Vaccine 32 (2014) 5957–5961
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Health care professionals’ awareness of, knowledge about and attitude to influenza vaccination Thamir M. Alshammari a,b,∗ , Lama S. AlFehaid c , Joud K. AlFraih d , Hisham S. Aljadhey b,e a
College of Pharmacy, Hail University, Hail, Saudi Arabia Medication Safety Research Chair, King Saud University, Riyadh, Saudi Arabia College of Pharmacy, King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia d Prince Mohammad bin Abdulaziz Hospital, Saudi Arabia e College of Pharmacy, King Saud University, Riyadh, Saudi Arabia b c
a r t i c l e
i n f o
Article history: Received 25 February 2014 Received in revised form 30 July 2014 Accepted 27 August 2014 Available online 11 September 2014 Keywords: Influenza vaccine Attitude and knowledge Healthcare professional Saudi Arabia
a b s t r a c t Objectives: Influenza vaccination is recommended to all health care professionals (HCPs). However, vaccination rate among HCPs is low and may be due to uncertainty about the effectiveness of the vaccine and fear of its adverse effects. Therefore, this study aimed to investigate the awareness, knowledge, and attitude of HCPs towards influenza vaccination and we ascertain reasons for not getting vaccinated. Method: A cross-sectional conducted in 6 major hospitals in Saudi Arabia. 245 anonymous questionnaires were distributed to a convenient sample of staff during the 2012–2013 influenza season. The validated questionnaire consists of five sections that collect information about: demographics, attitude towards influenza vaccination, knowledge about influenza virus and vaccination, current practice and awareness of published guidelines. Results: 242 completed questionnaires were received, a response rate of 98%. 38% of HCPs reported getting vaccinated. The most common reasons given by HCPs for not getting vaccinated were: fear of contracting illness (16%), belief that they are not at risk from influenza because they are young and healthy (13%) and being unaware of vaccine availability (13%). Non-availability of vaccine (43%) was the highest barrier for not providing vaccine for patients and HCPs followed by safety concerns for the patients (35%) and the respondents (33%). Almost 75% of HCPs were not aware of the influenza immunization guidelines published by the Advisory Committee on Immunization Practices and Centre for Disease Control. Conclusion: Despite the recommendations, only low percentage of HCPs in Saudi Arabian hospitals is vaccinated against influenza. The attention of health policy makers is needed to improve compliance of HCPs with guidelines on influenza vaccination. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction The United States Advisory Committee on Immunization Practices (ACIP) advises all HCPs to be vaccinated against influenza [1]. This recommendation and an increased risk of disease among HCPs compared with the general population notwithstanding, worldwide HCP compliance with influenza vaccination programmes is known to be low and is far below the level needed to achieve herd immunity [2,3]. The low vaccination rate in HCPs may be due
∗ Corresponding author at: Department of Clinical Pharmacy, College of Pharmacy, Hail University, P.O. Box 6166, Horan Street, Hail 81442, Saudi Arabia. Tel.: +966 505192886. E-mail addresses: [email protected], [email protected] (T.M. Alshammari). http://dx.doi.org/10.1016/j.vaccine.2014.08.061 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
to uncertainty about the effectiveness of the vaccine and fear of its adverse effects [4,5]. However, understanding these barriers is essential to overcoming low compliance with recommendations for vaccination. In our region, few studies have addressed these issues. In 2010, a study has been conducted in one hospital in Saudi Arabia found that there is a poor knowledge of HCPs towards influenza disease and its prevention and there is a misconception towards influenza vaccine among the respondents [5]. Another study has been conducted in the same year in three middle east countries and found there is a lower rate of vaccination among these countries [6]. In Saudi Arabia, there are no specific guideline for HCPs in all health care systems regarding influenza vaccination. However, the ministry of health advises all visitors to perform Hajj and/or Umrah to be vaccinated against seasonal influenza vaccine. Moreover, HCPs who are working during Hajj season are also recommended to get the seasonal influenza
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T.M. Alshammari et al. / Vaccine 32 (2014) 5957–5961
vaccine [7,8]. This study explored opinions about, knowledge of, and attitudes to seasonal influenza vaccination in HCPs; investigated the percentage of voluntary immunization against influenza vaccine among HCPs in Saudi Arabia and explored why HCPs did not get vaccinated. Strategies to improve influenza vaccination rates in HCPs in Saudi Arabia to make sure those HCPs and their patients are protected from influenza are proposed. 2. Method This study was a cross-sectional study conducted in 6 major governmental and private hospitals in Saudi Arabia. These hospitals included educational and military hospitals. An anonymous, self-administered questionnaire was distributed to HCPs during the 2012–2013 influenza season (between March and May 2013); completion of the questionnaire was voluntary. The study was approved by Medication Safety Research Chair, King Saud University. 2.1. Questionnaire items The questionnaire was composed of five sections. The first section concerned general information about the participant such as gender, professional title and specialty. The second section contained questions that measured attitude to influenza vaccination by asking whether participants routinely got vaccinated against influenza, and their reasons for not getting vaccinated. The third section assessed knowledge about influenza virus transmission, recommended frequency of vaccination and the perceived effectiveness and risks of the vaccine. The fourth section asked about current practice, including whether their workplace offered the influenza vaccine and whether they were interested in participating training related to the influenza vaccine. The final section tested awareness of published guidelines, susceptibility to and risks associated with influenza infections for HCPs, signs and symptoms of influenza infection, potential seriousness of influenza, availability of influenza vaccine in different dosage forms and vaccine properties. The questionnaire was validated and piloted on fifteen HCPs with research experience. Two trained pharmacists were responsible for distributing the questionnaires during visits to the participating hospitals. In some hospitals, the pharmacist interviewed participating HCPs and to obtain answers to the survey questions due to difficulties in these hospitals’ HCPs response; in other hospitals, the questionnaires were sent to the HCPs and completed questionnaires were collected during a revisit five days later. After 3 days a second collection visit was made. The questionnaire was voluntary and accepting in the participation in the study and a returned and complete questionnaire was taken as consent to participate. HCPs who had not completed the questionnaire within this period were considered non-respondents. 2.2. Statistical analysis Descriptive statistics were produced for all survey items. Data were analyzed using SAS version 9.2, the chi-squared test was used for comparisons between categorical variables, and bivariate analysis was used to examine associations between vaccination status and other independent variables. 3. Results A total of 245 questionnaires were randomly distributed in 6 major hospitals in Saudi Arabia with response rate of (98%, n = 242). Comparable numbers of HCPs from the different professions participated (physicians: 31%, pharmacists: 32.41%, nurses: 32%). A rather high proportion of HCPs (61.22%) had not received the influenza
Table 1 Demographic characteristics of participating healthcare professionals (HCPs). Characteristic Gender Male Female Professional title Physician Pharmacist Nurse Laboratory specialist Clinical pharmacist Pharmacy resident Physiotherapist Institution Governmental hospital Private hospital Botha Vaccinated against influenza Yes No a
Number
Percentage
118 127
48.16 51.84
76 75 80 1 6 1 6
31.02 30.61 32.65 0.41 2.45 0.41 2.45
171 72 2
69.80 29.39 0.82
95 150
38.78 61.22
Working in government and private hospitals.
vaccine (Table 1); there are a number of different possible reasons for non-compliance with vaccination among HCPs. Thirty-nine respondents (16%) stated that the vaccine would have a negative influence on their health and make them ill, thirty-two respondents (13%) believed they were not at risk of getting influenza as they were young and healthy. Nineteen respondents (8%) believed that they protected themselves from getting influenza by following all the required precautions e.g. washing hands and covering their nose and mouth when sneezing or coughing (Fig. 1). There was no significant difference in the rate of vaccination in pharmacists and other HCPs (p = 0.14), whilst the rate of vaccination in physicians was lower than for other HCPs (p = 0.03); nurses were the HCP group mostly likely to get vaccinated and had a higher rate of vaccination (p = 0.001). Caution is needed in interpreting these results as the total number of vaccinated HCPs was low. However, the majority of respondents (71%, n = 174) believed that the influenza vaccine is effective in preventing influenza. Of those, 44% have been vaccinated compared to 66% who did not (p = 0.01). Believe in the effectiveness of the vaccine was lower amongst pharmacists than other HCPs (p = 0.01); nurses were most likely to believe the vaccine to be effective, followed by physicians, nurses were more likely than other HCPs to believe the vaccine to be effective (p = 0.01). More than half the HCPs (65%, n = 158) said that Centre for Disease Control (CDC) recommended that they receive the influenza vaccine and the majority of HCPs believed that the influenza vaccine should be administered annually (80%, n = 195), (Table 2). Around 70% (n = 171) of HCPs believed that administration of the influenza vaccine should be part of their medical practice and over 71% (n = 174) of HCPs thought that they were encouraged to get vaccinated to protect them from catching influenza by direct exposure to sick patients, 51% (n = 126) believed that being vaccinated would minimize their sickness absence and loss of productivity and make them more able to take care of their patients. Eighty percent of participating HCPs had not received any training relating to influenza vaccination in the last 12 months; over 69% wanted to take training courses (such as continuing education on importance of influenza vaccine and the benefit of the vaccination) in vaccination. About 29% of the participants did not know whether their institution offered the influenza vaccine, although 50% reported that their institution did offer the influenza vaccine. About one third of the participants reported that they do not provide any information to the patients or public about the importance of influenza vaccination. Over one third (38%, n = 93) believed that influenza vaccination protects vulnerable patients and enhances patient safety during
T.M. Alshammari et al. / Vaccine 32 (2014) 5957–5961
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The vaccine doesn’t work The vccine is more dangerous than the virus They don’t like needles They can't afford to get the full shot The flu is not serious They do the right aseptic technique They don’t know where to get the full shot Youg & healthy Fear of contracting illness 0%
2%
4%
6%
8% 10% 12% 14% 16% 18%
Fig. 1. HCPs’ reasons for non-compliance with vaccination recommendations.
outbreaks of influenza. Barriers that HCPs believe that prevent them and their institutions from providing the influenza vaccine to some or all their patients and HCPs included, non-availability of vaccine (43%) followed by safety concerns for patients (35%) and for HCPs (33%). In addition, 19% and 13% of the participants think that both limited number of staff and lack of trained staff, respectively, were considered as barriers of not providing influenza vaccine. While, 14% considered cost of the vaccine is an important barrier (Fig. 2). About two thirds (65%, n = 159) of the HCPs were aware of influenza infection, but almost 75% (n = 184) were not aware of the ACIP or CDC guidelines on influenza immunization. Table 3 shows the awareness of HCPs towards influenza and influenza vaccine. About 85% of the respondents believe that influenza is more serious than common cold and 96% of them know the significant symptoms of influenza. Moreover, HCPs 76% of the respondents believe that asymptomatic infected HCPs could still spread the infection to other close people. In addition, 53% of the respondents believe that the influenza vaccine should have the correct mix of virus strains to work effectively. 4. Discussion Our study investigated knowledge of, and attitude to seasonal influenza vaccination in HCPs. Several studies have shown that influenza vaccination is effective in protecting HCPs against infection, minimizing transmission of the disease to their patients and decreasing mortality and morbidity among vulnerable patients;
vaccination also reduced absenteeism and improved the health status of HCPs [9–12]. The results of the present study revealed a low percentage of influenza immunization among HCPs (38%) during the 2012–2013 season despite the ACIP and CDC recommendations and HCPs being at high risk of infection. This rate is similar to that reported in other studies of influenza vaccination in HCPs in Saudi Arabia [5,13]. A cross-sectional study conducted by Rehmania and Memonet with 512 participants found influenza vaccination rate of 34% in the 2008–2009 season [5]. Rates in neighbouring countries have been very variable; a very low influenza vaccination rate was reported from United Arab Emirates (24.7%), but high rates were found in Kuwait (67.2%) and Oman (46.4%) [6]. However, we found no difference between the vaccination rate for pharmacists and other HCPs (p = 0.14), but physicians were less likely to get vaccinated than other HCPs (p = 0.03) and nurses more likely to get vaccinated than other HCPs (p = 0.001). Because the overall rate of vaccination of HCPs was low in our study the results should be interpreted with caution. Similarly to other reports [4–6], our data revealed significant gaps in HCPs’ knowledge about influenza vaccination. The low rate of immunization in HCPs practising in Saudi Arabia seems likely to be related to lack of knowledge and awareness; however this study did not demonstrate a consistent positive correlation between HPCs’ belief in the effectiveness of the influenza vaccine and the decision to be immunized. The results of our study showed that 71.43% of participants believed that influenza vaccine is effective in preventing influenza; nonetheless the self-reported vaccination rate was low. In addition, our
Need for ancillary supplies Need for proper storage of vaccine Training and readiness of staff Cost/reimbursement issues of vaccine Not enough staff to administer vaccine Safety concern for HCPs Safety concern for patients Vaccine is not available 0%
5%
10% 15% 20% 25% 30% 35% 40% 45% 50%
Fig. 2. Barriers to provision of the influenza vaccine in HCP institutions.
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Table 2 Knowledge of health care professionals (HCPs) about the influenza vaccine. Questions Do you think the influenza vaccine is effective in preventing the ‘flu?a Yes No Do you believe that the Centre for Disease Control (CDC) recommends that health care workers receive the’ flu shot?b Yes No I don’t know How often do you think the’ flu vaccine should be administered?c Every 6 months Every year Every 5 years Once in a lifetime Are you aware of the guidelines published by the Advisory Committee on Immunization Practices (ACIP) or Centre for Disease Control (CDC) for influenza immunization? Yes No a b c
Frequency
No. (%)
175 67
71.43 27.35
158 25 61
64.49 10.20 24.90
27 196 12 10
11.02 80 4.9 4.08
56 183
22.86 74.69
3 respondents (1.22%) did not answer this question. 1 respondents (0.41%) did not answer this question. 5 respondents (2.04%) did not answer this question.
data showed variable levels of awareness of and knowledge about influenza vaccination in HCPs (see Tables 2 and 3 for details), broadly in line with other studies [5,14,15]. Most HCPs had basic knowledge of the influenza vaccine and infection and most participating HCPs were aware that people with asymptomatic influenza can transmit influenza (75.5%); a find which contrasts with Khazaeipour et al.’s [16] study in which only 32.4% of HCPs stated that people with asymptomatic influenza can transmit influenza. Previous studies have reported variable rates of belief amongst healthcare workers (HCWs) that the influenza vaccine can cause influenza infection (38.1% to 78%) [14,15]; 48.16% of all respondents in our study shared this misconception. 80% of the participants were aware of the programme of influenza vaccination for HCPs yet 61% % [who may or may not have been aware] declined vaccination. Other studies have reported that in Saudi Arabia about 86% of participants were aware of the ACIP recommendation and in the three Middle East countries – United Arab Emirates, Kuwait and Oman – 48.5% of HCWs were aware of the CDC recommendations for vaccination against seasonal influenza [5,6]; we found much lower awareness of these guidelines: about 74.69% of participating HCPs were not aware of the ACIP or CDC recommendations for influenza immunization. In this study the most commonly reported reasons for non-compliance with vaccination recommendations were fear of contracting illness and concerns about side-effects of the influenza vaccine such as fever, fatigue and myalgia. These findings are consistent with other studies which investigated participants’ main reason for not taking up influenza vaccination. This suggests that vaccination campaigns should include facts about the rate of adverse reactions to the influenza vaccine. Other reasons given by HCPs for non-compliance included the belief that
Table 3 Awareness of healthcare professionals (HCPs) about influenza and the influenza vaccine. Questions
Correct
Incorrect
Health care professionals are less susceptible to influenza infections than other peoplea Number 39 190 15.92 77.55 Percentage Influenza is transmitted primarily by coughing and sneezinga Number 222 13 90.61 5.31 Percentage a Influenza is more serious than a “common cold” Number 210 16 Percentage 85.71 6.53 The signs and symptoms of influenza include fever, headache, sore throat, cough, nasal congestion, and aches and painsa Number 234 5 95.51 2.04 Percentage a HCPs can spread influenza even when they are feeling well Number 185 31 75.51 12.65 Percentage People with influenza can transmit the infection only after their symptoms appeara Number 60 146 24.49 59.59 Percentage Influenza is transmitted primarily by contact with blood and body fluidsa Number 48 162 19.75 66.67 Percentage Influenza vaccination may not work if the vaccine contains the wrong mix of virusesa Number 131 34 53.47 13.88 Percentage The flu shot contains live viruses that may cause some people to get influenzaa Number 118 67 48.16 27.35 Percentage Influenza vaccination does not work in some persons, even if the vaccine has the right mix of virusesa Number 122 35 49.80 14.29 Percentage Adults with influenza commonly experience nausea and vomiting or diarrheaa Number 88 83 35.92 33.88 Percentage a Symptoms typically appear 8–10 days after a person is exposed to influenza Number 96 58 39.18 23.67 Percentage a
2 respondents (0.82%) did not answer this questions.
Not sure 14 5.71 8 3.27 17 6.94 4 1.63 27 11.02 37 15.10 31 12.76 78 31.84 58 23.67 86 35.10 72 29.39 89 36.33
T.M. Alshammari et al. / Vaccine 32 (2014) 5957–5961
they were not at risk of getting influenza as they were young and healthy (13%); another study reported a somewhat similar result, with 6.2% of HCPs citing a belief that they were not at risk of infection as their reason for non-compliance with vaccination recommendations [16]. In this study, 43% of participants reported that availability of influenza vaccine was a barrier to their institution offering vaccination; the safety concerns of patients (35%) and HCPs (33%) were also cited as barriers to provision of vaccination to both patients and HCPs. In a study of attitudes and practice relating to influenza vaccination in registered nurses conducted in 4 US states vaccine supply (6%) and safety concerns (39%) were considered barriers to the provision of the influenza vaccination [17]. Awareness of availability of influenza vaccine is sometimes viewed as a barrier to influenza vaccination in HCPs, one study found that 98% of respondents were aware that their institution offered free vaccination [4]; but in our study about 29% of the participants did not know if their institution offered influenza vaccination and only 50% reported that their institution offered influenza vaccine. A lot of work is needed to increase HCPs’ compliance with influenza vaccination recommendations; interventions should include educational campaigns to address misconceptions. Successful vaccination programmes combine publicity and education for HCPs and other potential vaccine recipients, use of reminder and recall systems, assessment of organization-level vaccination rates combined with feedback to staff, and efforts to remove administrative and financial barriers to vaccination. This study has both strengths and limitations. The limitation of this study include that, influenza vaccination status was selfreported by respondents, not subject to independent verification and potentially influenced by social desirability bias. In addition, the results of this study cannot be generalized to other HCPs. Also, our sample size was either similar or smaller than in other studies. However, our study has several strengths; data was collected from 6 major hospitals, including government and private hospitals in order to assess practice in both types of hospital. The response rate for the survey was 98%, higher than that achieved in previously published studies. The majority of respondents were from government hospitals (69.80%). We also examined the vaccination rate according to professional title; this should enable interventions to improve compliance with influenza vaccination recommendations to target the group with the lowest rate of vaccination. 5. Conclusion Despite the recommendations, the percentage of HCPs who receive the influenza vaccine was low in Saudi Arabian hospitals. Concerns about the efficacy and safety of the influenza vaccine, fear of contracting illness, and unavailability of influenza vaccine in some hospitals were significantly associated with noncompliance with vaccination. More efforts by health authorities and
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regulatory in Saudi Arabia are needed to enhance compliance of all HCPs with recommendations for influenza vaccination; all HCPs should be encouraged to get vaccinated and make sure it is available in all hospitals, and special educational and campaign should be used to improve their knowledge and awareness. Conflict of interest There is no conflict of interest to declare. References [1] Pearson ML, Bridges CB, Harper SA. Influenza vaccination of health-care personnel: recommendations of the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006;55:1–16. [2] Song JY, Park CW, Jeong HW, Cheong HJ, Kim WJ, Kim SR. Effect of a hospital campaign for influenza vaccination of healthcare workers. Infect Control Hosp Epidemiol 2006;27:612–7. [3] Dey P, Halder S, Collins S, Benons L, Woodman C. Promoting uptake of influenza vaccination among health care workers: a randomized controlled trial. J Public Health Med 2001;23:346–8. [4] Douville LE, Myers A, Jackson MA, Lantos JD. Health care worker knowledge, attitudes, and beliefs regarding mandatory influenza vaccination. Arch Pediatr Adolesc Med 2010;164:33–7. [5] Rehmani R, Memon JI. Knowledge, attitudes and beliefs regarding influenza vaccination among healthcare workers in a Saudi hospital. Vaccine 2010;28:4283–7. [6] Abu-Gharbieh E, Fahmy S, Rasool BA, Khan S. Influenza vaccination: healthcare workers attitude in three Middle East countries. Int J Mol Sci 2010;7:319–25. [7] Ministry of Health (Saudi Arabia).Health regulations for the 1435HHajj season. 2014. http://www.moh.gov.sa/en/Hajj/News/Pages/News-201404-03-001.aspx [accessed on 23.05.14]. [8] World Health Organization (WHO). Weekly epidemiological record, 30. 2012. p. 277–88. http://www.who.int/wer/2012/wer8730.pdf?ua=1 [accessed on 23.05.14]. [9] Benet T, Regis C, Voirin N, Robert O, Lina B, Cronenberger S, et al. Influenza vaccination of healthcare workers in acute-care hospitals: a case–control study of its effect on hospital-acquired influenza among patients. BMC Infect Dis 2012;12:30. [10] Saxen H, Virtanen M. Randomized, placebo-controlled double blind study on the efficacy of influenza immunization on absenteeism of health care workers. Pediatr Infect Dis J 1999;18:779–83. [11] Carman WF, Elder AG, Wallace LA, McAulay K, Walker A, Murray GD, et al. Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: a randomised controlled trial. Lancet 2000;355:93–7. [12] Benowitz I, Esposito DB, Gracey KD, Shapiro ED, Vazquez M. Influenza vaccine given to pregnant women reduces hospitalization due to influenza in their infants. Clin Infect Dis 2010;51:1355–61. [13] Al-Tawfiq JA, Antony A, Abed MS. Attitudes towards influenza vaccination of multi-nationality health-care workers in Saudi Arabia. Vaccine 2009;27:5538–41. [14] Wicker S, Rabenau HF. Vaccination rates of healthcare workers vary according to their occupational group. Procedia Vaccinol 2011;4:14–8. [15] Nichol KL, Lind A, Margolis KL, Murdoch M, McFadden R, Hauge M, et al. The effectiveness of vaccination against influenza in healthy, working adults. N Engl J Med 1995;333:889–93. [16] Khazaeipour Z, Ranjbarnovin N, Hoseini N. Influenza immunization rates, knowledge, attitudes and practices of health care workers in Iran. J Infect Dev Ctries 2010;4:636–44. [17] Clark SJ, Cowan AE, Wortley PM. Influenza vaccination attitudes and practices among US registered nurses. Am J Infect Control 2009;37:551–6.
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Health care professionals’ awareness of, knowledge about and attitude to influenza vaccination Thamir M. Alshammari a,b,∗ , Lama S. AlFehaid c , Joud K. AlFraih d , Hisham S. Aljadhey b,e a
College of Pharmacy, Hail University, Hail, Saudi Arabia Medication Safety Research Chair, King Saud University, Riyadh, Saudi Arabia College of Pharmacy, King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia d Prince Mohammad bin Abdulaziz Hospital, Saudi Arabia e College of Pharmacy, King Saud University, Riyadh, Saudi Arabia b c
a r t i c l e
i n f o
Article history: Received 25 February 2014 Received in revised form 30 July 2014 Accepted 27 August 2014 Available online 11 September 2014 Keywords: Influenza vaccine Attitude and knowledge Healthcare professional Saudi Arabia
a b s t r a c t Objectives: Influenza vaccination is recommended to all health care professionals (HCPs). However, vaccination rate among HCPs is low and may be due to uncertainty about the effectiveness of the vaccine and fear of its adverse effects. Therefore, this study aimed to investigate the awareness, knowledge, and attitude of HCPs towards influenza vaccination and we ascertain reasons for not getting vaccinated. Method: A cross-sectional conducted in 6 major hospitals in Saudi Arabia. 245 anonymous questionnaires were distributed to a convenient sample of staff during the 2012–2013 influenza season. The validated questionnaire consists of five sections that collect information about: demographics, attitude towards influenza vaccination, knowledge about influenza virus and vaccination, current practice and awareness of published guidelines. Results: 242 completed questionnaires were received, a response rate of 98%. 38% of HCPs reported getting vaccinated. The most common reasons given by HCPs for not getting vaccinated were: fear of contracting illness (16%), belief that they are not at risk from influenza because they are young and healthy (13%) and being unaware of vaccine availability (13%). Non-availability of vaccine (43%) was the highest barrier for not providing vaccine for patients and HCPs followed by safety concerns for the patients (35%) and the respondents (33%). Almost 75% of HCPs were not aware of the influenza immunization guidelines published by the Advisory Committee on Immunization Practices and Centre for Disease Control. Conclusion: Despite the recommendations, only low percentage of HCPs in Saudi Arabian hospitals is vaccinated against influenza. The attention of health policy makers is needed to improve compliance of HCPs with guidelines on influenza vaccination. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction The United States Advisory Committee on Immunization Practices (ACIP) advises all HCPs to be vaccinated against influenza [1]. This recommendation and an increased risk of disease among HCPs compared with the general population notwithstanding, worldwide HCP compliance with influenza vaccination programmes is known to be low and is far below the level needed to achieve herd immunity [2,3]. The low vaccination rate in HCPs may be due
∗ Corresponding author at: Department of Clinical Pharmacy, College of Pharmacy, Hail University, P.O. Box 6166, Horan Street, Hail 81442, Saudi Arabia. Tel.: +966 505192886. E-mail addresses: [email protected], [email protected] (T.M. Alshammari). http://dx.doi.org/10.1016/j.vaccine.2014.08.061 0264-410X/© 2014 Elsevier Ltd. All rights reserved.
to uncertainty about the effectiveness of the vaccine and fear of its adverse effects [4,5]. However, understanding these barriers is essential to overcoming low compliance with recommendations for vaccination. In our region, few studies have addressed these issues. In 2010, a study has been conducted in one hospital in Saudi Arabia found that there is a poor knowledge of HCPs towards influenza disease and its prevention and there is a misconception towards influenza vaccine among the respondents [5]. Another study has been conducted in the same year in three middle east countries and found there is a lower rate of vaccination among these countries [6]. In Saudi Arabia, there are no specific guideline for HCPs in all health care systems regarding influenza vaccination. However, the ministry of health advises all visitors to perform Hajj and/or Umrah to be vaccinated against seasonal influenza vaccine. Moreover, HCPs who are working during Hajj season are also recommended to get the seasonal influenza
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vaccine [7,8]. This study explored opinions about, knowledge of, and attitudes to seasonal influenza vaccination in HCPs; investigated the percentage of voluntary immunization against influenza vaccine among HCPs in Saudi Arabia and explored why HCPs did not get vaccinated. Strategies to improve influenza vaccination rates in HCPs in Saudi Arabia to make sure those HCPs and their patients are protected from influenza are proposed. 2. Method This study was a cross-sectional study conducted in 6 major governmental and private hospitals in Saudi Arabia. These hospitals included educational and military hospitals. An anonymous, self-administered questionnaire was distributed to HCPs during the 2012–2013 influenza season (between March and May 2013); completion of the questionnaire was voluntary. The study was approved by Medication Safety Research Chair, King Saud University. 2.1. Questionnaire items The questionnaire was composed of five sections. The first section concerned general information about the participant such as gender, professional title and specialty. The second section contained questions that measured attitude to influenza vaccination by asking whether participants routinely got vaccinated against influenza, and their reasons for not getting vaccinated. The third section assessed knowledge about influenza virus transmission, recommended frequency of vaccination and the perceived effectiveness and risks of the vaccine. The fourth section asked about current practice, including whether their workplace offered the influenza vaccine and whether they were interested in participating training related to the influenza vaccine. The final section tested awareness of published guidelines, susceptibility to and risks associated with influenza infections for HCPs, signs and symptoms of influenza infection, potential seriousness of influenza, availability of influenza vaccine in different dosage forms and vaccine properties. The questionnaire was validated and piloted on fifteen HCPs with research experience. Two trained pharmacists were responsible for distributing the questionnaires during visits to the participating hospitals. In some hospitals, the pharmacist interviewed participating HCPs and to obtain answers to the survey questions due to difficulties in these hospitals’ HCPs response; in other hospitals, the questionnaires were sent to the HCPs and completed questionnaires were collected during a revisit five days later. After 3 days a second collection visit was made. The questionnaire was voluntary and accepting in the participation in the study and a returned and complete questionnaire was taken as consent to participate. HCPs who had not completed the questionnaire within this period were considered non-respondents. 2.2. Statistical analysis Descriptive statistics were produced for all survey items. Data were analyzed using SAS version 9.2, the chi-squared test was used for comparisons between categorical variables, and bivariate analysis was used to examine associations between vaccination status and other independent variables. 3. Results A total of 245 questionnaires were randomly distributed in 6 major hospitals in Saudi Arabia with response rate of (98%, n = 242). Comparable numbers of HCPs from the different professions participated (physicians: 31%, pharmacists: 32.41%, nurses: 32%). A rather high proportion of HCPs (61.22%) had not received the influenza
Table 1 Demographic characteristics of participating healthcare professionals (HCPs). Characteristic Gender Male Female Professional title Physician Pharmacist Nurse Laboratory specialist Clinical pharmacist Pharmacy resident Physiotherapist Institution Governmental hospital Private hospital Botha Vaccinated against influenza Yes No a
Number
Percentage
118 127
48.16 51.84
76 75 80 1 6 1 6
31.02 30.61 32.65 0.41 2.45 0.41 2.45
171 72 2
69.80 29.39 0.82
95 150
38.78 61.22
Working in government and private hospitals.
vaccine (Table 1); there are a number of different possible reasons for non-compliance with vaccination among HCPs. Thirty-nine respondents (16%) stated that the vaccine would have a negative influence on their health and make them ill, thirty-two respondents (13%) believed they were not at risk of getting influenza as they were young and healthy. Nineteen respondents (8%) believed that they protected themselves from getting influenza by following all the required precautions e.g. washing hands and covering their nose and mouth when sneezing or coughing (Fig. 1). There was no significant difference in the rate of vaccination in pharmacists and other HCPs (p = 0.14), whilst the rate of vaccination in physicians was lower than for other HCPs (p = 0.03); nurses were the HCP group mostly likely to get vaccinated and had a higher rate of vaccination (p = 0.001). Caution is needed in interpreting these results as the total number of vaccinated HCPs was low. However, the majority of respondents (71%, n = 174) believed that the influenza vaccine is effective in preventing influenza. Of those, 44% have been vaccinated compared to 66% who did not (p = 0.01). Believe in the effectiveness of the vaccine was lower amongst pharmacists than other HCPs (p = 0.01); nurses were most likely to believe the vaccine to be effective, followed by physicians, nurses were more likely than other HCPs to believe the vaccine to be effective (p = 0.01). More than half the HCPs (65%, n = 158) said that Centre for Disease Control (CDC) recommended that they receive the influenza vaccine and the majority of HCPs believed that the influenza vaccine should be administered annually (80%, n = 195), (Table 2). Around 70% (n = 171) of HCPs believed that administration of the influenza vaccine should be part of their medical practice and over 71% (n = 174) of HCPs thought that they were encouraged to get vaccinated to protect them from catching influenza by direct exposure to sick patients, 51% (n = 126) believed that being vaccinated would minimize their sickness absence and loss of productivity and make them more able to take care of their patients. Eighty percent of participating HCPs had not received any training relating to influenza vaccination in the last 12 months; over 69% wanted to take training courses (such as continuing education on importance of influenza vaccine and the benefit of the vaccination) in vaccination. About 29% of the participants did not know whether their institution offered the influenza vaccine, although 50% reported that their institution did offer the influenza vaccine. About one third of the participants reported that they do not provide any information to the patients or public about the importance of influenza vaccination. Over one third (38%, n = 93) believed that influenza vaccination protects vulnerable patients and enhances patient safety during
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The vaccine doesn’t work The vccine is more dangerous than the virus They don’t like needles They can't afford to get the full shot The flu is not serious They do the right aseptic technique They don’t know where to get the full shot Youg & healthy Fear of contracting illness 0%
2%
4%
6%
8% 10% 12% 14% 16% 18%
Fig. 1. HCPs’ reasons for non-compliance with vaccination recommendations.
outbreaks of influenza. Barriers that HCPs believe that prevent them and their institutions from providing the influenza vaccine to some or all their patients and HCPs included, non-availability of vaccine (43%) followed by safety concerns for patients (35%) and for HCPs (33%). In addition, 19% and 13% of the participants think that both limited number of staff and lack of trained staff, respectively, were considered as barriers of not providing influenza vaccine. While, 14% considered cost of the vaccine is an important barrier (Fig. 2). About two thirds (65%, n = 159) of the HCPs were aware of influenza infection, but almost 75% (n = 184) were not aware of the ACIP or CDC guidelines on influenza immunization. Table 3 shows the awareness of HCPs towards influenza and influenza vaccine. About 85% of the respondents believe that influenza is more serious than common cold and 96% of them know the significant symptoms of influenza. Moreover, HCPs 76% of the respondents believe that asymptomatic infected HCPs could still spread the infection to other close people. In addition, 53% of the respondents believe that the influenza vaccine should have the correct mix of virus strains to work effectively. 4. Discussion Our study investigated knowledge of, and attitude to seasonal influenza vaccination in HCPs. Several studies have shown that influenza vaccination is effective in protecting HCPs against infection, minimizing transmission of the disease to their patients and decreasing mortality and morbidity among vulnerable patients;
vaccination also reduced absenteeism and improved the health status of HCPs [9–12]. The results of the present study revealed a low percentage of influenza immunization among HCPs (38%) during the 2012–2013 season despite the ACIP and CDC recommendations and HCPs being at high risk of infection. This rate is similar to that reported in other studies of influenza vaccination in HCPs in Saudi Arabia [5,13]. A cross-sectional study conducted by Rehmania and Memonet with 512 participants found influenza vaccination rate of 34% in the 2008–2009 season [5]. Rates in neighbouring countries have been very variable; a very low influenza vaccination rate was reported from United Arab Emirates (24.7%), but high rates were found in Kuwait (67.2%) and Oman (46.4%) [6]. However, we found no difference between the vaccination rate for pharmacists and other HCPs (p = 0.14), but physicians were less likely to get vaccinated than other HCPs (p = 0.03) and nurses more likely to get vaccinated than other HCPs (p = 0.001). Because the overall rate of vaccination of HCPs was low in our study the results should be interpreted with caution. Similarly to other reports [4–6], our data revealed significant gaps in HCPs’ knowledge about influenza vaccination. The low rate of immunization in HCPs practising in Saudi Arabia seems likely to be related to lack of knowledge and awareness; however this study did not demonstrate a consistent positive correlation between HPCs’ belief in the effectiveness of the influenza vaccine and the decision to be immunized. The results of our study showed that 71.43% of participants believed that influenza vaccine is effective in preventing influenza; nonetheless the self-reported vaccination rate was low. In addition, our
Need for ancillary supplies Need for proper storage of vaccine Training and readiness of staff Cost/reimbursement issues of vaccine Not enough staff to administer vaccine Safety concern for HCPs Safety concern for patients Vaccine is not available 0%
5%
10% 15% 20% 25% 30% 35% 40% 45% 50%
Fig. 2. Barriers to provision of the influenza vaccine in HCP institutions.
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Table 2 Knowledge of health care professionals (HCPs) about the influenza vaccine. Questions Do you think the influenza vaccine is effective in preventing the ‘flu?a Yes No Do you believe that the Centre for Disease Control (CDC) recommends that health care workers receive the’ flu shot?b Yes No I don’t know How often do you think the’ flu vaccine should be administered?c Every 6 months Every year Every 5 years Once in a lifetime Are you aware of the guidelines published by the Advisory Committee on Immunization Practices (ACIP) or Centre for Disease Control (CDC) for influenza immunization? Yes No a b c
Frequency
No. (%)
175 67
71.43 27.35
158 25 61
64.49 10.20 24.90
27 196 12 10
11.02 80 4.9 4.08
56 183
22.86 74.69
3 respondents (1.22%) did not answer this question. 1 respondents (0.41%) did not answer this question. 5 respondents (2.04%) did not answer this question.
data showed variable levels of awareness of and knowledge about influenza vaccination in HCPs (see Tables 2 and 3 for details), broadly in line with other studies [5,14,15]. Most HCPs had basic knowledge of the influenza vaccine and infection and most participating HCPs were aware that people with asymptomatic influenza can transmit influenza (75.5%); a find which contrasts with Khazaeipour et al.’s [16] study in which only 32.4% of HCPs stated that people with asymptomatic influenza can transmit influenza. Previous studies have reported variable rates of belief amongst healthcare workers (HCWs) that the influenza vaccine can cause influenza infection (38.1% to 78%) [14,15]; 48.16% of all respondents in our study shared this misconception. 80% of the participants were aware of the programme of influenza vaccination for HCPs yet 61% % [who may or may not have been aware] declined vaccination. Other studies have reported that in Saudi Arabia about 86% of participants were aware of the ACIP recommendation and in the three Middle East countries – United Arab Emirates, Kuwait and Oman – 48.5% of HCWs were aware of the CDC recommendations for vaccination against seasonal influenza [5,6]; we found much lower awareness of these guidelines: about 74.69% of participating HCPs were not aware of the ACIP or CDC recommendations for influenza immunization. In this study the most commonly reported reasons for non-compliance with vaccination recommendations were fear of contracting illness and concerns about side-effects of the influenza vaccine such as fever, fatigue and myalgia. These findings are consistent with other studies which investigated participants’ main reason for not taking up influenza vaccination. This suggests that vaccination campaigns should include facts about the rate of adverse reactions to the influenza vaccine. Other reasons given by HCPs for non-compliance included the belief that
Table 3 Awareness of healthcare professionals (HCPs) about influenza and the influenza vaccine. Questions
Correct
Incorrect
Health care professionals are less susceptible to influenza infections than other peoplea Number 39 190 15.92 77.55 Percentage Influenza is transmitted primarily by coughing and sneezinga Number 222 13 90.61 5.31 Percentage a Influenza is more serious than a “common cold” Number 210 16 Percentage 85.71 6.53 The signs and symptoms of influenza include fever, headache, sore throat, cough, nasal congestion, and aches and painsa Number 234 5 95.51 2.04 Percentage a HCPs can spread influenza even when they are feeling well Number 185 31 75.51 12.65 Percentage People with influenza can transmit the infection only after their symptoms appeara Number 60 146 24.49 59.59 Percentage Influenza is transmitted primarily by contact with blood and body fluidsa Number 48 162 19.75 66.67 Percentage Influenza vaccination may not work if the vaccine contains the wrong mix of virusesa Number 131 34 53.47 13.88 Percentage The flu shot contains live viruses that may cause some people to get influenzaa Number 118 67 48.16 27.35 Percentage Influenza vaccination does not work in some persons, even if the vaccine has the right mix of virusesa Number 122 35 49.80 14.29 Percentage Adults with influenza commonly experience nausea and vomiting or diarrheaa Number 88 83 35.92 33.88 Percentage a Symptoms typically appear 8–10 days after a person is exposed to influenza Number 96 58 39.18 23.67 Percentage a
2 respondents (0.82%) did not answer this questions.
Not sure 14 5.71 8 3.27 17 6.94 4 1.63 27 11.02 37 15.10 31 12.76 78 31.84 58 23.67 86 35.10 72 29.39 89 36.33
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they were not at risk of getting influenza as they were young and healthy (13%); another study reported a somewhat similar result, with 6.2% of HCPs citing a belief that they were not at risk of infection as their reason for non-compliance with vaccination recommendations [16]. In this study, 43% of participants reported that availability of influenza vaccine was a barrier to their institution offering vaccination; the safety concerns of patients (35%) and HCPs (33%) were also cited as barriers to provision of vaccination to both patients and HCPs. In a study of attitudes and practice relating to influenza vaccination in registered nurses conducted in 4 US states vaccine supply (6%) and safety concerns (39%) were considered barriers to the provision of the influenza vaccination [17]. Awareness of availability of influenza vaccine is sometimes viewed as a barrier to influenza vaccination in HCPs, one study found that 98% of respondents were aware that their institution offered free vaccination [4]; but in our study about 29% of the participants did not know if their institution offered influenza vaccination and only 50% reported that their institution offered influenza vaccine. A lot of work is needed to increase HCPs’ compliance with influenza vaccination recommendations; interventions should include educational campaigns to address misconceptions. Successful vaccination programmes combine publicity and education for HCPs and other potential vaccine recipients, use of reminder and recall systems, assessment of organization-level vaccination rates combined with feedback to staff, and efforts to remove administrative and financial barriers to vaccination. This study has both strengths and limitations. The limitation of this study include that, influenza vaccination status was selfreported by respondents, not subject to independent verification and potentially influenced by social desirability bias. In addition, the results of this study cannot be generalized to other HCPs. Also, our sample size was either similar or smaller than in other studies. However, our study has several strengths; data was collected from 6 major hospitals, including government and private hospitals in order to assess practice in both types of hospital. The response rate for the survey was 98%, higher than that achieved in previously published studies. The majority of respondents were from government hospitals (69.80%). We also examined the vaccination rate according to professional title; this should enable interventions to improve compliance with influenza vaccination recommendations to target the group with the lowest rate of vaccination. 5. Conclusion Despite the recommendations, the percentage of HCPs who receive the influenza vaccine was low in Saudi Arabian hospitals. Concerns about the efficacy and safety of the influenza vaccine, fear of contracting illness, and unavailability of influenza vaccine in some hospitals were significantly associated with noncompliance with vaccination. More efforts by health authorities and
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regulatory in Saudi Arabia are needed to enhance compliance of all HCPs with recommendations for influenza vaccination; all HCPs should be encouraged to get vaccinated and make sure it is available in all hospitals, and special educational and campaign should be used to improve their knowledge and awareness. Conflict of interest There is no conflict of interest to declare. References [1] Pearson ML, Bridges CB, Harper SA. Influenza vaccination of health-care personnel: recommendations of the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006;55:1–16. [2] Song JY, Park CW, Jeong HW, Cheong HJ, Kim WJ, Kim SR. Effect of a hospital campaign for influenza vaccination of healthcare workers. Infect Control Hosp Epidemiol 2006;27:612–7. [3] Dey P, Halder S, Collins S, Benons L, Woodman C. Promoting uptake of influenza vaccination among health care workers: a randomized controlled trial. J Public Health Med 2001;23:346–8. [4] Douville LE, Myers A, Jackson MA, Lantos JD. Health care worker knowledge, attitudes, and beliefs regarding mandatory influenza vaccination. Arch Pediatr Adolesc Med 2010;164:33–7. [5] Rehmani R, Memon JI. Knowledge, attitudes and beliefs regarding influenza vaccination among healthcare workers in a Saudi hospital. Vaccine 2010;28:4283–7. [6] Abu-Gharbieh E, Fahmy S, Rasool BA, Khan S. Influenza vaccination: healthcare workers attitude in three Middle East countries. Int J Mol Sci 2010;7:319–25. [7] Ministry of Health (Saudi Arabia).Health regulations for the 1435HHajj season. 2014. http://www.moh.gov.sa/en/Hajj/News/Pages/News-201404-03-001.aspx [accessed on 23.05.14]. [8] World Health Organization (WHO). Weekly epidemiological record, 30. 2012. p. 277–88. http://www.who.int/wer/2012/wer8730.pdf?ua=1 [accessed on 23.05.14]. [9] Benet T, Regis C, Voirin N, Robert O, Lina B, Cronenberger S, et al. Influenza vaccination of healthcare workers in acute-care hospitals: a case–control study of its effect on hospital-acquired influenza among patients. BMC Infect Dis 2012;12:30. [10] Saxen H, Virtanen M. Randomized, placebo-controlled double blind study on the efficacy of influenza immunization on absenteeism of health care workers. Pediatr Infect Dis J 1999;18:779–83. [11] Carman WF, Elder AG, Wallace LA, McAulay K, Walker A, Murray GD, et al. Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: a randomised controlled trial. Lancet 2000;355:93–7. [12] Benowitz I, Esposito DB, Gracey KD, Shapiro ED, Vazquez M. Influenza vaccine given to pregnant women reduces hospitalization due to influenza in their infants. Clin Infect Dis 2010;51:1355–61. [13] Al-Tawfiq JA, Antony A, Abed MS. Attitudes towards influenza vaccination of multi-nationality health-care workers in Saudi Arabia. Vaccine 2009;27:5538–41. [14] Wicker S, Rabenau HF. Vaccination rates of healthcare workers vary according to their occupational group. Procedia Vaccinol 2011;4:14–8. [15] Nichol KL, Lind A, Margolis KL, Murdoch M, McFadden R, Hauge M, et al. The effectiveness of vaccination against influenza in healthy, working adults. N Engl J Med 1995;333:889–93. [16] Khazaeipour Z, Ranjbarnovin N, Hoseini N. Influenza immunization rates, knowledge, attitudes and practices of health care workers in Iran. J Infect Dev Ctries 2010;4:636–44. [17] Clark SJ, Cowan AE, Wortley PM. Influenza vaccination attitudes and practices among US registered nurses. Am J Infect Control 2009;37:551–6.
