![A hypothesis of the increased rate of type I and type II vasa previa in ART pregnancy. Reproduced and updated the data from Biomedicines. 2022 Jul 17; 10 (7): 1722. Matsuzaki S et al. [54]. (A) The combination of velamentous cord insertion and low-lying placenta is a high-risk condition of vasa previa. (B) Abnormal placenta such as bilobed placenta or the placenta with a succenturiate lobe is a risk factor of type II vasa previa. (C) Women with ART are more likely to have velamentous cord insertion and low-lying placenta compared to those without ART pregnancy. Increased rate of velamentous cord insertion and low-lying placenta may lead to the increased rate of type I vasa previa. (D) ART may be associated with the higher incidence of abnormal placenta. This may lead to the increased rate of type II vasa previa. Abbreviations: VP, vasa previa; ART, assisted reproductive technology; VCI, velamentous cord insertion; LLP, low-lying placenta; ↑, increase; ↑↑, markedly increase.](https://www.researchgate.net/publication/366333587/figure/fig3/AS:11431281210410914@1702046108292/A-hypothesis-of-the-increased-rate-of-type-I-and-type-II-vasa-previa-in-ART-pregnancy_Q320.jpg)
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Citation: Matsuzaki, S.; Ueda, Y.;
Matsuzaki, S.; Kakuda, M.; Lee, M.;
Takemoto, Y.; Hayashida, H.; Maeda,
M.; Kakubari, R.; Hisa, T.; et al. The
Characteristics and Obstetric
Outcomes of Type II Vasa Previa:
Systematic Review and
Meta-Analysis. Biomedicines 2022,10,
3263. https://doi.org/10.3390/
biomedicines10123263
Academic Editors: Agnieszka Kordek
and Andrzej Torbé
Received: 29 November 2022
Accepted: 12 December 2022
Published: 15 December 2022
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4.0/).
biomedicines
Systematic Review
The Characteristics and Obstetric Outcomes of Type II Vasa
Previa: Systematic Review and Meta-Analysis
Shinya Matsuzaki 1, 2, *, Yutaka Ueda 2,* , Satoko Matsuzaki 3, Mamoru Kakuda 2, Misooja Lee 4, Yuki Takemoto 1,
Harue Hayashida 1, Michihide Maeda 1, Reisa Kakubari 1, Tsuyoshi Hisa 1, Seiji Mabuchi 1and Shoji Kamiura 1
1Department of Gynecology, Osaka International Cancer Institute, Osaka 541-8567, Japan
2Department of Obstetrics and Gynecology, Osaka University Graduate School of Medicine,
Osaka 565-0871, Japan
3Department of Obstetrics and Gynecology, Osaka General Medical Center, Osaka 558-8558, Japan
4Department of Forensic Medicine, School of Medicine, Kindai University, Osaka 589-8511, Japan
*Correspondence: shinya.matsuzaki@oici.jp (S.M.); y.ueda@gyne.med.osaka-u.ac.jp (Y.U.);
Tel.: +81-6-6945-1181 (S.M.); +81-6-6879-3355 (Y.U.)
Abstract:
Vasa previa is a rare fetal life-threatening obstetric disease classified into types I and II. This
study aimed to examine the characteristics and obstetric outcomes of type II vasa previa. A systematic
review was performed, and 20 studies (1998–2022) were identified. The results from six studies
showed that type II vasa previa accounted for 21.3% of vasa previa cases. The characteristics and
obstetric outcomes (rate of assisted reproductive technology (ART), antenatal diagnosis, emergent
cesarean delivery, maternal transfusion, gestational age at delivery, and neonatal mortality) were
compared between type I and II vasa previa, and all outcomes of interest were similar. The association
between ART and abnormal placenta (bilobed placenta or succenturiate lobe) was examined in three
studies, and the results were as follows: (i) increased rate of succenturiate lobes (ART versus non-ART
pregnancy; OR (odds ratio) 6.97, 95% confidence interval (CI) 2.45–19.78); (ii) similar rate of abnormal
placenta (cleavage-stage versus blastocyst embryo transfer); (iii) increased rate of abnormal placenta
(frozen versus fresh embryo transfer; OR 2.97, 95%CI 1.10–7.96). Although the outcomes of type II
vasa previa appear to be similar to those of type I vasa previa, the current evidence is insufficient for
a robust conclusion.
Keywords:
assisted reproductive technique; vasa previa; bilobed placenta; succenturiate lobes;
accessary lobes; type II vasa previa
1. General Overview
The variant of abnormal placenta that is correlated with the most adverse obstetric
outcomes is vasa previa [
1
–
4
], which is characterized by unprotected cord vessels running
near or across the internal cervical os [
1
,
2
,
5
,
6
]. The distance between the unprotected
cord vessels and internal cervical os used to diagnose vasa previa is controversial, and
fetal blood vessels running within 2 cm of the internal cervical os are recognized as vasa
previa [
7
–
10
]. The estimated prevalence of vasa previa is approximately 0.05%, and an
extremely high fetal mortality rate of 44% has been reported in women with undiagnosed
vasa previa [
11
,
12
]. In general, vasa previa is classified into two types according to its
etiology [13–19].
The combination of low-lying placenta and velamentous cord insertion has been
considered as a high-risk condition of vasa previa [
2
,
20
,
21
], and this condition may be
a majority type of vasa previa, classified as type I. In the case of a bilobed placenta or
placenta with a succenturiate lobe, unprotected vessels connecting the lobes are often
observed [
3
,
14
,
22
,
23
]. If the unprotected vessels run within 2 cm of the internal cervical
os, this condition is classified as type II vasa previa [
3
,
22
]. Recent studies have suggested
an association between assisted reproductive technology (ART) and type I vasa previa,
Biomedicines 2022,10, 3263. https://doi.org/10.3390/biomedicines10123263 https://www.mdpi.com/journal/biomedicines
Biomedicines 2022,10, 3263 2 of 17
as women who conceive by ART are more likely to have velamentous cord insertion than
those who conceive spontaneously [
2
,
21
,
24
,
25
]. Type I vasa previa is considered to increase
with the increased number of ART pregnancies, whereas the association between ART use
and type II vasa previa has not previously been examined.
Unlike type I vasa previa, no previous systematic review has focused on type II vasa
previa, and the characteristics and prognosis of this type of vasa previa are understudied
due to its rarity. Moreover, no systematic review has compared the characteristics and
prognoses of type I and II vasa previa. Therefore, this systematic review aimed to examine
the characteristics and prognosis of type II compared to type I vasa previa. This study also
aimed to determine the association between ART and abnormal placenta (bilobed placenta
or placenta with a succenturiate lobe).
2. Systematic Literature Search
2.1. Approach for Systematic Review
A systematic literature search was performed to review previous studies on type II
vasa previa. This study aimed to determine the following outcomes of primary interest:
(i) estimated frequency of type II vasa previa, (ii) obstetric outcomes of type II vasa previa,
and (iii) comparison of characteristics between type I and type II vasa previa. The secondary
interest of this study was the effect of ART on the prevalence of abnormal placenta (bilobed
placenta or placenta with a succenturiate lobe). The influence of ART on the incidence of
abnormal placenta was examined according to the type of ART used in the sensitivity anal-
ysis. In this study, bilobed placenta and succenturiate lobe caused type II vasa previa; thus,
abnormal placenta was defined as bilobed placenta and placenta with succenturiate lobe.
Following the guidelines of the Preferred Reporting Items for Systematic Reviews
and Meta-Analyses statement published in 2020 [
26
], a systematic review was performed
using three electronic search engines (PubMed, the Cochrane Central Register of Controlled
Trials (CENTRAL), and Scopus) as previously described [
27
]. Previous studies published
before 31 August 2022 were searched and screened using words related to vasa previa and
abnormal placenta (Supplemental File S1). In PubMed and Cochrane searches, Medical
Subject Headings (MeSH terms) were also used.
2.2. Article Retrieval and Search Strategy
Studies were screened by inspecting the titles and abstracts of applicable studies, as
previously reported [
28
]. Titles and abstracts were screened by Shinya Matsuzaki and
Misooja Lee. to identify studies that examined the outcomes of interest. The type of study
was defined according to the included cases as follows: (i) case report (1 or 2), (ii) case
series (3–10), and (iii) original articles (11≥).
2.3. Study Selection
To examine the primary and secondary outcomes of interest, the inclusion criteria of
studies were as follows: (1) comparative studies comparing an experimental group (type
II vasa previa and ART pregnancy) and a control group (type I vasa previa and non-ART
pregnancy), (2) the incidence of type II vasa previa was clarified, (3) type II vasa previa
was reported in a case report or case series, and (4) the number of women with abnormal
placenta and ART was clearly identified. Among the eligible studies, comparative studies
that examined the outcomes of interest (sensitivity analysis) were further examined.
The exclusion criteria were as follows: (1) insufficient information to clearly identify
the number of patients with type II vasa previa, (2) no abstract or abstract was unavailable,
(3) articles not written in English, and (4) conference abstracts, editorials, letters, reviews,
systematic reviews, and meta-analyses.
Biomedicines 2022,10, 3263 3 of 17
2.4. Data Extraction
All the information was extracted by the first author (Shinya Matsuzaki). The first
author’s name, year of publication, study location, number of included cases, number of
experimental and control groups, and outcomes of interest were recorded. Data included
in the analysis were verified by a review author (Misooja Lee).
2.5. Analysis of Outcome Measures and Assessment of Bias Risk
The primary aim of the present study was to determine the frequency and obstetric
outcomes of type II vasa previa. Since we considered that knowing the differences in type
I and II vasa previa may be useful, the characteristics and obstetric outcomes comparing
women with type I vasa previa and type II vasa previa were investigated using the included
studies as co-primary outcomes. The secondary outcome of the present study was to
examine the effect of ART on the prevalence of abnormal placenta and to review the rate
of vasa previa in women with abnormal placenta. The influence of ART types on the
prevalence of abnormal placenta was determined using sensitivity analysis.
The risk of bias in non-randomized studies of interventions tool (ROBINS-I) was used
to assess the risk of bias in included comparator studies, as previously reported [29–32].
2.6. Meta-Analysis Plan
Information was accumulated from the included studies, hazards for the outcomes of
interest were calculated using odds ratios (ORs), and 95% confidence intervals (95%CIs) for
the outcomes were considered.
The heterogeneity across the studies to evaluate the outcome of interest was exam-
ined using the I
2
statistic, which weighs the proportion of the total variation. Fixed or
random-effects analysis was performed according to the heterogeneity among the studies,
as shown in Supplemental Table S1 [
33
]. A meta-analysis was conducted, and images
and figures were assembled using RevMan ver. 5.4.1 software (Cochrane Collaboration,
Copenhagen, Denmark).
2.7. Statistical Analysis
Differences in baseline demographics between the two groups were examined using
the chi-squared or Fisher’s exact tests, as appropriate. All statistical analyses were based
on two-sided hypotheses, and a pvalue < 0.05 was considered statistically significant. The
Statistical Package for Social Sciences (SPSS, version 28.0, IBM, Armonk, NY, USA
)
or
RevMan ver. 5.4.1 software (Cochrane Collaboration, Copenhagen, Denmark) were used
for analyses.
3. Results
3.1. Study Selection
Figure 1shows the selection scheme used in this study. First, 1364 studies were
identified, and 20 studies met the study criteria for descriptive analysis [
14
,
34
–
52
]. Two
studies reported by Suzuki et al. [
36
,
37
] used overlapped data (due to overlapping study
periods); however, the outcome of interest was different in these studies. The analysis of
the prevalence of vasa previa among women with succenturiate lobes was performed in a
study published in 2010 [
36
], and the effect of ART on the prevalence of succenturiate lobe
was examined using a study published in 2008 [37].
Biomedicines 2022,10, 3263 4 of 17
Biomedicines 2022, 10, x FOR PEER REVIEW 4 of 18
Figure 1. Study selection scheme of the systematic search of previous studies. Abbreviation: VP,
vasa previa.
3.2. Study Characteristics
The summary of 20 eligible studies is presented in Table 1. Of these (n = 20), 16 studies
investigated the vasa previa, and 4 studies concerned abnormal placenta. Regarding the
study type (n = 20), all studies were retrospective in nature, 14 were original articles, 4
were case series, and 2 were case reports. Of these (n = 20), the published years were be-
tween 1998 and 2022, and all studies were retrospective [14,34–52]. No prospective studies
or randomized controlled trials have been reported.
Among the eligible studies (n = 20), approximately one-third were reported from Eu-
rope (n = 6, 30.0%) [38,41,44–46,51] followed by Japan (n = 5, 25.0%) [36,37,39,47,48], the
United States (n = 5, 25.0%) [14,35,43,49,52], and others (n = 4, 20.0%) [34,40,42,50].
Table 1. Previous studies examining women with type II vasa previa.
Author Year Location Type Total VP N Frequency ART Outcome Type I vs. II
Degirmenci Y [38]
2022 GER Series -- 5 3 -- -- Yes --
Tachibana D [39] 2021 JPN Original -- 55 13 13/55 (23.6%) Yes Yes Yes
Gross A [40] 2021 AUS Original 5905 21 3 3/21 (14.3%) -- -- Yes
Sutera M [41] 2021 ITA Original 89,600
24 9 9/24 (37.5%) -- -- Yes
Liu N [42] 2021 CHN Original 79,647
157 12 12/157 (7.6%) Yes Yes Yes
Westcott JM [43] 2020 USA Original -- 122 35 35/122 (28.7%)
-- -- Yes
Melcer Y [44] 2017 GBR Original -- 32 11 11/32 (34.4%) Yes Yes Yes
Nohuz E [45] 2017 FRN Series -- 8 5 -- -- -- --
Catanzarite V [52]
2016 USA Original -- 96 25 25/96 (26.0%) -- -- --
Carnide C [46] 2012 PRT Case -- 1 1 -- -- Yes --
Kikuchi A [47] 2011 JPN Case -- 1 1 -- -- Yes --
Hasegawa J [48] 2010 JPN Series -- 10 4 -- -- Yes --
Chmait RH [49] 2010 USA Case -- 2 2 -- -- Yes --
Catanzarite V [14]
2001 USA Series -- 10 8 -- -- Yes --
Figure 1.
Study selection scheme of the systematic search of previous studies. Abbreviation: VP,
vasa previa.
3.2. Study Characteristics
The summary of 20 eligible studies is presented in Table 1. Of these (n = 20), 16 studies
investigated the vasa previa, and 4 studies concerned abnormal placenta. Regarding the
study type (n = 20), all studies were retrospective in nature, 14 were original articles, 4 were
case series, and 2 were case reports. Of these (n = 20), the published years were between
1998 and 2022, and all studies were retrospective [
14
,
34
–
52
]. No prospective studies or
randomized controlled trials have been reported.
Table 1. Previous studies examining women with type II vasa previa.
Author Year Location Type Total VP N Frequency ART Outcome Type I vs. II
Degirmenci Y [38] 2022 GER Series – 5 3 – – Yes –
Tachibana D [39] 2021 JPN Original – 55 13 13/55 (23.6%) Yes Yes Yes
Gross A [40] 2021 AUS Original 5905 21 3 3/21 (14.3%) – – Yes
Sutera M [41] 2021 ITA Original 89,600 24 9 9/24 (37.5%) – – Yes
Liu N [42] 2021 CHN Original 79,647 157 12 12/157 (7.6%) Yes Yes Yes
Westcott JM [43] 2020 USA Original – 122 35 35/122 (28.7%) – – Yes
Melcer Y [44] 2017 GBR Original – 32 11 11/32 (34.4%) Yes Yes Yes
Nohuz E [45] 2017 FRN Series – 8 5 – – – –
Catanzarite V [52] 2016 USA Original – 96 25 25/96 (26.0%) – – –
Carnide C [46] 2012 PRT Case – 1 1 – – Yes –
Kikuchi A [47] 2011 JPN Case – 1 1 – – Yes –
Hasegawa J [48] 2010 JPN Series – 10 4 – – Yes –
Chmait RH [49] 2010 USA Case – 2 2 – – Yes –
Catanzarite V [14] 2001 USA Series – 10 8 – – Yes –
Fung TY [50] 1998 HKG Series – 3 1 – – Yes –
Baschat AA [51] 1998 GER Series – 5 4 – – Yes –
Data are presented as numbers (percentage per column). Abbreviations: GER, Germany; JPN, Japan; AUS,
Australia; ITA, Italy; CHN, China; USA, United States of America; GBR, United Kingdom; FRN, France; PRT,
Portugal; HKG, Hong Kong; Type, type of study; N, number of included cases; VP, vasa previa; ART, assisted
reproductive technology pregnancy; Original, original article; Series, case series; Case, case report; vs., versus;
Outcome, obstetric outcomes were clarified; –, not applicable.
Among the eligible studies (n = 20), approximately one-third were reported from
Europe (n= 6, 30.0%) [
38
,
41
,
44
–
46
,
51
] followed by Japan (n= 5, 25.0%) [
36
,
37
,
39
,
47
,
48
], the
United States (n= 5, 25.0%) [14,35,43,49,52], and others (n= 4, 20.0%) [34,40,42,50].
Biomedicines 2022,10, 3263 5 of 17
3.3. Risk of Bias of Included Studies
The risk of bias assessment for the included comparator studies is presented in Sup-
plemental Table S2. Among the studies (n= 6), a possible moderate publication bias in
three studies [
40
,
42
,
43
] and severe publication bias in the other three studies [
39
,
41
,
44
]
were observed.
3.4. Number of Studies: Primary Outcome
A systematic review was performed to identify previous studies that included women
with type II vasa previa, and 16 studies met the criteria (Table 1) [
14
,
38
–
52
]. Of these (n= 16),
seven studies were original articles, six were case series, and the remaining three studies
were case reports. Among the case series and reports (n= 9), the studies included women
with vasa previa, and the outcomes were reported; however, no specific characteristics or
outcomes of type II vasa previa have been reported [
14
,
38
,
45
–
51
]. Moreover, no studies
have compared the characteristics and outcomes of type I and type II vasa previa.
3.4.1. Primary Outcome: The Incidence of Type II Vasa Previa
Seven studies were identified as original articles that examined the characteristics
and outcomes of type II vasa previa [
39
–
44
,
52
]. Among the original articles (n= 7), the
rate of type II vasa previa ranged from 7.6% to 37.5% in women with vasa previa. The
cumulative rate of type II vasa previa was 21.3% (108/507 cases) among women with vasa
previa. Furthermore, the number of women without vasa previa was mentioned in three
studies [40–42]. In these studies, the prevalence of type II vasa previa in pregnant women
was estimated, and the rate ranged from 0.01% to 0.05%.
3.4.2. Co-Primary Outcome: Number of Studies Comparing Type I and II Vasa Previa
Six studies examined the obstetric outcomes of vasa previa, dividing them into type I
and type II vasa previa (Tables 1and 2). All studies compared some characteristics between
type I and type II vasa previa [39–44].
Table 2. The comparison of characteristics and outcomes between type I and type II vasa previa.
Author Year Total N Type I Type II OR (95%CI)
ART
Tachibana D [
39
]
2021 55 20 #21/35 (60.0%) 5/20 (25.0%) 0.22 (0.07–0.75)
Liu N [42] 2021 157 12 28/141 (19.9%) 0/12 (0%) 0.16 (0.01–2.77)
Melcer Y [44] 2017 32 11 8/21 (38.1%) 6/11 (54.5%) 1.95 (0.09–2.45)
Antenatal Diagnosis
Sutera M [41] 2021 24 9 13/15 (86.7%) 7/9 (77.8%) 0.54 (0.06–4.69)
Liu N [42] 2021 157 12 121/141 (85.8%) 12/12 (100%) 1.06 (0.16–6.94)
Melcer Y [44] 2017 32 11 17/21 (81.0%) 9/11 (81.8%) 4.22 (0.24–74.04)
Emergent cesarean delivery
Tachibana D [
39
]
2021 55 20 #17/35 (48.6%) 9/20 (45.0%) 0.87 (0.29–2.61)
Liu N [42] 2021 157 12 38/141 (27.0%) 1/12 (8.3%) 0.25 (0.03–1.97)
Westcott JM [43] 2020 122 35 32/86 (37.2%) 14/35 (40%) 1.81 (0.84–3.91)
Melcer Y [44] 2017 32 11 6/21 (28.6%) 6/11 (54.5%) 3.00 (0.66–13.69)
GA at delivery
Tachibana D [
39
]
2021 55 20 #35.2 ±2.1 $34.3 ±1.6 0.90 (−0.09–1.89)
Liu N [42] 2021 157 12 35.2 ±1.9 35.0 ±1.6 0.20 (−0.76–1.16)
Melcer Y [44] 2017 32 11 36.4 ±1.4 37.4 ±1.5 −
1.00 (
−
2.07–0.07)
Maternal Transfusion
Tachibana D [
39
]
2021 55 20 #11/35 (31.4%) 10/20 (50.0%) 2.18 (0.70–6.76)
Neonatal Death
Tachibana D [
39
]
2021 55 20 #0/35 (0%) 0/20 (0%) –
Liu N [42] 2021 157 12 3/141 (2.1%) 2/12 (16.7%) 9.20 (1.37–61.56)
Gross A [40] 2021 21 3 0/18 (0%) 0/3 (0%) –
Data are presented as means
±
standard deviation or numbers (percentage per column).
$
In this study, continuous
data are shown as median and range values. The standard deviation was estimated using statistical algorithms
reported by Hozo et al. [
53
].
#
Seven cases were vasa previa with vessels branching out from the placental
surface and returning to the placental cotyledons (type III vasa previa). Abbreviations: Total, total number of
included cases; N, number of included cases; Type I, type I vasa previa; Type II, type II vasa previa; ART, assisted
reproductive technology; OR, odds ratio; CI, confidence interval.
Biomedicines 2022,10, 3263 6 of 17
3.4.3. Co-Primary Outcome: Characteristics and Obstetric Outcomes Comparing Type I
and II Vasa Previa
Among the studies that compared the characteristics and obstetric outcomes between
type I and II vasa previa (n= 6), three studies examined the rate of ART [
39
,
42
,
44
], three
determined the rate of antenatal diagnosis [
41
,
42
,
44
], four investigated the rate of emer-
gent cesarean delivery [
39
,
42
–
44
], one had information regarding maternal transfusion at
delivery [
39
], and three examined the rate of neonatal death, comparing women with type
I and type II vasa previa [39,40,42].
3.4.4. Co-Primary Outcome: The Rate of ART
A meta-analysis was conducted to determine the difference in the rate of ART preg-
nancy between type I and type II vasa previa (Table 2and Figure 2). A random-effects
analysis was conducted due to the considerable heterogeneity. In the unadjusted pooled
analysis (n= 3) [39,42,44], women with type I and type II vasa previa had a similar rate of
ART pregnancy (Figure 2) (odds ratio (OR) 0.47, 95% confidence interval (95%CI), 0.09–2.45;
heterogeneity: p= 0.06, I2= 64%).
Biomedicines 2022, 10, x FOR PEER REVIEW 7 of 18
Figure 2. Meta analysis of the characteristics and outcomes of type I and type II vasa previa. The
pooled odds ratios for (A) the rate of ART (unadjusted), (B) the rate of antenatal diagnosis (unad-
justed), (C) the rate of emergent cesarean delivery (unadjusted), and (D) gestational age at delivery
between women with type I and type II vasa previa are shown. Forest plots were ordered by the
year of publication and relative weight (%) of the study within the strata. The heterogeneity among
the studies in each analysis was as follows: substantial heterogeneity (A: I2 = 64%) in the unadjusted
analysis, no heterogeneity (B: I2 = 0%) in the unadjusted analysis, low heterogeneity (C: I2 = 23%) in
the unadjusted analysis, and substantial heterogeneity (D: I2 = 70%) in the unadjusted analysis. The
above results were calculated using RevMan ver. 5.4.1 and may differ slightly from the original
values. Abbreviations: CI, confidence interval; ART, assisted reproductive technology; Emergent
CD, emergent cesarean delivery; GA, gestational age.
Figure 2. Cont.
Biomedicines 2022,10, 3263 7 of 17
Biomedicines 2022, 10, x FOR PEER REVIEW 7 of 18
Figure 2. Meta analysis of the characteristics and outcomes of type I and type II vasa previa. The
pooled odds ratios for (A) the rate of ART (unadjusted), (B) the rate of antenatal diagnosis (unad-
justed), (C) the rate of emergent cesarean delivery (unadjusted), and (D) gestational age at delivery
between women with type I and type II vasa previa are shown. Forest plots were ordered by the
year of publication and relative weight (%) of the study within the strata. The heterogeneity among
the studies in each analysis was as follows: substantial heterogeneity (A: I2 = 64%) in the unadjusted
analysis, no heterogeneity (B: I2 = 0%) in the unadjusted analysis, low heterogeneity (C: I2 = 23%) in
the unadjusted analysis, and substantial heterogeneity (D: I2 = 70%) in the unadjusted analysis. The
above results were calculated using RevMan ver. 5.4.1 and may differ slightly from the original
values. Abbreviations: CI, confidence interval; ART, assisted reproductive technology; Emergent
CD, emergent cesarean delivery; GA, gestational age.
Figure 2.
Meta analysis of the characteristics and outcomes of type I and type II vasa previa. The
pooled odds ratios for (
A
) the rate of ART (unadjusted), (
B
) the rate of antenatal diagnosis (unad-
justed), (
C
) the rate of emergent cesarean delivery (unadjusted), and (
D
) gestational age at delivery
between women with type I and type II vasa previa are shown. Forest plots were ordered by the year
of publication and relative weight (%) of the study within the strata. The heterogeneity among the
studies in each analysis was as follows: substantial heterogeneity (
A
:I
2
= 64%) in the unadjusted
analysis, no heterogeneity (
B
:I
2
= 0%) in the unadjusted analysis, low heterogeneity (
C
:I
2
= 23%)
in the unadjusted analysis, and substantial heterogeneity (
D
:I
2
= 70%) in the unadjusted analysis.
The above results were calculated using RevMan ver. 5.4.1 and may differ slightly from the original
values. Abbreviations: CI, confidence interval; ART, assisted reproductive technology; Emergent CD,
emergent cesarean delivery; GA, gestational age.
3.4.5. Co-Primary Outcome: The Rate of Antenatal Diagnosis
Since type I and type II vasa previa have different etiologies, we hypothesized that
the antenatal diagnosis of type I and type II vasa previa may be different. Specifically,
we hypothesized that as type I vasa previa often has a low-lying placenta, the antenatal
diagnosis of this type may be higher than that of type II vasa previa. To compare type I and
type II vasa previa in the examination of antenatal diagnosis, three studies were included
in the meta-analysis [
41
,
42
,
44
]. In this analysis, a fixed-effects analysis was performed
because there was no heterogeneity among the studies. In the pooled unadjusted analysis,
the rate of antenatal diagnosis was similar between the two groups (Figure 2) (OR 1.32,
95%CI 0.41–4.31; heterogeneity: p= 0.51, I2= 0%).
3.4.6. Co-Primary Outcome: The Rate of Emergent Cesarean Delivery
To assess the difference in the rate of emergent cesarean delivery, a meta-analysis was
conducted, including four eligible studies [
39
,
42
–
44
]. Due to low heterogeneity among the
studies, a fixed-effects analysis was used. In the unadjusted pooled analysis, the emergent
cesarean delivery rate was similar between women with type I and type II vasa previa
(Figure 2) (OR 1.00, 95%CI 0.58–1.74; heterogeneity: p= 0.27, I2= 23%).
3.4.7. Co-Primary Outcome: Gestational Age at Delivery
The gestational age (GA) at delivery was also compared in the present meta-analysis.
In the pooled analysis examined by a random-effect analysis due to the considerable het-
erogeneity among the studies, no significant difference in gestational week at delivery was
observed between women with type I and type II vasa previa (Figure 2) (mean difference,
−0.05; 95%CI –1.11–1.00; heterogeneity: p= 0.04, I2= 70%).
3.4.8. Co-Primary Outcome: Maternal and Neonatal Outcomes
Only a limited examination was performed to assess maternal outcomes comparing
type I and type II vasa previa. Maternal transfusion rate was examined in one study, and
the rate of transfusion at delivery was similar between type I and type II vasa previa (OR
2.18, 95%CI 0.70–6.76).
Biomedicines 2022,10, 3263 8 of 17
No previous studies have compared the neonatal transfusion rate between type I and
type II vasa previa. Three studies compared the rate of neonatal death between type I and
type II vasa previa; however, two studies showed no neonatal death [
39
,
40
]. Therefore,
a meta-analysis of neonatal death could not be performed. Among the three studies (n= 3),
two studies showed no neonatal death [
39
,
40
] whereas type II vasa previa was associated
with an increased rate of neonatal death compared to type I vasa previa (OR 9.20, 95%CI
1.37–61.56) in another study [42].
3.5. Number of Studies: Secondary Outcome
Five studies were identified to examine secondary outcomes. Of these (n= 5), two
studies examined the rate of type II vasa previa in women with abnormal placenta [
36
,
40
].
However, no studies have examined the association between ART and the prevalence of
type II vasa previa, while one study examined the relationship between ART and abnormal
placenta [37].
3.5.1. Secondary Outcome: The Rate of Vasa Previa in Abnormal Placenta
Two studies provided information to estimate the rate of vasa previa in women with ab-
normal placenta (Table 3) [
36
,
40
]. In a Japanese single-institutional retrospective study [
36
],
type II vasa previa was observed in 1/83 (1.2%) women with succenturiate lobes of the
placenta (OR 68.5, 95%CI 6.15–762.3; women without succenturiate lobes of the placenta
(0.09%)). Moreover, in an Australian single-institutional retrospective study [
40
], three
women (4.4%) with type II vasa previa were found among women with 68 succenturiate
or bilobed placentas (OR 15.6, 95%CI 4.48–54.19; women without succenturiate or bilobed
placentas (0.3%)).
Table 3. The examination for secondary outcomes and sensitivity analysis.
Author Year N VP Placenta
The rate of vasa previa in women with succenturiate lobes
Gross A [40] 2021 68 3
Succenturiate lobes, bilobed
Suzuki S [36] 2010 83 1 Succenturiate lobes
Author Year N Ab Type of ART
ART and abnormal placenta
Volodarsky A [34] 2021 677 17 Blastocyst versus Cleavage
Sacha CR [35] 2020 1140 70 Frozen versus Fresh
Suzuki S [37] 2008 7713 47 ART versus non-ART
The number of values for each examination is shown. Abbreviations: N, number of included cases; VP, vasa
previa; ART, assisted reproductive technology; Placenta, type of abnormal placenta; Ab, number of abnormal
placenta; bilobed, bilobed placenta.
3.5.2. Secondary Outcome: The Association between ART and Abnormal Placenta
One Japanese single-institutional retrospective study examined the effect of ART on
the prevalence of succenturiate lobes of the placenta (Table 4) [
37
]. In this study (n= 7713),
ART pregnancy (4/105, 3.8%) was associated with an increased rate of succenturiate lobes
of the placenta (OR 6.97, 95%CI 2.45–19.78) compared to those in non-ART pregnancies
(43/7608, 0.6%). However, no study has examined the effect of ART on the incidence of
type II vasa previa.
Biomedicines 2022,10, 3263 9 of 17
Table 4. The association between ART and abnormal placenta.
Author Year Total N Placenta Exp Cont Unadjusted
OR (95%CI)
Adjusted
OR (95%CI)
ART vs. non-ART
Suzuki S [37] 2008 7713 47 Suc 4/105 (3.8%) 43/7608 (0.6%) 6.97 (2.45–19.78) –
Blastocyst vs. Cleavage (Fresh)
Volodarsky A [34] 2021 677 17 Bil, Suc 12/425 (3.3%) 5/252 (2.0%) 1.44 (0.50–4.12) –
Frozen vs. Fresh
Sacha CR [35] 2020 1140 70 Suc 22/211 (10.4%) 48/929 (5.2%) 2.50 (1.08–5.76) 2.97 (1.10–7.96)
Day 5 Frozen vs. Fresh
Sacha CR [35] 2020 630 39 Suc 20/184 (10.9%) 19/466 (4.1%) 6.72 (1.62–27.77) 5.32 (1.54–18.38)
The number of values for each examination is shown. Abbreviations: Total, total number of included cases; N,
number of abnormal placenta cases; Frozen, frozen embryo transfer; Fresh, fresh embryo transfer; vs., versus;
ART, assisted reproductive technology; Placenta, type of abnormal placenta; Exp, experimental group; Cont,
control group; OR, odds ratio; CI, confidence interval; Suc, succenturiate lobes; Bil, bilobed placenta; and –,
not applicable.
3.6. Number of Studies: Sensitivity Analysis
Although only a limited number of studies were available to determine the effect of
ART on the prevalence of abnormal placenta, ART pregnancies have the potential to increase
the rate of abnormal placenta when compared to non-ART pregnancies. A sensitivity
analysis was conducted to examine the incidence of abnormal placenta according to ART
type. In the sensitivity analysis, two studies were available to examine the outcomes of
interest [34,35].
The Rate of Abnormal Placenta According to the Type of ART
In a Canadian retrospective cohort study, the effect of embryo stage at transfer on
placental histopathology features was examined by comparing cleavage-stage (n= 252)
and blastocyst (n= 425) embryo transfer [
34
]. In this study, all fresh embryo transfers were
performed, and the two different stages at transfer had similar rates of bilobed placenta
and succenturiate lobes (OR 1.44, 95%CI 0.50–4.12).
In a US retrospective study, placental pathology was examined by comparing ART
pregnancies with fresh or frozen embryo transfers [
35
]. In this study, frozen embryo
transfer was associated with an increased rate of succenturiate lobes of the placenta, both
in univariate analysis (OR 2.50, 95%CI 1.08–5.76) and multivariate analysis (OR 2.97,
95%CI 1.10–7.96). Frozen embryo transfer was also associated with a higher incidence of
succenturiate lobes of the placenta both in univariate analysis (OR 6.72, 95%CI 1.62–27.77)
and multivariate analysis (OR 5.32, 95%CI 1.54–18.38), even when the cases were restricted
to day 5 transfers.
4. Discussion
4.1. Principal Findings
The principal findings of this study are as follows: (i) type II vasa previa accounts
for approximately 20% of vasa previa, and approximately 4% of abnormal placenta may
develop to vasa previa, (ii) the characteristics and maternal and neonatal outcomes may
be similar between type I and type II vasa previa, (iii) ART may be associated with an
increased rate of abnormal placenta, and (iv) the incidence of abnormal placenta may be
higher in frozen embryo transfer than in fresh embryo transfer. This association between
ART and a higher incidence of abnormal placenta is interesting. Nevertheless, since the
mechanism by which ART causes the development of abnormal placenta has not been
determined in a basic study, the mechanisms of the higher incidence of abnormal placenta
induced by ART are unresolved.
4.2. Strengths and Limitations
The strength of the present study is that it is likely to be the first systematic review
that focuses on the characteristics and outcomes of type II vasa previa. Since neonatal
morbidity and mortality are high in women with vasa previa, we believe that knowing the
Biomedicines 2022,10, 3263 10 of 17
characteristics and outcomes of type II vasa previa is useful for clinicians to improve its
neonatal outcomes. We also found that ART may be associated with an increased rate of
placental abnormalities. While no study has determined the effect of ART on the frequency
of type II vasa previa, we consider that ART has the potential to be correlated with a higher
occurrence of vasa previa compared to non-ART pregnancies.
Nevertheless, several notable limitations of this study must be recognized. First, all eli-
gible studies were retrospective in nature and included a limited number of cases; therefore,
unmeasured bias such as information bias and selection bias may exist. Second, the sample
size of type II vasa previa was low in all studies and the presence of a type II error needs
to be recognized. Most studies showed only a univariate analysis; therefore, confounding
factors could not be excluded. We need to recognize that this study is underpowered
to draw robust results regarding the characteristics and outcomes of type II vasa previa.
This weakness also needs to be recognized when interpreting the results regarding the
association between ART and an abnormal placenta. No studies used multivariate analysis
to examine the effect of ART on the incidence of abnormal placenta; therefore, the present
study cannot characterize ART as a risk factor for abnormal placenta.
Third, the diagnosis of abnormal placenta may be difficult, and the definition of
abnormal placenta was not described in the included studies. Due to the difficulty of
diagnosis and the fact that the definition of abnormal placenta may be different among
the studies, these points need to be recognized as a strong limitation of this study. Fourth,
this systematic review was not pre-registered, as we considered that eligible studies may
be limited; therefore, we conducted this study after a preliminary literature search. This
point leads to bias in the systematic review and needs to be recognized as a limitation of
the present study.
Fifth, the present study may have publication bias and requires careful interpretation.
For instance, women with a poor prognosis of type II vasa previa and undiagnosed cases
may not be reported. Sixth, recent studies have suggested that fetal blood vessels running
within 2 cm of the internal cervical os are considered vasa previa; however, the ideal
distance between fetal vessels and internal os is still under debate. The definition of vasa
previa may be different among the studies, and this point is a bias of this study when
interpreting the results of incidence and outcomes of type II vasa previa.
Finally, the association between the succenturiate lobe of the placenta and ART was
examined in a previous study; however, no study has examined the association between
bilobed placenta and ART. The effect of ART on the prevalence of type II vasa previa
remains unknown.
4.3. Comparison with Existing Literature
4.3.1. The Incidence of Type II Vasa Previa
The results of the present systematic review showed that type II vasa previa accounts
for approximately 20% of all vasa previa cases. A recent study reported that the incidence
of vasa previa may be increasing with the increasing number of ART pregnancies [
54
];
however, the trends of type II vasa previa are still unknown. If ART pregnancy is associated
with an increased prevalence of abnormal placenta; the incidence of type II vasa previa
is expected to increase. Further studies are warranted to examine the trends of type II
vasa previa.
4.3.2. The Different Characteristics between Type I and Type II Vasa Previa
The present systematic review showed that a limited number of studies comparing
type I and type II vasa previa are available. From the available data, the rate of ART,
antenatal diagnosis, GA at delivery, emergent cesarean delivery, and maternal transfusion
appeared to be similar. With regard to neonatal mortality, two of three studies [39,40] had
no neonatal death in either type I or type II vasa previa, whereas one study [
42
] showed
significantly higher neonatal mortality in women with type II vasa previa (OR 9.20, 95%CI
1.37–61.56) than in those with type I vasa previa. This point was not discussed in a previous
Biomedicines 2022,10, 3263 11 of 17
study [
42
], and further studies are required to determine the neonatal mortality in women
with type II vasa previa.
4.3.3. The Association between ART and Abnormal Placenta
With regard to vasa previa, previous studies have reported an association between
ART and an increased rate of vasa previa [
2
,
21
,
24
,
25
,
55
–
58
]. However, these were not
classified as type I or type II vasa previa. The association between ART pregnancy and an
increased rate of velamentous cord insertion has been reported; therefore, type I vasa previa
was considered to have increased in the past decade [
24
,
59
–
62
]. Unlike type I vasa previa,
the association between ART and type II vasa previa has not been focused on in previous
studies. To address this problem, the present study examined the association between ART
and abnormal placenta and revealed that this association remains understudied.
A study reported by Jauniaux E et al. in 1990 [
59
] was not included in this study since
the study could not be identified by the search terms of the present study; however, this
study also reported that ART pregnancy was associated with an increased rate of abnormal
placenta (11/50 (22%), p< 0.05) compared to those in non-ART pregnancies (3/50 (6%)).
While the available data are limited, ART has the potential to increase the rate of abnormal
placenta, and frozen embryo transfer appears to be associated with an increased rate of
abnormal placenta.
4.3.4. The Mechanism of Developing Type II Vasa Previa
The mechanism of developing bilobed placenta and succenturiate lobe is believed
to result from localized atrophy due to poor decidualization [
22
,
23
,
37
]. These changes
may be more likely to be observed in the lower uterine segment due to the poor blood
supply, and lead to type II vasa previa [
63
–
66
]. However, these statements are based on a
hypothesis, and the mechanisms of bilobed placenta, succenturiate lobe, and type II vasa
previa are still understudied [
67
]. Moreover, our systematic literature search revealed that
no basic research has examined the bilobed placenta and succenturiate lobe, focusing on
the mechanism of the development of type II vasa previa.
Unlike bilobed placenta and succenturiate lobe, the development of velamentous
cord insertion has been well discussed, and two major hypotheses have been proposed
(trophotropism hypothesis and polarity hypothesis) [
54
,
62
]. The trophotropism hypothesis
was proposed to explain the development of velamentous cord insertion. The placenta
in early pregnancy migrates with proceeding gestational weeks for a better blood supply
from a more vascularized area, and these migrations may lead to an unprotected cord
with velamentous cord insertion [
68
–
70
]. In our previous meta-analysis [
54
], ART was
associated with an increased rate of velamentous cord insertion. These results appear to
support the trophotropism theory, because ART disrupts the precise timeline of biological
action required for blastocyst implantation at multiple stages [62,71].
Since the mechanism of abnormal placenta development is understudied, the asso-
ciation between ART and abnormal placenta is difficult to discuss, and further studies
are warranted to resolve the mechanism of abnormal placenta development. The risk of
obstetrical complications such as placenta accreta spectrum is different among the types of
ART [
72
], and the assessment of the prevalence of abnormal placenta according to the type
of ART may help research to identify the mechanism of development of abnormal placenta.
4.3.5. The Association between ART and Vasa Previa
Although ART has been reported as a risk factor for vasa previa [
2
,
21
,
24
,
25
,
58
], our
previous study found only one comparative study compared the rate of vasa previa between
women who conceived by ART and without ART [
73
], and the study did not consider
the differences in the type of vasa previa. The majority of type I vasa previa consists of
a combination of a low-lying placenta and velamentous cord insertion [
1
,
2
,
5
]. Since ART
pregnancy is associated with an increased rate of both velamentous cord insertion
[59,74–78]
Biomedicines 2022,10, 3263 12 of 17
and abnormal placentation, including low-lying placenta [
75
,
79
–
83
], ART may be associated
with a higher incidence of type I vasa previa.
Although the association between ART and abnormal placenta remains understudied,
we consider that ART has the potential to be associated with a higher incidence of type
II vasa previa for the following reasons: (i) a previous study suggested an association
between ART use and increased rate of abnormal placentation, (ii) frozen embryo transfer
is associated with an increased rate of prevalence of abnormal placenta, and (iii) the rate of
ART pregnancy was similar between types I and II in the present study.
Although specific data regarding ART use and vasa previa are scarce, we hypothesized
that ART use is associated with increased rates of both type I and type II vasa previa. Based
on the results of our previous systematic review [
54
] and the present study, a possible
mechanism for the increased rate of type I and type II vasa previa in ART pregnancies is
presented in Figure 3.
Biomedicines 2022, 10, x FOR PEER REVIEW 13 of 18
Figure 3. A hypothesis of the increased rate of type I and type II vasa previa in ART pregnancy.
Reproduced and updated the data from Biomedicines. 2022 Jul 17; 10 (7): 1722. Matsuzaki S et al. [54].
(A) The combination of velamentous cord insertion and low-lying placenta is a high-risk condition
of vasa previa. (B) Abnormal placenta such as bilobed placenta or the placenta with a succenturiate
lobe is a risk factor of type II vasa previa. (C) Women with ART are more likely to have velamentous
cord insertion and low-lying placenta compared to those without ART pregnancy. Increased rate of
velamentous cord insertion and low-lying placenta may lead to the increased rate of type I vasa
previa. (D) ART may be associated with the higher incidence of abnormal placenta. This may lead
to the increased rate of type II vasa previa. Abbreviations: VP, vasa previa; ART, assisted reproduc-
tive technology; VCI, velamentous cord insertion; LLP, low-lying placenta ; ↑, increase; ↑↑, markedly
increase.
5. Conclusions and Implications
5.1. Implications for Practice
While the currently available evidence for type II vasa previa is scarce, the character-
istics and outcomes appear to be similar with type I vasa previa. Despite this is only our
opinion, one study has shown worse neonatal mortality in women with type II vasa pre-
via; therefore, clinicians may consider treating type II vasa previa as a high-risk type of
vasa previa. Elucidation of the cause of worse prognosis may contribute to a reduction in
neonatal death in type II vasa previa.
The present study has shown that approximately 1–4% of abnormal placentas are
complicated with type II vasa previa, and clinicians need to notify the presence of vasa
previa in such cases.
5.2. Implications for Clinical Research
Type II vasa previa is a rare disease and no systematic review has focused on this
subtype of vasa previa. Based on the limited available data, type II vasa previa has similar
Figure 3.
A hypothesis of the increased rate of type I and type II vasa previa in ART pregnancy.
Reproduced and updated the data from Biomedicines. 2022 Jul 17; 10 (7): 1722. Matsuzaki S et al. [
54
].
(
A
) The combination of velamentous cord insertion and low-lying placenta is a high-risk condition of
vasa previa. (
B
) Abnormal placenta such as bilobed placenta or the placenta with a succenturiate
lobe is a risk factor of type II vasa previa. (
C
) Women with ART are more likely to have velamentous
cord insertion and low-lying placenta compared to those without ART pregnancy. Increased rate
of velamentous cord insertion and low-lying placenta may lead to the increased rate of type I vasa
previa. (
D
) ART may be associated with the higher incidence of abnormal placenta. This may
lead to the increased rate of type II vasa previa. Abbreviations: VP, vasa previa; ART, assisted
reproductive technology; VCI, velamentous cord insertion; LLP, low-lying placenta;
↑
, increase;
↑↑
,
markedly increase.
Biomedicines 2022,10, 3263 13 of 17
5. Conclusions and Implications
5.1. Implications for Practice
While the currently available evidence for type II vasa previa is scarce, the charac-
teristics and outcomes appear to be similar with type I vasa previa. Despite this is only
our opinion, one study has shown worse neonatal mortality in women with type II vasa
previa; therefore, clinicians may consider treating type II vasa previa as a high-risk type of
vasa previa. Elucidation of the cause of worse prognosis may contribute to a reduction in
neonatal death in type II vasa previa.
The present study has shown that approximately 1–4% of abnormal placentas are
complicated with type II vasa previa, and clinicians need to notify the presence of vasa
previa in such cases.
5.2. Implications for Clinical Research
Type II vasa previa is a rare disease and no systematic review has focused on this
subtype of vasa previa. Based on the limited available data, type II vasa previa has similar
characteristics and obstetric outcomes as type I vasa previa. Future studies that focus on
type II vasa previa are warranted to consider optimal management according to the type of
vasa previa.
Current evidence on the association between ART and abnormal placenta remains
scarce. However, a prospective study and randomized controlled study may be difficult
to conduct, and a large-scale retrospective study may therefore be suitable to examine the
relationship between ART and abnormal placentation. To exclude confounding factors,
multivariate analysis, propensity score matching, and inverse probability of treatment
weighting are warranted.
Supplementary Materials:
The following are available online at https://www.mdpi.com/article/10
.3390/biomedicines10123263/s1, Supplemental File S1: The search strategy; Supplemental
Table S1
.
The definition of heterogeneity; Supplemental Table S2. Risk of bias assessment for the compara-
tor study.
Author Contributions:
S.M (Shinya Matsuzaki)., S.M (Satoko Matsuzaki)., Y.T., M.K., M.L., R.K.,
M.M., T.H., and Y.U. designed the study, initiated the collaborations, and cleaned and analyzed the
data. S.M. (Shinya Matsuzaki), Y.T., and H.H. created the figures and tables, interpreted the results,
and drafted the manuscript with others. S.M. (Shinya Matsuzaki) and Y.U. are the corresponding
authors of the study. S.M. (Satoko Matsuzaki), M.L., Y.T., and H.H. contributed to the literature
overview, intellectual inputs, interpreted the results, and edited the manuscript. M.K., S.M. (Seiji
Mabuchi), and S.K. contributed to the study concept and design, instructed on the analytic approach,
and interpreted the results. S.K. supervised the study and revised the manuscript. All authors have
read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement:
Ethical review and approval were waived for this study due
to the use of publicly available data.
Informed Consent Statement: Not applicable.
Data Availability Statement: All the studies used in this study are published in the literature.
Conflicts of Interest: The authors declare no conflict of interest.
Transparency:
The manuscript’s corresponding authors (S.M. [Shinya Matsuzaki] and Y.U.) affirm
that the manuscript is an honest, accurate, and transparent account of the study being reported; that
no important aspects of the study have been omitted; and that any discrepancies from the study as
planned (and, if relevant, registered) have been explained.
Biomedicines 2022,10, 3263 14 of 17
References
1.
Mitchell, S.J.; Ngo, G.; Maurel, K.A.; Hasegawa, J.; Arakaki, T.; Melcer, Y.; Maymon, R.; Vendittelli, F.; Shamshirsaz, A.A.; Erfani,
H.; et al. Timing of birth and adverse pregnancy outcomes in cases of prenatally diagnosed vasa previa: A systematic review and
meta-analysis. Am. J. Obstet. Gynecol. 2022,227, 173–181.e24. [CrossRef] [PubMed]
2.
Pavalagantharajah, S.; Villani, L.A.; D’Souza, R. Vasa previa and associated risk factors: A systematic review and meta-analysis.
Am. J. Obstet. Gynecol. MFM 2020,2, 100117. [CrossRef] [PubMed]
3.
Melcer, Y.; Maymon, R.; Jauniaux, E. Vasa previa: Prenatal diagnosis and management. Curr. Opin. Obstet. Gynecol.
2018
,30,
385–391. [CrossRef] [PubMed]
4.
Jauniaux, E.; Melcer, Y.; Maymon, R. Prenatal diagnosis and management of vasa previa in twin pregnancies: A case series and
systematic review. Am. J. Obstet. Gynecol. 2017,216, 568–575. [CrossRef] [PubMed]
5.
Matsuzaki, S.; Endo, M.; Kimura, T. Vasa previa with an intact amniotic membrane. Am. J. Obstet. Gynecol.
2017
,216, 616.e1–616.e2.
[CrossRef]
6.
Society of Maternal-Fetal (SMFM) Publications Committee; Sinkey, R.G.; Odibo, A.O.; Dashe, J.S. #37: Diagnosis and management
of vasa previa. Am. J. Obstet. Gynecol. 2015,213, 615–619. [CrossRef]
7.
Swank, M.L.; Garite, T.J.; Maurel, K.; Das, A.; Perlow, J.H.; Combs, C.A.; Fishman, S.; Vanderhoeven, J.; Nageotte, M.; Bush, M.;
et al. Vasa previa: Diagnosis and management. Am. J. Obstet. Gynecol. 2016,215, 223.e1–223.e6. [CrossRef]
8.
Klahr, R.; Fox, N.S.; Zafman, K.; Hill, M.B.; Connolly, C.T.; Rebarber, A. Frequency of spontaneous resolution of vasa previa with
advancing gestational age. Am. J. Obstet. Gynecol. 2019,221, 646.e1–646.e7. [CrossRef]
9.
Sinkey, R.G.; Odibo, A.O. Vasa previa screening strategies: Decision and cost-effectiveness analysis. Ultrasound Obs. Gynecol
2018
,
52, 522–529. [CrossRef]
10.
Green, A.; Chiu, S.; Manor, E.; Smith, L.; Oyelese, Y. The association of gestational age at delivery with neonatal outcomes in
prenatally diagnosed vasa previa. J. Matern. Fetal Neonatal Med. 2022,35, 10162–10167. [CrossRef]
11.
Gagnon, R. No. 231-Guidelines for the Management of Vasa Previa. J. Obstet. Gynaecol. Can. JOGC J. D’obstetrique Et Gynecol. Du
Can. JOGC 2017,39, e415–e421. [CrossRef] [PubMed]
12.
Tsakiridis, I.; Mamopoulos, A.; Athanasiadis, A.; Dagklis, T. Diagnosis and Management of Vasa Previa: A Comparison of 4
National Guidelines. Obs. Gynecol. Surv. 2019,74, 436–442. [CrossRef]
13.
Jauniaux, E.; Alfirevic, Z.; Bhide, A.G.; Burton, G.J.; Collins, S.L.; Silver, R. Vasa Praevia: Diagnosis and Management: Green-top
Guideline No. 27b. Bjog 2019,126, e49–e61. [CrossRef]
14.
Catanzarite, V.; Maida, C.; Thomas, W.; Mendoza, A.; Stanco, L.; Piacquadio, K.M. Prenatal sonographic diagnosis of vasa previa:
Ultrasound findings and obstetric outcome in ten cases. Ultrasound Obs. Gynecol. 2001,18, 109–115. [CrossRef] [PubMed]
15.
Ruiter, L.; Kok, N.; Limpens, J.; Derks, J.B.; de Graaf, I.M.; Mol, B.W.; Pajkrt, E. Systematic review of accuracy of ultrasound in the
diagnosis of vasa previa. Ultrasound Obs. Gynecol 2015,45, 516–522. [CrossRef] [PubMed]
16.
Rebarber, A.; Dolin, C.; Fox, N.S.; Klauser, C.K.; Saltzman, D.H.; Roman, A.S. Natural history of vasa previa across gestation
using a screening protocol. J. Ultrasound Med. 2014,33, 141–147. [CrossRef] [PubMed]
17.
Br˛eborowicz, G.H.; Markwitz, W.; Szpera-Go´zdziewicz, A.; Dera-Szymanowska, A.; Ropacka-Lesiak, M.; Szyma ´nski, P.;
Kubiaczyk-Paluch, B. Prenatal diagnosis of vasa previa. J. Matern. Fetal Neonatal Med. 2015,28, 1806–1808. [CrossRef]
18.
Baumfeld, Y.; Gutvirtz, G.; Shoham, I.; Sheiner, E. Fetal heart rate patterns of pregnancies with vasa previa and velamentous cord
insertion. Arch. Gynecol. Obstet. 2016,293, 361–367. [CrossRef]
19.
Ibirogba, E.R.; Shazly, S.A.; Chmait, R.H.; Ruano, R. Is there a role for fetoscopic laser ablation therapy in Type-2 vasa previa?
Ultrasound Obs. Gynecol. 2019,54, 696. [CrossRef]
20.
Siargkas, A.; Tsakiridis, I.; Pachi, C.; Mamopoulos, A.; Athanasiadis, A.; Dagklis, T. Impact of velamentous cord insertion on
perinatal outcomes: A systematic review and meta-analysis. Am. J. Obstet. Gynecol. MFM 2022,5, 100812. [CrossRef]
21.
Zhang, W.; Geris, S.; Al-Emara, N.; Ramadan, G.; Sotiriadis, A.; Akolekar, R. Perinatal outcome of pregnancies with prenatal
diagnosis of vasa previa: Systematic review and meta-analysis. Ultrasound Obs. Gynecol.
2021
,57, 710–719. [CrossRef] [PubMed]
22. Ruiter, L.; Kok, N.; Limpens, J.; Derks, J.B.; de Graaf, I.M.; Mol, B.; Pajkrt, E. Incidence of and risk indicators for vasa praevia: A
systematic review. BJOG 2016,123, 1278–1287. [CrossRef] [PubMed]
23.
Kamijo, K.; Miyamoto, T.; Ando, H.; Tanaka, Y.; Kikuchi, N.; Shinagawa, M.; Yamada, S.; Asaka, R.; Fuseya, C.; Ohira, S.; et al.
Clinical characteristics of a novel “Type 3” vasa previa: Case series at a single center. J. Matern. Fetal Neonatal Med.
2021
,35,
7730–7736. [CrossRef] [PubMed]
24.
Schachter, M.; Tovbin, Y.; Arieli, S.; Friedler, S.; Ron-El, R.; Sherman, D.
In vitro
fertilization is a risk factor for vasa previa. Fertil.
Steril. 2002,78, 642–643. [CrossRef]
25.
Pirtea, L.C.; Grigora¸s, D.; Sas, I.; Ilie, A.C.; Stana, L.G.; Motoc, A.G.; Jianu, A.M.; Mazilu, O.
In vitro
fertilization represents a risk
factor for vasa praevia. Rom. J. Morphol. Embryol. Rev. Roum. Morphol. Embryol. 2016,57, 627–632.
26.
Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Moher, D.
Updating guidance for reporting systematic reviews: Development of the PRISMA 2020 statement. J. Clin. Epidemiol.
2021
,134,
103–112. [CrossRef]
27.
Matsuzaki, S.; Lee, M.; Nagase, Y.; Jitsumori, M.; Matsuzaki, S.; Maeda, M.; Takiuchi, T.; Kakigano, A.; Mimura, K.; Ueda, Y.; et al.
A systematic review and meta-analysis of obstetric and maternal outcomes after prior uterine artery embolization. Sci. Rep.
2021
,
11, 16914. [CrossRef]
Biomedicines 2022,10, 3263 15 of 17
28.
Matsuzaki, S.; Endo, M.; Ueda, Y.; Mimura, K.; Kakigano, A.; Egawa-Takata, T.; Kumasawa, K.; Yoshino, K.; Kimura, T. A case
of acute Sheehan’s syndrome and literature review: A rare but life-threatening complication of postpartum hemorrhage. BMC
Pregnancy Childbirth 2017,17, 188. [CrossRef]
29.
Sterne, J.A.; Hernan, M.A.; Reeves, B.C.; Savovic, J.; Berkman, N.D.; Viswanathan, M.; Henry, D.; Altman, D.G.; Ansari, M.T.;
Boutron, I.; et al. ROBINS-I: A tool for assessing risk of bias in non-randomised studies of interventions. BMJ
2016
,355, i4919.
[CrossRef]
30.
Danna, S.M.; Graham, E.; Burns, R.J.; Deschenes, S.S.; Schmitz, N. Association between Depressive Symptoms and Cognitive
Function in Persons with Diabetes Mellitus: A Systematic Review. PLoS ONE 2016,11, e0160809. [CrossRef]
31.
ROBINS-I Detailed Guidance. 2016. Available online: https://www.riskofbias.info/welcome/home/current- version-of- robins-
i/robins-i-detailed-guidance-2016 (accessed on 30 September 2022).
32.
Matsuzaki, S.; Nagase, Y.; Ueda, Y.; Lee, M.; Matsuzaki, S.; Maeda, M.; Takiuchi, T.; Kakigano, A.; Mimura, K.; Endo, M.; et al.
The association of endometriosis with placenta previa and postpartum hemorrhage: A systematic review and meta-analysis. Am.
J. Obstet. Gynecol. MFM 2021,3, 100417. [CrossRef] [PubMed]
33.
Chapter 10: Analysing Data and Undertaking Meta-Analyses. In Cochrane Handbook for Systematic Reviews of Interventions, Version
6.1 ed; Cochrane: London, UK, 2020. Available online: https://training.cochrane.org/handbook/current/chapter-10 (accessed
on 30 September 2022).
34.
Volodarsky-Perel, A.; Ton Nu, T.N.; Buckett, W.; Machado-Gedeon, A.; Cui, Y.; Shaul, J.; Dahan, M.H. Effect of embryo stage at
transfer on placental histopathology features in singleton live births resulting from fresh embryo transfers. Fertil. Steril.
2021
,115,
673–682. [CrossRef] [PubMed]
35.
Sacha, C.R.; Harris, A.L.; James, K.; Basnet, K.; Freret, T.S.; Yeh, J.; Kaimal, A.; Souter, I.; Roberts, D.J. Placental pathology in live
births conceived with
in vitro
fertilization after fresh and frozen embryo transfer. Am. J. Obstet. Gynecol.
2020
,222, 360.e1–360.e16.
[CrossRef] [PubMed]
36.
Suzuki, S.; Igarashi, M.; Inde, Y.; Miyake, H. Abnormally shaped placentae in twin pregnancy. Arch. Gynecol. Obstet.
2010
,281,
65–69. [CrossRef]
37.
Suzuki, S.; Igarashi, M. Clinical significance of pregnancies with succenturiate lobes of placenta. Arch. Gynecol. Obstet.
2008
,277,
299–301. [CrossRef] [PubMed]
38.
Degirmenci, Y.; Steetskamp, J.; Macchiella, D.; Hasenburg, A.; Hasenburg, A. Vasa previa: A rare obstetric complication-A case
series and a literature review. Clin. Case Rep. 2022,10, e05608. [CrossRef] [PubMed]
39.
Tachibana, D.; Misugi, T.; Pooh, R.K.; Kitada, K.; Kurihara, Y.; Tahara, M.; Hamuro, A.; Nakano, A.; Koyama, M. Placental Types
and Effective Perinatal Management of Vasa Previa: Lessons from 55 Cases in a Single Institution. Diagnostics
2021
,11, 1369.
[CrossRef]
40.
Gross, A.; Markota Ajd, B.; Specht, C.; Scheier, M. Systematic screening for vasa previa at the 20-week anomaly scan. Acta Obstet.
Et Gynecol. Scand. 2021,100, 1694–1699. [CrossRef]
41.
Sutera, M.; Garofalo, A.; Pilloni, E.; Parisi, S.; Alemanno, M.G.; Menato, G.; Sciarrone, A.; Viora, E. Vasa previa: When antenatal
diagnosis can change fetal prognosis. J. Perinat. Med. 2021,49, 915–922. [CrossRef]
42.
Liu, N.; Hu, Q.; Liao, H.; Wang, X.; Yu, H. Vasa previa: Perinatal outcomes in singleton and multiple pregnancies. Biosci. Trends
2021,15, 118–125. [CrossRef]
43.
Westcott, J.M.; Simpson, S.; Chasen, S.; Vieira, L.; Stone, J.; Doulaveris, G.; Dar, P.; Bernstein, P.S.; Atallah, F.; Dolin, C.D.; et al.
Prenatally diagnosed vasa previa: Association with adverse obstetrical and neonatal outcomes. Am. J. Obstet. Gynecol. MFM
2020
,
2, 100206. [CrossRef] [PubMed]
44.
Melcer, Y.; Maymon, R.; Pekar-Zlotin, M.; Levinsohn-Tavor, O.; Tovbin, J.; Jauniaux, E. Evaluation of the impact of vasa previa on
feto-placental hormonal synthesis and fetal growth. Eur. J. Obstet. Gynecol. Reprod. Biol. 2017,215, 193–196. [CrossRef]
45.
Nohuz, E.; Boulay, E.; Gallot, D.; Lemery, D.; Vendittelli, F. Can we perform a prenatal diagnosis of vasa previa to improve its
obstetrical and neonatal outcomes? J. Gynecol. Obstet. Hum. Reprod. 2017,46, 373–377. [CrossRef] [PubMed]
46.
Carnide, C.; Jerónimo, M.; Faria, D.; Silva, I.S. Twin pregnancy complicated by vasa previa. BMJ Case Rep.
2012
,2012,
bcr2012006484. [CrossRef]
47.
Kikuchi, A.; Uemura, R.; Serikawa, T.; Takakuwa, K.; Tanaka, K. Clinical significances of magnetic resonance imaging in prenatal
diagnosis of vasa previa in a woman with bilobed placentas. J. Obstet. Gynaecol. Res. 2011,37, 75–78. [CrossRef]
48.
Hasegawa, J.; Farina, A.; Nakamura, M.; Matsuoka, R.; Ichizuka, K.; Sekizawa, A.; Okai, T. Analysis of the ultrasonographic
findings predictive of vasa previa. Prenat. Diagn. 2010,30, 1121–1125. [CrossRef]
49.
Chmait, R.H.; Chavira, E.; Kontopoulos, E.V.; Quintero, R.A. Third trimester fetoscopic laser ablation of type II vasa previa. J.
Matern. -Fetal Neonatal Med. 2010,23, 459–462. [CrossRef]
50.
Fung, T.Y.; Lau, T.K. Poor perinatal outcome associated with vasa previa: Is it preventable? A report of three cases and review of
the literature. Ultrasound Obs. Gynecol. 1998,12, 430–433. [CrossRef]
51.
Baschat, A.A.; Gembruch, U. Ante- and intrapartum diagnosis of vasa praevia in singleton pregnancies by colour coded Doppler
sonography. Eur. J. Obstet. Gynecol. Reprod. Biol. 1998,79, 19–25. [CrossRef]
52.
Catanzarite, V.; Cousins, L.; Daneshmand, S.; Schwendemann, W.; Casele, H.; Adamczak, J.; Tith, T.; Patel, A. Prenatally
Diagnosed Vasa Previa: A Single-Institution Series of 96 Cases. Obstet. Gynecol. 2016,128, 1153–1161. [CrossRef]
Biomedicines 2022,10, 3263 16 of 17
53.
Hozo, S.P.; Djulbegovic, B.; Hozo, I. Estimating the mean and variance from the median, range, and the size of a sample. BMC
Med. Res. Methodol. 2005,5, 13. [CrossRef] [PubMed]
54.
Matsuzaki, S.; Ueda, Y.; Matsuzaki, S.; Nagase, Y.; Kakuda, M.; Lee, M.; Maeda, M.; Kurahashi, H.; Hayashida, H.; Hisa, T.; et al.
Assisted Reproductive Technique and Abnormal Cord Insertion: A Systematic Review and Meta-Analysis. Biomedicines
2022
,10,
1722. [CrossRef] [PubMed]
55.
de Los Reyes, S.; Henderson, J.; Eke, A.C. A systematic review and meta-analysis of velamentous cord insertion among singleton
pregnancies and the risk of preterm delivery. Int. J. Gynaecol. Obstet. 2018,142, 9–14. [CrossRef] [PubMed]
56.
Ismail, K.I.; Hannigan, A.; O’Donoghue, K.; Cotter, A. Abnormal placental cord insertion and adverse pregnancy outcomes: A
systematic review and meta-analysis. Syst. Rev. 2017,6, 242. [CrossRef]
57.
Vahanian, S.A.; Lavery, J.A.; Ananth, C.V.; Vintzileos, A. Placental implantation abnormalities and risk of preterm delivery: A
systematic review and metaanalysis. Am. J. Obstet. Gynecol. 2015,213, S78–S90. [CrossRef]
58.
Society for Maternal-Fetal Medicine (SMFM); Ghidini, A.; Gandhi, M.; McCoy, J.; Kuller, J.A.; Publications Committee. Society
for Maternal-Fetal Medicine Consult Series #60: Management of pregnancies resulting from
in vitro
fertilization. Am. J. Obstet.
Gynecol. 2022,226, B2–B12. [CrossRef]
59.
Jauniaux, E.; Englert, Y.; Vanesse, M.; Hiden, M.; Wilkin, P. Pathologic features of placentas from singleton pregnancies obtained
by in vitro fertilization and embryo transfer. Obstet. Gynecol. 1990,76, 61–64.
60.
Yanaihara, A.; Hatakeyama, S.; Ohgi, S.; Motomura, K.; Taniguchi, R.; Hirano, A.; Takenaka, S.; Yanaihara, T. Difference in the
size of the placenta and umbilical cord between women with natural pregnancy and those with IVF pregnancy. J. Assist. Reprod.
Genet. 2018,35, 431–434. [CrossRef]
61.
Gavriil, P.; Jauniaux, E.; Leroy, F. Pathologic examination of placentas from singleton and twin pregnancies obtained after
in vitro
fertilization and embryo transfer. Pediatr. Pathol. 1993,13, 453–462. [CrossRef]
62.
Hasegawa, J.; Iwasaki, S.; Matsuoka, R.; Ichizuka, K.; Sekizawa, A.; Okai, T. Velamentous cord insertion caused by oblique
implantation after in vitro fertilization and embryo transfer. J. Obstet. Gynaecol. Res. 2011,37, 1698–1701. [CrossRef]
63.
Sinha, P.; Kaushik, S.; Kuruba, N.; Beweley, S. Vasa praevia: A missed diagnosis. J. Obstet. Gynaecol.
2008
,28, 600–603. [CrossRef]
64.
Jansen, C.; Kleinrouweler, C.E.; Kastelein, A.W.; Ruiter, L.; van Leeuwen, E.; Mol, B.W.; Pajkrt, E. Follow-up ultrasound in
second-trimester low-positioned anterior and posterior placentae: Prospective cohort study. Ultrasound Obs. Gynecol.
2020
,56,
725–731. [CrossRef] [PubMed]
65.
Hasegawa, J.; Matsuoka, R.; Ichizuka, K.; Otsuki, K.; Sekizawa, A.; Farina, A.; Okai, T. Cord insertion into the lower third of
the uterus in the first trimester is associated with placental and umbilical cord abnormalities. Ultrasound Obs. Gynecol
2006
,28,
183–186. [CrossRef]
66.
Silver, R.M. Abnormal Placentation: Placenta Previa, Vasa Previa, and Placenta Accreta. Obstet. Gynecol.
2015
,126, 654–668.
[CrossRef] [PubMed]
67.
Baergen, R.N.; Matrai, C. Placental Shape Aberrations. In Benirschke’s Pathology of the Human Placenta; Baergen, R.N., Burton, G.J.,
Kaplan, C.G., Eds.; Springer International Publishing: Cham, Switzerland, 2022; pp. 403–411.
68.
Monie, I.W. Velamentous Insertion of the Cord in Early Pregnancy. Am. J. Obstet. Gynecol.
1965
,93, 276–281. [CrossRef] [PubMed]
69.
Hasegawa, J.; Farina, A.; Simonazzi, G.; Bisulli, M.; Puccetti, C.; Pilu, G.; Gabrielli, S.; Rizzo, N. Umbilical cord insertion into
the lower segment of the uterus at 11 to 13 weeks’ gestation is associated with maternal serum PAPP-A. Prenat. Diagn.
2011
,31,
434–438. [CrossRef]
70.
Tsakiridis, I.; Dagklis, T.; Athanasiadis, A.; Dinas, K.; Sotiriadis, A. Impact of Marginal and Velamentous Cord Insertion on
Uterine Artery Doppler Indices, Fetal Growth, and Preeclampsia. J. Ultrasound Med. 2021,41, 2011–2018. [CrossRef]
71.
Hasegawa, J. Sonoembryological evaluations of the development of placenta previa and velamentous cord insertion. J. Obstet.
Gynaecol. Res. 2015,41, 1–5. [CrossRef]
72.
Matsuzaki, S.; Nagase, Y.; Takiuchi, T.; Kakigano, A.; Mimura, K.; Lee, M.; Matsuzaki, S.; Ueda, Y.; Tomimatsu, T.; Endo, M.;
et al. Antenatal diagnosis of placenta accreta spectrum after
in vitro
fertilization-embryo transfer: A systematic review and
meta-analysis. Sci. Rep. 2021,11, 9205. [CrossRef]
73.
Baulies, S.; Maiz, N.; Muñoz, A.; Torrents, M.; Echevarría, M.; Serra, B. Prenatal ultrasound diagnosis of vasa praevia and analysis
of risk factors. Prenat. Diagn. 2007,27, 595–599. [CrossRef]
74.
Yang, M.; Zheng, Y.; Li, M.; Li, W.; Li, X.; Zhang, X.; Wang, R.; Zhang, J.; Zhou, F.; Yang, Q.; et al. Clinical features of velamentous
umbilical cord insertion and vasa previa: A retrospective analysis based on 501 cases. Medicine
2020
,99, e23166. [CrossRef]
[PubMed]
75.
Cochrane, E.; Pando, C.; Kirschen, G.W.; Soucier, D.; Fuchs, A.; Garry, D.J. Assisted reproductive technologies (ART) and placental
abnormalities. J. Perinat. Med. 2020,48, 825–828. [CrossRef] [PubMed]
76.
O’Quinn, C.; Cooper, S.; Tang, S.; Wood, S. Antenatal Diagnosis of Marginal and Velamentous Placental Cord Insertion and
Pregnancy Outcomes. Obstet. Gynecol. 2020,135, 953–959. [CrossRef]
77.
Kalafat, E.; Thilaganathan, B.; Papageorghiou, A.; Bhide, A.; Khalil, A. Significance of placental cord insertion site in twin
pregnancy. Ultrasound Obs. Gynecol. 2018,52, 378–384. [CrossRef]
78.
Ebbing, C.; Johnsen, S.L.; Albrechtsen, S.; Sunde, I.D.; Vekseth, C.; Rasmussen, S. Velamentous or marginal cord insertion and the
risk of spontaneous preterm birth, prelabor rupture of the membranes, and anomalous cord length, a population-based study.
Acta Obstet. Et Gynecol. Scand. 2017,96, 78–85. [CrossRef]
Biomedicines 2022,10, 3263 17 of 17
79.
Wang, J.; Liu, Q.; Deng, B.; Chen, F.; Liu, X.; Cheng, J. Pregnancy outcomes of Chinese women undergoing IVF with embryonic
cryopreservation as compared to natural conception. BMC Pregnancy Childbirth 2021,21, 39. [CrossRef]
80.
Qin, J.; Sheng, X.; Wu, D.; Gao, S.; You, Y.; Yang, T.; Wang, H. Adverse Obstetric Outcomes Associated With In Vitro Fertilization
in Singleton Pregnancies. Reprod. Sci. 2017,24, 595–608. [CrossRef]
81.
Healy, D.L.; Breheny, S.; Halliday, J.; Jaques, A.; Rushford, D.; Garrett, C.; Talbot, J.M.; Baker, H.W. Prevalence and risk factors for
obstetric haemorrhage in 6730 singleton births after assisted reproductive technology in Victoria Australia. Hum. Reprod.
2010
,25,
265–274. [CrossRef]
82.
Sabban, H.; Zakhari, A.; Patenaude, V.; Tulandi, T.; Abenhaim, H.A. Obstetrical and perinatal morbidity and mortality among
in-vitro fertilization pregnancies: A population-based study. Arch. Gynecol. Obstet. 2017,296, 107–113. [CrossRef]
83.
Matsuzaki, S.; Ueda, Y.; Nagase, Y.; Matsuzaki, S.; Kakuda, M.; Kakuda, S.; Sakaguchi, H.; Hisa, T.; Kamiura, S. Placenta
Accreta Spectrum Disorder Complicated with Endometriosis: Systematic Review and Meta-Analysis. Biomedicines 2022,10, 390.
[CrossRef]
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