Impact of Wuhan lockdown on the indications of cesarean delivery and newborn weights during the epidemic period of COVID-19.

OBJECTIVE: To prevent the rapid spread of COVID-19, the Chinese government implemented a strict lockdown in Wuhan starting on 23 January, 2020, which inevitably led to the changes in indications for the mode of delivery. In this retrospective study, we present the changes in the indications for cesarean delivery (CD) and the birth weights of newborns after the lockdown in Wuhan.
METHODS: A total of 3,432 pregnant women in the third trimester of their pregnancies who gave birth in our hospital from 23 January 2019 to 24 March 2020 were selected as the observation group, while 7,159 pregnant women who gave birth from 1 January 2019 to 22 January 2020 were selected as the control group; control group was matched using propensity score matching (PSM). A comparative analysis of the two groups was performed with the chi-square test, t test and rank sum test.
RESULTS: The difference in the overall rate of CD between the two groups was not statistically significant (p<0.05). Among the indications for CD, CD on maternal request (CDMR) and fetal distress were also significantly more common in the observation group (p<0.05) than the control group. Furthermore, we found that the weight of newborns was significantly heavier in the observation group than in the control group when considering full-term or close-to-full-term births (p<0.05).
CONCLUSIONS: The results may provide useful information to management practices regarding pregnancy and childbirth after lockdown in other cities or countries, enabling better control of the rate of CD due to CDMR, reducing fetal distress, and controlling newborn weight. We recommend that pregnant women pay more attention to controlling the weight of newborns through diet and exercise.

Introduction

At the end of December 2019, a cluster of cases of coronavirus disease-2019 (COVID-19) were first reported in Wuhan, China [1]. On 23 January 2020, the municipal government of Wuhan announced the lockdown of the entire city, and China implemented a national emergency mechanism with different cities adopting different measures according to their respective situations. On 30 January 2020, the WHO declared COVID-19 to be a “public health emergency of international concern”, and the US recorded its first confirmed case of human-to-human transmission in Chicago [2, 3]. It is evident that the lockdown in Wuhan has played a critical role in limiting the scope of the COVID-19 epidemic in China.

Since then, the life-threatening COVID-19 outbreak has become a global pandemic. By 5 April 2020, the global number of confirmed cases had exceeded 1.1 million, with a daily increase of approximately 0.1 million cases. To cope with this disaster, an increasing number of government agencies in the US and European countries have implemented lockdown policies to prevent the rapid spread of COVID-19. During the lockdown, city residents are required to refrain from leaving home and to practice social distancing. In the past two months, scholars began to pay attention to the management of pregnancy and childbirth during the COVID-19 pandemic. Previous studies have shown that pregnancy while infected with severe acute respiratory syndrome coronavirus (SARS-CoV) was associated with adverse maternal and neonatal complications, such as spontaneous miscarriage, preterm delivery, intrauterine growth restriction, the need for endotracheal intubation, admission to the intensive care unit, renal failure, and disseminated intravascular coagulopathy [4, 5].

Although the possible risks associated with COVID-19 and the clinical characteristics of pregnant women with laboratory-confirmed COVID-19 have been investigated [6, 7], previous research has failed to address the impact of lockdown during the COVID-19 epidemic. Unlike other activities that can be carried out online or at home, delivery cannot be delayed arbitrarily or performed at home. The lockdown in Wuhan may have a significant impact on the outcome of pregnancy due to pathological factors, the timeliness of examinations, psychological panic, limited medical resources, difficulty accessing and transportation, etc. An essential question that is important for obstetricians to consider is how does the lockdown affect the indications for different modes of delivery and newborn health?

This study answers the question based on an analysis of the data from more than 10,000 cases from our working hospital in Wuhan, the Maternal and Child Hospital of Hubei Province, which has one of the largest obstetrics departments of all Chinese hospitals. The department delivered approximately 25,000 babies annually in the last five years. During the COVID-19 epidemic, our hospital was identified as a non-designated hospital with a fever clinic accept pregnant women who were not infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and those who were suspected of being infected. The latter patients who received laboratory-confirmation of infection via quantitative qPT-PCR for SARS-CoV-2 using a throat swab were transferred to designated hospitals for further treatment. During the lockdown in Wuhan, a total of 3,432 pregnant women underwent delivery in our birth center, and a few cases of COVID-19 were confirmed in pregnant women. In this study, we compared the indications for cesarean delivery (CD) and the birth weights of newborns born to 3,432 pregnant women who gave birth during lockdown and 7,159 propensity score-matched pregnant women who gave birth before the lockdown were selected as the control group.

Methods

Study design and patients

Fig 1 illustrates the subject selection process. Pregnant women who had given birth in the birth center of the Maternal and Child Health Hospital of Hubei Province from 23 January 2020 to 14 March 2020 were enrolled as the observation group. The age of the selected patients ranged from 18 to 50 years old. The exclusion criteria included a gestational age less than 28 weeks and intrauterine fetal death. A total of 3442 pregnant women were initially included, among whom 5 with gestational age less than 28 weeks of and 5 with intrauterine fetal death were excluded. The remaining 3432 patients constituted the observation group.

Fig 1

Population flow chart of the retrospective study.

From 29, 799 historical patients from 1 January 2019 to 22 January 2020, the control group included a total of 7,159 patients based on the propensity score matching (PSM) method as. The PSM method, a quasi-experimental design that has been used across disciplines to isolate treatment effects on a number of outcomes using observational data, was employed in this study to obtain matched patients to facilitate comparisons [8]. Based on three variables of age, gravidity, and parity, 7159 pregnant women were selected as the control group from the 29799 patients before the lockdown using the PSM method. The balanced scores of the two groups were 0.10312 and 0.10590, which were very similar.

Data collection

In our department, one nurse is responsible for the daily recording of the delivery information of all the pregnant women into the Electronic Medical Record System (EMRS). In this research, obstetricians extracted the required data, including epidemiological, demographic, clinical, laboratory, and pregnancy outcome data for both the observation group and control group. The neonates’ data including birth weight, clinical symptoms, Apgar score, and outcomes were also collected. During this period, all pregnant women with COVID-19 symptoms, such as fever, cough, and abnormal CT scan results, underwent nucleic acid detection of COVID-19 of SARS-COV02 from swab samples. In total, 13 pregnant women had confirmed COVID-19, including 8 pregnant women who underwent CD. Their throat swab samples were collected and sent to the local Chinese Center for Disease Control and Prevention (CDC), which was in charge of detecting SAS-COV-2 by qRT-PCR. The results for each woman suspected of having COVID-19 was entered into the EMRS.

Statistical methods

Statistical analysis was performed using SPSS 22.0. The chi-square test was used for the comparison of countable data. The t-test and Fisher’s exact probability method were used for the comparison of the means between the measurement data. The rank sum test was used for ranking variables. A difference was statistically significant at p<0.05.

Results

A comparison of the observation group and control group is shown in Table 1. There were no significant differences in maternal age, gravidity, parity history, or BMI between the two groups (p>0.05). At the same time, there were no differences in the proportions of preterm and term neonates between the two groups (p>0.05).

Table 1

Comparison of the general situation of pregnant women.

		Before lockdown (n = 7159)		After lockdown (n = 3432)		Chi-square	p-value
		No.	%	No.	%
Age	<35	6385	89	3095	90	2.43	0.12
	≥35	774	11	337	10
Gravida	1	3288	46	1544	45	1.44	0.70
	2	2003	28	981	29
	3	1113	16	527	15
	≥4	754	10	380	11
Para	Primipara	4685	65	2243	65	0.01	0.93
	Multiparas	2474	35	1189	35
BMI	<25	6665	93	3167	92	2.35	0.16
	≥25	494	7	265	8
Preterm and term births	Preterm	615	9	281	8	0.49	0.47
	Term	6544	91	3151	92

Table 2 shows the comparison of the rates of CD and vaginal delivery before and after lockdown. The data show that there was no significant difference between the two groups (p>0.05). In fact, the CD rate in the observation and control groups were 47.49% and 47.70%, respectively.

Table 2

CD rate and vaginal delivery rate before and after lockdown.

	Before lockdown (n = 7159)		After lockdown (n = 3432)		Chi-square	p-value
	No.	%	No.	%
Vaginal delivery	3759	53	1795	52	0.04	0.84
Cesarean delivery	3400	47	1637	48

Table 3 shows the comparison of the indications for CD. There were no significant differences in most of the pregnancy complications between the observation group and control group. The number of pregnant women who underwent CD due to fetal distress in the observation group was significantly higher than that in the control group (p<0.05). In addition, the incidence of CDMR in the observation group was significantly higher than that in the control group (p<0.05). CDMR was defined as a primary prelabor cesarean delivery performed on maternal request in the absence of any maternal or fetal indications [9]. In the observation group, 13 cases of COVID-19 were confirmed by chest CT scan and two positive laboratory tests for SARS-CoV-2 in throat swab samples. Eight of those 13 patients with confirmed COVID-19 underwent CD. There were 0 COVID-19 cases in the control group. The other indications for CD in the observation group were not significantly different than those in the control group.

Table 3

Comparison of the indications of CD.

	Before lockdown (n = 3400)		After lockdown (n = 1637)		Chi-square	p-value
	No.	%	No.	%
Scar uterus	1128	33	553	34	0.18	0.67
Fetal distress	537	15	297	18	4.41	<0.05
Abnormal fetal position	338	10	137	8	3.20	0.07
Cesarean delivery on maternal request (CDMR)	284	8	186	11	11.83	<0.05
Giant fetus	210	6	83	5	2.47	0.12
Hypertension	205	6	79	5	3.01	0.08
Multiple pregnancy	133	4	68	4	0.17	0.68
Placenta previa	94	3	32	2	2.97	0.09
Induction of labor failure	74	2	30	2	0.65	0.42
Prenatal fever	69	2	26	2	1.16	0.28
Labor abnormalities	46	1	22	1	0.02	0.98
ICPb	37	1	17	1	0.03	0.87
Placental abruption	33	1	13	1	0.38	0.54
Diabetes	31	1	12	1	0.42	0.52
Umbilical cord	22	1	5	0	2.42	0.12
Genital malformation	14	0	13	1	3.03	0.08
FGRc	11	0	1	0	3.20	0.07
COVID-19	0	0	8	0		<0.05△a
Others	34	1	17	1	0.02	0.90

a△means Fisher's exact probability method, because the frequency of cells appears 0

bICP means intrahepatic cholestasis of pregnancy

cFGR means fetal growth restriction

Neonatal asphyxia is divided into mild asphyxia and severe asphyxia, which are mainly evaluated based on the Apgar score. According to the Apgar score, a total score from 0 to 3 is classified as severe asphyxia, from 4 to 7 is classified as mildly asphyxiated, and from 8 to 10 is normal [10]. Table 4 shows that there was no significant difference in neonatal asphyxia between the two groups (p>0.05).

Table 4

Comparison result on neonatal asphyxia.

	Neonatal asphyxia						z-value	p-value
	Normal		Mild		Severe
	No.	%	No.	%	No.	%
Before lockdown	7097	99	51	1	11	0	0.54	0.46
After lockdown	3407	99	19	1	6	0

As shown in Table 5, the neonatal birth weight in the observation group was heavier than that in the control group among those with ≥34 gestational weeks (p<0.05). However, there was no significant difference among those with fewer than 34 gestational weeks (p>0.05).

Table 5

Newborn weight at different gestational age.

Newborn group	Before lockdown (g)	After lockdown (g)	t-value	p-value
28 ≤ gestational age(wks) <32	1,462±318	1479±231	-0.26	0.80
32 ≤ gestational age(wks) < 34	1,926±313	2,021±253	-1.54	0.13
34 ≤ gestational age(wks) < 37	2,583±424	2,652±3856	-2.06	<0.05
37 ≤ gestational age(wks) < 38	3,167±385	3,207±398	-2.95	<0.05
gestational age(wks) ≥39	3,402±370	3,426±384	-2.32	<0.05

Discussion

This paper presents a comparison of the indications for CD and newborn weights before and after the Wuhan lockdown. All the patients in the observation group and the control group were collected from the Maternal and Child Health Hospital of Hubei Province. During the lockdown to prevent the spread of the COVID-19 outbreak from 23 January 2020 to 13 March 2020, a total of 49,995 cases were confirmed in Wuhan with 2,446 deaths [11].

In our empirical study, the overall CD rate was not significant different between the observation group and the control group. The differences in most of the indications for CD between the observation group and control group were not significant. This may serve as reassurance to many pregnant women who are currently having to remain primarily at home that a lockdown is unlikely to dramatically affect complications of pregnancy. However, we empirically observed that the rate of CDMR increased significantly during this period. CDMR may reduce the risk of hemorrhage and transfusion, but is also potentially associated with a longer maternal hospital stay, an increased risk of respiratory problems for the infant, and the need for hysterectomy [9]. The main reason for the increase in the rate of CDMR was that the pregnant women in Wuhan were reluctant to wait for a natural birth due to fear of COVID-19 infection during hospitalization. After the city was locked down, 8 out of 13 pregnant women with confirmed COVID-19 underwent CD in our birth center. Severe COVID-19 was treated as an indication for CD according to the Chinese Expert Consensus [12]. If a pregnant woman had mild or asymptomatic COVID-19 and her cervix was dilated, vaginal delivery could be selected. If the fetus was in distress, the level of control of COVID-19 was unsatisfactory, or there were other indications for CD, CD was performed by obstetricians [13].

During the Wuhan lockdown, pregnant women had to remain in their homes, limiting their ability to exercise and attend appointments. They reduced the frequency of prenatal examinations because they were afraid of contracting COVID-19, and some pregnant women were never examined from the initiation of lockdown until delivery. Therefore, some important risk factors may not have been detected in a timely manner, leading to an increased incidence of fetal distress.

Through the comparison of the observation group and the control group, we found that lockdown may have led to heavier newborns with a gestational age greater than 34 weeks. The possible underlying contributory factors might include food and nutrition changes and lack of exercise. During pregnancy, balanced nutrition and adequate intake of vegetables and protein have a positive impact on the birth weight of the neonate [14-16]. However, due to the COVID-19 in Wuhan, supermarkets and vegetable markets were closed, and access to nutrient-rich food was relatively restricted. The relative lack of vegetables and food high in crude fiber, and the increased intake of carbohydrate-rich foods, such as rice and noodles, which were easily obtained and stored, led to an increase in neonatal weight. In addition, after the city was locked down, pregnant women became less active and exercised less. We recommend that during a city lockdown due to COVID-19, pregnant women should try to eat a balanced diet, increasing their intake of protein and vegetables as much as possible and controlling their intake of carbohydrates such as rice noodles, and increase their engagement in indoor activities.

Our research has some limitations. First, due to the reduction in or even absence of examinations of pregnant women, we could not collect the data on changes in body weight during this period. Second, the findings might have been affected by other factors, such as climate, food type, and other uncontrollable inputs, because the observation group was collected from a short period in 2020. The research question investigated in this study needs further exploration with other data sets.

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2 May 2020

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1 Jun 2020

PONE-D-20-12899

The Influence of lockdown on the indications of cesarean delivery and newborn weights during the epidemic period of COVID-19 in Wuhan

PLOS ONE

Dear Dr. Zhao,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

This paper represents a resubmission of a previously submitted paper that was reviewed extensively. The authors were provided the opportunity to tone down their claims and ensure that throughout the paper it was clear that they are not examining how COVID-19 affects pregnancy outcomes or analyze such samples. They chose the former approach. The original reviewers have reviewed the revised paper and expressed conflicting recommendations. However, both agree that the work is not "blockbuster", but it may provide some comfort to pregnant women having to quarantine that it will not drastically affect their neonates. In reviewing the journal guidelines, it will allow for descriptive papers, such as this one. That being sad, it still needs to meet certain standards in terms of the English and previous and current reviewer concerns need to be addressed. It is recommended to have the revised manuscript proofed by an outside individual before it is resubmitted. Both reviewers have also provided helpful comments.

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Reviewer #1: This toned-down manuscript with a more accurate title is much improved. It might be helpful to have a reader fluent in English correct some of the minor grammatical and style errors, even though the narrative is easy to follow and is readily comprehensible. Overall, the paper sends a reassuring message to women confined to home during a pandemic.

Reviewer #2: This is a revised version of a manuscript in which the authors report various metrics related to late pregnancy, Caesarian deliveries and other aspects of pregnancy in the Wuhan, China region during the pandemic. The manuscript has been improved, and a large number of problems identified by the reviewers have been addressed.

There has been great interest in whether the infection of a pregnant mother would result in any changes in the fetus during late gestation or the infants after birth. Although the current study does not address this, the questions the authors do address have some value as well, but perhaps not enough to justify a publication in a broad and general interest journal like this. It seems like these types of data would be more appropriate for a specialty human journal that focused on Ob/Gyn, rather than a general interest journal like PLOS One.

There are still a number of problems with the English. It was recommended in the initial review that the authors consider using this type of service, or get some other editorial help from a native English speaker. Just a few of the types of problems that occur in the manuscript are listed below; this is by no means a complete list.

Line 114: you cannot start a sentence with a numeral in English.

Line 120: SCORES

Line 155: you cannot start a sentence with a numeral in English.

Line 197: change “pregnant women were trapped in their homes” to “pregnant women were confined to their homes”

Line 197-198: change “and it was not convenient for them to go out for taking a walk.” To “and their ability to exercise was limited.”

Tables 1, 3 and 4: The authors should review rules on significant digits. It does not seem correct to show the percentage values with two places to the right of the decimal. Would not whole percentages perhaps be better?

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30 Jun 2020

Response to Editor

Q1. This paper represents a resubmission of a previously submitted paper that was reviewed extensively. The authors were provided the opportunity to tone down their claims and ensure that throughout the paper it was clear that they are not examining how COVID-19 affects pregnancy outcomes or analyze such samples. They chose the former approach. The original reviewers have reviewed the revised paper and expressed conflicting recommendations. However, both agree that the work is not "blockbuster", but it may provide some comfort to pregnant women having to quarantine that it will not drastically affect their neonates. In reviewing the journal guidelines, it will allow for descriptive papers, such as this one. That being sad, it still needs to meet certain standards in terms of the English and previous and current reviewer concerns need to be addressed. It is recommended to have the revised manuscript proofed by an outside individual before it is resubmitted. Both reviewers have also provided helpful comments.

Response: Thanks for your comments. Following the reviewers’ comments, we have revised the manuscript carefully. In order to enhance the writing, a well-known outside professional editing institution has assisted us in improving the English writing of our manuscript with charges., which has substantially improved the quality of the paper.

Response to Comments of Reviewer 1

Comments: This toned-down manuscript with a more accurate title is much improved. It might be helpful to have a reader fluent in English correct some of the minor grammatical and style errors, even though the narrative is easy to follow and is readily comprehensible. Overall, the paper sends a reassuring message to women confined to home during a pandemic.

Respond: Thanks for your positive comments with respect to our previous revision. In this round of revision, a professional institution has helped us in improving the English writing.

Response to Comments of Reviewer 2

Q1:There are still a number of problems with the English. It was recommended in the initial review that the authors consider using this type of service, or get some other editorial help from a native English speaker. Just a few of the types of problems that occur in the manuscript are listed below; this is by no means a complete list.

Line 114: you cannot start a sentence with a numeral in English.

Line 120: SCORES

Line 155: you cannot start a sentence with a numeral in English.

Line 197: change “pregnant women were trapped in their homes” to “pregnant women were confined to their homes”

Line 197-198: change “and it was not convenient for them to go out for taking a walk.” To “and their ability to exercise was limited.”

Response: Thanks for your comments. In the revised manuscript, we have corrected all the mistakes you pointed out. In addition, a well-known professional institution has helped us in improving the overall English writing.

Q2. Tables 1, 3 and 4: The authors should review rules on significant digits. It does not seem correct to show the percentage values with two places to the right of the decimal. Would not whole percentages perhaps be better?

Respond:According to your comments, we have reviewed the papers with respect to retrospective study published on PLOS ONE, which have been listed below. We decide the follow their rules on significant digits and also the percentage values. The corresponding tables Tables 1, 3 and 4 have been revised carefully.

Chu S, Chen Q, Chen Y, et al. Cesarean section without medical indication and risk of childhood asthma, and attenuation by breastfeeding[J]. PLoS One, 2017, 12(9): e0184920.

28 Jul 2020

Impact of Wuhan lockdown on the indications of cesarean delivery and newborn weights during the epidemic period of COVID-19

PONE-D-20-12899R1

Dear Dr. Zhao,

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Reviewer #1: All comments have been addressed

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Reviewer #1: (No Response)

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: (No Response)

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Reviewer #1: (No Response)

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Reviewer #1: (No Response)

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Reviewer #1: The paper is now suitable for publication. The written English is much improved and the the conclusions suitably muted.

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Reviewer #1: No

3 Aug 2020

PONE-D-20-12899R1

Impact of Wuhan lockdown on the indications of cesarean delivery and newborn weights during the epidemic period of COVID-19

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