Download as pdf or txt
Download as pdf or txt
You are on page 1of 12

Ultrasound Obstet Gynecol 2021; 57: 366–377

Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.23108

Definition, prevalence, clinical relevance and treatment of


T-shaped uterus: systematic review
M. A. COELHO NETO1,2 , A. LUDWIN3,4 , F. PETRAGLIA5 and W. P. MARTINS2
1
Department of Obstetrics and Gynecology, Faculty of Medicine of Ribeirão Preto, University of São Paulo (DGO-FRMP-USP), Ribeirão
Preto, Brazil; 2 SEMEAR Fertilidade, Reproductive Medicine, Ribeirão Preto, Brazil; 3 Department of Gynecology and Oncology,
Jagiellonian University, Krakow, Poland; 4 Ludwin & Ludwin Gynecology, Private Medical Center, Krakow, Poland; 5 Department of
Clinical and Experimental Biomedical Sciences, University of Florence, Florence, Italy

K E Y W O R D S: congenital uterine anomaly; diethylstilbestrol; dysmorphic uterus agreement; lateral indentation; Müllerian
ducts; T-shaped uterus

CONTRIBUTION and including at least 10 women were considered eligi-


ble. Studies regarding DES-related T-shaped uterus were
What are the novel findings of this work?
excluded because DES has not been used since 1971.
The prevalence, etiology and clinical relevance of
There were no restrictions on language, date of publica-
T-shaped uterus remain unclear. As most studies on
tion or status of publication.
T-shaped uterus use different definitions, it is probable
that women with a normal uterus are being subjected to Results Of 2504 records identified by the electronic
metroplasty. The evidence supporting surgical treatment search, 20 studies were included in the systematic
for T-shaped uterus is of very low quality, based largely review. The majority of studies were of poor quality.
on studies lacking a control group. In 11 of 16 studies reporting on the diagnosis of
T-shaped uterus, the diagnostic method used was
What are the clinical implications of this work? three-dimensional ultrasound. There is no consensus on
Surgical treatment for T-shaped uterus is not supported the definition of T-shaped uterus, but the most cited
by robust evidence. Expectant management should be criteria (4/16 studies) were of the European Society of
considered the most appropriate choice for women with Human Reproduction and Embryology and the European
a T-shaped uterus based on current research. Society for Gynaecological Endoscopy (ESHRE/ESGE;
2013). The prevalence of T-shaped uterus varied from
0.2% to 10% in the four included studies reporting
ABSTRACT such data. With respect to etiology (except for DES),
Objectives To summarize in a systematic review the cur- T-shaped uterus was considered a primary condition in
rent evidence regarding definitions, diagnosis, prevalence, three studies and secondary to adhesions in five and
etiology, clinical relevance and impact of surgical treat- adenomyosis in one. T-shaped uterus was related to
ment for T-shaped uterus not related to diethylstilbestrol worse reproductive outcome based on subfertility (nine
(DES) exposure, and to highlight areas on which future studies), miscarriage (seven studies), preterm delivery
research should focus. (two studies), ectopic pregnancy (one study) and repeat
implantation failure (seven studies). Of the 12 studies
Methods A search of PubMed, Scopus and EMBASE that reported on the effects of surgical treatment of
was performed on 9 April 2020 using the search terms T-shaped uterus by hysteroscopic metroplasty, some
‘t-shaped OR t-shape OR infantile OR (lateral indenta- mentioned an improvement in pregnancy rate (rates
tion) OR (diethylstilbestrol OR DES) AND (uterus OR ranging from 49.6% to 88%; eight studies), live-birth
uterine OR uteri) AND (anomaly OR anomalies OR rate (rates ranging from 35.1% to 76%; seven studies)
malformation OR malformations)’. Additionally, the ref- and term-delivery rate (four studies) and a reduction
erence lists of the included studies were searched manually in miscarriage (rates ranging from 7% to 49.6%; five
for other relevant publications. All studies presenting data studies) and ectopic pregnancy (one study). However,
on T-shaped uterus not associated with DES exposure the evidence is of very low quality with serious/critical

Correspondence to: Dr M. A. Coelho Neto, University of São Paulo, Department of Obstetrics and Gynecology, Medical School of Ribeirão
Preto, av. bandeirantes 3900 monte legre, Ribeirão Preto, São Paulo 14049-900, Brazil (e-mail: marcelalencar@hotmail.com)
Accepted: 16 August 2020

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. SYSTEMATIC REVIEW


14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
T-shaped uterus 367

risk of bias toward overestimating the intervention effect. This study aims to summarize in a systematic
Some authors reported no complications related to the review all available information regarding the definition
procedure, while others mentioned persistence of the (criteria), diagnosis (diagnostic tools, accuracy, reliability/
dysmorphism (rates ranging from 1.4% to 11%; three agreement), prevalence, etiology and clinical relevance
studies), bleeding (1.3%; one study), infection (2.6%; one and effectiveness of interventions for T-shaped uterus not
study) and adhesions (11.1% and 16.8%; two studies). related to DES exposure, and to highlight areas on which
future research should focus.
Conclusions The prevalence, etiology and clinical rele-
vance, with respect to reproductive outcome, of T-shaped
uterus remain unclear and there is no consensus on METHODS
the definition and diagnostic method for this condition.
The protocol of this systematic review was registered with
Expectant management should be considered the most
PROSPERO (registration number: CRD42019115131;
appropriate choice for everyday practice until randomized
http://www.crd.york.ac.uk/prospero/).
controlled trials show a benefit of intervention. © 2020
International Society of Ultrasound in Obstetrics and
Gynecology. Eligibility criteria
All studies related to T-shaped uterus not associated with
DES exposure in utero were included in this systematic
INTRODUCTION review, irrespective of their design. Cases series were
considered if they included at least 10 women. We
T-shaped uterus is considered a congenital uterine malfor-
included studies regardless of their objectives, since our
mation resulting from the failure of later embryological aim was to evaluate criteria for definition, diagnostic
development of the uterus1 . Until the 1980s, T-shaped method, prevalence, reproductive outcome and effective-
uterus was commonly related to diethylstilbestrol (DES) ness of intervention. We decided to exclude studies on
exposure in utero; however, decades after the withdrawal DES-related T-shaped uterus because this drug has not
of DES from use during pregnancy, women are still pre- been used since 1971 and, therefore, women included in
senting with T-shaped uterus and its cause remains poorly such studies encompass a different population from that
understood2 . A T-shaped uterus typically exhibits a nar- in which we were interested, as women currently at repro-
rowed uterine cavity with lateral indentations3 , with the ductive age have not been exposed to DES. However, we
shape of the endometrial cavity resembling the letter still included the term ‘diethylstilbestrol OR DES’ in our
T instead of a triangle2 . Three-dimensional ultrasound search because some authors might continue to use the
(3D-US) allows detailed visualization of the uterine cav- term DES-related anomaly to refer to T-shaped uterus.
ity, uterine walls and external contours of the uterus
in the mid-coronal plane4 , thus facilitating non-invasive
assessment of T-shaped uterus. Hysteroscopy, a minimally Search strategy and selection of studies
invasive method, enables visualization of the inside of the We searched PubMed, Scopus and EMBASE using the
cervical canal and endometrial cavity besides allowing following search terms: ‘t-shaped OR t-shape OR infantile
treatment of T-shaped uterus. OR (lateral indentation) OR (diethylstilbestrol OR DES)
The T-shaped uterus was first described by Kaufman AND (uterus OR uterine OR uteri) AND (anomaly OR
et al.5 in 1977 as a DES-related defect, then in 1979 by anomalies OR malformation OR malformations)’.
Buttram and Gibbons6 as a class-VI Müllerian anomaly The last electronic search was performed on 9 April
secondary to DES exposure in utero and later in the 2020. Titles and abstracts were reviewed independently
American Fertility Society (AFS) classification, in 1988, by two authors (W.P.M. and M.A.C.N.), who checked for
as a type-VII DES-related Müllerian duct defect7 . In duplicates and used pre-established criteria for inclusion
2013, the European Society of Human Reproduction and (T-shaped uterus not related to DES exposure). There
Embryology and the European Society for Gynaecological were no restrictions on language, date of publication or
Endoscopy (ESHRE/ESGE) proposed a definition for status of publication. The reference lists of the included
T-shaped uterus as a narrow uterine cavity due to studies and related reviews were searched manually for
thickened lateral walls, with proportions of 2/3 uterine potentially relevant articles not identified by the electronic
corpus and 1/3 cervix3 . search. Some references which the authors knew to be
The prevalence of T-shaped uterus8 and its impact on relevant were added manually if they had not already
reproductive outcome remain unknown9 . The presence been identified by the earlier searches.
of uterine anomalies is not evaluated in patients from Three authors (M.A.C.N., W.P.M. and A.L.) retrieved
the general population who are asymptomatic. Therefore, the full-text manuscripts of the references considered to be
the available studies on T-shaped uterus are largely on potentially eligible after screening the abstract. This step
patients with a history of impaired reproductive outcome. was particularly difficult since some of the publications
In these patients, hysteroscopic metroplasty has been were very old, mainly regarding DES exposure, or not in
considered as a treatment option2 , but there is no robust English. One author (A.L.) also asked the librarians of his
evidence regarding its efficacy or safety. institution to help retrieve some full-text manuscripts.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
368 Coelho Neto et al.

Data collection and extraction true effect is likely to be substantially different from that
observed in this review.
Data extraction was performed in a standardized way
by two authors (W.P.M. and M.A.C.N.). Disagreements
were solved by consultation with a third author (A.L.). Synthesis of results
Eligibility was assessed against the inclusion/exclusion
Data are presented in descriptive tables separately for
criteria, and studies were included or excluded, as
diagnostic criteria, prevalence, clinical relevance with
appropriate. The studies were characterized according
respect to reproductive outcome and effect of surgical
to their design.
treatment. As there were no studies considered to be
The following data were extracted from the eligible
sufficiently similar, the results of the individual studies
studies: criteria and method of diagnosis, prevalence,
could not be combined in a meta-analysis and they were
etiology and clinical relevance of T-shaped uterus
synthesized in tables.
with respect to reproductive outcome (subfertility,
previous miscarriage, recurrent miscarriage, miscarriage
per pregnancy, preterm birth, repeat implantation failure RESULTS
(RIF), ectopic pregnancy). For the studies that proposed
surgical intervention for the treatment of T-shaped uterus, Study selection and characteristics
the type of intervention and description of the method A total of 2504 records (PubMed, n = 505, Scopus,
were extracted together with the reported reproductive n = 750 and EMBASE, n = 1249) were identified by the
outcome. The primary outcomes of interest were live electronic search and 31 additional studies by manual
birth, clinical pregnancy and miscarriage. The authors of search. Of these, 729 were duplicates and 1674 were
the original studies were contacted to obtain additional excluded after reading the title and abstract as they
data whenever necessary. were not related to T-shaped uterus (Figure 1). We eval-
uated 132 potentially eligible records in full text, of
Quality assessment of studies which 112 were excluded because T-shaped uterus was
related to DES exposure (n = 64)5,13–75 ; the article was
For retrospective observational studies, the Newcastle– not related to T-shaped uterus (n = 26)76–101 ; the study
Ottawa quality assessment form for cohort studies was included fewer than 10 women with a T-shaped uterus
used to assess the risk of bias (http://www.ohri.ca/ (n = 15)4,102–115 ; no detailed results for T-shaped uterus
programs/clinical_epidemiology/oxford.asp). Reliability/ were reported (n = 4)116–119 ; and the article was a descrip-
agreement studies were judged according to the tive review (n = 3)120–122 . Therefore, 20 studies were
quality appraisal of diagnostic reliability (QAREL) eventually included in this systematic review2,9,123–140
tool10 . Diagnostic accuracy studies were judged (Figure 1).
according to QUADAS-2 (https://www.bristol.ac.uk/
population-health-sciences/projects/quadas/quadas-2/)11 .
Risk of bias was assessed independently by two Diagnosis of T-shaped uterus
researchers (M.A.C.N. and W.P.M.), and disagreements Sixteen studies mentioned the diagnostic methods and/
were solved by consultation with a third author (A.L.). or criteria for T-shaped uterus (Table S1)2,9,123–129,132,133,
135–138,140
. The most commonly cited diagnostic method
Overall quality of evidence was 3D-US (11 studies), while other methods mentioned
were magnetic resonance imaging (MRI), hysteroscopy,
The quality of the body of evidence was classified accord- hysterosalpingography and two-dimensional ultrasound.
ing to the Grading of Recommendations Assessment, Considering 3D-US and MRI as adequate methods for
Development and Evaluation (GRADE) criteria, which diagnosing uterine malformations because they allow
take into account risk of bias, consistency of the effect, visualization of the coronal view of the uterus, 12 studies
imprecision, indirectness and publication bias12 . The qual- mentioned at least one adequate method for diagnosing
ity of evidence was evaluated independently by two T-shaped uterus.
reviewers (M.A.C.N. and W.P.M.) and disagreements In four126,128,135,140 of the 16 studies, the diagnosis
were solved by discussion with a third author (A.L.). of T-shaped uterus was performed in a subjective way.
The quality of evidence was interpreted as follows12 . Four studies123,125,133,138 used the criteria proposed by
High quality: we are very confident that the true effect lies ESHRE/ESGE3 , according to which a T-shaped uterus
close to that observed in this review; moderate quality: presents with a narrow uterine cavity due to thickened
we are moderately confident in the effect estimate, the lateral walls without specifying a definition and cut-off
true effect is likely to be close to that observed in this for thickened lateral walls and narrow uterine cavity.
review, but there is a possibility that it is substantially Eight studies proposed their own criteria for diagnosing
different; low quality: our confidence in the effect estimate T-shaped uterus2,9,124,127,129,132,136,137 (Table S1). In the
is limited, the true effect may be substantially different studies of Neal et al.124 and Ludwin et al.9 , the diagnosis of
from that observed in this review; or very low quality: T-shaped uterus was made subjectively by experts as a first
we have very little confidence in the effect estimate, the step, before the authors proposed their own diagnostic

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
T-shaped uterus 369

criteria. The study of Ludwin et al.9 also compared Etiology of T-shaped uterus
the diagnostic accuracy of the subjective opinion of
Seven studies mentioned the etiology of T-shaped
individual experts to that of measurements performed
uterus2,124,126,129,131,133,137 , however, we found no
by 3D-US. The definition for T-shaped uterus proposed
research focusing on the cause of T-shaped uterus. Şükür
by the Congenital Uterine Malformation by Experts
et al.137 reported that the etiology of this condition is
(CUME) group, using strict measurable criteria and
unknown but is likely to be secondary to adhesions.
based on the diagnosis made most often by independent
Three studies124,129,133 reported that T-shaped uterus is a
experts, includes lateral indentation angle ≤ 130◦ , lateral
primary condition and five2,124,126,133,137 that it presents
indentation depth ≥ 7 mm and T-angle ≤ 40◦ , with
secondary to adhesions. One study linked T-shaped
good diagnostic accuracy and moderate interobserver
uterus to adenomyosis131 .
reproducibility9 . This classification was published recently
and is yet to be used by other authors.
Reproductive outcome
T-shaped uterus is generally reported to be associated with
Prevalence of T-shaped uterus worse reproductive outcome (Table 2). Nine studies high-
lighted a relationship between subfertility and T-shaped
Four studies included information about the prevalence uterus123–128,135,137,140 . Most of these studies included
of T-shaped uterus124,131,133,134 . The studies involved only patients with subfertility123,124,126,128,135,140 . More-
different populations; specifically, women undergoing over, two of these studies included women with unex-
hysteroscopy due to infertility133 , infertile women plained subfertility127,128 , while three others included
undergoing in-vitro fertilization (IVF)124 , patients with women with other cause of subfertility123,126,137 . Only
singleton pregnancy with uterine anomaly diagnosed two studies provided a control group for comparison
during pregnancy134 and women with adenomyosis131 , (subfertile patients with normal uterus)123,124 . In the
and, therefore, the prevalence of T-shaped uterus varied three studies that did not include solely women with
widely from 0.2 to 10% (Table 1). None of the studies subfertility125,127,137 , the prevalence of subfertility in
that provided data to infer prevalence mentioned objective women with a T-shaped uterus ranged from 45% to
measurements and respective cut-offs for the diagnosis of 74.2%, which was considered to be significantly higher
T-shaped uterus131,133,134 . than the 15% found in the general population141 .

Records identified through Records identified through


electronic search manual search
(n = 2504) (n = 31)

Total records
(n = 2535)

Duplicates removed (n = 729)

Title/abstract screened
(n = 1806)

Eligibility criteria not met (n = 1674)

Full-text articles assessed


for eligibility
(n = 132)

Excluded (n = 112):
• DES-related T-shaped uterus (n = 64)
• Not related to T-shaped uterus (n = 26)
• Fewer than 10 women with T-shaped uterus (n = 15)
• No results for T-shaped uterus (n = 4)
• Descriptive review (n = 3)

Included in systematic review


(n = 20)

Figure 1 Flowchart summarizing selection of studies on T-shaped uterus for inclusion in systematic review. DES, diethylstilbestrol.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
370 Coelho Neto et al.

Table 1 Prevalence of T-shaped uterus reported in included studies

Study Prevalence Population Observations

Di Spiezio 12/324 (3.7) Women undergoing hysteroscopy Prevalence of T-shaped uterus in excluded women is
Sardo (2015)133 due to infertility unknown. Diagnosis was made by hysteroscopy
and 3D ultrasound. Authors report they used
ESHRE/ESGE definition3 in their prospective study
performed between June 2011 and March 2012;
however, ESHRE/ESGE definition of T-shaped
uterus was unknown during study period
Fox (2014)134 10/4473 (0.2) Women with singleton pregnancy Diagnosis made based on 1998 American Fertility
> 22 weeks, diagnosed with Society classification
uterine anomaly during pregnancy
Neal (2019)124 10/648 (1.5) Infertile patients undergoing in-vitro Study mentions measurements and comparison of
fertilization T-shaped with normal and intermediate uterus, but
is not clear regarding criteria to diagnose T-shaped
uterus
Puente (2016)131 25/248 (10.1) Women with adenomyosis Study uses term ‘pseudo T-shaped’ uterus, which has
similar appearance to T-shaped uterus, but does
not include objective diagnostic criteria

Only first author of each study is given. Data are given as n/N (%).

The presence of subfertility in patients presenting with uterus123,124,126–128,139,140 . This varied between 3.7%
T-shaped uterus in the included studies does not allow and 35.1% in the studies that did not include solely
us to conclude that subfertility is consequent to T-shaped women with RIF. The definition of RIF was not uniform
uterus as this may be only a reflection of the inclusion between the studies, including two or more failed IVF
criteria used by the studies. cycles despite good quality embryos126,127 , absence of
Seven studies included patients with T-shaped uterus pregnancy after transfer of ≥ 5 embryos140 and three
and a history of previous miscarriage123–127,136,139 , or more failed IVF cycles123 , while one study described
with the prevalence varying between 22% and 50%. the number of RIF per patient128 . One study, which did
One study included only patients with a history of not provide a definition for RIF124 , included a control
miscarriage136 . Only two studies123,124 had a control group and showed an incidence of 10% in women with
group of patients with a normal uterus for comparison, T-shaped uterus vs 7% in women with normal uterus.
one of which showed that the history of miscarriage was The most accepted definition of RIF in the literature is
five times more common in patients with a T-shaped three consecutive failed IVF attempts with transfer of
uterus compared to those with a normal uterus124 and one to two embryos of high-grade quality, and based
the other that it was similar between the two groups123 . on this definition, the expected prevalence of RIF is
Five studies reported on the incidence of recurrent approximately 10%143 . Considering this 10% expected
miscarriage in women with a T-shaped uterus123–127 . prevalence of three consecutive negative pregnancy tests
Two of these studies compared the prevalence of recurrent following embryo transfer (the studies on T-shaped uterus
miscarriage between women with a T-shaped and those did not mention the quality of the embryos transferred
with a normal uterus, showing a higher prevalence in and therefore the expected prevalence would be higher),
patients with T-shaped uterus (20% vs 10.2% in Neal we found that one study showed a much higher incidence
et al.124 and 17.6% vs 10.8% in Uyar et al.123 , though (35.1%)123 of RIF in women with T-shaped uterus,
the difference did not reach statistical significance in the one reported a similar proportion (14.3%)126 and one
latter study). For the other studies, it is possible to infer reported a lower proportion (3.7%)128 of RIF in women
the higher prevalence of recurrent miscarriage in patients with T-shaped uterus.
with T-shaped uterus, which was 17.9–33.3%125–127 vs One study128 reported a 15.5% prevalence of ectopic
approximately 5% in the general population142 . One pregnancy in women with T-shaped uterus, much higher
study did not clarify what was defined as repeat pregnancy than the 1–2% expected in the general population144 .
loss124 . The definition used in most studies was two
or more spontaneous early pregnancy losses123,125–127
and two studies added a negative work-up including Effect of surgical treatment
karyotype analysis and antiphospholipid syndrome126,127 .
Two studies128,137 reported a very high rate (> 80%) of Since there are concerns that T-shaped uterus may be asso-
miscarriage per clinical pregnancy. One study134 reported ciated with poor reproductive outcome, some authors are
a high rate (20%) of preterm delivery related to T-shaped proposing hysteroscopic metroplasty as potential treat-
uterus, while in another study128 , no patient with a ment for T-shaped uterus in patients with a history
T-shaped uterus had preterm delivery. of impaired reproductive outcome. Recently, a cascade
Seven studies reported on the prevalence of of surgical reports on metroplasty of T-shaped uterus
RIF in patients presenting with a T-shaped has been published2,123,125–130,135–137,139 (Table S2). All

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
T-shaped uterus 371

the studies mentioned improvement of reproductive out- 83.3%123,125,127 , miscarriage rate between 7% and
come in patients with T-shaped uterus after metro- 49.6%123,125,127,128,137 and live-birth rate varied between
plasty: eight studies reported an increase in preg- 35.1% and 76%2,123,125,127,129,130,135 .
nancy rate123,125–128,135,137,139 , seven studies reported Complications related to the procedure varied between
increase in live-birth rate2,123,125,127,129,130,135 , five studies the studies, from no complications126–128,136 to per-
reported reduction in miscarriage rate2,127–129,137 , four sistence of the dysmorphism requiring complementary
studies reported increased term-delivery rate128,135–137 hysteroscopic approach (1.4%125 ; 3.8%137 ; 11%139 );
and one study reported reduction in ectopic-pregnancy bleeding (1.3%137 ); infection (2.6%137 ) and adhesions
rate128 (Table 3). After metroplasty, pregnancy rate (16.8%125 ; 11.1%139 ).
varied between 49.6% and 88%123,126,128,135,137,139 , One study did not ask for approval of the institu-
clinical pregnancy rate was between 43.2% and tional review board125 . The surgical technique used for

Table 2 Association of T-shaped uterus with reproductive outcome

Prevalence Prevalence
in women in women
with T-shaped with normal/
Study uterus arcuate uterus Conclusion

Subfertility
Alonso Pacheco (2019)127 27/60 (45.0) NR No comparison made in study; high risk vs general population
Boza (2019)126 56/56 (100) NR No comparison made in study; high risk vs general population
Di Spiezio Sardo (2020)125 92/124 (74.2) NR No comparison made in study; high risk vs general population
Ferro (2018)140 190/190 (100) NR No comparison made in study; high risk vs general population
Haydardedeoglu (2018)128 272/272 (100) NR No comparison made in study; high risk vs general population
Mounir (2012)135 88/88 (100) NR No comparison made in study; high risk vs general population
Neal (2019)124 10/10 (100) 472/472 (100) No conclusion
Şükür (2018)137 43/78 (55.1) NR No comparison made in study; high risk vs general population
Uyar (2019)123 74/74 (100) 148/148 (100) No conclusion
Previous miscarriage
Alonso Pacheco (2019)127 20/60 (33.3) NR No comparison made in study; high risk vs general population
Boza (2019)126 22/56 (39.3) NR No comparison made in study; high risk vs general population
Di Spiezio Sardo (2020)125 32/124 (25.8) NR No conclusion
Ferro (2009)139 4/18 (22.2) NR No conclusion
Giacomucci (2011)136 17/17 (100) NR No conclusion
Neal (2019)124 5/10 (50.0) 48/472 (10.2) T-shaped uterus is higher risk
Uyar (2019)123 19/74 (25.7) 25/148 (16.9) Similar risk
Recurrent miscarriage
Alonso Pacheco (2019)127 20/60 (33.3) NR No comparison made in study; high risk vs general population
Boza (2019)126 10/56 (17.9) NR No comparison made in study; high risk vs general population
Di Spiezio Sardo (2020)125 32/124 (25.8) NR No comparison made in study; high risk vs general population
Neal (2019)124 2/10 (20.0) 48/472 (10.2) T-shaped uterus is higher risk
Uyar (2019)123 13/74 (17.6) 16/148 (10.8) Similar risk
Miscarriage per pregnancy
Haydardedeoglu (2018)128 93/110 (84.5) NR No comparison made in study; high risk vs general population
Şükür (2018)137 63/75 (84.0) NR No comparison made in study; high risk vs general population
Preterm delivery
Fox (2014)134 2/10 (20) NR No conclusion
Haydardedeoglu (2018)128 0/110 (0) NR No conclusion
Repeat implantation failure
Alonso Pacheco (2019)127 16/60 (26.7) NR No comparison made in study; high risk vs general population
Boza (2019)126 8/56 (14.3) NR No comparison made in study; high risk vs general population
Ferro (2009)139 5/18 (27.8) NR No conclusion
Ferro (2018)140 190/190 (100) NR No comparison made in study; high risk vs general population
Haydardedeoglu (2018)128 10/272 (3.7) NR No comparison made in study; high risk vs general population
Neal (2019)124 1/10 (10.0) 31/472 (6.6) T-shaped uterus is higher risk
Uyar (2019)123 26/74 (35.1) 26/148 (17.6) T-shaped uterus is higher risk
Ectopic pregnancy
Haydardedeoglu (2018)128 17/110 (15.5) NR T-shaped uterus is higher risk

Only first author of each study is given. Data are given as n/N (%). In general population: prevalence of subfertility is about 15%141 ;
prevalence of previous miscarriage is near 15%159 ; prevalence of recurrent miscarriage (two or more losses < 24 weeks of gestation) is
5%142 ; prevalence of repeat implantation failure (after three consecutive in-vitro fertilization attempts, in which one or two high-grade
quality embryos were transferred in each cycle) is 10%143 ; preterm-delivery rate is 5–10% in singletons and 40–60% in multiples160 ;
ectopic-pregnancy prevalence is 1–2%144 . NR, not reported.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
372 Coelho Neto et al.

Table 3 Summary of conclusions of studies assessing hysteroscopic metroplasty for improvement of reproductive outcome in women with
T-shaped uterus

Study Pregnancy rate Live-birth rate Miscarriage rate Term-delivery rate Ectopic-pregnancy rate

Alonso Pacheco (2019)127 Improved Improved Reduced NR NR


Boza (2019)126 Improved NR NR NR NR
Di Spiezio Sardo (2020)125 Improved Improved Not clear NR NR
Ducellier-Azzola (2018)129 NR Improved Reduced NR NR
Fernandez (2011)2 NR Improved Reduced NR NR
Ferro (2009)139 Improved NR NR NR NR
Giacomucci (2011)136 NR NR NR Improved NR
Haydardedeoglu (2018)128 Improved NR Reduced Improved Reduced
Mounir (2012)135 Improved Improved NR Improved NR
Soekoer (2016)130 NR Improved NR NR NR
Şükür (2018)137 Improved NR Reduced Improved NR
Uyar (2019)123 Improved Improved Not clear NR NR

Only first author of each study is given. NR, not reported.

T-shaped uterus varied greatly across the identified studies DISCUSSION


(Table S2). Importantly, we did not find any randomized
controlled trial (RCT) evaluating the value of hystero- The prevalence of T-shaped uterus ranged between 0.2%
scopic metroplasty on treatment of T-shaped uterus, only and 10% in the studies included in this systematic review.
observational studies, none of which had a control group The etiology of T-shaped uterus is still unknown, being
of untreated women for comparison. Four studies recog- considered to be of primary origin or secondary to adhe-
sions or adenomyosis in different studies. Moreover, there
nized the controversy of indicating metroplasty for women
is no universal definition for T-shaped uterus and its diag-
with T-shaped uterus125,126,129,140 . Nine studies recog-
nosis is performed by different methods, mainly by 3D-US
nized the need of prospective controlled trials to delin-
(Figures 2 and 3). Studies on T-shaped uterus were largely
eate a recommendation for hysteroscopic metroplasty for
performed in women with impaired reproductive out-
patients with T-shaped uterus2,123,125–128,133,136,140 .
come and the benefits of surgical treatment for T-shaped
uterus seem to be largely exaggerated. This systematic
review revealed that the available evidence regarding the
Quality of studies
diagnosis, prevalence, clinical relevance and particularly
All of the retrospective observational studies included interventions for T-shaped uterus is of very low quality.
in the systematic review were considered to be of poor There is no consensus on the diagnostic criteria for
quality2,123–130,133,135–140 , except for the study of Fox T-shaped uterus. Four studies used the ESHRE/ESGE
et al.134 , which was rated as moderate quality (it was use- definition3 for T-shaped uterus, however, this definition
ful for the study of prevalence and clinical relevance of is unclear and likely to be misinterpreted as it is based
T-shaped uterus) (Table S3). The only identified diagnos- on the subjective assessment of the observer rather than
tic accuracy study9 was judged to have low risk of bias objective criteria. No measurable cut-offs were provided
according to QUADAS-2 (Table S4). The same study9 was
the only one assessing reliability/agreement in the diag-
nosis of T-shaped uterus and was considered to be of
moderate quality according to QAREL (Table S5). All the
studies assessing interventions were of poor quality (obser-
vational and quasiexperimental with before–after design).

Quality of evidence

The quality of the evidence was judged to be very


low according to GRADE. The quality of evidence was
downgraded two levels because only observational studies
were included. Further downgrade was performed because
of important limitations of the included studies, such as
lack of a control group and high risk of bias. Moreover, Figure 2 Hysterosalpingography of uterus with two patent tubes.
the quality of the evidence was also downgraded Shape of uterine cavity can be considered to resemble a T instead of
a triangle. However, diagnosis is dependent on subjective judgment
because of serious imprecision (studies with small sample
and it may not be reproducible between observers. Moreover,
size; median, 47 (interquartile range, 19.5–80.5)) and observer cannot be sure whether uterine cavity is assessed in
inconsistency of the results observed across the studies. coronal or oblique view.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
T-shaped uterus 373

for the definition of narrow uterine cavity and thickened to provide objective criteria for T-shaped uterus using
lateral walls. Using the ESHRE/ESGE classification, 70% as reference standard the decision made most often by
of women have a uterine malformation106 . Reports expert clinicians, surgeons and sonologists9 (Figure 4).
of surgical treatment for uterine malformations were The effectiveness of surgical treatment for T-shaped
uncommon before this classification was proposed106,145 , uterus was assessed based on only observational studies
which is associated with overestimation of uterine lacking a control group of untreated patients undergoing
anomalies and potential surgical treatment of patients expectant management. However, only well-designed
with a normal uterus146,147 . CUME was the first study RCTs would be able to assess the effectiveness and

Figure 3 Coronal view of uterus obtained using three-dimensional (3D) ultrasound (a,b), 3D sonohysterography with HDlive render
mode (c), 3D sonohysterography with volume contrast imaging (d) and 3D sonohysterography with automatic volume calculation software
(SonoAVC; SonoHysteroAVC technique) (e). Performing measurements with high reliability is challenging considering that subtle uterine
contractions and peristalsis can influence endometrial cavity and that quality of imaging is not perfect. One can consider saline 3D-sonohystero-
graphy to improve quality of imaging and delineation of uterine cavity contour. With additional use of automatic volume calculation
software161 , it is possible to assess uterine cavity volume, another interesting parameter for further research, and better understand diversity
of uterine morphology and its impact on reproductive outcome.

≤ 40° ≥ 7 mm ≤ 130°

Figure 4 Coronal view of uterus obtained with curved render modes of three-dimensional transvaginal sonography. Top row: HDlive mode;
bottom row: volume contrast imaging. Uterine cavity shape can be suspected to be T-shaped based on subjective impression (bottom row),
however, without measurements, reliability of diagnosis is only moderate among representative experts. According to Congenital Uterine
Malformation by Experts (CUME) group, three sonographic criteria should be present (lateral indentation depth ≥ 7 mm, lateral indentation
angle ≤ 130◦ and T-angle ≤ 40◦ ) for reliable and accurate diagnosis of T-shaped uterus9 . CUME definition of T-shaped uterus reflects
diagnosis made most often by several representative experts. When CUME definition and criteria are used, doctors and patients can be
confident that diagnosis of T-shaped uterus has high probability of being correct.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
374 Coelho Neto et al.

safety of the intervention148 . The challenges regarding metroplasty for dysmorphic uterus in patients with
T-shaped uterus are similar to those for septate uterus: a previous miscarriage158 (class U1 includes T-shaped
hysteroscopic septum resection for septate uterus has been uterus, uterus infantilis and other minor deformities3 )
performed worldwide for more than 30 years without included six studies, all of which were also included in
high-quality supporting evidence148–150 . The largest the present review2,125,126,129,133,137 , and concluded on
multicenter cohort study on septum resection in women the benefit of metroplasty based on a live-birth rate of
with a septate uterus included 257 patients diagnosed with 50%, clinical pregnancy rate of 73% and miscarriage
a septate uterus over a period of 37 years151 ; the diagnostic rate of 23%. Quality assessment of the studies, using the
methods and criteria varied in such a long interval, as did Newcastle–Ottawa Scale, showed an overall good score
the management of the patients149 . In this cohort, 80 of regarding the selection and comparability of the study
151 (53%) women who underwent metroplasty had at groups, as well as for ascertainment of the outcomes of
least one live birth, compared to 76 out of 106 (71.7%) interest158 , however, none of the studies had a control
who had expectant management, and the study concluded group.
that metroplasty does not improve live-birth rate or For future studies, there is a need for reliable and widely
decrease miscarriage or preterm birth when compared accepted criteria for diagnosing T-shaped uterus. We need
to expectant management151 . Another important issue of to assess initially whether women with reliable diagnosis
performing hysteroscopic metroplasty in patients with a of T-shaped uterus have worse reproductive outcome
septate uterus, despite the lack of good-quality evidence when compared to women with normal/arcuate uterus. If
about its effectiveness and safety, is the difficulty to evidence of impaired reproductive outcome is found, an
recruit participants in clinical trials when the patients RCT evaluating the effectiveness and safety of metroplasty
think that the intervention is effective, as a patient may is necessary before incorporating this intervention into
not want to be randomized in a trial in which there is clinical practice.
a possibility that they will not receive any treatment.
The only concluded RCT on the topic took 10 years to Conclusions
randomize 80 women152 , a very long time to provide some
light on the topic. Recently announced results confirm that The true prevalence, causes and clinical relevance of
septum resection related to ESHRE/ESGE classification T-shaped uterus are still unclear as the available
does not improve reproductive outcome153 . studies use different definitions and diagnostic criteria for
The studies reporting on reproductive outcome of this condition. Additionally, robust evidence is lacking
women with a T-shaped uterus, included in this systematic regarding the effect of proposed interventions for
review, used different inclusion criteria for women with T-shaped uterus, such as hysteroscopic metroplasty, as
history of impaired reproductive outcome in addition to there is currently no RCT on this topic and the available
different diagnostic methods and criteria for T-shaped observational studies use inconsistent diagnostic methods
uterus. The surgical technique proposed for treating the and definitions and do not have a control group for
condition varied between the studies. Therefore, it was comparison. We would discourage performing more
not possible to combine data in a meta-analysis due to uncontrolled before–after studies on T-shaped uterus,
the design and heterogeneity of the studies. The observed which are likely to add nothing to what is already
improvement in reproductive outcome related to surgical known. Until RCTs prove the benefit and safety of
treatment is most likely the result of very high risk of surgical treatment for T-shaped uterus, women should
bias toward overestimation of the treatment effect, as the not be exposed to the risk and financial burden of this
before–after design of the studies with the same group of intervention, which is also associated with a financial
women serving as test and control always favors the tested burden to healthcare systems and societies. Expectant
intervention, particularly when all included participants management should be considered the most appropriate
have not achieved success before the intervention148 . choice in daily practice for women with a T-shaped uterus.
A recently published review, focusing on reproductive
outcome following hysteroscopic metroplasty of patients
REFERENCES
with a T-shaped uterus and history of poor reproductive
outcome154 , concluded that hysteroscopic metroplasty 1. Acien P, Acien M. The presentation and management of complex female genital
malformations. Hum Reprod Update 2016; 22: 48–69.
is a simple procedure which can potentially improve 2. Fernandez H, Garbin O, Castaigne V, Gervaise A, Levaillant JM. Surgical approach
to and reproductive outcome after surgical correction of a T-shaped uterus. Hum
reproductive outcome, but the data are not robust. Of Reprod 2011; 26: 1730–1734.
the 15 studies included in that review, seven were also 3. Grimbizis GF, Gordts S, Di Spiezio Sardo A, Brucker S, De Angelis C, Gergolet M,
included in the present review2,129,130,133,135,136,138 , and Li TC, Tanos V, Brolmann H, Gianaroli L, Campo R. The ESHRE/ESGE consensus
on the classification of female genital tract congenital anomalies. Hum Reprod
of the rest, seven were not eligible (two due to DES 2013; 28: 2032–2044.
exposure155,156 , two due to inclusion of fewer than 10 4. Graupera B, Pascual MA, Hereter L, Browne JL, Ubeda B, Rodriguez I, Pedrero C.
Accuracy of three-dimensional ultrasound compared with magnetic resonance
women with T-shaped uterus113,114 , two not reporting imaging in diagnosis of Müllerian duct anomalies using ESHRE/ESGE consensus
the outcomes for T-shaped uterus separately118,119 and on the classification of congenital anomalies of the female genital tract. Ultrasound
Obstet Gynecol 2015; 46: 616–622.
one that did not mention T-shaped uterus157 ) and one 5. Kaufman RH, Binder GL, Gray PM, Adam E. Upper genital tract changes associated
with exposure in utero to diethylstilbestrol. Am J Obstet Gynecol 1977; 128: 51–59.
could not be identified because it was missing from 6. Buttram VC, Jr., Gibbons WE. Müllerian anomalies: a proposed classification. (An
the list of references. Another review on hysteroscopic analysis of 144 cases). Fertil Steril 1979; 32: 40–46.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
T-shaped uterus 375

7. The American Fertility Society classifications of adnexal adhesions, distal tubal 40. Claman P, Berger MJ. Phenotypic differences in upper genital tract abnormalities
occlusion, tubal occlusion secondary to tubal ligation, tubal pregnancies, Müllerian and reproductive history in dizygotic twins exposed to diethylstilbestrol in utero.
anomalies and intrauterine adhesions. Fertil Steril 1988; 49: 944–955. A case report. J Reprod Med 1990; 35: 431–433.
8. Chan YY, Jayaprakasan K, Zamora J, Thornton JG, Raine-Fenning N, 41. van Gils AP, Tham RT, Falke TH, Peters AA. Abnormalities of the uterus
Coomarasamy A. The prevalence of congenital uterine anomalies in unselected and cervix after diethylstilbestrol exposure: correlation of findings on MR and
and high-risk populations: a systematic review. Hum Reprod Update 2011; 17: hysterosalpingography. AJR Am J Roentgenol 1989; 153: 1235–1238.
761–771. 42. Kahn-Nathan J. Diethylstilbestrol exposition in utero. Effects on female genital
9. Ludwin A, Coelho Neto MA, Ludwin I, Nastri CO, Costa W, Acien M, Alcazar JL, tract. Contracept Fertil Sex 1989; 17: 243–245.
Benacerraf B, Condous G, DeCherney A, De Wilde RL, Diamond MP, Emanuel MH, 43. Hammond MG. Müllerian defects associated with repetitive spontaneous abortions.
Guerriero S, Hurd W, Levine D, Lindheim S, Pellicer A, Petraglia F, Saridogan E, Semin Reprod Med 1989; 7: 103–110.
Martins WP. Congenital Uterine Malformation by Experts (CUME): diagnostic 44. Senekjian EK, Potkul RK, Frey K, Herbst AL. Infertility among daughters either
criteria for T-shaped uterus. Ultrasound Obstet Gynecol 2020; 55: 815–829. exposed or not exposed to diethylstilbestrol. Am J Obstet Gynecol 1988; 158:
10. Lucas NP, Macaskill P, Irwig L, Bogduk N. The development of a quality appraisal 493–498.
tool for studies of diagnostic reliability (QAREL). J Clin Epidemiol 2010; 63: 45. Cunha GR, Taguchi O, Namikawa R, Nishizuka Y, Robboy SJ. Teratogenic effects
854–861. of clomiphene, tamoxifen, and diethylstilbestrol on the developing human female
11. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang genital tract. Hum Pathol 1987; 18: 1132–1143.
MM, Sterne JA, Bossuyt PM, Group Q-. QUADAS-2: a revised tool for the quality 46. Menczer J, Dulitzky M, Ben-Baruch G, Modan M. Primary infertility in women
assessment of diagnostic accuracy studies. Ann Intern Med 2011; 155: 529–536. exposed to diethylstilboestrol in utero. Br J Obstet Gynaecol 1986; 93: 503–507.
12. Balshem H, Helfand M, Schunemann HJ, Oxman AD, Kunz R, Brozek J, Vist GE, 47. Kaufman RH, Adam E, Noller K, Irwin JF, Gray M. Upper genital tract changes
Falck-Ytter Y, Meerpohl J, Norris S, Guyatt GH. GRADE guidelines: 3. Rating the and infertility in diethylstilbestrol-exposed women. Am J Obstet Gynecol 1986;
quality of evidence. J Clin Epidemiol 2011; 64: 401–406. 154: 1312–1318.
13. Ahmadi F, Haghighi H. Detection of Congenital Müllerian Anomalies by Real-time 48. Barber HR. An update on DES in the field of reproduction. Int J Fertil 1986; 31:
3D Sonography. J Reprod Infertil 2012; 13: 65–66. 130–144.
14. Mor E, Landay M, Paulson RJ. Endometrial receptivity is preserved in 49. Tchobroutsky C. [Reproduction in women exposed in utero to diethylstilbestrol
Diethylstilbestrol-associated and other Müllerian anomalies: evidence from tubal (DES)]. Sem Hop 1984; 60: 1743–1744.
embryo transfer. J Assist Reprod Genet 2009; 26: 65–68. 50. Nunley WC, Jr., Pope TL, Jr., Bateman BG. Upper reproductive tract radiographic
15. Poncelet C, Aissaoui F. [Uterine malformations and reproduction]. Gynecol Obstet findings in DES-exposed female offspring. AJR Am J Roentgenol 1984; 142:
Fertil 2007; 35: 821–825. 337–339.
16. Epelboin S. [Diethylstilbestrol exposure in utero. Polemics about metroplasty. The 51. Muasher SJ, Acosta AA, Garcia JE, Rosenwaks Z, Jones HW, Jr. Wedge metroplasty
cons]. Gynecol Obstet Fertil 2007; 35: 832–841. for the septate uterus: an update. Fertil Steril 1984; 42: 515–519.
17. Aubriot FX, Chapron C. [Diethylstilbestrol exposure in utero. Polemics about 52. Kaufman RH, Noller K, Adam E, Irwin J, Gray M, Jefferies JA, Hilton J. Upper
metroplasty. The pros]. Gynecol Obstet Fertil 2007; 35: 826–831. genital tract abnormalities and pregnancy outcome in diethylstilbestrol-exposed
18. Garbin O, Ziane A, Castaigne V, Rongieres C. [Do hysteroscopic metroplasties progeny. Am J Obstet Gynecol 1984; 148: 973–984.
really improve really reproductive outcome?]. Gynecol Obstet Fertil 2006; 34: 53. Huikeshoven FJ, Wallenburg HC. [DES, more than an oncological problem]. Ned
813–818. Tijdschr Geneeskd 1984; 128: 1553–1556.
54. Drapier E. [Fertility disorders attributable to the use of diethylstilbestrol during
19. Devi Wold AS, Pham N, Arici A. Anatomic factors in recurrent pregnancy loss.
intrauterine life]. Rev Fr Gynecol Obstet 1984; 79: 297–300, 303–295.
Semin Reprod Med 2006; 24: 25–32.
55. Buttram VC Jr. Müllerian anomalies and their management. Fertil Steril 1983; 40:
20. Porcu G, Heckenroth H. Malformations utérines et infertilité. EMC -
159–163.
Gynécologie-Obstétrique 2005; 2: 185–197.
56. Belaisch J. [Exposure to diethylstilbestrol during intrauterine life. Signs that should
21. Troiano RN, McCarthy SM. Müllerian duct anomalies: imaging and clinical issues.
suggest this. Therapeutic implications]. J Gynecol Obstet Biol Reprod (Paris) 1983;
Radiology 2004; 233: 19–34.
12: 481–488.
22. Lin PC. Reproductive outcomes in women with uterine anomalies. J Womens
57. Stillman RJ. In-utero exposure to diethylstilbestrol: adverse effects on the
Health (Larchmt) 2004; 13: 33–39.
reproductive tract and reproductive performance and male and female offspring.
23. Aubriot FX, Audebert A, Blanc B, Dechaud H, Elpelboin S, Fernandez H,
Am J Obstet Gynecol 1982; 142: 905–921.
Garbin O, Hamou J, Landowski P, Paniel BJ, Tournaire M, Salle B, Mergui
58. Mansi ML, Goldfarb AF. An analysis of pregnancy salvage in a selective DES
JL, Agence nationale d’accreditation et d’evaluation en santé. [Evaluation of
population. Infertility 1982; 5: 1–13.
enlargement uteroplasty in the treatment of uterine anomalies following exposure
59. Kinch RA. Diethylstilbestrol in pregnancy: an update. Can Med Assoc J 1982; 127:
to diethylstillbestrol (May 2003)]. Gynecol Obstet Fertil 2004; 32: 261–264.
812–813.
24. Troiano RN. Magnetic resonance imaging of Müllerian duct anomalies of the
60. Kaufman RH. Structural changes of the genital tract associated with in-utero
uterus. Top Magn Reson Imaging 2003; 14: 269–279.
exposure to diethylstilbestrol. Obstet Gynecol Annu 1982; 11: 187–202.
25. Siewert B, Hochman M, Levine D. Problems and Pitfalls in MR Evaluation of
61. Caby J. Uterine anomalies in young women exposed to diethylstilbestrol in utero.
Uterine Anomalies. J Womens Imaging 2002; 4: 100–107.
Hysterographic findings in three cases. Gynecologie 1982; 33: 515–521.
26. Aubriot FX, Hamou J, Dubuisson JB, Frydman R, Fernandez H. [Hysteroplasty for
62. Sandberg EC, Riffle NL, Higdon JV, Getman CE. Pregnancy outcome in women
enlargement: apropos of the results]. Gynecol Obstet Fertil 2001; 29: 888–893. exposed to diethylstilbestrol in utero. Am J Obstet Gynecol 1981; 140: 194–205.
27. Goldberg JM, Falcone T. Effect of diethylstilbestrol on reproductive function. Fertil 63. Ben-Baruch G, Menczer J, Mashiach S, Serr DM. Uterine anomalies in
Steril 1999; 72: 1–7. diethylstilbestrol-exposed women with fertility disorders. Acta Obstet Gynecol
28. Laurent S, Lanoue M, Lecomte C, Bourgeois L, Lecomte P. [Female fertility Scand 1981; 60: 395–397.
prognosis and diethylstilbestrol. Personal data and review of the literature]. 64. Viscomi GN, Gonzalez R, Taylor KJ. Ultrasound detection of uterine abnormalities
J Gynecol Obstet Biol Reprod (Paris) 1998; 27: 277–284. after diethylstilbestrol (DES) exposure. Radiology 1980; 136: 733–735.
29. Garbin O, Ohl J, Bettahar-Lebugle K, Domine S, Dellenbach P. [Transcervical 65. Pillsbury SG, Jr. Reproductive significance of changes in the endometrial cavity
hysteroplasty: indications, techniques and results. 125 cases]. Contracept Fertil Sex associated with exposure in utero to diethylstilbestrol. Am J Obstet Gynecol 1980;
1997; 25: 843-851. 137: 178–182.
30. Raga F, Bauset C, Remohi J, Bonilla-Musoles F, Simon C, Pellicer A. Reproductive 66. Kaufman RH, Adam E, Binder GL, Gerthoffer E. Upper genital tract changes and
impact of congenital Müllerian anomalies. Hum Reprod 1997; 12: 2277–2281. pregnancy outcome in offspring exposed in-utero to diethylstilbestrol. Am J Obstet
31. Noyes N, Liu HC, Sultan K, Rosenwaks Z. Endometrial pattern in Gynecol 1980; 137: 299–308.
diethylstilboestrol-exposed women undergoing in-vitro fertilization may be the most 67. Goldstein DP. The significance of cervical and uterine abnormalities in DES-exposed
significant predictor of pregnancy outcome. Hum Reprod 1996; 11: 2719–2723. females. J Adolesc Health Care 1980; 1: 86.
32. Lang JM, Lieberman E, Cohen A. A comparison of risk factors for preterm labor 68. Barnes AB, Colton T, Gundersen J, Noller KL, Tilley BC, Strama T, Townsend DE,
and term small-for-gestational-age birth. Epidemiology 1996; 7: 369–376. Hatab P, O’Brien PC. Fertility and outcome of pregnancy in women exposed in
33. Kipersztok S, Javitt M, Hill MC, Stillman RJ. Comparison of magnetic resonance utero to diethylstilbestrol. N Engl J Med 1980; 302: 609–613.
imaging and transvaginal ultrasonography with hysterosalpingography in the 69. Siegler AM, Wang CF, Friberg J. Fertility of the diethylstilbestrol-exposed offspring.
evaluation of women exposed to diethylstilbestrol. J Reprod Med 1996; 41: Fertil Steril 1979; 31: 601–607.
347–351. 70. Rennell CL. T-shaped uterus in diethylstilbestrol (DES) exposure. AJR Am
34. Minh HN, Smadja A, Gasnault JP. [From embryogenesis to pathogenesis of effects J Roentgenol 1979; 132: 979–980.
of diethylstilbestrol on the female genital tract]. Presse Med 1993; 22: 1052–1057. 71. Haney AF, Hammond CB, Soules MR, Creasman WT. Diethylstilbestrol-induced
35. Milhan D. DES exposure: implications for childbearing. Int J Childbirth Educ 1992; upper genital tract abnormalities. Fertil Steril 1979; 31: 142–146.
7: 21–28. 72. Kaufman RH, Adam E. Genital tract anomalies associated with in-utero exposure
36. Balasch J, Coll O, Jove I, Moreno V, Mulet J, Vanrell JA. Diethylstilbestrol-induced to diethylstilbestrol. Isr J Med Sci 1978; 14: 353–362.
Müllerian abnormalities, septate uterus, genital tuberculosis and twin pregnancy 73. Goldstein DP. Incompetent cervix in offspring exposed to diethylstilbestrol in utero.
with term delivery after in-vitro fertilization. Hum Reprod 1991; 6: 690–693. Obstet Gynecol 1978; 52: 73S–75S.
37. Sherer DM, Allen TA, Woods Jr JR. Endovaginal sonographic associated features 74. Garbin O, Dellenbach P. [Hysteroscopic metroplasty for uterine enlargement: a
of a T-shaped uterus due to in utero exposure to diethylstilbestrol (DES). J Diagn treatment for diethylbestrol-exposed and hypoplastic uteri]. J Gynecol Obstet Biol
Med Sonogr 1990; 6: 318–320. Reprod (Paris) 1996; 25: 41–46.
38. Lev-Toaff AS, Toaff ME, Friedman AC. Endovaginal sonographic appearance of a 75. Ansbacher R. Uterine anomalies and future pregnancies. Clin Perinatol 1983; 10:
DES uterus. J Ultrasound Med 1990; 9: 661–664. 295–304.
39. Karande VC, Lester RG, Muasher SJ, Jones DL, Acosta AA, Jones HW, Jr. Are 76. Bhagavath B, Ellie G, Griffiths KM, Winter T, Alur-Gupta S, Richardson C,
implantation and pregnancy outcome impaired in diethylstilbestrol-exposed women Lindheim SR. Uterine Malformations: An Update of Diagnosis, Management, and
after in vitro fertilization and embryo transfer? Fertil Steril 1990; 54: 287–291. Outcomes. Obstet Gynecol Surv 2017; 72: 377–392.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
376 Coelho Neto et al.

77. Heusinger K, Oppelt PG. Konnatale Fehlbildungen des weiblichen Genitaltrakts. 112. Agrawal G, Riherd JM, Busse RF, Hinshaw JL, Sadowski EA. Evaluation of uterine
Der Gynäkologe 2016; 49: 79–86. anomalies: 3D FRFSE cube versus standard 2D FRFSE. AJR Am J Roentgenol 2009;
78. Saravelos SH, Li TC. Intra- and inter-observer variability of uterine measurements 193: W558–562.
with three-dimensional ultrasound and implications for clinical practice. Reprod 113. Barranger E, Gervaise A, Doumerc S, Fernandez H. Reproductive performance after
Biomed Online 2015; 31: 557–564. hysteroscopic metroplasty in the hypoplastic uterus: a study of 29 cases. BJOG
79. Olpin JD, Heilbrun M. Imaging of Müllerian duct anomalies. Top Magn Reson 2002; 109: 1331–1334.
Imaging 2010; 21: 225–235. 114. Katz Z, Ben-Arie A, Lurie S, Manor M, Insler V. Beneficial effect of hysteroscopic
80. Raga F, Bonilla-Musoles F, Blanes J, Bailao LA, Osborne NG. Uterine anomalies metroplasty on the reproductive outcome in a ‘T-shaped’ uterus. Gynecol Obstet
with three-dimensional ultrasound (Müllerian duct malformations). Assist Reprod Invest 1996; 41: 41–43.
Rev 1996; 6: 126–141. 115. Golan A, Langer R, Neuman M, Wexler S, Segev E, David MP. Obstetric
81. Blanc B. Practical guidelines for paraclinical investigation ranking of unterovaginal outcome in women with congenital uterine malformations. J Reprod Med 1992; 37:
malformations. Gynecologie 1990; 41: 236–238. 233–236.
82. Rudigoz RC, Gaucherand P, Dargent D. [The obstetric outlook for malformations 116. Bermejo C, Martinez-Ten P, Ruiz-Lopez L, Estevez M, Gil MM. Classification
of the uterus]. J Gynecol Obstet Biol Reprod (Paris) 1989; 18: 185–191. of Uterine Anomalies by 3-Dimensional Ultrasonography Using ESHRE/ESGE
83. Lecoutour X, Bourgeot P, Segard C. [Obstetric outcome of the malformed uterus. Criteria: Interobserver Variability. Reprod Sci 2018; 25: 740–747.
Study of 155 pregnancies]. Re Fr Gynecol Obstet 1986; 81: 357–362. 117. Exacoustos C, Valeria R, Cobuzzi I, Zizolfi B, Di Spiezio A, Zupi E. 3D ultrasound
84. Leroy B, Bessis R, Nisand I, Jeny R, Jaudel S, Eboue F. [The value of ultrasonography to diagnose uterine anomalies. Hum Reprod 2016; 31: i60.
in the diagnosis of uterine malformations]. J Gynecol Obstet Biol Reprod (Paris) 118. Meier R, De Bruin C, Mestdagh G, Dhont N, Ombelet W, Campo R. Abstracts of
1984; 13: 250–253. the 23rd Annual congress of the European Society European Society (ESGE), 24–26
85. Blum M. Obstetric complications due to malformations of the uterus. Rev Fr September 2014, Square, Brussels. Gynecol Surg 2014; 11: 1–358.
Gynecol Obstet 1984; 79: 461–462. 119. Adriaensen P, Mestdagh G, Dhont N, Ombelet W, De Bruyn C, Rudi C.
86. de la Pena Regidor P, de Carballo P. [Approach to repeated pregnancy of Reproductive and obstetric outcomes of hysteroscopic correction of a dysmorphic
women with uterine malformation (author’s transl)]. Zentralbl Gynakol 1979; (U1). Gynecol Surg 2016; 13 (Suppl 1): 453.
101: 857–858. 120. Li Y, Phelps A, Zapala MA, MacKenzie JD, MacKenzie TC, Courtier J. Magnetic
87. Rauthe G, Vahrson H. [Infantile and hypoplastic uterus: a contribution to overcome resonance imaging of Müllerian duct anomalies in children. Pediatr Radiol 2016;
the confusion of terms (author’s transl)]. Geburtshilfe Frauenheilkd 1975; 35: 46: 796–805.
877–880. 121. Exacoustos C, Cobuzzi I, Romeo V. 2D Ultrasound (2D US) and Sonohysterography
88. Erbsloeh J. Normal shapes, variations and malformations in hysterosalpingography. (SHG) for the Diagnosis of Female Genital Anomalies. In Female Genital Tract
Radiologe 1975; 15: 2–10. Congenital Malformations. Springer–Verlag Ltd: London, UK, 2015; 63–78.
89. Kopaleischwili BI, Gotziridse OA, Friedman MM, Gogitschaischwili LG, Nikulin 122. Ahmadi F, Zafarani F, Shahrzad GS. Hysterosalpingographic Appearances of
PP. [New method for inducing functional hypertrophy of a hypoplastic uterus Female Genital Tract Tuberculosis: Part II: Uterus. Int J Fertil Steril 2014; 8:
(clinical-experimental study)]. Zentralbl Gynakol 1973; 95: 177–181. 13–20.
90. Empereur-Buisson R. Repeated abortions due to uterine anomaly. J Sci Med Lille 123. Uyar E, Usal D, Selam B, Cincik M, Bagis T. IVF outcomes after hysteroscopic
1971; 89: 317–321. metroplasty in patients with T- shaped uterus. Fertil Res Pract 2019; 5: 15.
124. Neal SA, Morin SJ, Werner MD, Gueye NA, Pirtea P, Scott RT, Jr., Goodman
91. Wery P. [Essential symptomatology of major types of uterine malformation]. Rev
LR. Three-dimensional ultrasound diagnosis of T-shaped uterus is associated with
Med Liege 1970; 25: 760–763.
adverse pregnancy outcomes after embryo transfer. Reprod Biomed Online 2019;
92. Vaesen F. [Treatment of uterine malformation]. Rev Med Liege 1970; 25: 764–766.
39: 777–783.
93. Poizat G. [Obstetrical complications of uterine malformations]. Rev Med Liege
125. Di Spiezio Sardo A, Campo R, Zizolfi B, Santangelo F, Meier Furst R, Di Cesare C,
1970; 25: 763–764.
Bettocchi S, Vitagliano A, Ombelet W. Long-Term Reproductive Outcomes after
94. Musset R, Muller P, Netter A, Solal R. [Necessity for a global classification of uterine
Hysteroscopic Treatment of Dysmorphic Uteri in Women with Reproductive
malformations. Associated urinary malformations. Interest of certain peculiarities
Failure: An European Multicenter Study. J Minim Invasive Gynecol 2020; 27:
in the light of 141 cases]. Gynecol Obstet (Paris) 1967; 66: 145–166.
755–762.
95. Chosson J. Attempt at embryologic classification of malformations of Müllerian
126. Boza A, Akin OD, Oguz SY, Misirlioglu S, Urman B. Surgical correction of T-shaped
origin of the female genital system. Rev Fr Gynecol Obstet 1967; 62: 695–702.
uteri in women with reproductive failure: Long term anatomical and reproductive
96. Serment H, Felce A, Hartung N, Tanguy Y. [Apropos of an unusual utero-vaginal
outcomes. J Gynecol Obstet Hum Reprod 2019; 48: 39–44.
malformation]. Bull Fed Soc Gynecol Obstet Lang Fr 1966; 18: 284–285.
127. Alonso Pacheco L, Lagana AS, Garzon S, Perez Garrido A, Flores Gornes A,
97. Rouchy R. [Repeated abortions & uterine malformations; Strassmann’s operation].
Ghezzi F. Hysteroscopic outpatient metroplasty for T-shaped uterus in women with
Bull Fed Soc Gynecol Obstet Lang Fr 1957; 9: 229–231.
reproductive failure: Results from a large prospective cohort study. Eur J Obstet
98. Louros N, Kaskarelis D. [Relations between uterine malformation, sterility and
Gynecol Reprod Biol 2019; 243: 173–178.
abortion]. Gynécol Prat 1957; 8: 299–306.
128. Haydardedeoglu B, Dogan Durdag G, Simsek S, Caglar Aytac P, Cok T, Bulgan
99. Hervet E. [Uterine malformation: new report of a reparative operation]. Bull Fed
Kilicdag E. Reproductive outcomes of office hysteroscopic metroplasty in women
Soc Gynecol Obstet Lang Fr 1957; 9: 504–510.
with unexplained infertility with dysmorphic uterus. Turk J Obstet Gynecol 2018;
100. Ravina J, Musset R, Michel H. [Hypertrophic elongation of the uterine cervix; three
15: 135–140.
observations on congenital hypertrophic elongation]. Bull Fed Soc Gynecol Obstet 129. Ducellier-Azzola G, Lecointre L, Hummel M, Pontvianne M, Garbin O.
Lang Fr 1956; 8: 59–63. Hysteroscopic enlargement metroplasty for T-shaped uterus: 24 years’ experience
101. Caderas De Kerleau J, Thuile F. [Infantile uterus and obstetrical consequences]. at the Strasbourg Medico-Surgical and Obstetrical Centre (CMCO). Eur J Obstet
Maroc Med 1952; 31: 918–920. Gynecol Reprod Biol 2018; 226: 30–34.
102. Kougioumtsidou A, Mikos T, Grimbizis GF, Karavida A, Theodoridis TD, 130. Soekoer Y, Seval MM, Ozmen B, Sonmezer M, Berker B, Atabekoglu CS. The
Sotiriadis A, Tarlatzis BC, Athanasiadis AP. Three-dimensional ultrasound in reproductive outcome after hysteroscopicmetroplasty in patients with deep uterine
the diagnosis and the classification of congenital uterine anomalies using the septum and T-shaped uterus. Fertil Steril 2016; 106 (Suppl 1): 453.
ESHRE/ESGE classification: a diagnostic accuracy study. Arch Gynecol Obstet 131. Puente JM, Fabris A, Patel J, Patel A, Cerrillo M, Requena A, Garcia-Velasco JA.
2019; 299: 779–789. Adenomyosis in infertile women: prevalence and the role of 3D ultrasound as a
103. Alonso Pacheco L, Lagana AS, Ghezzi F, Haimovich S, Azumendi Gomez P, marker of severity of the disease. Reprod Biol Endocrinol 2016; 14: 60.
Carugno J. Subtypes of T-shaped uterus. Fertil Steril 2019; 112: 399–400. 132. Exacoustos C, Romeo V, Zizolfi B, Cobuzzi I, Di Spiezio A, Zupi E. Dysmorphic
104. Thellier E, Levaillant JM, Pourcelot AG, Houllier M, Fernandez H, Capmas P. Are Uterine Congenital Anomalies: A New Lateral Angle and a Cavity Width Ratio on
3D ultrasound and office hysteroscopy useful for the assessment of uterine cavity 3D Ultrasound Coronal Section to Define Uterine Morphology. J Minim Invasive
after late foetal loss? J Gynecol Obstet Hum Reprod 2018; 47: 183–186. Gynecol 2015; 22: S73.
105. Ples L, Alexandrescu C, Ionescu CA, Arvatescu CA, Vladareanu S, Moga MA. 133. Di Spiezio Sardo A, Florio P, Nazzaro G, Spinelli M, Paladini D, Di Carlo C,
Three-dimensional scan of the uterine cavity of infertile women before assisted Nappi C. Hysteroscopic outpatient metroplasty to expand dysmorphic uteri
reproductive technology use. Medicine (Baltimore) 2018; 97: e12764. (HOME-DU technique): a pilot study. Reprod Biomed Online 2015; 30: 166–174.
106. Ludwin A, Ludwin I. Comparison of the ESHRE/ESGE and ASRM classifications of 134. Fox NS, Roman AS, Stern EM, Gerber RS, Saltzman DH, Rebarber A. Type
Müllerian duct anomalies in everyday practice. Hum Reprod 2015; 30: 569–580. of congenital uterine anomaly and adverse pregnancy outcomes. J Matern Fetal
107. Imboden S, Muller M, Raio L, Mueller MD, Tutschek B. Clinical significance of Neonatal Med 2014; 27: 949–953.
3D ultrasound compared to MRI in uterine malformations. Ultraschall Med 2014; 135. Mounir M. T shaped endometrial cavity and infertility. Gynecol Surg 2012; 9
35: 440–444. (Suppl 1): S1–37.
108. Jaslow CR, Kutteh WH. Effect of prior birth and miscarriage frequency on the 136. Giacomucci E, Bellavia E, Sandri F, Farina A, Scagliarini G. Term delivery rate
prevalence of acquired and congenital uterine anomalies in women with recurrent after hysteroscopic metroplasty in patients with recurrent spontaneous abortion and
miscarriage: a cross-sectional study. Fertil Steril 2013; 99: 1916–1922.e1. T-shaped, arcuate and septate uterus. Gynecol Obstet Invest 2011; 71: 183–188.
109. Fox N, Roman A, Saltzman D, Klauser C, Rebarber A. 517: Twin pregnancy in 137. Şükür YE, Yakıştıran B, Özmen B, Sönmezer M, Berker B, Atabekoğlu C.
patients with a uterine malformation. Am J Obstet Gynecol 2013; 208: S222. Hysteroscopic Corrections for Complete Septate and T-Shaped Uteri Have Similar
110. Jayaprakasan K, Chan YY, Sur S, Deb S, Clewes JS, Raine-Fenning NJ. Prevalence Surgical and Reproductive Outcome. Reprod Sci 2018; 1649–1654.
of uterine anomalies and their impact on early pregnancy in women conceiving after 138. De Bruyn C, Greet M, Willem O, Rudi C. The impact of hysteroscopic surgery for
assisted reproduction treatment. Ultrasound Obstet Gynecol 2011; 37: 727–732. dysmorphic uterus on reproductive and obstetric outcomes: Pilot study. Gynecol
111. Bermejo C, Martinez Ten P, Cantarero R, Diaz D, Perez Pedregosa J, Barron E, Surg 2013; 10: S101–S102.
Labrador E, Ruiz Lopez L. Three-dimensional ultrasound in the diagnosis of 139. Ferro J, Lizán C, Ayllón Y, Garrido N, Remohı́ J. Pregnancy results after
Müllerian duct anomalies and concordance with magnetic resonance imaging. hysteroscopical correction of ‘‘T-shape uterus’’. Hum Reprod 2009; 24 (suppl 1):
Ultrasound Obstet Gynecol 2010; 35: 593–601. i232–233.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.
14690705, 2021, 3, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.23108 by Cochrane Mexico, Wiley Online Library on [16/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
T-shaped uterus 377

140. Ferro J, Labarta E, Sanz C, Montoya P, Remohi J. Reproductive outcomes WA, Torrenga B, Torrance HL, Verhoeve HR, Huirne JAF, Hoek A, Nieboer TE,
after hysteroscopic metroplasty for women with dysmorphic uterus and recurrent van Rooij IAJ, Clark TJ, Robinson L, Stephenson MD, Mol BWJ, van der Veen F,
implantation failure. Facts Views Vis Obgyn 2018; 10: 63–68. van Wely M, Goddijn M. Septum resection in women with a septate uterus: a
141. National Institute for Health and Care Excellence (2013). Fertility problems: cohort study. Hum Reprod 2020; 35: 1578–1588.
assessment and treatment. [Clinical guideline CG156]. https://www.nice.org.uk/ 152. Rikken JFW, Kowalik CR, Emanuel MH, Bongers MY, Spinder T, de Kruif JH,
guidance/cg156 Bloemenkamp KWM, Jansen FW, Veersema S, Mulders A, Thurkow AL, Hald K,
142. Bender Atik R, Christiansen OB, Elson J, Kolte AM, Lewis S, Middeldorp S, Mohazzab A, Khalaf Y, Clark TJ, Farrugia M, van Vliet HA, Stephenson MS, van
Nelen W, Peramo B, Quenby S, Vermeulen N, Goddijn M. ESHRE guideline: der Veen F, van Wely M, Mol BWJ, Goddijn M. The randomised uterine septum
recurrent pregnancy loss. Hum Reprod Open 2018; 2018: hoy004. transsection trial (TRUST): design and protocol. BMC Womens Health 2018; 18:
143. Somigliana E, Vigano P, Busnelli A, Paffoni A, Vegetti W, Vercellini P. Repeated 163.
implantation failure at the crossroad between statistics, clinics and over-diagnosis. 153. Rikken J, Kowalik C, Emanuel MH, Bongers M, T. S, Jansen FW, Mulders A,
Reprod Biomed Online 2018; 36: 32–38. Padmehr R, Clark J, Van Vliet H, Stephenson M, Van Veen F, Mol BW,
144. Mol F, van Mello NM, Strandell A, Strandell K, Jurkovic D, Ross J, Barnhart KT, Van Wely M, Goddijn M. Septum resection versus expectant management in
Yalcinkaya TM, Verhoeve HR, Graziosi GCM, Koks CAM, Klinte I, Hogstrom L, women with a septate uterus: a randomised controlled trial (NTR 1676). Hum
Janssen I, Kragt H, Hoek A, Trimbos-Kemper TCM, Broekmans FJM, Willemsen Reprod 2020; 35 (Suppl): i23. https://www.eshre.eu/-/media/sitecore-files/Annual-
WNP, Ankum WM, Mol BW, van Wely M, van der Veen F, Hajenius PJ, European meeting/Virtual2020/HUMREP35suppl1-ESHRE-2020-cropped.pdf?la=en&
Surgery in Ectopic Pregnancy study g. Salpingotomy versus salpingectomy in hash=805DF7F9AD78091721117721D1ABE5F4E9A28AC3
women with tubal pregnancy (ESEP study): an open-label, multicentre, randomised 154. Sood A, Akhtar M. T-shaped Uterus in the 21(st) Century (Post DES era) - We
controlled trial. Lancet 2014; 383: 1483–1489. Need to Know More! J Hum Reprod Sci 2019; 12: 283–286.
145. Knez J, Saridogan E, Van Den Bosch T, Mavrelos D, Ambler G, Jurkovic D. 155. Garbin O, Ohl J, Bettahar-Lebugle K, Dellenbach P. Hysteroscopic metroplasty
ESHRE/ESGE female genital tract anomalies classification system-the potential in diethylstilboestrol-exposed and hypoplastic uterus: a report on 24 cases. Hum
impact of discarding arcuate uterus on clinical practice. Hum Reprod 2018; 33: Reprod 1998; 13: 2751–2755.
600–606. 156. Nagel TC, Malo JW. Hysteroscopic metroplasty in the diethylstilbestrol-exposed
146. Ludwin A, Martins WP, Nastri CO, Ludwin I, Coelho Neto MA, Leitao VM, uterus and similar nonfusion anomalies: effects on subsequent reproductive
Acien M, Alcazar JL, Benacerraf B, Condous G, De Wilde RL, Emanuel MH, performance: a preliminary report. Fertil Steril 1993; 59: 502–506.
Gibbons W, Guerriero S, Hurd WW, Levine D, Lindheim S, Pellicer A, Petraglia F, 157. Dzotsenidze TN, Davarashvili DI, Nikolaishvili TG, Peradze DG, Datunashvili
Saridogan E. Congenital Uterine Malformation by Experts (CUME): better criteria ED. [Contrast sono hysterosalpingography in the study of endometrial abnor-
for distinguishing between normal/arcuate and septate uterus? Ultrasound Obstet malities and tubal patency in infertile patients]. Georgian Med News 2006;
Gynecol 2018; 51: 101–109. 61–63.
147. Prior M, Richardson A, Asif S, Polanski L, Parris-Larkin M, Chandler J, Fogg L, 158. De Franciscis P, Riemma G, Schiattarella A, Cobellis L, Colacurci N, Vitale SG,
Jassal P, Thornton JG, Raine-Fenning NJ. Outcome of assisted reproduction Cianci A, Lohmeyer FM, La Verde M. Impact of Hysteroscopic Metroplasty on
in women with congenital uterine anomalies: a prospective observational study. Reproductive Outcomes of Women with a Dysmorphic Uterus and Recurrent
Ultrasound Obstet Gynecol 2018; 51: 110–117. Miscarriages: A Systematic Review and Meta-Analysis. J Gynecol Obstet Hum
148. Checa MA, Bellver J, Bosch E, Espinos JJ, Fabregues F, Fontes J, Garcia-Velasco J, Reprod 2020; 49: 101763.
Requena A. Hysteroscopic septum resection and reproductive medicine: A SWOT 159. Ford HB, Schust DJ. Recurrent pregnancy loss: etiology, diagnosis, and therapy.
analysis. Reprod Biomed Online 2018; 37: 709–715. Rev Obstet Gynecol 2009; 2: 76–83.
149. Ludwin A. Septum resection does not improve reproductive outcomes: truly? Hum 160. Zeitlin J, Szamotulska K, Drewniak N, Mohangoo AD, Chalmers J, Sakkeus L,
Reprod 2020; 35: 1495–1498. Irgens L, Gatt M, Gissler M, Blondel B, Euro-Peristat Preterm Study G. Preterm
150. Rikken JF, Kowalik CR, Emanuel MH, Mol BW, Van der Veen F, van Wely M, birth time trends in Europe: a study of 19 countries. BJOG 2013; 120:
Goddijn M. Septum resection for women of reproductive age with a septate uterus. 1356–1365.
Cochrane Database Syst Rev 2017; 1: CD008576. 161. Ludwin A, Martins WP, Ludwin I. Uterine cavity imaging, volume estimation
151. Rikken JFW, Verhorstert KWJ, Emanuel MH, Bongers MY, Spinder T, and quantification of degree of deformity using automatic volume calculation:
Kuchenbecker W, Jansen FW, van der Steeg JW, Janssen CAH, Kapiteijn K, Schols description of technique. Ultrasound Obstet Gynecol 2017; 50: 138–140.

SUPPORTING INFORMATION ON THE INTERNET

The following supporting information may be found in the online version of this article:
Table S1 Diagnostic methods and criteria for T-shaped uterus used by included studies
Table S2 Studies assessing effect of interventions for T-shaped uterus
Table S3 Quality of included observational studies according to Newcastle–Ottawa Scale
Table S4 Judgement of diagnostic accuracy studies according to QUADAS-2
Table S5 Judgement of reliability/agreement studies according to quality appraisal of diagnostic reliability tool

A video abstract of this article is available online.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology. Ultrasound Obstet Gynecol 2021; 57: 366–377.

You might also like