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Long-term complications of caesarean section.
The niche in the scar: a prospective cohort study
on niche prevalence and its relation to abnormal
uterine bleeding
LF van der Voet,a
AM Bij de Vaate,b
S Veersema,c
HAM Bro¨ lmann,b
JAF Huirneb
a
Department of Obstetrics and Gynaecology, Deventer Hospital, Deventer, the Netherlands b
Department of Obstetrics and Gynaecology,
VU University Medical Centre, Amsterdam, the Netherlands c
Department of Obstetrics and Gynaecology, St Antonius Hospital, Nieuwegein,
the Netherlands
Correspondence: LF van der Voet, N. Bolkesteinlaan 75, Deventer 7416 SE, the Netherlands. Email l.f.vandervoet@dz.nl
Accepted 29 September 2013.
Objective To study the prevalence of niches in the caesarean
scar in a random population, and the relationship with
postmenstrual spotting and urinary incontinence.
Design A prospective cohort study.
Setting A teaching hospital in the Netherlands.
Population Non-pregnant women delivered by caesarean section.
Methods Transvaginal ultrasound (TVU) and gel instillation
sonohysterography (GIS) were performed 6–12 weeks after
caesarean section. Women were followed by questionnaire and
menstruation score chart at 6–12 weeks, 6 months, and
12 months after caesarean section.
Main outcome measures Prevalence of a niche 6–12 weeks after
caesarean section, using TVU and GIS. Secondary outcomes:
relation to postmenstrual spotting and urinary incontinence 6 and
12 months after caesarean section; and niche characteristics,
evaluated by TVU and GIS.
Results Two hundred and sixty-three women were included.
Niche prevalence was 49.6% on evaluation with TVU and 64.5%
with GIS. Women with a niche measured by GIS reported more
postmenstrual spotting than women without a niche (OR 5.48,
95% CI 1.14–26.48). Women with residual myometrium at the
site of the uterine scar measuring <50% of the adjacent
myometrial thickness had postmenstrual spotting more often than
women with a residual myometrial thickness of >50% of the
adjacent myometrial thickness (OR 6.13, 95% CI 1.74–21.63).
Urinary incontinence was not related to the presence of a niche.
Conclusions A niche is present in 64.5% of women 6–12 weeks
after caesarean section, when examined by GIS. Postmenstrual
spotting is more prevalent in women with a niche and in women
with a residual myometrial thickness of <50% of the adjacent
myometrium.
Keywords Abnormal uterine bleeding, caesarean section,
caesarean section scar, niche, postmenstrual spotting,
ultrasonography.
Please cite this paper as: van der Voet LF, Bij de Vaate AM, Veersema S, Bro¨lmann HAM, Huirne JAF. Long-term complications of caesarean section. The
niche in the scar: a prospective cohort study on niche prevalence and its relation to abnormal uterine bleeding. BJOG 2014;121:236–244.
Introduction
Concern regarding the association between delivery by cae-
sarean section and long-term maternal morbidity is grow-
ing, as the rate of caesarean section continues to increase.
In the Netherlands the caesarean section rate increased
from 7.4 to 15.8% during the period 1990–2008,1
and in
the USA it increased from 21.2 to 32.8% from 1990 to
2011.2
The long-term complications of caesarean section in
relation to future reproduction have been comprehensively
examined.3,4
In the past decade several articles have
described a defect that can be seen on ultrasound at the
site of the caesarean section scar, known as a ‘niche’.5,6
A niche is defined as a triangular anechoic structure at the
site of the scar or a gap in the myometrium of the anterior
lower uterine segment at the site of a previous caesarean
section.7,8
Niche prevalence depends on the method used
for evaluation and the population investigated.9–16
In
non-pregnant women the scar is visible with transvaginal
ultrasonography (TVU) and contrast sonohysterography
using either saline (saline infusion sonohysterography, SIS)
or gel (gel instillation sonohysterography, GIS).5,6
There
236 ª 2013 Royal College of Obstetricians and Gynaecologists
DOI: 10.1111/1471-0528.12542
www.bjog.org
General gynaecology
have been several reports of an association between abnor-
mal bleeding and a niche.8,10–12,15
In particular, postmen-
strual spotting seems to be a predominant symptom in
women with a niche10,11
; however, most of these studies
included symptomatic patients, resulting in a possible selec-
tion bias. Given the proximity of the niche to the bladder,
it has been postulated that the local accumulation of fluid
and scarring might disturb bladder function11
; however,
prospective studies assessing both bleeding symptoms and
urinary symptoms in relation to the presence of a niche in
a random population of women with a history of caesarean
section are scarce. As far as we are aware, none of the
reported studies asked women to participate at the time of
caesarean section. The aim of our study was to determine
the prevalence of niches in the caesarean section scar in a
random population of women enrolled immediately after
caesarean section, using both TVU and GIS 6–12 weeks
after caesarean section, and to examine the relationship
between the niche and postmenstrual spotting and urinary
incontinence.
Methods
Study design and population
We conducted a prospective observational cohort study.
The trial was registered in the Dutch trial register (trial
number NTR-2887). The study was performed in St Anto-
nius Hospital, Nieuwegein: a teaching hospital in the Neth-
erlands. The protocol was approved by the local medical
ethics committee (VCMO NL18722.100.07 R-07.14A/
SCAR.). Participants were recruited between November
2007 and September 2010. Specially trained midwives asked
all women over 18 years of age who underwent a caesarean
section at St Antonius Hospital during the inclusion period
to participate, within 3 days of the caesarean section.
Exclusion criteria were twin pregnancies, known uterine
anomalies, or the suspicion of a uterine infection, defined
as a positive culture or fever and abdominal pain with dis-
charge. After providing written informed consent, all par-
ticipants were evaluated by TVU followed by GIS 6–
12 weeks after the caesarean section. A GIS was not per-
formed when there were suspected placental remnants,
intrauterine haematomas, intrauterine fluid accumulation,
or a possible pregnancy (i.e. a visit during the midluteal
phase in women not using adequate contraception).
Women were followed by questionnaires and menstruation
score charts at 6–12 weeks, 6 months, and 12 months after
the caesarean section.
Transvaginal ultrasound
All TVU and GIS procedures were performed at St
Antonius Hospital by three experienced examiners (L.V.,
S.V., and M.S.). TVU was performed using a 7.5–MHz
transducer (Philips Sonicare HD 11.XE, Philips Medical
Systems, Eindhoven, the Netherlands). Women were exam-
ined after emptying their bladder. The uterus, uterine scar,
and niche, if present, were examined in a standardised way.
The position, length, and width of the uterus and double
thickness of the endometrium were registered in the mid-
sagittal plane. A niche was defined as an anechoic space
(with or without fluid) at least 2 mm deep at the presumed
site of the caesarean section scar. The uterus was screened
for the presence of caesarean section scar(s) using parallel
sagittal planes going from left to right, until the plane with
the largest niche depth was defined. The uterus was also
scanned in the transverse plane. When a niche was identi-
fied, it was measured in the sagittal plane in which the
niche had the greatest depth; the depths of the niche and
of the residual myometrium at the site of the scar and of
the adjacent normal myometrium were measured in real
time (see Figure 1). In cases when more than one caesarean
section scar was present the largest niche was measured.
Gel instillation sonography
A speculum was inserted and a catheter (SIS Rudigoz Cath-
eter, CCD International, Paris, France) was placed inside
the uterus. Gel (Endosgel, Farco-Pharma GmbH, K€oln,
Germany) was flushed inside the uterine cavity and cervix
while retracting the catheter. A maximum volume of
10 cm3
was instilled, or less if uterine cramps occurred or
reflux was observed from the cervix. The speculum was
removed, the vaginal probe was reinserted, and the pres-
ence of a niche was recorded in the sagittal plane where
the niche had the greatest depth. Niche characteristics were
measured and recorded as described above (Figure 1). The
shape was classified according to the previous classifications
published by Bij de Vaate et al.11
The presence of uterine
polyps, fibroids, or other intrauterine abnormalities was
noted.
Sagittal plane
1
2
3
RM
AMT
Figure 1. Schematic presentation of niche measurement. The
following measurements were performed: (1) niche depth (in the
sagittal plane); (2) residual myometrium (RM), from the serosal
surface of the uterus (without the white lining of the serosa) to the
apex of the niche, perpendicular to the endometrium (in sagittal plane);
(3) adjacent myometrial thickness (AMT). Adapted from Bij de Vaate
et al.11
237ª 2013 Royal College of Obstetricians and Gynaecologists
Niche prevalence and abnormal uterine bleeding
Data collection
The characteristics of participants, including contraceptive
use, breastfeeding, bleeding characteristics before preg-
nancy, and detailed obstetric history (dates of previous
caesarean section, indication, and characteristics of the last
pregnancy and caesarean section) were noted immediately
after informed consent was given. Current contraceptive
use and bleeding pattern were recorded at 6–12 weeks after
the caesarean section. Women completed and returned a
questionnaire at 6 and 12 months after the caesarean sec-
tion. The questionnaire included questions on current
medication or contraceptive use, breastfeeding, bleeding
pattern (including duration of menstruation, postmenstrual
spotting, vaginal discharge, and urinary incontinence).
They were also asked to complete a validated menstrual
score chart: the Pictorial Blood Assessment Chart
(PBAC).17
All data were recorded in a web-based database
by two research nurses. The results of the ultrasound scans
were not recorded in the case notes, and women and their
doctors were not informed of the ultrasound findings. All
women who underwent TVU were included in the analyses.
Only women who underwent both TVU and GIS were
included in the comparison of TVU and GIS measurement
outcomes.
The primary outcome was the prevalence of a niche as
measured by TVU and GIS 6–12 weeks after caesarean sec-
tion. Secondary outcome measures included details of the
bleeding pattern, including postmenstrual spotting (defined
as more than 2 days of brownish discharge after the end of
the menstrual period), number of days of menstrual bleed-
ing, urinary incontinence at 6 and 12 months after caesar-
ean section, and the relationship of these with a niche, and
niche characteristics (i.e. depth, residual myometrium, and
the ratio of the residual myometrium divided by the total
thickness of the adjacent anterior myometrium), identified
by TVU and GIS.
Statistical analyses
Data were analysed using the SPSS 20 (SPSS Inc., Chicago,
IL, USA). Differences in baseline characteristics were com-
pared using the chi-square test, Fisher’s exact test, Student’s
t–test, or the Mann–Whitney U–test, depending on the
type and distribution of the variables. Logistic regression
analysis was planned to analyse the relationship between
the presence of a niche and postmenstrual spotting.
Potential confounding factors were predefined, and
included age, breastfeeding, body mass index (BMI), BMI
above 25 kg/m2
, oral contraceptive use, and use of the
levonorgestrel intrauterine system (LNG-IUS). These poten-
tial confounding factors were tested using univariate
analysis. All tests were two-sided. A two-tailed P < 0.05
was considered to be statistically significant.
Results
Between November 2007 and September 2010, 350 women
gave informed consent to participate in the study within
3 days of their caesarean section at St Antonius Hospital.
Of these, 276 were willing to receive a TVU at 6–12 weeks,
and 263 women could be included. TVU was used to
examine 263 women, and 197 underwent both TVU and
GIS (see Figure 2). Two women underwent a second cae-
sarean section during the study period, but only the results
of the first caesarean section and the related TVU and GIS
were included in the study. TVU and GIS were performed
at a mean of 7.6 Æ 1.7 (SD) weeks after caesarean section.
In total, 72% (191/263) of all women who underwent a
TVU completed the questionnaire at 6 months, and 69%
(172/249) of the women who received a questionnaire at
12 months after the caesarean section completed it. Of all
the women who completed the questionnaire at 12 months,
45 were pregnant again. Of the women who underwent
both a TVU and GIS the response rate was 73% at
12 months. Baseline characteristics and sonography results
at 6–12 weeks after caesarean section are shown in Table 1.
The majority of the women (71%) analysed had had only
one previous caesarean section. Sixty-four (24%) had had
two and eleven (4%) had had three previous caesarean sec-
tions. One caesarean section was carried out by a J–shaped
or ‘hockey stick’ incision. All other women had a transverse
lower segment incision. The uterus was closed in two layers
in four women and in one layer in all others. Most caesar-
ean sections (55%) were performed because of an emer-
gency. During the sonographic evaluation at 6–12 weeks
after caesarean section, 55% of the women were breastfeed-
ing and 77% were amenorrhoeic. At 6–12 weeks, the
women reported using the following methods of contracep-
tion: no contraception, 36%; oral contraceptives, 10%; pro-
gesterone only pill, 3%; sterilisation, 4%; condoms, 42%;
and other, 5%. The difference in contraceptive use was not
statistically significant between patients with or without a
niche.
There were no differences regarding the rate of primary
or emergency caesarean section, age, or parity between
women who were included in our analyses and those who
refused to participate, those who did not undergo a GIS,
or those who did not complete the questionnaire at
12 months.
Niche prevalence and characteristics
Niche prevalence was 49.6% when evaluated by TVU and
64.5% when evaluated by GIS. In three women it was not
possible to identify the scar in the uterus with TVU. With
GIS all scars were visible. In women with one caesarean
section, 62% who underwent GIS had a niche, compared
238 ª 2013 Royal College of Obstetricians and Gynaecologists
van der Voet et al.
with 68.2% of women with two caesarean sections and
77.8% of women with three caesarean sections. Sonograph-
ic characteristics of the uterus are shown in Tables 1 and 2.
The length and width of the uterus were no different
between women who had or did not have a niche. The
niche was deeper when examined by GIS than by TVU
(2.32 Æ 3.35 and 3.03 Æ 3.1 mm, respectively; P < 0.001).
The thickness of the residual myometrium at the site of the
uterine scar was approximately 2 mm less in women with a
niche compared with those without a niche, as measured
by TVU and GIS (P < 0.001 and P = 0.005, respectively;
see Table 1). The mean ratio between the thickness of the
residual myometrium at the site of the niche and the thick-
ness of the adjacent myometrium was 0.74 Æ 0.58 in all
women who underwent GIS. The ratio was <0.5 in 22% of
these women. Most niches detected by GIS had a semicir-
cular shape (55%); 24% had a triangular shape, 10% had a
droplet shape, 6% were inclusion cysts, and 7% had
another shape.
Bleeding pattern and urological symptoms
The questionnaire at 6 months was completed by 191
women. Information on the menstrual cycle was available
for only 59 women. Given the large proportion of women
who were still breastfeeding or who did not yet have a
regular menstrual cycle we decided not to analyse the
outcomes at 6 months. The questionnaire at 12 months
was completed by 172 women. The menstrual pattern
could not be analysed in 45 of these women because of a
subsequent pregnancy. Ten of these women completed the
information on the basis of their menstruation pattern
before pregnancy. Information on the menstrual cycle and
contraceptive use was available for 137 women, of whom
17 were amenorrhoeic because of LNG-IUD or another
hormonal contraceptive. Postmenstrual spotting was
reported by 13 out of 45 (28.9%) women with a niche
detected by GIS, compared with two women out of 29
(6.9%) without a niche detected by GIS (OR 5.48, 95% CI
1.14–26.48; Table 3). Including only primiparae, again post-
menstrual spotting was reported more frequently in women
with a niche detected by both TVU or GIS compared with
those without a niche (31 versus 4% for TVU and 32 versus
0% for GIS; OR 9.7, 95% CI 1.1–85.6). Women with a ratio
of residual myometrium of less than half of the adjacent
myometrium (ratio <0.5) measured by TVU or GIS
reported postmenstrual spotting more often than women
with a ratio of >0.5 (OR 7.2, 95% CI 1.74–21.62, and OR
6.1, 95% CI 1.94–26.70, respectively; Table 4).
Excluded (n = 87):
• Women not willing to undergo TVU
at 6–12 weeks after caesarean (74)
• Twin pregnancy (6)
• Uterus anomaly (1)
• New pregnancy (2)
• >12 weeks after caesarean (1)
• Pelvic inflammatory disease (1)
• Woman’s second caesarean
during study period (2)
Transvaginal ultrasound (TVU)
(n = 263)
Excludedfrom GIS ( n = 66):
• Placental remnant/haematoma (8)
• Pelvic inflammatory disease (6)
• Woman's request (6)
• Unprotected intercourse (3)
• Failed GIS (no distension) (11)
• Failed GIS (pain) (12):
• Intrauterine fluid (13)
• Other (7)
Gel instillation sonography (GIS)
(n = 197)
Questionnaire completed 12 months after
caesarean section
(n = 172)
Non-responders (77)
Lost to follow-up (14)
• Incorrect address/moved (12)
• Refusal to continue the study (2)
Women willing to
participate
(n = 350)
Figure 2. Flow diagram of study participants.
239ª 2013 Royal College of Obstetricians and Gynaecologists
Niche prevalence and abnormal uterine bleeding
Using univariate analyses none of the predefined con-
founding factors or baseline characteristics were related to
postmenstrual spotting: all had P > 0.1 (LNG-IUD use,
P = 0.11; oral contraceptive use, P = 0.24; breastfeeding,
P = 1.0; age, P = 1.0; BMI, P = 1.0; BMI > 25 kg/m2
,
P = 0.40), and therefore the planned logistic regression was
not performed. We did not find any significant differences
between women with or without a niche concerning the
existence of (combined) urinary incontinence, urge inconti-
nence, or stress incontinence (see Table 3).
Discussion
Main findings
All caesarean section scars could be identified using GIS.
Using this technique the prevalence of niches at the site of
these caesarean section scars was high (64.5%) in a random
population. Comparing the results of GIS with TVU, niche
prevalence was higher, measured niche depth was greater,
and residual myometrium was thinner when detected by
GIS. Postmenstrual spotting 1 year after caesarean section
was strongly related to the presence of a niche detected by
both TVU and GIS. One out of three women with a niche
detected by GIS reported postmenstrual spotting, compared
with one out of ten women without a niche. Postmenstrual
spotting was related to a residual : adjacent myometrium
ratio of <50%, which might indicate that this is a relevant
parameter for niche size. The prevalence of urinary inconti-
nence was not related to the presence or absence of a
niche.
Table 2. Comparison of transvaginal ultrasound and gel instillation
sonohysterography results (n = 197)*
TVU GIS P (95% CI)
Niche depth of all women,
mean (ÆSD)**
2.32
(Æ3.35)
3.03
(Æ3.1)
<0.001
(0.38–1.02)
Niche depth of women with
niche on GIS, mean (ÆSD)**
3.43
(Æ3.67)
4.77
(Æ2.64)
<0.001
(0.92–1.79)
Residual myometrial thickness
of all women, mean (ÆSD)
9.58
(Æ4.39)
9.11
(Æ3.8)
0.06
(–0.24 to 0.96)
Residual myometrial thickness
of women with niche on GIS,
mean (ÆSD)
9.30
(Æ4.67)
8.59
(Æ3.75)
0.03
(0.09–1.38)
*Of the 263 women in total, only the 197 women who underwent
both TVU and GIS were included in this table.
**Niche depth was recorded as 0 when no niche was observed.
Table 1. Characteristics of the study participants
All women
(n = 263)
Niche (TVU)
(n = 129)
No niche (TVU)
(n = 131)
P* Niche (GIS)
(n = 127)
No niche
(GIS) (n = 70)
P**
Baseline characteristics
Age (years), mean (ÆSD) 32.46 (Æ4.15) 32.66 (Æ4.16) 32.26 (Æ4.15) 0.44 32.51 (Æ4.11) 32.73 (Æ3.85) 0.72
Parity, mean (ÆSD) 1.54 (Æ0.70) 1.55 (Æ0.73) 1.54 (Æ0.68) 0.96 1.57 (Æ0.78) 1.50 (Æ0.68) 0.52
BMI (kg/m2
), mean (ÆSD) 25.70 (Æ5.58) 26.15 (Æ5.48) 25.28 (Æ5.66) 0.28 25.98 (Æ5.83) 24.98 (Æ5.19) 0.29
Number of caesarean sections,
mean (ÆSD)
1.33 (Æ0.56) 1.35 (Æ0.57) 1.31 (Æ0.54) 0.55 1.35 (Æ0.59) 1.26 (Æ0.50) 0.26
Visit at 6–12 weeks after caesarean section
Weeks after caesarean section,
mean (ÆSD)
7.58 (Æ1.74) 7.40 (Æ1.40) 7.74 (Æ2.01) 0.12 7.66 (Æ1.77) 7.72 (Æ1.92) 0.82
Breastfeeding, number
(percentage)***
142 (55%) 67 (52%) 75 (Æ59%) 0.38 64 (53%) 41 (61%) 0.29
Ultrasonographic results at 6–12 weeks after caesarean section
Double endometrial thickness TVU
(mm), mean (ÆSD)
5.49 (Æ3.80) 5.61 (Æ3.85) 5.36 (Æ5.77) 0.61 5.36 (Æ3.57) 4.86 (Æ3.33) 0.34
Uterus length TVU (cm), mean
(ÆSD)
7.18 (Æ1.43) 7.29 (Æ1.52) 7.07 (Æ1.32) 0.23 7.09 (Æ1.38) 7.11 (Æ1.47) 0.92
Uterus width TVU (cm), mean
(ÆSD)
4.23 (Æ0.94) 4.26 (Æ0.81) 4.19 (Æ1.07) 0.59 4.27 (Æ0.84) 4.17 (Æ1.20) 0.49
Thickness of myometrium at site of
caesarean section scar (mm),
mean (ÆSD)
9.59 (Æ4.18) 8.51 (Æ3.90) 10.73 (Æ4.18) <0.001 8.59 (Æ3.81) 10.20 (Æ3.59) 0.005
*P value between niche and no niche during TVU.
**P value between niche and no niche during GIS.
***No information on breastfeeding for 13 patients at 6–12 weeks after caesarean section.
240 ª 2013 Royal College of Obstetricians and Gynaecologists
van der Voet et al.
Strengths and limitations of the study
To the best of our knowledge this is the first study that
has recruited participants at a very early stage after their
caesarean section (within 3 days), followed by early exami-
nation (within 3 months) by both TVS and GIS, and with
the sequential completion of menstrual questionnaires up
Table 3. Uterine bleeding pattern and urological symptoms at 12 months after caesarean section
Niche
(TVU)
No niche
(TVU)
P* Niche
(GIS)
No niche
(GIS)
P** OR
(95% CI)
No. of women with postmenstrual spotting (n = 91/74)*** 13 (26) 5 (12) 0.10 13 (28.9) 2 (6.9) 0.02 5.48 (1.14–26.48)
Days of blood loss during menstruation, mean (ÆSD)
(n = 91/83)***
5.9 (2.57) 6.1 (2.84) 0.75 5.5 (Æ2.1) 5.5 (Æ1.4) 0.98
No. of women with vaginal discharge (n = 137/98)*** 11 (14) 11 (18) 0.84 7 (11) 8 (23) 0.15
No. of women taking oral contraceptives (n = 137/109)*** 19 (25) 13 (21) 0.61 19 (28) 10 (24) 0.82
No. of women with LNG-IUD (n = 137/109)*** 9 (12) 8 (13) 0.82 10 (15) 2 (5) 0.21
No. of women with amenorrhoea (n = 137/109)*** 12 (16) 5 (8) 0.18 9 (13) 3 (7) 0.53
No. of women with incontinence (n = 115/90)*** 20 (31) 17 (34) 0.71 19 (33) 10 (29) 0.82
No. of women with stress incontinence (n = 115/90)*** 15 (23) 11 (22) 0.89 14 (25) 6 (17) 0.45
No. of women with urge incontinence (n = 115/90)*** 4 (6) 3 (6) 0.97 2 (4) 2 (6) 0.63
No. of pregnant women (n = 260/197)*** 17 (13) 28 (21) 0.08 21 (16.5) 15 (21) 0.40
No. lost to follow–up/non-responders (n = 263/197) 42 (33) 49 (37) 0.41 45 (35) 18 (26) 0.16
Total (n = 260/197)*** 129 (49.6) 131 (50.4) 127 (64.5) 70 (35.5)
Data are presented as number (%), unless indicated with mean (ÆSD).
Three women for whom the presence of a niche could not be determined were excluded.
*P value between niche and no niche during TVU.
**P value between niche and no niche during GIS.
***Number of women who completed the questionnaire for a specific parameter and who underwent TVU/GIS, respectively.
Table 4. Niche characteristics in women with or without postmenstrual spotting (n = 91/74)*
Postmenstrual
spotting (TVU)
(n = 18)
No postmenstrual
spotting (TVU)
(n = 73)
P (OR, 95% CI)** Post-menstrual
spotting (GIS)
(n = 15)
No postmenstrual
spotting (GIS)
(n = 59)
P (OR, 95%CI)***
Niche depth (mm),
mean (ÆSD)
5.46 (Æ2.50) 5.15 (Æ2.77) 0.72 5.45 (Æ2.76) 4.86 (Æ2.50) 0.47
Residual thickness of
myometrium at the
site of the caesarean
scar (mm), mean
(ÆSD)
8.92 (Æ4.76) 9.31 (Æ4.28) 0.73 8.19 (Æ5.06) 9.22 (Æ4.11) 0.40
No. of women with
ratio RM/AM <50%
**** (TVU n = 69;
GIS n = 73)
8 (61%) 10 (18%) 0.03
(7.2,1.94–26.70)
8 (57%) 10 (18%) 0.005
(6.13,1.74–21.63)
Mean ratio RM/
AM****
0.50 0.72 0.008 0.53 0.70 0.03
AM, adjacent myometrium; RM, residual myometrium.
*Number of women who completed the postmenstrual spotting questionnaire and who underwent TVU/GIS, respectively. All patients who
completed the questionnaire on postmenstrual spotting were included.
**P value between patients with and without postmenstrual spotting who underwent TVU.
***P value between patients with and without postmenstrual spotting who received a GIS.
****Ratio RM/AM = residual myometrial thickness at the site of the caesarean scar/myometrial thickness of the adjacent myometrium, presented
in numbers (percentage).
241ª 2013 Royal College of Obstetricians and Gynaecologists
Niche prevalence and abnormal uterine bleeding
to 1 year after the caesarean section. Only two prospective
studies have evaluated niches in an unselected popula-
tion.11,18
Both these studies recruited patients at
6–12 months after caesarean section. The Bij de Vaate
et al.11
study was carried out by our study group, but in a
different population and with the examinations performed
by a different examiner. In the present study, early scan-
ning (3 months after the caesarean section) meant that the
vast majority of the women were still amenorrhoeic, so the
influence of abnormal uterine bleeding on the willingness
of women to participate (selection bias) is expected to be
limited. An additional advantage of early sonographic eval-
uation is that, because of amenorrhoea in most patients,
the potential confounding effect of variations in timing of
the measurements during the menstrual cycle and related
endometrial thickness is limited. In addition, women were
consecutively asked to participate by research midwives,
and the registration of the results was independent of clini-
cal considerations. Women and their doctors were not
informed whether or not a niche was observed to prevent
possible bias in reporting their bleeding pattern. Although
complete post-caesarean section scar healing may take up
to 6 months,6
we do not know the exact time needed to
develop a niche. We defined a niche as an anechoic space
(with or without fluid) with a depth of at least 2 mm at
the presumed site of the caesarean section scar. This should
not be confused with the caesarean section scar itself. As
demonstrated in this study, a scar is almost always visible
and is reflected as a hypoechoic indentation of the myome-
trium at the location of the caesarean section. We expect
the uterine scar to continue to heal beyond 6–12 weeks,
and this might differ in performance with time. However,
we consider it very unlikely that niches (i.e. discontinua-
tions and fluid-stained spaces in the myometrium) will heal
after this period. However, changes in a niche over time
are not unlikely. Sustained accumulation of fluid may, in
theory, increase niche size over time, but no data are cur-
rently available to confirm this theory.
A possible limitation of our study is that not all women
who were delivered by caesarean section during the study
period were asked to participate. Women were asked con-
secutively by trained midwives during their day and night
shifts, but these midwives were not always present. Because
the absence of the midwives was randomly distributed over
the week, we consider this potential effect on selection bias
to be minor. This is underlined by the lack of differences
in baseline characteristics between women who were asked
to participate and those who were not, with regards to
elective or emergency caesarean section, age, and parity. In
addition, we did not observe any differences in these
parameters between included and excluded women, or
those who were not willing to undergo a GIS or who did
not complete the questionnaire.
Patients with a previous twin pregnancy or a known
uterine anomaly were excluded in order to assemble a
homogeneous group and to prevent undesired effects of
unknown confounding factors; however, whether these fac-
tors would in fact introduce significant confounding effects
is a topic for further discussion. We also decided not to
perform a GIS in patients with a placental remnant,
haematoma, or fluid in the uterine cavity detected by TVU.
Consequently, a relatively small proportion of all patients
who provided informed consent were analysed. Whether it
is correct to exclude women with intrauterine fluid collec-
tion from examination by GIS should be further discussed.
This was decided before the start of the study, and was
included in the study protocol; however, it can be postu-
lated that this group might have been particularly symp-
tomatic and prone to postmenstrual spotting. We could
not observe any relationship between niches and urinary
incontinence, but we did not report other urinary symp-
toms, such as urgency. An additional shortcoming of the
study is that we did not measure the niche width in the
sagittal plane or the niche length in the transverse plane, as
recently proposed by Naji et al.5
(our study had already
begun before that publication). Therefore, we could not
analyse the relationship between these parameters and
niche symptomatology. We also did not determine the
reproducibility of our measurements.
Clinical implications of the findings and relation
to published data
We were able to identify the caesarean section scar with GIS
in 100% of the women. This is in line with another study
examining women within 3 months of a caesarean section.19
The observed niche prevalence rate of 49.6% using TVU is
comparable with the reported prevalence (42%) in a
prospective cohort study of an unselected population.9
Different prevalence rates (28 and 61%) were reported in
prospective studies in populations evaluated at 6 months
and at 6–12 months after a caesarean section.11,13
Different
definitions of a niche and different timing after the caesar-
ean section may both affect the niche detection rate.
Vikhareva Osser et al.13
used the definition ‘any visible
defect’, and Bij de Vaate et al.11
used ‘any indentation of at
least 1 mm’. We used a cut-off level of 2 mm; however,
consensus on the exact cut-off levels is lacking. Early scan-
ning may facilitate the recognition of the location of the
caesarean section scar in the uterine wall as a result of
incomplete scar healing, and this may increase the detection
of small niches. In addition, the related thin endometrium
resulting from breastfeeding in the majority of the women
may also improve niche recognition and measurement.
We used the same terminology as that suggested by Naji
et al.,5
and measured the depth and residual myometrial
thickness in the sagittal plane as described. Niche
242 ª 2013 Royal College of Obstetricians and Gynaecologists
van der Voet et al.
prevalence using GIS was 64.5% in our study, which is
comparable with the reported prevalence using GIS or SIS
in random, unselected populations (56, 59.5, 59, and
78%).10,11,14,18
Niche prevalence was higher using GIS than
with TVU only. These findings are in line with the reported
findings of three studies comparing GIS or SIS with
TVU.10,11,18
These studies showed a higher niche prevalence
with sonohysterography than with TVU without contrast,
and thus GIS may be more accurate at detecting niches.
Although the niches that were detected using GIS but were
missed using TVU were smaller than those detected by
both TVU and GIS, they can be clinically relevant. This is
underlined by the strong relationship we found between
postmenstrual spotting and niches on GIS.11
An additional
argument for using GIS rather than TVU is that the resid-
ual myometrium measured using GIS was significantly
thinner. The residual myometrium is considered to be the
main limiting factor for eventual hysteroscopic niche resec-
tions to treat related bleeding symptoms. Most publications
report a required residual myometrium of 2–3 mm for
hysteroscopic niche resection, given the risk of perforation
and/or bladder injury.20
In order to prevent undesired
complications during hysteroscopic niche resections we
propose that a GIS or SIS be used rather than TVU for the
preoperative evaluation of the residual myometrium. Sev-
eral previous studies indicated a relationship between large
niches and postmenstrual spotting. Bij de Vaate et al.11
reported the niche volume to be related to postmenstrual
spotting. We were not able to calculate niche volume
because of the lack of stored three-dimensional volumes. In
order to assess the relationship between large niches and
postmenstrual spotting, we decided not to take an absolute
measurement of residual myometrium, but to relate it to
the adjacent myometrium. We defined large niches as those
with a residual myometrium with thickness of <50% of
that of the adjacent myometrium. This parameter was sig-
nificantly related to postmenstrual spotting. This parameter
and cut-off level were also used by Ofilli-Yebovi et al.,15
who reported a high prevalence of women with a ratio of
less of than 50% in a population with gynaecological symp-
toms. A potential relationship between niche size and post-
menstrual spotting is in line with the hypothesis that
spotting is induced by the accumulation of blood inside
the niche.6,7
A depth of more than half the myometrial
thickness makes the anterior part of the niche possibly
large enough to obstruct the direct outflow of menstrual
blood. This, in combination with lower contractility as a
result of fibrosis, may induce the accumulation of blood in
a niche.
One out of three women with a niche observed by GIS
reported postmenstrual spotting. This is in line with the pre-
vious reported prevalence of postmenstrual spotting in
patients with a niche.10,11
Given the high prevalence of post-
menstrual spotting after caesarean section, this should be
part of routine counselling before elective caesarean section.
Future perspectives
Future research should focus on the relationship of niches
to subsequent fertility, obstetric complications such as uter-
ine rupture, and on the impact of a niche on a woman’s
well-being. There is a lack of information on the impact of
niche-related bleeding disorders on women’s quality of life,
their sexual function, and their willingness to undergo
treatment for related symptoms.
Conclusion
In conclusion, the caesarean section scar was visible in all
women at 6–12 weeks after caesarean section using GIS. The
prevalence of niches detected by GIS is high after caesarean
section (64.5%), and more niches are detected using GIS
than using TVU, with a larger observed niche size and reduced
residual myometrial thickness. The presence of a niche is
related to postmenstrual spotting. Postmenstrual spotting is
more frequent in patients with large niches (defined as a
residual myometrium of thickness <50% of that of the
adjacent myometrium) than in patients with smaller niches.
Disclosure of interests
None of the authors have any relevant financial, personal,
political, or religious interest linked to the subject of this
article.
Contribution to authorship
The study was conceived by L.V., J.H., H.B., and S.V., and
L.V. and S.V. performed the ultrasounds and collected the
data. Analysis of the data was performed by L.V. and J.H.
The first draft was written by L.V. and J.H. S.V., H.B., and
A.B. helped to supervise the article up to the final draft.
Details of ethics approval
The study received ethics approval from the united com-
mittee on research involving human subjects (VCMO),
Nieuwegein, the Netherlands (27 September 2007; ref. no.
NL18722.100.07 R-07.14A/SCAR).
Funding
No benefits in any form have been received or will be
received from a commercial party related directly or indi-
rectly to the subject of this article.
Acknowledgements
We thank K.W. Van den Berg-Swart and C. van Dam-Bou-
rens, research nurses, for recording all the collected data in
the database. We thank M. Stigter-de Vries MD for
performing the ultrasounds. &
243ª 2013 Royal College of Obstetricians and Gynaecologists
Niche prevalence and abnormal uterine bleeding
References
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van der Voet et al.

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C.s. scar nich

  • 1. Long-term complications of caesarean section. The niche in the scar: a prospective cohort study on niche prevalence and its relation to abnormal uterine bleeding LF van der Voet,a AM Bij de Vaate,b S Veersema,c HAM Bro¨ lmann,b JAF Huirneb a Department of Obstetrics and Gynaecology, Deventer Hospital, Deventer, the Netherlands b Department of Obstetrics and Gynaecology, VU University Medical Centre, Amsterdam, the Netherlands c Department of Obstetrics and Gynaecology, St Antonius Hospital, Nieuwegein, the Netherlands Correspondence: LF van der Voet, N. Bolkesteinlaan 75, Deventer 7416 SE, the Netherlands. Email l.f.vandervoet@dz.nl Accepted 29 September 2013. Objective To study the prevalence of niches in the caesarean scar in a random population, and the relationship with postmenstrual spotting and urinary incontinence. Design A prospective cohort study. Setting A teaching hospital in the Netherlands. Population Non-pregnant women delivered by caesarean section. Methods Transvaginal ultrasound (TVU) and gel instillation sonohysterography (GIS) were performed 6–12 weeks after caesarean section. Women were followed by questionnaire and menstruation score chart at 6–12 weeks, 6 months, and 12 months after caesarean section. Main outcome measures Prevalence of a niche 6–12 weeks after caesarean section, using TVU and GIS. Secondary outcomes: relation to postmenstrual spotting and urinary incontinence 6 and 12 months after caesarean section; and niche characteristics, evaluated by TVU and GIS. Results Two hundred and sixty-three women were included. Niche prevalence was 49.6% on evaluation with TVU and 64.5% with GIS. Women with a niche measured by GIS reported more postmenstrual spotting than women without a niche (OR 5.48, 95% CI 1.14–26.48). Women with residual myometrium at the site of the uterine scar measuring <50% of the adjacent myometrial thickness had postmenstrual spotting more often than women with a residual myometrial thickness of >50% of the adjacent myometrial thickness (OR 6.13, 95% CI 1.74–21.63). Urinary incontinence was not related to the presence of a niche. Conclusions A niche is present in 64.5% of women 6–12 weeks after caesarean section, when examined by GIS. Postmenstrual spotting is more prevalent in women with a niche and in women with a residual myometrial thickness of <50% of the adjacent myometrium. Keywords Abnormal uterine bleeding, caesarean section, caesarean section scar, niche, postmenstrual spotting, ultrasonography. Please cite this paper as: van der Voet LF, Bij de Vaate AM, Veersema S, Bro¨lmann HAM, Huirne JAF. Long-term complications of caesarean section. The niche in the scar: a prospective cohort study on niche prevalence and its relation to abnormal uterine bleeding. BJOG 2014;121:236–244. Introduction Concern regarding the association between delivery by cae- sarean section and long-term maternal morbidity is grow- ing, as the rate of caesarean section continues to increase. In the Netherlands the caesarean section rate increased from 7.4 to 15.8% during the period 1990–2008,1 and in the USA it increased from 21.2 to 32.8% from 1990 to 2011.2 The long-term complications of caesarean section in relation to future reproduction have been comprehensively examined.3,4 In the past decade several articles have described a defect that can be seen on ultrasound at the site of the caesarean section scar, known as a ‘niche’.5,6 A niche is defined as a triangular anechoic structure at the site of the scar or a gap in the myometrium of the anterior lower uterine segment at the site of a previous caesarean section.7,8 Niche prevalence depends on the method used for evaluation and the population investigated.9–16 In non-pregnant women the scar is visible with transvaginal ultrasonography (TVU) and contrast sonohysterography using either saline (saline infusion sonohysterography, SIS) or gel (gel instillation sonohysterography, GIS).5,6 There 236 ª 2013 Royal College of Obstetricians and Gynaecologists DOI: 10.1111/1471-0528.12542 www.bjog.org General gynaecology
  • 2. have been several reports of an association between abnor- mal bleeding and a niche.8,10–12,15 In particular, postmen- strual spotting seems to be a predominant symptom in women with a niche10,11 ; however, most of these studies included symptomatic patients, resulting in a possible selec- tion bias. Given the proximity of the niche to the bladder, it has been postulated that the local accumulation of fluid and scarring might disturb bladder function11 ; however, prospective studies assessing both bleeding symptoms and urinary symptoms in relation to the presence of a niche in a random population of women with a history of caesarean section are scarce. As far as we are aware, none of the reported studies asked women to participate at the time of caesarean section. The aim of our study was to determine the prevalence of niches in the caesarean section scar in a random population of women enrolled immediately after caesarean section, using both TVU and GIS 6–12 weeks after caesarean section, and to examine the relationship between the niche and postmenstrual spotting and urinary incontinence. Methods Study design and population We conducted a prospective observational cohort study. The trial was registered in the Dutch trial register (trial number NTR-2887). The study was performed in St Anto- nius Hospital, Nieuwegein: a teaching hospital in the Neth- erlands. The protocol was approved by the local medical ethics committee (VCMO NL18722.100.07 R-07.14A/ SCAR.). Participants were recruited between November 2007 and September 2010. Specially trained midwives asked all women over 18 years of age who underwent a caesarean section at St Antonius Hospital during the inclusion period to participate, within 3 days of the caesarean section. Exclusion criteria were twin pregnancies, known uterine anomalies, or the suspicion of a uterine infection, defined as a positive culture or fever and abdominal pain with dis- charge. After providing written informed consent, all par- ticipants were evaluated by TVU followed by GIS 6– 12 weeks after the caesarean section. A GIS was not per- formed when there were suspected placental remnants, intrauterine haematomas, intrauterine fluid accumulation, or a possible pregnancy (i.e. a visit during the midluteal phase in women not using adequate contraception). Women were followed by questionnaires and menstruation score charts at 6–12 weeks, 6 months, and 12 months after the caesarean section. Transvaginal ultrasound All TVU and GIS procedures were performed at St Antonius Hospital by three experienced examiners (L.V., S.V., and M.S.). TVU was performed using a 7.5–MHz transducer (Philips Sonicare HD 11.XE, Philips Medical Systems, Eindhoven, the Netherlands). Women were exam- ined after emptying their bladder. The uterus, uterine scar, and niche, if present, were examined in a standardised way. The position, length, and width of the uterus and double thickness of the endometrium were registered in the mid- sagittal plane. A niche was defined as an anechoic space (with or without fluid) at least 2 mm deep at the presumed site of the caesarean section scar. The uterus was screened for the presence of caesarean section scar(s) using parallel sagittal planes going from left to right, until the plane with the largest niche depth was defined. The uterus was also scanned in the transverse plane. When a niche was identi- fied, it was measured in the sagittal plane in which the niche had the greatest depth; the depths of the niche and of the residual myometrium at the site of the scar and of the adjacent normal myometrium were measured in real time (see Figure 1). In cases when more than one caesarean section scar was present the largest niche was measured. Gel instillation sonography A speculum was inserted and a catheter (SIS Rudigoz Cath- eter, CCD International, Paris, France) was placed inside the uterus. Gel (Endosgel, Farco-Pharma GmbH, K€oln, Germany) was flushed inside the uterine cavity and cervix while retracting the catheter. A maximum volume of 10 cm3 was instilled, or less if uterine cramps occurred or reflux was observed from the cervix. The speculum was removed, the vaginal probe was reinserted, and the pres- ence of a niche was recorded in the sagittal plane where the niche had the greatest depth. Niche characteristics were measured and recorded as described above (Figure 1). The shape was classified according to the previous classifications published by Bij de Vaate et al.11 The presence of uterine polyps, fibroids, or other intrauterine abnormalities was noted. Sagittal plane 1 2 3 RM AMT Figure 1. Schematic presentation of niche measurement. The following measurements were performed: (1) niche depth (in the sagittal plane); (2) residual myometrium (RM), from the serosal surface of the uterus (without the white lining of the serosa) to the apex of the niche, perpendicular to the endometrium (in sagittal plane); (3) adjacent myometrial thickness (AMT). Adapted from Bij de Vaate et al.11 237ª 2013 Royal College of Obstetricians and Gynaecologists Niche prevalence and abnormal uterine bleeding
  • 3. Data collection The characteristics of participants, including contraceptive use, breastfeeding, bleeding characteristics before preg- nancy, and detailed obstetric history (dates of previous caesarean section, indication, and characteristics of the last pregnancy and caesarean section) were noted immediately after informed consent was given. Current contraceptive use and bleeding pattern were recorded at 6–12 weeks after the caesarean section. Women completed and returned a questionnaire at 6 and 12 months after the caesarean sec- tion. The questionnaire included questions on current medication or contraceptive use, breastfeeding, bleeding pattern (including duration of menstruation, postmenstrual spotting, vaginal discharge, and urinary incontinence). They were also asked to complete a validated menstrual score chart: the Pictorial Blood Assessment Chart (PBAC).17 All data were recorded in a web-based database by two research nurses. The results of the ultrasound scans were not recorded in the case notes, and women and their doctors were not informed of the ultrasound findings. All women who underwent TVU were included in the analyses. Only women who underwent both TVU and GIS were included in the comparison of TVU and GIS measurement outcomes. The primary outcome was the prevalence of a niche as measured by TVU and GIS 6–12 weeks after caesarean sec- tion. Secondary outcome measures included details of the bleeding pattern, including postmenstrual spotting (defined as more than 2 days of brownish discharge after the end of the menstrual period), number of days of menstrual bleed- ing, urinary incontinence at 6 and 12 months after caesar- ean section, and the relationship of these with a niche, and niche characteristics (i.e. depth, residual myometrium, and the ratio of the residual myometrium divided by the total thickness of the adjacent anterior myometrium), identified by TVU and GIS. Statistical analyses Data were analysed using the SPSS 20 (SPSS Inc., Chicago, IL, USA). Differences in baseline characteristics were com- pared using the chi-square test, Fisher’s exact test, Student’s t–test, or the Mann–Whitney U–test, depending on the type and distribution of the variables. Logistic regression analysis was planned to analyse the relationship between the presence of a niche and postmenstrual spotting. Potential confounding factors were predefined, and included age, breastfeeding, body mass index (BMI), BMI above 25 kg/m2 , oral contraceptive use, and use of the levonorgestrel intrauterine system (LNG-IUS). These poten- tial confounding factors were tested using univariate analysis. All tests were two-sided. A two-tailed P < 0.05 was considered to be statistically significant. Results Between November 2007 and September 2010, 350 women gave informed consent to participate in the study within 3 days of their caesarean section at St Antonius Hospital. Of these, 276 were willing to receive a TVU at 6–12 weeks, and 263 women could be included. TVU was used to examine 263 women, and 197 underwent both TVU and GIS (see Figure 2). Two women underwent a second cae- sarean section during the study period, but only the results of the first caesarean section and the related TVU and GIS were included in the study. TVU and GIS were performed at a mean of 7.6 Æ 1.7 (SD) weeks after caesarean section. In total, 72% (191/263) of all women who underwent a TVU completed the questionnaire at 6 months, and 69% (172/249) of the women who received a questionnaire at 12 months after the caesarean section completed it. Of all the women who completed the questionnaire at 12 months, 45 were pregnant again. Of the women who underwent both a TVU and GIS the response rate was 73% at 12 months. Baseline characteristics and sonography results at 6–12 weeks after caesarean section are shown in Table 1. The majority of the women (71%) analysed had had only one previous caesarean section. Sixty-four (24%) had had two and eleven (4%) had had three previous caesarean sec- tions. One caesarean section was carried out by a J–shaped or ‘hockey stick’ incision. All other women had a transverse lower segment incision. The uterus was closed in two layers in four women and in one layer in all others. Most caesar- ean sections (55%) were performed because of an emer- gency. During the sonographic evaluation at 6–12 weeks after caesarean section, 55% of the women were breastfeed- ing and 77% were amenorrhoeic. At 6–12 weeks, the women reported using the following methods of contracep- tion: no contraception, 36%; oral contraceptives, 10%; pro- gesterone only pill, 3%; sterilisation, 4%; condoms, 42%; and other, 5%. The difference in contraceptive use was not statistically significant between patients with or without a niche. There were no differences regarding the rate of primary or emergency caesarean section, age, or parity between women who were included in our analyses and those who refused to participate, those who did not undergo a GIS, or those who did not complete the questionnaire at 12 months. Niche prevalence and characteristics Niche prevalence was 49.6% when evaluated by TVU and 64.5% when evaluated by GIS. In three women it was not possible to identify the scar in the uterus with TVU. With GIS all scars were visible. In women with one caesarean section, 62% who underwent GIS had a niche, compared 238 ª 2013 Royal College of Obstetricians and Gynaecologists van der Voet et al.
  • 4. with 68.2% of women with two caesarean sections and 77.8% of women with three caesarean sections. Sonograph- ic characteristics of the uterus are shown in Tables 1 and 2. The length and width of the uterus were no different between women who had or did not have a niche. The niche was deeper when examined by GIS than by TVU (2.32 Æ 3.35 and 3.03 Æ 3.1 mm, respectively; P < 0.001). The thickness of the residual myometrium at the site of the uterine scar was approximately 2 mm less in women with a niche compared with those without a niche, as measured by TVU and GIS (P < 0.001 and P = 0.005, respectively; see Table 1). The mean ratio between the thickness of the residual myometrium at the site of the niche and the thick- ness of the adjacent myometrium was 0.74 Æ 0.58 in all women who underwent GIS. The ratio was <0.5 in 22% of these women. Most niches detected by GIS had a semicir- cular shape (55%); 24% had a triangular shape, 10% had a droplet shape, 6% were inclusion cysts, and 7% had another shape. Bleeding pattern and urological symptoms The questionnaire at 6 months was completed by 191 women. Information on the menstrual cycle was available for only 59 women. Given the large proportion of women who were still breastfeeding or who did not yet have a regular menstrual cycle we decided not to analyse the outcomes at 6 months. The questionnaire at 12 months was completed by 172 women. The menstrual pattern could not be analysed in 45 of these women because of a subsequent pregnancy. Ten of these women completed the information on the basis of their menstruation pattern before pregnancy. Information on the menstrual cycle and contraceptive use was available for 137 women, of whom 17 were amenorrhoeic because of LNG-IUD or another hormonal contraceptive. Postmenstrual spotting was reported by 13 out of 45 (28.9%) women with a niche detected by GIS, compared with two women out of 29 (6.9%) without a niche detected by GIS (OR 5.48, 95% CI 1.14–26.48; Table 3). Including only primiparae, again post- menstrual spotting was reported more frequently in women with a niche detected by both TVU or GIS compared with those without a niche (31 versus 4% for TVU and 32 versus 0% for GIS; OR 9.7, 95% CI 1.1–85.6). Women with a ratio of residual myometrium of less than half of the adjacent myometrium (ratio <0.5) measured by TVU or GIS reported postmenstrual spotting more often than women with a ratio of >0.5 (OR 7.2, 95% CI 1.74–21.62, and OR 6.1, 95% CI 1.94–26.70, respectively; Table 4). Excluded (n = 87): • Women not willing to undergo TVU at 6–12 weeks after caesarean (74) • Twin pregnancy (6) • Uterus anomaly (1) • New pregnancy (2) • >12 weeks after caesarean (1) • Pelvic inflammatory disease (1) • Woman’s second caesarean during study period (2) Transvaginal ultrasound (TVU) (n = 263) Excludedfrom GIS ( n = 66): • Placental remnant/haematoma (8) • Pelvic inflammatory disease (6) • Woman's request (6) • Unprotected intercourse (3) • Failed GIS (no distension) (11) • Failed GIS (pain) (12): • Intrauterine fluid (13) • Other (7) Gel instillation sonography (GIS) (n = 197) Questionnaire completed 12 months after caesarean section (n = 172) Non-responders (77) Lost to follow-up (14) • Incorrect address/moved (12) • Refusal to continue the study (2) Women willing to participate (n = 350) Figure 2. Flow diagram of study participants. 239ª 2013 Royal College of Obstetricians and Gynaecologists Niche prevalence and abnormal uterine bleeding
  • 5. Using univariate analyses none of the predefined con- founding factors or baseline characteristics were related to postmenstrual spotting: all had P > 0.1 (LNG-IUD use, P = 0.11; oral contraceptive use, P = 0.24; breastfeeding, P = 1.0; age, P = 1.0; BMI, P = 1.0; BMI > 25 kg/m2 , P = 0.40), and therefore the planned logistic regression was not performed. We did not find any significant differences between women with or without a niche concerning the existence of (combined) urinary incontinence, urge inconti- nence, or stress incontinence (see Table 3). Discussion Main findings All caesarean section scars could be identified using GIS. Using this technique the prevalence of niches at the site of these caesarean section scars was high (64.5%) in a random population. Comparing the results of GIS with TVU, niche prevalence was higher, measured niche depth was greater, and residual myometrium was thinner when detected by GIS. Postmenstrual spotting 1 year after caesarean section was strongly related to the presence of a niche detected by both TVU and GIS. One out of three women with a niche detected by GIS reported postmenstrual spotting, compared with one out of ten women without a niche. Postmenstrual spotting was related to a residual : adjacent myometrium ratio of <50%, which might indicate that this is a relevant parameter for niche size. The prevalence of urinary inconti- nence was not related to the presence or absence of a niche. Table 2. Comparison of transvaginal ultrasound and gel instillation sonohysterography results (n = 197)* TVU GIS P (95% CI) Niche depth of all women, mean (ÆSD)** 2.32 (Æ3.35) 3.03 (Æ3.1) <0.001 (0.38–1.02) Niche depth of women with niche on GIS, mean (ÆSD)** 3.43 (Æ3.67) 4.77 (Æ2.64) <0.001 (0.92–1.79) Residual myometrial thickness of all women, mean (ÆSD) 9.58 (Æ4.39) 9.11 (Æ3.8) 0.06 (–0.24 to 0.96) Residual myometrial thickness of women with niche on GIS, mean (ÆSD) 9.30 (Æ4.67) 8.59 (Æ3.75) 0.03 (0.09–1.38) *Of the 263 women in total, only the 197 women who underwent both TVU and GIS were included in this table. **Niche depth was recorded as 0 when no niche was observed. Table 1. Characteristics of the study participants All women (n = 263) Niche (TVU) (n = 129) No niche (TVU) (n = 131) P* Niche (GIS) (n = 127) No niche (GIS) (n = 70) P** Baseline characteristics Age (years), mean (ÆSD) 32.46 (Æ4.15) 32.66 (Æ4.16) 32.26 (Æ4.15) 0.44 32.51 (Æ4.11) 32.73 (Æ3.85) 0.72 Parity, mean (ÆSD) 1.54 (Æ0.70) 1.55 (Æ0.73) 1.54 (Æ0.68) 0.96 1.57 (Æ0.78) 1.50 (Æ0.68) 0.52 BMI (kg/m2 ), mean (ÆSD) 25.70 (Æ5.58) 26.15 (Æ5.48) 25.28 (Æ5.66) 0.28 25.98 (Æ5.83) 24.98 (Æ5.19) 0.29 Number of caesarean sections, mean (ÆSD) 1.33 (Æ0.56) 1.35 (Æ0.57) 1.31 (Æ0.54) 0.55 1.35 (Æ0.59) 1.26 (Æ0.50) 0.26 Visit at 6–12 weeks after caesarean section Weeks after caesarean section, mean (ÆSD) 7.58 (Æ1.74) 7.40 (Æ1.40) 7.74 (Æ2.01) 0.12 7.66 (Æ1.77) 7.72 (Æ1.92) 0.82 Breastfeeding, number (percentage)*** 142 (55%) 67 (52%) 75 (Æ59%) 0.38 64 (53%) 41 (61%) 0.29 Ultrasonographic results at 6–12 weeks after caesarean section Double endometrial thickness TVU (mm), mean (ÆSD) 5.49 (Æ3.80) 5.61 (Æ3.85) 5.36 (Æ5.77) 0.61 5.36 (Æ3.57) 4.86 (Æ3.33) 0.34 Uterus length TVU (cm), mean (ÆSD) 7.18 (Æ1.43) 7.29 (Æ1.52) 7.07 (Æ1.32) 0.23 7.09 (Æ1.38) 7.11 (Æ1.47) 0.92 Uterus width TVU (cm), mean (ÆSD) 4.23 (Æ0.94) 4.26 (Æ0.81) 4.19 (Æ1.07) 0.59 4.27 (Æ0.84) 4.17 (Æ1.20) 0.49 Thickness of myometrium at site of caesarean section scar (mm), mean (ÆSD) 9.59 (Æ4.18) 8.51 (Æ3.90) 10.73 (Æ4.18) <0.001 8.59 (Æ3.81) 10.20 (Æ3.59) 0.005 *P value between niche and no niche during TVU. **P value between niche and no niche during GIS. ***No information on breastfeeding for 13 patients at 6–12 weeks after caesarean section. 240 ª 2013 Royal College of Obstetricians and Gynaecologists van der Voet et al.
  • 6. Strengths and limitations of the study To the best of our knowledge this is the first study that has recruited participants at a very early stage after their caesarean section (within 3 days), followed by early exami- nation (within 3 months) by both TVS and GIS, and with the sequential completion of menstrual questionnaires up Table 3. Uterine bleeding pattern and urological symptoms at 12 months after caesarean section Niche (TVU) No niche (TVU) P* Niche (GIS) No niche (GIS) P** OR (95% CI) No. of women with postmenstrual spotting (n = 91/74)*** 13 (26) 5 (12) 0.10 13 (28.9) 2 (6.9) 0.02 5.48 (1.14–26.48) Days of blood loss during menstruation, mean (ÆSD) (n = 91/83)*** 5.9 (2.57) 6.1 (2.84) 0.75 5.5 (Æ2.1) 5.5 (Æ1.4) 0.98 No. of women with vaginal discharge (n = 137/98)*** 11 (14) 11 (18) 0.84 7 (11) 8 (23) 0.15 No. of women taking oral contraceptives (n = 137/109)*** 19 (25) 13 (21) 0.61 19 (28) 10 (24) 0.82 No. of women with LNG-IUD (n = 137/109)*** 9 (12) 8 (13) 0.82 10 (15) 2 (5) 0.21 No. of women with amenorrhoea (n = 137/109)*** 12 (16) 5 (8) 0.18 9 (13) 3 (7) 0.53 No. of women with incontinence (n = 115/90)*** 20 (31) 17 (34) 0.71 19 (33) 10 (29) 0.82 No. of women with stress incontinence (n = 115/90)*** 15 (23) 11 (22) 0.89 14 (25) 6 (17) 0.45 No. of women with urge incontinence (n = 115/90)*** 4 (6) 3 (6) 0.97 2 (4) 2 (6) 0.63 No. of pregnant women (n = 260/197)*** 17 (13) 28 (21) 0.08 21 (16.5) 15 (21) 0.40 No. lost to follow–up/non-responders (n = 263/197) 42 (33) 49 (37) 0.41 45 (35) 18 (26) 0.16 Total (n = 260/197)*** 129 (49.6) 131 (50.4) 127 (64.5) 70 (35.5) Data are presented as number (%), unless indicated with mean (ÆSD). Three women for whom the presence of a niche could not be determined were excluded. *P value between niche and no niche during TVU. **P value between niche and no niche during GIS. ***Number of women who completed the questionnaire for a specific parameter and who underwent TVU/GIS, respectively. Table 4. Niche characteristics in women with or without postmenstrual spotting (n = 91/74)* Postmenstrual spotting (TVU) (n = 18) No postmenstrual spotting (TVU) (n = 73) P (OR, 95% CI)** Post-menstrual spotting (GIS) (n = 15) No postmenstrual spotting (GIS) (n = 59) P (OR, 95%CI)*** Niche depth (mm), mean (ÆSD) 5.46 (Æ2.50) 5.15 (Æ2.77) 0.72 5.45 (Æ2.76) 4.86 (Æ2.50) 0.47 Residual thickness of myometrium at the site of the caesarean scar (mm), mean (ÆSD) 8.92 (Æ4.76) 9.31 (Æ4.28) 0.73 8.19 (Æ5.06) 9.22 (Æ4.11) 0.40 No. of women with ratio RM/AM <50% **** (TVU n = 69; GIS n = 73) 8 (61%) 10 (18%) 0.03 (7.2,1.94–26.70) 8 (57%) 10 (18%) 0.005 (6.13,1.74–21.63) Mean ratio RM/ AM**** 0.50 0.72 0.008 0.53 0.70 0.03 AM, adjacent myometrium; RM, residual myometrium. *Number of women who completed the postmenstrual spotting questionnaire and who underwent TVU/GIS, respectively. All patients who completed the questionnaire on postmenstrual spotting were included. **P value between patients with and without postmenstrual spotting who underwent TVU. ***P value between patients with and without postmenstrual spotting who received a GIS. ****Ratio RM/AM = residual myometrial thickness at the site of the caesarean scar/myometrial thickness of the adjacent myometrium, presented in numbers (percentage). 241ª 2013 Royal College of Obstetricians and Gynaecologists Niche prevalence and abnormal uterine bleeding
  • 7. to 1 year after the caesarean section. Only two prospective studies have evaluated niches in an unselected popula- tion.11,18 Both these studies recruited patients at 6–12 months after caesarean section. The Bij de Vaate et al.11 study was carried out by our study group, but in a different population and with the examinations performed by a different examiner. In the present study, early scan- ning (3 months after the caesarean section) meant that the vast majority of the women were still amenorrhoeic, so the influence of abnormal uterine bleeding on the willingness of women to participate (selection bias) is expected to be limited. An additional advantage of early sonographic eval- uation is that, because of amenorrhoea in most patients, the potential confounding effect of variations in timing of the measurements during the menstrual cycle and related endometrial thickness is limited. In addition, women were consecutively asked to participate by research midwives, and the registration of the results was independent of clini- cal considerations. Women and their doctors were not informed whether or not a niche was observed to prevent possible bias in reporting their bleeding pattern. Although complete post-caesarean section scar healing may take up to 6 months,6 we do not know the exact time needed to develop a niche. We defined a niche as an anechoic space (with or without fluid) with a depth of at least 2 mm at the presumed site of the caesarean section scar. This should not be confused with the caesarean section scar itself. As demonstrated in this study, a scar is almost always visible and is reflected as a hypoechoic indentation of the myome- trium at the location of the caesarean section. We expect the uterine scar to continue to heal beyond 6–12 weeks, and this might differ in performance with time. However, we consider it very unlikely that niches (i.e. discontinua- tions and fluid-stained spaces in the myometrium) will heal after this period. However, changes in a niche over time are not unlikely. Sustained accumulation of fluid may, in theory, increase niche size over time, but no data are cur- rently available to confirm this theory. A possible limitation of our study is that not all women who were delivered by caesarean section during the study period were asked to participate. Women were asked con- secutively by trained midwives during their day and night shifts, but these midwives were not always present. Because the absence of the midwives was randomly distributed over the week, we consider this potential effect on selection bias to be minor. This is underlined by the lack of differences in baseline characteristics between women who were asked to participate and those who were not, with regards to elective or emergency caesarean section, age, and parity. In addition, we did not observe any differences in these parameters between included and excluded women, or those who were not willing to undergo a GIS or who did not complete the questionnaire. Patients with a previous twin pregnancy or a known uterine anomaly were excluded in order to assemble a homogeneous group and to prevent undesired effects of unknown confounding factors; however, whether these fac- tors would in fact introduce significant confounding effects is a topic for further discussion. We also decided not to perform a GIS in patients with a placental remnant, haematoma, or fluid in the uterine cavity detected by TVU. Consequently, a relatively small proportion of all patients who provided informed consent were analysed. Whether it is correct to exclude women with intrauterine fluid collec- tion from examination by GIS should be further discussed. This was decided before the start of the study, and was included in the study protocol; however, it can be postu- lated that this group might have been particularly symp- tomatic and prone to postmenstrual spotting. We could not observe any relationship between niches and urinary incontinence, but we did not report other urinary symp- toms, such as urgency. An additional shortcoming of the study is that we did not measure the niche width in the sagittal plane or the niche length in the transverse plane, as recently proposed by Naji et al.5 (our study had already begun before that publication). Therefore, we could not analyse the relationship between these parameters and niche symptomatology. We also did not determine the reproducibility of our measurements. Clinical implications of the findings and relation to published data We were able to identify the caesarean section scar with GIS in 100% of the women. This is in line with another study examining women within 3 months of a caesarean section.19 The observed niche prevalence rate of 49.6% using TVU is comparable with the reported prevalence (42%) in a prospective cohort study of an unselected population.9 Different prevalence rates (28 and 61%) were reported in prospective studies in populations evaluated at 6 months and at 6–12 months after a caesarean section.11,13 Different definitions of a niche and different timing after the caesar- ean section may both affect the niche detection rate. Vikhareva Osser et al.13 used the definition ‘any visible defect’, and Bij de Vaate et al.11 used ‘any indentation of at least 1 mm’. We used a cut-off level of 2 mm; however, consensus on the exact cut-off levels is lacking. Early scan- ning may facilitate the recognition of the location of the caesarean section scar in the uterine wall as a result of incomplete scar healing, and this may increase the detection of small niches. In addition, the related thin endometrium resulting from breastfeeding in the majority of the women may also improve niche recognition and measurement. We used the same terminology as that suggested by Naji et al.,5 and measured the depth and residual myometrial thickness in the sagittal plane as described. Niche 242 ª 2013 Royal College of Obstetricians and Gynaecologists van der Voet et al.
  • 8. prevalence using GIS was 64.5% in our study, which is comparable with the reported prevalence using GIS or SIS in random, unselected populations (56, 59.5, 59, and 78%).10,11,14,18 Niche prevalence was higher using GIS than with TVU only. These findings are in line with the reported findings of three studies comparing GIS or SIS with TVU.10,11,18 These studies showed a higher niche prevalence with sonohysterography than with TVU without contrast, and thus GIS may be more accurate at detecting niches. Although the niches that were detected using GIS but were missed using TVU were smaller than those detected by both TVU and GIS, they can be clinically relevant. This is underlined by the strong relationship we found between postmenstrual spotting and niches on GIS.11 An additional argument for using GIS rather than TVU is that the resid- ual myometrium measured using GIS was significantly thinner. The residual myometrium is considered to be the main limiting factor for eventual hysteroscopic niche resec- tions to treat related bleeding symptoms. Most publications report a required residual myometrium of 2–3 mm for hysteroscopic niche resection, given the risk of perforation and/or bladder injury.20 In order to prevent undesired complications during hysteroscopic niche resections we propose that a GIS or SIS be used rather than TVU for the preoperative evaluation of the residual myometrium. Sev- eral previous studies indicated a relationship between large niches and postmenstrual spotting. Bij de Vaate et al.11 reported the niche volume to be related to postmenstrual spotting. We were not able to calculate niche volume because of the lack of stored three-dimensional volumes. In order to assess the relationship between large niches and postmenstrual spotting, we decided not to take an absolute measurement of residual myometrium, but to relate it to the adjacent myometrium. We defined large niches as those with a residual myometrium with thickness of <50% of that of the adjacent myometrium. This parameter was sig- nificantly related to postmenstrual spotting. This parameter and cut-off level were also used by Ofilli-Yebovi et al.,15 who reported a high prevalence of women with a ratio of less of than 50% in a population with gynaecological symp- toms. A potential relationship between niche size and post- menstrual spotting is in line with the hypothesis that spotting is induced by the accumulation of blood inside the niche.6,7 A depth of more than half the myometrial thickness makes the anterior part of the niche possibly large enough to obstruct the direct outflow of menstrual blood. This, in combination with lower contractility as a result of fibrosis, may induce the accumulation of blood in a niche. One out of three women with a niche observed by GIS reported postmenstrual spotting. This is in line with the pre- vious reported prevalence of postmenstrual spotting in patients with a niche.10,11 Given the high prevalence of post- menstrual spotting after caesarean section, this should be part of routine counselling before elective caesarean section. Future perspectives Future research should focus on the relationship of niches to subsequent fertility, obstetric complications such as uter- ine rupture, and on the impact of a niche on a woman’s well-being. There is a lack of information on the impact of niche-related bleeding disorders on women’s quality of life, their sexual function, and their willingness to undergo treatment for related symptoms. Conclusion In conclusion, the caesarean section scar was visible in all women at 6–12 weeks after caesarean section using GIS. The prevalence of niches detected by GIS is high after caesarean section (64.5%), and more niches are detected using GIS than using TVU, with a larger observed niche size and reduced residual myometrial thickness. The presence of a niche is related to postmenstrual spotting. Postmenstrual spotting is more frequent in patients with large niches (defined as a residual myometrium of thickness <50% of that of the adjacent myometrium) than in patients with smaller niches. Disclosure of interests None of the authors have any relevant financial, personal, political, or religious interest linked to the subject of this article. Contribution to authorship The study was conceived by L.V., J.H., H.B., and S.V., and L.V. and S.V. performed the ultrasounds and collected the data. Analysis of the data was performed by L.V. and J.H. The first draft was written by L.V. and J.H. S.V., H.B., and A.B. helped to supervise the article up to the final draft. Details of ethics approval The study received ethics approval from the united com- mittee on research involving human subjects (VCMO), Nieuwegein, the Netherlands (27 September 2007; ref. no. NL18722.100.07 R-07.14A/SCAR). Funding No benefits in any form have been received or will be received from a commercial party related directly or indi- rectly to the subject of this article. Acknowledgements We thank K.W. Van den Berg-Swart and C. van Dam-Bou- rens, research nurses, for recording all the collected data in the database. We thank M. Stigter-de Vries MD for performing the ultrasounds. & 243ª 2013 Royal College of Obstetricians and Gynaecologists Niche prevalence and abnormal uterine bleeding
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