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Ultrasound Obstet Gynecol 2006; 28: 178182

Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.2797

Sonographic findings of placental lacunae and the prediction


of adherent placenta in women with placenta previa totalis
and prior Cesarean section
J. I. YANG, Y. K. LIM, H. S. KIM, K. H. CHANG, J. P. LEE, and H. S. RYU
Department of Obstetrics and Gynecology, Ajou University School of Medicine, Suwon, Korea

K E Y W O R D S: adherent placenta; intraplacental lacuna; placenta previa totalis

ABSTRACT number of massive transfusions and intensive care unit


admissions and cases of disseminated intravascular coag-
Objective To investigate the value of transvaginal ulopathy and Cesarean hysterectomy were significantly
sonographic findings of intraplacental lacunae for greater in those with lacunae (P < 0.0001).
predicting adherent placenta and clinical outcome in
patients with placenta previa totalis and a history of Conclusion Transvaginal sonographic findings of intra-
Cesarean section. placental lacunae in patients with placenta previa totalis
and a history of Cesarean section are useful in the
Methods Fifty-one patients with placenta previa totalis
prediction of adherent placenta and may have a role
diagnosed by transvaginal sonography and with a history
in the prediction of clinical outcome. Copyright 2006
of Cesarean section who delivered at our hospital
ISUOG. Published by John Wiley & Sons, Ltd.
were included in the study. The sonographic findings
of intraplacental lacunae were classified into one of
four grades. Pathological analysis of the placenta was
performed for all patients who delivered, and in INTRODUCTION
cases of hysterectomy, examination of the uterus was
Adherent placenta, including placenta accreta and its
also performed. The placental findings and obstetric
variants placenta increta and percreta, occurs as a
complications, including massive transfusion, intensive
result of placental villi penetrating the myometrium
care unit admission and Cesarean hysterectomy, were
through a defect in the decidua basalis. It is a major
compared with the grade of lacuna.
cause of obstetric hemorrhage and is thus associated
Results Lacunae were classified as Grade 1+ in 10 cases, with increased maternal morbidity and mortality. Early
Grade 2+ in 11 cases, Grade 3+ in five cases and as diagnosis can improve the perinatal prognosis by enabling
Grade 0 (i.e. lacunae were absent) in the remaining 25 preparations for a possible obstetric emergency to be made
cases. When lacunae of Grade 1+ were considered, the and avoiding obstetric complications such as Cesarean
sensitivity, specificity, positive predictive value and nega- hysterectomy and massive transfusion1 . However, in most
tive predictive value of diagnosing adherent placenta were cases adherent placenta is diagnosed at the time of delivery
86.9%, 78.6%, 76.9% and 88.0%, respectively. When when total removal of the placenta from the uterus fails
lacunae of Grade 2+ were considered, the sensitivity, and hemorrhage occurs.
specificity, positive predictive value and negative predic- The sonographic characteristics of adherent placenta
tive value of diagnosing placenta increta or percreta were include loss of the normal hypoechoic retroplacental
100%, 97.2%, 93.8% and 100%, respectively. Hysterec- myometrial zone, thinning or disruption of the hyper-
tomy was performed in 18 cases, among whom two cases echogenic uterine serosabladder wall interface, and
showed Grade 1+ lacunae, 11 cases showed Grade 2+ presence of focal exophytic masses and intraplacental
lacunae, and five cases showed Grade 3+ lacunae. No lacunae2 . Of these, the presence of intraplacental lacu-
hysterectomy was performed in any case in which lacu- nae was the first criterion to be associated with placenta
nae were absent. Compared to those without lacunae, the accreta and it was reported that the larger and more

Correspondence to: Dr J. I. Yang, Department of Obstetrics & Gynecology, Ajou University School of Medicine, San-5, Wonchon-dong,
Yongtong-ku, Kyunggi-do, Suwon, Korea 442-749 (e-mail: yangji@ajou.ac.kr)
Accepted: 3 April 2006

Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
Intraplacental lacunae in placenta previa totalis with prior Cesarean section 179

irregular the intraplacental lacunae became, the higher the Intraplacental lacunae were graded as: Grade 0 when
frequency of placenta accreta3 . Comstock et al. reported none was seen (Figure 1a), Grade 1+ when one to three
that ultrasound examination during the second and third generally small lacunae were present (Figure 1b), Grade
trimesters provides the most reliable data to be used in 2+ when four to six larger or more irregular lacunae
diagnosing placenta accreta4 . were present (Figure 1c), and Grade 3+ when there were
The aim of this study was to investigate the value many throughout the placenta, some appearing large and
of intraplacental lacunae observed on transvaginal irregular in shape (Figure 1d). The examinations were
sonography for predicting the prognosis in patients with performed by two examiners (J. I. Y. and H. S. K.), whose
a history of Cesarean section and with placenta previa consensus opinion was finally recorded.
totalis, which are risk factors for placenta accreta. Adherent placenta was determined following surgery
and pathological analysis of the placenta, and in the
cases of Cesarean hysterectomy uterine pathology was
METHODS
also examined. Pathological diagnosis of the uterus was
The study population consisted of 51 women with a classified according to the depth of myometrial invasion
history of previous Cesarean section who were diagnosed as placenta accreta, placenta increta, or placenta percreta.
with placenta previa totalis and delivered between January In cases in which the placenta was difficult to detach from
1996 and February 2004. Ultrasound examinations were the uterus or in which a part of the placenta remained
performed throughout the second and third trimesters attached, if massive bleeding occurred on the placental
of pregnancy, and placenta previa totalis was defined site after its removal, a diagnosis of placenta accreta was
as the placenta covering the entire endocervix at made based on the operators opinion5 .
the time of delivery. Transvaginal sonography (ATL- Obstetric complications, including frequency of massive
UM9, Ultramark 9, Advanced Technology Laboratories, transfusion of more than four pints of packed red blood
Bothell, WA, USA and ALOKA SSD 5500, Corometrics cells, need for admission into intensive care unit, presence
Ultrasound Medical Systems, Wallingford, CT, USA) was of disseminated intravascular coagulopathy and Cesarean
performed to assess the presence and extent of lacunae hysterectomy, were recorded. Pathological findings and
within the placenta and classify them into four grades obstetric complications were analyzed according to the
from Grade 0 to Grade 3 according to Finbergs criteria2 . presence and absence of intraplacental lacunae.

Figure 1 Grading of intraplacental lacunae by transvaginal sonography: Grade 0 (a), Grade 1 (b), Grade 2 (c) and Grade 3 (d).

Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2006; 28: 178182.
180 Yang et al.

Students t-test, the Chi-square test and multiple In the cases with Grade 1+ lacunae (i.e. when
regression analysis were performed using the SPSS at least one lacuna was present within the placental
statistical package (version 11.5, SPSS Inc, Chicago, IL, parenchyma) the sensitivity, specificity, positive predictive
USA). value and negative predictive value for the diagnosis
of adherent placenta were 86.9%, 78.6%, 76.9% and
88.0%, respectively. In the cases with Grade 2+
RESULTS lacunae, the sensitivity, specificity, positive predictive
value and negative predictive values for diagnosing
Patient characteristics are shown in Table 1. The presence placenta increta or percreta were 100%, 97.2%, 93.8%
of lacunae within the placental parenchyma was noted and 100%, respectively (Table 3).
in 26 cases and none was seen in 25 cases. The placenta Obstetric complications were more frequent in cases
was located anteriorly in all but one case in which it was in which lacunae were present (Table 4). Cesarean
posterior. One prior Cesarean section had been performed hysterectomy was performed in 18 cases, and all of
in 46 cases (90.2%), two in four cases (7.8%) and these cases showed intraplacental lacunae on transvaginal
there was one case (2.0%) in which three prior Cesarean sonography; two cases showed Grade 1+ lacunae, 11
sections had been performed. When the cases with lacunae cases showed Grade 2+ lacunae and five cases showed
were compared with those in which no lacunae were Grade 3+ lacunae. Of the cases where no lacunae were
seen, gravidity, parity and number of previous Cesarean seen, none underwent hysterectomy.
sections were significantly higher in those with lacunae. Maternal death occurred in one case, and this patient
Maternal age, gestational age at delivery, number of had two previous Cesarean deliveries and showed Grade
dilatation and evacuations and neonatal body weight were 2+ lacunae on transvaginal sonography. Emergency
not significantly different between the groups (Table 1). Cesarean hysterectomy was performed owing to massive
The distribution of lacunae by grade among the cases is bleeding, but a thromboembolism blocked the right
shown in Table 2. More serious variants of adherent ventricle during the surgery and led to the patients death.
placenta (increta and percreta) were associated with Surgicopathological findings in this case revealed placenta
Grade 2 and 3 placental lacunae (Table 2). increta.

Table 1 Clinical characteristics according to lacunae (mean SD)


Table 3 Diagnostic accuracy of adherent placenta according to
lacunae
Lacunae
Sensitivity Specificity PPV NPV
Characteristic Absent (n = 25) Present (n = 26) P
(%) (%) (%) (%)

Maternal age (years) 31.6 4.2 32.7 4.6 NS


Diagnosis of adherent 86.9 78.6 76.9 88.0
Gestational age at 36.0 3.8 36.5 1.8 NS
placenta when
delivery (weeks)
lacunae were
Gravidity 3.4 1.1 4.3 1.4 0.020
Grade 1
Parity 1.1 0.3 1.5 0.6 0.025
Diagnosis of increta, or 100 97.2 93.8 100
Number of previous 1.2 1.1 1.8 1.3 NS
percreta when
dilatation and
lacunae were
curretage
Grade 2
Number of previous 1.0 0.2 1.4 0.6 0.006
Cesarean sections
Neonatal body weight 2831 657 3087 522 NS NPV, negative predictive value; PPV, positive predictive value.
(g)

NS, not significant; P determined by Students t-test and Chi-square Table 4 Obstetric complications according to lacunae
test.
Lacunae

Table 2 Distribution of adherent placenta according to lacunar Absent Present


grade (n = 25) (n = 26) P

Grading Transfusion (pints) 2.30 2.99 23.37 18.14 < 0.0001


Massive transfusion 6 (24.0%) 23 (88.5%) < 0.0001
Adherent Grade 0 Grade 1 Grade 2 Grade 3 ( 4 pints of PRBC)
placenta (n = 25) (n = 10) (n = 11) ( n = 5) DIC 6 (23.1%) < 0.0001
ICU admission 12 (46.2%) < 0.0001
None 22 6 Cesarean hysterectomy 18 (69.2%) < 0.0001
Accreta 3 4 1
Increta 5 4 DIC, disseminated intravascular coagulopathy; ICU, intensive care
Percreta 5 1 unit; PRBC, packed red blood cells. Analysis by multiple regression
Total 25 10 11 5 analysis (variables: gravidity, parity, Cesarean section, curettage,
anterior placenta).

Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2006; 28: 178182.
Intraplacental lacunae in placenta previa totalis with prior Cesarean section 181

DISCUSSION lacunae presented with a significantly higher rate of


clinical complication, especially related to the need for
Adherent placenta rarely occurs, but it is a major cause massive transfusion, admission to the intensive care unit
of obstetric bleeding. It can also cause uterine perforation and Cesarean hysterectomy.
and infection and is thus clinically very important. The use of color Doppler imaging can improve the
Adherent placenta can occur in the lower uterus, in the accuracy of diagnosis of adherent placenta since the depth
scar from a previous Cesarean delivery, and at the site of of invasion of the placenta into the uterine myometrium
dilatation and curettage, where the decidua basalis may or serosa can be more accurately determined, especially
be defective. The incidence of adherent placenta has been in cases where the placenta is located anteriorly10 13 .
reported as 1 in 2500 deliveries by Read et al.6 while Magnetic resonance imaging (MRI) can also be used
Gielchinsky et al.5 reported a rate of 0.9%. Its incidence, in the diagnosis14,15 and is particularly helpful when
along with that of placenta previa, has increased with the placenta is located posteriorly14 . Chou et al. used
increasing incidence of Cesarean delivery1 . the following criteria for diagnosing adherent placenta:
The diagnosis of adherent placenta is usually made diffuse or focal lacunar flow, hypervascularity of the
on delivery of the placenta, but predicting it prenatally bladderuterine serosa interface, prominent subplacental
with the use of ultrasonography is becoming increasingly venous complex and loss of subplacental Doppler vascular
common. The conventional sonographic criteria for signals. They reported a sensitivity of 82.4%, specificity
adherent placenta include absence of normal hypoechoic of 96.8%, a positive predictive value of 87.5% and
retroplacental myometrial zone, thinning or disruption a negative predictive value of 95.3%16 . Other useful
of the hyperechogenic uterine serosabladder interface, indicators on color Doppler imaging include low velocity,
the presence of focal mass-like elevations or extensions non-pulsatile flow or low-resistance pulsatile intervillous
of placental tissue beyond the uterine serosa, and flow velocity17,18 . Lerner et al. stated that since the
the presence of intraplacental lacunae. Using these existence of flow within the lacunae alone shows 100%
sonographic criteria, Finberg and Williams2 achieved sensitivity and 83% positive predictive value in diagnosing
a 77.8% positive predictive value and 93.3% negative placenta accreta, color Doppler imaging results can be
predictive value, and Guy et al. reported a 62.5% positive added to the pre-existing data on intraplacental lacunae
predictive value for adherent placenta7 . to improve the rate of diagnosis12 .
Intraplacental lacunae are vascular lakes of various Color Doppler examinations were carried out at the
sizes and shapes seen within placental parenchyma. They time of the present study but as both lacunae with
were first reported by Kerr de Mendonca3 in 1988, turbulent flow and lacunae without flow simultane-
and Hoffmann-Tretin et al.8 and Finberg and Williams2 ously appeared within the same placenta, we decided
subsequently used this as a criterion for the diagnosis of to confine our analysis to the grayscale ultrasound
adherent placenta. Their exact mechanism of development findings. However, since intraplacental lacunae tend to
is unknown, but the large amount of blood flow and high have a bleeding characteristic which stems from their
flow rate of adherent placenta9 , as well as inappropriate developmental mechanism, the comparison of adher-
placental implantation10 are reported to cause mechanical ent placenta and obstetric complications between lacu-
disruption of the placenta. Finberg and Williams classified nae with turbulent flow and those without flow is
these lacunae according to the number, size and shape considered to be helpful in predicting the clinical out-
into four grades, and reported that the higher the lacunar come.
grade, the higher the frequency of adherent placenta2 . In summary, intraplacental lacunae in patients with
Recently Comstock et al. reported that of the four criteria placenta previa totalis and with a prior Cesarean section
for diagnosing placenta accreta using ultrasonographic can be useful in predicting adherent placenta, and the
examination during the second and third trimesters, that presence of Grade 2+ lacunae is strongly associated with
of intraplacental lacunae was found to be the most reliable variants of placenta accreta such as placenta increta and
one, with 93% sensitivity and 93% positive predictive percreta. Furthermore, in cases where lacunae are seen,
value4,11 . Furthermore, they reported that intraplacental the incidence of maternal complications such as massive
lacunae were first observed at about the 15th gestational transfusion, admission to the intensive care unit and
week, thus they serve as useful indicators for the early Cesarean hysterectomy related to massive intraoperative
diagnosis of placenta accreta at around 1520 weeks bleeding increases significantly. Thus, the existence of
gestation, with a sensitivity of 79% and positive predictive intraplacental lacunae in patients with placenta previa
value of 92%. The data from the present study showed totalis with prior Cesarean section can be useful in
similar results with respect to the accuracy of predicting determining the patients clinical outcome, as well as
adherent placenta using the presence of intraplacental in counseling the patient, and in preparing her for
lacunae as the diagnostic criterion. There were three false- surgery.
negative cases but the outcome was good in each case
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Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2006; 28: 178182.

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