The Journal of Maternal-Fetal & Neonatal Medicine

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Placenta accreta spectrum into the parametrium,

morbidity differences between upper and lower
location

José M. Palacios-Jaraquemada, Álbaro Nieto-Calvache, Rozi Aditya

Aryananda & Nicolás Basanta

To cite this article: José M. Palacios-Jaraquemada, Álbaro Nieto-Calvache, Rozi Aditya

Aryananda & Nicolás Basanta (2023) Placenta accreta spectrum into the parametrium,
morbidity differences between upper and lower location, The Journal of Maternal-Fetal &
Neonatal Medicine, 36:1, 2183764, DOI: 10.1080/14767058.2023.2183764

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THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE
2023, VOL. 36, NO. 1, 2183764
https://doi.org/10.1080/14767058.2023.2183764

ORIGINAL ARTICLE

Placenta accreta spectrum into the parametrium, morbidity differences

between upper and lower location
Jos
e M. Palacios-Jaraquemadaa,b,c 
, Albaro Nieto-Calvached, Rozi Aditya Aryanandac,e and
Nicolas Basantab,f
a
CEMIC University Hospital and Universitas Airlangga, Surabaya, Indonesia; bSchool of Medicine, 1st Anatomy Chair, University of
Buenos Aires, Buenos Aires, Argentina; cDepartment of Obstetrics and Gynecology, Universitas Airlangga, Surabaya, Indonesia;
d
Placenta Accreta Spectrum Clinic, Fundacion Valle del Lili, Cali, Colombia; eDr. Soetomo Academic General Hospital, Surabaya,
Indonesia; fSchool of Medicine, Fernandez Hospital and 1st Anatomy Chair, University of Buenos Aires, Buenos Aires, Argentina

ABSTRACT ARTICLE HISTORY

Objective: To demonstrate the surgical and morbidity differences between upper and lower Received 12 March 2022
parametrial placenta invasion (PPI). Revised 2 November 2022
Materials and methods: Forty patients with placenta accreta spectrum (PAS) into the parame- Accepted 16 February 2023
trium underwent surgery between 2015 and 2020. Based on the peritoneal reflection, the study
KEYWORDS
compared two types of parametrial placental invasion (PPI), upper or lower. Surgical approach Placenta accreta spectrum;
to PAS follows a conservative-resective method. Before delivery, surgical staging by pelvic fascia parametrial invasion;
dissection established a final diagnosis of placental invasion. In upper PPI cases, the team intraoperative diagnosis;
attempted to repair the uterus after resecting all invaded tissues or performing a hysterectomy. maternal morbidity; massive
In cases of lower PPI, experts performed a hysterectomy in all cases. The team only used prox- blood loss
imal vascular (aortic occlusion) control in cases of lower PPI. Surgical dissection for lower PPI
started finding the ureter in the pararectal space, ligating all the tissues (placenta and newly
formed vessels) to create a tunnel to release the ureter from the placenta and placenta supple-
tory vessels. Overall, at least three pieces of the invaded area were sent for histological analysis.
Results: Forty patients with PPI were included, 13 in the upper parametrium and 27 in the lower par-
ametrium. MRI indicated PPI in 33/40 patients; in three, the diagnosis was presumed by ultrasound or
medical background. The intrasurgical staging categorizes 13 cases of PPI performed and finds diag-
nosis in seven undetected cases. The expertise team completed a total hysterectomy in 2/13 upper
PPI cases and all lower PPI cases (27/27). Hysterectomies in the upper PPI group were performed by
extensive damage of the lateral uterine wall or with a tube compromise. Ureteral injury ensued in six
cases, corresponding to cases without catheterization or incomplete ureteral identification. All aortic
vascular proximal control (aortic balloon, internal aortic compression, or aortic loop) was efficient for
controlling bleeding; in contrast, ligature of the internal iliac artery resulted in a useless procedure,
resulting in uncontrollable bleeding and maternal death (2/27). All patients had antecedents of pla-
cental removal, abortion, curettage after a cesarean section, or repeated D&C.
Conclusions: Lower PAS parametrial involvement is uncommon but associated with elevated
maternal morbidity. Upper and lower PPI has different surgical risks and technical approaches;
consequently, an accurate diagnosis is needed. The clinical background of manual placental
removal, abortion, and curettage after a cesarean or repeated D&C could be ideally studied to
diagnose a possible PPI. For patients with high-risk antecedents or unsure ultrasound, a T2
weight MRI is always recommended. Performing comprehensive surgical staging in PAS allows
the efficient diagnosis of PPI before using some procedures.

Introduction implies a relatively low frequency of complications,

Placenta accreta spectrum (PAS) is a heterogeneous but highly complex cases may require many hospital
disease with severe maternal morbidity and fewer resources and lead to severe maternal morbidity [1]
severe forms. Therefore, treatment by expert groups and even death [2]. In addition, the location of

CONTACT Jose M. Palacios-Jaraquemada jpalaciosjaraquemada@gmail.com; jpalacios@fmed.uba.ar Galvan 4102, C1431 City of Buenos Aires,
Argentina
Supplemental data for this article is available online at https://doi.org/10.1080/14767058.2023.2183764
ß 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits
unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the
posting of the Accepted Manuscript in a repository by the author(s) or with their consent.
2 J. M. PALACIOS-JARAQUEMADA ET AL.
placental invasion is related to a particular surgical dif-
ficulty and morbidity [1], especially when the lower
part of the bladder, cervix, or parametrium are
involved [3].
Information about PAS with parametrial involve-
ment is negligible [4]. In addition, few existing articles
describe the clinical results of these women, almost
always mentioning the use of a high number of trans-
fusions [5–7], aortic occlusion [5, 7], multiple admis-
sions to the operating theater [8], elevated illness, and
long-term severe sequelae [8].
PAS with parametrial placental invasion (PPI)
cases implies the involvement of many arterial
pedicles through multiple sources, and the obstetri-
cian does not often handle them. Moreover, the par-
ametrial space, mainly located under the peritoneal
reflection, is the pelvis’s narrow and deep area near
the ureter and multiple vascular structures [7]. Thus,
it is necessary to establish management guidelines
for PAS specialists and general obstetricians. PPI
may be divided into upper or lower cases based on
their position with the peritoneal reflection. While
upper PPI may only require an average procedure,
an inadequate approach to lower PPI could lead to
fast, uncontrollable bleeding, severe morbidity, and
even mortality [9].
Although PAS is not an actual placental invasion,
just a placental protrusion, we continue using the
term “invasion” because average readers frequently
use it.
We describe the clinical results of PAS cases with
parametrial placenta invasion (PPI) in three low- and
middle-income countries and propose a sequential
approach for management accordingly.
Materials and methods
Forty patients with PAS into the parametrium under-
went surgery between January 2015 and December
2020. The specialist team received the patients in pri-
vate, university, and public hospitals in Buenos Aires,
Argentina, in the Valle de Lili Foundation, Cali,
Colombia, and in the Dr. Soetomo General Hospital,
Indonesia. Furthermore, the senior specialist per-
formed a prenatal study image in all the patients,
including abdominal, transvaginal ultrasound, and T2
weight, ultrafast magnetic resonance imaging (MRI). In
addition, the study split patients into two types of PPI
groups regarding whether the placental invasion was
above (upper) or below (lower) the peritoneal reflec-
tion line. The surgical approach to PAS was performed
following a general description mentioned by a
conservative-resective method [10]. Before delivery,
the surgeon performed a pelvic coalesced fascia dis-
section to achieve a definitive diagnosis of placental
invasion. Experts performed surgical staging after cut-
ting inside the round ligament, completed a dissection
of the broad ligament folds, and separated the entire
vesicouterine fold (Figure 1). Direct observation of the
parametrial space between the two sheets of the
broad ligament was classified as follows: class 0, no
PPI; class A, PPI-like lateral uterine dehiscence, without
strong tissue adherence of neovascularization; and
class B, PPI with evidence of newly formed vessels in
the placenta or with firm tissue adherence to the pel-
vic wall.
In upper PPI cases, the surgical team attempts to
repair the uterus after resection of invaded tissues or
performing a hysterectomy; overall, hemostasis was
completed by uterine artery clamping taking part of
the myometrium. Which procedure (conservative
repair or resective-ablative) was performed depending
on the women’s desire for future pregnancy. In cases
of lower PPI, experts performed a hysterectomy in all
instances. First, the urologist inserted a simple ureteral
catheter. In cases of lower PPI, a recurrent stopping to
ureteral catheter advance indicated that the procedure
should be stopped due to the risk of PPI rupture and
massive, unexpected bleeding [11]. Next, the urologist
repaired any detected cases of ureteral injuries by
resection borders, use of a double J catheter, four
stitches for ureteral approximation, and drainage;
immediate repair could bring satisfactory surgical
results and fewer complications [12]. In cases of hid-
den ureteral damage, its integrity was reestablished by
ureteral reimplantation within 7–10 days. Specialists
only used upper proximal vascular control in all
patients with lower PPI. In four instances, the vascular
surgeons used an elastomeric infrarenal aortic balloon
(REBOATM, Prytime Medical, Boerne, TX). In three
placed abdominal aortic loops [13], an obstetrician
performed internal aortic compression, and in two, a
bilateral internal iliac artery was ligated.
Surgical dissection for lower PPI cases started find-
ing the ureter in the pararectal space (Video 1). Then,
a surgical retractor separated the round ligament lat-
erally to expose a PPI area covering the ureter
(Supplementary Material 1, F1). Later, the surgeon
ligated the placenta and newly formed vessels above
the ureter using Vicryl number 0 (Supplementary
Material 1, F2), creating a tunnel to release the ureter
from the placenta and connecting vessels. Due to the
pelvic ureteral blood supply coming to the lateral side,
ligatures must be applied internally to the ureter

Figure 1. A scheme showing the basic steps for intrasurgical PAS staging. Left: After cutting the peritoneum medially to the
round ligament (RL), fingers open the parametrial space between avascular fascia sheets. Right: From the upper position (A), the
index goes down (B) by the subperitoneal tissue until crossing the fingers behind the bladder (BL) to perform a Pelosi maneuver.
IA: invaded area.
(Supplementary Material 1, F3). Then, the PPI is wholly
separated to perform hysterectomy [14], reducing the
risk of unexpected bleeding.
In all cases, at least three pieces of the invaded area
were sent for histological analysis. Continuous statistical
variables were expressed as medians and interquartile
ranges and analyzed with the Mann–Whitney U-test.
Categorical variables included proportions and compari-
sons using the Chi-square or Fisher’s exact test
(Statistical Package Stata, version 14.0, StataCorp.,
College Station, TX). Approval was obtained from the
Ethics Committee under protocol number 550-2015.
Discussion
Main findings
Lower parametrial PAS involvement is an infrequent but
potentially life-threatening situation [15]. At surgery,
the surgical team confirmed 40 cases of PPI, 13 in the
upper parametrium and 27 in the lower parametrium.
MRI indicated PPI in 21/32 patients; in seven, the identi-
fication was performed by surgical staging, and in three,
the diagnosis was presumed by ultrasound [16]. False-
positive ultrasound interpretations resulted in cases in
which accreta were suspected to be a clinical concern
but turned out to not be present [17]. Conversely, false-
negative readings may lead to a circumstance with
unanticipated complications or tragic consequences
[18]; for this reason, high-risk patients must be operated
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 3
on as PAS-positive to decrease maternal morbidity [19].
The coexistence of MRI signs in the lateral uterine wall
was associated with an elevated risk of bleeding [20]
and complications [21]; an MRI study would facilitate
preoperative planning and evaluation of maternal out-
comes in most cases with maternal risk factors.
Therefore, MRI should be used for at-risk patients to
accurately identify the placental location, regardless of
the ultrasonography results. The intrasurgical staging
categorizes the position and features of the invaded
placenta and newly formed between the lateral uterus
and the iliac internal vascular fascia (Figure 2).
All PPIs had a medical background, for instance,
manual removal of the placenta [22], iterative D&C
[23], and curettage after cesarean section or abortion
[24]. Lower PPI showed more complications, blood
loss, a requirement of proximal vascular control, lon-
ger operative time, and urinary injuries than upper PPI
(Table 1). The possibility of unexpected massive bleed-
ing increases in lower PPI; heavy bleeding is associ-
ated with the presence of newly formed vessels but
not connected with the size of the lower PPI
(Supplementary Material F4). Surgical diagnosis of
lower PPI with the mentioned features means the rise
of unwanted blood loss [7] and the alert to stop any
dissection until aortic vascular control is performed.
The efficiency of aortic vascular management was dir-
ectly associated with its application, obtaining the
best results when used before and not during or after
4 J. M. PALACIOS-JARAQUEMADA ET AL.

Figure 2. Parasagittal cut on the right female pelvis. An embalmed corpse, the peritoneal sheet of the parametrium was transillu-
minated. Notice that the parametrium in a straight space has plenty of arteries, veins, and the ureter.

Table 1. Clinical results of patients with upper and lower type 2 PAS placenta invasion.
Upper type 2 PASa (n ¼ 13) Lower type 2 PASb (n ¼ 27) p value
c
Bleeding 1500 (1400–2000) 2000 (1500–2500) .0120
Operative time (min)c 100 (60–130) 120 (60–230) .3452
Bladder lesion, n (%) 1 (7.7) 7 (25.9) .0347
Ureteral lesion, n (%) 0 6 (22.2) .0232
Vascular occlusion requirement, n (%) 3 (23.1) 11 (40.7) .0010
Pelvic tamponade, n (%) 0 6 (22.2) .0232
Transfusion, N (%) 10 (76.9) 27 (100) .0419
RBCs transfusedc 2 (0.5–2.5) 4 (2–4) .0393
Accreta, n (%) 3 (23.1) 5 (18.5) .1943
Increta, n (%) 3 (23.1) 3 (11.1)
Percreta, n (%) 7 (53.8) 19 (70.4)
Maternal death, n (%) 0 2 (7.4)
Manual removal of the placenta 7 1
Repeated D&C 4 7
Curettage after cesarean 2 7
Abortion by curettage 0 12 NA
abc
Significance is p < .05.

the parametrial dissection. The use of iliac internal vas-
cular control resulted in uncontrollable massive bleed-
ing and fasted and not immediately recognized blood
loss volume [25,26], coagulopathy, and metabolic acid-
osis that lead to two cases of maternal death. In both
cases, the surgical team underestimated a small piece
of lower PPI and surprised by uncontrollable bleeding
despite bilateral internal iliac vascular control. During
active bleeding or persistent oozing, damage control
surgery [27] was attempted using pelvic packing.
However, it was completely useless because blood and
clots went unsuspectingly through pelvic subperitoneal
spaces and retroperitoneal areas (Supplementary
Material F5). In upper PPI, control bleeding was effi-
ciently controlled only using uterine vessel compression
(Supplementary Material F6). In all cases of upper PPI,
the uterine repair was technically possible, but the deci-
sion for a resective procedure was the final choice of
the obstetrician according to the mother’s preferences.
All cases of ureteral ligature occurred in patients
without ureteral catheterization due to complete identi-
fication; then, the ureter was reimplanted [28] within 7–
10 days without further complications.
Internal manual compression of the aorta effectively
controls pelvic bleeding in unexpected parametrial
bleeding and facilitates dissection maneuvers.
Histology analysis confirmed PAS, and over 120 sam-
ples (three samples from 40 cases) were collected in a
100% placenta percreta. PAS is not an authentic inva-
sion but just a placental protrusion, although

morbidity and blood loss are closely associated with
the invasion topography and not with a placental
degree invasion [10].
Strengths and limitations
The study’s main strength is that is we collected a
high number of cases of this uncommon PAS location.
The use of aortic vascular control and precise ureteral
dissection demonstrated safety and decreased blood
loss [29] in patients with a lower PPI. Compared to
existing papers, this study represents the most exten-
sive series about PPI and could be an outstanding
guide for experts and beginners. A surgical guide in
severe cases of PAS proposes an alternative to leaving
the placenta in situ; although, this option is connected
with severe maternal morbidity, especially in placenta
percreta [30]. The main limitation of our study is a
poor comparison with other publications because they
are only a few case reports. Furthermore, lower PPI is
connected with hazardous surgery, massive and
uncontrollable bleeding, severe maternal morbidity,
and even death; probably by this cause, hospitals or
doctors are not prone to publish their results.
Moreover, the low frequency of PPI made it impos-
sible to collect information from centers with limited
PAS cases by year. Although Argentina legalized abor-
tion some years ago, Argentina, Colombia, and
Indonesia are countries with a high rate of unlawful
abortions, procedures closely connected to uterine
damage. Maternal mortality in percreta is approxi-
mately 7% [31], but this is a general value; this rate is
likely significantly higher in lower PPI. Although the
publication appears to be substantial, the relative val-
ues for PAS complications are not enough to estimate
a real statistical significance [32].
Interpretation
The presence of newly formed vessels or a direct pla-
cental attachment (without serosa) in the lower PPI
indicated the possibility of uncontrollable massive
bleeding [33] independent of extrauterine placenta
size. Lower PPI bleeding is associated with challenging
hemostasis, first by the diversity of their blood supply
source [34] and second by the particularly deep and
narrow placental invasion anatomy. Upper PPI seems
impressive, but it is not technically difficult to handle
when performing expertise groups. Due to the thick
and healthy myometrium in the upper uterus concern-
ing the lower PPI, the use of aortic vascular control is
only recommended in cases of lower PPI, especially in
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 5
the presence of newly formed vessels or firm placental
adherence to iliac internal elements. First, the newly
formed vessels have multiple connections with the
lower anastomotic circle [35]; second, the possibility of
undiagnosed extension to the ischiorectal through the
levator ani muscle (roof of the ischiorectal fossae) is
unknown until deep dissection.
The concomitant use of aortic vascular control and
ureteral-specific dissection is safe to minimize the sur-
gical risk in lower PPI. It is expected that the surgeons
handling a complicated case of PAS think to avoid
touching the placenta and leaving it in situ as a defini-
tive treatment or addressing it later with a delayed
hysterectomy. In the case of early and massive, unex-
pected bleeding, a surgical solution is problematic,
first, due to placental placement and second, due to
the risk of coagulopathy, hypovolemic shock, and
metabolic acidosis. In these cases, primary aortic vas-
cular control is a priority to have time to replace vol-
ume, restore a clot, and stabilize hemodynamic
parameters [36]. Although unpublished, massive
embolization by lower PPI is not recommended in the
case of a wide pelvic and extra pelvic anastomotic net
[37]. Although there are some prospective randomized
trials [38,39], retrospective cohort and physiology
research about the internal iliac ligature [40], and
studies that have demonstrated its inefficacy in cases
of pelvisubperitoneal bleeding, the use of internal iliac
artery occlusion is associated with severe complica-
tions [41–43] and even death [44,45].
Conversely, the aortic vascular control below renal
arteries blocks the iliac internal, external, some aortic,
and femoral anastomotic components bilaterally in a
simple way. Consequently, it is an invaluable tool to
achieve hemostasis in lower PPI. Comparable efficacy
of aortic blocking has been demonstrated using a spe-
cific aortic balloon, an aortic cross-clamp [46], or inex-
pensive aortic slinging [13].
Conclusions
Lower PAS parametrial involvement is uncommon but
is associated with elevated maternal morbidity. Upper
and lower PPI have different surgical risks and require
different technical approaches; consequently, accurate
identification is greatly needed.
Women with a clinical background of manual pla-
cental removal, abortion, or repeated D&C must be
carefully examined to diagnose a possible PPI. For
patients with high-risk antecedents or doubtful ultra-
sound, a T2 weight MRI is recommended. Performing
comprehensive surgical staging in PAS allows the
6 J. M. PALACIOS-JARAQUEMADA ET AL.
efficient diagnosis of PPI efficiently and before using
any dissection maneuvers that cause unexpected mas-
sive bleeding. Knowing what to do or not do is essen-
tial for avoiding unnecessary organ ablation and
uncontrollable massive bleeding.
Acknowledgements
The authors thank Fabian Cabrera, graphic design program
Professor, from Universidad del Valle, Cali, Colombia.
Author contributions
Palacios-Jaraquemada JM contributed to the conception,
planning and carrying out analysis, and writing up of this
work. Nieto-Calvache A, Aditya Aryananda R, and Basanta N
contributed to carrying out, analyzing, and correcting the
manuscript.
Disclosure statement
Palacios Jaraquemada JM is an Editorial Board of the Journal
of Maternal, Fetal, and Neonatal Medicine. Basanta N, Nieto-
Calvache A, and Aditya Aryananda R have no conflicts of
interest to declare. All procedures performed in studies
involving human participants were performed according to
the ethical standards of the institutional and national
research committees. Informed consent was obtained from
the patients included in the study. The authors declare that
there are no conflicts of interest.
Funding
No financial funds.
ORCID
Jose M. Palacios-Jaraquemada http://orcid.org/0000-0002-
5240-5320
Rozi Aditya Aryananda http://orcid.org/0000-0001-6674-
7682
References
[1] Kingdom JC, Hobson SR, Murji A, et al. Minimizing
surgical blood loss at cesarean hysterectomy for pla-
centa previa with evidence of placenta increta or pla-
centa percreta: the state of play in 2020. Am J Obstet
Gynecol. 2020;223(3):322–329.
[2] Nieto-Calvache AJ, Palacios-Jaraquemada JM, Osanan
G, et al. Lack of experience is a main cause of mater-
nal death in placenta accreta spectrum patients. Acta
Obstet Gynecol Scand. 2021;100(8):1445–1453.
[3] Palacios-Jaraquemada JM, D’Antonio F, Buca D, et al.
Systematic review on near-miss cases of placenta
accreta spectrum disorders: correlation with invasion
topography, prenatal imaging, and surgical outcome.
J Matern Fetal Neonatal Med. 2020;33(19):3377–3384.
[4] Palacios Jaraquemada JM, Bruno CH. Magnetic reson-
ance imaging in 300 cases of placenta accreta: surgi-
cal correlation of new findings. Acta Obstet Gynecol
Scand. 2005;84(8):716–724.
[5] Al-Omari W, Elbiss HM, Hammad FT. Placenta percreta
invading the urinary bladder and parametrium.
J Obstet Gynaecol. 2012;32(4):396–397.
[6] Borekci B, Ingec M, Kumtepe Y, et al. Difficulty of the
surgical management of a case with placenta percreta
invading towards parametrium. J Obstet Gynaecol
Res. 2008;34(3):402–404.
[7] Seoud M, Cheaib S, Birjawi G, et al. Successful treat-
ment of severe retroperitoneal bleeding with recom-
binant factor VIIa in women with placenta percreta
invading into the left broad ligament: unusual
repeated antepartum intra-abdominal bleeding.
J Obstet Gynaecol Res. 2010;36(1):183–186.
[8] Vahdat M, Mehdizadeh A, Sariri E, et al. Placenta per-
creta invading broad ligament and parametrium in a
woman with two previous cesarean sections: a case
report. Case Rep Obstet Gynecol. 2012;2012:251381.
[9] Zhu B, Yang K, Cai L. Discussion on the timing of bal-
loon occlusion of the abdominal aorta during a cae-
sarean section in patients with pernicious placenta
previa complicated with placenta accreta. Biomed Res
Int. 2017;2017:8604849.
[10] Palacios-Jaraquemada JM, Fiorillo A, Hamer J, et al.
Placenta accreta spectrum: a hysterectomy can be
prevented in almost 80% of cases using a resective-
reconstructive technique. J Matern Fetal Neonatal
Med. 2022;35(2):275–282.
[11] Dyer RB, Chen MY, Zagoria RJ, et al. Complications of
ureteral stent placement. Radiographics. 2002;22(5):
1005–1022.
[12] Rao D, Yu H, Zhu H, et al. The diagnosis and treat-
ment of iatrogenic ureteral and bladder injury caused
by traditional gynaecology and obstetrics operation.
Arch Gynecol Obstet. 2012;285(3):763–765.
[13] Long ML, Cheng CX, Xia AB, et al. Temporary loop
ligation of the abdominal aorta during cesarean hys-
terectomy for reducing blood loss in placenta accrete.
Taiwan J Obstet Gynecol. 2015;54(3):323–325.
[14] Takeda S, Takeda J, Murayama Y. Placenta previa
accreta spectrum: cesarean hysterectomy. Surg J.
2021;7(Suppl. 1):S28–S37.
[15] Chen X, Shan R, Song Q, et al. Placenta percreta eval-
uated by MRI: correlation with maternal morbidity.
Arch Gynecol Obstet. 2020;301(3):851–857.
[16] Calı G, Foti F, Minneci G. 3D power Doppler in the
evaluation of abnormally invasive placenta. J Perinat
Med. 2017;45(6):701–709.
[17] Bowman ZS, Eller AG, Kennedy AM, et al. Accuracy of
ultrasound for the prediction of placenta accreta. Am
J Obstet Gynecol. 2014;211(2):177.e1–177.e7.
[18] Nageotte MP. Always be vigilant for placenta accreta.
Am J Obstet Gynecol. 2014;211(2):87–88.
[19] Reeder CF, Sylvester-Armstrong KR, Silva LM, et al.
Outcomes of pregnancies at high-risk for placenta
accreta spectrum following negative diagnostic imag-
ing. J Perinat Med. 2022;50(5):595–600.
[20] Bourgioti C, Zafeiropoulou K, Fotopoulos S, et al. MRI
prognosticators for adverse maternal and neonatal

clinical outcome in patients at high risk for placenta
accreta spectrum (PAS) disorders. J Magn Reson
Imaging. 2019;50(2):602–618.
[21] Woodward PJ, Kennedy AM, Einerson BD. Is there a
role for MRI in the management of placenta accreta
spectrum? Curr Obstet Gynecol Rep. 2019;8(3):64–70.
[22] Sivasankar C. Perioperative management of undiag-
nosed placenta percreta: case report and manage-
ment strategies. Int J Womens Health. 2012;4:
451–454.
[23] Cooper AC. The rate of placenta accreta and previous
exposure to uterine surgery. Yale Medicine Thesis
Digital Library; 2012. p. 1702. Available from: http://
elischolar.library.yale.edu/ymtdl/1702
[24] Harris LH, Grossman D. Complications of unsafe and
self-managed abortion. N Engl J Med. 2020;382(11):
1029–1040.
[25] Bhananker SM, Ramaiah R. Trends in trauma transfu-
sion. Int J Crit Illn Inj Sci. 2011;1(1):51–56.
[26] Hancock A, Weeks AD, Lavender DT. Is accurate and
reliable blood loss estimation the ’crucial step’ in
early detection of postpartum haemorrhage: an inte-
grative review of the literature. BMC Pregnancy
Childbirth. 2015;15:230.
[27] Carvajal JA, Ramos I, Kusanovic JP, et al. Damage-con-
trol resuscitation in obstetrics. J Matern Fetal
Neonatal Med. 2022;35(4):785–798.
[28] Rizvi JH, Zuberi NF. Prevention and treatment of urin-
ary tract injuries during obstetrics and gynaecological
procedures. In: Ratnam SS, editor. Textbook of obstet-
rics and gynecology for post-graduates. Vol. 2.
London: Orient Longman; 2003. p. 366–374.
[29] Soleymani Majd H, Collins SL, Addley S, et al. The
modified radical peripartum cesarean hysterectomy
(Soleymani-Alazzam-Collins technique): a systematic,
safe procedure for the management of severe pla-
centa accreta spectrum. Am J Obstet Gynecol. 2021;
225(2):175.e1–175.e10.
[30] Marcellin L, Delorme P, Bonnet MP, et al. Placenta
percreta is associated with more frequent severe
maternal morbidity than placenta accreta. Am
J Obstet Gynecol. 2018;219(2):193.e1–193.e9.
[31] O’Brien JM, Barton JR, Donaldson ES. The manage-
ment of placenta percreta: conservative and operative
strategies. Am J Obstet Gynecol. 1996;175(6):1632–
1638.
[32] Leppink J, Winston K, O’Sullivan P. Statistical signifi-
cance does not imply a real effect. Perspect Med
Educ. 2016;5(2):122–124.
[33] Ishibashi H, Miyamoto M, Iwahashi H, et al. Criteria for
placenta accreta spectrum in the International
Federation of Gynaecology and Obstetrics Classification,
THE JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE 7
and topographic invasion area are associated with mas-
sive bleeding in patients with placenta previa. Acta
Obstet Gynecol Scand. 2021;100(6):1019–1025.
[34] Palacios-Jaraquemada JM, Garcıa-Mo naco R, Barbosa
NE, et al. Lower uterine blood supply: extrauterine
anastomotic system and its application in surgical
devascularization techniques. Acta Obstet Gynecol
Scand. 2007;86(2):228–234.
[35] Gonzalez J, Albeniz LF, Ciancio G. Vascular problems
of the pelvis. In: Lanzer P, editor. PanVascular medi-
cine. Berlin, Heidelberg: Springer; 2015. p. 3793–3820.
[36] Palacios-Jaraquemada J, Fiorillo A. Conservative
approach in heavy postpartum hemorrhage associ-
ated with coagulopathy. Acta Obstet Gynecol Scand.
2010;89(9):1222–1225.
[37] Bratila E, Bratila CP, Coroleuca CB, et al. Collateral cir-
culation in the female pelvis and the extrauterine
anastomosis system. Rom J Anat. 2015;14(2):223–227.
[38] Yu SCH, Cheng YKY, Tse WT, et al. Perioperative
prophylactic internal iliac artery balloon occlusion in
the prevention of postpartum hemorrhage in pla-
centa previa: a randomized controlled trial. Am J
Obstet Gynecol. 2020;223(1):117.e1–117.e13.
[39] Hussein AM, Dakhly DMR, Raslan AN, et al. The role of
prophylactic internal iliac artery ligation in abnormally
invasive placenta undergoing caesarean hysterec-
tomy: a randomized control trial. J Matern Fetal
Neonatal Med. 2019;32(20):3386–3392.
[40] Burchell RC. Internal iliac artery ligation: hemodynam-
ics. Obstet Gynecol. 1964;24:737–739.
[41] Gandhi MR, Kadikar GK. Laceration of the internal iliac
vein during internal iliac artery ligation. Natl J Med
Res. 2013;3(2):190–192.
[42] Gagnon J, Boucher L, Kaufman I, et al. Iliac artery rup-
ture related to balloon insertion for placenta accreta
causing maternal hemorrhage and neonatal com-
promise. Can J Anaesth. 2013;60(12):1212–1217.
[43] Dzsinich C. Ligation of the large vessels in the pelvis.
CME J Gynecol Oncol. 2004;9:38–40.
[44] Oderich GS, Panneton JM, Hofer J, et al. Iatrogenic
operative injuries of abdominal and pelvic veins: a
potentially lethal complication. J Vasc Surg. 2004;
39(5):931–936.
[45] Burchell RC, Mengert WF. Internal iliac artery ligation:
a series of 200 patients. J Int Fed Obstet Gynecol.
1969;7(2):85–92.
[46] Stubbs MK, Wellbeloved MA, Vally JC. The manage-
ment of patients with placenta percreta: a case series
comparing the use of resuscitative endovascular bal-
loon occlusion of the aorta with aortic cross clamp.
Indian J Anaesth. 2020;64(6):520–523.