A comparative study of the morphology of congenitaluterine anomalies in women with and without a history ofrecurrent ®rst trimester miscarriage

R.Salim1, L.Regan2, B.Woelfer1, M.Backos2 and D.Jurkovic1,3

1Early Pregnancy and Gynaecology Assessment Unit, King's College Hospital, Denmark Hill, London SE5 8RX and 2Recurrent

Miscarriage Clinic, St Mary's Hospital, Paddington, London W2 1NY, UK

3To whom correspondence should be addressed. E-mail: davor.jurkovic@kcl.ac.uk

BACKGROUND: The true impact of congenital uterine anomalies on reproductive outcomes is unknown. The aim

of this study was to examine differences in the morphology of uterine anomalies found in women with and without a

history of recurrent miscarriage. METHODS: A total of 509 women with a history of unexplained recurrent miscar-

riage and 1976 low risk women were examined for the presence of congenital uterine anomalies by three-dimen-

sional ultrasound. The anomalies were classi®ed according to the American Fertility Society classi®cation. In

addition, the size of fundal distortion (F) and the length of the remaining uterine cavity (C) were measured to calcu-

late a distortion ratio (F/F+C). The ®ndings were compared with the measurements obtained in low risk women

with an incidental ®nding of uterine anomaly. RESULTS: In all, 121 anomalies were detected in the recurrent mis-

carriage group and 105 in low risk women. There was no signi®cant difference in relative frequency of various

anomalies or depth of fundal distortion between the two groups. However, with both arcuate and subseptate uteri,

the length of remaining uterine cavity was signi®cantly shorter (P < 0.01) and the distortion ratio was signi®cantly

higher (P < 0.01) in the recurrent miscarriage group. CONCLUSION: The distortion of uterine anatomy is more

severe in congenital anomalies, which are found in women with a history of recurrent ®rst trimester miscarriage.

Key words: congenital uterine anomalies/recurrent miscarriage/three-dimensional ultrasound

Introduction

Congenital uterine anomalies have been implicated as a cause

of adverse pregnancy outcomes (Acien, 1993; Raga et al.,

1997). Women with a history of infertility or miscarriage are,

therefore, often offered surgery in an attempt to restore uterine

anatomy and improve the prognosis for future pregnancies

(Pellicer, 1997). The reported prevalence of congenital uterine

anomalies in women with recurrent pregnancy loss varies

between 6 and 38% (Makino et al., 1992a; Clifford et al., 1994;

Acien, 1996). This wide variation is likely to re¯ect differences

in the diagnostic criteria and techniques used for diagnosis.

Although most authors subscribe to the American Fertility

Society Classi®cation of Uterine anomalies (American Fertility

Society, 1988), the ®nal diagnosis is based on the subjective

impression of the clinician performing the test. So far, no

published study has investigated the reproducibility of different

tests used in routine clinical practice for the diagnosis of

uterine anomalies.

Most studies of uterine anomalies have been performed on

women with either a history of infertility or recurrent

pregnancy loss. However, little is known about the prevalence

and reproductive implications of uterine anomalies in the

general population. In the absence of such data, it is dif®cult to

be certain whether uterine anomalies are indeed a major cause

of recurrent pregnancy loss. We have recently reported on the

prevalence and morphological characteristics of uterine anom-

alies detected on screening low risk women using three-

dimensional ultrasound (Jurkovic et al., 1997; Woelfer et al.,

2001). In this study, we have used the same technique and

diagnostic criteria to investigate women with recurrent preg-

nancy loss. The aim of the study was to investigate the

prevalence and severity of uterine anomalies in women with

recurrent pregnancy loss and then to compare the results to the

®ndings in low risk women.

Materials and methods

A total of 522 consecutive women with a history of recurrent

miscarriage was prospectively recruited from the Recurrent

Miscarriage Clinics at St Mary's and King's College Hospitals,

London, between August 1997 and January 2001. All women were

screened for the presence of antiphospholipid antibodies and both

partners had peripheral blood karyotyping. All women also underwent

a transvaginal ultrasound scan as a part of the investigations into the

causes of recurrent pregnancy loss. The inclusion criteria were a

Human Reproduction Vol.18, No.1 pp. 162±166, 2003 DOI: 10.1093/humrep/deg030

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history of three or more consecutive unexplained pregnancy losses

before 14 weeks gestation. The control group consisted of 2034 pre-

menopausal women without a history of infertility of recurrent

miscarriage who were referred for an ultrasound scan for a variety of

indications unrelated to reproductive outcomes. Exclusion criteria in

both groups of women were an ongoing pregnancy, presence of

uterine ®broids distorting the uterine cavity, previous hysterectomy or

myomectomy and inadequate visualization of the uterine cavity. The

study was approved by the Research Ethics Committees of both

institutions, and informed consent was obtained for the trial from all

participants.

Two-dimensional ultrasound was used ®rst to screen for congenital

uterine anomalies. Uterine anomalies were suspected when there was

evidence of duplication of uterine cavity or when the interstitial

portion of either Fallopian tube could not be seen. All women with

suspected anomalies were then examined by three-dimensional

ultrasound (Combison 530 3-D Voluson, Kretztechnik, Zipf,

Austria). In order to obtain three-dimensional ultrasound images, the

uterus was visualized in the longitudinal plane. A three-dimensional

ultrasound volume was then generated by the automatic sweep of the

mechanical transducer. The acquired volumes were in the shape of a

truncated cone with the depth of 4.3±8.6 cm and a vertical angle a =

90°. The volumes were immediately stored on removable hard disk

cartridges (Magneto-Optic 3.0¢, 640 MB; Olympus Optical Co.,

Hamburg, Germany). The analysis of uterine morphology was then

performed online using the technique of planar reformatted sections

with the interstitial portions of the Fallopian tubes as reference points

(Jurkovic and Aslam, 1998). In all cases, the ultrasound operator was

aware of the clinical diagnosis of the woman being examined.

Congenital uterine anomalies were classi®ed in accordance with the

modi®ed American Fertility Society Classi®cation (Woelfer et al.,

2001). In addition, in each case of arcuate and subseptate uterus a

distance was measured between the midpoint of the line joining the

two internal tubal ostia and the distal tip of fundal indentation or

uterine septum. Further measurements were then taken from this point

to the level of the internal os, this measurement representing the length

of the unaffected uterine cavity. The degree of distortion of uterine

architecture was then quanti®ed by the ratio F/F+C, where F was the

length of the uterine septum or depth of the fundal indentation and C

was the length of the remaining uterine cavity (Figure 1).

Reproducibility of three-dimensional ultrasound measurement of

fundal indentation/septum length (F) and the residual normal cavity

length (C) was assessed in a randomly selected sample of 21 women,

which included eight arcuate and 13 subseptate uteri. In order to

examine inter-observer reproducibility, two experienced operators

(R.S. and B.W.) performed two blinded measurements of each

parameter. The mean differences for the measurements of F and C

between R.S. and B.W. were 0.157 mm (95% limits of agreement

from ±1.137 to 1.451 mm) and 0.514 mm (95% limits of agreement

from 0.596 to 1.624 mm) respectively.

Both operators were also tested for the intra-observer variability of

measurement. The mean differences for measurements of F were

±0.157 mm (95% limits of agreement from ±2.54 to 2.23 mm) and

0.277 mm (95% limits of agreement from ±2.13 to 2.69 mm) for

operators R.S. and B.W. respectively. The mean differences for

measurement of C were 0.138 mm (95% limits of agreement from

±2.87 to 3.02 mm) and 0.110 (95% limits of agreement from ±1.91 to

2.13 mm) for operators R.S. and B.W. respectively.

A database ®le was set up using Microsoft Excel for Windows

(Redmond, WA, USA) to facilitate data entry and retrieval. Statistical

analysis was performed using SPSS for Windows (Version 6.0; SPSS,

Inc., Chicago, IL, USA). Student's t-test was used to compare the

mean ages of the women and septum length or depth of fundal

indentation, in arcuate uteri, and distortion ratio. Pearson's c2-test was

used to compare relative proportions of various types of uterine

anomalies between control and recurrent miscarriage groups. The

Mann±Whitney test for non-parametric data was used to compare the

differences in proportions of women who had been pregnant, ®rst

Figure 1. A coronal view of a septate uterus demonstrating thenormal outer uterine contour. The length of the septum (F) ismeasured between its distal tip and the midpoint of the lineadjoining tubal ostia. The length of the residual uterine cavity(C) was measured between the distal tip of the septum and theinternal os.

Table I. Demographics of women with uterine anomalies included in the ®nal data analysis

Low risk(n = 105)

Recurrent miscarriage(n = 121)

P

Mean age (range) 32.4 (18±48) 34.9 (21±45) <0.001Total no. of women who were pregnant in the past (%) 56 (53.3) 121 (100) <0.001Total no. of pregnancies 126 491 ±No. of pregnancies per woman (mean and range) 1.26 (0±9) 4.0 (3±11) <0.001First trimester miscarriage (%) 37 (29.4) 411 (83.7) <0.001Second trimester miscarriage (%) 9 (7.1) 35 (7.0) 0.020Pre-term labours (%) 14 (11.1) 9 (1.8) 0.423Live births (%) 68 (53.9) 36 (7.3) 0.012

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trimester miscarriage, second trimester miscarriage, pre-term labours

and live births.

Results

A total of 509 women with a history of recurrent miscarriage

was included in the ®nal data analysis. Thirteen women (2.6%)

were excluded: three were found to have submucous ®broids,

which were signi®cantly distorting the uterine cavity, and nine

women had an irregular uterine cavity following previous

uterine surgery. An additional patient with the diagnosis of an

arcuate uterus tested positive for antiphospholipid antibodies

and therefore she was also excluded from the ®nal data

analysis. Of the 509 women who were included in the ®nal

analysis, 388 (76.2%) had a normal uterus and uterine

anomalies were diagnosed in 121 (23.8%) (Table I). In the

control group, satisfactory three-dimensional ultrasound

images were obtained in 1976 women (97.1%) with 43

women being excluded due to the presence of submucous

®broids, 11 due to the presence of an intrauterine contraceptive

device and four women were excluded due to an irregular

uterine cavity following myomectomy. A conclusive diagnosis

of congenital uterine anomaly was made in 105 (5.3%) women.

The most common anomalies in both groups were arcuate

and subseptate uterus, which accounted for >90% of cases

(Table II). There was no signi®cant difference in the relative

proportions of congenital uterine anomalies in the two groups

of women. Morphological characteristics of uterine anomalies

in women with recurrent miscarriage were compared with the

control group. Depth of fundal indentation, in arcuate uteri, and

septum length, in subseptate uteri, were not signi®cantly

different between the two groups of women. However, in both

arcuate and subseptate uteri, the length of the normal uterine

cavity was signi®cantly shorter and the degree of distortion of

the uterine cavity was signi®cantly higher in women with a

history of recurrent miscarriage (Table III). In order to

eliminate a potential effect of parity on uterine morphology,

comparisons were also performed in the cohort of nulliparous

women only. This revealed similar results except that the depth

of fundal indentation in arcuate uteri in the recurrent miscar-

riage group was signi®cantly greater compared with that in low

risk women (Table IV).

Discussion

In this study, congenital uterine anomalies were found in

23.8% of women with recurrent miscarriage. The most

common anomaly, however, was the arcuate uterus, whilst

major anomalies were present in 6.9% of women. Previous

studies of women with a history of recurrent early pregnancy

loss have shown a variable prevalence of congenital uterine

anomalies. In one study (Clifford et al., 1994), major uterine

Table II. Relative proportions of congenital uterine anomalies in low riskwomen and those with a history of recurrent miscarriage

Uterine anomaly Recurrent miscarriage n (%) Low risk n (%)

Arcuate uterus 86 (71.1) 72 (68.6)Subseptate uterus 27 (22.3) 28 (26.6)Bicornuate uterus 6 (5.0) 4 (3.8)Unicornuate uterus 2 (1.6) 1 (1.0)Total 121 (100) 105 (100)

Table III. Comparison of uterine morphology in all women with congenital uterine anomalies

Arcuate Subseptate

Recurrentmiscarriage

Low risk t P Recurrentmiscarriage

Low risk t P

No. of women 86 72 27 28Mean septum length/fundal 5.57 (2.72) 5.42 (1.77) ±0.383 NS 21.78 (5.42) 18.73 (8.76) NS NSindentation (mm)Mean cavity length (mm) 24.08 (5.44) 29.60 (6.09) 6.069 < 0.001 14.24 (5.34) 24.84 (11.43) 4.380 < 0.001Mean degree of distortion, a/a+b 0.18 (0.004) 0.16 (0.004) ±2.955 0.004 0.60 (0.12) 0.40 (0.25) ±3.848 < 0.001

Values in parentheses are SD.NS = non-signi®cant.

Table IV. Comparison of uterine morphology in nulliparous women with congenital uterine anomalies

Arcuate Subseptate

Recurrentmiscarriage

Low risk t P Recurrentmiscarriage

Low risk t P

No. of women 56 42 21 17Mean septum length/fundal indentation (mm) 5.84 (2.84) 4.77 (1.58) ±2.376 0.019 21.33 (21.33) 17.0 (5.72) ±2.021 NSMean cavity length (mm) 23.61 (5.3) 27.65 (5.69) 3.765 0.001 15.04 (5.25) 23.53 (12.4) 2.847 0.007Mean degree of distortion, F/F+C 0.2 (0.01) 0.15 (0.004) ±3.628 0.001 0.59 (0.12) 0.40 (0.28) ±2.734 0.010

Values in parentheses are SD.NS = non-signi®cant.

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anomalies were found in nine out of 500 cases (1.8%). Another

large screening study of 1200 Japanese women found major

anomalies in 4.6% of women (Makino et al., 1992a), whilst in a

study of 55 women (Tulppala et al., 1993), major uterine

anomalies were found in four cases (7.2%). The prevalence of

major uterine anomalies in our study is broadly in agreement

with these previous studies, which used invasive diagnostic

techniques to detect uterine anomalies. The lower prevalence

reported by Clifford et al. (1994) may be explained by the low

sensitivity of two-dimensional transabdominal ultrasound for

the diagnosis of congenital uterine defects.

The potential signi®cance of uterine anomalies in the context

of recurrent pregnancy loss cannot be established without

comparisons with the low risk population. In a previous

screening study of 1022 low risk women, we found major

congenital uterine anomalies in 2.3% of cases (Jurkovic et al.,

1997), which is comparable with the prevalence of 1.7% in this

series. Similar results have been reported by others who have

used a combination of invasive tests to screen for uterine

anomalies in women undergoing tubal sterilization. One study

(Ashton et al., 1988) found major anomalies in 1.9% of cases

using hysterosalpingography and hysteroscopy, whilst Simon

et al. (1991) reported the prevalence of 3.2% using a

combination of laparoscopy and hysterosalpingography. A

recent study (Byrne et al., 2000), using transabdominal two-

dimensional ultrasound to screen for anomalies, found preva-

lence of only 0.4% in 2065 low risk women. Similar to the

study by Clifford et al. (1994), this low prevalence is likely to

be the re¯ection of the poor sensitivity of transabdominal two-

dimensional ultrasound for the diagnosis of uterine anomalies.

The results of these studies show that the prevalence of

major congenital uterine anomalies is ~3-fold higher in women

with history of recurrent miscarriage compared with the low

risk population. This suggests that congenital uterine anomal-

ies may indeed be responsible for pregnancy loss in a small

proportion of women with recurrent miscarriages.

A recent literature review showed that the most common

major uterine anomaly in women with recurrent pregnancy loss

is subseptate uterus (Homer et al., 2000). The results of our

study are similar, showing that the subseptate uterus was the

most common major uterine anomaly, accounting for 77% of

cases. The subseptate uterus was also the most common

anomaly in low risk women, accounting for 70±90% of cases

(Simon et al., 1991; Jurkovic et al., 1997; Raga et al., 1997).

Subseptate uterus accounted for 84% of major anomalies found

in low risk women in the present study, which is again

consistent with the data from the literature.

The pathophysiology of early pregnancy loss in cases of

subseptate uterus is explained by the inability of the relatively

avascular septum to provide adequate blood supply to the

developing embryo (Burchell et al., 1978). This view is

supported by histological evaluation of the septum, which

showed signi®cantly reduced vascular supply in relation to the

rest of the uterus (Nakada et al., 1989; Dabirasha® et al., 1995).

If this theory is correct, then the likelihood of miscarriage

caused by septal implantation should increase with the severity

of the disruption of uterine morphology.

Makino et al. (1992b) tried to quantify the degree of

distortion of the uterine cavity by calculating the ratio between

the fundal distortion and the length of the uterine cavity on

hysterosalpinography. They found no association between the

severity of uterine anomaly and the number of previous

miscarriages. In contrast, the results of this study showed that

the degree of distortion of the uterine cavity in subseptate

uterus was higher in women with recurrent miscarriage,

compared with low risk women. This was mainly due to the

reduced length of unaffected cavity, rather than the increased

septum length. Differences between our and Makino's study

could be a result of different measurement techniques and

different de®nition of recurrent miscarriage in their study,

which included women with only two consecutive ®rst

trimester losses. Nevertheless our results indicate that the

distortion of the uterine anatomy in subseptate uterus is greater

in women with recurrent pregnancy loss. This ®nding supports

the hypothesis of septal implantation as a potential cause of

miscarriage as the likelihood of septal implantation increases

with an increasing ratio of septal size to functional cavity.

The prevalence of arcuate uterus in women with recurrent

miscarriage was 17%, which is signi®cantly higher compared

with the prevalence of 3.2% in low risk women (Jurkovic et al.,

1997). In addition, similar to the subseptate uterus, the

distortion of uterine cavity was greater in women with

recurrent ®rst trimester loss. The diagnosis of arcuate uterus

is dif®cult using conventional methods such as hysteroscopy or

laparoscopy and the diagnostic criteria are far from clear

(Golan et al., 1992). As a result, little is known about its

prevalence and clinical signi®cance. However, all studies

report an increase in adverse reproductive outcomes, mostly

second trimester loss (Tulandi et al., 1980; Acien, 1993; Raga

et al., 1997; Woelfer et al., 2001). The pathophysiology of

miscarriage in women with arcuate uterus remains unknown.

The only therapeutic intervention that has been proposed to

decrease the risk of miscarriage is the insertion of cervical

suture (Golan et al., 1990). However, this intervention is

unlikely to be helpful in women with a history of ®rst trimester

pregnancy loss.

This study also demonstrates the bene®ts of using three-

dimensional ultrasound for the diagnosis of uterine abnormal-

ities. The accuracy of three-dimensional ultrasound compared

with the traditional methods for the assessment of uterine

morphology has been assessed and was found to be satisfactory

(Jurkovic et al., 1995; Raga et al., 1996). The main advantage

of this technique is the ability to describe uterine anomalies in

quantitative terms and store ultrasound volumes permanently

in a form which enables further re-examination and independ-

ent evaluation of the diagnosis (Jurkovic and Aslam, 1998).

This provides an opportunity to pool diagnostic information

from a large number of diagnostic centres and to describe

anomalies using uniform diagnostic criteria. Accumulation of

such a large number of data may help to provide us with better

answers in the future about the clinical signi®cance and

optimal management of many different types of uterine

anomalies.

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