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Online ISSN
1305-3124

Established
1993

Editors-in-Chief
​Cihat Şen, ​Nicola Volpe

Editors
Cecilia Villain, Daniel Rolnik, M. Mar Gil

Managing Editors
Murat Yayla, Oluş Api

Statistics Editor
Resul Arısoy

Article info

Has the COVID-19 delayed the diagnosis of fetal anomalies and reduced in the follow-up of high-risk pregnancies?. Perinatal Journal 2022;30(2):- DOI: 10.2399/prn.22.0302003

Author(s) Information

Eda Özden Tokalıoğlu,
Şule Göncü Ayhan,
Fatma Didem Yücel Yetişkin,
Deniz Oluklu,
Berchan Besimoğlu,
Esin Merve Erol Koç,
Betül Yakıştıran,
Atakan Tanaçan,
Elif Gül Eyi,
Özlem Moraloğlu Tekin,
Dilek Şahin

  1. Department of Obstetrics & Gynecology, Ankara City Hospital, Ankara, Turkey
Correspondence

Eda Özden Tokalıoğlu, Department of Obstetrics & Gynecology, Ankara City Hospital, Ankara, Turkey, [email protected]

Publication History

Manuscript Received: February 18, 2022

Manuscript Accepted: March 08, 2022

Earlyview Date: March 08, 2022

Conflicts of Interest

No conflicts declared.

Objective
COVID-19 has deeply affected our lives in social, economic, education, health issues. Pregnant women have had concerns about routine antenatal care visits and decreased follow-up numbers due to concern of COVID-19 transmission. We aimed to evaluate whether there is a delay in the diagnosis of fetal anomaly during the COVID-19 pandemic period, whether patients diagnosed with fetal anomaly attend antenatal care regularly and to investigate the factors that prevent them from regular follow-up. 
Methods
Pregnant women diagnosed with fetal anomaly during pandemic period (01 March 2020- 01 September 2020) and diagnosed with fetal anomaly before pandemic period (01 September 2019- 28 February 2020) were compared with a questionnaire in terms of antenatal follow-up frequency and gestational week of fetal anomaly diagnosis. 
Results
In the during pandemic period group, regular pregnancy follow-up was decreased from 87% to 51% because of maternal anxiety, fear of virus transmission in hospital and the anxiety of passing it on to baby. Attending a detailed ultrasound scan for detecting fetal anomaly at 18-22 weeks was significantly lower in the during pandemic group. In the pandemic period, the most commonly diagnosed fetal anomalies were central and peripheral nervous system, cardiovascular and gastrointestinal system anomalies similar to the before pandemic period. The mean frequency of follow-ups in the third trimester in the before pandemic period group and during pandemic period group were 6.02 (±2.36) times and 4.02 (±1.97) times, respectively and it was a considerable and statistically significant decrease. In addition, the mean week of fetal anomaly diagnosis was 23±6 weeks in during pandemic group, while it was 22±5 weeks in before pandemic group, and there was no statistically significant difference. 
Conclusion
Antenatal follow-up of the patients has been decreased significantly during the pandemic period, although it does not seem to cause delay in the diagnosis of fetal anomaly. In experienced perinatal centers, if the concerns of patients are relieved and they are examined under suitable conditions for the pandemic, there will be no delay in diagnosis of fetal anomalies. 
Keywords

fetal anomaly, antenatal care, COVID-19, prenatal screening

Introduction
COVID-19 was declared as a pandemic by the World Health Organization and since that time, it has deeply affected our lives in social, economic, health, education issues [1]. The public has instructed to stay at home and reduced hospital admissions for non-emergency situations by authorities. In Turkey, lockdowns were imposed, the number of outpatient clinic visits and examination hours was reduced, the number of attendants for inpatients was limited, and elective surgeries were postponed.
Pregnant women had to consider both their own health and the health of the fetus during the pandemic and the uncertainty about how the disease would affect the course of pregnancy also created a source of stress and anxiety [2, 3]. Because of this reason, they have had concerns about routine antenatal care visits and decreased follow-up numbers due to concern of COVID-19 transmission [4]. This situation can be at least as harmful as the COVID-19 disease itself.
During the pandemic, many obstetric associations have suggested and limited antenatal care visits with first trimester scan in 11-13th weeks, detailed ultrasound screening in 20-22nd weeks, laboratory tests and vaccines at 28th week, group B streptococcus and HIV screening at 36th week and other visits via telehealth systems [5, 6].  In our country, it has reduced the number of antenatal care by following these recommendations. However, it was not possible to limit the number of follow-ups of pregnant women who were followed up by high-risk pregnancy units. Delayed diagnosis and interventions at pregnancies with fetal chromosomal or structural anomalies can lead to negative consequences on both mother and fetus health [7].
There are a limited number of studies on obstetric follow-up and fetal anomaly diagnosis and treatment in the literature [8-10]. In none of these studies, the week of fetal anomaly diagnosis, the frequency and factors affecting the frequency of antenatal follow-ups of pregnancies with fetal anomalies in the pandemic process were mentioned.  We aimed to evaluate whether there is a delay in the diagnosis of a fetal anomaly during the COVID-19 pandemic period, whether patients diagnosed with fetal anomaly attend antenatal care regularly and to investigate the factors that prevent them from regular follow-up. 
 
Methods
In this questionnaire-based study, 100 pregnant women diagnosed with fetal anomaly during the pandemic period (DPP) (01 March 2020- 01 September 2020) and 100 pregnant women diagnosed with fetal anomaly before the pandemic period (BPP) (01 September 2019- 28 February 2020) were included. The study was approved by Turkish Ministry of Health (T18_44_28) and Ankara City Hospital Ethics Committee (E1-20-1145). The questionnaires were applied to the first group diagnosed with a fetal anomaly in the pandemic period at the high-risk pregnancy outpatient clinic. The second group diagnosed with fetal anomaly before the pandemic period was asked questions by phone.
Our questionnaire consisted of 3 parts. In the first part of the questionnaire, questions were asked to the patients in order to determine their demographic characteristics, in the second part their clinical characteristics, in the third part their compliance with pregnancy follow-up.
Statistical analyses were performed by Statistical Package fort he Social Sciences version 25.0 (IBM Corp., Armonk, NY, USA). Visual (histograms, probability plots) and analytical methods ( Shapiro-Wilk’s test) were used in order to determine normality of distribution. Since our data were not in normal distribution, we presented medians and interquartile range values for descriptive analysis. We used Mann- Whitney U test to compare two groups for non-normally distributed parameters.  Pearson’s Chi-Square test was performed to compare categorical variables among the groups. Additionally, Fisher’s exact test was used for nominal variables between groups when necessary. We used percentages to express categorical variables. Correlation analysis was performed by Pearson’s test. P value<0.05 was regarded as statistically significant. The sample size was calculated by G-Power; for an alpha of 0.05 with 90% power gave an effect size of 0.3, requiring a minimum of 91 subjects per group.
Results
Descriptive characteristics of the patients were given in Table-1. Descriptive characteristics were not significantly different between the two groups. There was no difference between before and during the pandemic period in terms of folic acid, vitamin D, multivitamin and antianemic intake as recommended by the government’s health system (Table-2).
In the DPP group, regular pregnancy follow-up was 87% before pandemic which was decreased to 51% during the pandemic period. In DPP group, 43 of 49 patients who did not come to follow-up regularly, stated COVID-19 as the reason for not coming to follow-up, remaining 6 patients stated the reasons as difficulty in transportation to the hospital, familial problems, and lack of knowledge about the follow-up (Table-2).
When the two groups were compared, attending first trimester scan, second trimester scan and oral glucose tolerance test was not significantly different (p> 0.05).  However, attending a detailed ultrasound scan for detecting fetal anomaly at 18-22 weeks was significantly lower in the pandemic group (p = 0.01) (Table-3). Comparing the two groups, the mean frequency of follow-ups in the third trimester in the BPP and DPP were 6.02 (±2.36) times and 4.02 (±1.97) times, respectively and a considerable and statistically significant decrease in the frequency of follow-up in the DPP was found (p< 0.001).
Distribution of the fetal anomalies was shown in Table-4. In the pandemic period, the most commonly diagnosed fetal anomalies were central and peripheral nervous system, cardiovascular and gastrointestinal system anomalies similar to the before pandemic period. In the DPP and BPP groups, the mean weeks of fetal anomaly diagnosis were 23 ± 6 and 22 ± 5, respectively and there was no statistically significant difference between the two groups (p= 0.636).
A weak positive correlation was found between spouse education status, folic acid intake and frequency of follow-up in the third trimester after pandemic (r= 0.179 and p=0.01 for spouse education status and r=0.147 and p=0.03 for folic acid intake). There was a weak negative correlation for gravida and a strong positive correlation for fetal anomaly history in previous pregnancies was found with regular pregnancy follow-up after pandemic (r=- 0.220 and p=0.02 for gravida and r=1.000 and p<0.001 for fetal anomaly diagnosed in previous pregnancies). 
Discussion
The present study revealed there was a decrease in pregnancy follow-up because of maternal anxiety, fear of virus transmission in hospital, the anxiety of passing it on to the baby. Besides, this study demonstrated that the reduction in prenatal visits did not cause a delay in the diagnosis of fetal anomaly.
In the pre-pandemic period, the frequencies of regular antenatal follow-up of the two groups were found to be similar. While pregnant women in the DPP group regularly attended pregnancy follow-ups before the pandemic, in the post-pandemic period the frequency of regular antenatal follow-ups was decreased. This result strongly supported our concern that pregnant women have not received adequate antenatal care at the time of the pandemic. Peahl et al. found a 31.6% decrease in the antenatal visit frequency between the pre-pandemic period and the post-pandemic period similar to our result [11]. In a study, it was determined that the number of admissions to cardiology outpatient clinics for all reasons decreased during the pandemic period [12]. In a recent study about pediatric cancers, 3 children with hematologic cancer who were late in admission to the hospital because of COVID-19 and came in a life-threatening situation were presented [13]. Snapiri et al. presented seven children with delay on diagnosis of complicated appendicitis because of parental concern, telemedicine use and insufficient evaluation [14]. The decrease in the number of hospital admissions and delayed diagnosis seems to have affected due to pandemic affected not only pregnant women but also other patient groups.
The mean week of fetal anomaly diagnosis was 23 weeks in the post-pandemic group, while it was 22 weeks in the before pandemic group, and there was no statistically significant difference contrary to assumption. Our hospital is a tertiary center with a high capacity that receives referrals from all over the region. We did not reduce the number of outpatient clinics or patients even during the peak of he pandemic. In our opinion, because of these reasons there was no delay in the diagnosis of fetal anomalies.
There was no difference between before and during the pandemic period in the use of folic acid, vitamin D, multivitamin and antianemic. The reason for this was probably that the use of these drugs is supported within the government health policy and patients can get these drugs without prescriptions from health centers and family physicians without going to the hospital.
Although the rates of first trimester scan, second trimester scan and oral glucose tolerance test were similar in the pre and post-pandemic group, it was observed that the detailed ultrasonography rate decreased statistically significantly in the post-pandemic group. The reason for the decrease may be social distance is the least and time is the longest in the detailed ultrasonography among the antenatal screening test.
In our study, while the rate of the invasive procedures was 17% in the group diagnosed with fetal anomaly before the pandemic, the rate was 16% in those diagnosed during the pandemic period, and we did not observe any significant decrease. The reason for this may be that most of our patients are referred from other centers and our perinatology clinic is the highly experienced last step center. In addition, we informed the patient in detail that fetal diagnostic procedures are time sensitive and delaying them may worsen outcome for pregnant and fetus. In a review conducted by Deprest et al., it was stated that the risk of spontaneous vertical transmission of the coronavirus for invasive diagnostic procedures is minimal and unproven. They concluded that the risk of vertical transmission should not prevent minimally invasive procedures such as chorionic villus sampling or amniocentesis (8).
In the DPP group, there was a significant decrease in antenatal follow-ups in the third trimester. After the diagnosis of fetal anomaly, most of the patients disrupted their follow-ups in the third trimester during the pandemic period. In addition to this, while there was not a correlation between maternal educational status, a positive correlation was found between the education status of the spouse and the frequency of follow-up in the third trimester. In our society, because of cultural factors paternity factors are very important for issues of perinatal care.
A negative correlation was found between the patient's gravida and the frequency of follow-up during the pandemic period. As the patient's gravida decreases, her concerns about the baby may be weighed down to her concerns about the COVID-19. There was a positive correlation between follow-up during the pandemic period and fetal anomaly history in previous pregnancies. In many studies, anxiety and stress levels were found to be very high in mothers with disabled children [15, 16]. In addition to maternal anxiety, patients who had a disabled child was diagnosed with fetal anomaly during antenatal follow-up in their previous pregnancy may have increased trust in the antenatal care and screening tests.
Conclusion
In conclusion, antenatal follow-up of the patients has been decreased significantly during the pandemic period, although it does not seem to cause delay in the diagnosis of fetal anomaly. In experienced perinatal centers, if the concerns of the patients are relieved and they are examined under suitable conditions for the pandemic, there will be no delay in the diagnosis of fetal anomalies. Our study is valuable since there are very few studies in the literature about how prenatal follow-ups are being affected during the pandemic period and there is no study on the follow-up of pregnant women diagnosed with a fetal anomaly.
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File/Dsecription
Table-1
Comparison of descriptive characteristics of pregnant women diagnosed with fetal anomaly during pandemic period (group 1) and pregnant women diagnosed with fetal anomaly before pandemic period (group 2)
Table-2
Comparison of clinical characteristics of pregnant women diagnosed with fetal anomaly during pandemic period ( group 1 ) and pregnant women diagnosed with fetal anomaly before pandemic period ( group 2)
Table-3
Comparison of compliance for antenatal follow-up of pregnant women diagnosed with fetal anomaly during pandemic period ( group 1 ) and pregnant women diagnosed with fetal anomaly before pandemic period ( group 2)
Table-4
Comparison of fetal anomalies between pregnant women diagnosed with fetal anomaly during pandemic period ( group 1 ) and pregnant women diagnosed with fetal anomaly before pandemic period ( group 2)