The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational&nbsp;study

Othman Sami Salih; Manal Khalid Abdulridha

doi:10.12688/f1000research.131229.1

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Research Article

The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study

[version 1; peer review: 2 approved with reservations, 1 not approved]

Othman Sami Salih ¹, Manal Khalid Abdulridha¹

PUBLISHED 27 Feb 2023

Author details Author details

¹ Department of Clinical Pharmacy, College of Pharmacy, Mustansiriyah University, Baghdad, 14022, Iraq

Othman Sami Salih
Roles: Conceptualization, Data Curation, Formal Analysis, Methodology, Project Administration, Software, Writing – Original Draft Preparation

Manal Khalid Abdulridha
Roles: Conceptualization, Methodology, Software, Supervision, Validation, Visualization, Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS

This article is included in the Emerging Diseases and Outbreaks gateway.

Abstract

Background: COVID-19-infected pregnant women may be asymptomatic or symptomatic. Symptomatic tend to have a severe infection and could be at increased risk of complications such as preterm birth, NICU, and stillbirth. This study aimed to identify the most common signs and symptoms and assess the pre-existing risk of COVID-19 infection during pregnancy: length of hospital stay, premature labor, and complications according to the severity of COVID-19 illness.
Methods: This retrospective study was conducted in the obstetric and gynecological wards of 359 pregnant women. After reviewing medical records, patient and disease data were collected.
Results: Most patients were asymptomatic and mild. The most common signs and symptoms were fever, cough, and dyspnea. COVID-19 infected pregnant with a medical history of hypertension, or diabetes had more severe COVID-19 infection. COVID-19-infected pregnant women with severe illness or aged ≥ 40 years had a prolonged hospital stay. Severe COVID-19 disease was significantly associated with preterm birth, stillbirth, and the need for a neonatal intensive care unit.
Conclusion: Severe COVID-19 infection in pregnancy is linked to pregnancy and birth complications, mainly among pregnant women with a positive medical history.

Keywords

COVID-19, pregnancy, pregnancy outcomes, risk factors, severity

Corresponding author: Othman Sami Salih

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2023 Sami Salih O and Khalid Abdulridha M. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Sami Salih O and Khalid Abdulridha M. The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study [version 1; peer review: 2 approved with reservations, 1 not approved]. F1000Research 2023, 12:220 (https://doi.org/10.12688/f1000research.131229.1) First published: 27 Feb 2023, 12:220 (https://doi.org/10.12688/f1000research.131229.1) Latest published: 27 Feb 2023, 12:220 (https://doi.org/10.12688/f1000research.131229.1)

Introduction

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the source of the coronavirus disease 19 (COVID-19), a highly contagious and dangerous viral illness that led to a global pandemic a significant loss of human life.¹ Severe acute respiratory syndrome coronavirus infection in pregnant women can cause either asymptomatic or symptomatic disease (mild, moderate, severe, and critical).²^,³ Although the risk of developing severe illness is minimal, pregnant women with COVID-19 are more likely to do so than non-pregnant people. In addition, after adjusting for age, race/ethnicity, and underlying medical conditions, pregnant women had noticeably higher rates of intensive care unit (ICU) admission, mechanical ventilation, extracorporeal membrane oxygenation, and mortality.⁴

Contrary to pregnant and previously pregnant women without the illness, COVID-19-positive pregnant women had a higher risk of stillbirth and preterm birth.⁵ In addition, pregnancy-related physiological and immunological changes substantially impact the severity and effects of viral infections.⁶ For example, increased ACE2 expression, changes in the immune system to ensure the acceptance of the fetus, and changes in the respiratory system causing hyperventilation are all factors that could enhance vulnerability to COVID-19 infection during pregnancy.⁷

Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms. Being overweight or obese, being older than 35 years, and having pre-existing comorbidities (hypertension, diabetes, lung diseases) are all variables that increase the risk of developing a severe illness.⁸ To determine how long COVID-19 patients stay in hospitals, it is critical to examine their risk factors. According to a study from China in 2022, patients aged ≥ 45 and those with severe COVID-19 infection tended to stay longer in the hospital.⁹

The advantages of COVID-19 immunization, which include a decreased risk of severe illness and hospitalization for the pregnant woman and a reduced risk of hospitalization for the newborn in the first six months of life, should be discussed with expectant mothers.¹⁰ All eligible individuals, including those who are pregnant, nursing, or planning a pregnancy, should receive a COVID-19 vaccine or a series of vaccines, according to recommendations from the Society for Maternal-Fetal Medicine, American College of Obstetricians and Gynecologists, and CDC. If a person is qualified, the booster dosages are also included.¹¹ The primary objectives of this study were to identify the most common symptoms associated with COVID-19 infection during pregnancy and assess the pre-existing risk of hospitalization, preterm delivery, and other complications related to COVID-19 illness, taking into account the severity of the disease.

Methods

Ethical considerations

The institutional scientific and ethical committees of the Faculty of Pharmacy, Mustansiriyah University, and the Baghdad Health Directorate, Al-Karkh, formally approved the research protocol on November 10, 2021 (Ethics Board approval code: 2021099).

Consent

Since the data has been anonymized, and because it is impracticable to obtain consent. The ethical committee waived the need for consent to participate. There is sufficient protection of participants’ privacy and an adequate plan to protect the confidentiality of data.

Study design

This observational retrospective study was carried out in the obstetrics and gynecology wards of Al-Yarmouk Teaching Hospital and Karkh Hospital for childbirth between November 15, 2021, and August 27, 2022, where pregnant women with COVID-19 were admitted to the hospital for treatment or to give birth.

Sample size

The sample size was determined and computed using the computer application G*Power 3.1.9.7 (RRID: SCR 013726). The smallest total sample size was 314 patients, with an effect size of 0.20 and 95% power at a two-tailed alpha of 0.05 and a 95% confidence interval (f). After reviewing the hospital’s medical records or files, the biostatistics department provided 450 patient records; only 359 were selected for the research, while the rest fulfilled the exclusion criteria Figure 1.

Figure 1. Study participants flowchart.

Inclusion criteria

1. Pregnant women with COVID-19 positive PCR or Rapid test results with or without symptoms.
2. Pregnant women were admitted for the treatment of COVID-19.
3. Pregnant women with COVID-19 were admitted for delivery.

Exclusion criteria

1. Medical records of COVID-19-infected pregnant women with missing data (unknown PCR or rapid test)
2. Pregnant women with other viral infections
3. In vitro fertilization (IVF) pregnancy.

Data collection

Information was gathered using the research team’s specially created data collection form to match the study’s objectives. Information on the patient’s age, gestational age, comorbidities (diabetes, hypertension, and anemia), and gynecological and obstetrical history (parity, gravidity, abortion, and the number of previous C-sections). Pregnancy outcomes and birth status (abortion, preterm birth, stillbirth, and requirement for NICU).

The severity of COVID-19 infection was categorized according to the following¹²^–¹⁴:

Asymptomatic: No symptoms.

Mild disease: Fever, cough, sore throat, nausea, vomiting, diarrhea, loss of taste or smell but no dyspnea; normal O₂ saturation and standard chest X-ray.

Moderate disease: Symptoms of mild disease plus evidence of lower respiratory tract infection (exam and imaging), O₂ saturation ≥ 94% on room air.

Severe disease: Symptoms of moderate disease but O₂ saturation < 94%, PaO₂/FiO₂ < 300 mmHg, respiratory frequency > 30 breaths per minute, or lung infiltrates > 50%.

Critical disease: Symptoms of severe disease but intubated with respiratory failure, septic shock, and multiorgan dysfunction.

Bias

Since research operations, data collection, data entry, and data quality assurance are unplanned, retrospective cohort studies are frequently thought to have a higher bias. Using old data may affect any of these categories. But the authors of this study were keen to ensure that every eligible individual has an equal probability of selection. The research developed for settings considered, data completeness and quality assessment were conducted to ensure less bias during sample selection and study procedure.

Statistical analyses

The collected data were analyzed using SPSS version 25 statistical program for Windows (RRID: SCR 016479). The data are presented as mean ± standard deviation, number, and frequency. The chi-squared test was used to determine the significance of the associations between related categorical variables. Odds ratios were used to quantify the relationship between exposure and disease. Binary logistic regression was used to predict the relationship between independent and predicted variables. A two-sample t-test was used to determine the significance of differences between the means of the numerical data. A P-value less than 0.05 were considered a discrimination point for significance.

Results

Characteristics of COVID-19 infected pregnant women

The mean age of COVID-19-infected pregnant women was 26.78-year ± 6.694 standard deviation (between 15-46 years), gestational age was 35.77-week ± 6.133 standard deviation (between 6-42 weeks), and birth weight at delivery was 2937.10 gram ± 607.457 standard deviation. Eight women were in the first trimester (2.2%), 15 in the second trimester (4.2%), and the majority of the cases (336) were in the third trimester (93.6%) as presented in Table 1.

Table 1. Characteristics of COVID-19 infected pregnant women.

Variable		N	Mean	SD
Age		359	26.78 year	6.694
Gestational age		359	35.77 week	6.133
Birth weight		283	2936.22 gram	605.797
Trimester	First	8	2.2%
	Second	15	4.2%
	Third	336	93.6%

The severity of COVID-19 among pregnant women

Data present that 43.5% of the cases were asymptomatic, 35.4% were mild, 13.9% were moderate, and 7.2% were severe COVID-19 cases (Figure 2).

Figure 2. Distribution of COVID-19-infected pregnant women according to the severity.

Length of hospital stay according to age and severity of COVID-19 infected pregnant women

Study findings revealed that COVID-19-infected pregnant women with severe infection or aged ≥40 years had more extended hospital stays (≥3 days) than those with non-severe illness or aged less than 40 years (P-value < 0.05) (Table 2).

Table 2. Length of Hospital Stay according to age and severity of COVID-19 Infected Pregnant Women.

Severity	Hospital stay				P-value	Odd Ratio	95%CI
	≥3 days		<3 days
	N	%	N	%
Severe (n = 26)	8	30.8%	18	69.2%	0.004**	3.450	1.41-8.47
Not severe (n = 333)	38	11.4%	295	88.6%	0.004**	3.450	1.41-8.47
Age ≥ 40	6	35.3	11	64.7	0.004**	4.118	1.44-11.74
Age < 40	40	11.7	302	88.3	0.004**	4.118	1.44-11.74

** P-value < 0.01 was considered highly significant.

Distribution of signs and symptoms of COVID-19 infected pregnant women according to the severity

Table 3 shows those COVID-19-infected pregnant women who suffered from fever, cough, shortness of breath, and dyspnea had significantly more severe COVID-19 infection than those who did not suffer from the above clinical manifestations. P value = 0.001 for all conditions. Other symptoms didn’t differ among severity P-value > 0.05.

Table 3. Distribution of COVID-19 signs and symptoms according to the severity.

Symptoms	Severe (n = 26)		Not severe (n = 333)		P-value
Symptoms	N	%	N	%	P-value
Fever	24	12.8%	163	87.2%	0.001**
Cough	14	18.4%	62	81.6%	0.001**
SOB/dyspnea	20	44.4	25	55.6%	0.001**
Diarrhea	1	6.7%	14	93.3%	0.930
Vomiting	3	14.3%	18	85.7%	0.199
Nausea	1	12.5%	7	87.5%	0.495
Musculoskeletal pain	1	7.7%	12	92.3%	0.949
Headache	4	13.3%	26	86.7%	0.179
Weakness	4	14.3%	24	85.7%	0.134
Loss of smell or taste	1	6.3%	15	93.8%	0.875
Sore throat	2	12.8%	13	87.2%	0.352

** P-value < 0.01 was considered highly significant.

Prediction of signs and symptoms

Table 4 showed that fever and shortness of breath were the most predictable signs and symptoms that may result in severe COVID-19 after adjustment for other symptoms that showed a significant association with the severity of COVID-19 condition according to the chi-square test presented in Table 3.

Table 4. Prediction of signs and symptoms that may result in severe COVID-19.

Sign/symptoms	B	S.E.	Wald	df	P-value	Exp(B)
Fever	1.749	0.817	4.58	1	0.032*	5.747
Cough	-0.713	0.619	1.329	1	0.249	0.490
SOB/dyspnea	3.676	0.632	33.83	1	0.001**	39.51
Constant	-4.446	1.092	16.59	1	0.001	0.012

* P-value < 0.05 was considered significant.

** P-value < 0.01 was considered highly significant.

Distribution of COVID-19 medications

Table 5 shows that COVID-19-infected pregnant women who received multiple antibiotics, oxygen therapy, steroids, enoxaparin, and CPAP had significantly more severe COVID-19 infection than those who did not need the above treatments. P-value = 0.001 for all conditions.

Table 5. Distribution of medications among pregnant women according to the severity.

Variables		Severe (n = 26)		Not severe (n = 333)		P-value
Variables		N	%	N	%	P-value
Antibiotics	No antibiotics	1	1.2%	81	98.8%	0.001**
	One antibiotic	10	5.7%	165	94.3%
	Multiple antibiotics	15	14.7%	87	85.3%
Antiviral	No anti-viral	23	7.5%	285	92.5%	0.686
Antiviral	Antiviral	3	5.9%	48	94.1%	0.686
O₂		22	95.7%	1	4.3%	0.001**
Steroids		17	20.7%	65	79.3%	0.001**
Supplement		4	6.6%	57	93.4%	0.821
Enoxaparin		18	15.9%	95	84.1%	0.001**
CPAP		4	100.0%	0	0.0%	0.001**

** P-value < 0.01 was considered highly significant.

Distribution of risk factors of COVID-19 pregnant women according to the severity

Table 6 presents the distribution of the recorded risk factors according to COVID-19 severity. Pregnant women with a history of diabetes, hypertension, and previous cesarean sections presented with a significant predominance of severe cases. The mean age of severe COVID-19-infected pregnant women was significantly higher than that of not severe cases (P-value = 0.001), while gestational age did not reveal any difference between severity types (P-value > 0.05).

Table 6. Distribution of risk factors of COVID-19 pregnant women according to the severity.

Risk factors	Severe (n = 26)		Not severe (n = 333)		P-value
Risk factors	N	%	N	%	P-value
Diabetes	4	36.4%	7	63.6%	0.001**
Hypertension	14	31.1%	31	68.9%	0.001**
Anemia	15	10.1%	134	89.9%	0.082
Previous cesarean	15	10.9%	123	89.1%	0.036*

Risk factors	Severe			Not severe			PV
Risk factors	N	Mean	SD	N	Mean	SD	PV
Age	26	32.19	7.451	333	26.35	6.455	0.001**
Gestational age	26	35.23	4.752	333	35.81	6.232	0.658

* P-value < 0.05 was considered significant.

** P-value < 0.01 was considered highly significant.

Predictions of risk factors after adjustment of other independent factors

After adjustment for other risk factors, hypertension was found to be the most predictive risk factor for severe COVID-19 infection among pregnant women with a positive medical history (Table 7), according to the chi-square test presented in Table 6.

Table 7. Predictions of risk factors after adjustment of other independent factors.

Risk factors	B	S.E.	Wald	df	P-value	Exp(B)
DM	1.458	0.768	3.604	1	0.058	4.297
HT	2.216	0.462	23.057	1	0.001**	9.173
Previous C/S	-0.305	0.459	0.442	1	0.506	0.737
Constant	-3.950	1.654	5.707	1	0.017	0.019

** P-value < 0.01 was considered highly significant.

Pregnancy outcomes and birth status among COVID-19 infected pregnant women

Figure 3 shows that 5.1% of pregnancies ended with abortion, and 31.22% needed NICU and 6.4% ended with stillbirths among all the studied cases. Pregnancy outcomes according to the severity of covid-19 infection, as presented in Table 5, showed that 35% (7 out of 20) of stillbirth deliveries were in mothers with severe COVID-19 infection, which is significantly higher than stillbirth in non-severe cases, 65% (13 out of 294). (P-value = 0.001), (OR = 8.8), (95%CI = 3.1-24.8). Severe COVID-19-infected pregnant women delivered 13.9% (11 out of 79) of babies requiring NICU admission, significantly higher than mothers with non-severe infection (28%; 68 out of 239) (P-value = 0.014), (OR = 2.8), (95%CI = 1.2-6.4). Severe COVID-19-infected pregnant women delivered 19.4% (14 of 72) of preterm babies, significantly higher than mothers with non-severe infections (24.6%, 58/235) (P-value = 0.001), (OR = 5.16), (95%CI = 2.23-11.95) (see Table 8).

Figure 3. Pregnancy outcomes and birth status (X-axis represents the percentage, and Y-axis represents the complications).

Table 8. Pregnancy outcomes according to the severity of covid-19 infection.

Variable	Stillbirth		NICU		Abortion		Preterm
Variable	N	%	N	%	N	%	N	%
Severe (n = 25)	7	35.0	11	13.9	1	6.3	14	19.4
Not severe (n = 333)	13	65.0	68	86.1	15	93.8	58	80.6
P-value	0.001**		0.014*		0.842		0.001**
Odd ratio	8.8		2.8		0.811		5.16
95%CI	3.1-24.8		1.2-6.4		0.1-6.4		2.23-11.95

* P-value < 0.05 was considered significant.

** P-value < 0.01 was considered highly significant.

Discussion

In the current study, the mean age of the 359 pregnant women was approximately 26 years, and most of them were admitted to the hospital in the third trimester (gestational age of 35.77 weeks). These data agree with others, where the higher hospitalization rate of pregnant women with COVID-19 was in the third trimester.¹⁵^,¹⁶

Recently, human health has been severely threatened by COVID-19 infections that can range in severity from asymptomatic to severe (O₂ saturation < 94%, hypoxia, lung involvement, and increased respiratory rate) or critical (multiorgan dysfunction and respiratory failure).¹⁷ According to recent research, pregnant women are more likely to experience severe illnesses, including the need for hospitalization, ICU admission, and mechanical ventilation.¹⁸ Asymptomatic and mild pregnancy cases (43.5%, 35.4%) in the current study represented the most hospitalized cases, while severe cases represented the least (7.2%) of the total cases. These results agree with previous studies, which revealed that most COVID-19-infected pregnant women were asymptomatic and had mild cases.¹⁹^,²⁰

The length of hospital stay (LOHS) was defined as the duration between the patient’s admission to the hospital and discharge. Data on duration of stay provide insights into the effectiveness of care over time, including associations between length of stay and hospital-acquired conditions (HACs). For example, extended hospital stays have been linked to high mortality rates for specific diseases and an increased risk of hospital-acquired infections. The current study showed that patients who experienced significantly extended LOHS (equal to or more than three days) were those with severe COVID-19 infection and those aged ≥ 40 years. This result agrees with Wang et al. in 2022, who reported similar findings concerning the age and severity of illness with hospital stay.⁹

The most common symptoms of COVID-19 are fever, cough, dyspnea, and myalgia.⁵^,²¹ COVID-19-infected pregnant women in this study had a fever, cough, shortness of breath, and other signs and symptoms such as nausea, vomiting, diarrhea, headache, weakness, and loss of smell or taste, which occurred in a small percentage of the included cases. These results agree with Gillian et al. in 2020, who reported that fever, cough, and SOB were the most common symptoms in pregnant women with COVID-19 infection.²² The common symptoms were more pronounced among severe COVID-19 infected pregnant women (P-value = 0.001) than those with mild or moderate cases. After adjusting for other signs and symptoms, fever and shortness of breath were the most predictable indicators of severity using binary logistic regression. Although Lian et al., in 2021, stated similar results regarding fever but argued by considering cough as a predictor of developing severe illness,²³ the reason behind this argument may be due to pregnancy itself, as the shortness of breath may occur in normal pregnancy by excluding the pathological causes. It is a challenge for clinicians to differentiate.²⁴

The data obtained in this study documented the use of multiple antibiotics in severe cases, representing 14.7% of total medications. Cephalosporins were the most commonly used group in 73% of the cases, followed by macrolides, doxycycline, and aminoglycosides. However, the use of carbapenems, quinolones, and penicillins was much lower. The use of multiple antibiotics among COVID-19-infected pregnant women, despite several guidelines that recommend antibiotics, except in the presence of secondary bacterial infection.²⁵^,²⁶

Medical oxygen is an essential medicine in treating COVID-19 and is used mainly to alleviate the severity of the infection.²⁷ According to the Society for Maternal-Fetal Medicine, the target SpO₂ for pregnant women should be higher than that recommended for the general population (SpO₂ 92%) owing to the increased O₂ demand during pregnancy.²⁸ Oxygen therapy was used in 23 patients in this study; of them, 22 patients had severe COVID-19 infection, all of whom showed improvement in clinical status and alleviation of the severity of the disease. According to numerous randomized trials, systemic corticosteroid therapy enhances clinical outcomes and lowers mortality in COVID-19 hospitalized patients who require supplementary oxygen.²⁹^–³¹ In contrast, systemic corticosteroids have not been proven beneficial and may even be harmful in COVID-19 hospitalized patients who do not need additional oxygen.³²^,³³ In Pregnant women at risk of premature delivery, a brief course of betamethasone or Dexamethasone, which is known to cross the placenta, is frequently used to reduce neonatal complications of prematurity and decrease maternal mortality.³⁴^,³⁵ In 22.8% of the cases included in this study, corticosteroids were used for both maternal and fetal purposes; however, pregnant women with COVID-19 infection who received corticosteroids had a more severe COVID-19 disease than those who did not (P = 0.001), so the more severe infection results in greater corticosteroid use, which is in line with national guidelines.

Inflammation and prothrombotic conditions have been linked to COVID-19, and fibrin breakdown products, fibrinogen, and D-dimer levels have increased.³⁶ Some studies have linked the elevation of these markers to worse clinical outcomes.³⁷^,³⁸ In addition, pregnant women have a higher risk of thromboembolism than non-pregnant women because pregnancy is a hypercoagulable state.³⁹ Although there are no data for or against the use of anticoagulant therapy in the context of COVID-19 during pregnancy, the American College of Obstetricians and Gynecologists (ACOG) advises that VTE prophylaxis can be considered for pregnant women hospitalized with COVID-19, especially for those with severe disease. In the current study, enoxaparin was used in 31.5% of the cases, and its use was significantly associated with severe COVID-19 in pregnant women compared to those with non-severe disease (P = 0.001). Moreover, patients with COVID-19 successfully used CPAP to avoid endotracheal intubation. However, there is little information regarding the use of CPAP in expecting mothers with acute respiratory failure (ARF) caused by SARS-CoV-2 pneumonia.⁴⁰ In this study, CPAP use was significantly associated with severe COVID-19 in pregnant women (P = 0.001), and there was no need for it in the non-severe cases.

Numerous risk factors have been linked to the progression of COVID-19 into a severe and critical stage, including advanced age, male sex, and underlying comorbidities such as hypertension, diabetes, obesity, chronic lung diseases, heart, liver, and kidney diseases, tumors, and pregnancy.⁴¹^,⁴² In the current study, COVID-19-infected pregnant women with a history of diabetes, hypertension, and previous cesarean section presented with a significant predominance of severe cases. In addition, the mean age of severe COVID-19-infected pregnant women was significantly higher (32.19 years) than that of non-severe patients. Allotey et al. 2020 mentioned that pregnant women with diabetes, hypertension, BMI > 30, and age > 35 years tend to have severe COVID-19 infection.⁵ Pregnant women with previous C-sections tend to have a severe infection, which may be due to the increased number of C-sections accompanied by additional complications.⁴³ Also, individuals with COVID-19 with high blood pressure are related to higher mortality; the severity of COVID-19 may be exacerbated by inflammation and dysfunction of the immune system, gastrointestinal tract, and renin-angiotensin-aldosterone system; in addition, changes in innate cellular immunity contribute to high glucose environment, besides to more virulent growth of microbes.⁴⁴^,⁴⁵

After adjusting for risk factors that showed a significant association with the severity of infection (hypertension, diabetes, and previous C-section), predictions of risk factors were made using binary logistic regression to determine the most predictable risk factor. The test revealed that the incidence of COVID-19-infected pregnant women presenting with hypertension and diabetes developing severe infection was 9.173 and 4.297, respectively. These results are in agreement. In addition, Lian et al., in 2021, stated that patients with advanced age, H.T., and hypertension tend to have more severe COVID-19 infection.²³

Because COVID-19 affects both the mother and the fetus and negatively impacts pregnancy outcomes, pregnant women with the infection need particular care and attention.⁴⁶ This study explored the association between the severity of COVID-19 and adverse pregnancy outcomes. Among the entire study population, 6.3% (n = 20) of pregnant women had a stillbirth, 25% (n = 79) were admitted to the NICU, 4.8% (n = 16) had an abortion, and 22.6% (n = 72) had preterm delivery. There were 26 cases of COVID-19-infected pregnant women who presented with severe infection (delivery occurred in 25 patients) and had a higher rate of stillbirth deliveries (7 out of 25). In addition, admission to the NICU was higher among severe COVID-19-infected pregnant women (11 out of 24) and had preterm delivery (14 out of 25) than among non-severe cases. These results agree with those of Dileep et al. in 2022, who reported a strong association between the severity of COVID-19 infection and preterm birth, NICU admission, and low birth weight.⁴⁶ Another study reported severe COVID-19 disease in pregnant women was associated with preterm and stillbirth deliveries.⁴⁷

Study limitations

The collected data were retrospectively limited to two hospitals during one year. As a result, some of the collected data (particularly laboratory investigations) were not generally distributed in the patient’s records. In addition, the medical staff did not document important information, such as weight and body mass index (BMI), which strongly contributes to severity.

Conclusions

Most COVID-19-infected pregnant women tend to have asymptomatic or mild cases of infection. However, severe COVID-19 illness is linked to pregnancy and birth complications, mainly among pregnant women with a positive medical history.

Data availability

Underlying data

Zenodo: Underlying data for the impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study, https://doi.org/10.5281/zenodo.7607351.⁴⁸

This project contains the following underlying data:

‐ Article data.xlsx (underlying data of COVID-19 cases)

Reporting guidelines

Zenodo: STROBE checklist for: The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study, https://doi.org/10.5281/zenodo.7607382.⁴⁹

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgments

The author would like to thank Mustansiriyah University in Baghdad, Iraq, for its support in the present work, and special thanks to all field participants.

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Comments on this article Comments (1)

Version 1

VERSION 1 PUBLISHED 27 Feb 2023

Reader Comment 28 Mar 2023

Yasir Elsanousi, Division of Medical & Health Services, Alsabeel Charitable Health Center, Omdurman, Sudan

28 Mar 2023

Reader Comment

Thank you for this important research.
My comments toward improvement of this manuscript:

(A) Major Concern:
1) The Title: is not fully informative as it reflects only a single ... Continue reading Thank you for this important research.
My comments toward improvement of this manuscript:

(A) Major Concern:
1) The Title: is not fully informative as it reflects only a single part of the (about three) objectives described in the Introduction and Abstract of this article.

(B) Moderate and Minor Concerns:
*1) ‘Introduction’:
Authors may wish to present epidemiological data of the global and local burden of the disease in general and in this group. The rationale/significance of the study should be clearly explained in this section

*2) Sentence in introduction:”is the source of the coronavirus disease“
Suggestion: Change ‘source’ to a more appropriate expression (e.g. ‘causative agent’)

*3) Sentence in introduction:”global pandemic a significant loss"
-"global pandemic and significant loss”

*4) Sentence in introduction:”Severe acute respiratory syndrome coronavirus infection in pregnant women can cause...”
Substitute with the acronym ("SARS-CoV-2 infection in pregnant...etc")

*5) Sentence in introduction:”…than non-pregnant people"
Substitute 'people' with 'women' or 'ones'

*6) Sentence in introduction:”Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms”
To remove any misunderstanding it is better to complete the idea by linking it together with the other more important and relevant fact about being more likely to require ICU admission and mechanical ventilation. Remember to cite.

*7) Sentence in introduction:”according to recommendations from the Society for Maternal- Fetal Medicine, American College of Obstetricians and Gynecologists, and CDC"
The mentioned bodies may be operating in USA only. The population under study is in Iraq. So unless the Iraqi authority had adopted them, authors may wish to change to “according to international protocols and recommendations”

*8) Sentence in introduction:”The primary objectives of this study were to identify the most common symptoms associated with COVID-19 infection during pregnancy”
Should mention “Iraqi women”

*9) Methods::
Authors may wish to succinctly introduce data about the study area.

*10) Study design
It is preferable to bring this part first before the ethical considerations and consent paragraphs and move the latter two to the end of the section.

*11) Inclusion criteria, item 1 “Pregnant women with COVID-19 positive PCR … without symptoms”:
Unless authors mean OPD patients, this broad inclusion criteria already covers the next two (2 and 3)

*12) Figure1. in the ‘Excluded’ label:
Since data were secondary from patients’ files and no consent was sought, how come “13 declined to participate”?

*13) Exclusion criteria:
Authors may wish to briefly mention reasons for exclusion in items 2 and 3

*14) Sentence in ‘Bias’: “But the authors of this study were keen to ensure that every eligible individual has an equal probability of selection…etc”
Authors may either show clearly what they exactly did to avoid bias or they may rephrase and summarize the whole paragraph and move down to be included within the limitations.

*15) Figure 3:
Live healthy birth should also be added as an outcome, otherwise label the Figure as: “unfavorable (or abnormal) outcomes of pregnancy …etc”

*16) Table 8:
Same as above

*17a) Conclusion:
Too brief. Should be extended a bit to reiterate all the objectives, summarize the important findings and include some recommendations.

*17b) Conclusion; sentence “…pregnant women with a positive medical history.
“Authors may wish to clearly name these medical conditions here.

*18) Other observations:
I feel as if an important risk factor was overlooked: 'twin/multiple pregnancy' ..??

Thank you
Yasir E. A. Elsanousi, MBBCh, DTM&H, MeHM, EMDM
Infectious Disease Specialist, Disaster Medicine Consultant
Thank you for this important research.
My comments toward improvement of this manuscript:

(A) Major Concern:
1) The Title: is not fully informative as it reflects only a single part of the (about three) objectives described in the Introduction and Abstract of this article.

(B) Moderate and Minor Concerns:
*1) ‘Introduction’:
Authors may wish to present epidemiological data of the global and local burden of the disease in general and in this group. The rationale/significance of the study should be clearly explained in this section

*2) Sentence in introduction:”is the source of the coronavirus disease“
Suggestion: Change ‘source’ to a more appropriate expression (e.g. ‘causative agent’)

*3) Sentence in introduction:”global pandemic a significant loss"
-"global pandemic and significant loss”

*4) Sentence in introduction:”Severe acute respiratory syndrome coronavirus infection in pregnant women can cause...”
Substitute with the acronym ("SARS-CoV-2 infection in pregnant...etc")

*5) Sentence in introduction:”…than non-pregnant people"
Substitute 'people' with 'women' or 'ones'

*6) Sentence in introduction:”Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms”
To remove any misunderstanding it is better to complete the idea by linking it together with the other more important and relevant fact about being more likely to require ICU admission and mechanical ventilation. Remember to cite.

*7) Sentence in introduction:”according to recommendations from the Society for Maternal- Fetal Medicine, American College of Obstetricians and Gynecologists, and CDC"
The mentioned bodies may be operating in USA only. The population under study is in Iraq. So unless the Iraqi authority had adopted them, authors may wish to change to “according to international protocols and recommendations”

*8) Sentence in introduction:”The primary objectives of this study were to identify the most common symptoms associated with COVID-19 infection during pregnancy”
Should mention “Iraqi women”

*9) Methods::
Authors may wish to succinctly introduce data about the study area.

*10) Study design
It is preferable to bring this part first before the ethical considerations and consent paragraphs and move the latter two to the end of the section.

*11) Inclusion criteria, item 1 “Pregnant women with COVID-19 positive PCR … without symptoms”:
Unless authors mean OPD patients, this broad inclusion criteria already covers the next two (2 and 3)

*12) Figure1. in the ‘Excluded’ label:
Since data were secondary from patients’ files and no consent was sought, how come “13 declined to participate”?

*13) Exclusion criteria:
Authors may wish to briefly mention reasons for exclusion in items 2 and 3

*14) Sentence in ‘Bias’: “But the authors of this study were keen to ensure that every eligible individual has an equal probability of selection…etc”
Authors may either show clearly what they exactly did to avoid bias or they may rephrase and summarize the whole paragraph and move down to be included within the limitations.

*15) Figure 3:
Live healthy birth should also be added as an outcome, otherwise label the Figure as: “unfavorable (or abnormal) outcomes of pregnancy …etc”

*16) Table 8:
Same as above

*17a) Conclusion:
Too brief. Should be extended a bit to reiterate all the objectives, summarize the important findings and include some recommendations.

*17b) Conclusion; sentence “…pregnant women with a positive medical history.
“Authors may wish to clearly name these medical conditions here.

*18) Other observations:
I feel as if an important risk factor was overlooked: 'twin/multiple pregnancy' ..??

Thank you
Yasir E. A. Elsanousi, MBBCh, DTM&H, MeHM, EMDM
Infectious Disease Specialist, Disaster Medicine Consultant
Competing Interests: I have no competing interests to disclose. Close
Report a concern
Comment

Author details Author details

¹ Department of Clinical Pharmacy, College of Pharmacy, Mustansiriyah University, Baghdad, 14022, Iraq

Othman Sami Salih
Roles: Conceptualization, Data Curation, Formal Analysis, Methodology, Project Administration, Software, Writing – Original Draft Preparation

Manal Khalid Abdulridha
Roles: Conceptualization, Methodology, Software, Supervision, Validation, Visualization, Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

Article Versions (1)

version 1

Published: 27 Feb 2023, 12:220

https://doi.org/10.12688/f1000research.131229.1

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© 2023 Sami Salih O and Khalid Abdulridha M. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Sami Salih O and Khalid Abdulridha M. The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study [version 1; peer review: 2 approved with reservations, 1 not approved]. F1000Research 2023, 12:220 (https://doi.org/10.12688/f1000research.131229.1)

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Current Reviewer Status: ?

Key to Reviewer Statuses VIEW HIDE

ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested

Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.

Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions

Version 1

VERSION 1

PUBLISHED 27 Feb 2023

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Reviewer Report 17 Oct 2023

Joao Eudes Magalhaes, Faculdade de Ciências Médicas, Universidade de Pernambuco, Recife, Brazil

Not Approved

https://doi.org/10.5256/f1000research.144044.r210968

I received this manuscript on pregnancy outcomes and their correlation with the severity of COVID with enthusiasm. Although there is already a substantial body of literature published on the subject, it is always important to understand regional realities.

... Continue reading

I received this manuscript on pregnancy outcomes and their correlation with the severity of COVID with enthusiasm. Although there is already a substantial body of literature published on the subject, it is always important to understand regional realities.

However, the reading was challenging, primarily due to English grammatical errors. This will require special attention from the authors in a new version.

The Introduction needs to be rewritten to better express what has already been published on the topic. I especially suggest that the authors include the various existing systematic reviews on COVID in pregnant women. It is also important to clarify the objectives.

In the methods section, it was not clear what estimation was used for sample size calculation.

In the results section, some data are redundantly presented in both the text and the tables and graphs, so I suggest keeping only the text for greater clarity.

Notwithstanding, most of the data analyses were not adequately presented for a more detailed assessment of this study. In several instances, the authors assumed a result contrary to what is demonstrated. For example, “(...) in Table 5, showed that 35% (7 out of 20) of stillbirth deliveries were in mothers with severe COVID-19 infection, which is significantly higher than stillbirth in non-severe cases, 65% (13 out of 294)”. How can 35% be significantly higher than 65%? This same premise was used to indicate several other comparisons throughout the results.

Unfortunately, it was not possible to analyze the discussion and conclusion once the authors used wrong interpretations even if they were based on correctly presented results.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Partly
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

I cannot comment. A qualified statistician is required.
Are all the source data underlying the results available to ensure full reproducibility?

Partly
Are the conclusions drawn adequately supported by the results?

No

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Neurology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to state that I do not consider it to be of an acceptable scientific standard, for reasons outlined above.

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Reviewer Report 08 Oct 2023

Erin Oakley, Milken Institute School of Public Health, The George Washington University, Washington, District of Columbia, USA

Approved with Reservations

https://doi.org/10.5256/f1000research.144044.r206633

First, I commend the authors on a thoughtful and thorough study of COVID-19 severity in pregnancy. The analysis is well done and will be useful to inform the body of knowledge around risk factors for severe COVID-19 (and related poor ... Continue reading

First, I commend the authors on a thoughtful and thorough study of COVID-19 severity in pregnancy. The analysis is well done and will be useful to inform the body of knowledge around risk factors for severe COVID-19 (and related poor pregnancy outcomes).

One overall question I had when reading the paper is, do you have any insight as to what variant(s) of SARS-CoV-2 was circulating in Iraq at the time of the study? It seems that the data was collected in late 2021 through mid-2022, so this context may be relevant to note somewhere in the paper (perhaps in the discussion). There has been some evidence that the Delta variant in particular was associated with poor pregnancy outcomes.

In the abstract, I am unclear about what the conclusion statement "mainly among pregnant women with a positive medical history" means. Could you please clarify does this mean among pregnant women with pre-existing comorbidities?

In the introduction, it seems like these two statements (from paragraph 1 and paragraph 3, respectively) are in conflict:
"Although the risk of developing severe illness is minimal, pregnant women with COVID-19 are more likely to do so than non-pregnant people." (paragraph 1)
"Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms." (paragraph 3)
Are these two statements based on conflicting evidence from different studies? Or, did you find in the literature that pregnant women were less likely to develop symptoms but more likely to develop severe symptoms rather than mild ones? It would be helpful to clarify.

In the section "Characteristics of COVID-19 infected pregnant women", it would be helpful to confirm:

Is the gestational age given the age at infection onset (rather than pregnancy outcome)?
Why only 283 observations for birthweight?
Could you disaggregate Table 1 by disease severity? This would be an interesting addition.
Also, is it possible to share more about the distribution of participants by reason for admission? Based on your inclusion criteria, women could be recruited to the study based on admission for treatment of COVID-19 or admission for delivery (or both?).

Noting a small typo in Figure 2 (should read "severe" in the yellow category).

In the section "Length of hospital stay according to age and severity of COVID-19 infected pregnancy women", it would be helpful to confirm:

How did you treat observations that were hospitalized for childbirth but were also infected (i.e., those asymptomatic cases or cases with more mild infection)? It looks like this table includes both admissions for childbirth and admissions for COVID-19 together. Understandably, it may be difficult to disentangle reasons for admission if someone has COVID-19 at the time of labor and delivery.

In the section "Distribution of signs and symptoms of COVID-19 infected pregnant women according to the severity": These are interesting findings. I wonder if your point would be better illustrated in Table 3 if you changed the way percentages are reported. Right now, the table shows that 87.2% of those with fever had a non-severe infection and 12.8% of those with fever had a severe infection. However, the point you make in the paragraph above Table 3 is that those who had severe infections were more likely to have a fever. I suggest instead of presenting the % column how it currently is, you consider instead presenting the % of participants in each severity category who had that symptom. For e.g.: 92% of participants with severe infection had fever vs. 50% of participants with non-severe infection. (Same suggestion for Table 5, Table 6, Table 8).

Would it be possible to add confidence intervals to the last column of Table 4?

In the section "Distribution of risk factors of COVID-19 [in] pregnant women according to the severity": These findings are really interesting and well-presented. A few points to clarify:

For diabetes, does this include pre-existing diabetes prior to pregnancy, gestational diabetes, or both?
For hypertension, does this include pre-existing hypertension prior to pregnancy, pregnancy-related hypertension, or both?
How is anemia defined?
You mention that mean maternal age is higher among severe cases than non-severe, but this is not included in Table 6 or Table 7. Did you consider including this in your risk factor analysis?

In the section "Pregnancy outcomes and birth status among COVID-19 infected pregnant women" the same recommendation as above, perhaps consider sharing the percentage of pregnancies that ended in stillbirth among severe and non-severe cases (per Table 8: 7/25 = 28% for severe and 13/333 = 4% for non-severe) rather than the percentage of total stillbirths that occurred in each group. I think this would help to illustrate your findings a bit better that adverse outcomes are more common among the severe cases than among the non-severe.

Thank you for sharing the data for this study -- this is well-presented and very informative. A few points to clarify when looking at the data compared to the study:

In the data, there are 20 stillbirths/359 observations (5.6%) and 16 abortions/359 observations (4.5%). This conflicts with Figure 3 (which shows 6.4% stillbirth and 5.1% abortion). Are some participants excluded from Figure 3 (e.g., perhaps due to loss of follow-up?) If so, this would be helpful to clarify in the paper or in the notes about how many pregnancies were followed through until the endpoint. Also, perhaps you could add an indicator to the dataset for "loss to follow-up prior to delivery" if this is the case so that others can reproduce the results.
Further, the key at the top of the file lists 2 values for "Preterm" (1=yes, 2=no), but there are actually three values presented in this column (0, 1, 2).
Also one further clarification for the data, what is the difference in the variable "pregnancy outcome" between 0 = "no pregnancy complication" and 2 = "healthy"? This would be useful for readers to interpret the data.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Partly
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Systematic review; meta-analysis; maternal health

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Reviewer Report 15 Aug 2023

Hayder Adnan Fawzi, Department of Pharmacy, Al-Mustafa University ‎College, Baghdad, Iraq

Approved with Reservations

https://doi.org/10.5256/f1000research.144044.r193261

The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study

Methods: Data collection

Where the information came from the patients? Datasheet or by other means? Please emphasize more about ... Continue reading

The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study

Methods: Data collection

Where the information came from the patients? Datasheet or by other means? Please emphasize more about the methods of gathering information.
Regarding “Ethical considerations”

There are two institutes that approved the study, yet only one ethical approval is present, please provide both ethical approval codes, and submit the ethical approval as underlying data.

Regarding the title of “Table 1”

Needs adjustment since it includes information regarding the neonate, it is better to use” Table 1. Neonatal and maternal characteristics”

Regarding table 3, 5, 6

Calculate the percentage by column not by raw, since you omitted the number that indicates the no signs or symptoms (e.g., fever vs. no fever), for more clarity. In addition, some of the variables violate the principle that applied to the proper use of chi-square. How did you handle a sample with an expected frequency of less than 5%? Like Nausea, Diarrhea, and others?

Regarding table 4

Report using OR and its 95% confidence interval and remove the term Exp(β) and change it to OR.

This sentence “Table 4 showed that fever and shortness of breath were the most predictable signs and symptoms that may result in severe COVID-19 after adjustment for other symptoms that showed a significant association with the severity of COVID-19 condition according to the chi-square test presented in Table 3.”

First, the chi-square test used is lower accuracy compared to logistic regression in Table 4, so please focus on using the outcome reported in Table 4. I would prefer to use only one statistical test (in Table 4) and remove the statistical analysis in Table 3, and merge the descriptive with the logistic analysis in one table.

The same note applied to tables 6 and 7 (merge both and report using logistic analysis)

Regarding figure 3

Draw using publication-level figures like GraphPad prism, and SAS.

Regarding the result

Too many tables that can be easily merged into fewer tables.

You did not use multivariate analysis which is lacking in your results and that affects your conclusion, if possible include them in your final analysis.

Discussion

Please start the discussion with the main subject of the article i.e. pregnancy outcomes and the impact of COVID-19 on it.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Pharmaceutical science, clinical pharmacy, pharmacogenetics, medicine, and clinical trials.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Version 1

VERSION 1 PUBLISHED 27 Feb 2023

Reader Comment 28 Mar 2023

Yasir Elsanousi, Division of Medical & Health Services, Alsabeel Charitable Health Center, Omdurman, Sudan

28 Mar 2023

Reader Comment

Thank you for this important research.
My comments toward improvement of this manuscript:

(A) Major Concern:
1) The Title: is not fully informative as it reflects only a single ... Continue reading Thank you for this important research.
My comments toward improvement of this manuscript:

(A) Major Concern:
1) The Title: is not fully informative as it reflects only a single part of the (about three) objectives described in the Introduction and Abstract of this article.

(B) Moderate and Minor Concerns:
*1) ‘Introduction’:
Authors may wish to present epidemiological data of the global and local burden of the disease in general and in this group. The rationale/significance of the study should be clearly explained in this section

*2) Sentence in introduction:”is the source of the coronavirus disease“
Suggestion: Change ‘source’ to a more appropriate expression (e.g. ‘causative agent’)

*3) Sentence in introduction:”global pandemic a significant loss"
-"global pandemic and significant loss”

*4) Sentence in introduction:”Severe acute respiratory syndrome coronavirus infection in pregnant women can cause...”
Substitute with the acronym ("SARS-CoV-2 infection in pregnant...etc")

*5) Sentence in introduction:”…than non-pregnant people"
Substitute 'people' with 'women' or 'ones'

*6) Sentence in introduction:”Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms”
To remove any misunderstanding it is better to complete the idea by linking it together with the other more important and relevant fact about being more likely to require ICU admission and mechanical ventilation. Remember to cite.

*7) Sentence in introduction:”according to recommendations from the Society for Maternal- Fetal Medicine, American College of Obstetricians and Gynecologists, and CDC"
The mentioned bodies may be operating in USA only. The population under study is in Iraq. So unless the Iraqi authority had adopted them, authors may wish to change to “according to international protocols and recommendations”

*8) Sentence in introduction:”The primary objectives of this study were to identify the most common symptoms associated with COVID-19 infection during pregnancy”
Should mention “Iraqi women”

*9) Methods::
Authors may wish to succinctly introduce data about the study area.

*10) Study design
It is preferable to bring this part first before the ethical considerations and consent paragraphs and move the latter two to the end of the section.

*11) Inclusion criteria, item 1 “Pregnant women with COVID-19 positive PCR … without symptoms”:
Unless authors mean OPD patients, this broad inclusion criteria already covers the next two (2 and 3)

*12) Figure1. in the ‘Excluded’ label:
Since data were secondary from patients’ files and no consent was sought, how come “13 declined to participate”?

*13) Exclusion criteria:
Authors may wish to briefly mention reasons for exclusion in items 2 and 3

*14) Sentence in ‘Bias’: “But the authors of this study were keen to ensure that every eligible individual has an equal probability of selection…etc”
Authors may either show clearly what they exactly did to avoid bias or they may rephrase and summarize the whole paragraph and move down to be included within the limitations.

*15) Figure 3:
Live healthy birth should also be added as an outcome, otherwise label the Figure as: “unfavorable (or abnormal) outcomes of pregnancy …etc”

*16) Table 8:
Same as above

*17a) Conclusion:
Too brief. Should be extended a bit to reiterate all the objectives, summarize the important findings and include some recommendations.

*17b) Conclusion; sentence “…pregnant women with a positive medical history.
“Authors may wish to clearly name these medical conditions here.

*18) Other observations:
I feel as if an important risk factor was overlooked: 'twin/multiple pregnancy' ..??

Thank you
Yasir E. A. Elsanousi, MBBCh, DTM&H, MeHM, EMDM
Infectious Disease Specialist, Disaster Medicine Consultant
Thank you for this important research.
My comments toward improvement of this manuscript:

(A) Major Concern:
1) The Title: is not fully informative as it reflects only a single part of the (about three) objectives described in the Introduction and Abstract of this article.

(B) Moderate and Minor Concerns:
*1) ‘Introduction’:
Authors may wish to present epidemiological data of the global and local burden of the disease in general and in this group. The rationale/significance of the study should be clearly explained in this section

*2) Sentence in introduction:”is the source of the coronavirus disease“
Suggestion: Change ‘source’ to a more appropriate expression (e.g. ‘causative agent’)

*3) Sentence in introduction:”global pandemic a significant loss"
-"global pandemic and significant loss”

*4) Sentence in introduction:”Severe acute respiratory syndrome coronavirus infection in pregnant women can cause...”
Substitute with the acronym ("SARS-CoV-2 infection in pregnant...etc")

*5) Sentence in introduction:”…than non-pregnant people"
Substitute 'people' with 'women' or 'ones'

*6) Sentence in introduction:”Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms”
To remove any misunderstanding it is better to complete the idea by linking it together with the other more important and relevant fact about being more likely to require ICU admission and mechanical ventilation. Remember to cite.

*7) Sentence in introduction:”according to recommendations from the Society for Maternal- Fetal Medicine, American College of Obstetricians and Gynecologists, and CDC"
The mentioned bodies may be operating in USA only. The population under study is in Iraq. So unless the Iraqi authority had adopted them, authors may wish to change to “according to international protocols and recommendations”

*8) Sentence in introduction:”The primary objectives of this study were to identify the most common symptoms associated with COVID-19 infection during pregnancy”
Should mention “Iraqi women”

*9) Methods::
Authors may wish to succinctly introduce data about the study area.

*10) Study design
It is preferable to bring this part first before the ethical considerations and consent paragraphs and move the latter two to the end of the section.

*11) Inclusion criteria, item 1 “Pregnant women with COVID-19 positive PCR … without symptoms”:
Unless authors mean OPD patients, this broad inclusion criteria already covers the next two (2 and 3)

*12) Figure1. in the ‘Excluded’ label:
Since data were secondary from patients’ files and no consent was sought, how come “13 declined to participate”?

*13) Exclusion criteria:
Authors may wish to briefly mention reasons for exclusion in items 2 and 3

*14) Sentence in ‘Bias’: “But the authors of this study were keen to ensure that every eligible individual has an equal probability of selection…etc”
Authors may either show clearly what they exactly did to avoid bias or they may rephrase and summarize the whole paragraph and move down to be included within the limitations.

*15) Figure 3:
Live healthy birth should also be added as an outcome, otherwise label the Figure as: “unfavorable (or abnormal) outcomes of pregnancy …etc”

*16) Table 8:
Same as above

*17a) Conclusion:
Too brief. Should be extended a bit to reiterate all the objectives, summarize the important findings and include some recommendations.

*17b) Conclusion; sentence “…pregnant women with a positive medical history.
“Authors may wish to clearly name these medical conditions here.

*18) Other observations:
I feel as if an important risk factor was overlooked: 'twin/multiple pregnancy' ..??

Thank you
Yasir E. A. Elsanousi, MBBCh, DTM&H, MeHM, EMDM
Infectious Disease Specialist, Disaster Medicine Consultant
Competing Interests: I have no competing interests to disclose. Close
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	1	2	3
Version 1 27 Feb 23	read	read	read

Hayder Adnan Fawzi, Al-Mustafa University ‎College, Baghdad, Iraq
Erin Oakley, The George Washington University, Washington, USA
Joao Eudes Magalhaes, Universidade de Pernambuco, Recife, Brazil

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Reviewer Report

3 Views

17 Oct 2023 | for Version 1

Joao Eudes Magalhaes, Faculdade de Ciências Médicas, Universidade de Pernambuco, Recife, Brazil

3 Views Cite this report Responses(0)

Not Approved

I received this manuscript on pregnancy outcomes and their correlation with the severity of COVID with enthusiasm. Although there is already a substantial body of literature published on the subject, it is always important to understand regional realities.

However, the reading was challenging, primarily due to English grammatical errors. This will require special attention from the authors in a new version.

The Introduction needs to be rewritten to better express what has already been published on the topic. I especially suggest that the authors include the various existing systematic reviews on COVID in pregnant women. It is also important to clarify the objectives.

In the methods section, it was not clear what estimation was used for sample size calculation.

In the results section, some data are redundantly presented in both the text and the tables and graphs, so I suggest keeping only the text for greater clarity.

Notwithstanding, most of the data analyses were not adequately presented for a more detailed assessment of this study. In several instances, the authors assumed a result contrary to what is demonstrated. For example, “(...) in Table 5, showed that 35% (7 out of 20) of stillbirth deliveries were in mothers with severe COVID-19 infection, which is significantly higher than stillbirth in non-severe cases, 65% (13 out of 294)”. How can 35% be significantly higher than 65%? This same premise was used to indicate several other comparisons throughout the results.

Unfortunately, it was not possible to analyze the discussion and conclusion once the authors used wrong interpretations even if they were based on correctly presented results.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Partly
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

I cannot comment. A qualified statistician is required.
Are all the source data underlying the results available to ensure full reproducibility?

Partly
Are the conclusions drawn adequately supported by the results?

No

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Neurology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to state that I do not consider it to be of an acceptable scientific standard, for reasons outlined above.

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7 Views

08 Oct 2023 | for Version 1

Erin Oakley, Milken Institute School of Public Health, The George Washington University, Washington, District of Columbia, USA

7 Views Cite this report Responses(0)

Approved With Reservations

First, I commend the authors on a thoughtful and thorough study of COVID-19 severity in pregnancy. The analysis is well done and will be useful to inform the body of knowledge around risk factors for severe COVID-19 (and related poor pregnancy outcomes).

One overall question I had when reading the paper is, do you have any insight as to what variant(s) of SARS-CoV-2 was circulating in Iraq at the time of the study? It seems that the data was collected in late 2021 through mid-2022, so this context may be relevant to note somewhere in the paper (perhaps in the discussion). There has been some evidence that the Delta variant in particular was associated with poor pregnancy outcomes.

In the abstract, I am unclear about what the conclusion statement "mainly among pregnant women with a positive medical history" means. Could you please clarify does this mean among pregnant women with pre-existing comorbidities?

In the introduction, it seems like these two statements (from paragraph 1 and paragraph 3, respectively) are in conflict:
"Although the risk of developing severe illness is minimal, pregnant women with COVID-19 are more likely to do so than non-pregnant people." (paragraph 1)
"Compared to non-pregnant women, pregnant women with COVID-19 are less likely to experience symptoms." (paragraph 3)
Are these two statements based on conflicting evidence from different studies? Or, did you find in the literature that pregnant women were less likely to develop symptoms but more likely to develop severe symptoms rather than mild ones? It would be helpful to clarify.

In the section "Characteristics of COVID-19 infected pregnant women", it would be helpful to confirm:

Is the gestational age given the age at infection onset (rather than pregnancy outcome)?
Why only 283 observations for birthweight?
Could you disaggregate Table 1 by disease severity? This would be an interesting addition.
Also, is it possible to share more about the distribution of participants by reason for admission? Based on your inclusion criteria, women could be recruited to the study based on admission for treatment of COVID-19 or admission for delivery (or both?).

Noting a small typo in Figure 2 (should read "severe" in the yellow category).

In the section "Length of hospital stay according to age and severity of COVID-19 infected pregnancy women", it would be helpful to confirm:

How did you treat observations that were hospitalized for childbirth but were also infected (i.e., those asymptomatic cases or cases with more mild infection)? It looks like this table includes both admissions for childbirth and admissions for COVID-19 together. Understandably, it may be difficult to disentangle reasons for admission if someone has COVID-19 at the time of labor and delivery.

In the section "Distribution of signs and symptoms of COVID-19 infected pregnant women according to the severity": These are interesting findings. I wonder if your point would be better illustrated in Table 3 if you changed the way percentages are reported. Right now, the table shows that 87.2% of those with fever had a non-severe infection and 12.8% of those with fever had a severe infection. However, the point you make in the paragraph above Table 3 is that those who had severe infections were more likely to have a fever. I suggest instead of presenting the % column how it currently is, you consider instead presenting the % of participants in each severity category who had that symptom. For e.g.: 92% of participants with severe infection had fever vs. 50% of participants with non-severe infection. (Same suggestion for Table 5, Table 6, Table 8).

Would it be possible to add confidence intervals to the last column of Table 4?

In the section "Distribution of risk factors of COVID-19 [in] pregnant women according to the severity": These findings are really interesting and well-presented. A few points to clarify:

For diabetes, does this include pre-existing diabetes prior to pregnancy, gestational diabetes, or both?
For hypertension, does this include pre-existing hypertension prior to pregnancy, pregnancy-related hypertension, or both?
How is anemia defined?
You mention that mean maternal age is higher among severe cases than non-severe, but this is not included in Table 6 or Table 7. Did you consider including this in your risk factor analysis?

In the section "Pregnancy outcomes and birth status among COVID-19 infected pregnant women" the same recommendation as above, perhaps consider sharing the percentage of pregnancies that ended in stillbirth among severe and non-severe cases (per Table 8: 7/25 = 28% for severe and 13/333 = 4% for non-severe) rather than the percentage of total stillbirths that occurred in each group. I think this would help to illustrate your findings a bit better that adverse outcomes are more common among the severe cases than among the non-severe.

Thank you for sharing the data for this study -- this is well-presented and very informative. A few points to clarify when looking at the data compared to the study:

In the data, there are 20 stillbirths/359 observations (5.6%) and 16 abortions/359 observations (4.5%). This conflicts with Figure 3 (which shows 6.4% stillbirth and 5.1% abortion). Are some participants excluded from Figure 3 (e.g., perhaps due to loss of follow-up?) If so, this would be helpful to clarify in the paper or in the notes about how many pregnancies were followed through until the endpoint. Also, perhaps you could add an indicator to the dataset for "loss to follow-up prior to delivery" if this is the case so that others can reproduce the results.
Further, the key at the top of the file lists 2 values for "Preterm" (1=yes, 2=no), but there are actually three values presented in this column (0, 1, 2).
Also one further clarification for the data, what is the difference in the variable "pregnancy outcome" between 0 = "no pregnancy complication" and 2 = "healthy"? This would be useful for readers to interpret the data.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Partly
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Systematic review; meta-analysis; maternal health

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Reviewer Report

9 Views

15 Aug 2023 | for Version 1

Hayder Adnan Fawzi, Department of Pharmacy, Al-Mustafa University ‎College, Baghdad, Iraq

9 Views Cite this report Responses(0)

Approved With Reservations

The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study

Methods: Data collection

Where the information came from the patients? Datasheet or by other means? Please emphasize more about the methods of gathering information.
Regarding “Ethical considerations”

There are two institutes that approved the study, yet only one ethical approval is present, please provide both ethical approval codes, and submit the ethical approval as underlying data.

Regarding the title of “Table 1”

Needs adjustment since it includes information regarding the neonate, it is better to use” Table 1. Neonatal and maternal characteristics”

Regarding table 3, 5, 6

Calculate the percentage by column not by raw, since you omitted the number that indicates the no signs or symptoms (e.g., fever vs. no fever), for more clarity. In addition, some of the variables violate the principle that applied to the proper use of chi-square. How did you handle a sample with an expected frequency of less than 5%? Like Nausea, Diarrhea, and others?

Regarding table 4

Report using OR and its 95% confidence interval and remove the term Exp(β) and change it to OR.

This sentence “Table 4 showed that fever and shortness of breath were the most predictable signs and symptoms that may result in severe COVID-19 after adjustment for other symptoms that showed a significant association with the severity of COVID-19 condition according to the chi-square test presented in Table 3.”

First, the chi-square test used is lower accuracy compared to logistic regression in Table 4, so please focus on using the outcome reported in Table 4. I would prefer to use only one statistical test (in Table 4) and remove the statistical analysis in Table 3, and merge the descriptive with the logistic analysis in one table.

The same note applied to tables 6 and 7 (merge both and report using logistic analysis)

Regarding figure 3

Draw using publication-level figures like GraphPad prism, and SAS.

Regarding the result

Too many tables that can be easily merged into fewer tables.

You did not use multivariate analysis which is lacking in your results and that affects your conclusion, if possible include them in your final analysis.

Discussion

Please start the discussion with the main subject of the article i.e. pregnancy outcomes and the impact of COVID-19 on it.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Pharmaceutical science, clinical pharmacy, pharmacogenetics, medicine, and clinical trials.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

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The impact of COVID-19 severity on pregnancy outcomes among Iraqi women: a retrospective observational study

Abstract

Keywords

Introduction

Methods

Ethical considerations

Consent

Study design

Sample size

Figure 1. Study participants flowchart.

Inclusion criteria

Exclusion criteria

Data collection

Bias

Statistical analyses

Results

Characteristics of COVID-19 infected pregnant women

Table 1. Characteristics of COVID-19 infected pregnant women.

The severity of COVID-19 among pregnant women

Figure 2. Distribution of COVID-19-infected pregnant women according to the severity.

Length of hospital stay according to age and severity of COVID-19 infected pregnant women

Table 2. Length of Hospital Stay according to age and severity of COVID-19 Infected Pregnant Women.

Distribution of signs and symptoms of COVID-19 infected pregnant women according to the severity

Table 3. Distribution of COVID-19 signs and symptoms according to the severity.

Prediction of signs and symptoms

Table 4. Prediction of signs and symptoms that may result in severe COVID-19.

Table 5. Distribution of medications among pregnant women according to the severity.

Distribution of risk factors of COVID-19 pregnant women according to the severity

Table 6. Distribution of risk factors of COVID-19 pregnant women according to the severity.

Predictions of risk factors after adjustment of other independent factors

Table 7. Predictions of risk factors after adjustment of other independent factors.

Pregnancy outcomes and birth status among COVID-19 infected pregnant women

Figure 3. Pregnancy outcomes and birth status (X-axis represents the percentage, and Y-axis represents the complications).

Table 8. Pregnancy outcomes according to the severity of covid-19 infection.

Discussion

Study limitations

Conclusions

Data availability

Underlying data

Reporting guidelines

Acknowledgments

References

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