Influenza and pertussis are the most poorly controlled vaccine-preventable diseases in the United States, with infants among the highest risk groups for these diseases.1,2 “Cocooning,” meaning vaccinating close contacts against these 2 diseases, is a strategy that is advocated for protection of these young infants from both the diseases.3,4 Ideally, cocooning strategies would provide vaccination to all the close contacts of the infant.
Influenza causes high morbidity and mortality among both pregnant women and young infants.1 Influenza vaccination of pregnant women has been shown to reduce respiratory illness among pregnant women, preterm birth, small-for-gestational-age birth, and respiratory illness and hospitalization among infants younger than 6 months.5–11 Despite these benefits, vaccination coverage among pregnant women has been very low (24% for 2007–2008 and 11% for 2008–2009).1 Vaccination coverage during and after the pandemic 2009–2010 season improved,12 but the most recent vaccination coverage of 50.5%13 remains far below the Healthy People 2020 goal of 80%.14 While maternal vaccination offers clear benefit to the infant, efforts to vaccinate other close contacts remain important, as infants remain at risk of severe influenza illness even if their mother has been vaccinated.
Pertussis has the highest incidence and is most severe in infants younger than 1 year. Most deaths occur in infants younger than 4 months,2 before they may have established immunity from childhood diphtheria-tetanus-acellular pertussis vaccines. Pertussis incidence and deaths have significantly increased in recent years, with incidence levels approaching the prevaccine era, with 41,880 cases and 14 deaths in infants younger than 1 year in 2012.15 Before 2011, the primary strategy recommended by the Centers for Disease Control and Prevention for protecting young infants from pertussis was cocooning,4,16 which has been shown to provide protection against infant pertussis cases.17 While vaccinating postpartum mothers has been moderately successful, vaccinating fathers or other close contacts18 remains a significant challenge, and in a significant proportion of cases of infant pertussis, close contacts other than the mother were the likely source of infection.19 Given this and other factors,20–23 the recommendation for pregnant women has evolved such that now the Advisory Committee on Immunization Practices recommends tetanus-diphtheria-acellular pertussis (Tdap) vaccine in every pregnancy between 27 and 36 weeks, regardless of prior immunization history,15 in order to offer the newborn some level of immunity.15 Nonetheless, because of the ongoing pertussis epidemic, efforts to cocoon infants remain a priority.
We undertook this study to better understand how certain factors affect the receipt of Tdap and influenza vaccines among pregnant women as well as the other close contacts of their newborn. Therefore, the objectives of this study were to describe the following among women who had recently given birth: (1) receipt of influenza and Tdap vaccines by themselves and close contacts of their newborn infant (ie, cocooning); (2) attitudes regarding vaccination; (3) experiences related to provider recommendations for these vaccines during pregnancy; (4) the association between maternal vaccination and vaccination of the infant’s close contacts and (5) factors associated with influenza and Tdap cocooning.
MATERIALS AND METHODS
From February 2013 to April 2013, an e-mail survey was administered to the 613 eligible women identified. All study participants were patients at 1 of the 9 obstetrics and gynecology (OB/GYN) practices (6 urban and 3 rural) in Colorado. Women were eligible for the study if they had agreed to be contacted for a follow-up survey after completing a previous paper-based survey (on a different topic), had provided a working e-mail address and had an estimated date of delivery before December 15, 2012. The recommendation for Tdap vaccine at the time of this study was for all women to receive Tdap vaccine during pregnancy at >20 weeks if they had not previously received Tdap vaccine. This study was approved by the Colorado Multi-Institutional Review Board.
Questions assessed vaccination status for Tdap and influenza vaccines for the respondents themselves and their infants’ close contacts, including their relationship to the newborn and influenza and Tdap vaccination history. The next portion of the survey was based on the Health Belief Model (HBM), which has been used previously to predict vaccination behavior among pregnant women.24–26 After reading a brief description of influenza and pertussis infections and vaccines, 4-point Likert scales were used to assess the 5 domains of the HBM including the following: perceived benefits of vaccination, perceived barriers to vaccination, perceived susceptibility to influenza or pertussis, severity of these infections and social norms. Other questions queried the types of clinical settings where vaccines had been received, whether the mother had been given instructions to receive either vaccine for themselves or the infant’s close contacts, and if so, which staff had provided it. Demographic characteristics collected included age, education, race/ethnicity, household income, insurance type and child’s birth date. The full survey is available upon request.
The survey was administered through e-mail in English using Research Electronic Data Capture.27 Before sending the mails, e-mail addresses were tested for validity using the e-mail validation service Email-Checker.com. Dillman methodology of survey administration (2009) was followed and was modified to accommodate exclusively online administration.28 We sent an introductory e-mail signed by office managers or physicians in the patients’ OB/GYN practices informing the patient that a survey would be taken, followed by the survey link and an introductory letter 7 days later. Up to 7 e-mails were sent as well as 1 reminder phone call was made for those nonrespondents who had provided a working phone number. A $5 gift card was sent electronically upon completion of the survey.
Descriptive statistics were generated for all survey questions. The primary outcomes assessed were maternal reports of cocooning the infant with Tdap and influenza vaccination, defining cocooning as the mother’s self-report that she and at least 1 other “close contact” of the infant had received vaccination. Internal reliability for HBM domains was measured by Cronbach alpha, with value ≥0.6 defined as acceptable. Scale measures used in the analyses were calculated by averaging the score across all statements related to the measure (range of possible values = 0–3). Separate analyses were done for each vaccine. The association between cocooning and each HBM item, domain with good internal reliability and demographic variable was assessed using Wilcoxon rank sum, χ2, Mantel–Haenszel χ2 or Fisher exact tests as appropriate. Items that were found to be possibly significantly associated (P ≤0.1) with the main study outcomes in bivariate analyses were simultaneously entered in a multivariable model. All analyses were performed in SAS 9.4 (Cary, NC).
The response rate was 45% (274 of 613). Differences between respondents and nonrespondents were assessed using limited data available from the previous paper survey. Available data showed that survey respondents were slightly older than nonrespondents (30.7 years vs. 29.4 years, P = 0.005), were more likely to report having a primary care provider besides their OB/GYN (57% vs. 46%, P = 0.006) and were more likely to have reported receiving influenza immunization in the prior season (52% vs. 38%, P < 0.001) and Tdap vaccination since 2005 (31% vs. 15%, P < 0.001). The characteristics of respondents are shown in Table (Supplemental Digital Content 1, http://links.lww.com/INF/C233). The study population was predominantly White (82%), highly educated (67% college graduates or with advanced degree) and privately insured (81%). The mean number of close contacts per newborn was 5.1 (standard deviation, 3.0).
Sixty-seven percent of respondents reported that they had received both influenza and Tdap vaccines during the specified time frames. Seventy-four percent of mothers reported having received influenza vaccine during the current influenza season. Of these, 2% reported receipt before pregnancy, 46% while pregnant and 52% after delivery. Sites of receipt of influenza vaccine included their OB/GYN provider’s office (40%), another medical provider’s office (21%), hospital after delivery (10%), retail pharmacy/grocery (8%), public health department (2%) or other (19%, most responses listed as “work”). Eighty-six percent of mothers reported that they had received a Tdap vaccine since 2005. Of these, 35% reported receipt before the recent pregnancy, 14% during the recent pregnancy and 52% sometime after delivery. Sites of receipt of Tdap vaccine included a hospital after delivery (46%), another medical provider’s office (25%), their OB/GYN provider’s office (16%), a public health department (4%), a retail pharmacy/grocery (1%) and other (8%).
Over one-half of respondents strongly agreed that they worried that either they or someone else would infect their baby with influenza or pertussis (Table 1). Over three-fourth of respondents strongly agreed that it would be really bad if their baby got influenza or pertussis. More respondents strongly agreed that Tdap vaccine is a good way to protect the health of newborn babies (73%) than those who strongly agreed with the same statement about influenza vaccine (59%, P < 0.0001). The most commonly reported barrier was regarding the safety of influenza vaccine, with 13% strongly agreeing and 33% somewhat agreeing that they worry about its safety. A similar but slightly lower proportion of women reported concerns about the safety of Tdap vaccine and vaccines in general. Three percent of respondents strongly agreed and 19% somewhat agreed that it is dangerous for pregnant women to get vaccines. More than half of the respondents strongly agreed with all of the social norms statements.
Seventy-one percent of respondents reported having received a recommendation for influenza vaccine from their obstetrician, and 64% reported the same about Tdap vaccine. Fifty-two percent and 51% reported receiving a recommendation from their obstetrician that close contacts of their newborn infant receive influenza and Tdap vaccine, respectively. Smaller percentages reported having received similar recommendations from other staff members in the OB/GYN office (Fig. 1).
Sixty-one percent of mothers reported that they and at least 1 close contact of their newborn had received influenza vaccine, and 67% reported this for Tdap. Infants whose mothers reported receipt of influenza vaccine for themselves had a mean of 2.8 close contacts (median = 3) who also received influenza vaccine when compared with 0.9 (median = 0) contacts for mothers who did not receive influenza vaccine (P < 0.0001). The difference was also striking for Tdap, with infants whose mothers reported Tdap receipt having on an average of 2.4 contacts (median = 2) who also received it versus 0.8 (median = 0) for infants whose mothers did not report Tdap receipt (P < 0.0001). Twenty-five percent reported that they and all their close contacts had received influenza vaccine. The same was true for Tdap vaccine (25%), whereas only 14% reported that they and all their close contacts had received both influenza and Tdap vaccines.
In bivariate analyses for each vaccine (Table 2), mothers who reported cocooning were slightly older and more likely to be White than Hispanic or other race. For influenza vaccine cocooning, specifically, all HBM domains except perceived severity were associated. Specifically, the likelihood of cocooning increased with increased perceived benefits of vaccination, perceived susceptibility to illness and normative influences, and the likelihood of cocooning decreased with higher perceived barriers. Obstetrician recommendation for both mothers and close contacts to receive the vaccine was also associated with cocooning. Three domains (benefits, barriers and susceptibility) and obstetrician recommendation for the mothers maintained this association after adjustment in multivariable models.
In addition, mothers who reported cocooning against pertussis were more highly educated and less likely to report having Medicaid insurance. All 5 HBM domains were associated with cocooning for Tdap vaccine in bivariate analyses. Of these, barriers and susceptibility maintained this association with Tdap cocooning after adjustment in multivariable models. Obstetrician recommendation for the mother to receive the Tdap vaccine was also associated with cocooning. Hispanic race also maintained the association after adjustment, with a lower likelihood of cocooning when compared with White race.
In this survey of postpartum mothers, we found relatively high percentages reporting receipt of influenza and Tdap vaccines for themselves, with 67% reporting having received both vaccines. Additionally, about 6 of 10 and 7 of 10 of these mothers reported that at least 1 close contact of their newborn had been vaccinated against influenza and pertussis, respectively, which we defined as “cocooning.” Mothers reported generally greater perceived benefits from Tdap vaccine than from influenza vaccine. However, close to one-half had general concerns about vaccine safety. About two-thirds of respondents reported having received a recommendation from their obstetrician for both influenza vaccine and Tdap vaccine, and about half had received recommendations regarding cocooning. Cocooning was associated with several psychological domains corresponding to attitudes about vaccination and importantly also with a recommendation to be vaccinated from the obstetrician. For Tdap but not influenza vaccine, cocooning was negatively associated with Hispanic race, a finding that is difficult to explain based on our study but which requires further explanation.
A striking finding from our study was the association of maternal receipt of vaccination with the receipt of vaccination of newborn’s close contacts, which we found for both influenza and pertussis vaccination. Approximately 3 times as many infants’ close contacts were vaccinated among mothers who got these vaccines when compared with mothers who did not receive these vaccines. While there is likely some degree of reporting bias in this finding, it could suggest that mothers strongly influence the rest of the household when it comes to vaccination. However, it is also possible that these mothers were simply from households with a strong culture of vaccination, so that they were influenced by the household rather than vice versa. The findings from the multivariable model were consistent with the idea of the mother influencing the household: provider recommendation was known to be associated with maternal receipt of vaccine,3,29–35 and in our study, it was also associated with vaccination of their infants’ close contacts. This finding has important implications: while there has been significant effort at trying to vaccinate the close contacts of newborn infants, whether in hospitals or in pediatricians’ offices, resources and educational efforts may be better allocated to educating mothers who are hesitant to be vaccinated of the benefits and safety of vaccination. One might posit that once they are convinced of the importance of vaccination, they would then do the work of making sure that other close contacts of their newborn are also vaccinated.
The findings of our multivariable models help inform potential educational messages for pregnant women. While it is not surprising that higher perceived susceptibility to infection and lower perceived barriers to vaccination were associated with cocooning for both vaccines, the strongest association for influenza vaccine, greater even than obstetrician recommendation, was high perceived benefits to vaccination. This is consistent with the findings of a study from the 2012–2013 influenza season, which found that among pregnant women who received a recommendation from a health care provider and were offered influenza vaccine but refused it, the most common concerns were that the vaccine would cause influenza, safety risk to the baby and not believing that the vaccination was effective.13 The implication is that educational efforts and interventions among pregnant women regarding influenza vaccine could be focused on increasing the understanding of the benefits of vaccination to the newborn infant and its safety during pregnancy.
Because more women in the US are receiving prenatal care from advanced practitioners such as nurse midwives, physician assistants and nurse practitioners,36 our study results suggest that educational efforts aimed at increasing vaccination among pregnant women should be focused not only on obstetricians but also on advanced practitioners. In this study, pregnant women were more likely to have received recommendations for vaccination and cocooning specifically from obstetricians than from advanced practitioners. It is possible that our sample reported this simply because they saw obstetricians more often than advanced practitioners, so this finding should be considered hypothesis-generating rather than conclusive. Nonetheless, most of the prior studies regarding attitudes about vaccination in pregnancy have been among obstetricians themselves, with little exploration of attitudes of advanced practitioners. Educational efforts targeted at advanced practitioners and ancillary staff could increase the frequency of vaccine recommendations, promoting a “culture of vaccination” within the obstetrical setting.
Women in our study reported multiple settings for influenza and Tdap vaccination, with the obstetrics provider’s office the most common site for influenza vaccination and the hospital after delivery the most common site for Tdap vaccination. Our study was conducted for about 1 year after the recommendation to give Tdap vaccination in pregnancy, suggesting that many providers were still not stocking Tdap vaccine at the time of the survey but rather relying on the delivering hospitals to provide it. Providers who do not stock these vaccines should consider that recommending a vaccine, while important, is not enough: they must stock and administer it as well, as women whose providers do not stock vaccine are less likely to receive it.13 Providers may still be concerned about the financial and logistical barriers associated with stocking and administering vaccines.37–39 However, these barriers have decreased as the Affordable Care Act requires first dollar coverage (no copay) for all the Advisory Committee on Immunization Practices-recommended vaccines.40 Providers can access resources to aid them in providing vaccines, such as the toolkits created by the American College of Obstetrics and Gynecology for vaccination within OB/GYN practices.41
This study had several limitations. First, the respondents may have been more likely to have more favorable attitudes toward vaccination than nonrespondents. Also, vaccination status was based on self-report and may not have been accurate, particularly when reporting for the close contacts of newborns. Moreover, the high reported rates of vaccination may reflect social desirability bias.42 An additional limitation is that the study population was exclusively English-speaking as well as relatively well-educated and affluent, which is very likely to limit its generalizability. In addition, the finding of a negative association of Hispanic race with cocooning may have resulted from this sample bias. Sample bias or the broader availability of influenza vaccine may also account for the finding that influenza vaccine was more acceptable than Tdap among Hispanics, which contradicts previous experience.
This study confirms the findings of prior studies about the importance of obstetrician recommendation to pregnant women to receive vaccines and adds to the literature that that influence applies to the vaccination of close contacts as well. Close contacts of newborns are also more likely to be vaccinated if the mother herself is vaccinated, suggesting that educational efforts regarding the importance of cocooning newborns may best be directed at pregnant women. Future educational interventions should be directed at addressing identified barriers to vaccination and stressing the benefits of vaccination, particularly for influenza vaccine.
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