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2 Placenta accreta spectrum: pathophysiology 57
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4 and evidence-based anatomy for prenatal 59
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6 ultrasound imaging 61
7 Q9 Q1 Eric Jauniaux, MD, PhD, FRCOG; Sally Collins; Graham J. Burton 62
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9 64
Introduction
10 65
The first case series of placenta accreta Placenta accreta spectrum is a complex obstetric complication associated with high
11 66
(PA) was published in 1937 by Irving and maternal morbidity. It is a relatively new disorder of placentation, and is the consequence
12 1 67
Hertig. They reviewed 18 cases, which of damage to the endometrium-myometrial interface of the uterine wall. When first
13 68
they described clinically as “the described 80 years ago, it mainly occurred after manual removal of the placenta, uterine
14 69
abnormal adherence of the afterbirth in curettage, or endometritis. Superficial damage leads primarily to an abnormally adherent
15 70
whole or in parts to the underlying placenta, and is diagnosed as the complete or partial absence of the decidua on his-
16 71
uterine wall” and histologically as “the tology. Today, the main cause of placenta accreta spectrum is uterine surgery and, in
17 72
complete or partial absence of the particular, uterine scar secondary to cesarean delivery. In the absence of endometrial
18 73
decidua basalis,” signs that are still used reepithelialization of the scar area the trophoblast and villous tissue can invade deeply
19 74
today. They described all their cases as within the myometrium, including its circulation, and reach the surrounding pelvic or-
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“vera” or “adherenta” where the villi gans. The cellular changes in the trophoblast observed in placenta accreta spectrum are
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were attached to the surface of the probably secondary to the unusual myometrial environment in which it develops, and not
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myometrium without invading it. a primary defect of trophoblast biology leading to excessive invasion of the myometrium.
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The grading classification of PA ac- Placenta accreta spectrum was separated by pathologists into 3 categories: placenta
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cording to the depth of villous invasive- creta when the villi simply adhere to the myometrium, placenta increta when the villi
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ness inside the myometrium was invade the myometrium, and placenta percreta where the villi invade the full thickness of
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introduced by modern pathologists in the myometrium. Several prenatal ultrasound signs of placenta accreta spectrum were
27 2-4 82
the 1960s. They separated PA into 3 reported over the last 35 years, principally the disappearance of the normal uteropla-
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categories: placenta creta when the villi cental interface (clear zone), extreme thinning of the underlying myometrium, and
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simply adhere to the myometrium, vascular changes within the placenta (lacunae) and placental bed (hypervascularity). The
30 85
placenta increta (PI) when the villi pathophysiological basis of these signs is due to permanent damage of the uterine wall as
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invade the myometrium, and placenta far as the serosa, with placental tissue reaching the deep uterine circulation. Adherent
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percreta (PP) where the villi invade the and invasive placentation may coexist in the same placental bed and evolve with
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full thickness of the myometrium advancing gestation. This may explain why no single, or set combination of, ultrasound
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½F1 (Figure 1). This terminology is still used sign(s) was found to be specific for the depth of abnormal placentation, and accurate for
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by most pathologists. It is, however, the differential diagnosis between adherent and invasive placentation. Correlation of
36 91
often impossible to clinically differen- pathological and clinical findings with prenatal imaging is essential to improve screening,
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tiate between these categories, especially diagnosis, and management of placenta accreta spectrum, and standardized protocols
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need to be developed.
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40 Q2 From EGA Institute for Women’s Health, Faculty Key words: cesarean delivery, increta, percreta, placenta accrete, prenatal diagnosis, 95
41 of Population Health Sciences, University ultrasound imaging 96
College London, London (Dr Jauniaux); Nuffield 97
42
Department of Obstetrics and Gynecology,
43 University of Oxford, and the Fetal Medicine Unit,
98
44 John Radcliffe Hospital, Oxford (Dr Collins); and 99
45 Center for Trophoblast Research, Department as they may coexist in the same placental In PAS, the lack of a plane of cleavage 100
46 of Physiology, Development, and Neuroscience, bed (Figure 2), and confusion frequently between the placental basal plate and the ½F2 101
University of Cambridge, Cambridge occurs among clinicians regarding the uterine wall leads to major hemorrhage 102
47
48
(Dr Burton); United Kingdom. difference between the terms “accrete” if an attempt is made to forcibly 103
49
Received May 26, 2017; accepted May 31, and “creta.” Given the lack of interna- remove villous tissue embedded within 104
2017.
50 tional consensus on nomenclature, for the myometrium.5-8 The severity of the 105
The authors report no conflict of interest. the purposes of this review, we refer to it complications varies according to the
51 106
Corresponding author: Eric Jauniaux, MD, PhD, as the PA spectrum (PAS), which in- depth of villous invasion. In PP, not only
52 107
FRCOG. e.jauniaux@ucl.ac.uk
53 cludes both abnormal adherence and is there potential villous invasion of 108
0002-9378/$36.00 abnormal invasion. We then use placenta surrounding pelvic organs, but excessive
54 ª 2017 Elsevier Inc. All rights reserved. 109
55 http://dx.doi.org/10.1016/j.ajog.2017.05.067 creta, PI, and PP for specific examples neovascularity is often present making 110
where the histology is known. any surgical procedure technically

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111 167
112 population studies indicated that it re- 168
FIGURE 1
113
Q7 mains undiagnosed before delivery in 169
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114 between half19,20 and two thirds21 of 170
115 cases. The cost and limited access of MRI 171
116 make it impractical as a screening tool, 172
117 and ultrasound has therefore become 173
118 essential in identifying women at high 174
119 risk of PAS and tailoring their manage- 175
120 ment. Although many ultrasound diag- 176
121 nostic signs have been described, wide 177
122 heterogeneity in both study design and 178
123 terminology used by different authors 179
124 has made it difficult to define the ultra- 180
125 sound markers that enable the different 181
126 grades of villous adhesion or invasion to 182
127 be distinguished.18 In this review, we 183
128 evaluated the pathophysiology of 184
129 different ultrasound signs associated 185
130 with PAS to better understand their 186
131 relevance to prenatal screening and 187
132 diagnosis of accreta placentation. 188
133 189
134 Pathophysiology of the PAS 190
135 Several concepts have been proposed to 191
136 explain why and how PAS occurs. The 192
137 oldest concept is based on a theoretical 193
138 primary defect of trophoblast biology 194
139 leading to excessive invasion of the 195
140 myometrium. The current prevailing 196
141 hypothesis is that a secondary defect of 197
142 the endometrium-myometrial interface 198
143 leads to a failure of normal decidualiza- 199
144 tion in the area of a uterine scar, allowing 200
145 abnormally deep placental anchoring 201
146 villi and trophoblast infiltration.5 There 202
147 is no doubt that the decidua normally 203
148 regulates trophoblast invasion, as evi- 204
149 denced by the aggressive invasion of the 205
150 muscular and serosal layers seen at sites 206
151 of ectopic implantation in the fallopian 207
152Q8 Anterior placenta (P) previa on cesarean scar and different grades of P previa accreta: creta (PC) tube22 or in the abdomen.23 208
153 where P villi adhere to myometrium (M); increta (PI) where villi invade M; and percreta (PP) where villi 209
154 invade entire M and cross uterine serosa (S). Scar implantation 210
155 Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017.
During the secretory phase of the 211
156 menstrual cycle, the endometrium 212
157 transforms into a well-vascularized 213
158 receptive tissue, which is characterized 214
159 difficult. Multidisciplinary teamwork PAS was reported in 1967 by Sadovsky by the proliferation and differentiation 215
160 and operator experience has been shown et al13 using radioisotope placentog- of the stromal cells into decidual cells, 216
161 to reduce collateral damage, with several raphy, and the first prenatal ultrasound the infiltration of maternal immune 217
162 studies demonstrating that maternal description was made by Tabsh et al14 cells, and vascular remodeling of the 218
163 morbidity is significantly reduced by in 1982. endometrial vessels.24,25 Decidualization 219
164 delivery in a specialist center.9-12 Thus, Ultrasound imaging and magnetic of the endometrium stroma precedes 220
165 the prenatal diagnosis of PAS has resonance imaging (MRI) are now blastocyst attachment and trophoblast 221
166 become essential to its management and commonly used for the prenatal diag- infiltration. The process is complex and 222
outcome. The first prenatal diagnosis of nosis of PAS.15-18 However, recent involves many local uterine components

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224 and external maternal cells and hor- 280
FIGURE 2
225 mones. It is essential for implantation 281
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226 and normal placental development. 282
227 The development of PAS has been 283
228 mainly linked to surgical damage, which 284
229 disrupts the integrity of the uterine 285
230 endometrium and smooth muscle layers 286
231 of the myometrium. The increased use of 287
232 cesarean delivery (CD) has had a direct 288
233 effect on the incidence of all grades of 289
234 accreta placentation, but cases have been 290
235 described following smaller and more 291
236 superficial damage to the uterine wall 292
237 such as that associated with uterine 293
curettage, manual removal of the Anterior placenta previa accreta combining areas of abnormal adherence and invasion: creta (PC),
238 increta (PI), and percreta (PP).
294
239 placenta, or postpartum endome- 295
240 tritis.1,3-5 Cases of PAS were even D, decidua; M, myometrium; S, serosa.
296
described in primigravida women with Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017.
241 297
242 no surgical history, but presenting with a 298
243 uterine pathology such as bicornuate 299
244 uterus, adenomyosis, submucous fi- that the uterine vascular resistance is placentation with no clinical symptoms 300
245 broids, or myotonic dystrophy.3-5 These increased, while the volume blood flow is in early pregnancy allowing the preg- 301
246 latter cases suggest that microscopic de- decreased, compared to women with a nancy to continue in the second 302
247 fects of the endometrium or in- previous vaginal birth.29 These data 303
248 terferences with its normal biological suggest that the blood circulation 304
249 functions may lead to abnormal villous around the scar is impaired. Poor FIGURE 3
305
tissue adhesion or even invasion. vascularization of the scar area may lead - - -

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250 306
251 A uterine scar may range from a small or contribute to permanent focal myo- 307
252 defect of the decidua and superficial metrial degeneration, as well as reduced 308
253 myometrium to a wide and deep defect or absent reepithelialization of the scar 309
254 of the myometrium with clear loss of area. 310
255 substance from the endometrial cavity Prior CD and, in particular, prior 311
256 down to the uterine serosa.26 In women prelabor CD are associated with a 2-fold 312
257 with a history of prior CD, scar defects increase in the risk of placenta previa in 313
258 were found to range between 20-65% of subsequent pregnancies.30 Only 4.1% of 314
259 the myometrium after delivery on women with 1 prior CD presenting with 315
260 transvaginal ultrasound. Women with a placenta previa will also have PAS,31 316
261 residual myometrial thickness of <50% demonstrating that normal implanta- 317
262 of the adjacent myometrium are more tion can occur over scar tissue. A cesar- 318
263 likely to develop chronic complications ean scar pregnancy is the implantation of 319
264 such as intermenstrual spotting.27 The a sonographically detectable gestational 320
265 myometrial fibers around a scar often sac into a uterine scar. It has been sug- 321
266 show hyalinization or degenerative gested that a scar pregnancy is not a 322
267 changes, with a local increase in fibrous separate entity from PAS, but rather a 323
268 tissue and infiltration by inflammatory continuum of the same condition.32,33 324
269 cells.3 The comparison of ultrasound However, not all scar pregnancies 325
270 features of uterine cesarean scar with require major surgery or life-saving 326
271 histological findings has shown that hysterectomy at the time of delivery,34 327
272 large and deep myometrial defects are suggesting that in some cases the scar 328
Placental cotyledon in A, normal and B, increta
273 often associated with absence of reepi- defect can be large enough to host an 329
placentation reaching deep myometrial circula-
274 thelialization of the scar area.28 Leuko- entire gestational sac without the villi of 330
tion. Note distortion of normal cotyledon anat-
275 cyte recruitment to the endometrium the definitive placenta implanting deep 331
omy in increta placentation with loss of
276 during the secretory phase may also be into the remaining myometrium or into 332
intercotyledon septa and formation of lacuna (L).
277 affected by the presence of a CD scar. A the uterine serosa. This also suggests that 333
Jauniaux. Pathophysiology and ultrasound imaging of
278 recent study of the uterine circulation in if the gestational sac implants by the side placenta accreta spectrum. Am J Obstet Gynecol 2017. 334
women with a previous CD has shown of a CD scar this may lead to focal accreta

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335 391
336 decidual stroma. These cells are collec- submucous fibroid, will probably lead to 392
FIGURE 4
337 tively called extravillous trophoblast mainly superficial abnormally adherent 393
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338 (EVT). They differentiate primarily into placentation. This possibly explains the 394
339 interstitial and endovascular sub- very rare cases of PAS reported in pri- 395
340 populations that migrate through the miparous women.3-5 396
341 decidual stroma and down into the lu- Stronger labeling of the villous syn- 397
342 mens of the spiral arteries, respectively. cytiotrophoblast for epidermal growth 398
343 Interstitial EVT invade the uterine wall factor receptor was observed in PAS 399
344 as far as the inner third of the uterine compared to normal pregnancies,43-45 400
345 myometrium, where they fuse to form suggesting that abnormal villous adher- 401
346 multinucleated trophoblast giant cells ence develops as a result of aberrant 402
347 (MNGC).38 This area is known as the expression of growth-, angiogenesis-, 403
348 junctional zone (JZ).37 Migration of the and invasion-related factors in tropho- 404
349 EVT is facilitated by their secretion of a blast populations. However, there was no 405
Microscopic view of placental bed from hyster-
350 variety of matrix metalloproteinases change in staining intensity for EVT, and 406
ectomy specimen at 34 weeks in pregnancy
351 comprising collagenases, gelatinases, the functional significance of differences 407
complicated by placenta previa increta (hema-
and stromelysins.4 During normal in receptor expression between the syn-
352 toxylin-eosin stain 4) showing disruption of 408
353 migration these enzymes break down the cytiotrophoblast, which has no invasive 409
decidua (D) by placental villi (PV) and very thin
354 extracellular matrix between the capacity, and the invasive EVT in PAS is 410
myometrium (M).
355 decidual cells, but can equally well digest difficult to interpret. Increased vascular 411
Jauniaux. Pathophysiology and ultrasound imaging of
356 placenta accreta spectrum. Am J Obstet Gynecol 2017. scar tissue if implantation overlies a endothelial growth factor and phos- 412
357 myometrial lesion. photyrosine immunostaining was also 413
358 In accreta placentation, EVT cells observed in EVT cells from placenta 414
359 trimester without being diagnosed as invade the uterine wall to a greater previa accreta.46 These cells also coex- 415
360 PAS. depth, are hypertrophic, and their pressed vimentin and cytokeratin-7, an 416
361 Overall, these data support the numbers are increased whereas the epithelial-to-mesenchymal transition 417
362 concept that macroscopic and/or number of MNGC is reduced.39-41 It is feature and tumorlike cell phenotype.46 418
363 microscopic disruptions to the uterine not clear from these observations One of the mechanisms proposed by 419
364 cavity inflict permanent damage to the whether the EVTs are genuinely hyper- which EVTs lose their invasive pheno- 420
365 endometrium-myometrial interface. plastic since cell densities rather than type is through syncytial-type fusion 421
366 This damage has a primary impact on total numbers were reported. In PAS, the into MNGC.35 More recently, lower 422
367 the biology of the scar area creating proliferative index and apoptotic rate are immunostaining for soluble fms-like 423
368 conditions for preferential attachment of similar to normally implanted placentas tyrosine kinase, which is a potent anti- 424
369 the blastocyst to the scar tissue as well as and so it may be that the normal number angiogenic growth factor, was found in 425
370 a secondary impact on decidualization of of EVTs is packed into a smaller volume the EVT cells in cases of PAS.47 These 426
371 the endometrium around the scar. The of decidua. Deeper trophoblast invasion findings suggest that vascular endothelial 427
372 absence of decidua in first-trimester of the myometrium and infiltration of growth factor and soluble fms-like 428
373 cases of PAS35 refutes previous sugges- chorionic villi into myometrial vascular tyrosine kinase play a pivotal role in the 429
374 tions that the decidual layer is normal at spaces was recently documented in both pathological programming of EVTs to- 430
375 the beginning of gestation and atrophies PI and PP.42 These events lead to an ward increased motility and invasiveness 431
376 as pregnancy progresses. absence of the normal plane of cleavage in PAS. The cellular changes in the 432
377 above the decidua basalis, thus, pre- trophoblast observed in PAS are prob- 433
378 Scar placentation venting placental separation after de- ably also secondary to the unusual 434
379 Human placentation is almost unique livery in cases of PAS (Figure 5). Deeper myometrial environment in which it 435
380 among mammals in that it is physio- placental tissue invasion may not be due develops. In particular, the loss of the Q3 436
381 logically highly invasive. Soon after to a further invasion of EVT in the physiological uteroplacental oxygen ½F3 ½F4 437
382 implantation, mononuclear cyto- uterine wall. This may arise secondary to gradient can have a direct impact on ½F5 438
383 trophoblast cells proliferate at the tips of dehiscence of a scar, possibly under the cytotrophoblastic differentiation pat- 439
384 anchoring villi, and form columns of actions of matrix metalloproteinases, terns.48,49 There may also be differences 440
385 cells that merge together to form the leading to the presence of chorionic in the local populations of maternal 441
386 cytotrophoblastic shell that encapsulates villi deep within the uterine wall, and immune cells that interact with the EVT, 442
387 the conceptus.36,37 Those cells on the thus giving EVTs greater access to the notably the uterine natural killer cells 443
388 outer surface that make contact with the deep myometrium (Figure 4). Overall, that release cytokines regulating 444
389 decidua undergo a partial epithelial- superficial damage, such as after a invasion.50 445
390 mesenchymal transition, lose their pro- curettage, or distortion of the deciduo- Overall, these findings emphasize the 446
liferative potential, and invade the myometrial layer, such as with a role of the decidua in modulating

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448 FIGURE 5 504
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458 514
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460 516
461 517
462 Microscopic views of placental bed from hysterectomy specimens with placenta in situ (Boyd Collection, Center for Trophoblast Research, University of 518
463 Cambridge, Cambridge, United Kingdom). A, Specimen H1094 CRL 73 mm showing thick decidua (D) between placental villi (PV) and myometrium (M) 519
464 (hematoxylin-eosin stain 2.5). B and C, Specimen H751 CRL 260 mm. D is much thinner (hematoxylin-eosin stain 2.5) and absent in some areas 520
465 (reticulin 10). Scale bar ¼ 0.5 mm (A and B) or 0.1 mm (C). 521
Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017.
466 522
467 523
468 524
469 placentation. Its replacement by scar lumen of the uterus. As they reach the JZ, In normal placentation, EVT cells 525
470 tissue results in secondary dysfunctional each radial artery gives off lateral penetrate the JZ via the action of their 526
471 decidualization and trophoblastic over- branches, the basal arteries, that supply proteases on the intercellular ground 527
472 invasiveness in PAS. There is no firm the myometrium and deeper basalis part substance, affecting its mechanical and 528
473 evidence of a primary trophoblastic of the endometrium. The vessel then electrophysiological properties. The 529
474 biological defect in any of the different continues as a spiral artery. Each spiral structure and properties of the walls of 530
475 grades of PAS, unlike those observed in artery gives off small branches supplying the spiral arteries are also changed.37 The 531
476 placental insufficiency and hydatidiform the capillary plexus surrounding the remodeling of the arteries is character- 532
477 moles. uterine glands. In the nonpregnant state, ized by the progressive loss of myocytes 533
478 the walls of the spiral and radial arteries from their media and their internal 534
479 Vascular remodeling contain large quantities of smooth elastic lamina, which are replaced by 535
480 Uterine arteries provide the main blood muscle equipped with a rich autonomic fibrinoid material. Consequently, these 536
481 supply to the uterus.51 They give rise to innervation that makes them highly vessels lose their responsiveness to 537
482 the arcuate arteries that in turn give rise responsive to both exogenous and circulating vasoactive compounds and 538
483 to the radial arteries directed toward the endogenous adrenergic stimuli.49 become a low-resistance vascular 539
484 540
485 541
486 542
FIGURE 6
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490 546
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496 552
497 553
498 554
499 555
500 Transabdominal ultrasound longitudinal views of same part of placental (P) bed of low-lying P at 32 weeks using same machine settings. Full bladder (B) 556
501 with A, minimal and B, increased probe pressure. C, Empty B and minimal probe pressure. Note changes in clear zone (arrows). 557
502 Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017. 558

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559 615
560 Prenatal imaging and macroscopic 616
FIGURE 7
561 observation at delivery of the hyper- 617
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562 vascularity of the placental bed in most 618
563 cases of invasive placentation suggest a 619
564 phenomenon of neovascularization 620
565 around the scar area in addition to the 621
566 vasodilatation of the radial and/or 622
567 arcuate uterine vasculature in the accreta 623
568 area. 624
569 625
570 Ultrasound changes seen in PAS 626
571 A wide variety of different medical and 627
572 nonmedical terms have been used to 628
573 describe placental lesions on ultrasound 629
574 since the first description of a complete 630
575 hydatidiform mole by MacVicar and 631
576 Donald53 in 1963. The ultrasound fea- 632
Transabdominal ultrasound longitudinal views of placental bed at 34 weeks in pregnancy after 3 prior
577 tures of PAS were essentially described by 633
cesarean deliveries showing changes on clear zone (arrows) with probe pressure (right).
578 Finberg and Williams54 for gray-scale 634
Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017.
579 and by Chou et al55,56 for color 635
580 Doppler imaging (CDI), and both have 636
581 been used by many authors of subse- 637
582 network through dilatation.49 This probably due to atrophy of the uterine quent cases reports and cohort series.18 638
583 transformation, termed “physiological circulation within the scar area in Very few authors reported on the use of 639
584 changes,” results in the metamorphosis nonpregnant women with prior CD.29 transvaginal sonography in PAS outside 640
585 of small-caliber spiral vessels into flaccid There is no clinical evidence of utero- the location and follow-up of placenta 641
586 distended arteries with a 5- to 10-fold placental insufficiency and impairment previa accreta.57 Thus, most case reports 642
587 dilation at the vessel mouth (Figure 3). of fetal growth associated with any of the and cohort studies described ultrasound 643
588 This dilatation is generalized, but different grades of PAS. This is in images obtained transabdominally from 644
589 nonuniform with considerable variation contrast with the reduction in tropho- PAS diagnosed in the late second and 645
590 in size between arteries within the same blast invasion and failure of conversion early third trimesters. This, and the fact 646
591 specimen, and even at different points of the spiral arteries observed in com- that the resolution of ultrasound imag- 647
592 along individual arteries.49 The terminal plications of pregnancy, such as pre- ing improved over the last 3 decades, 648
593 coils of the spiral arteries are extremely eclampsia and fetal growth restriction. may explain the wide variation in ter- 649
594 dilated, often reaching 2-3 mm in This suggests that in both abnormally minology used to describe the prenatal 650
595 diameter, which represents an approxi- adherent and invasive placentation the ultrasound features associated with PAS. 651
596 mately 4-fold increase in the diameter of incomplete remodeling of the spiral ar- In 2016, The European Working 652
597 the vessel at the myometrial-endometrial teries is limited to the accreta area Group on Abnormally Invasive Placenta 653
598 boundary and within the distal myo- without impacting entire placental proposed standardized descriptions of 654
599 metrium.49 Around 30-50 spiral arteries function. Another possible hypothesis is ultrasound signs used for the prenatal 655
600 are transformed during the first and that in the absence of a decidua, the diagnosis of PAS,58 the pathophysiology 656
601 early second trimesters. In normal normal release of proteases and cyto- of which we analyzed below. 657
602 pregnancies transformation of these kines from activated maternal immune 658
603 uteroplacental arteries is completed cells is missing, impairing arterial Loss of the clear zone 659
604 around midgestation.51 By contrast, the remodeling focally. Loss of the clear zone is used when the 660
605 segment just below the JZ represents the In cases of invasive placentation, an normal hypoechoic retroplacental zone 661
606 limit of physiological trophoblast inva- unusual uteroplacental vasculature was in the myometrium under the placental 662
607 sion and the radial and arcuate arteries observed in which physiological changes bed is not visible on ultrasound. It was 663
608 remain highly vasoreactive throughout were present in large arteries deep in the one of the first signs identified by gray- 664
609 pregnancy.49 myometrium.52 Invasion of larger ves- scale ultrasound imaging in cases of 665
610 If the numbers of interstitial EVTs are sels beyond the level of the JZ is probably PAS.59,60 This sign is supposed to 666
611 increased in PAS, spiral artery remodel- determined by access rather than a pre- represent an abnormal extension of the 667
612 ing has been described as reduced, more existing defect in trophoblastic differ- placental villi through the decidua 668
613 so in cases of PAS without local entiation that would produce basalis into the myometrium and was 669
614 decidua.41,52 Decidua is sometimes uncontrolled invasion of EVT through used by many authors as a marker of PAS 670
completely absent in the accreta area,52 the entire depth of the myometrium.35 on gray-scale ultrasound.18

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671 727
672 The anatomy of the placental bed 728
FIGURE 8
673 changes with advancing gestation. At the 729
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674 end of the first trimester, when the 730
675 definitive placenta is fully formed it is 731
676 made of 2 layers, ie, a thick decidua 732
677 containing numerous glands and the 733
678 terminal coils of spiral arteries and the 734
679 superficial myometrium containing the 735
680 basal arteries. As pregnancy advances, 736
681 the decidual layer becomes thinner and 737
682 discontinuous (Figure 5) and the myo- 738
683 metrium will also become thinner and 739
684 more heterogeneous due to the pro- 740
685 gressive dilatation of the uteroplacental 741
686 circulation. These layers generate an 742
687 echolucent ultrasound signal under the 743
688½F6 placenta (Figure 6). Myometrial thinning secondary to uterine thinning at scar defect. A, Transabdominal ultrasound 744
689 Loss of the clear zone has been re- longitudinal view of placenta (P) previa at 36 weeks showing myometrium defect (arrow) under 745
690 ported in around 70% of cases in those bladder (B). Note absence of clear zone and myometrium in area. B, Findings at surgery later same 746
691 series that included data on the depth of day of “uterine window” (arrow). 747
692 villous myometrial invasion.18 Some Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017. 748
693 authors found that this sign is not ac- 749
694 curate for the diagnosis of PAS as its 750
695 appearance will vary with advancing may partly dehisce or become so thin In true PAS, especially PP, the myo- 751
696 gestation.61,62 In addition, it will also that the placenta can be seen through it metrium appears excessively thin or 752
697 change with the location of the placenta at delivery; this phenomenon should be undetectable due to villous invasion. 753
698 inside the uterine cavity, direct pressure described as a “uterine window” This not only results in the loss of the 754
699 of the ultrasound probes, and/or filling (Figure 8) as it represents deficient clear zone but also changes the echoge- ½F8 755
700½F7 of the bladder (Figures 6 and 7) and may myometrium rather than abnormal nicity of the myometrium itself, result- 756
701 be obscured by the amount of scar tissue placentation. ing in a loss of visual contrast between 757
702 present. 758
703 759
704 Myometrial thinning 760
FIGURE 9
705 Myometrial thinning to <1 mm, or to - - - 761

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706 where the myometrium becomes unde- 762
707 tectable on ultrasound, has been used as 763
708 a prenatal diagnostic sign for PAS63-66 764
709 but it is only reported in 50% of cohort 765
710 studies.18 This can be seen when the 766
711 placenta develops underneath a major 767
712 scar defect, where the myometrium is 768
713 thinner than normal or completely 769
714 replaced by scar tissue. In this case, the 770
715 myometrium will become thinner with 771
716 advancing gestation independently of 772
717 any abnormal villous invasion. This 773
718 thinning effect is more pronounced in 774
719 the third trimester, in particular, >32-34 775
720 weeks when the lower uterine segment is 776
721 further stretched by the combined action 777
722 of fetal presentation and Braxton-Hicks Myometrial thinning secondary to abnormally invasive placenta (P) accreta. A, Transabdominal 778
723 uterine contractions. This may ultrasound longitudinal view of P previa at 36 weeks showing no clear zone or myometrium 779
724 contribute to false-positive diagnoses detectable (arrow) between P and bladder (B). B, Findings at surgery later same day showing 780
725 where extreme myometrial thinning is neovascularization and myometrial distension over accreta area. 781
726 incorrectly diagnosed as abnormal in- Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017. 782
vasion. Occasionally, the myometrium

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784 echogenic cystic lesions) has been asso- 840
FIGURE 10
785 ciated with the development of inter- 841
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- - -
786 villous thrombosis69 and uteroplacental 842
787 insufficiency.70,71 The shape and num- 843
788 ber of lakes will vary with gestational age, 844
789 with the location of the placenta inside 845
790 the uterine cavity, and with direct pres- 846
791 sure of the ultrasound probes 847
792 (Figure 12). 848
793 The difference between the lacunae 849
794 associated with abnormal invasion and 850
795 placental lakes is not clear cut, but 851
796 relates to number, shape, location, and 852
797 Transabdominal ultrasound longitudinal views of placenta (P) previa accreta at 36 weeks. A, “Moth- velocity of the blood flow inside the 853
798 eaten” area with numerous lacunae of different size and shape secondary; and B, high-velocity, space. Finberg and Williams54 854
799 turbulent blood flow within lacunae on color Doppler imaging next to bladder (B). attempted to classify these features, 855
800 Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017. with grade 3 representing the lacunae 856
801 seen with invasive placentation. The 857
802 lacunae are often numerous in one 858
803 placental tissue and myometrium. In transabdominal (Figure 10) and trans- part of the placenta, large and irregular ½F10859
804 invasive placentation, as the villi breach vaginal (Figure 11) ultrasound. It is the in size. They develop secondary to the ½F11860
805 the serosa, the myometrial echogenicity most common ultrasound sign distortion of the anatomy of 1 coty- 861
806 becomes indistinguishable from that of described in PAS with around 80% of the ledons including an interlobular 862
807½F9 the placental tissue (Figure 9). The so- authors reporting them antenatally, septa3 due to the arrival of high- 863
808 nographer must take care with this sign independently of the depth of invasion.18 velocity (peak systolic velocity often 864
809 as, like the clear zone, myometrial Other terms have been used to describe >10 cm/s) maternal blood from a 865
810 thickness will be influenced by direct these spaces including “placental radial or arcuate artery (Figure 13).72 ½F13866
811 pressure of ultrasound probes and full- lakes”6,55,67 and “Swiss cheese.”67,68 Placental lakes may also arise second- 867
812 ness of the maternal bladder. Placental lakes are seen as echolucent ary to the presence of a larger than 868
813 areas often in the center of a lobule or average feeder vessel supplying an 869
814 Placental lacunae cotyledon (Figure 12), under the chori- increased blood flow volume to the ½F12870
815 Placental lacunae are numerous, large, onic plate or in the marginal zone. These lobule (Figure 13), thus focally distort- 871
816 irregular sonolucent intraplacental lakes are a common finding in normal ing its anatomy, but the impact on 872
817 spaces often described on ultra- pregnancies from the end of the first the cotyledon is less pronounced as 873
818 sound5,54,60,61 giving the placenta a trimester but changes in their peripheral the vessel involved is a spiral artery 874
819 “moth-eaten” appearance in PAS in both echogenicity (resulting in the term (Figure 3). However, in normal placen- 875
820 tation, it is unlikely that there will be 876
821 many such vessels resulting in fewer 877
822 lakes and the underlying myometrium 878
FIGURE 11
823 is of normal thickness. Both lacunae 879
- - -
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824 and lakes become more prominent 880

825 from the end of the first trimester when 881
826 the intervillous circulation is estab- 882
827 lished48,49 and will change in size and 883
828 shape as pregnancy advances. 884
829 By contrast, the “Swiss cheese” 885
830 transformation of the placenta de- 886
831 scribes the cystic hydropic changes of 887
832 the villi found in a partial hydatidiform 888
833 mole.73 These lesions are smaller and 889
834 distributed at random within the 890
835 Transvaginal ultrasound views of placenta previa increta at 20 weeks. A, “Moth-eaten” appearance placental structure. They never contain 891
836 of placenta with numerous lacunae of different size and shape secondary (arrow); and B, high- a fetal circulation and thus the “Swiss 892
837 velocity, turbulent blood flow within lacunae on color Doppler imaging. cheese” terminology should not be 893
838 Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017. used to describe the vascular lacunae 894
found in PAS.

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895 951
896 Bladder wall interruption 952
FIGURE 12
897 This is often described on gray-scale ul- 953
- - -

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898 trasound as an interruption, loss, or ir- 954
899 regularity of the bladder wall or of the 955
900 hyperechoic line between uterine serosa 956
901 and bladder lumen.54,74 This sign may 957
902 arise as a direct result of villous invasion 958
903 into the muscle of the posterior wall of 959
904 the bladder, thereby changing its echo- 960
905 genicity, but is most likely an ultrasound 961
906 artefact arising from the massive neo- 962
907 vascularity found within the peritoneal 963
908 fold between the anterior wall of 964
Transabdominal ultrasound longitudinal views of placenta (P) at 33 weeks’ gestation in pregnancies
909 the uterus and the posterior wall of the 965
with no surgical history and no P accreta at birth. A, Centrocotyledon lake (arrow) with minimal (left)
½F14
910 bladder (Figure 14). Insonation of the 966
and increased (right) probe pressure. B, Multiple irregular lakes mimicking “moth-eaten” appear-
911 walls of the numerous tangled vessels 967
ance such as that seen in invasive placentation.
912 disrupts the flat surface required to 968
Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017.
913 provide the bright straight line usually 969
914 seen resulting in the apparent 970
915 interruptions. 971
916 Care must be taken by the sonogra- exophytic mass are collectively re- persistence of significant blood flow 972
917 pher to ensure that the break seen in the ported in 33% of the cases of invasive after delivery in PAS81 as well as dif- 973
918 bright line representing the posterior placentation.18 ferences seen in vessel distribution, size, 974
919 bladder wall is a genuine area of echo- and spatial organization in the placental 975
920 lucency and not artefact as a result of Subplacental and/or uterovesical bed area. Invasion into these shunts is 976
921 ultrasound dropout from the angle of hypervascularity the proposed cause of the large areas of 977
922 insonation. This results from excessive dilatation of abnormal vascular confluence seen with 978
923 the uteroplacental circulation beyond 3-dimensional power Doppler imaging 979
924 Placental bulge the spiral arteries, ie, including the radial in cases of PP.76 In addition, the 980
925 Placental bulge describes the ballooning and arcuate arteries, and is a prominent vasculature characteristics of the 981
926 of the uterus containing the placenta feature of PAS on prenatal ultra- placental bed may vary in PAS 982
927 away from its expected plane into the sound.18,55,56,74,76-79 This is often depending on the position of the 983
928 surrounding tissue, usually the bladder. accompanied by extensive neo- placenta inside the uterine cavity, 984
929 This sign is seen on ultrasound vascularization within the peritoneum, whether near to or far from the main 985
930 (Figure 14) and MRI. It most likely especially between the anterior wall of uterine arteries, and on the remodeling 986
931 represents villous invasion deep into the uterus and the posterior wall of the of the myometrial circulation around 987
932 and/or through the myometrium bladder. the scar area. Thus, like the placental 988
933 resulting in loss of structural integrity of CDI (Figures 10 and 11) has enabled bed, myometrial thickness, and lacunae, 989
934 the surrounding uterine muscle. The visualization of the uteroplacental cir- the vascular features under and around 990
935 placenta will then bulge outward into culation in greater detail; up to 81% of the accreta area will change with 991
936 surrounding structures. This phenome- cases of PI and 75% of cases of PP advancing gestation. 992
937 non is seen at laparotomy and has been present with hypervascularization pat- 993
938 described as the snowman sign.75 terns within or under the placental bed Placental lacunae feeder vessels 994
939 (the subplacental zone).18 In addition, These are seen as vessels with high- 995
940 Exophytic mass vessel distributions are more heteroge- velocity blood flow arising from the 996
941 Exophytic mass describes the invasion neous in PI with the size and spatial deep arterial vasculature of the myome- 997
942 of the villous tissue through the myo- organization of the PI vascular archi- trium, ie, radial or arcuate arteries, and 998
943 metrium and the serosa into adjacent tecture at the uteroplacental interface feeding the lacunae (Figure 13). An ul- 999
944 extrauterine organs, usually the differing from normal placentation.79 A trasound study found that the total area 1000
945 bladder. This focal exophytic mass of combination of sonography, vascular occupied by vessels in normal and PI 1001
946 placental tissue, extending beyond the casting, and oxygen measurements has placental beds is similar, but that vessels 1002
947 uterine serosa, should only occur in shown that an extensive network of are significantly sparser and larger in 1003
948 cases of PP. In case reports and cohort arteriovenous shunts normally exist invasive placentation.79 This could 1004
949 studies that provide detailed data on within the myometrium in the placental explain the abnormal hemodynamics 1005
950 the depth of invasion, bladder wall bed.80 Villous invasion into these deep underlying the development of the 1006
interruption, bladder bulge, and shunts may partly explain the lacunae in invasive placentation.

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1007 1063
1008 abnormal placental attachment, degree 1064
FIGURE 13
1009 of invasion, and/or spatial relationship of 1065
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- - -
1010 the accreta villous tissue with the previ- 1066
1011 ous CD scar, cervix, main uterine cir- 1067
1012 culation, etc. In a recent systematic 1068
1013 review, we found that detailed correla- 1069
1014 tions between ultrasound findings and 1070
1015 accreta grading of a delivery were only 1071
1016 reported in 34 of 1078 cases,18 although 1072
1017 >90% of the cases had a cesarean hys- 1073
1018 terectomy or a secondary hysterectomy 1074
1019 after a failed attempt at conservative 1075
1020 management. This limits the correlation 1076
1021 between prenatal ultrasound features 1077
1022 and clinical evidence at the time of de- 1078
1023 livery. This will also lead inevitably to 1079
1024 false-positive diagnosis of PAS in many 1080
1025 cases, in particular when the surgeon is 1081
1026 able to remove the placenta manually 1082
1027 and the bleeding is secondary to uterine Q4 1083
1028 atonia and not to damage of the myo- 1084
1029 metrial circulation, or when the placenta 1085
1030 is previa and there is a scar dehiscence 1086
1031 with placental tissue visible through the 1087
1032 uterine serosa. 1088
1033 The first histopathological series of PA 1089
1034 by Irving and Hertig1 included only cases 1090
1035 of abnormal adherence. All of their 18 1091
1036 cases presented clinically as failure of the 1092
1037 placenta to separate and 14 required a 1093
1038 secondary hysterectomy to control the 1094
1039 bleeding. In 7 cases, the obstetrician 1095
1040 could remove the placenta manually and 1096
1041 in 3 cases the retained villous tissue was 1097
1042 removed by curettage. None of their 1098
Transabdominal ultrasound longitudinal views of placenta (P). A, P previa accreta at 20 weeks with cases of hysterectomy with placenta in
1043 feeding artery from arcuate circulation between P and bladder (B) entering lacuna. B, Cen- 1099
1044 situ presented with macroscopic evi- 1100
trocotyledon lake at 28 weeks’ gestation in uncomplicated pregnancy. Note presence of uterine dence of an excessive dilatation of the
1045 myometrium (M). C, Velocity flow entering lake from corresponding feeder spiral artery. 1101
1046 radial and arcuate circulation, and in all 1102
Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017. cases the diagnosis was made exclusively
1047 1103
1048 on the histological finding of “complete 1104
1049 or partial absence of the decidua with 1105
1050 Bridging vessels Collectively, these CDI features have villi directly embedded in the myome- 1106
1051 Bridging vessels are seen as CD signals been reported in 66% of the cases of trium.” Only 1 of their patients (case 12) 1107
1052 arising in the myometrium and appearing abnormally invasive placenta diagnosed had a prior CD, and the only different 1108
1053 to travel beyond the uterine serosa and prenatally,18 and are due to the dilatation pathological finding in that case was that 1109
1054 into the bladder before disappearing of large and deeper myometrial vessels the scar area where the placenta was 1110
1055 (Figure 14). This bridging is an ultrasound below the JZ of normal implantation. attached was thinner than the rest of the 1111
1056 artefact as these vessels do not traverse uterine wall. All their remaining patients 1112
1057 between the myometrium and bladder but Pathological correlations had a history of manual removal, curet- 1113
1058 are actually the contorted vessels of the Many imaging cohort studies on PAS do tage, and/or endometritis, suggesting 1114
1059 neovascularity within the peritoneum not include a histopathological confir- that minor traumas and/or chronic 1115
1060 caught in cross-section in a 2-dimensional mation, or when they do it is limited to a inflammation can lead an abnormally 1116
1061 image (Figure 14). They have been referred brief description of the number of cases adherent placenta in the next pregnancy. 1117
1062 to as “bladder varicosities” in cases of that were examined without a precise On 1 occasion, they found on micro- 1118
placenta previa accreta.77,78 description of the extension of the scopic examination “an increased

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1119 1175
1120 FIGURE 14 1176
1121 1177
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- - -
1122 1178
1123 1179
1124 1180
1125 1181
1126 1182
1127 1183
1128 1184
1129 1185
1130 1186
1131 1187
1132 1188
1133 Placenta (P) previa accreta. Transabdominal ultrasound longitudinal views at 28 weeks. A, Bladder (B) bulge demonstrating B wall interruption (arrow) 1189
1134 and B, bridging vessels on color Doppler imaging. C, Surgery at 34 weeks showing extensive neovascularity and myometrial distension over increta area. 1190
1135 Jauniaux. Pathophysiology and ultrasound imaging of placenta accreta spectrum. Am J Obstet Gynecol 2017.
1191
1136 1192
1137 1193
1138 1194
1139 number of dilated veins in the superficial between adherent and invasive placentation. Both are the consequence of 1195
1140 layers of the myometrium.” Similarly, of placentation. a deciduomyometrial disorder, and the 1196
1141 the 86 cases of PAS included in their Attempts at manual removal of the trophoblastic changes of accreta placen- 1197
1142 literature review up to 1935, there were placenta can distort the spatial rela- tation are probably secondary to their 1198
1143 19 cases of previous manual removal of tionship between the accreta villous migration beyond the JZ and their 1199
1144 the placenta, 10 cases of previous curet- tissue and the uterine wall.2 This may exposure to a different biological envi- 1200
1145 tage, 3 cases of endometritis, and only 1 limit in some cases the accuracy of the ronment. This loss of control by the 1201
1146 case of prior CD.1 microscopic diagnosis, in particular, if decidua of trophoblast invasion and spi- 1202
1147 Until the 1970s, the diagnosis of PAS the histological examination of the ral artery remodeling gives the EVT 1203
1148 was almost exclusively histologi- uteroplacental interface is incomplete.2-5 greater access to the deep myometrium 1204
1149 cal2,3,82,83 and only very rare cases of PI Macroscopic changes in the radial/ and its circulation. The depth of pene- 1205
1150 and PP were reported in the literature arcuate circulation may not always be tration of the villous tissue is likely to be 1206
1151 before that period, and without evi- obvious to the pathologist as the related to the extent of the deciduomyo- 1207
1152 dence of obvious macroscopic uterine vasculature will collapse during the metrial damage. Microscopic damage 1208
1153 vascular changes.84-86 Luke et al2 were hysterectomy procedure. The decidual secondary to manual removal, uterine 1209
1154 the first to highlight the need to layer becomes thinner and discontin- curettage, and endometritis are more 1210
1155 differentiate between abnormally uous with advancing gestation likely to lead to superficial adherent 1211
1156 adherent and abnormally invasive pla- (Figure 5), and this can also make the placentation. By contrast, a surgical scar 1212
1157 centas, and suggested using the microscopic diagnosis of adherent defect is associated with both the absence 1213
1158 “adherent or invasive placenta” to placenta difficult in particular if the of endometrial reepithelialization of the 1214
1159 describe the overall group of PAS. accreta area of the myometrium is not scar area and vascular remodeling around 1215
1160 Modern pathological studies have also extensively sampled.2 Dannheim et al87 the scar area and favors the development 1216
1161 shown that the lateral extension of a recently proposed methods of gross of invasive placentation. 1217
1162 PAS can vary and be focal, partial, or dissection, microscopic examination, In the adherent placenta, the chori- 1218
1163 total according to the number of accreta and reporting of hysterectomy speci- onic villi are in direct contact with the 1219
1164 lobules involved.2-5 They have also mens containing PAS. Their protocol myometrium with no obvious plane of 1220
1165 shown that the degree of villous adhe- facilitates retrospective correlation with cleavage. The clinical differential diag- 1221
1166 sion or invasion is rarely uniform surgical and imaging findings as well as nosis between an abnormally adherent 1222
1167 across the placental bed and that many standardized tissue sampling for po- placenta and a retained placenta can be 1223
1168 cases of PAS have creta and increta tential research. It is essential that difficult if the placenta is only partially 1224
1169 areas (Figure 2). The fact that accreta similar protocols are used to improve adherent. In invasive placentation, the 1225
1170 placentation can be heterogeneous may not only the diagnosis but also the placental villi penetrate deeply within 1226
1171 explain why no ultrasound sign, or management of PAS. the uterine wall, including in the myo- 1227
1172 combination of ultrasound signs, has so metrial circulation, and cannot be 1228
1173 far been found to be specific of the Conclusions removed manually or by curettage. With 1229
1174 depth of accreta placentation and ac- PAS is a histopathologic term that defines the exponential increase of CD around 1230
curate for the differential diagnosis abnormally adherent and invasive the world and with increasing maternal

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1231 1287
age and the need for artificial reproduc- 12. Shamshirsaz AA, Fox KA, Salmanian B, section. Oxford: Oxford University Press; 2016:
1232 et al. Maternal morbidity in patients with morbidly 129-44. 1288
1233 tive techniques and minor uterine sur- 1289
adherent placenta treated with and without a 27. van der Voet LF, Bij de Vaate AM,
1234 gical procedures, the number of PAS standardized multidisciplinary approach. Am J Veersema S, Brölmann HA, Huirne JA. Long- 1290
1235 cases, and in particular invasive placen- Obstet Gynecol 2015;212:218.e1-9. term complications of cesarean section. The 1291
1236 tation, will continue to increase. 13. Sadovsky E, Palti Z, Polishuk WZ, niche in the scar: a prospective cohort study on
1292
1237 Ultrasound signs of adherent and Robinson E. Atypical placentography in placenta niche prevalence and its relation to abnormal
1293
invasive placentation vary with gestational accreta. Obstet Gynecol 1967;29:784-7. uterine bleeding. BJOG 2014;121:236-44.
1238 14. Tabsh KM, Brinkman CR III, King W. Ultra- 28. Ben-Nagi J, Walker A, Jurkovic D, Yazbek J, 1294
1239 age, and depend on the thickness and sound diagnosis of placenta increta. J Clin Ul- Aplin JD. Effect of cesarean delivery on the 1295
1240 composition of the placental bed, prior trasound 1982;10:288-90. endometrium. Int J Gynaecol Obstet 2009;106: 1296
1241 scar defects, depth of invasion, and lateral 15. D’Antonio F, Iacovella C, Bhide A. Prenatal 30-4.
1297
extension of villous tissue. Abnormal identification of invasive placentation using ul- 29. Flo K, Widnes C, Vårtun Å, Acharya G.
1242 trasound: systematic review and meta-analysis. Blood flow to the scarred gravid uterus at 22-24 1298
1243 adherence and invasion may coexist in the 1299
Ultrasound Obstet Gynecol 2013;42:509-17. weeks of gestation. BJOG 2014;121:210-5.
1244 same placental bed, and thus accurate 16. Meng X, Xie L, Song W. Comparing the 30. Downes KL, Hinkle SN, Sjaarda LA, 1300
1245 correlation of pathological and clinical diagnostic value of ultrasound and magnetic Albert PS, Grantz KL. Prior prelabor or intra- 1301
1246 findings with imaging is essential. It is resonance imaging for placenta accreta: a sys- partum cesarean delivery and risk of placenta
1302
1247 therefore necessary that these protocols tematic review and meta-analysis. Ultrasound previa. Am J Obstet Gynecol 2015;212:669.
1303
are standardized and used by both clini- Med Biol 2013;39:1958-65. e1-6.
1248 17. D’Antonio F, Iacovella C, Palacios- 31. Jauniaux E, Bhide A. Prenatal ultrasound 1304
1249 cians and pathologists to improve the Jaraquemada J, Bruno CH, Manzoli L, Bhide A. diagnosis and outcome of placenta previa 1305
1250 diagnostic accuracy of ultrasound imag- Prenatal identification of invasive placentation accreta after cesarean delivery: a systematic 1306
1251 ing and to define ultrasound signs that using magnetic resonance imaging: systematic review and meta-analysis. Am J Obstet Gynecol
1307
may be useful in the screening of women review and meta-analysis. Ultrasound Obstet 2017. Q5
1252 Gynecol 2014;44:8-16. 32. Timor-Tritsch IE, Monteagudo A, Cali G, 1308
at high risk of PAS. -
1253 18. Jauniaux E, Collins SL, Jurkovic D, et al. Cesarean scar pregnancy and early 1309
1254 Burton GJ. Accreta placentation. A systematic placenta accreta share common histology. Ul- 1310
1255 review of prenatal ultrasound imaging and trasound Obstet Gynecol 2014;43:383-95. 1311
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