Efficacy of bowel ultrasound to diagnose necrotizing enterocolitis in extremely low birthweight infants

Abstract

BACKGROUND:

Bowel ultrasound (US) is one of the methods used to enhance diagnostic accuracy of necrotizing enterocolitis (NEC) and its associated complications in premature newborns.

AIM:

To explore the diagnostic accuracy of bowel US in extremely low birth weight (ELBW) infants with NEC.

METHODS:

A single-center retrospective case-control study included 84 extremely low birth weight (ELBW) infants. The infants were divided into three groups: Group 1 –infants with NEC (n = 26); Group 2 –infants with feeding problems (n = 28); Group 3 –control group (n = 30).

RESULTS:

The specific bowel US findings in premature newborns with NEC (stage 3) included bowel wall thinning, complex (echogenic) ascites, and pneumoperitoneum, p < 0.05. The diagnostic effectiveness of these sonographic signs was 96.8% (sensitivity 75.0% and specificity 97.6%), p < 0.05. These findings with high specificity were associated with the need for surgical intervention, poor outcomes, or increased mortality. Stage 2 NEC which did not require surgery showed impaired differentiation of the bowel wall layers, absent or decreased bowel peristalsis, pneumatosis intestinalis, portal venous gas, or simple ascites, with a diagnostic accuracy of 82.9% (sensitivity 55.6%, specificity 91.4%, p < 0.05).

CONCLUSIONS:

Bowel US can be used as an adjunct to abdominal radiography to aid in the diagnosis of infants with suspected NEC by providing more detailed evaluation of the intestine.

Keywords

Bowel ultrasound extremely low birth weight intestine necrotizing enterocolitis premature newborns

Abbreviations

celiac artery

confidence intervals

ELBW

extremely low birth weight

gestational age

gastrointestinal

IQR

interquartile ranges

NEC

necrotizing enterocolitis

odds ratios

PDA

Patent ductus arteriosus

resistive index

SMA

superior mesenteric artery

Ultrasonography, ultrasound

1 Introduction

Necrotizing enterocolitis (NEC) is a frequent cause of morbidity and mortality in extremely low birth weight (ELBW) infants [1]. Early and correct diagnosis and timely initiation of treatment are extremely important. Clinical diagnosis is usually confirmed with abdominal radiography. Specific signs of NEC include dilated bowel loops, multiple air-fluid levels, intramural bowel wall gas (pneumatosis intestinalis), gas in the portal venous system, and, in the case of bowel perforation, pneumoperitoneum. However, in the early stages of the disease, it may be extremely difficult to diagnose NEC in premature infants: Radiographs may fail to show specific signs and multiple radiographs may overexpose newborns to ionizing radiation.

Ultrasonography (US) is an alternative imaging modality for the diagnosis and management of NEC. This diagnostic tool has been used for over 40 years [2]; however, its clinical application for this indication needs further clarification. US can detect both pneumatosis and portal venous gas earlier than radiography [3, 4]. Moreover, US can assess the condition of the bowel wall, detect thickening, impaired perfusion, and decreased peristalsis, and the presence and nature of free fluid in the abdominal cavity. However, data regarding the diagnostic reliability and prognostic value of abdominal US are contradictory. Currently, US findings have little impact on the choice of therapy [5]. The importance of Doppler indicators (resistive index [RI] of the celiac artery (CA) and superior mesenteric artery (SMA)] in premature infants has been the subject of numerous studies. However, the results are controversial.

This research was aimed to study the diagnostic significance of various US signs in extremely low birth weight infants with NEC.

2 Patients and methods

The study group included 84 premature ELBW infants born between 2017 and 2019 in the National Medical Research Center for Obstetrics, Gynecology and Perinatology named after academician V.I. Kulakov of the Ministry of Health of the Russian Federation. Premature infants with multiple malformations, congenital heart defects, hemolytic disease of the newborn, and non-immune hydrops fetalis were not included in the study.

The majority of the premature infants (54 of 84, 64%) had abnormal enteral feeding, including severe bloating, bowel paresis, gastric residual contents exceeding 50% of a single feeding volume, bile-stained gastric residuals, and rumination or vomiting.

The diagnosis and staging of NEC was performed according to the Bell classification [6] and its modified version by Walsh and Kliegman [7]. In ELBW infants, enteral feeding disorders can be a sign of early NEC (stage 1), or of functional gastrointestinal (GI) disorders associated with infection. It may be difficult to distinguish these two conditions at early stages, so these newborns were included in the same study group.

Depending upon the combination of clinical and laboratory data, subjects were divided into 3 study groups:

Group 1 –evident signs of NEC (stage 2 or stage 3) (n = 26) –NEC group;

Group 2 –functional GI disorders and/or suspected NEC stage 1 without disease progression (n = 28) –GI dyskinesia group;

Group 3 –no signs of NEC or functional GI disorders (n = 30) –control group.

Babies with signs of enteral feeding disorders were examined according to generally accepted standards [8]. Abdominal radiography in anteroposterior and lateral projections was performed in search of dilated bowel loops, multiple air-fluid levels, pneumatosis, and free gas in the abdominal cavity. All newborns underwent abdominal and bowel US on days 1, 3, and 7, in cases of worsening and the presence of enteral feeding failure and NEC. Newborns were examined with micro-convex and linear probes. US was performed with the infant in the supine position, using multisectional scanning of each quadrant in transverse and sagittal planes. The following parameters were assessed: the diameter of bowel loops; intestinal wall thickness, echogenicity, layer differentiation, pneumatosis; presence of portal venous gas; free gas in the abdominal cavity (pneumoperitoneum); free abdominal fluid (echogenic/anechogenic); and intestinal peristalsis (active/reduction/not determined). Thickness of the bowel wall of pathologically altered loop was measured three times and the maximum value was recorded in the case of thickening or the minimum in the case of thinning. Presence of pinpoint hyperechogenic areas in the bowel wall and portal vessels were deemed specific for pneumatosis intestinalis and the presence of gas in the portal venous system (Fig. 1 A,B). Free gas in the abdomen was identified by the presence of linear or pinpoint echogenic areas outside the intestine with reverberation artifacts (Fig. 2).

Fig. 1

Abdominal sonograms. A. Pneumatosis intestinalis –hyperechoic spots (gas microbubbles) within the bowel wall (arrow), small amount of anechogenic free fluid around the bowel loop. B. Gas microbubbles within the portal vein and intrahepatic branches (arrows).

Fig. 2

Abdominal sonogram. Free gas in the abdominal cavity (arrows), thickened bowel wall (2,98 mm) with increased echogenicity and impaired differentiation of the layers, small amount of free fluid around the bowel loop.

To evaluate the arterial bowel blood flow, the resistive index (RI) of the celiac artery (CA) and superior mesenteric artery (SMA) were assessed using pulsed wave Doppler US.

2.1 Statistical analyses

Statistical software (SPSS, v.17.0, IBM, Armonk, NY) was used for data analysis. For quantitative data, median and interquartile ranges (IQR) were used. For qualitative data, frequency rates (%) were used. Kruskal-Wallis and Mann-Whitney U-tests were utilized to compare data. To predict the probability of NEC outcome using quantitative and/or qualitative parameters, a binary logistic regression equation was used. The dependent variable was a probability of NEC (stage 2 or stage 3). Independent variables were US indicators that had statistically significant differences between the groups at comparative analyses. Differences were considered statistically significant if p < 0.05.

3 Results

In Group 1, 20/26 (76.9%) newborns had NEC stage 2 (13 survived, 7 died) and 6/26 (23.1%) had NEC stage 3 requiring surgical treatment (4 survived, 2 died). The median age of NEC onset (Me [IQR]) was 15.5 (8–31.5) days of life. The US findings were assessed in each group, and in NEC stage 2 and NEC stage 3 subgroups separately. All newborns had comparable birthweights, gestational ages (GA), and Apgar scores (Table 1).

Table 1
Demographics

Parameters Group 1 Group 2 Control group P-value

NEC (n = 26) GI dyskinesia (n = 28) (n = 30)

GA, weeks, median (IQR) 27.6 (26.0–29.0) 27.5 (26.4–30.0) 28 (26.8–29.0) 0.263

Birth weight, grams, median (IQR) 799 (640–880) 800 (720–980) 814 (680–940) 0.396

Apgar, 1 min, score 6 and less, (%) 20 (76,9) 21 (75) 16 (50) 0.092

Apgar, 5 min, score 6 and less, (%) 11 (42,3) 10 (35,7) 7 (23,3) 0.083

Small for GA, (%) 8 (30.8) 9 (32.1) 4 (13.3) 0.397

Parameters	Group 1	Group 2	Control group	P-value
GA, weeks, median (IQR)	27.6 (26.0–29.0)	27.5 (26.4–30.0)	28 (26.8–29.0)	0.263
Birth weight, grams, median (IQR)	799 (640–880)	800 (720–980)	814 (680–940)	0.396
Apgar, 1 min, score 6 and less, (%)	20 (76,9)	21 (75)	16 (50)	0.092
Apgar, 5 min, score 6 and less, (%)	11 (42,3)	10 (35,7)	7 (23,3)	0.083
Small for GA, (%)	8 (30.8)	9 (32.1)	4 (13.3)	0.397

NEC –necrotizing enterocolitis, GI –gastrointestinal, GA –gestational age, IQR –interquartile ranges, p –coefficient of significance of differences between the groups. Differences were considered statistically significant at p < 0.05.

The incidence of the studied US findings in the groups of newborns is presented in Table 2 and Table 3. US signs of dilated bowel loops, thickening or thinning of walls, reduction of peristalsis, gas in the portal venous system, and free fluid in the abdominal cavity were found significantly more often in patients with NEC compared to patients with GI dyskinesia and the control group. Increased echogenicity of the bowel wall and impaired layer differentiation, the presence of pneumatosis, free gas in the abdominal cavity, and echogenic free fluid in the abdominal cavity were found only in the NEC group. At the same time, the dilated bowel loops, reduction of peristalsis, anechogenic free fluid in the abdominal cavity and gas in the portal venous system were found in all 3 groups. Gas in the portal venous system was found statistically more often in infants with NEC –in 6 of 26 (23.1%) patients; it was also found in 3 of 28 (10.7%) babies with GI dyskinesia, and in 1 of 30 (3.3%) in the control group. Most infants with US signs of gas in the portal venous system had an umbilical vein catheter: One baby (100%) of the control group, 2 of 3 (66.7%) in the group with GI dyskinesia, and 3 of 6 (50%) in the NEC group.

Table 2

Incidence of ultrasound signs in the groups of newborns

Ultrasound signs:	Group 1	Group 2	Control group	P-value
	NEC (n = 26)	GI dyskinesia (n = 28)	(n = 30)
Dilated bowel loops (diameter > 10 mm), (%)	19 (73.1)	5 (17.8)	3 (17.6)	p_1,3 = 0.023
p₁_,₂ = 0.016
p₂_,₃ = 0.524
Thickened bowel wall (≥2,4 mm), (%)	16 (61.5)	4 (14.3)	0	p_1,2 = 0.026
Increased echogenicity of the bowel wall, (%)	16 (61.5)	0	0	–
Thinned bowel wall (≤1 mm), (%)	10 (38.5)	4 (14.3)	0	p_1,2 = 0.034
Impaired differentiation of the bowel wall layers, (%)	12 (46.2)	0	0	–
Absent peristalsis, (%)	13 (50.0)	2 (7.1)	0	p₁_,₂ = 0.058
Reduction of peristalsis, (%)	25 (96.2)	18 (64.3)	5 (29.4)	p₁_,₃ = 0.012
				p₂_,₃ = 0.062
				p₁_,₂ = 0.041
Pneumatosis intestinalis, (%)	15 (57.7)	0	0	–
Gas in the portal venous system, (%)	6 (23.1)	3 (10.7)	1 (3.3)	p_1,3 = 0.048
				p₂_,₃ = 0.256
				p₁_,₂ = 0.174
Pneumoperitoneum, (%)	4 (15.4)	0	0	–
Ascites, (%)	25 (96.2)	15 (53.6)	7 (41.2)	p₁_,₃ = 0.015
				p₂_,₃ = 0.044
				p₁_,₂ = 0.035
Echogenic free fluid, (%)	5 (19.2)	0	0	–
Anechoic free fluid, (%)	20 (77.0)	15 (53.6)	7 (41.2)	p₁_,₃ = 0.022
				p₂_,₃ = 0.043
				p₁_,₂ = 0.276

NEC –necrotizing enterocolitis, GI –gastrointestinal.

Table 3

US findings in NEC stage 2 and stage 3 patients

Ultrasound signs:	NEC stage 2 (n = 20)	NEC stage 3 (n = 6)	P-value
Dilated bowel loops (diameter > 10 mm), (%)	15 (75.0)	4 (66.7)	0.156
Thickened bowel wall (≥2,4 mm), (%)	13 (65.0)	3 (50.0)	0.365
Increased echogenicity of the bowel wall, (%)	6 (30.0)	4 (66.7)	0.714
Thinned bowel wall (≤1 mm), (%)	5 (25.0)	5 (83.3)	0.042
Impaired differentiation of the bowel wall layers, (%)	8 (46.2)	4 (66.7)	0.113
Reduction of peristalsis, (%)	6 (30.0)	5 (83.3)	0.044
Pneumatosis intestinalis, (%)	11 (55.0)	4 (66.7)	0.115
Gas in the portal venous system, (%)	3 (15.0)	3 (50.0)	0.063
Pneumoperitoneum, (%)	0	4 (66.7)	–
Free fluid in the abdominal cavity, (%)	19 (95.0)	6 (100.0)	0.318
Echogenic free fluid, (%)	2 (10.0)	3 (50.0)	0.048
Anechoic free fluid, (%)	17 (85.0)	3 (50.0)	0.114

US –ultrasound, NEC- necrotizing enterocolitis.

Free gas in the abdominal cavity, indicating bowel perforation, further confirmed by abdominal radiography, was found in 4 of 26 (15.4%) with NEC. According to radiographic examination, babies with NEC had dilated bowel loops in 13 of 26 (50%) cases, and free gas in the abdominal cavity in 4 of 26 (15.4%).

Using binary logistic regression specific US signs of the probability of developing the surgical stage of NEC were identified: thinning of the bowel wall and its increased echogenicity, echogenic free fluid in abdominal cavity, pneumoperitoneum (p = 0.001, the diagnostic effectiveness of the combination of US signs mentioned above was 96.8%, sensitivity –75.0%, specificity –97.6%).

Impaired differentiation of the bowel wall layers, absence/ reduction of peristalsis, pneumatosis, gas in the portal venous system and free fluid in the abdominal cavity had a direct correlation with the probability of developing of NEC stage 2 (p = 0.001, diagnostic effectiveness of the combination of US signs was 82.9% sensitivity –55.6% and specificity –91.4%).

The results of abdominal US with Doppler and assessment of RI SMA and CA in the newborns on days 3 and 7 of life and before the manifestation of NEC are presented in Tables 4 and 5. There were no statistically significant differences in RI of SMA and RI CA on days 3 or 7 between the groups (Table 4). However, it should be noted that RI SMA and RI CA were higher in groups with NEC and GI dyskinesia than in the control group. Patent ductus arteriosus (PDA) was detected in 11/84 (13.1%) infants. PDA was detected more frequently in infants with NEC than in the other groups (Table 5). Newborns with PDA in Groups 1 and 2 had higher values of RI SMA and RI CA on days 3 and 7 than neonates in the control group (Table 5). When comparing Doppler US indicators in newborns with NEC stages 2 and 3 before the manifestation of the disease, RI SMA and RI CA were higher in the presence of PDA. In the absence of PDA, RI SMA and RI CA did not statistically differ between the groups, while the presence of PDA was a significant factor associated with higher RI SMA and RI CA in Group 1 than in the control group (Tables 4–6).

Table 4

Indicators of Doppler in the studied groups on days 3 and 7

Doppler indicators	Group 1	Group 2	Control group	P-value
	NEC (n = 26)	GI dyskinesia (n = 28)	(n = 30)
Day 3
RI SMA, median (IQR)	0.89 (0.71–0.90)	0.88 (0.72–0.95)	0.82 (0.70–0.88)	p₁_,₂ = 0.246
				p₁_,₃ = 0.475
				p₂_,₃ = 0.235
RI CA, median (IQR)	0.86 (0.75–0.88)	0.76 (0.74–0.82)	0.74 (0.72–0.89)	p₁_,₂ = 0.088
				p₁_,₃ = 0.076
				p₂_,₃ = 0.435
Day 7
RI SMA, median (IQR)	0.87 (0.85–1.0)	0.88 (0.86–0.96)	0.84 (0.76–0.92)	p₁_,₂ = 0.296
				p₁_,₃ = 0.723
				p₂_,₃ = 0.235
RI CA, median (IQR)	0.91 (0.90–0.96)	–	0.84 (0.76–0.92)	p₁_,₃ = 0.475

NEC- necrotizing enterocolitis, GI –gastrointestinal, IQR –interquartile ranges, RI SMA –resistive index of the superior mesenteric artery, RI CA- resistive index of the celiac artery.

Table 5

Indicators of Doppler US in newborns with PDA

Doppler US indicators	Group 1	Group 2	Control group	P-value
	NEC (n = 26)	GI dyskinesia (n = 28)	(n = 30)
Newborns with PDA (n = 11)
Day 3
RI SMA, median (IQR)	0.98 (0.90–1.1) n = 5	0.90 (0.89–1.0) n = 3	0.84 (0.76–0.92) n = 3	p_1,2 = 0.283
				p_1,3 = 0.018
				p_2,3 = 0.035
RI CA, median (IQR)	0.91 (0.86–1.0) n = 5	0.88 (0.72–0.95) n = 3	0.80 (0.72–0.90) n = 3	p_1,2 = 0.366
				p_1,3 = 0.046
				p_2,3 = 0.042
Newborns with PDA (n = 11)
Day 7
RI SMA, median (IQR)	0.97 (0.90–1.1) n = 5	0.95 (0.88–1.0) n = 3	0.84 (0.80–0.95) n = 2	p_1,2 = 0.256
				p_1,3 = 0.015
				p_2,3 = 0.024
RI CA, median (IQR)	0.93 (0.90–0.83) n = 3	–	0.82 (0.72–0.94) n = 2	p_1,3 = 0.127

US –ultrasound, NEC- necrotizing enterocolitis, GI –gastrointestinal, IQR –interquartile ranges, PDA –patent ductus arteriosus, RI SMA –resistive index of the superior mesenteric artery, RI CA- resistive index of the celiac artery.

Table 6

Indicators of Doppler US in 1 Group of newborns with and without PDA before the manifestation of NEC

Newborns with NEC (n = 26)	Newborns with PDA (n = 8)	Newborns without PDA (n = 18)	P-value
Doppler US indicators:
RI SMA, median (IQR)	0.97 (0.90–1.1) n = 5	0.89 (0.71–0.90)	0.035
RI CA, median (IQR)	0.93 (0.90–0.83) n = 3	0.86 (0.75–0.88)	0.033

US –ultrasound, NEC –necrotizing enterocolitis, IQR –interquartile ranges, PDA- patent ductus arteriosus, RI SMA –resistive index of the superior mesenteric artery, RI CA- resistive index of the celiac artery.

4 Discussion

In recent years, the number of studies examining abdominal US in cases of suspected NEC has been increasing. Abdominal radiography is still the “reference standard” for diagnosis. However, in very premature infants, the radiographic picture of NEC may be non-specific. US allows visualization of bowel structures in real time, providing additional information through signs that may not be detectable using radiography. Although US is not a new tool, there are many obstacles to its widespread use, including lack of specialists, lack of awareness among clinicians on how to interpret the findings, and insufficient integration of US criteria into clinical practice [9]. Data from international studies suggest that US is an informative method to improve the diagnostic accuracy in NEC [10]. It may identify specific changes in the early stages of the disease, the presence of bowel necrosis before perforation occurs, i.e., at the stage where more aggressive treatment, including surgery, may be helpful. Earlier surgery for advanced NEC stages may result in better outcomes in premature infants [9, 11]. Because it is portable and non-ionizing, repeat studies can be performed without risk. Lazow S.P. et al. [12] assessed and identified four US predictors of NEC stage 3 in 83 infants: erythema of the abdominal wall (OR: 8.2, p = 0.048), gas in the portal venous system (OR: 29.8, p = 0.014), echogenic free fluid in the abdomen (OR: 17.2, p = 0.027) and thickened bowel wall (OR: 12.5, p = 0.030). A meta-analysis of 2018 [13] identified US signs that may be linked with surgery or death in NEC patients. According to our study signs that had a direct correlation with the probability of developing NEC stage 3 and perforation of the bowel wall included thinning and increased echogenicity of the bowel wall, echogenic free fluid in the abdominal cavity and pneumoperitoneum. Both radiographic examination and US revealed free gas in the abdominal cavity. The presence of gas in the portal venous system in most cases was associated with umbilical vein catheterisation. A comparative analysis of the subgroups with and without an umbilical catheter was not carried out due to the small number of patients.

Cuna A. et al. [14] performed a systematic analysis to assess the diagnostic accuracy of US in NEC. The study included 462 infants. The common NEC signs identified by US (gas in the portal venous system, pneumatosis, and free gas in the abdominal cavity) had an overall sensitivity ranging from 0.27 to 0.48 and an overall specificity ranging from 0.91 to 0.99. Thinning of the bowel wall and absence of peristalsis had low sensitivity (0.22 and 0.30) but high specificity (0.96 and 0.96) for NEC. Assessment of free fluid in the abdominal cavity had low sensitivity and high specificity (0.45 and 0.92). Therefore, it was concluded that individual US findings have low sensitivity and high specificity for NEC. In our study, in infants with NEC stage 2, US findings also had relatively low sensitivity and high specificity (55.6% and 91.4%, respectively). Radiographic examination of infants with non-surgical NEC revealed only dilated bowel loops, and, therefore US appeared more informative. However, the US signs should be interpreted in accordance with the clinical and laboratory findings.

US is considered to be effective for assessing not only of the state of the bowel loops and peristalsis, but bowel wall perfusion as well. Aliev M.M. et al. [15] used color abdominal Doppler US in newborns with NEC. Typical signs of NEC stage 2 were pneumatosis, thinning of the bowel wall (less than 1 mm), decrease or lack of bowel peristalsis, and lack of perfusion. In NEC stage 3 there was no bowel peristalsis, pneumatosis of the bowel wall and absence of perfusion. There was one case with gas in the portal venous system. In our study a qualitative assessment of bowel perfusion based on color Doppler US was not performed. We have determined the indicators of arterial bowel blood flow by pulsed wave Doppler. Many studies of this method show contradictory results. Some authors note increased blood flow velocities in SMA and CA in NEC patients compared to healthy infants [16], while others have shown significant decrease of blood flow velocities in bowel arteries in NEC patients [17]. The study by Urboniene et al., showed that increased RI SMA over 0.75 had sensitivity of 96.3% and specificity of 90.9% for NEC diagnosis in premature infants [18], while the study by Guang et al. found no association between RI SMA and NEC [19]. The interpretation of blood flow changes in large arteries, including bowel arteries, is complicated by the state of PDA [20 –22]. In our study, Doppler measurements did not show high diagnostic significance; RI SMA and RI CA values in the studied groups did not differ significantly. The presence of PDA appeared to be an independent factor associated with increased RI SMA and RI CA in all groups, regardless of the presence or absence of NEC. This raises a question whether routine assessment of RI SMA and RI CA is reasonable in ELBW infants. Meanwhile, babies with NEC, compared to other groups, more often had PDA, which may be one of the risk factors for the development of NEC.

4.1 Limitations of this study

First, our study was retrospective, and thus is at risk for selection bias and residual confounding. Second, the current study was based on data from a single Research Center; therefore, the generalizability of our observations may be limited. Third, all imaging, whether plain radiographs or US, is subjective, even though all operators were skilled for evaluation of an infant with NEC. Furthermore, there are no generally agreed specific US signs to determine the diagnostic criteria for NEC, and timing of US follow-up is not yet standardized. Fourth, the challenge is that the criteria include a number of characteristics with varying sensitivity and specificity that are not weighted by the importance to the diagnosis of NEC. This can lead to over- or underestimation of NEC in ELBW infants.

5 Conclusion

Abdominal US is an important supplementary method for diagnosing NEC and its complications, in ELBW infants. Specific US findings of advanced NEC requiring surgery were thinning and increased echogenicity of the bowel wall, echogenic free fluid in the abdominal cavity, and pneumoperitoneum. Milder stages of NEC were characterized by impaired differentiation of the bowel wall layers, absence/reduction of peristalsis, pneumatosis, gas in the portal venous system, and free fluid in the abdominal cavity. Abdominal US should be combined with abdominal radiography as a standard diagnostic imaging algorithm in ELBW infants suspected to have NEC.

5.1 Compliance with ethical standards

The study was approved by the Ethics Committee (Protocol No. 12 of November 17, 2016) and Academic Council (Protocol No. 19 of November 29, 2016) of the National Medical Research Center for Obstetrics, Gynecology and Perinatology named after Academician V.I. Kulakov of the Ministry of Health of the Russian Federation. All participants signed informed consent to participate in the study.

Conflict of interest

The authors declare no conflict of interest.

Funding

No funding.

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