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Original Research

Influenza A(H1N1)pdm09 infection in pregnant and non-pregnant women hospitalized in Singapore, May e December 2009 C. Lim a, L.W. Ang a,*, S.H. Tey a, L. James a, D. Kanagalingam b, L.L. Su c, H.K. Tan b, E.L. Yong c, M.L. Lim d a

Epidemiology and Disease Control Division, Ministry of Health, Singapore Department of Obstetrics & Gynaecology, Singapore General Hospital, Singapore c Department Obstetrics & Gynaecology, National University Hospital, Singapore d Department of Maternal Fetal Medicine, KK Women's and Children's Hospital, Singapore b

article info

abstract

Article history:

Objectives: The aim of this study was to compare the demographic and clinical character-

Received 13 October 2014

istics of pregnant women and non-pregnant women of childbearing age hospitalized with

Received in revised form

laboratory-confirmed influenza A(H1N1)pdm09 infection in Singapore, and to assess

20 April 2015

whether pregnancy was a risk factor associated with the development of influenza-related

Accepted 20 April 2015

complications.

Available online 27 May 2015

Study design: Retrospective observational study. Methods: We retrospectively identified and collected information from available medical

Keywords:

records of all women admitted to three tertiary hospitals between 26 May 2009 and 31

A(H1N1)pdm09

December 2009 with laboratory-confirmed influenza A(H1N1)pdm09 infection who were

Complications

either pregnant or non-pregnant and of childbearing age between 15 and 50 years.

Hospitalization

Results: A total of 222 women, of whom 81 (36.5%) were pregnant, were hospitalized during

Pregnancy

the study period. Pregnant women were significantly more likely to be hospitalized with

Singapore

influenza A(H1N1)pdm09 infection than non-pregnant women of childbearing age (relative risk 26.3; 95% confidence interval: 20.1e34.6). Among those hospitalized, the proportion of pregnant women having at least one underlying medical condition that could predispose them to influenza-related complications was significantly lower than that of non-pregnant women (32.1% versus 56.0%, P < 0.001). The median time from onset of symptoms to administration of anti-viral drugs was significantly shorter among pregnant women than among non-pregnant women (three days versus five days, P < 0.001). The median length of stay in hospital was also significantly shorter among pregnant women than that of nonpregnant women (two days versus three days, P ¼ 0.002). About 4.9% of pregnant women developed influenza-related complications, compared with 12.8% among non-pregnant women (P ¼ 0.066).

* Corresponding author. Epidemiology and Disease Control Division, Ministry of Health, Singapore, College of Medicine Building, 16 College Road, Singapore 169854, Singapore. Tel.: þ65 6325 1682. E-mail address: [email protected] (L.W. Ang). http://dx.doi.org/10.1016/j.puhe.2015.04.013 0033-3506/© 2015 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.

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Conclusions: Pregnant women with influenza A(H1N1)pdm09 infection were at a higher risk of hospitalization. Upon hospitalization, they were not at a higher risk of developing influenza-related complications. © 2015 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.

Introduction Evidence from experiences with seasonal influenza and past influenza pandemics1e5 has identified pregnant women as one of the groups at high risk for severe complications related to influenza A(H1N1)pdm09 infection, including hospitalizations, intensive care unit (ICU) admissions and deaths. Early case series of maternal hospitalizations and deaths associated with influenza A(H1N1)pdm09 infection had raised concerns that pregnant women were more severely affected, with pregnant women having higher rates of hospitalization, ICU admissions, and mortality compared to that of the general population.6e8 However, as the pandemic progressed, studies which investigated the effects of influenza A(H1N1)pdm09 infection in pregnancy had differential findings on the severity of illness. Whilst some studies reported an increased risk of severe illness, other studies had found decreased risk of admission to ICU among hospitalized cases.7e11 There had been two studies on pregnant women diagnosed with influenza A(H1N1)pdm09 infection seen at a tertiary referral centre in Singapore. A cohort study of pregnant women diagnosed with influenza A(H1N1)pdm09 infection indicated that the need for hospitalization was significantly associated with presenting symptoms of breathlessness and co-morbidity.12 The finding of an observational study on pregnant women who subsequently delivered suggested that influenza A(H1N1)pdm09 infection did not result in adverse effects on their obstetric outcomes.13 There are few studies to date that have compared characteristics of pregnant women with that of non-pregnant women of childbearing age, to ascertain if pregnancy is a risk factor associated with the development of complications among women of childbearing age hospitalized with influenza A(H1N1)pdm09 infection. In this study, the epidemiology of both hospitalized pregnant women and non-pregnant women of childbearing age diagnosed with influenza A(H1N1)pdm09 infection in Singapore was described. Our aims were to 1) estimate the hospitalization rate of influenza A(H1N1)pdm09 infection among pregnant women and non-pregnant women of childbearing age, 2) compare the demographic and clinical characteristics of these two groups, and 3) assess whether pregnancy was a risk factor associated with the development of complications among women of childbearing age hospitalized with influenza A(H1N1)pdm09 infection.

Materials and methods We retrospectively identified all women admitted to three tertiary public acute-care hospitals between 26 May and 31

December 2009 with laboratory-confirmed influenza A(H1N1) pdm09 infection who were either pregnant or of childbearing age between 15 and 50 years based on their admissions and laboratory records. Among the seven tertiary public acutecare hospitals in Singapore, three which have an obstetrics and gynaecology department were included in this study. Data were extracted from all available hospital records using a standard form. The data collection included patients' demographic characteristics such as age and ethnicity, medical information such as the presence of co-morbidities, defined as those that confer a higher risk of influenzarelated complications as specified by the Advisory Committee on Immunization Practices (ACIP),14 clinical symptoms upon presentation, complications developed if any, as well as admission and discharge diagnoses. Complications developed in women in our study were confined to those that were influenza-related, which include pneumonia and exacerbations of underlying pulmonary disease. While the focus was on the comparison of pregnant women with non-pregnant women of childbearing age, obstetric complications were described to provide a better understanding of the clinical characteristics of the pregnant women included in the study. There were studies linking obesity to the severity of influenza A(H1N1)pdm09 infection.15e20 However, subject to varying practices of the individual hospitals, obesity may have been defined subjectively, as body mass index (BMI) or height and/or weight were not routinely recorded in patients' medical records. In this study, obesity was not reported due to the high proportion of patients (54.5%) with missing information on BMI in the data form. Clinical data on history of vaccination against influenza, whether the patient had been admitted to intensive care unit, use of mechanical ventilation and dates on anti-viral treatment were also collected, where applicable. Additional information on gestational age of pregnancy and parity as well as outcome of pregnant women admitted to the hospitals during the study period was also collected. The study protocol was approved by the SingHealth Centralised Institutional Review Board (CIRB) and the National Healthcare Group Domain Specific Review Board (DSRB).

Statistical analysis We estimated the population of pregnant women in Singapore at any time point during the study period based on previously published methods,6,10,21 by adding the following two numbers: (1) sum of the number of live births, adjusted for multiple births, and stillbirths, multiplied by 9/12, since pregnancy lasts about nine months, and (2) the number of abortions multiplied by 2/12 since these pregnancies last an average of two months. The population of non-pregnant

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women of child-bearing age was estimated by subtracting the estimated number of pregnant women from the 2009 total population estimates of women aged 15e50 years in Singapore. We estimated that there were 31,355 pregnant women and 1,438,310 non-pregnant women aged 15e50 years in Singapore. As the distribution of length of hospital stay was highly skewed, the median and interquartile range (IQR) were computed instead of the mean and standard deviation. To assess differences in demographic and clinical characteristics between pregnant and non-pregnant women, the KruskaleWallis test was applied to continuous variables, while the Fisher's exact test or Chi-square test was applied to categorical variables, where appropriate. A P-value < 0.05 was considered to be statistically significant. All analyses were carried out using the statistical software R, version 2.14.2.

Results A total of 222 women aged 15e50 years with laboratoryconfirmed influenza A(H1N1)pdm09 infection, of whom 81 (36.5%) were pregnant, were admitted to the three tertiary public acute hospitals between 26 May 2009 and 31 December 2009. The hospitalization rate of influenza A(H1N1)pdm09 infection was significantly higher among pregnant than nonpregnant women aged 15e50 years (258.3 per 100,000 population of pregnant women compared with 9.8 per 100,000 nonpregnant women population); relative risk 26.3 (95% CI: 20.1 e 34.6). Fig. 1 shows the temporal distribution of women with laboratory-confirmed influenza A(H1N1)pdm09 infection admitted to the three public acute hospitals between 26 May and 31 December 2009. The majority of the women (88.3%)

771

were admitted between epidemiological week (E-week, from Sunday to Saturday) 25 (21e27 June) and E-week 35 (30 August e 5 September). An increase in admission of pregnant women was observed from E-week 26 (28 June e 4 July) which peaked in E-week 30 (26 July e 1 September), and decreased over the subsequent weeks. This temporal pattern was also observed in the admission of non-pregnant women of child-bearing age, with the increase observed one week earlier in E-week 25. Table 1 summarises the demographic and clinical characteristics of pregnant and non-pregnant women of childbearing age with influenza A(H1N1)pdm09 infection. Nearly half of the pregnant women (46.9%) hospitalized were aged between 25 and 34 years, which was double the proportion of non-pregnant women in the same age group (22.7%). A significantly lower proportion of pregnant women presented with fever above 38  C, compared to non-pregnant women (30.9% versus 80.9%, P < 0.001), while a significantly higher proportion of pregnant women presented with rhinorrhoea (54.3% versus 39.0%, P < 0.035). No significant differences were observed for presentation of other clinical symptoms. About one-third of pregnant women (32.1%) reported having at least one underlying medical condition that could predispose them to influenza-related complications, which was significantly lower compared to 56.0% among non-pregnant women (P < 0.001). In particular, the proportion of pregnant women with diabetes was significantly lower than that of nonpregnant women (2.5% versus 17.0%, P < 0.001). None of the pregnant women reported having chronic renal disease or were immune-compromised, as compared to 12.8% and 9.2% of non-pregnant women having the two medical conditions, respectively (P < 0.001and P ¼ 0.003, respectively). The median time from onset of illness to presentation at hospital was the same at two days for both groups. More than 90% of women in both groups received anti-viral drugs

Fig. 1 e Weekly number of women with laboratory confirmed influenza A(H1N1)pdm09 infection admitted to hospitals by pregnancy status between 26 May and 31 December 2009.

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Table 1 e Demographic and clinical characteristics of pregnant and non-pregnant women of child-bearing age (15e50 years) hospitalized with influenza A(H1N1)pdm09 infection. Characteristic Age (years) (%) 15e24 25e34 35e44 45 Ethnic group (%) Singapore Residents Chinese Malay Indian Others Foreigners Clinical presentation Fever >38  C (%) Cough (%) Rhinorrhea (%) Sore throat (%) Headache (%) Myalgia (%) Shortness of breath (%) Presence of comorbidity conditions (%) Chronic lung disease Diabetes Cardiac disease Chronic renal disease Chronic liver disease Immunocompromised Hematological disorder History of asthma (%)b 1 comorbid condition present (%)c Received any influenza vaccination (%) Interval between onset of illness and presentation to hospital [median no. of days (IQR)]d Use of anti-viral drugs (%) Onset of symptoms to administration of anti-viral drugs [median no. of days (IQR)] Administration of anti-viral drugs after admission (%) Presence of complications (%)e Admitted to ICU (%) Use of ventilator support (%) Total length of stay [median no. of days (IQR)] Nosocomial infection (%)f Deaths (%)

All (n ¼ 222)

Pregnant (n ¼ 81)

Non-pregnant (n ¼ 141)

P-value

Influenza A(H1N1)pdm09 infection in pregnant and non-pregnant women hospitalized in Singapore, May - December 2009.

The aim of this study was to compare the demographic and clinical characteristics of pregnant women and non-pregnant women of childbearing age hospita...
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