Knowledge, attitudes and practices on influenza vaccination during pregnancy in Quito, Ecuador

Background Vaccination is the most effective way to prevent infection and severe outcomes caused by influenza viruses in pregnant women and their children. In Ecuador, the coverage of seasonal influenza vaccination in pregnant women is low. The aim of this study was to assess the knowledge, attitudes, and practices (KAP) of pregnant women toward influenza vaccination in Quito-Ecuador. Methods A cross-sectional study enrolled 842 women who delivered at three main public gynecological-obstetric units of the Metropolitan District of Quito. A questionnaire regarding demographics, antenatal care, risk conditions and knowledge, attitudes and practices related to influenza vaccination was administered. We examined factors associated with vaccination using log-binomial regression models. Results A low vaccination rate (36.6%) against influenza was observed among pregnant women. The factors associated with vaccination included the recommendations from health providers (adjusted PR: 15.84; CI 95% 9.62–26.10), belief in the safety of the influenza vaccine (adjusted PR: 1.53; CI 95% 1.03–2.37) and antenatal care (adjusted PR: 1.21; CI 95% 1.01–1.47). The most common reasons for not vaccinating included the lack of recommendation from health care providers (73.9%) and lack of access to vaccine (9.0%). Conclusions Health educational programs aimed at pregnant women and antenatal care providers have the most potential to increase influenza vaccination rates. Further studies are needed to understand the barriers of health care providers regarding influenza vaccination in Ecuador. Supplementary Information The online version contains supplementary material available at 10.1186/s12889-020-10061-4.


Background
Pregnant women and infants under 6 months are among the population subgroups considered to be at high risk for serious influenza-related morbidity and mortality, as illustrated during the 1918 and 2009-2010 influenza A (H1N1) pandemics [1]. The mechanical, hormonal, and relevant immunologic alterations that occur during pregnancy may enhance the susceptibility to viral infections and the risk of influenza complications [2,3]. In 2018, a study estimated that a large proportion of influenzavirus-associated acute lower respiratory infections (ALRI) hospitalizations and in-hospital deaths occurred among young infants and among children in low-income and lower middle-income countries [4]. Influenza can cause primary infections or is also associated with higher rates of secondary bacterial infections [5]. Therefore, maternal influenza immunization could play a role in reducing the burden of all-cause ALRI [4].
In 2012, World Health Organization (WHO) recommended that countries should consider pregnant women as a priority group for vaccination [6]. Several studies have shown that maternal influenza immunization could protect pregnant women from severe complications related to influenza virus infection [7][8][9], and that infants up to 6 months of age from vaccinated women may also benefit [10][11][12][13]. For example, in a pooled analysis of three maternal influenza immunization trials in South Africa, Mali and Nepal, there was 20% reduction in allcause severe clinical pneumonia in infants under 6 months [10]. In addition, a recent systematic review and meta-analysis reported that maternal influenza vaccination was associated with a 48 and 72% reduced risk of infants having laboratory-confirmed influenza infection and associated hospitalization, respectively [14].
The Ministry of Public Health (MOPH) of Ecuador incorporated the seasonal influenza vaccine to its national vaccination schedule in 2006 and priority groups were included progressively according to WHO recommendations [15]. The MOPH supplies the Northern Hemisphere influenza vaccine free of charge through annual campaigns. In addition, the vaccine must be recommended and offered by health providers, especially those in primary care, during the flu season campaign period. In May 2016, an additional vaccination campaign focusing on priority groups was developed due to an outbreak presented earlier that month [15]. The importance of annual influenza vaccination is highlighted in different media and healthcare centers as well as on MOPH's website. Despite these efforts, Ecuador has reported low coverage rates of the influenza vaccine in pregnant women (55% in 2015, 63% in 2016, 55% in 2017 and 67% in 2018) [15,16].
Many studies have tried to determine the factors influencing coverage of vaccination against influenza during pregnancy. Different authors have highlighted that vaccination recommendation by health professionals is the main reason why pregnant women chose to be vaccinated against influenza [17][18][19][20][21]. Other studies have identified additional influences such as: socio-economic characteristics, fear of side effects, doubts about the safety and effectiveness of the vaccine, fear of needles/ pain or under-estimation of personal risk [22][23][24][25].
Currently, in Ecuador, there is no available data on the factors affecting vaccination among pregnant women. A KAP survey is usually conducted to identify needs, problems and barriers to help plan and implement public health interventions, set program priorities and make program decisions [26]. Therefore, this study aimed to assess knowledge, attitudes, and practices (KAP) of pregnant women regarding influenza vaccination in Quito, Ecuador and to determine the influencing factors associated with vaccination during 2015-2016 campaign. The results of this study may help health authorities plan and implement policies to improve influenza vaccination coverage among pregnant women.

Study design and setting
In Ecuador, two influenza vaccination campaigns were carried out for all priority groups, including pregnant women (December to February 2015-2016 and May 2016). We carried a cross-sectional survey on the knowledge, attitudes, and practices regarding the influenza vaccination during pregnancy from September 2016 to January 2017 in three public hospitals in Quito, the capital of Ecuador. Quito sits at an altitude of 2850 m above sea level and has 2,239,191 inhabitants being the second most populous city in Ecuador [27].

Study population and sampling
The three public hospitals chosen (Hospital Luz Elena Arismendi, Hospital Isidro Ayora and Hospital Pablo Arturo Suárez) had the highest number of births in 2015 and each hospital is located in a specific area of the city (south, center and north, respectively). In these hospitals, women in immediate postpartum period between 18 and 50 years old were recruited. We interviewed a sample of 854 women (Luz Elena Arismendi, n = 168; Isidro Ayora, n = 536 and Pablo Arturo Suárez, n = 150 women) with probability of selection proportional to the number of live births reported for each health care facility in 2015. This sample size provided 80% power to detect a 10% difference in survey responses to questions about knowledge, attitudes and practices between vaccinated and unvaccinated women (assuming 50% of surveyed women are vaccinated, a 10% non-response rate and alpha = 0.05). Women who did not reside within the Metropolitan District of Quito were excluded from the study.

Data collection and recruitment
Participant enrollment into the study was carried out by convenience sampling in the postpartum wards of the three hospitals until sample size was reached. Signed informed consent was obtained from each eligible woman interested in enrolling prior to administration of the survey. Illiterate mothers consented by their thumb print after verbal consent. A KAP questionnaire was applied in Spanish by two experienced survey interviewers without medical background who were trained by the authors of the present study (Additional file 1). The survey included questions on demographics, educational level, employment, antenatal care, high-risk conditions, knowledge (influenza, influenza vaccine and severity of influenza), attitudes (perception of vaccine safety and effectiveness) and practices (uptake of influenza vaccine) about influenza vaccine, influenza vaccine during pregnancy, reasons for not receiving vaccination, health provider recommendation and offer of the vaccine. To validate the questionnaire, a team of experts (Influenza Division, CDC, Atlanta, USA) reviewed the items to ensure clarity and adequacy of comprehension prior to administration. Field validation was then carried out and the survey instrument was adjusted accordingly. Selfreported data about influenza vaccination was corroborated through vaccination cards and medical records.

Statistical analysis
For the analysis of the data, the vaccination report of the mother was used. Age was categorized in four groups: 18-24, 25-30, 31-35, ≥36. Patients were classified as high obstetric risk if they reported having diagnosis of bronchitis, asthma, chronic obstructive pulmonary disease, cystic fibrosis, diabetes, HIV, cardiovascular disease, chronic kidney disease or stroke. We calculated the percentage of women that were vaccinated against influenza by provider recommendation and the offer of influenza vaccination. Among unvaccinated persons, we categorized the main reasons reported for not being vaccinated into 4 main groups: access issues, not wanting or needing the vaccine, concern with safety, lack of offer / recommendation of the vaccine. We also assessed the categorized main reported reasons for not being vaccinated by demographic characteristics, education, number of children, antenatal care, and high-risk conditions. Finally, we analyzed the relationship of receipt of influenza vaccination with predictors for vaccination (age, educational level, marital status, employment, antenatal care, number of children, high-risk conditions, gestational age at birth, recommendation or offer of vaccination by health care provider, and knowledge and attitudes about vaccination) by bivariate and multivariate analysis (log-binomial regression). We present unadjusted and adjusted prevalence ratios (PRs) with 95% confidence intervals. Data were analyzed using STATA® software (version 14.0).

Characteristics of study population
A total of 854 pregnant women were invited to participate in the survey and accepted by written consent to participate in the study (24 mothers refused to participate). Of those invited, 12 (1.4%) were excluded because they were not residents of Quito and only arrived at selected hospitals for delivery. Therefore, 842 pregnant women were included in the analysis.
The characteristics of the sample are described in Table 1. Almost three-quarters of participants in this survey were between 18 and 30 years old, 86% were mixed-race women and 58% finished high school. Most women were married or cohabited with a partner (79%), 44.2% were homemakers and approximately two thirds (65%) of women reported having at least one other child prior to this pregnancy. Nearly all women (98.7%) reported attending at least one antenatal visit and 81% reported more than four antenatal visits. Only 8% of women reported having chronic diseases.

Vaccination rate in pregnant women
The percentage of women who reported having been vaccinated against influenza at any time in their pregnancy was 36.6%. Sixty percent of women have been vaccinated during the second trimester of pregnancy. Vaccination data was confirmed with the vaccination card and/or medical records in 67% of vaccinated women (Table 1).

Knowledge and attitudes regarding influenza and influenza vaccination
Knowledge about the severity of influenza and the existence of a vaccine was higher among women who reported having been vaccinated compared to those who reported not having been vaccinated (p = 0.017 and p < 0.001, respectively, Fig. 1a and b). Vaccinated women perceived that the influenza vaccine is safe (95.8% vs 71.7%, respectively) and effective (68.5% vs. 61.4%, respectively) in a higher proportion than unvaccinated women (p < 0.001 y p = 0.030, respectively, Fig. 1c and d).

Reasons for not receiving influenza vaccination
The most frequent reason identified as a barrier to vaccination among pregnant women was the lack of recommendation/offer of the vaccine by the health provider (73.9%). Other reasons in smaller proportion were lack of access (9.0%), concern with the safety of the vaccine (6.2%), not wanting/needing the vaccine (3.7%) and other causes (7.3%) ( Table 2). The most common reasons for non-vaccination among women with complete basic education or higher were also related to not having received a recommendation/offer of the vaccine by the health care provider, vaccine safety concerns and other reasons, whereas for women without any educational level or with incomplete basic education, not wanting/needing the vaccine and access barriers were the most common reason for non-vaccination. (p = 0.001, Table 2).

Provider recommendation and offer of influenza vaccination
Among women who indicated that their health care provider recommended and offered the influenza vaccine, 82.7% reported having been vaccinated for influenza since the end of 2015. Among those who reported that their health care provider recommended but did not offer vaccination against influenza, 15.0% reported having been vaccinated for influenza. Finally, 4.3% of the respondents who did not receive either a recommendation or an influenza vaccination offer, reported having been vaccinated (p < 0.001, Fig. 2).

Relationship between determinants and vaccination
A larger number of antenatal care visits, knowledge about vaccine safety, and having received recommendation (with or without offer of the vaccine) by health care personnel were associated with vaccination during pregnancy in both the bivariate and multivariate analysis (Table 3). Specifically, the vaccination rate was 1.67 times higher in women who reported having five or more antenatal controls during pregnancy than in women who reported having fewer than five controls and the association was maintained after adjustment by other predictors (adjusted PR 1.21, 95% CI 1.01-1.47). Women who perceived vaccination against influenza as safe had higher vaccination rates than those who did not (adjusted PR 1.53, 95% CI 1.03-2.37). Finally, women who reported receiving recommendation but were not offered vaccination and those who reported receiving both recommendation and were offered vaccination had 3.17 (95% CI 1.57-6.40) and 15.84 (95% CI 9.62-26.10) greater likelihood of having received the vaccine compared to women who did not receive a recommendation/offer.

Discusion
Our study found a low influenza vaccination rate in pregnant women in Quito-Ecuador and identified some barriers that could contribute to low vaccination coverage. Those women who were vaccinated knew about the severity of influenza, about the existence of a vaccine, and perceived vaccination against influenza as safe and effective. The main barrier for not receiving the vaccine was the lack of recommendation/offer regarding influenza vaccine by health care providers. Among the determinants, recommendation/offer of vaccine increases the likelihood of vaccination in pregnancy. Other factors associated with vaccination were knowledge about vaccine safety and more than five antenatal care visits.
The vaccination rate reported in this study (36.6%) is lower than those reported for Ecuador in 2015 (55%) and 2016 (63%) and for those reported by other   [16]. However, the coverage could be underestimated due to the low percentage of women with perinatal or vaccination cards [28]. In Ecuador, the coverage of all vaccines (including the influenza vaccine) has shown a gradual decrease since 2013 to 2016, and a slight increase from 2017 [15] . The Evaluation of National Strategy of Immunizations revealed two elements related to this fact: 1) the Immunization Program underwent a transition, becoming part of the National Immunization Strategy. This fact implied a disaggregation of functions between different actors without an effective articulation of actions; and 2) the lack of budget allocation in a sustainable manner for operational activities of vaccination strategy [15]. Given these facts and the results of the present study, there is an urgent need to implement a contingency plan to improve short-term vaccination coverage and reduce the risk of transmission of vaccine-preventable diseases in Ecuador.
Our results are in agreement with previous studies that show that a compelling recommendation from a provider is one of the most important factors in a pregnant woman's decision to get vaccinated [21,25,[29][30][31][32].
Indeed, the lack of recommendation was a barrier for vaccination among pregnant women. Knowledge about influenza and vaccination by health workers has an impact on the decisions made regarding the vaccination of their patients and themselves. Studies show that maternal care providers with high levels of knowledge and positive attitudes consistently discuss and recommend influenza vaccine to their patients in greater proportion than other health providers [33][34][35][36]. Similarly, health professionals who know the national guidelines on influenza vaccination are more likely to discuss and recommend the vaccine than those who do not know them [37]. To our knowledge, there are no studies in Ecuador on the knowledge and attitudes of health workers regarding the influenza vaccination. Other studies demonstrate that health care workers are often reluctant to receive a vaccine [38,39], have concerns about side effects, demonstrate a lack of faith in its efficacy and have concerns in the severity of the disease [40,41]. Understanding health provider barriers is vitally important because it is not possible to overcome vaccination barriers among pregnant women if health providers themselves are not fully convinced about the benefits of maternal immunization.   Most common other reasons were: "Don't know", "I had already been vaccinated before pregnancy" c Fourteen people did not answer the question Working to promote practices related to the recommendation and offer of influenza vaccination among antenatal care providers (physicians, obstetricians, nurses and midwifes) will be crucial to improving vaccination coverage during pregnancy. A recent study in five lower-middle and upper-middle income countries from Latin America reported a training gap related to maternal and neonatal immunization (MNI) programs in the pre-graduate curriculum of universities. Moreover, all five countries reported continuous training for health workers mostly addressed to personnel that administer vaccines, but not health care providers who recommend them [42]. Another study highlights the need to involve midwives and obstetricians in vaccine promotion and training as they usually have close and trust-based relationships with their pregnant patients [43]. Therefore, the incorporation or reinforcement of MNI programs in the university curriculum for the training of doctors, nurses, obstetricians, and midwives as well as continuous training for all antenatal care providers could be crucial for increasing influenza vaccine uptake during pregnancy.
In the present study, women who reported perceiving the influenza vaccine as safe and effective had the highest vaccination rates and vaccine safety concern was a reason for not receiving vaccination among 6.2% of nonvaccinated women. Lack of knowledge due to insufficient information about the safety of the influenza vaccine has previously been linked to lower vaccination rates [22,23,44]. The vaccine is considered safe throughout pregnancy and during lactation, and has been administered to pregnant women for many years without having observed adverse effects [1]. Therefore, efforts are needed to educate pregnant women and the population in general regarding the safety and effectiveness of the influenza vaccine to improve vaccination coverage of this risk group.
Having five or more antenatal visits increased the probability of vaccination which is in accordance to other studies [45][46][47]. Antenatal check-ups are essential to promoting the benefits of influenza vaccination and to offering the vaccine to pregnant women [48]. To increase vaccination coverage, it would be necessary to offer the influenza vaccine for a longer period rather than just one or two vaccination campaigns. This strategy would benefit women who have few prenatal visits or who are late in attending their first visit. Altogether, different strategies of vaccine delivery to pregnant women need to be evaluated to inform policy decisions in countries where influenza circulation is not confined to a single seasonal peak.
Our study showed different reasons for not being vaccinated according to educational level of women. The main reasons for lack of vaccination among illiterate women or with incomplete basic education was not need/want the vaccine and lack of access to vaccination. Studies have shown that people who have a higher education level and/or household income are more likely to receive preventive health services because they may have more knowledge about the importance of healthpreventive care and the effectiveness of preventive strategies and more access to health-related services [49,50].
Some limitations were identified in this study. Firstly, cross-sectional studies do not allow inferring causality because temporal sequence cannot be established. Second, the study sample was not randomly selected but rather a convenience sample, which makes generalization difficult and affects the external validity. We selected a population that is homogeneous with respect to socioeconomic level (lower and lower-middle class population) who use the public health system; therefore, the results could be representative of this group in Quito. Third, this study corresponds to the 2015-2016 influenza-vaccination campaign; however, the results are relevant considering the low vaccination coverage during the last years and the lack of information on the barriers related to vaccination during pregnancy in Ecuador. Finally, 30 % of vaccinated women lacked documentation of influenza vaccine status and selfreport of vaccination could be affected by social desirability and forgetfulness; however, analysis of a subsample that included only those with written documentation of vaccination showed similar findings.

Conclusion
In conclusion, the low rate of vaccination of pregnant women in Quito supports the need to establish health educational programs to increase the knowledge about seasonal influenza and on the efficacy and safety of vaccination among this population. These results also call for further studies on barriers of health providers regarding influenza vaccination in Ecuador. Education and training of all antenatal care providers, including obstetricians and midwives is needed to enhance their role as vaccinators, which could potentially increase the number   interpretation of data, writing of the report or decision to submit the article for publication.

Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author (Ana L. Moncayo) on reasonable request.
Ethics approval and consent to participate Signed informed consent was obtained from all participants after explaining the objectives and risks inherent to the study. Participants were assured of their rights to participate/withdraw their consent.

Consent for publication
Not applicable.

Competing interests
The authors declare that they have no competing interests.