      • Mousty E.
      • Chalouhi G.
      • Salomon L.J.
      • Bernard J.P.
      • Ville Y.
      Screening for placenta accreta at 11-14 weeks of gestation.
      • Hamada S.
      • Hasegawa J.
      • Nakamura M.
      • et al.
      Ultrasonographic findings of placenta lacunae and a lack of a clear zone in cases with placenta previa and normal placenta.
      • Chou M.M.
      • Chen W.C.
      • Tseng J.J.
      • Chen Y.F.
      • Yeh T.T.
      • Ho E.S.
      Prenatal detection of bladder wall involvement in invasive placentation with sequential two-dimensional and adjunctive three-dimensional ultrasonography.
      • Shih J.C.
      • Palacios-Jaraquemada J.M.
      • Su Y.N.
      • et al.
      Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
      • Wong H.S.
      • Zuccollo J.
      • Tait J.
      • Pringle K.
      Antenatal topographical assessment of placenta accreta with ultrasound.
      • Wong H.S.
      • Cheung Y.K.
      • Strand L.
      • et al.
      Specific sonographic features of placenta accreta: tissue interface disruption on gray-scale imaging and evidence of vessels crossing interface-disruption sites on Doppler imaging.
      • Japaraj R.P.
      • Mimin T.S.
      • Mukudan K.
      Antenatal diagnosis of placenta previa accreta in patients with previous cesarean scar.
      • Yang J.I.
      • Lim Y.K.
      • Kim H.S.
      • Chang K.H.
      • Lee J.P.
      • Ryu H.S.
      Sonographic findings of placental lacunae and the prediction of adherent placenta in women with placenta previa totalis and prior cesarean section.
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      • Jauniaux E.
      • Bhide A.
      • Kennedy A.
      • et al.
      FIGO consensus guidelines on placenta accreta spectrum disorders: prenatal diagnosis and screening.
      • Collins S.L.
      • Ashcroft A.
      • Braun T.
      • et al.
      Proposal for standardized ultrasound descriptors of abnormally invasive placenta (AIP).
      • Levine D.
      • Hulka C.A.
      • Ludmir J.
      • Li W.
      • Edelman R.R.
      Placenta accreta: evaluation with color Doppler US, power Doppler US, and MR imaging.
      The task force held a face-to-face meeting in December 2018 in Boston, MA, to review each subcommittee’s findings and recommendations. Expert consensus opinion was obtained when available data could not provide clear definitions for each PAS marker and/or the optimal approach for screening. In addition, research gaps were noted.
      Table 1Task force participating members and societies
      Alfred AbuhamadSMFM, Co-Chair
      Scott A. ShainkerSMFM, Co-Chair
      Beverly ColemanACR
      Ilan E. Timor-TritschGOHO
      Amarnath BhideISUOG
      Bryann BromleyAIUM
      Alison G. CahillACOG
      Joshua A. CopelGOHO
      Manisha GhandiACOG
      Jonathan L. Hecht
      Pathology consultant, Department of Pathology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA.
      Katherine M. JohnsonSMFM
      Deborah LevineSRU
      Joan MastrobattistaAIUM
      Jennifer PhilipsSMFM
      Lawrence D. PlattGOHO
      Alireza A. ShamshirsazGOHO
      Thomas D. ShippARDMS
      Robert M. SilverSMFM
      Lynn L. SimpsonSMFM
      ACOG, American College of Obstetricians and Gynecologists; ACR, American College of Radiologists; AIUM, American Institute of Ultrasound in Medicine; ARDMS, American Registry for Diagnostic Medical Sonography; GOHO, Gottesfeld-Hohler Memorial Society; ISUOG, International Society of Ultrasound in Obstetrics and Gynecology; SMFM, Society for Maternal-Fetal Medicine; SRU, Society of Radiologists in Ultrasound.
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      a Pathology consultant, Department of Pathology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA.

      Literature Review

      As outlined in a recent Obstetrics Care Consensus, ultrasound is the primary screening modality for PAS.
      American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine
      Obstetrics Care Consensus No. 7: placenta accreta spectrum.
      Ultrasound markers of PAS can be seen early in the first trimester, although historically screening is predominantly performed in the second and third trimesters of pregnancy. The ultrasound marker with the strongest association with PAS is a persistent placenta previa at the time of delivery, in the setting of a previous cesarean delivery.
      • Warshak C.R.
      • Ramos G.A.
      • Eskander R.
      • et al.
      Effect of predelivery diagnosis in 99 consecutive cases of placenta accreta.
      ,
      • Eller A.G.
      • Bennett M.A.
      • Sharshiner M.
      • et al.
      Maternal morbidity in cases of placenta accreta managed by a multidisciplinary care team compared with standard obstetric care.
      Other classic sonographic markers of PAS include the presence of placental lacunae (Figure 1), loss of the retroplacental hypoechoic zone (Figure 2), thinning of the retroplacental myometrium (Figure 3), hypervascularity of the uterovesicle or retroplacental space (Figure 4), extension of placental tissue into the uterus and/or bladder, and placental bridging vessels (Figures 5 and 6).
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      ,
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      • Jauniaux E.
      • Bhide A.
      • Kennedy A.
      • et al.
      FIGO consensus guidelines on placenta accreta spectrum disorders: prenatal diagnosis and screening.
      • Collins S.L.
      • Ashcroft A.
      • Braun T.
      • et al.
      Proposal for standardized ultrasound descriptors of abnormally invasive placenta (AIP).
      ,
      • Esakoff T.F.
      • Sparks T.N.
      • Kaimal A.J.
      • et al.
      Diagnosis and morbidity of placenta accreta.
      • Warshak C.R.
      • Eskander R.
      • Hull A.D.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      The presence of excessive color Doppler flow in the retroplacental space along with abnormal placental bridging vessels has also been associated with PAS (Figure 6).
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      ,
      American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine
      Obstetrics Care Consensus No. 7: placenta accreta spectrum.
      ,
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      ,
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.
      Figure thumbnail gr1
      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.
      Figure thumbnail gr2
      Figure 2Retroplacental hypoechoic zone
      Transvaginal midline sagittal grayscale imaging of placenta previa. A, Normal-appearing retroplacental hypoechoic zone (arrows). B, Abnormal or loss of the retroplacental hypoechoic zone (arrows) in 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.
      Figure thumbnail gr3
      Figure 3Myometrial thinning
      Transabdominal midline sagittal grayscale imaging from a patient with focal placenta accreta spectrum. The area with normal myometrial thickness (asterisks) is compared to areas with myometrial thinning (arrows).
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      Figure thumbnail gr4
      Figure 4Hypervascularity of the uterovesical space
      Transabdominal midline sagittal ultrasound in grayscale imaging (A) and color Doppler imaging (B) of placenta accreta spectrum demonstrating hypervascularity of the uterovesical space. Note the presence of a large blood clot (asterisk) in the lower uterine segment.
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      Figure thumbnail gr5
      Figure 5Uteroplacental interface
      Transvaginal midline sagittal imaging of placenta previa with placenta accreta spectrum. A, Grayscale imaging demonstrating irregularities along the uteroplacental interface (arrows) and bulging of the lower uterine segment into the bladder (asterisk). B, Color Doppler imaging highlighting hypervascularity 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.
      Figure thumbnail gr6
      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 uterine contour with bulging of the lower uterine segment (small arrows) into the posterior bladder wall and interruption of the bladder wall (large arrow). B, Color Doppler 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.
      Task force members identified several significant limitations to the current literature on this subject. Most studies are retrospective in design, lack control “low-risk” comparison groups, and do not provide clear definitions of the PAS markers being studied, which limits the ability to make comparisons among studies and combines many of the reported diagnostic performance statistics.
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      It is important to note that most studies were designed to highlight associations between ultrasound markers and PAS; thus, results cannot be inferred to reflect on the diagnostic and predictive accuracy of these markers. Furthermore, most of the studies included cases with surgically or histologically confirmed placenta accreta, making it difficult to extrapolate information regarding the validity of PAS markers in the first-trimester ultrasound.

      First Trimester

      Several PAS ultrasound markers have been described in the first trimester. The prevalence and type of markers of PAS in the first trimester vary between the early first trimester of pregnancy (6–9 weeks of gestation) and the later first trimester of pregnancy (11–14 weeks of gestation).
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      In a patient with a previous cesarean delivery, implantation of a gestational sac in the lower uterine segment on ultrasound early in the first trimester is one of the most common markers for PAS in the first trimester. A cesarean scar pregnancy (CSP), defined as a gestational sac implanted in the lower uterine segment within or in close proximity to the cesarean scar, markedly increases the risk of PAS (Figures 7 and 8).
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      ,
      • Timor-Tritsch I.E.
      • Monteagudo A.
      • Cali G.
      • et al.
      Cesarean scar pregnancy is a precursor of morbidly adherent placenta.
      ,
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Outcome of cesarean scar pregnancy managed expectantly: systematic review and meta-analysis.
      When a gestational sac is implanted within a cesarean scar “niche,” extrauterine extension of placental tissue and the need for hysterectomy is substantially increased.
      • Kaelin Agten A.
      • Cali G.
      • Monteagudo A.
      • Oviedo J.
      • Ramos J.
      • Timor-Tritsch I.E.
      The clinical outcome of cesarean scar pregnancies implanted “on the scar” versus “in the niche.”.
      Histopathologically, a CSP is not distinguishable from that of second trimester PAS, suggesting that they represent a continuum in the pathogenesis of the disease.
      • Timor-Tritsch I.E.
      • Monteagudo A.
      • Cali G.
      • et al.
      Cesarean scar pregnancy and early placenta accreta share common histology.
      In 1 study of 68 patients with prenatally identified PAS confirmed at delivery and a technically adequate ultrasound examination between 6 and 9 weeks of gestation, all were noted to have a low implantation of the gestational sac.
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      Figure thumbnail gr7
      Figure 7Cesarean scar pregnancy
      Transvaginal midline sagittal ultrasound in grayscale imaging demonstrating a cesarean scar pregnancy. Note the teardrop shape of the gestational sac (A) in close proximity to an empty bladder (B) and touching the internal cervical os (arrow) of the cervix (C).
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      Figure thumbnail gr8
      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.
      In the late first trimester, a low implantation of the gestational sac is identified in approximately 28% of patients with PAS (Figure 9).
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      This is explained by the growth of the gestational sac toward the fundal portion of the endometrium as the pregnancy progresses. If the placenta is anterior and under the cesarean scar, it can remain anchored to the cesarean scar significantly raising the risk of PAS.
      Figure thumbnail gr9
      Figure 9Low implantation pregnancy
      A, TVUS at 11 weeks of gestation in grayscale imaging in a pregnancy with low implantation of the gestational sac. Note that the placenta is covering the internal os (arrow) of the cervix (C). B, TVUS at 11 weeks of gestation in color Doppler imaging in a pregnancy with low implantation of the gestational sac. Note the presence of an extensive vascularity extending into the cervix (C).
      TVUS, transvaginal ultrasound.
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      In a recent systematic review and meta-analysis evaluating the first-trimester detection of PAS in high-risk women, a gestational sac implanted in close proximity to a uterine scar was identified in 82.4% of women (95% confidence interval [CI], 85.8–95.7) with confirmed PAS.
      • D’Antonio F.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      First-trimester detection of abnormally invasive placenta in high-risk women: systematic review and meta-analysis.
      However, the sensitivity of this finding in the same analysis was found to only be 44% (95% CI, 21.5–69.2), highlighting the limitations of assessing the risk in the first trimester.
      • D’Antonio F.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      First-trimester detection of abnormally invasive placenta in high-risk women: systematic review and meta-analysis.
      Other markers that have traditionally been described in the second and third trimesters have also been identified in the late first trimester and are variably associated with PAS.
      • D’Antonio F.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      First-trimester detection of abnormally invasive placenta in high-risk women: systematic review and meta-analysis.
      The definitions of the individual markers have been inconsistent but include the presence of placental lacunae, an abnormal bladder interface, uterovesicular hypervascularity, and loss of the retroplacental clear zone.
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      ,
      • Rac M.W.
      • Moschos E.
      • Wells C.E.
      • McIntire D.D.
      • Dashe J.S.
      • Twickler D.M.
      Sonographic findings of morbidly adherent placenta in the first trimester.
      ,
      • Ballas J.
      • Pretorius D.
      • Hull A.D.
      • Resnik R.
      • Ramos G.A.
      Identifying sonographic markers for placenta accreta in the first trimester.
      ,
      • Cali G.
      • Forlani F.
      • Foti F.
      • et al.
      Diagnostic accuracy of first-trimester ultrasound in detecting abnormally invasive placenta in high-risk women with placenta previa.
      This last marker is particularly helpful in determining the extent of PAS, carrying a sensitivity of 84.3% and diagnostic odds ratio (DOR) of 23.8 (95% CI, 10.6–57.2).
      • Cali G.
      • Forlani F.
      • Foti F.
      • et al.
      Diagnostic accuracy of first-trimester ultrasound in detecting abnormally invasive placenta in high-risk women with placenta previa.
      For cases that were ultimately determined to be placenta percreta at the time of delivery, the sensitivity of this marker was 92.1% with a DOR of 20.4 (95% CI, 6.0–108.7). Placental lacunae and posterior bladder wall interruption or abnormalities were also noted in the late first trimester in cases of percreta, each with sensitivities between 80% and 90%.
      • Cali G.
      • Forlani F.
      • Foti F.
      • et al.
      Diagnostic accuracy of first-trimester ultrasound in detecting abnormally invasive placenta in high-risk women with placenta previa.
      Anterior placentation at the first-trimester sonographic evaluation is more common in women with PAS at delivery.
      • Calì G.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      Changes in ultrasonography indicators of abnormally invasive placenta during pregnancy.
      ,
      • Rac M.W.
      • Moschos E.
      • Wells C.E.
      • McIntire D.D.
      • Dashe J.S.
      • Twickler D.M.
      Sonographic findings of morbidly adherent placenta in the first trimester.
      ,
      • Ballas J.
      • Pretorius D.
      • Hull A.D.
      • Resnik R.
      • Ramos G.A.
      Identifying sonographic markers for placenta accreta in the first trimester.
      Similar to findings in the second and third trimesters, the presence of multiple PAS markers in the first trimester increased the diagnostic accuracy.
      • D’Antonio F.
      • Timor-Tritsch I.E.
      • Palacios-Jaraquemada J.
      • et al.
      First-trimester detection of abnormally invasive placenta in high-risk women: systematic review and meta-analysis.
      • Cali G.
      • Forlani F.
      • Foti F.
      • et al.
      Diagnostic accuracy of first-trimester ultrasound in detecting abnormally invasive placenta in high-risk women with placenta previa.
      • Panaiotova J.
      • Tokunaka M.
      • Krajewska K.
      • Zosmer N.
      • Nicolaides K.H.
      Screening for morbidly adherent placenta in early pregnancy.

      Second and Third Trimesters

      Placental lacunae

      The presence of placental lacunae has been commonly reported in association with PAS.
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      ,
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      ,
      • Guy G.P.
      • Peisner D.B.
      • Timor-Tritsch I.E.
      Ultrasonographic evaluation of uteroplacental blood flow patterns of abnormally located and adherent placentas.
      Often described as numerous, large, and irregular echolucencies within the parenchyma of the placenta, placental lacunae should raise the concern for underlying PAS.
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      ,
      • Guy G.P.
      • Peisner D.B.
      • Timor-Tritsch I.E.
      Ultrasonographic evaluation of uteroplacental blood flow patterns of abnormally located and adherent placentas.
      Previous studies in PAS differ substantially in the definition of lacunae with regard to the required size, number, and presence of blood flow in lacunae. Lacunar blood flow has been described as low-velocity flow in some reports, although others report turbulent high-velocity flow.
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      ,
      • Calì G.
      • Giambanco L.
      • Puccio G.
      • Forlani F.
      Morbidly adherent placenta: evaluation of ultrasound diagnostic criteria and differentiation of placenta accreta from percreta.
      ,
      • Shih J.C.
      • Palacios-Jaraquemada J.M.
      • Su Y.N.
      • et al.
      Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
      ,
      • El Behery M.M.
      • Rasha L.E.
      • El Alfy Y.
      Cell-free placental mRNA in maternal plasma to predict placental invasion in patients with placenta accreta.
      Finberg and Williams,
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      in their 1992 seminal work on ultrasound markers of PAS, proposed a placental lacunae vascular space grading system, with grade 0 indicating no placental lacunae, grade 1+ including placentas with 1 to 3 small lacunae, grade 2+ containing 4 to 6 larger and irregular lacunae, and grade 3+ describing a placenta with many large and “bizarre-appearing” lacunae throughout (Figure 1). Grade 3+ should raise a high degree of concern for PAS. Yang et al
      • Yang J.I.
      • Lim Y.K.
      • Kim H.S.
      • Chang K.H.
      • Lee J.P.
      • Ryu H.S.
      Sonographic findings of placental lacunae and the prediction of adherent placenta in women with placenta previa totalis and prior cesarean section.
      investigated the association of lacunae with maternal complications in 51 pregnancies at risk of PAS, with previous cesarean delivery and persistent placenta previa. The authors found that the need for cesarean hysterectomy and maternal complications positively correlated with the number of lacunae.
      • Yang J.I.
      • Lim Y.K.
      • Kim H.S.
      • Chang K.H.
      • Lee J.P.
      • Ryu H.S.
      Sonographic findings of placental lacunae and the prediction of adherent placenta in women with placenta previa totalis and prior cesarean section.
      Furthermore, the absence of lacunae in pregnancies with placenta previa and previous cesarean delivery is a reassuring sign with negative predictive values (NPV) ranging from 88% to 100% for PAS.
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      ,
      • Yang J.I.
      • Lim Y.K.
      • Kim H.S.
      • Chang K.H.
      • Lee J.P.
      • Ryu H.S.
      Sonographic findings of placental lacunae and the prediction of adherent placenta in women with placenta previa totalis and prior cesarean section.
      ,
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.

      Abnormal uteroplacental interface

      Abnormal uteroplacental interface has been described as loss of the retroplacental hypoechoic zone, myometrial thinning, and increased vascularity on color Doppler.
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      ,
      • Philips J.
      • Gurganus M.
      • DeShields S.
      • et al.
      Prevalence of sonographic markers of placenta accreta spectrum in low-risk pregnancies.
      ,
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      There is substantial variation in the definition and statistical performance of the loss of the retroplacental hypoechoic zone for predicting PAS.
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      ,
      • Zosmer N.
      • Jauniaux E.
      • Bunce C.
      • Panaiotova J.
      • Shaikh H.
      • Nicholaides K.H.
      Interobserver agreement on standardized ultrasound and histopathologic signs for the prenatal diagnosis of placenta accreta spectrum disorders.
      ,
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      ,
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      The classic definition of myometrial thinning is a retroplacental myometrial thickness of <1 mm. However, only 50% of cohort studies of PAS provided a working definition of this marker.
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      ,
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.
      In addition, myometrial thinning is often seen in advancing gestation and can be more pronounced in women with previous cesarean delivery.
      • Hoffmann J.
      • Exner M.
      • Bremicker K.
      • Grothoff M.
      • Stumpp P.
      • Stepan H.
      Comparison of the lower uterine segment in pregnant women with and without previous cesarean section in 3 T MRI.
      This marker can be iatrogenically produced and/or exaggerated with undue transducer pressure, highlighting the need to minimize transducer pressure on the abdomen when examining the placenta.
      • Collins S.L.
      • Ashcroft A.
      • Braun T.
      • et al.
      Proposal for standardized ultrasound descriptors of abnormally invasive placenta (AIP).
      ,
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.

      Uterovesical interface

      Uterovesical interface markers include bridging vessels, increased vascularity between the uterus and bladder, and interruption of the bladder wall. Bridging vessels represent neovascularity atop the uterine serosa and frequently within the uterovesical interface, depending on placental position.
      • Levine D.
      • Hulka C.A.
      • Ludmir J.
      • Li W.
      • Edelman R.R.
      Placenta accreta: evaluation with color Doppler US, power Doppler US, and MR imaging.
      ,
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.
      ,
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      The color Doppler finding of neovascularity is found in most cases of PAS and reflects the engorged myometrial vessels in the area of placentation. The hypervascular uterovesicle interface also reflects the dilation of the uteroplacental vasculature and the chaotic vascular growth and flow within this space.
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      Sensitivity and specificity of hypervascular uterovesical interface are variably reported as ranging from 11% to 100% and 36% to 100%, respectively.
      • Bowman Z.S.
      • Eller A.G.
      • Kennedy A.M.
      • et al.
      Accuracy of ultrasound for the prediction of placenta accreta.
      ,
      • Japaraj R.P.
      • Mimin T.S.
      • Mukudan K.
      Antenatal diagnosis of placenta previa accreta in patients with previous cesarean scar.
      ,
      • Haidar Z.A.
      • Papanna R.
      • Sibai B.M.
      • et al.
      Can 3-dimensional power Doppler indices improve the prenatal diagnosis of a potentially morbidly adherent placenta in patients with placenta previa?.
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      • Twickler D.M.
      • Lucas M.J.
      • Balis A.B.
      • et al.
      Color flow mapping for myometrial invasion in women with a prior cesarean delivery.
      • Maged A.M.
      • Abdelaal H.
      • Salah E.
      • et al.
      Prevalence and diagnostic accuracy of Doppler ultrasound of placenta accreta in Egypt.
      • Kumar I.
      • Verma A.
      • Ojha R.
      • Shukla R.C.
      • Jain M.
      • Srivastava A.
      Invasive placental disorders: a prospective US and MRI comparative analysis.
      Bladder varicosities are often seen in the absence of PAS and in the setting of placenta previa.
      • Levine D.
      • Hulka C.A.
      • Ludmir J.
      • Li W.
      • Edelman R.R.
      Placenta accreta: evaluation with color Doppler US, power Doppler US, and MR imaging.
      ,
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      In addition, hypervascularity of the lower uterine segment and/or cervix can be seen in placenta previa without PAS, highlighting the difficulty in assessing this marker. Interruption of the echogenic bladder wall, especially with placental tissue, is a clear marker of PAS as it represents an extension of placental tissue beyond the uterus (Figure 6). Engorged vessels in the uterovesical interface may result in ultrasound echo dropout, thus mimicking placental extension into the uteroplacental interface.
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.

      Miscellaneous markers

      There are numerous other miscellaneous markers for PAS that have been described. Of these, placental bulge, exophytic placental mass, and cervical vascular extension were reviewed by the committee. The placental bulge is described as a deviation of the uterine serosa, away from the expected planes, changing the uterine contour (Figures 5, 6, and 10).
      • Zosmer N.
      • Jauniaux E.
      • Bunce C.
      • Panaiotova J.
      • Shaikh H.
      • Nicholaides K.H.
      Interobserver agreement on standardized ultrasound and histopathologic signs for the prenatal diagnosis of placenta accreta spectrum disorders.
      ,
      • Riteau A.S.
      • Tassin M.
      • Chambon G.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      ,
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.
      In a small study comparing ultrasound and magnetic resonance imaging (MRI) features that may predict placental invasion, the placental bulge was found to have a specificity of 88%, highlighting this marker as a reassuring sign when absent.
      • Riteau A.S.
      • Tassin M.
      • Chambon G.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      An exophytic mass represents a protrusion of placental tissue outside the uterus and is diagnostic of placenta percreta when seen. Similarly, the absence of this finding is reassuring, as it carries an 80% to 100% specificity, albeit with a maximal sensitivity of 42%.
      • Riteau A.S.
      • Tassin M.
      • Chambon G.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      ,
      • Shih J.C.
      • Palacios-Jaraquemada J.M.
      • Su Y.N.
      • et al.
      Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
      ,
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      In 1 systematic review of PAS, only cases of placenta increta and placenta percreta had a placental bulge or an exophytic mass, highlighting their relative rarity in clinical practice.
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      Vascular cervical extension is defined by placental extension into the cervix involving at least the inner one-third, best seen on TVUS. This marker performs poorly, however, as it was identified in greater than 50% of the time in a low-risk cohort without PAS.
      • Philips J.
      • Gurganus M.
      • DeShields S.
      • et al.
      Prevalence of sonographic markers of placenta accreta spectrum in low-risk pregnancies.
      Figure thumbnail gr10
      Figure 10Abnormal uterine contour
      Transabdominal midline sagittal ultrasound imaging with an extended view of a pregnancy with placenta accreta spectrum. Note the presence of a placental bulge and thickening in the lower uterine segment (arrows) and into the bladder (B). Double arrows indicate the difference in the placental thickness in the upper and lower segments of the uterus.
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.

      Combined markers

      When ultrasound markers are combined, their performance improves substantially, yielding a sensitivity of 81.1% (95% CI, 69–94), specificity of 98.9% (95% CI, 98–100), PPV of 90.9% (95% CI, 82–100), and NPV of 97.5 (95% CI, 96–99).
      • Pilloni E.
      • Alemanno M.G.
      • Gaglioti P.
      • et al.
      Accuracy of ultrasound in antenatal diagnosis of placental attachment disorders.
      Thinning of the myometrium and loss of the retroplacental clear zone seem to have the highest interobserver agreements.
      • Zosmer N.
      • Jauniaux E.
      • Bunce C.
      • Panaiotova J.
      • Shaikh H.
      • Nicholaides K.H.
      Interobserver agreement on standardized ultrasound and histopathologic signs for the prenatal diagnosis of placenta accreta spectrum disorders.
      Most data regarding the predictability of PAS ultrasound markers have been derived in single centers with a relatively high volume of PAS cases. The true sensitivity of these markers in the community setting remains unknown.

      Existing Consensus Guidelines

      The European Working Group on Abnormally Invasive Placenta (EW-AIP) and the International Federation of Gynecology and Obstetrics (FIGO) developed language outlining various PAS ultrasound markers and suggested standardized definitions for each.
      • Jauniaux E.
      • Bhide A.
      • Kennedy A.
      • et al.
      FIGO consensus guidelines on placenta accreta spectrum disorders: prenatal diagnosis and screening.
      ,
      • Collins S.L.
      • Ashcroft A.
      • Braun T.
      • et al.
      Proposal for standardized ultrasound descriptors of abnormally invasive placenta (AIP).
      The EW-AIP established a list of 11 PAS ultrasound markers (6 in 2-dimensional [2D] grayscale, 4 in 2D color Doppler, and 1 in 3-dimensional [3D] power Doppler). This was derived from the analysis of 23 manuscripts reviewed by an expert panel. The panel placed importance on defining each PAS marker without ambiguity but did not report on their predictive values.
      • Collins S.L.
      • Ashcroft A.
      • Braun T.
      • et al.
      Proposal for standardized ultrasound descriptors of abnormally invasive placenta (AIP).
      The recent FIGO consensus guidelines for PAS prenatal screening and diagnosis listed the EW-AIP 11 markers along with their definitions. These guidelines did not recommend using certain markers over others, and acknowledged that none carries 100% sensitivity and specificity. The FIGO consensus guidelines also commented on the role of a CSP as the first-trimester precursor to PAS.
      • Jauniaux E.
      • Bhide A.
      • Kennedy A.
      • et al.
      FIGO consensus guidelines on placenta accreta spectrum disorders: prenatal diagnosis and screening.
      Taking these published definitions into account, we reviewed the general utility of each ultrasound marker and utilized the these published definitions when possible and appropriate. We also attempted to consolidate some ultrasound PAS markers to simplify language and streamline definitions.

      Ultrasound Approach and Definitions of Placenta Accreta Spectrum Markers

      General considerations

      We recommend starting the assessment with transabdominal imaging to obtain an overview of placental location and start assessing the regions of concern. TVUS is strongly recommended for the assessment of PAS. Transvaginal imaging optimizes resolution and allows for a detailed assessment of the lower uterine segment, posterior bladder wall, and cervix. The bladder should be partially full. Color Doppler should be utilized to assess for vascularity and placental extension into the uterine wall and surrounding structures. The transducer should be adjusted to operate at the highest clinically appropriate frequency, realizing that there is a trade-off between resolution and beam penetration.
      AIUM-ACR-ACOG-SMFM-SRU practice parameter for the performance of standard diagnostic obstetric ultrasound examinations.
      Ultrasound image magnification should be performed to enhance the visualization of target regions. When assessing the retroplacental region, perpendicular orientation of the angle of insonation and applying minimal transducer pressure are recommended. Given the continuum of disease from CSP to PAS, screening for PAS should begin early in the first trimester and continue throughout the pregnancy until practitioners have concluded whether there is sonographic concern for PAS.

      First trimester

      In the first trimester, a detailed evaluation of the uterus is necessary to determine the location of the gestational sac or placenta (depending on gestational age) in reference to the bladder, internal os, and cesarean scar. When performing TVUS, the maternal bladder should be partially filled, enough to allow for a sonographic window, without overfilling, which can result in distortion of the uterovesical interface. The target area should be magnified to occupy at least one-half of the ultrasound image, and focal zones should be appropriately placed. After 10 weeks of gestation, color Doppler can be used to assess for the presence of hypervascularity and lacunae; when possible, color Doppler should be limited to the placental region and not overlap the fetus. The definition of first-trimester PAS markers and the proposed ultrasound approach are presented in Table 2 and Box 1, respectively.
      Table 2Definitions of placenta accreta spectrum markers in the first trimester of pregnancy
      MarkerDefinition
      Cesarean scar pregnancyGestational sac implantation in part or totally within the cesarean scar.
      Gestational sac may have a teardrop or triangular shape.
      Low implantation pregnancyGestational sac located close to the internal cervical os (up to 8 6/7 weeks of gestation) and/or placental implantation located posterior to a partially filled maternal bladder (up to 13 6/7 weeks of gestation).
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      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 internal cervical 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 and other clinical factors).
      Color Doppler should be limited to the areas of interest and avoid the embryo or fetus whenever possible.


      • 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.
      Shainker. Special Report of the SMFM: Definition of markers and ultrasound examination in pregnancies at risk of PAS. Am J Obstet Gynecol 2021.
      a Color Doppler should be limited to the areas of interest and avoid the embryo or fetus whenever possible.

      Second and third trimesters

      The antenatal diagnosis of PAS is most often made in the second and third trimesters of pregnancy. Classic sonographic markers of PAS are typically described in women with anterior placentae previa and previous cesarean deliveries.
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      ,
      American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine
      Obstetrics Care Consensus No. 7: placenta accreta spectrum.
      Table 3 lists the proposed definitions of PAS ultrasound markers in the second and third trimesters of pregnancy. Other than placenta previa, placenta lacunae are frequently described as classic ultrasound markers of PAS. Lacunae can often be found in low-risk non-PAS pregnancies; however, when present in women with risk factors, they carry the highest sensitivity of all 2D grayscale markers.
      • Philips J.
      • Gurganus M.
      • DeShields S.
      • et al.
      Prevalence of sonographic markers of placenta accreta spectrum in low-risk pregnancies.
      ,
      • D’Antonio F.
      • Iacovella C.
      • Bhide A.
      Prenatal identification of invasive placentation using ultrasound: systematic review and meta-analysis.
      When lacunae are large, numerous, and with irregular borders, their association with PAS is increased.
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      Lacunae tend to congregate near the area of placental invasion; thus, the presence of lacunae blood flow on grayscale and color Doppler is also associated with PAS.
      Table 3Definitions of PAS markers in the second and third trimesters of pregnancy
      MarkerDefinition
      Placental lacunaeIrregular, hypoechoic spaces within the placenta containing vascular flow (which can be seen on grayscale and/or color Doppler imaging).
      The following lacunae findings are associated with high risk of PAS:Multiple (often defined as ≥3) • Large size• Irregular borders• High velocity
      Some studies suggest a velocity of >15 cm/s as the threshold for high peak systolic velocity
      and/or turbulent flow within
      Abnormal uteroplacental interfaceLoss of the retroplacental hypoechoic zone between the placenta and myometrium.
      This space represents the uterine decidua and has been described as the “clear zone.”
      This marker is often located along the posterior bladder wall resulting in partial or complete interruption or irregularities of the uterovesical interface.
      Thinning of the retroplacental myometrium (previously described as myometrial thickness of <1 mm).
      Abnormal uterine contour (placental bulge)Placental tissue distorting the uterine contour resulting in a bulge-like appearance.
      Exophytic massPlacental tissue extruding beyond the uterine serosa.
      Bridging vesselVessel that extends from the placenta across the myometrium and beyond the uterine serosa.
      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.
      a Some studies suggest a velocity of >15 cm/s as the threshold for high peak systolic velocity
      b This space represents the uterine decidua and has been described as the “clear zone.”
      Sonographic assessment of the uteroplacental interface includes evaluation of the loss of the retroplacental hypoechoic zone and thinning of the retroplacental myometrium.
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      ,
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      ,
      • Zosmer N.
      • Jauniaux E.
      • Bunce C.
      • Panaiotova J.
      • Shaikh H.
      • Nicholaides K.H.
      Interobserver agreement on standardized ultrasound and histopathologic signs for the prenatal diagnosis of placenta accreta spectrum disorders.
      ,
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      ,
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      ,
      • Jauniaux E.
      • Collins S.
      • Burton G.J.
      Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging.
      The uteroplacental interface is often inferior to the posterior bladder wall. Similar to other PAS markers in women with an anterior placenta and previous cesarean delivery, the uteroplacental interface is best seen utilizing a combination of transabdominal and transvaginal imaging with a partially filled bladder.
      The uterine contour is optimally evaluated when the placenta is anterior, utilizing a partially filled bladder as the acoustic window. This marker, often referred to as the “placental bulge,” can be seen on both transabdominal and transvaginal imaging. The bulge does not always reflect a “through-and-through” defect of the uterine wall; rather, it highlights the area of scar dehiscence and thinning of the myometrium in areas of PAS.
      • Hubinont C.
      • Mhallem M.
      • Baldin P.
      • Debieve F.
      • Bernard P.
      • Jauniaux E.
      A clinico-pathologic study of placenta percreta.
      ,
      • Jauniaux E.
      • Collins S.L.
      • Jurkovic D.
      • Burton G.J.
      Accreta placentation: a systematic review of prenatal ultrasound imaging and grading of villous invasiveness.
      ,
      • Dannheim K.
      • Shainker S.A.
      • Hecht J.L.
      Hysterectomy for placenta accreta; methods for gross and microscopic pathology examination.
      Although this finding has not been correlated specifically with increased morbidity or mortality, its presence raises the concern for extrauterine placental extension (placenta percreta). Color Doppler is often helpful to determine the extent of vascular invasion.
      Bridging vessels are defined as vessels, identified on color Doppler, that extend from the placenta across the myometrium and/or beyond the uterine serosa. This has been considered as one of the “classic markers” of PAS over the years but has lacked consistency in its definition.
      • Belfort M.A.
      Publications Committee, Society for Maternal-Fetal Medicine
      Placenta accreta.
      ,
      • Bhide A.
      • Sebire N.
      • Abuhamad A.
      • Acharya G.
      • Silver R.
      Morbidly adherent placenta: the need for standardization.
      Typically seen running perpendicular to the long axis of the uterus, bridging vessels are often associated with the presence of a placental bulge with placental tissue extending beyond the uterine serosa.
      • Collins S.L.
      • Ashcroft A.
      • Braun T.
      • et al.
      Proposal for standardized ultrasound descriptors of abnormally invasive placenta (AIP).
      Unlike other markers that can often be seen in cases without PAS, this marker is rarely seen in cases without PAS.
      • Philips J.
      • Gurganus M.
      • DeShields S.
      • et al.
      Prevalence of sonographic markers of placenta accreta spectrum in low-risk pregnancies.
      It is important to note that the placenta is a 3D structure, and thus, comprehensive sonographic assessment is required in pregnancies at risk of PAS. This is best performed by obtaining several parasagittal and transverse planes of the placenta during the ultrasound examination. Special attention should be given to the retroplacental area and the lower segment and cervical regions. This is best achieved with a combined transabdominal and transvaginal approach. Table 4 presents the sonographic approach in the second and third trimesters of pregnancy.
      Table 4Approach to ultrasound examination in the second and third trimesters of pregnancy
      MarkerApproaches
      LacunaeDetailed evaluation of the entire placenta in orthogonal planes.
      Lacunae should be evaluated using grayscale and color Doppler imaging.
      Doppler assessment should generally be performed with a low-velocity scale, low wall filters, and high gain to maximize detection of flow
      Some studies suggest a velocity of >15 cm/s as the threshold for high peak systolic velocity
      (adjusting as needed for body habitus and other clinical factors).
      Abnormal uteroplacental interfaceEvaluation of the uteroplacental interface is optimized by perpendicular orientation of the transducer to the area of interest with minimal transducer pressure.
      Transvaginal ultrasound is recommended in the setting of an anterior, low-lying placenta or placenta previa.
      Imaging should be performed with a partially filled maternal bladder.
      Optimization of gain settings to help differentiate between placental and myometrial tissues.
      The area of interest should be magnified so that it occupies at least half of the ultrasound image with the focal zone at appropriate depth.
      Myometrial measurement should be made perpendicular to the long axis of the uterus and measured at the thinnest site (commonly along the uterine scar).
      Abnormal uterine contour (placental bulge)Placental tissue distorting the uterine contour resulting in a bulge-like appearance (this is best appreciated in a midsagittal plane of the uterus).
      Exophytic massPlacental tissue visualized beyond the uterine serosa.
      Bridging vesselDoppler assessment of vessels extending from the placenta across the myometrium and beyond the uterine serosa.
      Bridging vessels need to be differentiated from bladder varicosities, which are not placental in origin and do not increase risk of 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.
      a Some studies suggest a velocity of >15 cm/s as the threshold for high peak systolic velocity
      b Bridging vessels need to be differentiated from bladder varicosities, which are not placental in origin and do not increase risk of placenta accreta spectrum.

      Discussion

      This document, endorsed by AIUM, SMFM, ACR, and GOHO, supported by ACOG and ISUOG, and approved by SRU, with ARDMS participating in the development and production of the document, presents a consensus-based approach to ultrasound examination and assessment of PAS. Pregnancies with PAS are at a significantly increased risk of maternal and fetal morbidities and mortalities. Prenatal detection of PAS reduces pregnancy complications and improves outcomes.
      • Shamshirsaz A.A.
      • Fox K.A.
      • Salmanian B.
      • et al.
      Maternal morbidity in patients with morbidly adherent placenta treated with and without a standardized multidisciplinary approach.
      ,
      American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine
      Obstetrics Care Consensus No. 7: placenta accreta spectrum.
      ,
      • Erfani H.
      • Fox K.A.
      • Clark S.L.
      • et al.
      Maternal outcomes in unexpected placenta accreta spectrum disorders: single-center experience with a multidisciplinary team.
      ,
      • Eller A.G.
      • Bennett M.A.
      • Sharshiner M.
      • et al.
      Maternal morbidity in cases of placenta accreta managed by a multidisciplinary care team compared with standard obstetric care.
      Several PAS markers have been identified and studied. There has been an effort to standardize the definitions of PAS markers, with the ultimate goal of improving risk stratification by ultrasound resulting in improved prenatal detection and thus positively impacting pregnancy outcomes. This task force, assembled by SMFM with representation from multiple societies and organizations, provides definitions for PAS markers along with a standardized approach to the ultrasound examination in pregnancies at risk of PAS.
      It is important to recognize that the proposed definitions of PAS markers are based on the current literature, along with expert opinion when data are lacking. As ultrasound technology advances with improved tools, the detection of abnormal placental invasion and vasculature should be greatly enhanced. Advancement in ultrasound technology may render the definitions of some existing PAS markers obsolete. An example is the current definition of abnormal placental vasculature. Emerging ultrasound technology has resulted in significant improvements in the sonographic detection of low-velocity vascular flow. Accordingly, this may result in difficulty differentiating normal from abnormal placental flow.
      It is also important to note that many of the markers presented in this document have been studied in women with previous cesarean deliveries and placenta previa. In women without these risk factors, however, the markers are seen often and typically in the absence of PAS.
      • Philips J.
      • Gurganus M.
      • DeShields S.
      • et al.
      Prevalence of sonographic markers of placenta accreta spectrum in low-risk pregnancies.
      As such, the recommended ultrasound approach to women without these risk factors remains largely unknown and is an area of great interest.
      There are several limitations of ultrasound in detecting PAS. Ultrasound is an operator-dependent imaging modality and, thus, is highly dependent on the skills of the examiner performing the ultrasound. The detection rates will depend on placental location and maternal imaging conditions that impact sonographic visualization of markers. A standardized approach to the performance of the ultrasound examination along with consensus-based definitions of PAS markers will result in more consistency in diagnosis and allows for the evaluation of markers across centers to improve diagnostic performance. Despite optimizing a systematic approach to ultrasound examination for PAS markers, inherent limitations of ultrasound may diminish detection rates. These include posterior placentation, with limited sound penetration and resolution; elevated maternal BMI; and uterine leiomyomata. The task force also identified research gaps for sonographic markers of PAS (Box 2). We hope that future research will use the definitions hereby provided along with a standardized approach to the ultrasound examination to facilitate data comparison. In addition, although the scope of this task force was focused on ultrasound examination, we hope similar efforts are made in the future to provide guidance on the use of MRI for the evaluation of PAS.
      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.
      As PAS has become more prevalent, the need for agreement on the definitions of ultrasound markers and sonographic approach to the patient at risk of PAS is crucial. This document provides necessary steps toward consistency in the definitions of PAS markers and the approach to diagnosis. Accurate antenatal diagnosis is paramount in optimizing maternal and fetal outcomes. Further work will be needed to measure the impact of the proposed standardized definitions, along with the approach to ultrasound examination.

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      Linked Article

      • January 2021 (vol. 224, no. 1, pages B2, B3, B12, B13)
        American Journal of Obstetrics & GynecologyVol. 225Issue 1
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          Shainker SA, Coleman B, Timor-Tritsch IE, et al. Special Report of the Society for Maternal-Fetal Medicine Placenta Accreta Spectrum Ultrasound Marker Task Force: consensus on definition of markers and approach to the ultrasound examination in pregnancies at risk for placenta accreta spectrum. Am J Obstet Gynecol 2021;224(1):B2-B14.
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