Pregnancy and delivery management in women with congenital heart defects in the fetus: challenges and contemporary approaches

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INTRODUCTION

Congenital heart defects (CHDs) are the most prevalent developmental anomalies in children and remain a leading cause of infant mortality. The prevalence of CHD in children varies widely, ranging from 4 to 50 cases per 1,000 live births [1]. Although most cases of CHD are not life-threatening in utero, fetal death can occur in 20% of cases [2], with an increased risk of adverse pregnancy outcomes including preterm delivery and neurological complications [3, 4]. ЭPotential adverse sequelae have led to increased efforts to detect and monitor CHD during pregnancy to ensure optimal postpartum outcomes. In recent years, rapid advances in intrauterine imaging and fetal surgery allow modifying the course of CHD [5–7]. Currently, fetal cardiac surgery is a multidisciplinary field that contributes to earlier detection of fetal cardiovascular disease that affects neonatal outcomes. However, research on perinatal cardiac care has often been limited to small case series or single-center studies due to the relatively low rates of severe CHD and the historical lack of interdisciplinary collaboration in this area. Therefore, further advances in comprehensive studies and management of fetal CHD will require continued interdisciplinary, multi-center collaboration to optimize outcomes and access to care.

AIM. The aim of this review is to analyze recent publications on advances in the management of fetal and neonatal patients with CHD, including novel approaches to prenatal diagnosis and perinatal care, and to provide recommendations for improved access to specialized care and future research.

METHODS

PubMed, eLibrary, and Google Scholar databases were searched for publications. The following keywords and their combinations were used in both Russian and English: врождённые пороки сердца / congenital heart defects, ВПС/CHD, фетальная кардиология / fetal cardiology, внутриутробная визуализация / intrauterine imaging, фетальная хирургия / fetal surgery. The authors independently reviewed the titles and abstracts of the articles and then extracted the full text of the relevant studies. The review included relevant experimental and clinical studies published in Russian and English.

PRISMA guidelines were used to select articles. The review included all relevant articles published up to September 2024. The search yielded 3,157 articles from PubMed and 1,416 articles from eLibrary. Duplicate and incomplete articles were excluded.

The authors independently evaluated the titles and abstracts of all identified articles. The full text of potentially eligible articles was read for final selection. Any disagreement between authors was settled by consensus. Figure 1 shows the search algorithm.

 

Fig. 1. Study selection algorithm.

 

RESULTS AND DISCUSSION

Prenatal Diagnosis of Fetal Heart Condition

Role of Prenatal Diagnosis of CHD in Pregnancy Outcomes

Studies evaluating the effect of prenatal diagnosis of CHD on mortality rates, especially for ductus-dependent CHD, are inconsistent. A population-based study by Oster et al. [8] found higher mortality rates in newborns with prenatal diagnosis of CHD. The authors hypothesized that prenatal diagnosis could identify difficult-to-treat, high-risk patients, but patients with undiagnosed CHD at the time of death were not included. A meta-analysis by Holland et al. [9] revealed increased mortality rates in patients with a postnatal diagnosis of CHD, especially in the preoperative period. Other studies have found no difference in mortality rates between prenatal and postnatal diagnosis of CHD in the preoperative or postoperative period [4, 10]. However, confounding factors introduce significant selection bias, including a higher potential for severe disease in newborns with prenatal diagnosis and for death before tertiary hospitalization in newborns with postnatal diagnosis of CHD.

Although prenatal diagnosis has no significant effect on fetal/neonatal mortality rates, several studies have shown that patients with a postnatal diagnosis of CHD have more severe preoperative clinical manifestations and are more likely to have neurological complications [4, 11]. Studies conducted by Mahle et al. [12] in patients with hypoplastic left heart syndrome (HLHS) and Peyvandi et al. [11] in patients with HLHS and transposition of the great arteries showed lower rates of neurological complications in patients with prenatal diagnosis of CHD, including a lower risk of intraoperative coma and less severe preoperative brain damage on a magnetic resonance imaging scan. Although there is no evidence that patients with postnatal diagnosis of CHD have higher mortality rates, the simultaneous improvement in perioperative emergency care and surgical management may challenge the use of mortality as an independent outcome measure. Further studies are needed to compare long-term morbidity and mortality in patients with prenatal and postnatal diagnosis of CHD.

Recent Advances in Fetal Cardiac Imaging

The development of earlier and more sensitive and accurate prenatal screening for CHD is an important area of research in fetal cardiology and obstetrics. Recent research has focused on improving standardized prenatal screening and using first-trimester cardiac screening. Fetal cardiac screening is indicated in all pregnancies, usually during an obstetric examination at 18 to 22 weeks of gestation [13]. Current guidelines, including multidisciplinary guidelines published in 2018 by the American Institute of Ultrasound in Medicine (AIUM), American College of Radiology (ACR), American College of Obstetricians and Gynecologists (ACOG), Society for Maternal-Fetal Medicine (SMFM) and Society of Radiologist in Ultrasound (SRU), as well as guidelines published in 2022 by the International Society of Ultrasound in Obstetrics & Gynecology (ISUOG) recommend fetal cardiac screening, including assessment of heart rhythm, heart size/position, ventricles, and ventricular outflow tracts [14, 15]. Doppler ultrasound is also recommended in the updated 2023 ISUOG guidelines [16]. Patients with significant or suspected maternal/fetal risk factors for CHD on ultrasound should be referred to a fetal cardiologist for fetal echocardiography. This diagnostic modality included additional evaluation of the interventricular septum, superior and inferior vena cava, ducts, and aortic arches [16, 17]. Primary fetal echocardiography in patients at high risk for CHD is recommended between 18 and 22 weeks of gestation [16, 18, 19]. However, patients with suspected CHD based on obstetric ultrasound should be referred for earlier evaluation.

The majority of pregnancies resulting in fetal CHD occur in low-risk patients, highlighting the need for careful screening [20]. Routine obstetrics screening provides a virtually universal opportunity to detect CHD. The use of standard cardiac screening views has increased significantly. The four-chamber cardiac view alone detects 30%–60% of congenital heart defects [21], whereas additional evaluation of the ventricular outflow tracts increases sensitivity to 60%–90% [22]. Increased physician awareness and additional cardiac screening capabilities have improved the prenatal diagnosis of CHD [18, 23], but the real-world clinical effectiveness of standardized screening protocols remains suboptimal [24, 25]. Further improvement in CHD diagnosis is limited by center-specific fetal CHD volume and experience, local patient care patterns and disparities in access to care [23].

New approaches, including the use of artificial intelligence (AI), are being actively explored to improve prenatal CHD detection and screening [26]. A recent study by Day et al. [27] compared the performance of an AI-based model with a current screening program for HLHS. The study showed that the AI-based model performed worse. Universal fetal echocardiography has been proposed as an alternative, but low cost-effectiveness, resource allocation, and healthcare accessibility are significant barriers [23]. Further research on prenatal CHD diagnosis and new approaches to increase the sensitivity of obstetric screening are needed to improve fetal cardiac diagnosis.

Historically, device resolution and technology have limited fetal echocardiography in early pregnancy. However, recent advances in ultrasound imaging, including color Doppler, high-resolution high-frequency transducers, and 3D/4D echocardiography [28], as well as improved training and experience of sonographers, allow earlier and more comprehensive cardiac screening, timely access to expert fetal cardiac diagnosis, and selection of appropriate pregnancy and delivery management strategies. Several small studies evaluating the feasibility of early fetal echocardiography in high-risk patients have demonstrated a 60%–95% sensitivity for CHD when performed in the late first and early second trimesters [29, 30]. However, these studies were conducted in large tertiary referral centers with sonographers trained in fetal echocardiography. A retrospective study published in 2024 evaluated the feasibility of first-trimester cardiac screening during routine obstetric ultrasound in a large population of fetuses at low risk for CHD in Denmark [31]. A complete cardiac evaluation was performed in 85% of the total population, but only 25% were diagnosed with CHD in the first trimester [31]. Other studies evaluating early obstetric screening in low-risk groups show detection rates of 50%–70% at 11–14 weeks of gestation using different screening protocols [32, 33].

Current clinical imaging guidelines provide varying recommendations for first-trimester cardiac screening, taking into account established technical limitations and expert needs. The ISUOG recommends local, 4-chamber and 3-vessel views in low-risk groups during the first trimester using a high-frequency transabdominal transducer to optimize resolution [16, 34]. The AIUM recommends first-trimester screening between 12 weeks 0 days and 13 weeks 6 days of gestation for high-risk patients or those with suspected fetal anomalies [35]. The American Society of Echocardiography (ASE) recognizes the possibility of fetal echocardiography in the early second trimester. However, the ASE recommends repeat testing at 18–22 weeks due to the difficulty of comprehensive testing in early pregnancy [36].

Therefore, first trimester screening and early fetal echocardiography between 12 and 16 weeks of gestation are most effective in detecting CHD in high-risk groups or when a cardiac anomaly is suspected. However, its use in real-world clinical settings is limited because the detection rate is still lower than in the later stages of pregnancy and its performance is currently dependent on the doctor experience [31].

Perinatal Cardiology

Multidisciplinary fetal cardiac care is needed to address the complex medical and psychosocial needs of families with a prenatal diagnosis of CHD. Although there are limited data on the effectiveness of multidisciplinary management, active collaboration between specialists allows planning of the place and timing of delivery and postpartum surgery [37]. Despite the established collaboration between fetal cardiologists and obstetricians/gynecologists, the involvement of other specialists in fetal cardiac care is not common. A large survey of 41 quaternary intensive care units evaluated differences in clinical practice for patients with CHD [38]. The study found that the nature and type of collaboration varied widely, but only 31% had regular prenatal consultations with neonatologists [38]. In addition, other specialists were involved in counseling: nurse coordinators in 86% of cases, but social care workers in only 69% of cases, psychologists in 34% of cases, and palliative care specialists in 7% of cases [38]. However, the studies show that involvement of these specialists can reduce anxiety and improve communication and shared decision-making [38–40]. Comprehensive diagnosis and specialized perinatal care involve many specialists, including obstetricians/gynecologists, cardiologists, fetal and cardiothoracic surgeons, radiologists, anesthesiologists, palliative care specialists, medical geneticists, psychologists, and social care workers [41, 42].

It is difficult to conduct robust studies to support the development of comprehensive perinatal cardiac care guidelines because of the relatively low rates of CHD, variable treatment options, and barriers to interdisciplinary collaboration [43]. Recently, consortia have emerged to promote collaboration in perinatal care and research (e.g., Fetal Heart Society) [43]. Multidisciplinary guidelines for the diagnosis and optimal management of prenatally diagnosed CHD have been developed by the American Heart Association (AHA), AIUM, and the International Fetal Medicine and Surgical Society / the North American Fetal Therapy Network (IFMSS/NAFT) [19, 44]. The Fetal Cardiology Task Force of the Association for European Pediatric and Congenital Cardiology has developed fetal cardiology guidelines for European countries, emphasizing the need for collaboration between cardiologists and obstetricians/gynecologists to ensure accurate diagnosis, appropriate support, clear communication, timely management and treatment, and continued research [45]. Several recent studies have evaluated various multidisciplinary management protocols for pregnant women with a fetus with CHD. Wautletet et al. [46] used a multidisciplinary management protocol for pregnant women with univentricular fetuses to standardize prenatal visits, screening, management, and specialist consultations. However, the generalizability of this study is limited because it was conducted in a large center with easy access to highly specialized care. Ronai et al. [37] evaluated the effectiveness of a multidisciplinary model including fetal cardiology, neonatology, and genetic counseling. No newborns required unexpected interventions, confirming the ability of the model to accurately predict postnatal physiology and influence perinatal management/outcomes [37]. A retrospective study conducted by the University of California Fetal-Maternal Consortium found that a standardized clinical evaluation and management plan resulted in higher rates of vaginal delivery (61% vs. 50%) and term delivery (48% vs. 34%) [47].

Multidisciplinary pregnancy management models are feasible and can impact critical CHD outcomes. Maternal and neonatal safety is essential, and special attention is given to effective monitoring of a fetus with CHD through the collaborative efforts of cardiologists, neonatologists, obstetricians/gynecologists, and other specialists [48]. Multidisciplinary teams provide high-quality care, comprehensive and timely support, and ongoing psychosocial support [38]. The development of healthcare algorithms and consensus clinical guidelines helps to standardize team-based prenatal care to reduce maternal risk, improve neonatal outcomes, and reduce healthcare costs [47, 48]. Future research should focus on a clear consensus on effective interdisciplinary care and consider ways to improve its accessibility.

Prenatal Counseling

Once CHD is diagnosed, the next important step for fetal cardiologists and obstetricians/gynecologists is to provide timely and accurate support. Counseling is an integral part of pediatric cardiology and requires special knowledge of echocardiography, cardiac physiology, prenatal and postnatal treatment options, and long-term management and outcomes of CHD. The 2014 AHA Scientific Statement on the Diagnosis and Treatment of Fetal Cardiac Disease highlights the role of counseling and psychosocial support following the diagnosis of fetal CHD [49]. In addition, Williams et al. [50] found that prenatal diagnosis improved parental awareness of neonatal CHD even with formal education, highlighting the importance of such counseling to provide a basis for informed parental involvement. Despite the essential role of prenatal counseling, there are few relevant studies on the most effective counseling techniques and several relevant guidelines.

A few small studies evaluated prenatal counseling needs from the parents’ perspective, including perceptions of important counseling topics and their impact on actual parental awareness. Kovacevic et al. [51, 52] developed a questionnaire to assess parents’ counseling needs and found that only 45% of patients considered counseling successful. The results showed that medical information was difficult to understand during communication, but comprehension could be improved by providing patients with written handouts, increasing the length of the consultation, and providing a private room [51, 52]. In a small Swedish study by Bratt et al. [53], parents were interviewed after prenatal diagnosis of CHD to assess the content and structure of the consultations. Parents were found to appreciate the understanding of the CHD diagnosis, practical advice about the birth and future daily living of their child, and the opportunity to communicate with others in a similar situation. Timely and understandable face-to-face information, especially visual, was critical [51–54]. Finally, Arya et al. [55] interviewed parents of older children with CHD and compared their prenatal education / counseling expectations with those of cardiologists. In general, parents consistently rated educational issues as more important than cardiologic ones, with the most significant differences in the quality of life, including lifelong surgeries, need for transplantation, exercise limitations, and potential impact on future family history of CHD [55]. Studies are inconclusive about how much information should be given to patients; too much information may increase anxiety, whereas too little information may affect the perception of the diagnosis [55]. However, both parents and cardiologists considered it important to understand heart disease nomenclature, postpartum intervention options, short- and long-term survival, comorbidities, and health care options [55]. Parents always appreciate being informed, especially about future outcomes and quality of life [53–55].

Two recent studies evaluated 3D printing to improve practical understanding compared with standard counseling [56, 57]. Although parents find 3D models useful and helpful in communicating with healthcare professionals, the effectiveness of these models in improving parental awareness of CHD anatomy and surgical options remains controversial [56, 57]. These studies suggest the potential use of new methods to improve prenatal counseling.

A multidisciplinary approach plays a critical role in clinical decision-making. Current practice includes consultation with specialists experienced in prenatal and postnatal diagnosis and management of CHD. However, provision of honest and accurate information about the diagnosis, prognosis, and potential treatment options, as well as timely and ongoing dialogue with parents should be a priority [54, 58]. Visual aids such as diagrams and models can help assess the level of knowledge that parents have about the disease. In addition, a multidisciplinary team ensures a consistent approach and a wide range of support tools that contribute to the achievement of management goals [54, 58]. Therefore, further research and guidelines are needed to improve the effectiveness of intrauterine counseling and training of fetal cardiologists.

Several recent studies have shown that prenatal diagnosis of CHD increases maternal stress during pregnancy and for several months after delivery [59, 60]. Maternal stress can affect fetal health through growth and development, risk of preterm delivery, and postnatal neurodevelopment [59, 61, 62]. However, parent surveys consistently show a preference for prenatal diagnosis over postnatal diagnosis [60, 63]. Maternal stress/anxiety/depression can be prevented by maternal social support from the social environment [61] and consultation with qualified psychologists [64].

Labor Management

Optimal management of the mother and fetus with CHD dyad is the goal of multidisciplinary perinatal cardiac care. Key components of such management include planning the place, timing, and mode of delivery, based on the impact on both mother and fetus. This area of perinatal care requires close interaction between different specialists, although data on the effectiveness of multidisciplinary labor management are limited [37].

The high rates of preterm delivery in pregnancies complicated by CHD, due to intrauterine and maternal causes, persist and affect infant morbidity and mortality [65]. Therefore, induced labor or cesarean section for prenatal diagnosis of CHD is often coordinated by tertiary referral centers and is considered safe after 37 weeks of gestation [66]. However, analysis of full-term newborns with CHD born between 37 and 40 weeks of gestation shows further reductions in hospital length of stay, pulmonary complications, and mortality with each additional week of gestation [49, 66–68]. These data suggest that morbidity and mortality are reduced with later gestation, so delivery should occur closer to 40 weeks of gestation whenever possible. Therefore, most fetal cardiologists recommend watchful waiting until 39 weeks of gestation to plan delivery, minimize morbidity and mortality, and coordinate care. Despite this generalization, delivery recommendations should be specific to CHD. For example, in certain types of CHD, including Ebstein anomaly, tetralogy of Fallot with absent pulmonary valve, or any diagnosis with severe valvular regurgitation, delivery before 39 weeks of gestation should be considered due to the increased risk of intrauterine fetal death [69].

Some studies evaluated delivery methods in pregnancies with CHD, including vaginal delivery, induction of labor, planned cesarean section, and cesarean section after trial of labor, and found no differences in overall Apgar scores, duration of preoperative intubation, metabolic acidosis, length of hospital stay, or mortality [68, 70–74]. In addition, a study of patients with HLHS found no differences in the need for intensive care based on mode of delivery [71]. A trial of labor with careful maternal-fetal monitoring by an experienced obstetric team and prompt access to neonatal intensive care is warranted because a fetus with CHD is often stable in utero [71, 72].

The choice of a place of delivery should balance the ability to safely monitor the mother and fetus with easy access to tertiary care. Studies of newborns with ductus-dependent CHD show that delivery near a cardiac surgery center (<10 min) is associated with lower preoperative mortality [49, 75]. However, another study compared delivery in a tertiary referral center with delivery in other types of centers and showed no difference in mortality rates for newborns with duct-dependent CHD [76]. Therefore, studies provide inconsistent data on neonatal outcomes associated with the place of delivery. The current standard of care is to recommend a place of delivery near, but not necessarily in, a cardiac surgery center. However, delivery in a cardiac surgery center is recommended for newborns requiring immediate postnatal intervention, such as newborns with total anomalous pulmonary venous drainage or HLHS with patent foramen ovale or intact atrial septum. In some cases, this may require the mother to relocate prior to the estimated date of delivery. Maternal health studies show that pregnancies complicated by fetal CHD are at increased risk for maternal morbidity, including intensive care unit admission, need for blood transfusion, unplanned surgery, and hospital transfer, even after adjustment for known risk factors [77]. This study emphasizes the need for multidisciplinary discussion of safe place of delivery based on the risks associated with differences in maternal and neonatal care between centers. In some countries, multidisciplinary clinics have been established to manage these patients, driven by collaborative protocols between fetal cardiologists and obstetricians/gynecologists and an increasing interest in delivering infants as close as possible to medical centers that can provide timely postpartum care. Further studies to evaluate the performance of these clinics, including maternal and neonatal outcomes, will help inform future guidelines for CHD management.

The choice between early and delayed umbilical cord clamping in newborns with CHD is a special focus of labor management. A risk–benefit ratio of delayed cord clamping has been well studied in healthy preterm infants. However, there are limited data in infants with CHD, who have increased fluid overload and blood viscosity due to increased volume and concentration overload [78]. A small pilot randomized controlled trial of 30 critically ill neonates with CHD, published in 2015 by Backes et al. [79], demonstrated that delayed umbilical cord clamping is safe and feasible. No differences were found in specific safety parameters such as Apgar score, bilirubin, preoperative mortality and polycythemia, and postoperative morbidity [79]. Another retrospective study by Fite et al. [78] reviewed the medical records of 160 critically ill newborns with CHD and found no differences in pre- or postpartum hemoglobin levels with delayed versus early umbilical cord clamping. These studies suggest that delayed umbilical cord clamping should be recommended whenever possible, based on its safety profile and potential benefit in the early postpartum period. However, further studies evaluating long-term outcomes are needed to confirm whether this practice should be recommended.

Fetal Surgery Techniques

Some infants with CHD require prenatal cardiac surgery with timely involvement of fetal cardiologists. Fetal cardiac surgery is a rapidly evolving area of CHD treatment, both to improve prenatal/postnatal survival and to stop disease progression [80]. In Russia, intrauterine treatment of CHD is performed only at the Almazov Federal Center of Heart, Blood, and Endocrinology, St. Petersburg (isolated surgeries), in Irkutsk and Yekaterinburg. It is currently difficult to evaluate the effectiveness and availability of fetal cardiac surgery due to the relatively low rates of treatable fetal CHD and the limited number of medical centers with sufficient capacity and experience to achieve optimal outcomes [7, 81]. In this area, medical care has become regionalized with the emergence of specialized centers for fetal cardiac surgery [44]. These medical centers provide the multidisciplinary care necessary for successful fetal cardiac surgery, but their lack creates problems with access to surgical care [7, 44]. In addition, this limitation justifies the importance of interagency consortia and registries to promote collaboration and transparency in fetal cardiac surgery and scientific research [44].

Role of Socioeconomic Factors

Access to prenatal diagnosis, perinatal management and cardiac care is critical due to a trend toward institutionalization. Socioeconomic factors are one of the elements that influence the availability of healthcare, which can lead to adverse maternal and infant outcomes [82–84]. High social deprivation is associated with later ultrasound screening, longer interval between screening ultrasound and fetal echocardiography, and later diagnosis of CHD, according to studies evaluating the association between socioeconomic factors and access to fetal cardiac care [82, 83]. These findings were confirmed by Krishnan et al. [85], who found that the lower socioeconomic quartile was associated with lower rates of prenatal diagnosis of HLHS and transposition of the great vessels. Delayed fetal diagnosis or failure to recognize a critical stage of CHD may affect safe delivery planning and, consequently, postpartum outcomes. In addition, the potential need to relocate for delivery may create additional challenges for the family in some types of CHD. Early pregnancy screening for social determinants to ensure timely multidisciplinary support and access to care is now recognized as an important healthcare issue. In addition, a recent American Heart Association/American College of Cardiology (AHA/ACC) report recognizes the importance of these factors and provides definitions of cardiac-related social determinants of health (SDOH) and a thorough review of specific data elements useful in researching the impact of SDOH at the intrapersonal, interpersonal, and societal levels [86]. This new document standardizes future research on SDOH and the impact of SDOH on the prenatal CHD management.

CONCLUSION

Rapid advances in fetal cardiac diagnosis, perinatal maternal-fetal monitoring, and fetal surgery have significantly improved the course of pregnancy and maternal-fetal/neonatal outcomes in CHD. Early fetal echocardiography and routine obstetric screening have improved the early identification of pregnancies complicated by CHD. Novel approaches to prenatal counseling are explored and standardized algorithms are developed to optimize fetal cardiac care and ensure multidisciplinary perinatal family support and labor management. Fetal cardiac surgery is effective in only a small population of patients with CHD, and access to care is still limited to few tertiary referral centers. However, broader access to other fetal cardiac surgery options offers opportunities to improve both prenatal and postnatal CHD outcomes. Future progress will require multidisciplinary and multicenter collaboration to advance research, optimize CHD outcomes, and ensure access to high-quality fetal cardiac care.

ADDITIONAL INFORMATION

Authors’ contribution. I.O. Bedoeva, L.K. Pagieva: collection and analysis of literary data, scientific editing of the manuscript; M.T. Shamsueva, Yu.P. Nemkova: collection and analysis of literary data, writing the manuscript; M.M. Shigalugova: analysis of literary data, editing the text of the manuscript; B.I. Plieva: data analysis, editing and approval of the text; M.V. Kudzieva: writing a manuscript, extracting and analyzing literary data; A.M. Kireychev: editing the text of the article, analyzing literary data; D.E. Kanbekova: collecting literary data, writing the text of the article; I.I. Abramov: approval of the final version of the manuscript, editing the text of the article; V.V. Kortieva: analysis of literary data, assistance in writing the article; M.V. Ustinova, Z.M. Magomedova: analysis of literary data, assistance in writing the article, editing and approval of the final version of the article. All authors confirm that their authorship meets the international ICMJE criteria (all authors have made a significant contribution to the development of the concept, research and preparation of the article, read and approved the final version before publication).

Funding source. This study was not supported by any external sources of funding. The study was carried out within the framework of interuniversity cooperation in the scientific community of the Department of Obstetrics and Gynecology No. 1 of the Bashkir State Medical University.

Disclosure of interest. The authors declares that there are no obvious and potential conflicts of interest associated with the publication of this article.

About the authors

Irina O. Bedoeva

North-Ossetian State Medical Academy

Author for correspondence.
Email: bestielal@rambler.ru
ORCID iD: 0009-0003-0232-9475

Student

Russian Federation, 40 Pushkinskaya st, Vladikavkaz, 362025

Lika K. Pagieva

North-Ossetian State Medical Academy

Email: pagievalika@yandex.ru
ORCID iD: 0009-0002-7448-0994

Student

Russian Federation, 40 Pushkinskaya st, Vladikavkaz, 362025

Medina T. Shamsueva

North-Ossetian State Medical Academy

Email: Shamsuevam@mail.ru
ORCID iD: 0009-0007-6853-9095

Student

Russian Federation, 40 Pushkinskaya st, Vladikavkaz, 362025

Yulia P. Nemkova

N.I. Pirogov Russian National Research Medical University

Email: ulianemkova523@gmail.com
ORCID iD: 0009-0005-2784-980X

Student

Russian Federation, Moscow

Milana M. Shigalugova

North-Ossetian State Medical Academy

Email: milanashigalugova07@gmail.com
ORCID iD: 0009-0009-5296-0920

Student

Russian Federation, 40 Pushkinskaya st, Vladikavkaz, 362025

Bella I. Plieva

North-Ossetian State Medical Academy

Email: bellapl@mail.ru
ORCID iD: 0009-0004-7466-7809

Student

Russian Federation, 40 Pushkinskaya st, Vladikavkaz, 362025

Mariya V. Kudzieva

North-Ossetian State Medical Academy

Email: kudzieva1@mail.ru
ORCID iD: 0009-0001-6082-5050

Student

Russian Federation, 40 Pushkinskaya st, Vladikavkaz, 362025

Aleksey M. Kireychev

N.I. Pirogov Russian National Research Medical University

Email: KirAlex2000@yandex.ru
ORCID iD: 0009-0007-6486-9505

Student

Russian Federation, Moscow

Darya E. Kanbekova

Bashkir State Medical University

Email: grilonova@gmail.com
ORCID iD: 0009-0003-9291-0537

Student

Russian Federation, Ufa

Igor I. Abramov

Tula State University

Email: ai89190742045@yandex.ru
ORCID iD: 0009-0001-8556-1346

Student

Russian Federation, Tula

Victoria V. Kortieva

Rostov State Medical University

Email: 220300viktoria@mail.ru
ORCID iD: 0009-0007-6491-760X

Student

Russian Federation, Rostov-on-Don

Milena V. Ustinova

Kuban State Medical University

Email: gmilaaaaa@mail.ru
ORCID iD: 0009-0000-8528-5022

Student

Russian Federation, Krasnodar

Zirifa M. Magomedova

Dagestan State Medical University

Email: miss.zirifa@yandex.ru
ORCID iD: 0009-0009-6945-8128

Student

Russian Federation, Makhachkala

References

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