ABSTRACT
Pregnant women and infants are at relatively high risk for influenza- and pertussis-related morbidity and mortality. Vaccination is the most important prevention strategy for both diseases. We evaluated knowledge and acceptance of influenza and pertussis vaccinations among pregnant women. We performed a cross-sectional survey of 465 pregnant women receiving prenatal care at the obstetric outpatient clinic in a tertiary medical center in Turkey between November 2015 and May 2016. We used a questionnaire investigating the knowledge of pertussis and influenza to evaluate potential influences on the acceptance or rejection of pertussis or influenza vaccinations. The acceptance rates of pertussis and influenza vaccinations were 11.2% and 19.8%, respectively. Maternal age, education level, employment status, number of gestations, and gestational age did not affect the rate of acceptance of these vaccinations. On the other hand, pregnant women who had a history of vaccination during their adolescence and in previous pregnancies were significantly more likely to accept pertussis vaccination. Knowledge about the risks of pertussis and influenza diseases for pregnant women and their children has a significant effect on vaccination acceptance. Even in low socioeconomic status groups, a recommendation for vaccinations by the primary obstetrician was significantly predictive of acceptance of both pertussis and influenza vaccination. This study revealed that the acceptance rates of pertussis and influenza vaccination among pregnant women are very low in Turkey. Healthcare worker recommendations and increased awareness about pertussis and influenza morbidity and mortality in pregnant women and infants are essential to improve the rates of vaccination acceptance during pregnancy.
Introduction
Respiratory infections such as influenza and pertussis can cause severe complications, hospitalization,and even death for pregnant women and their infants. For pregnant women, this is believed to be mostly due to pregnancy-related immunosuppression that results in susceptibility and a decreased immune response to infection. Children under six months old have an immature immune system, resulting in decreased responses to viral and bacterial infections.Citation1–Citation4 Vaccinating pregnant women is one of the most effective measures to protect both pregnant women and their infants from these infections and their complications.Citation5,Citation6 Previous studies have shown that antenatal vaccination protects not only mothers but also their infants, who are too young for vaccination, from these diseases through the placental maternal-fetal transfer of antibodies.Citation7–Citation9
The Centers for Disease Control and Prevention (CDC) and the American College of Obstetricians and Gynecologists (ACOG) recommend antenatal influenza vaccination at any gestational age to protect both mothers and their babies. Research has shown that influenza vaccination is relatively safe during pregnancy and effective at reducing adverse maternal, fetal, and neonatal outcomes.Citation10,Citation11 Since 2013, the Advisory Committee on Immunization Practices (ACIP) and the CDC have recommended antenatal Tdap (tetanus, diphtheria, and acellular pertussis) vaccination during each pregnancy regardless of previous vaccination status.Citation12 Turkey does not include influenza and pertussis vaccinations in the national vaccination schedule for pregnant women. In Turkey, a few studies have been conducted to investigate the vaccination status of pregnant women and their children and the factors that affect this status.Citation13–Citation15 Despite these studies, there is little information available about pregnant women’s awareness and acceptance of influenza and pertussis vaccinations in Turkey.
This study aimed to determine the level of knowledge and acceptance of influenza and pertussis vaccinations among pregnant women receiving prenatal care at a large metropolitan hospital in Istanbul, with the goal that better policies could be developed to improve vaccination acceptance during pregnancy by investigating the factors that affect acceptance.
Materials and methods
We performed a cross-sectional observational study using a 45-item questionnaire to evaluate participants’ knowledge of pertussis and influenza as well as the potential influencing factors regarding the acceptance or rejection of pertussis and influenza vaccinations. The participants for the study comprised pregnant women who were receiving routine prenatal care at an obstetric outpatient clinic in a tertiary medical center in Turkey between November 2015 and May 2016. Before starting the study, the questionnaire was piloted to 50 pregnant women at the same hospital. The study participants were randomly selected from the pool of those who completed the survey at the obstetric outpatient clinic. Signed informed consent was obtained from all participants. Each participant’s name and signature were recorded on the informed consent form. The survey was developed from the current literature by the research team, and each survey was conducted face-to-face with all of the participants.
The survey contained questions on demographics, knowledge, attitudes, and beliefs regarding pertussis and influenza as well as pertussis and influenza vaccinations. The primary outcome of the survey was to determine whether pregnant women would accept influenza and pertussis vaccinations if offered. The demographic questions included in the survey comprised questions about age, marital status, education level, gestational age, number of gestations, and number of children. We also asked the participants whether they had researched prenatal care during their current pregnancy; when they first attended prenatal care; where they received prenatal care; if (and why) they had any complications or needed hospitalization; and who in their family made their healthcare decisions. In terms of vaccinations, we asked whether or not vaccinations had been recommended to them; whether they planned to get any vaccinations in their current pregnancy; who/what had recommended tetanus, pertussis, and influenza vaccinations; what type of vaccines had been administered to them and when; and whether any post-vaccination complications had occurred. We also asked about their history of vaccinations during adolescence and previous pregnancies; how they perceived those who had recommended vaccines to them; and their reasons for accepting or rejecting pertussis and influenza vaccinations. In terms of knowledge, we asked whether they had heard about pertussis before; whether they believed that pregnant women and their babies are at risk of contracting pertussis and/or influenza; and whether pertussis and influenza vaccinations are safe and protective for pregnant women and their babies.
Statistical analyses
Data were entered into Microsoft Office Excel 2010 (Microsoft, Redmond, WA, USA). Statistical analysis was performed using SPSS version 22.0 (IBM, SPSS). Normally distributed data were assessed using means and the Student’s t test. The significance of nonparametric data was assessed using the Mann–Whitney U test. The statistical significance of dichotomous outcomes was determined using the chi-square test, Fisher’s exact test, the Fisher–Freeman–Halton test, and Yates’s continuity correction. A multivariate logistic regression analysis was performed. A value of p < .05 was considered statistically significant. The Ethics Committee at Marmara University School of Medicine approved this study.
Results
Demographic and clinical characteristics
A total of 465 pregnant women participated in the survey. Among these participants, 52 (11.2%) accepted pertussis vaccinations and 92 (19.8%) accepted influenza vaccinations during pregnancy if offered. The mean age of the participants was 27.8 years (age range: 17–42 years). More than half of the women were housewives (77.6%). Almost all participants were married (98.9%). The majority of participants (63.9) had high-school education only, and just 8.8% of participants had university-level education. At the time of the survey, 65% of the women were in their second trimester and 24% in their third trimester. Only 64 (14%) participants reported seeking antenatal care during their current pregnancy. In total, 24% of participants reported having general health problems during their pregnancy. Participants who were seeking antenatal care during pregnancy were significantly more likely to accept influenza vaccinations (p = .014). No other demographic or clinical characterics had a significant effect on the acceptance of influenza and pertussis vaccinations ( and ).
Table 1. Demographic and clinical characteristics of pregnant women by intention to accept pertussis vaccination
Table 2. Demographic and clinical characteristics of pregnant women by intention to accept influenza vaccination
Influenza and pertussis knowledge, vaccine recommendations, administration history, and vaccination acceptance
Participants who had a history of pertussis vaccinations during their adolescence or previous pregnancies were significantly more likely to accept a pertussis vaccination (p = .01 and p = .013, respectively) (). However, a history of influenza vaccinations during childhood, adolescence, or prior pregnancy did not affect influenza vaccination acceptance during pregnancy. In terms of the vaccines administered during prior pregnancies, 171 (37%) participants received a tetanus vaccine, and just one received a tetanus and influenza vaccine. Just 24 (5%) participants had heard of pertussis. Those who had heard of pertussis and influenza and believed maternal vaccines to be safe were significantly more likely to accept pertussis and influenza vaccinations. Those who agreed that they and their babies were at risk of contracting pertussis and influenza and that their babies would be protected by their vaccination were also significantly more likely to accept pertussis and influenza vaccinations. However, no significant association was found between a history of influenza vaccinations during adolescence or previous pregnancies and influenza vaccination acceptance. Participants who understood that pertussis vaccinations during pregnancy can prevent infant infection had a high rate of pertussis vaccinations. As expected, those who were either planning to get vaccinated during pregnancy or agreed that pregnant women should be vaccinated against pertussis were significantly more likely to accept pertussis vaccinations (p = .039 and p = .000, respectively) ( and ).
Table 3. Vaccination history, pertussis disease knowledge, vaccine recommendation by intention to accept pertussis vaccination
Table 4. Vaccination history, influenza disease knowledge, vaccine recommendation by intention to accept influenza vaccination
Reasons to accept pertussis and influenza vaccinations
Among the reasons for the participants accepting pertussis vaccinations were due to the recommendations of a doctor (obstetrician or pediatrician), healthcare worker, Turkish Ministry of Health worker, or international organization worker. These recommendations were significantly associated with pertussis vaccination acceptance. However, only the recommendation of an obstetrician was significantly associated with influenza vaccination acceptance. No other factors led to influenza and pertussis vaccination acceptance ( and ).
Table 5. Reasons to accept pertussis vaccination during pregnancy
Table 6. Reasons to accept influenza vaccination during pregnancy
Multivariate analysis for pertussis and influenza vaccination acceptance
In the multivariate analysis, we detected independent associations between pertussis vaccination acceptance and a history of pertussis vaccination during adolescence (OR = 7,395; 95% CI: 1,635–33,453), a history of pertussis vaccination during previous pregnancies (OR = 3,147; 95% CI: 1,107–8,946), and unvaccinated women identified as most likely to get pertussis (OR = 6,425; 95% CI: 1,668–24,739).
We also detected significant associations between influenza vaccination acceptance and knowledge among participants that getting vaccinations when pregnant can protect their babies from disease (OR = 3,265; 95% CI: 1,393–7,657).
No the other variables demonstrated a significant effect on vaccination acceptance rates in the multivariate analysis ( and ).
Table 7. Multivariate logistic regression analyses examining factors affecting pertussis vaccination acceptance
Table 8. Multivariate logistic regression analyses examining factors affecting influenza vaccination acceptance
Discussion
In this study, acceptance rates of pertussis and influenza vaccines were 11.2% and 19.8%, respectively. This outcome suggests that vaccinations during pregnancy pose a particular challenge. Despite the importance of maternal immunization against pertussis and influenza in both pregnant women and their babies, vaccine acceptance rates are low, even in developed countries.Citation16–Citation19 In a cross-sectional survey of 402 pregnant women, Varan et al. reported that 57% of participants accepted pertussis vaccination if offered.Citation17 In another study, D’Alessandro et al. reported that none of the participants accepted the Tdap vaccination and that just 1.4% of participants accepted the influenza vaccination during pregnancy.Citation18 In a cross-sectional survey of 198 pregnant Turkish women, Celikel et al. demonstrated that only 3% of pregnant women received a seasonal influenza vaccination.Citation13 Similar to these studies, we found the rates of pertussis and influenza vaccination acceptance among pregnant women to be very low. It is necessary to determine the reasons for these low vaccination rates so that better strategies can be developed to improve vaccination acceptance during pregnancy.
Numerous studies in the extant literature have evaluated the factors associated with vaccination acceptance during pregnancy. A recent study by Ben Natan et al. conducted on pregnant Israeli women reported that native-born women were more likely to express an intention to be vaccinated.Citation20 In a cross-sectional observational study of pregnant women, Khan et al. showed that pregnant women with more than three children were significantly less likely to accept influenza vaccinations.Citation21 In another study, Hu et al. reported that the demographic characteristics were significantly different between pregnant women who accepted and did not accept the influenza vaccination.Citation22 We found that no demographic or clinical factors had a significant effect on influenza and pertussis vaccination acceptance. This may be explained by the fact that our sample mostly consisted of housewives of low socioeconomic status.
In this study, only 24 (5%) participants had heard of pertussis and only 26 (5.5%) knew that babies can contact pertussis. Thus, knowledge and awareness of pertussis was very low in our study population. We found that if pregnant women had knowledge of pertussis and knowledge of the risk it poses to babies, they were more likely to accept pertussis vaccinations during pregnancy. Moreover, knowledge about the safety and protection that the pertussis vaccine offers babies was shown to have a positive influence on pertussis vaccination acceptance during pregnancy. However, the acceptance of the influenza vaccination during pregnancy was mainly affected by knowledge about the disease itself, the safety of the vaccine, and protection for the baby. Our findings suggest that increased awareness and knowledge of these diseases can improve pertussis and influenza vaccination acceptance during pregnancy. Prior studies have also demonstrated the association between awareness of the diseases and vaccine acceptance.Citation17,Citation23–Citation26 In a convenience survey of pregnant women, Healy et al. reported that the most important factors associated with vaccination acceptance were safety for the baby and mother, sufficient information, and adequate vaccine education, with mean scores of 4.7, 4.5, and 4.2, respectively, on a 5-point scale.Citation23 In another study, Pathirana et al. showed that increased knowledge in patients is one of the most important factors affecting vaccination acceptance during pregnancy.Citation24 McCarty et al. also reported extremely low awareness of the benefits of influenza vaccinations during pregnancy.Citation25
Our study determined different factors that influence both pertussis and influenza vaccination acceptance during pregnancy. We showed that influenza and pertussis vaccination acceptance is higher if the vaccination is recommended by the pregnant woman’s primary obstetrician. Consistent with previous studies, this study demonstrated the important role that healthcare workers can play in improving vaccination acceptance during pregnancy.Citation23,Citation27,Citation28 A recent study by Strassberg et al. reported that the recommendations of healthcare workers, in combination with educational materials, have a significant effect on both Tdap and influenza vaccination acceptance.Citation27 In another recent study, Arriola et al. showed that pregnant women who were recommended vaccinations by their healthcare workers were significantly more likely to accept influenza vaccinations.Citation28 The findings from these studies show that education, when coupled with vaccine recommendations made by healthcare workers, could improve the rate of vaccination coverage during pregnancy. Previous studies reported that pregnant women’s safety and efficacy concerns were the most common reasons for vaccination rejection.Citation17,Citation21,Citation29 Educational programs might improve vaccination acceptance during pregnancy by emphasizing vaccine safety and efficacy.Citation29,Citation30 Previous studies conducted on different demographic groups have shown that the recommendations of healthcare workers are positively associated with vaccination acceptance.Citation31–Citation34
This study has several limitations. First, the study was conducted in one medical center rather than in multiple centers, meaning that generalizing the study’s findings to Turkey’s wider population should be done with caution. Second, the results were based on self-reported information about the knowledge and acceptance of vaccinations. The participants’ medical and immunization records were unavailable. Third, the majority of the participants were housewives of low socioeconomic status. Thus, the findings may not be applicable to all pregnant women.
To conclude, our findings highlight the important role that healthcare workers can play, in conjunction with increased knowledge about pertussis and influenza, in improving vaccination acceptance during pregnancy. Efforts to educate pregnant women and healthcare workers may improve pertussis and influenza vaccination acceptance during pregnancy.
Disclosure of potential conflicts of interest
No potential conflicts of interest were disclosed.
References
- Centers for Disease Control and Prevention. Epidemiology and prevention of vaccine-preventable diseases. 13thed. Washington (DC.): Public Health Foundation; 2015.
- Mor G, Cardenas I. The immune system in pregnancy: a unique complexity. Am J Reprod Immunol. 2010;63:425–33. doi:10.1111/(ISSN)1600-0897.
- Henninger M, Naleway A, Crane B, Donahue J, Irving S. Predictors of seasonal influenza vaccination during pregnancy. Obstet Gynecol. 2013;121:741–49. doi:10.1097/AOG.0b013e3182878a5a.
- Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, Sugerman DE, Druckenmiller JK, Ritger KA, Chugh R, et al. Hospitalized patients with 2009 H1N1 influenza in the united states, April–june 2009. N Engl J Med. 2009;361:1935–44. doi:10.1056/NEJMoa0906695.
- Lindsey B, Kampmann B, Jones C. Maternal immunization as a strategy to decrease susceptibility to infection in newborn infants. Curr Opin Infect Dis. 2013;26:248–53. doi:10.1097/QCO.0b013e3283607a58.
- Centers for Disease Control and Prevention. Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices—united states, 2013–2014. MMWR. 2013;62(RR07):1–43.
- Thompson MG, Li DK, Shifflett P, Sokolow LZ, Ferber JR, Kurosky S, Bozeman S, Reynolds SB, Odouli R, Henninger ML, et al. Effectiveness of seasonal trivalent influenza vaccine for preventing influenza virüs illness among pregnant women: apopulation-based case-control study during the 2010–2011 and 2011–2012 influenza seasons. Clin Infect Dis. 2014;58:449–57. doi:10.1093/cid/cit750.
- Poehling KA, Szilagyi PG, Staat MA, Snively BM, Payne DC, Bridges CB, Chu SY, Light LS, Prill MM, Finelli L, et al. Impact of maternal immunization on influenza hospitalizations in infants. Am J Obstet Gynecol. 2011;204:141–48.
- Healy CM, Rench MA, Baker CJ. Importance of timing of maternal combined tetanus, diphtheria, and acellular pertussis (Tdap) immunization and protection of young infants. Clin Infect Dis. 2013;56:539–44. doi:10.1093/cid/cis923.
- Kharbanda EO, Vazquez-Benitez G, Lipkind H, Naleway A, Lee G. Nordin JD Inactivated influenza vaccine during pregnancy and risks for adverse obstetric events. Obstet Gynecol. 2013;122:659–67. doi:10.1097/AOG.0b013e3182a1118a.
- Fell DB, Platt RW, Lanes A, Wilson K, Kaufman JS, Basso O, Buckeridge D. Fetal death and preterm birth associated with maternal influenza vaccination: systematic review. Int J Obst Gynaecol. 2015;122:17–26. doi:10.1111/1471-0528.12977.
- Centers for Disease Control and Prevention (CDC). Updated recommendations for use of tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis vaccine (Tdap) in pregnant women—advisory Committee on Immunization Practices (ACIP), 2012. MMWR Morb Mortal Wkly Rep 2013;62:131–35.
- Celikel A, Ustunsoz A, Guvenc G. Determination of vaccination status of pregnant women during pregnancy and the affecting factors. J Clin Nurs. 2014;23:2142–50. doi:10.1111/jocn.2014.23.issue-15pt16.
- Gündüz S, Yüksel NC, Aktoprak HB, Canbal M, Kaya M. Attitudes towards influenza vaccination in high socioeconomic status Turkish parents. Turk J Med Sci. 2014;44:649–55. doi:10.3906/sag-1305-43.
- Oguz MM, Camurdan AD, Aksakal FN, Altinel Acoglu E. Social contact patterns of infants in deciding vaccination strategy: a prospective, cross-sectional, single-centre study. Epidemiol Infect. 2018;146:1157–66. doi:10.1017/S0950268818001048.
- Healy CM, Rench MA, Castagnini LA, Baker CJ. Pertussis immunization in a high- risk postpartum population. Vaccine. 2009;27:5599–602. doi:10.1016/j.vaccine.2009.07.030.
- Varan AK, Esteves-Jaramillo A, Richardson V, Esparza-Aguilar M, Cervantes-Powell P, Omer SB. Intention to accept Bordetella pertussis booster vaccine during pregnancy in Mexico City. Vaccine. 2014;32:785–92. doi:10.1016/j.vaccine.2013.12.054.
- D’Alessandro A, Napolitano F, D’Ambrosio A, Angelillo IF. Vaccination knowledge and acceptability among pregnant women in Italy. Hum Vaccin Immunother. 2018;14:1573–79. doi:10.1080/21645515.2018.1483809.
- O’Grady KA, Dunbar M, Medlin LG, Hall KK, Toombs M, Meiklejohn J, McHugh L, Massey PD, Creighton A, Andrews RM. Uptake of influenza vaccination in pregnancy amongst Australian aboriginal and torres strait Islander women: a mixed-methods pilot study. BMC Res Notes. 2015;8:169. doi:10.1186/s13104-015-1147-3.
- Ben Natan M, El Kravchenko B, Sakashidlo K, Mor S. What drives pregnant women’s decisions to accept the pertussis vaccine? Appl Nurs Res. 2017;38:60–63. doi:10.1016/j.apnr.2017.09.013.
- Khan AA, Varan AK, Esteves-Jaramillo A, Siddiqui M, Sultana S, Ali AS, Zaidi AKM, Omer SB. Influenza vaccine acceptance among pregnant women in urban slum areas, Karachi, Pakistan. Vaccine. 2015;33:5103–09. doi:10.1016/j.vaccine.2015.08.014.
- Hu Y, Wang Y, Liang H, Chen Y. Seasonal influenza vaccine acceptance among pregnant women in Zhejiang Province, China: evidence based on health belief model. Int J Environ Res Public Health. 2017;14:E1551. doi:10.3390/ijerph14121551.
- Healy CM, Rench MA, Montesinos DP, Ng N, Swaim LS. Knowledge and attitiudes of pregnant women and their providers towards recommendations for immunization during pregnancy. Vaccine. 2015;33:5445–545. doi:10.1016/j.vaccine.2015.08.028.
- Pathirana J, Nkambule J, Black S. Determinants of maternal immunization in developing countries. Vaccine. 2015;33:2971–77. doi:10.1016/j.vaccine.2015.04.070.
- McCarthy EA, Pollock WE, Tapper L, Sommerville M, McDonald S. Increasing uptake of influenza vaccine by pregnant women post H1N1 pandemic: a longitudinal study in Melbourne, Australia, 2010 to 2014. BMC Pregnancy Childbirth. 2015;15:53. doi:10.1186/s12884-015-0486-3.
- Ko HS, Jo YS, Kim YH, Park YG, Wie JH, Cheon J, Moon HB, Lee Y, Shin JC. Knowledge and acceptability about adult pertussis immunization in Korean Women of childbearing age. Yonsei Med J. 2015;56:1071–78. doi:10.3349/ymj.2015.56.4.1071.
- Strassberg ER, Power M, Schulkin J, Stark LM, Mackeen AD, Murtough KL, Paglia MJ Patient attitudes toward influenza and tetanus, diphtheria and acellular pertussis vaccination in pregnancy. Vaccine. 2018;36:4548–54. doi:10.1016/j.vaccine.2018.05.121.
- Arriola CS, Vasconez N, Bresee J. Ministry of civic power for health of Nicaragua, Ropero AM. Knowledge, attitudes and practices about influenza vaccination among pregnant women and healthcare providers serving pregnant women in Managua, Nicaragua. Vaccine. 2018;36:3686–93. doi:10.1016/j.vaccine.2018.05.013.
- Napolitano F, Napolitano P, Angelillo IF. Seasonal influenza vaccination in pregnant women: knowledge, attitudes, and behaviors in Italy. BMC Infect Dis. 2017;17:48. doi:10.1186/s12879-016-2138-2.
- Stark LM, Power ML, Turrentine M, Samelson R, Siddiqui MM, Paglia MJ, Strassberg ER, Kelly E, Murtough KL, Schulkin J, et al. Influenza vaccination among pregnant women: patient beliefs and medical provider practices. Infect Dis Obstet Gynecol. 2016;2016:3281975. doi:10.1155/2016/3281975.
- Maertens K, Cabore RN, Huygen K, Hens N, Van Damme P, Leuridan E. Pertussis vaccination during pregnancy in Belgium: results of a prospective controlled cohort study. Vaccine. 2016;3:142–50. doi:10.1016/j.vaccine.2015.10.100.
- Napolitano F, Napolitano P, Liguori G, Angelillo IF. Human papillomavirus infection and vaccination: knowledge and attitudes among young males in Italy. Hum Vaccin Immunother. 2016;12:1504–10. doi:10.1080/21645515.2016.1156271.
- Vezzosi L, Santagati G, Angelillo IF. Knowledge, attitudes, and behaviors of parents towards varicella and its vaccination. BMC Infect Dis. 2017;17:172. doi:10.1186/s12879-017-2247-6.
- Krishnaswamy S, Cheng AC, Wallace EM, Buttery J, Giles ML. Understanding the barriers to uptake of antenatal vaccination by women from culturally and linguistically diverse backgrounds: a cross-sectional study. Hum Vaccin Immunother. 2018;14(7):1591–1598.