Risk of preterm birth in maternal influenza or SARS-CoV-2 infection: a systematic review and meta-analysis
• We searched eligible studies in five databases including PubMed, Embase, Cochrane Library, Web of Science, and CNKI to investigate the impact of maternal influenza infection on preterm birth. This meta-analysis finally included twenty-four studies involving 24,760,890 patients, and we found that maternal influenza infection significantly increased the risk of preterm birth, especially for women infected with influenza A, B, and SARS-CoV-2.
What is known and what is new?
• At present, there is a controversy on the impact of influenza infection on preterm birth.
• This current meta-analysis provides the most reliable results available to resolve this dispute and to provide clinical evidence.
What is the implication, and what should change now?
• Our analysis suggested that doctors and pregnant women should take active steps to avoid influenza infection during pregnancy to reduce the possibility of preterm birth.
Influenza is a major threat to global health and is an important cause of lower respiratory tract infections and other respiratory diseases (1). Although influenza’s infection and mortality rates have decreased with the widespread availability of vaccines, it still causes approximately 250,000 to 500,000 deaths globally each year, especially in people over 65 years old (2-4). Approximately 0.6% pregnant women had hospitalization during the influenza season. Influenza-related hospitalizations and deaths are mainly caused by associated complications, including pneumonia, cardiovascular events, worsening of chronic underlying disease, and reduced function (5-7). Moreover, influenza infection not only causes adverse pregnancy outcomes but also negatively impacts the infant’s health (8,9).
Preterm birth is generally defined as a live birth that occurs before 37 weeks of pregnancy and is a common adverse pregnancy outcome (9). It affects approximately 11% of births worldwide and is a major cause of maternal and fetal morbidity and mortality (10-12). Although many interventions have been evaluated, there is little high-quality evidence to confirm their effectiveness in reducing preterm birth (13,14).
Concerning the effect of influenza infection during pregnancy on preterm birth, most studies have demonstrated that influenza infection did not increase the probability of preterm birth (15-29); however, some other studies found that influenza infection was a risk factor for preterm birth (30-38). Therefore, we conducted this systematic review and meta-analysis to assess the impact of influenza infection on preterm birth and hopefully provide evidence for the need for influenza vaccination of pregnant women and the allocation of medical resources. We present the following article in accordance with the MOOSE reporting checklist (39) (available at https://tp.amegroups.com/article/view/10.21037/tp-23-134/rc).
Text words were used to search for eligible studies, and the search strategy included the following terms: pregnancy, influenza, and preterm birth. As for pregnancy, the text words were as follows: pregnancy OR pregnant OR Pregnant women OR mothers OR gestation. As for influenza, the text words were as follows: influenza OR respiratory tract infections OR upper respiratory tract infections OR respiratory infection OR common cold OR acute coryza OR flu OR grippe. The search was restricted to the title, abstract, and keywords. Both English and Chinese language articles were allowed.
Inclusion and exclusion criteria
The inclusion criteria were as follows: (I) influenza infection in pregnant women; and (II) preterm birth was reported. The exclusion criteria were as follows: (I) insufficient data for comparison; (II) insufficient data to assess the pooled effect of influenza on preterm birth; and (III) study types such as conferences abstracts, trials, reviews, meta-analyses, case reports, letters to the editor, or comments.
The above search strategy was employed in five databases, including PubMed, Embase, Cochrane Library, Web of Science, and China National Knowledge Infrastructure (CNKI). Next, duplicate records were removed, and then, studies with irrelevant content (according to their titles and abstracts) were excluded. Finally, except for studies without full texts, the remaining studies were independently screened by two authors based on the inclusion and exclusion criteria, while discrepancies between the authors were resolved by group discussion.
All clinic information were collected from medical records. The following data were collected from the selected studies: first author, published year, published country, study period, sample size, study type, influenza type, cut-off or definition of preterm birth, findings, and Newcastle-Ottawa Scale (NOS) score. Patients were divided into the influenza-positive group and the influenza-negative group, and the number of preterm birth were collected. Two authors independently extracted data and reached a consensus to prevent any extraction errors.
The NOS score was used to assess the quality of the included studies based on selection, comparability, and outcome (40). Cohort selection included the representativeness of exposure, selection of the non-exposure, ascertainment of exposure, and demonstration that the outcome was not present at the start. Comparability was based on the design and analysis of cohorts. The assessment of outcome included assessment, long follow-up for outcomes to occur, and adequacy of follow-up. Studies that scored >7 were considered high quality; otherwise, the study was considered low quality.
As for the risk of preterm birth in women infected with influenza, odds ratios (ORs) and confidence intervals (CIs) were preferred and were estimated using raw data from reconstructed 2*2 tables. The effect values including relative risks (RRs) and hazards ratios (HRs) were crudely used as ORs. Then, the ORs and CIs were pooled using the random-effect model, and P<0.1 was considered statistically significant.
The I2 value and the chi-squared test were used to evaluate the statistical heterogeneity (41,42); the I²<30% was considered non-important, 30–60% was considered moderate, and >60% was considered substantial. A forest plot was used to display the results of the meta-analysis. Subgroup analysis based on similarity in different aspects was used for further analysis. A funnel plot was used to assess the publication bias. All data analyses were performed using STATA SE V16.0 software.
A total of 951 studies were identified after performing the search strategy in five databases on December 29, 2022 (151 studies in PubMed, 206 studies in Embase, 25 studies in Cochrane Library, 542 studies in Web of Science, and 27 studies in CNKI). Among these, 214 duplicate records were removed before screening. Then, 685 records were excluded after examining their titles and abstracts. Eight studies with unavailable full text were excepted, 20 studies were excluded because no comparisons or critical data were missing, and 24 studies were finally selected based on the inclusion and exclusion criteria (Figure 1).
The current meta-analysis included 24 eligible studies involving 24,760,890 patients. Ten studies were conducted in the USA, four studies were conducted in Canada, two studies were conducted in Norway, and the remaining studies were conducted in Hungary, Thailand, Turkey, Spain, the UK, Brazil, Korea, and Sweden. The year of publication ranged from 2003 to 2022, and all of the included studies were cohort studies. The influenza types included seasonal influenza, influenza A (H1N1, H3N1, H3N2), influenza B (Yamagata, Victoria), and Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). Other study data including the author, study period, sample size, cut-off or definition of preterm birth, findings, and NOS score were shown in Table 1.
|Author||Year||Country||Study period||Sample size||Study type||Influenza type||Cut-off or definition of PTB||Findings||NOS score|
|Acs N (15)||2006||Hungary||1980–1996||38151||Cohort||Seasonal||37 completed weeks (259 days)||Mothers with influenza in pregnancy had a lower proportion of PTB||8|
|Cox S (30)||2006||USA||1998–2002||6277508||Cohort||Influenza A(H3N2), A(H3N1), and B||International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) diagnosis code 644||During influenza season, hospitalized pregnant women with respiratory illness had significantly longer lengths of stay and higher odds of delivery complications compared to hospitalized pregnant women without respiratory illness||9|
|Dawood FS (16)||2021||Thailand||2017–2018||11277||Prospective cohort||87% influenza A (H1N1, H3N2), and 13% influenza B (Yamagata, Victoria)||37 weeks||Antenatal influenza was not associated with PTB||8|
|Doyle TJ (31)||2013||USA||2009–2010||295934||Retrospective cohort||Influenza A(H1N1)||37 weeks||Children born to women with pH1N1 illness during pregnancy were at an increased risk of PTB||9|
|Ersoy AO (17)||2017||Turkey||2014–2015||35||Cohort||77.8% influenza A and 22.2% influenza B||37 weeks||Preterm deliveries in pregnant women did not differ significantly between influenza-positive and influenza-negative pregnant women in a non-vaccinated study population||5|
|Fell DB (18)||2018||Canada||2009–2011||192082||Retrospective cohort||Influenza A (H1N1)||37 completed weeks||In the general obstetrical population, there was no association between pH1N1 influenza illness and PTB||9|
|Hansen C (19)||2012||USA||2008–2010||107889||Cohort||25% seasonal virus and 75% Influenza A (H1N1)||37 weeks||Among infants delivered by women with a diagnosis of A(H1N1)pdm09 or seasonal influenza virus infection, the prevalence of PTB was similar to those among infants delivered by women without a diagnosis||9|
|Hartert TV (20)||2003||USA||1985–1993||880||Matched cohort study||Seasonal influenza||37 completed weeks||We detected no significant increase in the adverse perinatal outcomes associated with respiratory hospitalizations during the influenza season||6|
|Laake I (21)||2018||Norway||2009||1258||Cohort||Influenza A (H1N1)||37 completed weeks||No significant associations between influenza and risk of PTB were observed||7|
|Martin A (32)||2013||USA||1998–2008||15739700||Cohort||Influenza A (H1N1, H3N2) and B||ICD-9-CM diagnosis code 644.2||Among live births, there were higher odds of preterm delivery||9|
|McNeil SA (22)||2011||Canada||1990–2002||132588||Retrospective cohort study||Seasonal influenza||37 weeks||Infants who were born to mothers who had been hospitalized for respiratory illness during the influenza season at any time during pregnancy were not associated with PTB||9|
|Morken NH (23)||2011||Norway||1999–2008||265931||Prospective cohort||Seasonal influenza||between gestational weeks 22 + 0 days and 36 + 6 days||Only ear-nose-throat infection in early pregnancy was associated with an increased risk of spontaneous preterm delivery||9|
|Naresh A (24)||2013||USA||2009–2010||841||Multicenter observational cohort study||Influenza A (H1N1)||37 completed weeks||Pregnant women with mild clinical illness secondary to 2009 H1N1 influenza were not at a greater risk of adverse pregnancy outcomes||6|
|Newsome K (33)||2019||USA||2009||1941||Matched retrospective cohort||Influenza A (H1N1)||37 weeks||Severely ill women with 2009 H1N1 influenza during pregnancy were more likely to have adverse birth outcomes than women without influenza||7|
|Nieto-Pascual L (25)||2013||Spain||2009–2010||168||Cohort||Influenza A (H1N1)||37 weeks||No differences were found between the obstetric and perinatal outcomes of both affected and unaffected or treated and untreated cohorts||6|
|Pierce M (34)||2011||UK||2009–2010||1476||Cohort||Influenza A (H1N1)||37 weeks||Women infected with 2009/H1N1 influenza in pregnancy were at risk of poor pregnancy outcomes, with an increased risk of preterm and very preterm delivery||7|
|Prasad N (26)||2019||USA||2012–2015||83||Cohort||Influenza A (H1N1, H3N2) and B||37 weeks||There was no significant difference in premature delivery between influenza-positive and influenza-negative patients||5|
|Regan AK (35)||2020||Canada||2009||4750||Retrospective cohort||Seasonal influenza||between ≥20 and <37 weeks||Compared to non-hospitalized women, the risk of PTB was greater among women hospitalized with influenza-associated acute respiratory or febrile illness||7|
|Regan AK (36)||2022||USA||2020–2021||78283||Cohort||SARS-CoV-2||NA||Prenatal SARS-CoV-2 infection was associated with an increased risk of adverse pregnancy outcomes||8|
|Rogers VL (27)||2010||USA||2003–2004||31064||Prospective observational study||Influenza A (H3N2)||37 weeks||Compared with our general obstetric population, there was no significant difference in obstetric or neonatal complications||8|
|da Silva AA (28)||2014||Brazil||2009||243||Prospective cohort study||82.7% influenza A (H1N1), and 17.3% seasonal influenza A||37 weeks||There were no differences in the perinatal outcomes||5|
|Song JY (37)||2020||Korea||2007–2010||1563626||Retrospective cohort study||ICD-10 code J09, J10, and J11||37 weeks||Multivariate analysis revealed that maternal influenza infection significantly increased the risk of PTB||9|
|Stephansson O (38)||2022||Sweden||2020–2021||14665||Prospective cohort study||SARS-CoV-2||37+0 weeks||Compared with term births, test-positivity was higher in medically-indicated PTB but not significantly increased in spontaneous PTB||8|
|Tuyishime JD (29)||2003||Canada||2002||517||Cohort||Influenza A||NA||There was no indication of an increased frequency of adverse perinatal outcomes associated with influenza-like illness during pregnancy||6|
Note: 37 completed weeks means 37+0 weeks; 37 weeks means for 37+0 weeks to 37+7 weeks. NOS, Newcastle-Ottawa Scales; PTB, preterm birth NA, not assessed; ICD-9-CM, International Classification of Diseases, Ninth Revision, Clinical Modification; SARS-CoV-2, Severe Acute Respiratory Syndrome Coronavirus 2.
Preterm birth of influenza infection
Although more than half of the included studies reported that influenza infection was not associated with preterm birth, the current meta-analysis found there were more preterm births in women infected with influenza during pregnancy (OR =1.52, 95% CI: 1.18 to 1.97, I2=97.35%, P=0.00). Notably, one study provided separate ORs for two influenza types. See Figure 2.
Preterm births according to the different types of influenza
A subgroup analysis was conducted according to the similarity in influenza types and found that there were still more preterm births in women infected with influenza A and B (OR =2.05, 95% CI: 1.26 to 3.32, I2=96.14%, P<0.1) and SARS-CoV-2 (OR =2.16, 95% CI: 1.75 to 2.66, I2=0.00%, P<0.1). However, infection with influenza A alone (OR =1.38, 95% CI: 0.96 to 2.00, I2=85.36%, P>0.1) or seasonal influenza (OR =1.15, 95% CI: 0.91 to 1.44, I2=91.93%, P>0.1) did not increase the risk of preterm birth. Moreover, statistical heterogeneity remained high within most subgroups; the only subgroup in which heterogeneity was substantially reduced was that containing only studies of SARS-CoV-2. However, there was significant heterogeneity between the subgroups (P=0.00), which signified that the influenza subtypes might be a source of heterogeneity (Figure 3).
Preterm birth in different areas
As the spread of influenza varies geographically, studies were divided into four continent groups according to the countries in which they were carried out. Following the subgroup analysis, we found that influenza infection was still a risk factor in North America (OR =1.55, 95% CI: 1.09 to 2.21, I2=96.71%, P<0.1), Europe (OR =1.56, 95% CI: 1.01 to 2.41, I2=92.38%, P<0.1), and Asia (OR =1.41, 95% CI: 1.34 to 1.49, I2=0%, P<0.1). However, statistical heterogeneity remained high within most subgroups, and the heterogeneity between the subgroups was not significant (Figure 4).
Preterm birth during different periods
We identified a significant number of studies that focused on the 2009–2010 pandemic and grouped them according to the study period. The analysis showed that influenza infection had no significant effect on preterm birth before 2009 (OR =1.52, 95% CI: 0.81 to 2.85, I2=99.08%, P>0.1) but increased the risk of preterm birth during 2009–2010 (OR =1.35, 95% CI: 1.11 to 1.66, I2=83.58%, P<0.1) and after 2010 (OR =2.04, 95% CI: 1.51 to 2.75, I2=36.32%, P<0.1). However, statistical heterogeneity remained high within most subgroups, and the heterogeneity between the subgroups was not significant (Figure 5).
A funnel plot was used to assess the publication bias. Although there were some points outside the 95% CIs, the funnel plot remained relatively symmetrical (Figure 6).
Each study was sequentially excluded for sensitivity analysis, and the results were not significantly different, which meant the results were relatively robust.
This meta-analysis included 24 studies and found that pregnant women infected with influenza during pregnancy had a higher risk of preterm birth, especially for the influenza A and B and SARS-CoV-2 viruses.
Preterm birth is a syndrome of unclear etiologies, with the majority of cases being spontaneous (43). It can be triggered by a variety of factors, such as infection, cervical pathology, uterine overdistension, progesterone deficiency, and maternal-fetal stress (44-46). These different etiologies can activate complex pathological pathways, leading to uterine contraction, cervical ripening, and fetal membrane rupture (47). While some measures can be taken to identify the risk of preterm birth, such as cervical length measurement by transvaginal ultrasound (TVUE), more interventional triggers need to be identified to reduce the incidence of preterm birth (48).
As for influenza infection, most of the studies included in this meta-analysis revealed that antenatal influenza was not associated with preterm birth (15-29), and some even found a lower proportion of preterm births in mothers with influenza in pregnancy (15,19,21,23,27-29). However, Pierce et al. demonstrated that women infected with H1N1 influenza were at risk of an increased risk of preterm and very preterm delivery (34). Moreover, Regan et al. also showed that prenatal SARS-CoV-2 infection increased the risk of adverse pregnancy outcomes (36). Based on the current inconsistencies in the literature, we hoped to provide more accurate results through meta-analysis to guide clinical decisions.
The potential effects of the influenza virus on the mother and fetus are not well understood. Since influenza viruses are rarely passed through the placenta, the infection is more likely to cause preterm birth through other mechanisms, such as maternal fever and inflammatory responses (49-51). Elevated levels of pro-inflammatory cytokines in the body can cause immune perturbation, leading to the sluggish establishment of immune tolerance and excessive inflammation, which in turn affects placental function (52,53). Notably, feto-maternal immune tolerance is also a key feature in some other pregnancy complications (54,55).
Furthermore, pro-inflammatory cytokines in the vaginal fluid can also play a role in determining the timing of pregnancy by influencing the microbiome (56). The abundance of taxa associated with preterm birth tends to decrease in the vaginal environment during the entire pregnancy (57,58). Pro-inflammatory cytokines are highly associated with the ecological dysregulation of bacterial taxa (for example, A. vaginae, G. vaginalis, and Megasphaera type 1), which contribute to preterm birth (58,59). However, carriage rates of the vaginal microbiome and specific microbial taxa vary considerably between populations and this mechanism needs to be further validated in a multi-ethnic population.
This was the first meta-analysis investigating the impact of maternal influenza infection on preterm birth, but there were some limitations. Firstly, besides influenza-positive patients, this study included pregnant women hospitalized with acute respiratory illness during the influenza season and could not classify them according to the influenza test results. Secondly, further studies on the clinical outcomes of influenza B infection are needed in the future, and more research on the impact of SARS-CoV-2 on pregnancy outcomes is also expected.
Although a majority of studies suggested that influenza infection during pregnancy did not increase the probability of preterm birth, this meta-analysis found that women infected with influenza had a higher risk of preterm birth. We hope that more relevant public health measures such as vaccination can be enacted to increase the awareness of pregnant women and protect them from infection.
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(English Language Editor: A. Kassem)