Korean J Intern Med > Volume 34(5); 2019 > Article
Choi, Choi, Noh, Song, Kim, Park, Lee, Seo, Baek, Choi, and Cheong: Clinical and economic analysis of the 2009 H1N1 influenza pandemic among pregnant Korean women

Abstract

Background/Aims

Unlike Western countries, the 2009 pandemic influenza infection among pregnant women was reported as mild in a previous interim study in South Korea. However, several mortalities were reported thereafter, suggesting that nationwide data were lacking.

Methods

This case-control study covers the entire 2009 pandemic inf luenza period, from May 2009 to February 2010. The clinical and economic data of pregnant (case) and age-matched non-pregnant (control) women with influenza A (H1N1) pdm09 virus (H1N1pdm09) infection were retrospectively collected from nine hospitals in South Korea.

Results

A total of 130 pregnant women with H1N1pdm09 infection were identified. The mean age of the pregnant women was 31.1 years (range, 19 to 41) and mean gestational age was 18.4 weeks (range, 3 to 40). Both case and control groups were similar in terms of age (p = 0.43) and comorbidities (p = 0.18). The overall rate of complications was comparable between the two groups (p = 0.648). However, mortality was reported only among the cases, so mean economic per capita burden is estimated to be higher for pregnant women compared to the control (4,821,992 Korean won [KRW] vs. 351,233 KRW, p = 0.31). Obstetric complications were observed in 12 cases, including preterm labor (n = 7), low birth-weight (n = 3), miscarriage (n = 1), stillbirth (n = 1), and cleft lip (n = 1).

Conclusions

Although statistically insignificant, the detrimental impact of influenza A H1N1pdm09 on pregnancy can be serious in some complicated cases in South Korea. Thus, the strong recommendation of influenza vaccination should be maintained for pregnant women as a high priority.

INTRODUCTION

Influenza is a major global cause of morbidity and mortality, resulting in an estimated three to five million cases of severe illness and 250,000 to 500,000 deaths annually [1,2]. The risk of complication from influenza is known to increase depending on risk factors, including age, comorbidity, and pregnancy [1-3]. Changes in the immune system, heart, and lungs of pregnant women make them more susceptible to severe illness from influenza, and result in serious problems for the unborn fetus, including premature labor and delivery [4-6]. The impact of influenza on pregnancy has been reported in previous pandemics, particularly the increased risk of complications among pregnant women compared to general population [7,8]. The 2009 influenza A (H1N1) pdm09 virus (H1N1pdm09) pandemic was the first influenza pandemic to occur in the era of modern obstetric and intensive care management; however, during this pandemic, these similar and serious outcomes were also found among pregnant women in many countries [3,9-14]. Accordingly, the World Health Organization recommends influenza vaccination for pregnant women as the highest priority group.
In contrast to most studies from countries other than Korea, which showed worse clinical courses from influenza during pregnancy in the 2009 pandemic, a few countries reported that influenza A H1N1pdm09 infection did not cause significant concern among pregnant women [15-18]. This regional disparity warrants the need to evaluate the significance of pregnancy in diverse geographic regions. In South Korea, multi-center analysis reported mild clinical features in pregnancy without any mortality during the 2009 pandemic [19]. However, after this interim analysis, several fatal cases were reported [20,21], suggesting that nationwide data on the clinical impact of the 2009 pandemic influenza on pregnant Korean women were lacking.
In this study, pregnant women with influenza A H1N1pdm09 infection were evaluated in comparison with non-pregnant controls with respect to disease complications and economic burden.

METHODS

Selection of study subjects

We performed a retrospective case-control study in women of reproductive age (ages between 18 and 44 years) admitted to nine university hospitals in cities of South Korea (Seoul, n = 2; Incheon, n = 1; Ansan, n = 1; Suwon, n = 1; Wonju, n = 1; Daegu, n = 1; Busan, n = 1, and Gwangju, n = 1) between May 2, 2009 (date of confirmation of the first case of pandemic influenza A(H1N1) pdm09 in Korea) and February 28, 2010 (decline of the influenza pandemic). A case was defined as a pregnant woman with laboratory-confirmed H1N1pdm09 infection, and was an outpatient or inpatient. H1N1pdm09 infection was diagnosed from respiratory specimens by using the rapid antigen test or real-time reverse-transcription polymerase chain reaction assay. Age-matched controls (age of case ± 5 years) were non-pregnant women with pandemic influenza infection who had visited the same hospital as a study subject during the study period. If multiple persons met the inclusion criteria, the person who visited the hospital on the nearest date to that of a respective case patient was selected as a control.

Data collection

A standardized case report form was used to collect the following data from the patients’ medical records: age, trimester of pregnancy (in case of pregnancy), previous medical history, hospital admission, intensive care unit (ICU) admission, duration of hospitalization, influenzarelated complications and mortality, obstetric results, medical treatments and procedures, and medical costs.

Calculation of medical costs

We classified costs as direct and indirect, and we used formula from a previous study for the calculation of medical costs [22]. Direct cost, the cost incurred during hospitalization or while visiting a clinic, was subdivided into direct medical cost and direct non-medical cost. The direct medical cost was defined as the cost of treatment. This was extracted from the hospital’s financial database, which included both outpatient and inpatient cost information such as: hospitalization expenditures, nursing, influenza-related prescription drugs, examination, fees, and so forth. Medication costs among outpatients were calculated by quantifying the total price using the reference price (http://www.kimsonline.co.kr/drugcenter/calculator/drugcalculator) of prescription drugs that were verified as influenza-related drugs by health-care professionals in each hospital. The direct non-medical cost was defined as a sum of transport expenses and nursing costs [23]. Data from the Korea Health Panel (2010) were used for transport expenses (7,597 Korean won [KRW]), which were corrected using the traffic price index of Korean Statistical Information Service (KOSIS) [24]. In the case of hospitalized patients, the transport expenses were calculated triple including the two visits of guardian per hospitalization. The nursing cost was applied as KRW 60,000 per day, according to the result of “research on the institutionalization of nursing services” reported by the Ministry of Health and Welfare and the Korean Institute for Health and Social Affairs.
For estimating the indirect costs, the human capital approach was used, which is based on the cost of lost workdays owing to the disease. Annual data of KOSIS were used to determine the employment rate and average daily income [24]. Based on the results of a previous study, the proportion was presumed to be one-thirds which meant that the indirect cost of three patients at a clinic was equivalent to that of one patient in a hospital ward [25]. The cost of lost income due to early death was restrictively applied to persons aged 20 to 65 years with an annual interest rate of 3%. The estimated costs of disease were calculated in KRW.

Statistical analysis

Data were analyzed using SPSS software version 12.0 for Windows (SPSS Inc., Chicago, IL, USA). Basic frequencies and proportions were calculated. We conducted univariate and bivariate analyses to compare the characteristics of the pregnant women with those of infected non-pregnant women; chi-square and Fisher exact tests were performed to test the significance of the differences in the proportions.

Ethical approval

This study was performed with the approval of the Institution Review Boards (IRBs) of the selected university hospitals (IRB No. AS14085, KUGH11088). The study was performed in accordance with the Helsinki Declaration of 1975, as revised in 2000. Each patient in the current study was informed about data usage for this investigation. However, because this study was a retrospective medical record- based study and the study subjects were de-identified, the IRB waived the need for written consent from the patients.

RESULTS

During the study period, 130 pregnant women with influenza A H1N1pdm09 infection presented to our hospitals. The characteristics of these women and the matched control group are shown in Table 1. The mean age of the pregnant women was 31.1 years (range, 19 to 41); 107 women (82.3%) were in the first or second trimester of pregnancy and 23 (17.7%) were in the third trimester of pregnancy. Overall, only five patients (3.8%) had medical comorbidities that put them at an increased risk of influenza-related morbidity.
The two groups were similar in terms of age (p = 0.43) and comorbidity (p = 0.18). It was difficult to assess the significance of comorbidities because of the low prevalence. Among 201 women (77.3%) with available data of vaccination history, the vaccination rate among the pregnant women was 32% which was similar to that of non-pregnant women (p = 0.631).
Receipt of antiviral treatment between the two groups was significantly different (71.5% of pregnant women and 87.7% of non-pregnant women, p = 0.001). However, in terms of starting antiviral treatment within 2 days of symptom-onset, the two groups showed similar results (75.6% and 79.1%, for pregnant and non-pregnant women, respectively) (p = 0.559).
The comparison of disease burden between the pregnant and non-pregnant women with influenza A H1N1pdm09 infection is shown in Table 2. Although the incidence was too small to verify any significant result, the overall rate of complications was similar between the two groups (p = 0.648), and mortality was reported only in the pregnant group. Overall 13 of the pregnant women (10%) were admitted. The hospitalization rate was higher among the pregnant women (p = 0.051), but the hospitalization period was shorter, with a mean length of hospital stay of 7.3 days among the pregnant women and 12.8 days in the non-pregnant group. Most pregnant women were admitted due to influenza-like illness (11 of 13 cases, of whom nine were uncomplicated, and two were complicated influenza-like illnesses), except two cases with pregnancy-related complications. We had two pregnant women with influenza A H1N1pdm09 infection complicated by pneumonia, one of whom died. The patient who died was a 30-year-old woman at 31 weeks of gestation, with gestational diabetes diagnosed at 28 weeks, who present with a 3-day history of fever, cough, and breathlessness. Despite receiving oseltamivir treatment and ICU care, she died on day 26 of hospitalization. Two non-pregnant women had infections that were complicated by pneumonia; neither of them was admitted to ICU or died.
Among the patients in the study, obstetric complications included preterm labor (n = 7), low birth-weight (n = 3), miscarriage (n = 1), stillbirth (n = 1), and cleft lip (n = 1) (Table 3). In the analysis of pregnant women with obstetric complications, the median maternal age was 30.5 years (range, 19 to 33) and only three of them (25%) had comorbidity. Of these cases with obstetric complications, only one had a respiratory complication during the treatment period, and she died owing to pneumonia.
When pregnant women with influenza A H1N1pdm09 infection were classified by gestational age, there was no substantial difference between the groups in terms of maternal age and comorbidities. Pregnancy-related complications and hospitalization rate tended to increase in the third trimester (pregnancy-related complications [n = 12], 13% in the third trimester, 8.3% in the second, and 8.5% in the first, p = 0.787; or hospitalization rate [n = 13], 17.4% in the third trimester, 8.3% in the second, and 8.5% in the first, p = 0.428). Assessing the association between respiratory complications and the stage of pregnancy was not possible because of the small number of events (n = 2).
Although not statistically significant, the overall economic per capita burden tended to be higher for pregnant women than for non-pregnant women (4,821,992 KRW and 351,233 KRW, respectively, p = 0.31) (Table 2). With the exception of one death, the average per capita burden for the pregnant women was 400,242 KRW, which was similar for both groups (p = 0.457), and direct medical costs accounted for more than 70% of the costs in both groups. However, in the analysis that included the one death, the cost owing to lost workdays was dramatically increased, changing the largest proportion of economic burden to indirect costs (86.7%) in the case group.

DISCUSSION

To the best of our knowledge, this was the first study to analyze the clinical impact of influenza infection on pregnant women during the entire period of the most recent pandemic influenza season in South Korea. This hospital-based case-control study identified the clinical and economic burdens of pandemic influenza A H1N1pdm09 infection among pregnant Korean women in comparison with those among non-pregnant women. There were no significant differences found between the two groups. Although the higher rate of admission could be understood in relation to disease severity, the preferential hospitalization of pregnant women might lead to an overestimation of the influenza burden in pregnant women. Evidence of this is found in the shorter length of hospital stay and the hospitalization of the majority of pregnant women owing to uncomplicated influenza-like illnesses.
The obstetric complications observed in this study were similar to those of the general population. Among 73 patients (56.2% of total) with available data, preterm delivery was 9.6%. This was much lower than previously found in countries outside Korea, with a premature birth rate of 15% to 36% [12,14,26,27] but similar to a baseline rate of preterm birth of 9.6% worldwide [28]. The incidence of low birth weight of 4.1% was also lower than the 9% to 30% reported in studies outside Korea [12,14,17] but similar to 4.9% reported in Korea birth statistics, 2009 [29]. Fetal abnormalities were recorded in one case (cleft lip, n = 1). It seemed to be more common in the study group than in the general population as reported in Korea (0.8% vs. 0.1%) [30]; however, these findings should be interpreted with caution considering the small number of events. Furthermore, it is difficult to confirm that these fetal abnormalities were directly related to influenza A H1N1pdm09 infection.
Observations from past pandemics and seasonal influenza epidemics have identified pregnant women to be susceptible to influenza-related mortality and morbidity. The 2009 pandemic outbreak appeared to be a severe one, as reported in the United States, Australia, and France [10,12,14,26]. However, a low clinical burden was also reported in some Asian countries including Japan, Singapore, and Indian Island [15-17]. In Korea, as shown in this study, pregnant women did not carry a higher burden of the disease than non-pregnant women did after influenza A H1N1pdm09 infection. Such mild clinical features among Korean pregnant women may be explained by several factors. First, the majority (96.2%) of our patients had no recognized comorbidities except for the pregnancy itself. In the United States, Australia and France, which reported a greater pandemic severity in pregnancy, overall 21% to 56% of infected pregnant women had documented comorbidities [10,12-14,26,31]. Second, a smaller number of pregnant women in their third trimester were enrolled in our study (17.7%) than in previous studies that reported worse outcomes (26% to 78%) [10,12,31]. Data from previous pandemics and seasonal influenza suggest that the risk of influenza complications might be higher in the advanced stages of pregnancy [27,32,33]. In accordance with this, our study observed a higher proportion of influenza-related complications occurring in the third trimester of pregnancy. The underlying mechanism is not well understood, but the physiologic changes that accompany the advanced stages of pregnancy such as decreased functional capacity of the lungs and increased oxygen consumption may support the concern about the increased risk of serious complications [33]. Third, early antiviral treatment might be related to favorable clinical outcome. Among the pregnant women, the majority (75.6%) received antivirals within 2 days of the onset of symptoms. Other countries that reported greater pandemic severity such as the United States and Australia also reported a similar proportion of antiviral use among pregnant women with influenza infection (50% to 85%) [10,26,31], but less than half of them received oseltamivir within 2 days of the onset of symptoms. Similarly, a French study found that delayed administration of antivirals was strongly associated with severe outcomes, regardless of antiviral use. Fourth, the high seasonal influenza vaccination rate among pregnant women could be interpreted as reflecting heightened public interest. The vaccination rate for seasonal influenza was only 4% among Korean pregnant women before the 2009 pandemic [34]; however, as many as 32% of the pregnant women were vaccinated during the pandemic season in this study. Increased interest may have aided in preventing them from contracting influenza or developing severe complications. Fifth, although not examined in this study, the maternal complications were low compared to other studies, which might be due to the relatively low prevalence of obesity in Korean women. Based on the Organisation for Economic Co-operation and Development (OECD) report, the prevalence of obesity (body mass index > 30) among Korean women was 4.1%, the lowest among OECD countries, except Japan [35]. Based on this report, Japan, China, and India, which also reported less pandemic severity among pregnant women [15,17,18], have a prevalence of obesity of less than 5%, suggesting that the lower rate of severe complications seen in Asian countries might be attributable to a relatively low body mass index. It was known that obesity was associated with increased maternal complications [18]. Lastly, cultural differences such as an easily accessible health care system in Korea might explain the mild course of the pandemic influenza in pregnant Korean women. This is supported by the findings that two-thirds of pregnant women were admitted to hospital within 24 hours of the onset of symptoms, compared to a median 1.5 to 6 days of interval between symptoms and presentation in other countries [14,26,31,36]. In addition, other factors such as genetic susceptibility, family size, crowding [37], local immunity and regional differences in virus strain [38,39] could be probable factors to explain our results of milder cases.
This study has the following limitations. First, this study had a retrospective design. We did not collect certain data that were relevant to influenza infection and pregnancy such as obesity. In addition, data related to gestational age and birth weight was only available in 56.2% of total cases. Second, this study was only conducted at tertiary referral hospitals. This might not be a significant bias among pregnant women because tertiary hospitals in Korea are easily accessible, and pregnant women with fever tended to visit tertiary referral hospitals. However, for the control group of these young patients with influenza, tertiary referral hospital can be a bias. Considering this, the clinical outcome among pregnant women with influenza infection might be underestimated. However, the baseline characteristics including comorbidities were not significantly different between the two groups in this study. Third, this study did not distinguish between seasonal influenza vaccine and pandemic monovalent vaccine. However, considering that monovalent influenza A H1N1pdm09 vaccine was not available for use in pregnant women until December 21, and 80% (104/130) of the pregnant women in this study were admitted before this date, the effect of the pandemic vaccine was thought to be negligible. Therefore we cannot estimate vaccine effectiveness in this study, but we can use the result to understand the public interest by observing the overall increased vaccination rate.
In conclusion, compared to non-pregnant women, pregnant women with influenza A H1N1pdm09 infection in South Korea did not carry a significant risk of complications. However, the overall economic burden in pregnant women was estimated to be higher because of one death reported in the pregnant group. The clinical outcome of influenza infection among pregnant women might be influenced by gestational age, accessibility to medical care, the timing of antiviral treatment, and host factors. Although statistical significance was not shown in this study, influenza vaccination should be recommended to pregnant women as a high priority, considering the serious and detrimental impact of influenza-related complications on pregnancy.

KEY MESSAGE

1. The economic burden of the 2009 pandemic influenza was higher for pregnant women than for non-pregnant women.
2. Obstetric complications were observed in 9.2% of the pregnant women during the 2009 pandemic influenza.
3. This study supports the current Korean recommendation to administer inf luenza vaccine during pregnancy as a high priority.

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

Acknowledgments

This study was supported by a grant of the Korea Healthcare Technology R&D Project from the Ministry of Health and Welfare Republic of Korea (No. A103001).

Table 1.
Characteristics of pregnant (case) and non-pregnant women (age-matched controls) with confirmed pandemic influenza A H1N1pdm09 virus infection
Characteristic Pregnant women (n = 130) Non-pregnant women (n = 130) p value
Age, yr 31.1 ± 4.3 30.7 ± 4.7 0.43
 < 20 2 (1.5) 1 (0.8)
 20–29 41 (31.5) 48 (36.9)
 30–34 58 (44.6) 55 (42.3)
 35–49 29 (22.3) 26 (20)
 < 20 or ≥ 35 31 (23.8) 27 (20.8)
Gestational age, wk 18.4 ± 9.5 - -
 1st trimester (1–13 wk) 47 (36.1) - -
 2nd trimester (14–28 wk) 60 (46.2) - -
 3rd trimester (≥ 29 wk) 23 (17.7) - -
One or more comorbidity 5 (3.8) 10 (7.7) 0.18
 Diabetes 1 (0.8) 0 1.00
 Chronic cardiovascular disease 0 0 -
 Chronic cerebral disease 0 0 -
 Neuromuscular disease 0 1 (0.8) 1.00
 Chronic pulmonary disease 0 2 (1.5) 0.50
 Asthma 1 (0.8) 1 (0.8) 1.00
 Chronic renal disease 0 0 -
 Chronic hepatic disease 1 (0.8) 2 (1.5) 1.00
 Solid cancer 0 1 (0.8) 1.00
 Bone marrow/organ transplantation 0 0 -
 Autoimmune disease 0 2 (1.5) 0.50
 Immunosuppressant use 0 1 (0.8) 1.00
 Thyroid disease 2 (1.5) 2 (1.5) 1.00
 Smoking 0 0 -
 > 1 comorbidity 0 2 (1.5) 0.50
Influenza vaccinationa 31 (32.0) 30 (28.8) 0.63
Antiviral agent use 93 (71.5) 114 (87.7) < 0.01
 Oseltamivir 89 (68.5) 107 (82.3) 0.01
 Zanamivir 4 (3.1) 7 (5.4) 0.36
Interval between onset of illness and antiviral treatment, dayb 1.91 ± 2.1 1.49 ± 1.5 0.11
 2 Days or less 65 (75.6) 87 (79.1) 0.56
 5 Days or more 5 (5.8) 6 (5.5) 1.00
Interval between onset of illness and presentation, day 1.23 ± 1.6 1.07 ± 1.2 0.42
Interval between presentation and initiation of antiviral treatment, day 0.69 ± 1.3 0.44 ± 0.9 0.13

Values are presented as mean ± SD or number (%).

a Vaccination regardless of vaccination time before admission. Data were available for 201 cases (97 pregnant and 104 non-pregnant women).

b Data were available for 196 cases (86 pregnant and 110 non-pregnant women).

Table 2.
The Comparison of Influenza-related complications and economic burden between pregnant and non-pregnant women with pandemic influenza A H1N1pdm09 virus infection
Pregnant women (n = 130) Non-pregnant women (n = 130) p value
Overall complicationsa 2 (1.5) 4 (3.1) 0.648
Pneumonia 2 (1.5) 2 (1.5) 1.000
Emergency department visit 52 (40.0) 44 (33.8) 0.304
Hospitalization 13 (10.0) 5 (3.8) 0.051
Duration of hospitalization, day 7.3 (3–26) 12.8 (6–35) 0.230
Intensive care unit admission 1 (0.8) 0 1.000
Death 1 (0.8) 0 1.000
Medical cost per person, KRW 499,303.32 ± 2,446,141.91 264,531.98 ± 315,138.00 0.279
Overall economic burden per person, KRW 4,821,992.44 ± 5,0418,554.97 351,233.50 ± 522,308.03 0.313

Values are presented as number (%), mean (range), or mean ± SD.

KRW, Korean won.

a Pneumonia (n = 2) in pregnant women; pneumonia (n = 2), sinusitis (n = 1), elevated liver enzyme (n = 1) in non-pregnant women.

Table 3.
The pregnancy-related complications among pregnant women with pandemic influenza A H1N1pdm09 virus infection
Pregnant women (n = 130)
Gestational age at birth, wka 38.6 ± 1.50
 Preterm birth 7/73 (9.6)
Birth weight, kga 3.24 ± 0.44
 Low birth weight (< 2.5 kg) 3/73 (4.1)
Spontaneous miscarriage 1 (0.8)
Stillbirth 1 (0.8)
Fetal abnormalityb 1 (0.8)

Values are presented as mean ± SD or number (%).

a Only 73 cases (56.2% of total) was available regarding the gestational week and birth weight. One case showed both preterm labor and low-birth weight.

b Refers to cleft lip (n = 1).

REFERENCES

1. World Health Organization. Influenza (seasonal). Fact sheet no. 211 [Internet]. Geneva (CH): World Health Organization, 2009. [cited 2017 Sep 29]. Available from: http://www.who.int/mediacentre/factsheets/fs211/en.

2. Centers for Disease Control and Prevention. People at high risk of developing flu-related complications [Internet]. Atlanta (GA): Centers for Disease Control and Prevention, 2016. [cited 2017 Sep 29]. Available from: https://www.cdc.gov/flu/about/disease/high_risk.htm.

3. Louie JK, Acosta M, Jamieson DJ, Honein MA, California Pandemic (H1N1) Working Group. Severe 2009 H1N1 influenza in pregnant and postpartum women in California. N Engl J Med 2010;362:27–35.
crossref pmid
4. Jamieson DJ, Theiler RN, Rasmussen SA. Emerging infections and pregnancy. Emerg Infect Dis 2006;12:1638–1643.
crossref pmid pmc
5. McNeil SA, Dodds LA, Fell DB, et al. Effect of respiratory hospitalization during pregnancy on infant outcomes. Am J Obstet Gynecol 2011;204:S54–S57.
crossref pmid
6. Mendez-Figueroa H, Raker C, Anderson BL. Neonatal characteristics and outcomes of pregnancies complicated by influenza infection during the 2009 pandemic. Am J Obstet Gynecol 2011;204:S58–S63.
crossref pmid pmc
7. Harris JW. Influenza occurring in pregnant women: a statistical study of thirteen hundred and fifty cases. JAMA 1919;72:978–980.
crossref
8. Hardy JM, Azarowicz EN, Mannini A, Medearis DN Jr, Cooke RE. The effect of Asian influenza on the outcome of pregnancy, Baltimore, 1957-1958. Am J Public Health Nations Health 1961;51:1182–1188.
crossref pmid pmc
9. Goodnight WH, Soper DE. Pneumonia in pregnancy. Crit Care Med 2005;33:S390–S397.
crossref pmid
10. Hewagama S, Walker SP, Stuart RL, et al. 2009 H1N1 influenza A and pregnancy outcomes in Victoria, Australia. Clin Infect Dis 2010;50:686–690.
crossref pmid pdf
11. Jain S, Kamimoto L, Bramley AM, et al. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med 2009;361:1935–1944.
crossref pmid
12. Dubar G, Azria E, Tesniere A, et al. French experience of 2009 A/H1N1v influenza in pregnant women. PLoS One 2010;5:e13112.
crossref pmid pmc
13. Vaillant L, La Ruche G, Tarantola A, Barboza P, epidemic intelligence team at InVS. Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009. Euro Surveill 2009;14:19309.
crossref pmid
14. ANZIC Influenza Investigators and Australasian Maternity Outcomes Surveillance System. Critical illness due to 2009 A/H1N1 influenza in pregnant and postpartum women: population based cohort study. BMJ 2010;340:c1279.
crossref pmid pmc
15. Gerardin P, El Amrani R, Cyrille B, et al. Low clinical burden of 2009 pandemic influenza A (H1N1) infection during pregnancy on the island of La Reunion. PLoS One 2010;5:e10896.
crossref pmid pmc
16. Lim ML, Chong CY, Tee WS, Lim WY, Chee JJ. Influenza A/H1N1 (2009) infection in pregnancy: an Asian perspective. BJOG 2010;117:551–556.
crossref pmid
17. Yamada T, Yamada T, Morikawa M, et al. Pandemic (H1N1) 2009 in pregnant Japanese women in Hokkaido. J Obstet Gynaecol Res 2012;38:130–136.
crossref pmid
18. Yu H, Feng Z, Uyeki TM, et al. Risk factors for severe illness with 2009 pandemic influenza A (H1N1) virus infection in China. Clin Infect Dis 2011;52:457–465.
crossref pmid pmc pdf
19. Kim BN, Kwak YG, Moon CS, et al. Pandemic influenza (H1N1 2009) among pregnant Korean women. Infect Chemother 2011;43:55–59.
crossref
20. An JH, Kim HN, Choi OJ, et al. Was 2009 pandemic influenza A (H1N1) mild among pregnant Korean women? Chonnam Med J 2013;49:96–99.
crossref pmid pmc
21. Hur JA. A fatal case in pregnant woman infected by H1N1 2009 in Korea. Infect Chemother 2011;43:225–228.
crossref
22. Jung YH, Ko S. The socioeconomic cost of diseases in Korea. J Prev Med Public Health 2006;39:499–504.
crossref pmid
23. Ministry of Health and Welfare; Korea Institute for Health and Social Affairs. The Third Korea National Health and Nutrition Examination Survey (KNHANES III), 2005. Gwacheon: Ministry of Health and Welfare, 2006.

24. Korean Statistical Information Service (KOSIS). Statistical annual report (2009/2010) [Internet]. Daejeon (KR): Statistics Korea, 2013. [cited 2017 Sep 29]. Available from: http://www.kosis.kr.

25. No I, Suh M, Kim Y. Socioeconomic costs of alcohol and policy issues. Seoul: Korea Institute for Health and Social Affairs, 1997;80–82.

26. Creanga AA, Johnson TF, Graitcer SB, et al. Severity of 2009 pandemic influenza A (H1N1) virus infection in pregnant women. Obstet Gynecol 2010;115:717–726.
crossref pmid
27. Siston AM, Rasmussen SA, Honein MA, et al. Pandemic 2009 influenza A(H1N1) virus illness among pregnant women in the United States. JAMA 2010;303:1517–1525.
crossref pmid pmc
28. Beck S, Wojdyla D, Say L, et al. The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ 2010;88:31–38.
crossref pmid pmc
29. Korea Statistical Information Service (KOSIS). Birth statistics for Korea [Internet]. Daejeon (KR): Statistics Korea, 2013. [cited 2014 Aug 26]. Available from: http://kostat.go.kr/portal/korea/kor_nw/2/1/index.board?bmode=read&aSeq=329402.

30. Lee CW, Hwang SM, Lee YS, Kim MA, Seo K. Prevalence of orofacial clefts in Korean live births. Obstet Gynecol Sci 2015;58:196–202.
crossref pmid pmc
31. Jamieson DJ, Honein MA, Rasmussen SA, et al. H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 2009;374:451–458.
crossref pmid
32. Freeman DW, Barno A. Deaths from Asian influenza associated with pregnancy. Am J Obstet Gynecol 1959;78:1172–1175.
crossref pmid
33. Neuzil KM, Reed GW, Mitchel EF, Simonsen L, Griffin MR. Impact of influenza on acute cardiopulmonary hospitalizations in pregnant women. Am J Epidemiol 1998;148:1094–1102.
crossref pmid pdf
34. Kim MJ, Lee SY, Lee KS, et al. Influenza vaccine coverage rate and related factors on pregnant women. Infect Chemother 2009;41:349–354.
crossref
35. Organisation for Economic Co-operation and Development (OECD). OECD obesity update 2012 [Internet]. Paris: OECD, 2012. [cited 2017 Sep 29]. Available from: http://www.oecd.org/health/49716427.pdf.

36. Rolland-Harris E, Vachon J, Kropp R, et al. Hospitalization of pregnant women with pandemic A(H1N1) 2009 influenza in Canada. Epidemiol Infect 2012;140:1316–1327.
crossref pmid
37. La Ruche G, Tarantola A, Barboza P, et al. The 2009 pandemic H1N1 influenza and indigenous populations of the Americas and the Pacific. Euro Surveill 2009;14:19366.
crossref pmid
38. Miller MA, Viboud C, Balinska M, Simonsen L. The signature features of influenza pandemics: implications for policy. N Engl J Med 2009;360:2595–2598.
crossref pmid
39. Simonsen L, Spreeuwenberg P, Lustig R, et al. Global mortality estimates for the 2009 influenza pandemic from the GLaMOR project: a modeling study. PLoS Med 2013;10:e1001558.
crossref pmid pmc
TOOLS
METRICS Graph View
  • 3 Web of Science
  • 3 Crossref
  • 3 Scopus
  • 7,631 View
  • 215 Download
Related articles

Editorial Office
101-2501, Lotte Castle President, 109 Mapo-daero, Mapo-gu, Seoul 04146, Korea
Tel: +82-2-2271-6792    Fax: +82-2-790-0993    E-mail: kaim@kams.or.kr                

Copyright © 2024 by Korean Association of Internal Medicine.

Close layer
prev next