Original papers

Impact of selected risk factors on uterine healing after

cesarean section in women with single-layer uterine closure:
A prospective study using two- and three-dimensional
transvaginal ultrasonography
Joanna Budny-WińskaA–D, Aleksandra Zimmer-StelmachB,C, Michał PomorskiD–F
2nd Department of Gynecology and Obstetrics, Wroclaw Medical University, Poland

A – research concept and design; B – collection and/or assembly of data; C – data analysis and interpretation;
D – writing the article; E – critical revision of the article; F – final approval of the article

Advances in Clinical and Experimental Medicine, ISSN 1899–5276 (print), ISSN 2451–2680 (online) Adv Clin Exp Med. 2022;31(1):41–48

Address for correspondence

Joanna Budny-Wińska
Abstract
E-mail: [Link]-winska@[Link] Background. Modern obstetrics must meet many challenges, including long-term complications resulting
from the presence of a uterine niche after cesarean section.
Funding sources
None declared Objectives. To assess the impact of selected risk factors on the uterine healing process after cesarean section.
The uterus was closed with a single-layer continuous suture covering the entire thickness of the myometrium,
Conflict of interest excluding the decidua.
None declared
Materials and methods. A prospective, case-controlled study was carried out at 2nd Department of Gy-
necology and Obstetrics, Wroclaw Medical University, Poland. Women who delivered by cesarean section
Received on June 20, 2021 at our Department were invited to undergo an ultrasonographic assessment of the cesarean section scar
Reviewed on August 11, 2021
Accepted on September 22, 2021
from 6 to 9 weeks after the procedure. In all cases, the uterus was closed with a single-layer continuous
suture. The ultrasound examination of the niche was performed according to the modified Delphi protocol.
Published online on November 4, 2021 The volume of the niche was calculated and a 3D model was created. The obtained data were analyzed with
clinical information from the maternal medical history and the course of the pregnancy.
Results. A total of 204 patients participated in the study. Five patients had a residual myometrial thick-
ness (RMT) <2.2 mm and 35 had a residual myometrial thickness to adjacent myometrial thickness ratio
(RMT/AMT) ≤0.5. In 45% of women, pregnancy course was complicated by gestational diabetes mellitus
(GDM), gestational hypertension and hypothyroidism. The cervical canal was colonized with pathogenic flora
in 22% of women. No correlation between maternal and gestational age at delivery, presence of medical
complications during pregnancy, colonization of the cervical canal, and presence of niche and its parameters
were found.
Cite as
Budny-Wińska J, Zimmer-Stelmach A, Pomorski M. Impact Conclusions. Our study revealed that the selected risk factors, such as systemic diseases during pregnancy
of selected risk factors on uterine healing after cesarean and in the maternal medical history, as well as the colonization of the cervical canal, have no impact on uterine
section in women with single-layer uterine closure: scar healing in women undergoing single-layer uterine closure spanning the entire thickness of the myo-
A prospective study using two- and three-dimensional
transvaginal ultrasonography. Adv Clin Exp Med. metrium, excluding the decidua.
2022;31(1):41–48. doi:10.17219/acem/142519
Key words: 3D ultrasonography, cesarean scar niche, risk factors of cesarean scar niche, systemic diseases
DOI during pregnancy, single-layer suture
10.17219/acem/142519

Copyright
Copyright by Author(s)
This is an article distributed under the terms of the
Creative Commons Attribution 3.0 Unported (CC BY 3.0)
([Link]
42 J. Budny-Wińska, A. Zimmer-Stelmach, M. Pomorski. Uterine healing after cesarean section

Background as directly life-threatening conditions (uterine rupture,

cesarean scar pregnancy).6,14–17 Additionally, cesarean scar
Modern obstetrics must meet many challenges, in- niches may increase the risk of complications in gyneco-
cluding the increased frequency of cesarean sections and logical procedures such as embryo transfer and intrauter-
long-term complications resulting from the presence ine device placement and removal.18,19
of a uterine niche after cesarean section. Additionally, Due to the potentially dangerous consequences result-
worldwide, there has been an increased incidence and ing from the presence of a uterine niche after cesarean
prevalence of systemic diseases appearing in pregnancy, section, it is necessary to develop preventive strategies
such as gestational hypertension and gestational diabetes aimed at reducing the risk of isthmocele formation, and
mellitus (GDM).1,2 The another challenge for obstetricians thus preventing adverse outcomes. To achieve this, it is es-
is the increased rate of pregnancy among older women3,4 sential to identify related risk factors for the formation
due to the sociocultural changes in family planning that of a uterine niche after cesarean section, and to develop
leads to the postponement of maternal plans, as well appropriate diagnostic and therapeutic protocols. There-
as the improved availability and effectiveness of assisted fore, in the past several years, numerous studies have been
reproductive methods. published concerning the uterine scar niche, but most
The consequence of cesarean section is a scar formation of them have been performed using selected populations
within the uterine muscle. In recent years, the rate of deliv- of symptomatic women.
eries by cesarean section has increased all over the world.
In Poland, the rate of cesarean section is 44.8% (data from
Statistics Poland for 2019). The World Health Organiza- Objectives
tion (WHO) recommends an ideal cesarean section rate
of 10–15% of all births. This percentage is associated with This study aimed to assess the impact of the most
a decrease in maternal and neonatal mortality. Above this common risk factors in obstetrics on the uterine heal-
level, the increased incidence of cesarean delivery is no ing process after cesarean section, using a prospectively
longer associated with reduced mortality.5 collected and unselected population, in which the uterus
With rising cesarean rates, the incidence of cesar- was closed with a single-layer continuous suture cover-
ean-related iatrogenic complications is also on the rise. ing the entire thickness of the myometrium, excluding
In cases of incomplete healing, a niche can develop within the decidua.
the scar.
Various imaging methods including two- and three-
dimensional ultrasonography, sonohysterography, hys- Materials and methods
terography, hysteroscopy, and magnetic resonance im-
aging (MRI) can be used to assess the anterior uterine Study design
wall and to diagnose a cesarean scar niche.6–8 Despite
the availability of various diagnostic methods, there are This prospective descriptive study was designed to as-
no clear diagnostic criteria for uterine niches after ce- sess the prevalence and risk factors for improper uterine
sarean section. In 2019, the European Niche Taskforce healing after cesarean delivery and niche formation. This
defined a uterine niche as an indentation of at least 2 mm study is a continuation of our previous research, in which
in the uterine myometrium at the site of the cesarean we assessed the impact of mode and number of previous
scar, assessed using transvaginal ultrasound.9 The in- cesarean sections, type of uterine incision expansion,
cidence of uterine niches varies widely in the literature, operator’s experience, uterine flexion, and stage of labor
ranging from 24% to 84%.10–13 at the time of cesarean section on uterine healing.20
Differences in the frequency of uterine niches result from
the use of different diagnostic criteria, the time elapsed Setting and participants
after the cesarean procedure and the diagnostic method
used. The incidence is often underestimated because many The study was carried out at 2nd Department of Gynecol-
women are asymptomatic and clinicians may not consider ogy and Obstetrics, Wroclaw Medical University, Poland.
a niche as a cause of a patient’s symptoms, due to lack The study protocol was accepted by the ethics commit-
of awareness.8 tee (approval No. KB 221/2016 and No. KB 153/2020) and
Most of the small uterine niches after cesarean section all participants signed an informed consent form before
are asymptomatic and do not pose a threat to the health participating in the study. The study was conducted in ac-
or life of the patient. However, the consequences of cordance with the 1964 Declaration of Helsinki and its
the presence of the large and symptomatic cesarean scar later amendments.
niche include uterine bleeding, chronic pelvic pain, re- Women who delivered by cesarean section at our De-
duced fertility, complications in subsequent pregnancies partment from 2017 to 2019 were invited to undergo
(morbidly adherent placenta, placenta previa), as well an ultrasonographic assessment of the cesarean section
Adv Clin Exp Med. 2022;31(1):41–48 43

scar. They were recruited either before the cesarean deliv- Inclusion and exclusion criteria
ery (elective surgery) or within 2 days after the operation
(emergency cesarean delivery). Patients who agreed to par- The inclusion criteria were low transverse uterine inci-
ticipate in the study were scheduled for the ultrasound sion, single-layer continuous full thickness uterine closure,
examination from 6 to 9 weeks after the cesarean section. uneventful postoperative course and singleton pregnancy.
The exclusion criteria included a vertical or inverted “T”
Surgical technique uterine incision, congenital uterine malformations and
the use of more than 3 additional hemostatic uterine sutures.
The cesarean section procedures were performed
by various obstetricians working in our Department using Statistical analyses
a standardized manner, i.e., low transverse uterine incision
with a single-layer continuous suture covering the entire Data were collected and recorded using an Excel spread-
thickness of the myometrium, excluding the decidua. All sheet. Statistical analyses were performed using the STA-
physicians used the same suture material (Surgicryl® 910 TISTICA v. 13.3 PL package (StatSoft Inc., Tulsa, USA).
polyglactine-braided synthetic absorbable suture; SMI AG, For quantitative variables, basic descriptive statistics
St. Vith, Belgium). were calculated (for all patients and taking into account
the assumed division into groups), while the frequency
Ultrasound examination of occurrence of their individual variants was calculated
for qualitative variables (also taking into account the as-
The examinations were conducted using a Voluson sumed division). The Mann–Whitney U test, post hoc
V8 Expert ultrasound machine (General Electric Medi- comparisons for the Kruskal–Wallis analysis of variance
cal Systems, Chicago, USA) with a 4–9 MHz transvaginal (ANOVA) test and non-parametric Spearman’s rank cor-
3D probe. All transvaginal ultrasound examinations were relation test were used in the analysis of non-parametric
performed by the first author, who was blinded to clini- data. The Pearson’s χ2 test and Fisher’s exact test were used
cal information. During the examination, the parameters to evaluate the differences in the distributions of qualita-
of the niche were assessed and a 3D model was created. tive variables. The criterion for statistical significance was
All data were saved on the internal hard drive of the ultra- set at a p-value <0.05.
sound machine. According to the international definition,
a niche was defined as an indentation in the myometrium
of at least 2 mm.9 All measurements were obtained on a sag- Results
ittal view of the uterus. To standardize the ultrasound eval-
uation, all examinations were performed using the modified A total of 204 patients participated in the study. The mean
Delphi protocol, and the exams performed prior to the pub- age was 32.25 years (standard deviation (SD) ±4.156) and
lication of the modified Delphi protocol were reloaded and the mean gestational age was 37.863 weeks (SD ±2.43).
recalculated in accordance with the guidelines.9 A total of 117 (57%) participants had no previous deliver-
The following niche parameters were assessed according ies. Of the 204 patients, 56 (27%) had at least 1 cesarean
to the modified Delphi protocol: width (W [mm]), height section in the past, while 32 (16%) had at least 1 previous
(D [mm]), volume of the anechoic triangle, residual myo- vaginal delivery. Eighty-two (40%) patients underwent
metrial thickness (RMT [mm]), and adjacent myometrial emergency cesarean delivery and 122 (60%) underwent
thickness (AMT [mm]). Additionally, the following param- elective cesarean delivery. The most common reasons for
eters were calculated: the RMT/AMT ratio, the RMT/W elective cesarean delivery were previous cesarean delivery
ratio and the RMT/D ratio. (40%) and breech presentation (9%). The most common
The VOCAL program was used to create 3D models reasons for emergency cesarean delivery were impending
and calculate the volume of the niche. The following set- fetal asphyxia (40%) and prolonged labor (17%).
tings were used: manual trace and rotation angle of 15°. Out of all examined women, 153 were diagnosed with
The boundaries of the anechoic niche were manually a niche after cesarean section (75%). Five of those patients
outlined on the touch screen of the Voluson V8 Expert had a RMT < 2.2 mm and 35 patients had an RMT/AMT
ultrasound machine. ratio of 0.5 or less. The mean RMT value in the study group
was 8.3 mm (SD ±3.37).
Clinical data analysis The course of pregnancy was uncomplicated by preg-
nancy-related systemic diseases in 55% (n = 112) of women.
Clinical information, such as laboratory results, ma- In this group, uterine scar niches were diagnosed after
ternal medical history pregnancy, and cesarean section cesarean section in 71% (n = 79) of patients. In contrast,
course, was collected from the medical record and ana- in 21 patients (10%) with GDM, a uterine niche was di-
lyzed after ultrasonographic assessment of the cesarean agnosed after cesarean section in 91% of these women.
section scar. In 11% of respondents, their pregnancy was complicated
44 J. Budny-Wińska, A. Zimmer-Stelmach, M. Pomorski. Uterine healing after cesarean section

Table 1. Comparison of the analyzed variables and the occurrence of uterine niche after the cesarean section
Chronic diseases
Gestational diabetes Gestational hypertension Culture of cervical canal
Variable in pregnancy
yes no yes no yes no negative positive
Niche, n (%) 75 (49) 78 (51) 18 (12) 135 (88) 14 (9) 139 (91) 92 (79) 24 (21)
Non-niche, n (%) 17 (33) 34 (67) 3 (6) 48 (94) 9 (18) 42 (82) 32 (76) 10 (24)
p-value* 0.0536 0.2949 0.1236 0.6665

*Fisher’s exact test.

Table 2. Characteristics of the parameters of the cesarean scar niche depending on the occurrence of systemic diseases during pregnancy and cervical
colonization (Mann–Whitney U test)
Chronic diseases Gestational Hypothyroidism Culture
Gestational diabetes
Variable in pregnancy hypertension in pregnancy of cervical canal
yes no yes no yes no yes no positive negative
Height [cm]
Mean (SD) 0.50 (0.24) 0.49 (0.20) 0.54 (0.24) 0.49 (0.22) 0.51 (0.33) 0.49 (0.21) 0.49 (0.21) 0.51 (0.23) 0.49 (0.18) 0.52 (0.23)
p-value 0.7150 0.5091 0.5491 0.7047 0.5346
Width [cm]
Mean (SD) 0.80 (0.36) 0.83 (0.37) 0.80 (0.33) 0.82 (0.37) 0.79 (0.43) 0.82 (0.35) 0.80 (0.34) 0.83 (0.37) 0.76 (0.24) 0.84 (0.40)
p-value 0.4332 0.9848 0.4332 0.6807 0.5435
Residual myometrial thickness [cm]
Mean (SD) 0.84 (0.35) 0.82 (0.33) 0.84 (0.30) 0.83 (0.34) 0.87 (0.32) 0.82 (0.34) 0.82 (0.35) 0.83 (0.33) 0.81 (0.29) 0.82 (0.35)
p-value 0.3905 0.9487 0.3905 0.8058 0.8590
Adjacent myometrial thickness [cm]
Mean (SD) 1.25 (0.38) 1.17 (0.38) 1.32 (0.41) 1.19 (0.38) 1.21 (0.32) 1.21 (0.39) 1.23 (0.38) 1.20 (0.39) 1.16 (0.28) 1.22 (0.41)
p-value 0.6636 0.4952 0.9373 0.6962 0.7239
Residual myometrial thickness/adjacent myometrial thickness
Mean (SD) 0.67 (0.21) 0.71 (0.22) 0.64 (0.16) 0.70 (0.22) 0.74 (0.24) 0.69 (0.21) 0.66 (0.21) 0.71 (0.22) 0.71 (0.22) 0.68 (0.23)
p-value 0.7392 0.9782 0.5172 0.8663 0.5840
Residual myometrial thickness/width
Mean (SD) 1.24 (0.88) 1.05 (0.57) 1.18 (0.62) 1.14 (0.76) 1.24 (0.73) 1.14 (0.74) 1.18 (0.76) 1.13 (0.73) 1.04 (0.49) 1.16 (0.81)
p-value 0.4332 0.6176 0.4332 0.9496 0.7950
Residual myometrial thickness/height
Mean (SD) 1.96 (1.40) 1.81 (1.19) 1.76 (0.90) 1.89 (1.34) 1.98 (1.15) 1.87 (1.31) 1.94 (1.49) 1.86 (1.20) 1.65 (0.74) 1.82 (1.30)
p-value 0.5153 0.9782 0.5153 0.8663 0.8740
Niche volume [cm3]
Mean (SD) 0.15 (0.20) 0.15 (0.25) 0.12 (0.10) 0.15 (0.24) 0.18 (0.28) 0.14 (0.22) 0.14 (0.20) 0.15 (0.24) 0.09 (0.14) 0.17 (0.27)
p-value 0.9850 0.7231 0.9850 0.8728 0.0362

SD – standard deviation.

by gestational hypertension (n = 28), and among them, 65% from 158 pregnant women on admission to the hospital.
were diagnosed with a niche of the uterus after cesarean In 78% (n = 124) of pregnant women, a negative culture
section. Out of the 59 (29%) patients who developed hypo- was reported. In 22% (n = 34) of women, the culture was
thyroidism during their pregnancy, 85% were diagnosed positive for pathogenic flora such as Staphylococcus aga-
with a uterine niche after cesarean section. There was lactiae spp (n = 8, 24%), Candida (including C. albicans
no statistical correlation between the prevalence or pa- spp, C. glabrata spp; n = 10.29%), Enterococcus (including
rameters of a uterine niche after cesarean section and E. faecalis spp; n = 4.12%), Escherichia coli spp (n = 6.18%),
the abovementioned medical complications of pregnancy. Klebsiella pneumoniae spp (n = 4.12%), and Pseudomo-
In our study, there were no cases of postoperative, symp- nas putida spp (n = 1.3%). The percentage of identified
tomatic infections. However, the influence of cervical canal niches in women with negative culture was 74% (n = 92).
colonization by microbes on the healing of uterine scars The same percentage of niches was found in the group
was evaluated. Swabs from the cervical canal were taken of women with positive cultures from the cervical canal
Adv Clin Exp Med. 2022;31(1):41–48 45

Table 3. Comparison of the maternal age and the occurrence of uterine niche after cesarean section
Variable ≤25 years 25–30 years 31–35 years 36–40 years >40 years
Niche, n (%) 8 (5) 45 (29) 73 (48) 21 (14) 6 (4)
Non-niche, n (%) 4 (8) 13 (25) 23 (45) 10 (20) 1 (2)
p-value 0.7346*

*Pearson’s χ2 test, degrees of freedom (df) = 4.

Table 4. Comparison of the parameters of the cesarean scar niche depending on maternal age
Variable ≤25 years 25–30 years 31–35 years 36–40 years >40 years p-value*
H [cm], mean (SD) 0.49 (0.29) 0.47 (0.19) 0.50 (0.22) 0.52 (0.27) 0.47 (0.23) 0.8210
W [cm], mean (SD) 0.84 (0.21) 0.83 (0.42) 0.83 (0.37) 0.73 (0.24) 0.84 (0.22) 0.6992
RMT [cm], mean (SD) 0.9 (0.33) 0.87 (0.35) 0.81 (0.34) 0.80 (0.33) 0.80 (0.31) 0.6749
AMT [cm], mean (SD) 1.30 (0.40) 1.24 (0.39) 1.20 (0.38) 1.15 (0.41) 1.21 (0.45) 0.8959
RMT/AMT 0.72 (0.25) 0.70 (0.21) 0.68 (0.22) 0.71 (0.23) 0.68 (0.17) 0.8408
RMT/W 0.92 (0.40) 1.21 (0.69) 1.13 (0.80) 1.17 (0.79) 1.02 (0.57) 0.7671
RMT/H 1.61 (0.86) 2.06 (1.31) 1.83 (1.31) 1.81 (1.47) 1.90 (1.00) 0.5102
Niche volume [cm3],
0.20 (0.21) 0.16 (0.30) 0.14 (0.20) 0.12 (0.11) 0.16 (0.25) 0.8994
mean (SD)

H – height; W – width; RMT – residual myometrial thickness; AMT – adjacent myometrial thickness; SD – standard deviation; *Kruskal–Wallis analysis
of variance (ANOVA) test.

Table 5. Comparison of the occurrence of uterine scar niche by gestational age and history of miscarriages
Preterm delivery Miscarriage in the past
Variable
yes no yes no
Niche, n (%) 11 (22) 40 (78) 10 (20) 41 (80)
Non-niche, n (%) 22 (14) 131 (86) 33 (22) 120 (78)
p-value* 0.2720 0.8448

*Fisher’s exact test.

(n = 25, 74%). In this study, no statistically significant cor- Discussion

relation was found between the prevalence and parameters
of the uterine scar niche and the colonization of the cervix Currently, there are no guidelines concerning the opti-
by pathogens. Table 1 and Table 2 present the comparison mal timing for cesarean section scar assessment.
data between the incidence and parameters of cesarean Most of the research concerning uterine niches after ce-
scar niche and systemic diseases appearing in pregnancy, sarean section have focused on examining women with
and the colonization of the cervix by pathogenic bacteria. symptoms related to its presence. The interval between
The study group was divided into subgroups by age. cesarean section and evaluation of the cesarean scar var-
Table 3 presents the detailed characteristics of each ied in different publications. Most publications assessed
subgroup. the uterine scar from 6 to 8 weeks, 6 months,21 1 year,22
Also, the impact of gestational age at the time of ce- or more than 5 years23,24 after performing the cesarean
sarean section was assessed. In 16% of patients (n = 33), section. This study aimed to evaluate the influence of in-
cesarean section was performed on a preterm pregnancy dividual factors and systemic diseases appearing during
in which 67% (n = 22) of these resulted in a uterine niche. pregnancy on the process of uterine healing after ce-
In women undergoing cesarean section at term (n = 171, sarean section. In this study, every woman who had ce-
84% of patients), the percentage of uterine scar niches af- sarean section with a single-layer, full thickness uterine
ter cesarean section was 77% (n = 132). For women with closure excluding the decidua, was invited for a uterine
a history of miscarriages (n = 43, 21% of patients), a niche scar examination. The examination was performed from
was diagnosed in 33 (77%) of these patients. There was 6 to 9 weeks after the operation, during which the uterine
no statistical correlation between the prevalence or pa- scar was still healing and no clinical symptoms are present.
rameters of the niche after cesarean section and maternal Van der Voet et al. found that the prevalence of niches did
age during cesarean section, preterm delivery and history not change with time (niches found during an examina-
of miscarriages (Table 4,5,6). tion at 6–12 weeks after the cesarean section were also
46 J. Budny-Wińska, A. Zimmer-Stelmach, M. Pomorski. Uterine healing after cesarean section

Table 6. Comparison of analyzed parameters of cesarean scar niche depending on the history of miscarriages and gestational age
History of miscarriages Gestational age
Variable
no yes p-value* preterm delivery term delivery p-value*
H [cm], mean (SD) 0.50 (0.23) 0.50 (0.18) 0.4301 0.48 (0.24) 0.52 (0.22) 0.3757
W [cm], mean (SD) 0.80 (0.32) 0.90 (0.48) 0.3868 0.81(0.48) 0.82 (0.34) 0.3081
RMT [cm], mean (SD) 0.84 (0.34) 0.79 (0.34) 0.2912 0.89 (0.36) 0.82 (0.33) 0.2423
AMT [cm], mean (SD) 1.22 (0.39) 1.17 (0.35) 0.5697 1.23 (0.41) 1.21 (0.38) 0.8455
RMT/AMT 0.70 (0.21) 0.67 (0.87) 0.3472 0.73 (0.22) 0.69 (0.21) 0.3672
RMT/W 1.15 (0.65) 1.12 (1.01) 0.2202 1.16 (0.61) 1.14 (0.76) 0.5342
RMT/H 1.91 (1.27) 1.77 (1.40) 0.1832 2.03 (1.41) 1.86 (1.28) 0.7800
Niche volume [cm3], mean (SD) 0.13 (0.17) 0.20 (0.37) 0.9947 0.23 (0.43) 0.13 (0.17) 0.9588

H – height; W – width; RMT – residual myometrial thickness; AMT – adjacent myometrial thickness; SD – standard deviation; *Mann–Whitney U test.

present on an examination performed 1 year after cesarean transverse uterine incision with single-layer full thickness
section).25 uterine closure using the same suture material.
Transvaginal ultrasound examination at 6–9 weeks after There was also no correlation between the param-
cesarean section allows for the identification of patients eters of the niche, incidence of niches and a woman’s age
with a potential risk of abnormal uterine healing after cesar- at the time of cesarean section, which is in line with other
ean section, due to a large niche that may threaten the next studies.29 In the study by Pomorski et al., a positive cor-
pregnancy or be the cause of cesarean scar syndrome. Pa- relation was found between the height of the niche and
tients with a large niche and low RMT, as well as physi- the mother’s age. 30 In another publication, the presence
cians treating them need to be aware of the risk of possible of a niche was significantly associated with younger ma-
complications as soon as possible. Currently, in our clinical ternal age at the time of cesarean section. In this study,
practice, we found many women with abnormal uterine younger patients had cesarean section performed during
bleeding related to the niche, who are unnecessarily treated the active phase of labor.31 According to some studies, per-
by other doctors with oral contraceptives or invasive proce- forming cesarean section during the active phase of labor
dures such as dilatation and curettage. Moreover, women or phase II of labor increases the risk of a large niche for-
with extremely low RMT face life-threatening complica- mation.11,33 In our study, only 6 patients were in the active
tions in subsequent pregnancies due to the risk of scar rup- phase of labor (dilation >4 cm to full dilation of cervix) and
ture at 21 weeks of gestation.26 Taking into consideration 10 patients were in phase II of labor at the time of cesarean
the above problems and the limited knowledge gynecolo- section. Therefore, due to the low numbers, we did not use
gists have of niche-related complications, we suggest cesar- these variables in the statistical analysis of the subgroups
ean section scar assessment be routinely performed in all of maternal age.
women who have undergone cesarean section at the end There are conflicting reports in the literature regarding
of puerperium. the impact of gestational age on niche formation. In our
In this study, all niches, whether classified as small study, no relationship was found between gestational age
or large, were assessed using two and three-dimensional at the time of delivery and the prevalence and parameters
ultrasound.7 Even though 2 meta-analyses have con- of the niche. This finding is supported by other studies.29,30,32
cluded single-layer closure to be associated with de- On the other hand, Vikhareva and Valentin found that de-
creased RMT in comparison to double-layer sutures, in our livery before 37 weeks gestation was a predictor of large
study group, only 2.4% of women had a RMT < 2.2 mm. niches.33 The study by Hayakawa et al. demonstrated a posi-
An RMT < 2.2 mm is considered a risk factor for severe scar tive link between the gestational age of 37–41 weeks at de-
complications in subsequent pregnancies.9 Both of these livery and the presence of wedge niches.34
meta-analyses have shown no differences in the risk of ma- The influence of medical conditions associated with
ternal morbidity or long-term outcomes between single- pregnancy on uterine niche development was analyzed. No
compared to double-layer uterine closure.27,28 correlation was found between GDM and the prevalence
This study is a continuation of our previous research and parameters of niches. However, Antila-Långsjö et al.
in which we proved there was no correlation between found GDM and higher body mass index (BMI) to be posi-
an operator’s experience and the prevalence and parameters tively correlated with the incidence of uterine niche after
of uterine niches after cesarean section.20 The lack of a rela- cesarean section.11 Interestingly, such a correlation has
tionship between the operator’s experience and the forma- not been found for pregestational diabetes. In our study,
tion of a uterine niche after cesarean section is supported the mean prepregnancy BMI in women diagnosed with
in the literature.11 It should be emphasized that all cesarean cesarean scar niche was 27.1 (±6.1) kg/m2 compared to 25.1
sections were performed in a standardized manner, i.e., low (±5.3) kg/m 2 in women without a niche. Consequently,
Adv Clin Exp Med. 2022;31(1):41–48 47

it means that most of the women in this study were over- The etiology of a uterine niche after cesarean section
weight. In other studies, no correlation was found between is multifactorial. In our study, we evaluated a few poten-
BMI and the presence of a uterine niche. 33,34 tial factors that could disturb the proper healing process
Our study also evaluated the influence of gestational hy- of the uterus. The effect of other important individual risk
pertension on uterine healing. No statistically significant factors such as BMI, corticosteroid use, previous myomec-
correlation was found between the frequency of occur- tomy and smoking status on the prevalence and param-
rence or parameters of a niche and the presence of ges- eters of cesarean section niche was not investigated in our
tational hypertension. To our knowledge, only 1 other study, which is a limitation.
study evaluated the effect gestational hypertension has
on the incidence of uterine scar defect – and failed to show
any correlation. 35 Considering the influence of preg- Conclusions
nancy-related systemic diseases, it is impossible to ignore
the influence of hypothyroidism on tissue metabolism. Two- and three-dimensional ultrasonographic cesar-
The correlation between hypothyroidism and a higher risk ean scar assessment revealed that the selected risk factors
of perioperative complications has been known for a long concerning systemic diseases during pregnancy, mater-
time. 36 To date, no other studies have been performed nal medical history and colonization of the cervical canal
to assess the effect of hypothyroidism on uterine healing have no impact on uterine scar healing in women with
after cesarean section. In our study, no relationship was single-layer uterine closure covering the entire thickness
found between hypothyroidism and uterine scar niche of the myometrium, excluding the decidua.
parameters. When assessing the impact of individual
diseases on uterus healing and comparing conflicting ORCID iDs
reports in the literature, it should be remembered that Joanna Budny-Wińska  [Link]
Aleksandra Zimmer-Stelmach  [Link]
each population has its own individual characteristics Michał Pomorski  [Link]
and the incidences of GDM, gestational hypertension and
hypothyroidism vary worldwide. References
In our study, the effect cervical colonization by microor- 1. Anna V, van der Ploeg HP, Cheung NW, Huxley RR, Bauman AE. Socio­
ganisms has on the prevalence and parameters of a uterine demographic correlates of the increasing trend in prevalence of gesta-
tional diabetes mellitus in a large population of women between 1995
niche was evaluated, because previous studies have cor-
and 2005. Diabetes Care. 2008;31(12):2288–2293. doi:10.2337/dc08-1038
related the bacterial load of the cervix with the bacterial 2. Guariguata L, Linnenkamp U, Beagley J, Whiting DR, Cho NH. Global
load within the uterine cavity.37,38 This suggests that cervi- estimates of the prevalence of hyperglycaemia in pregnancy. Diabetes
cal microbiota may be a source of microbes for coloniza- Res Clin Pract. 2014;103(2):176–185. doi:10.1016/[Link].2013.11.003
3. Johnson JA, Tough S; SOGC GENETICS COMMITTEE. Delayed child-
tion of the uterine cavity and may influence the healing bearing. J Obstet Gynaecol Can. 2012;34(1):80–93. doi:10.1016/S1701-
process of the cesarean section scar. However, our study 2163(16)35138-6
showed no correlation between the cervical colonization 4. Rendtorff R, Hinkson L, Kiver V, Dröge LA, Henrich W. Pregnancies
in women aged 45 years and older: A 10-year retrospective analysis
and the prevalence and parameters of uterine niches after in Berlin. Geburtshilfe Frauenheilkd. 2017;77(3):268–275. doi:10.1055/
cesarean section. This may be due to the use of periopera- s-0043-100105
tive antibiotics for surgical prophylaxis. Although, further 5. Betran AP, Torloni MR, Zhang J, et al. What is the optimal rate of cae-
sarean section at population level? A systematic review of ecologic
research is needed to confirm this hypothesis. studies. Reprod Health. 2015;12:57. doi:10.1186/s12978-015-0043-6
In other studies, the influence of inflammatory processes 6. Pomorski M, Fuchs T, Zimmer M. Prediction of uterine dehiscence using
such as postpartum fever,33,35 the application of antibiot- ultrasonographic parameters of cesarean section scar in the nonpreg-
ics during childbirth, 39 perinatal and puerperal infection nant uterus: A prospective observational study. BMC Pregnancy Childbirth.
2014;14:365. doi:10.1186/s12884-014-0365-3
in the form of chorioamnionitis, postoperative wound in- 7. Ludwin A, Martins WP, Ludwin I. Evaluation of uterine niche by three-
fection, urinary tract infection, and endometritis34 were dimensional sonohysterography and volumetric quantification: Tech-
analyzed, but no correlation between the abovementioned niques and scoring classification system. Ultrasound Obstet Gynecol.
2019;53(1):139–143. doi:10.1002/uog.19181
variables and the prevalence of niches after cesarean sec- 8. Setubal A, Alves J, Osório F, et al. Treatment for uterine isthmocele,
tion was found. a pouchlike defect at the site of a cesarean section scar. J Minim Invasive
Gynecol. 2018;25(1):38–46. doi:10.1016/[Link].2017.09.022
9. Jordans IPM, de Leeuw RA, Stegwee SI, et al. Sonographic examina-
Limitations tion of uterine niche in non-pregnant women: A modified Delphi pro-
cedure. Ultrasound Obstet Gynecol. 2019;53(1):107–115. doi:10.1002/
The main limitation of our study is the lack of compari- uog.19049
10. van der Voet LF, Bij de Vaate AM, Veersema S, Brölmann HA, Huirne JA.
son between a single-layer continuous uterine suture and
Long-term complications of caesarean section: The niche in the scar.
a double-layer uterine suture closure, due to the single- A prospective cohort study on niche prevalence and its relation to
layer continuous uterine suture being the standard of care abnormal uterine bleeding. BJOG. 2014;121(2):236–244. doi:10.1111/
at our Department. The other limitation is that we were 1471-0528.12542
11. Antila-Långsjö RM, Mäenpää JU, Huhtala HS, Tomás EI, Staff SM.
checking the colonization of the cervical canal without Cesarean scar defect: A prospective study on risk factors. Am J Obstet
uterine cavity colonization. Gynecol. 2018;219(5):458.e1–458.e8. doi:10.1016/[Link].2018.09.004
48 J. Budny-Wińska, A. Zimmer-Stelmach, M. Pomorski. Uterine healing after cesarean section

12. Vikhareva O, Rickle GS, Lavesson T, Nedopekina E, Brandell K, 26. Pomorski M, Fuchs T, Budny-Winska J, Zimmer A, Zimmer M. Natural
Salvesen KÅ. Hysterotomy level at Cesarean section and occurrence history of caesarean scar pregnancy. Ginekol Pol. 2019;90(6):351–352.
of large scar defects: A randomized single-blind trial. Ultrasound doi:10.5603/GP.a2019.0054
Obstet Gynecol. 2019;53(4):438–442. doi:10.1002/uog.20184 27. Di Spiezio Sardo A, Saccone G, McCurdy R, Bujold E, Bifulco G,
13. Bij de Vaate AJ, van der Voet LF, Naji O, et al. Prevalence, potential Berghella V. Risk of Cesarean scar defect following single- vs double-
risk factors for development and symptoms related to the presence layer uterine closure: Systematic review and meta-analysis of random-
of uterine niches following Cesarean section: Systematic review. ized controlled trials. Ultrasound Obstet Gynecol. 2017;50(5):578–583.
Ultrasound Obstet Gynecol. 2014;43(4):372–382. doi:10.1002/uog.13199 doi:10.1002/uog.17401
14. Vikhareva Osser O, Valentin L. Clinical importance of appearance of 28. Roberge S, Demers S, Berghella V, Chaillet N, Moore L, Bujold E. Impact
cesarean hysterotomy scar at transvaginal ultrasonography in non- of single- vs double-layer closure on adverse outcomes and uterine
pregnant women. Obstet Gynecol. 2011;117(3):525–532. doi:10.1097/ scar defect: A systematic review and metaanalysis. Am J Obstet Gynecol.
AOG.0b013e318209abf0 2014;211(5):453–460. doi:10.1016/[Link].2014.06.014
15. Kaelin Agten A, Cali G, Monteagudo A, Oviedo J, Ramos J, Timor- 29. Ofili-Yebovi D, Ben-Nagi J, Sawyer E, et al. Deficient lower-segment
Tritsch I. The clinical outcome of cesarean scar pregnancies implant- Cesarean section scars: Prevalence and risk factors. Ultrasound Obstet
ed “on the scar” versus “in the niche”. Am J Obstet Gynecol. 2017; Gynecol. 2008;31(1):72–77. doi:10.1002/uog.5200
216(5):510.e1–510.e6. doi:10.1016/[Link].2017.01.019 30. Pomorski M, Fuchs T, Rosner-Tenerowicz A, Zimmer M. Morphology
16. Vervoort A, Vissers J, Hehenkamp W, Brölmann H, Huirne J. The effect of the cesarean section scar in the non-pregnant uterus after one
of laparoscopic resection of large niches in the uterine caesarean scar elective cesarean section. Ginekol Pol. 2017;88(4):174–179. doi:10.5603/
on symptoms, ultrasound findings and quality of life: A prospective GP.a2017.0034
cohort study. BJOG. 2018;125(3):317–325. doi:10.1111/1471-0528.14822 31. Pomorski M, Fuchs T, Rosner-Tenerowicz A, Zimmer M. Standard-
17. Pomorski M, Fuchs T, Rosner-Tenerowicz A, Zimmer M. Sonographic ized ultrasonographic approach for the assessment of risk factors
evaluation of surgical repair of uterine cesarean scar defects. J Clin of incomplete healing of the cesarean section scar in the uterus.
Ultrasound. 2017;45(8):455–460. doi:10.1002/jcu.22449 Eur J Obstet Gynecol Reprod Biol. 2016;205:141–145. doi:10.1016/j.
18. Tower AM, Frishman GN. Cesarean scar defects: An underrecognized ejogrb.2016.08.032
cause of abnormal uterine bleeding and other gynecologic compli- 32. Yazicioglu F, Gökdogan A, Kelekci S, Aygün M, Savan K. Incomplete
cations. J Minim Invasive Gynecol. 2013;20(5):562–572. doi:10.1016/j. healing of the uterine incision after caesarean section: Is it prevent-
jmig.2013.03.008 able? Eur J Obstet Gynecol Reprod Biol. 2006;124(1):32–36. doi:10.1016/j.
19. Patounakis G, Ozcan MC, Chason RJ, et al. Impact of a prior cesar- ejogrb.2005.03.023
ean delivery on embryo transfer: A prospective study. Fertil Steril. 33. Vikhareva Osser O, Valentin L. Risk factors for incomplete healing of
2016;106(2):311–316. doi:10.1016/[Link].2016.03.045 the uterine incision after caesarean section. BJOG. 2010;117(9):1119–1126.
20. Budny-Winska J, Zimmer-Stelmach A, Pomorski M. Two- and three- doi:10.1111/j.1471-0528.2010.02631.x
dimensional transvaginal ultrasound in assessment of the impact 34. Hayakawa H, Itakura A, Mitsui T, et al. Methods for myometrium clo-
of selected obstetric risk factors on cesarean scar niche formation: sure and other factors impacting effects on cesarean section scars of
The case-controlled study. Ginekol Pol. 2021;92(5):378–382. doi:10. the uterine segment detected by the ultrasonography. Acta Obstet
5603/GP.a2021.0024 Gynecol Scand. 2006;85(4):429–434. doi:10.1080/00016340500430436
21. Osser OV, Jokubkiene L, Valentin L. High prevalence of defects in 35. Pan H, Zeng M, Xu T, et al. The prevalence and risk predictors of cesar-
Cesarean section scars at transvaginal ultrasound examination. ean scar defect at 6 weeks postpartum in Shanghai, China: A pro-
Ultrasound Obstet Gynecol. 2009;34(1):90–97. doi:10.1002/uog.6395 spective cohort study. Acta Obstet Gynecol Scand. 2019;98(4):413–422.
22. Bij de Vaate AJ, Brölmann HA, van der Voet LF, van der Slikke JW, doi:10.1111/aogs.13505
Veersema S, Huirne JA. Ultrasound evaluation of the Cesarean scar: 36. Chen HY, Chen SJ, Hsieh FJ. Observation of cesarean section scar by trans-
Relation between a niche and postmenstrual spotting. Ultrasound vaginal ultrasonography. Ultrasound Med Biol. 1990;16(5):443–447.
Obstet Gynecol. 2011;37(1):93–99. doi:10.1002/uog.8864 doi:10.1016/0301-5629(90)90166-a
23. Armstrong V, Hansen WF, Van Voorhis BJ, Syrop CH. Detection of 37. Chen C, Song X, Wei W, et al. The microbiota continuum along the female
cesarean scars by transvaginal ultrasound. Obstet Gynecol. 2003; reproductive tract and its relation to uterine-related diseases.
101(1):61–65. doi:10.1016/s0029-7844(02)02450-x Nat Commun. 2017;8(1):875. doi:10.1038/s41467-017-00901-0
24. Chen HY, Chen SJ, Hsieh FJ. Observation of cesarean section scar 38. Winters AD, Romero R, Gervasi MT, et al. Does the endometrial cav-
by transvaginal ultrasonography. Ultrasound Med Biol. 1990;16(5): ity have a molecular microbial signature? Sci Rep. 2019;9(1):9905.
443–447. doi:10.1016/0301-5629(90)90166-a doi:10.1038/s41598-019-46173-0
25. van der Voet LF, Jordans IPM, Brölmann HAM, Veersema S, Huirne JAF. 39. Voet LLFV, Vaate AMJB, Heymans MW, Brölmann HAM, Veersema S,
Changes in the uterine scar during the first year after a caesare- Huirne JAF. Prognostic factors for niche development in the uterine
an section: A prospective longitudinal study. Gynecol Obstet Invest. caesarean section scar. Eur J Obstet Gynecol Reprod Biol. 2017;213:31–32.
2018;83(2):164–170. doi:10.1159/000478046 doi:10.1016/[Link].2017.03.039