Volume 13, Issue 4 , Pages 476-482, July 2009
Influenza vaccination uptake among students and clinical staff of a university in Iran
Article Outline
Summary
Objective
To identify barriers to our occupational health and safety influenza vaccination program for clinical staff at the Shiraz University of Medical Science.
Methods
Between November 2005 and February 2006, a random stratified sample of 884 healthcare workers (HCWs) from three university teaching hospitals were asked to complete a study questionnaire.
Results
The influenza vaccine uptake rate for the current season was 5.2%. The most common reason for uptake was a belief that the nature of their work made them susceptible to influenza (73%). Reasons for not being vaccinated included: vaccine not available (35%), had little information on vaccine safety (16%), influenza is not a serious disease (14%), and immunization was not needed (13%). HCWs who believed they were at risk of influenza (mean 15.3 vs. 11.1, p
=0.007) and that the vaccine is effective against influenza (mean 16.7 vs. 12.4, p=0.02) had significantly higher knowledge scores compared with others who did not hold these beliefs about their own vulnerability and the efficacy of the vaccine. Males were more likely than females to intend not to be vaccinated next season (OR=2.9, p=0.031), and those vaccinated for the current season were more likely to intend to be vaccinated next season (OR=5.5, p=0.002). HCWs who recommended the vaccine to family/co-workers and to their patients were also more likely (OR=9.8, p=0.000 and OR=2.4, p=0.000, respectively) to intend to be vaccinated next season.
Conclusions
Convenient and free vaccination programs will increase influenza vaccination rates. To protect our HCWs and their patients, we need extensive and sustained efforts to increase HCW awareness about their vulnerability to influenza and the efficacy of the influenza vaccine.
Keywords: Influenza, Vaccination, Healthcare workers
Introduction
Healthcare-associated transmission of influenza has been documented in many different patient populations and clinical settings, including neonatal intensive care, geriatric wards, and long-term care facilities.1, 2, 3, 4, 5, 6 Transmission occurs from patient to patient, visitor to patient, and between the patient and their healthcare worker (HCW), with substantial morbidity and even mortality in the very old and the very young, the immunosuppressed, and those with chronic illnesses.7, 8, 9 Because of the transmission mechanism and incubation period of influenza, healthcare- and occupationally-acquired influenza is often under-recognized, except in the setting of large outbreaks. Influenza immunization has direct and secondary benefits by protecting the HCW from occupationally-acquired infection and the subsequent transmission from HCW to patient and HCW to HCW.
The Advisory Committee for Immunization Practices (ACIP) of the Centers for Disease Control and Prevention (CDC), USA, has strongly recommended annual influenza immunization for HCWs with direct patient contact since 1984,10 and in 199310 extended this recommendation to every HCW.7, 8, 9, 10 In highly resourced healthcare systems, the uptake of immunization in eligible HCWs without contraindications has not yet reached 100% and ranges from 38% to 87%,11, 12, 13, 14, 15, 16 even though the understanding of the benefits of immunization is generally high.11, 12, 13, 14, 15, 16 All Iranian HCWs with clinical responsibilities are advised by the Ministry of Health17 to participate in seasonal influenza vaccination programs that are offered at every staff health clinic in the public hospital system. There are, however, no data available on the annual uptake in the clinical staff of the hospitals of Shiraz, Iran. Our aims were to determine the influenza immunization status of HCWs and to understand the barriers to immunization by assessing related knowledge, attitudes, and behavior of HCWs.
Methods
Setting
Between November 2005 and February 2006, medical, dentistry, midwifery, and nursing students of Shiraz University of Medical Sciences and nurses from three major teaching hospitals of Shiraz University of Medical Sciences with 750, 400, and 202 beds were surveyed. All groups completed the questionnaires while the research assistant waited to collect them in anonymous batches.
Study design
Eight hundred and eighty-four HCWs were identified from a stratified sample and received a self-administered questionnaire. These included 110 fifth-year medical students, 51 sixth-year medical students, 51 interns, 169 medical residents, 102 dentistry students, 40 dentistry residents, 129 nursing students, 65 midwifery students, and 167 nurses.
The questionnaire had been developed previously,11 and was modified to collect information on age, sex, marital status, children aged ≤16 years living at home, uptake of influenza immunization for the 2005–2006 season, previous adverse reaction to influenza immunization, barriers to and facilitators for influenza immunization, perceived benefits of immunization, intention to be immunized, recommendation of the vaccine to family, co-workers, and patients, and 35 influenza immunization-related knowledge items.
Using the set of reasons reported by Toy et al.,11 we compared the reasons commonly given for uptake or not of the influenza vaccine by medical residents from the Iranian healthcare system with those reported by medical residents from the USA, a country with a highly resourced healthcare system.11 Seven reasons given for being immunized included: (1) a belief that they were at risk of influenza due to the nature of their work, (2) to reduce the risk of transmission to patients, (3) a belief that the vaccine is safe and (4) effective, (5) a belief that influenza is a serious disease, (6) they were encouraged by other employees, and (7) they had a chronic illness. Eleven reasons given for not being immunized included: (1) procrastinated/forgot, (2) not interested, (3) not in a high-risk group, (4) not likely to get influenza, (5) the vaccine is not effective, (6) do not like needles, (7) concern about adverse effects, (8) concern about pain and discomfort, (9) influenza is not a serious disease, (10) did not know the vaccine was available, and (11) allergic to the vaccine.
Statistical analysis
Univariate and multivariate analyses were performed using EpiInfo version 6.0 (CDC, Atlanta, GA, USA) and SPSS version 14.0 (SPSS Inc., Chicago, IL, USA). A test of the questionnaire for internal consistency identified a high Cronbach alpha correlation coefficient, r=0.87. The response rates differed by item, hence the frequency distributions were calculated using the denominator for the individual item. Several items were re-categorized as dichotomous variables in preparation for a multiple logistic regression model. The sum of all correct answers to the 35 knowledge items about recommended target populations for immunization that each scored 1, resulted in a continuous variable with a value ranging from 0 to 35. Mean and standard deviations, median and lower and upper quartiles were calculated for the 35-item knowledge scores. Responses for likelihood used a four-point scale for items measuring recommend vaccine to patients, frequency of re-vaccination, and effectiveness of the vaccine, which were recategorized into correct/incorrect. Reasons cited for immunization or no immunization by medical residents in the USA11 and Iran were tested for rank order using the Ridit test. Responses as proportions were compared between groups using the Chi-square or Fisher's exact test. Comparisons between the means of the knowledge score were performed using analysis of covariance (ANCOVA).
Two backwards (non-conditional) stepwise multiple logistic regression analyses were used to identify predictors of (a) not being vaccinated for the season and (b) for intention to be immunized the following season. The model to test intention to be immunized the following season also included being in receipt of the vaccine this season. First-order interaction terms between recommendation to family and co-workers and recommendation to patients were entered. Items not entered into the model because of homogeneity were: hospital offer of vaccine, free vaccine, and health status. Alpha was set at the 5% level.
Results
The majority (96%, 851/884) of the distributed questionnaires were returned – all from the fifth-year medical students, 95% from the sixth-year medical students and interns, 90% from the medical residents and dentistry students, and all from the dentistry residents, nursing students, midwifery students, and nurses. More females responded to the questionnaire (61%) than males, 34% of participants were married, with just over one third (38%) having children ≤16 years of age, and the age of all participants ranged from 18 to 59 years (mean 25.9 years, SD 5.4 years). Nearly all (92%) participants rated their health as good to excellent.
Influenza immunization rate
The influenza immunization rate for the 2005–2006 season was low at 5.2%. The uptake rate was significantly different between the three clinical groups (Chi-square=106.04, p<0.0001), with nurses having the highest rate (21%, 95% CI 15–28%, 35/167) and lower rates in dentistry students (5%, 95% CI 2–11%, 4/82) and medical residents (2%, 95% CI 0.5–5%, 3/152). More than half of the participants did not intend to be vaccinated next season (53%, 95% CI 50–57%, p=0.008) and prior immunization history was uncommon (7%, 95% CI 5–9%). Of those who had a prior immunization history, nearly one quarter (22%, 95% CI 12–35%, 13/58) recalled adverse effects that included myalgia (38%), malaise (31%), fever (23%), and general influenza-like illness (8%).
More participants believed they would recommend the vaccine to their family and co-workers (68%, 95% CI 64–70%, p<0.0001) compared with those who would not. Just over half (54%, 95% CI 51–58%) would recommend the vaccine to their patients compared with HCWs who would not (p=0.0004).
Reasons associated with vaccine uptake and failure to be immunized
The most common reasons given for not being immunized for the season included: vaccine not available (35%, 281/807), had little information on the safety of the vaccine (16%, 133/807), influenza is not a serious disease (14%, 114/807), and immunization is not needed (13%). The most common reason given by immunized participants for being immunized was a belief of being at risk of influenza because of the nature of their work (73%, 32/44), to prevent the risk of transmission to patients (27%, 12/44), the efficacy of the vaccine (25%, 11/44), and influenza is a serious disease (23%, 10/44).
Male HCWs who were not immunized were 65 times (95% CI 39.1–10.7, p<0.0001) more likely to believe they were not at risk of acquiring influenza and 1.4 times (95% CI 1.0–2.0, p=0.033) more likely to believe influenza was not a serious disease compared with non-immunized females. Females who were <31 years of age were 4.7 times (95% CI 2.1–10.4, p<0.0001) more likely to be immunized for the season compared with older females. Age was not associated with uptake in males (p=0.3).
Medical knowledge
The knowledge score for the aggregated 35 items ranged from 0 to 33 (mean 14.1, standard deviation 7.2, median 14, lower quartile 9, upper quartile 19). Mean knowledge scores differed between the healthcare professions. Nursing students, midwifery students, and trained nurses were found to have significantly lower knowledge scores compared with many of their medical colleagues (Table 1). Fifth-year medical students had significantly lower scores than their senior counterparts, medical residents (−4.2, p<0.0001), sixth-year medical students (−4.5, p<0.0001), and interns (−2.8, p=0.018). HCWs who believed they were at risk of influenza because of the nature of their work (mean 15.3 vs. 11.1, p=0.007) and those who believed that the vaccine is effective against influenza (mean 16.7 vs. 12.4, p=0.02) had significantly higher knowledge scores compared with others who did not hold these beliefs about their own vulnerability and the efficacy of the vaccine.
Table 1. The mean difference (p-value) in knowledge score of healthcare workers (columns) compared with their senior and junior colleagues (rows).
| Sixth-year medical student | Intern | Medical resident | Dentistry student | Dentistry resident | Nursing student | Midwifery student | Nurse | |
|---|---|---|---|---|---|---|---|---|
| Fifth-year medical student | −4.5 | −2.8 | −4.2 | 2.8 | −0.8 | 1.2 | 2.1 | 2.1 |
| (<0.0001) | (0.018) | (<0.0001) | (0.005) | (0.548) | (0.185) | (0.053) | (0.043) | |
| Sixth-year medical student | 1.7 | 0.4 | 7.3 | 3.7 | 5.7 | 6.6 | 6.6 | |
| (0.208) | (0.762) | (<0.0001) | (0.012) | (<0.0001) | (<0.0001) | (<0.0001) | ||
| Intern | −1.4 | 5.6 | 2.0 | 4.0 | 4.9 | 4.9 | ||
| (0.238) | (<0.0001) | (0.163) | (0.001) | (<0.0001) | (<0.0001) | |||
| Medical resident | 6.9 | 3.4 | 5.4 | 6.3 | 6.3 | |||
| (<0.0001) | (0.006) | (<0.0001) | (<0.0001) | (<0.0001) | ||||
| Dentistry student | −3.6 | −1.6 | −0.7 | −0.7 | ||||
| (0.008) | (0.106) | (0.563) | (0.513) | |||||
| Dentistry resident | 2.0 | 2.9 | 2.9 | |||||
| (0.136) | (0.046) | (0.022) | ||||||
| Nursing student | 0.9 | 0. 9 | ||||||
| (0.387) | (0.375) | |||||||
| Midwifery student | −0.01 | |||||||
| (0.992) |
Population groups recommended to receive the influenza vaccine
Just over a half of all participants knew that the CDC recommended immunization for physicians and nurses or for persons aged ≥50 years and other risk groups (Table 2).
Table 2. Percentage of target populations correctly identified by healthcare professions as recommended by the CDC to receive the influenza immunization.
| Populations | Percentage (n) | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Fifth-year medical student N=106 | Sixth-year medical student N=48 | Intern N=50 | Medical resident N=150 | Dentistry student N=92 | Dentistry resident N=40 | Nursing student N=121 | Midwifery student N=65 | Nurse N=160 | All HCWs | |
| Persons ≥50 years of age | 54 (57) | 77 (37) | 62 (31) | 73 (109) | 36 (33) | 50 (20) | 46 (56) | 35 (23) | 50 (80) | 54 (446) |
| Households with high-risk patient | 33 (35) | 60 (29) | 54 (27) | 41 (62) | 48 (44) | 60 (24) | 59 (71) | 40 (26) | 59 (95) | 50 (413) |
| Physicians and nurses | 57 (60) | 60 (29) | 62 (31) | 53 (79) | 48 (44) | 67 (27) | 59 (71) | 46 (30) | 72 (115) | 58 (486) |
| Long-term care residents | 42 (45) | 65 (31) | 58 (29) | 62 (93) | 38 (35) | 60 (24) | 27 (33) | 34 (22) | 38 (60) | 45 (372) |
| Patients with: | ||||||||||
| Asthma | 41 (43) | 50 (24) | 54 (27) | 65 (98) | 21 (19) | 32 (13) | 35 (42) | 26 (17) | 39 (63) | 42 (346) |
| Chemotherapy | 38 (40) | 60 (29) | 56 (28) | 47 (70) | 16 (15) | 35 (14) | 30 (36) | 25 (16) | 32 (51) | 36 (299) |
| HIV/AIDS | 46 (49) | 69 (33) | 68 (34) | 50 (75) | 22 (20) | 37 (15) | 29 (35) | 34 (22) | 31 (50) | 40 (333) |
| Long-term steroids | 45 (48) | 71 (34) | 62 (31) | 52 (78) | 21 (19) | 47 (19) | 25 (30) | 20 (13) | 29 (46) | 38 (318) |
| COPD | 48 (51) | 65 (31) | 64 (31) | 81 (122) | 28 (26) | 40 (16) | 35 (42) | 28 (18) | 38 (61) | 48 (398) |
| Diabetes | 35 (37) | 50 (24) | 44 (22) | 51 (77) | 27 (25) | 35 (14) | 25 (30) | 21 (14) | 25 (40) | 34 (283) |
| Congestive heart failure | 14 (15) | 33 (16) | 38 (19) | 60 (90) | 14 (13) | 2 (1) | 16 (20) | 21 (14) | 24 (38) | 27 (226) |
| Renal failure | 22 (23) | 33 (16) | 36 (18) | 55 (83) | 13 (12) | 10 (4) | 14 (17) | 18 (12) | 20 (32) | 26 (217) |
Compared with medical residents in the USA,11 close to half or fewer of the Iranian medical residents identified physicians and nurses (88% US medical residents vs. 53% Iranian medical residents, p<0.001), patients with cancer (81% vs. 47%, p<0.001), patients with HIV (81% vs. 50%, p<0.001), women in their third trimester of pregnancy (60% vs. 18%, p<0.001), household members of high-risk patients (81% vs. 41%, p<0.001), and patients with diabetes (79% vs. 51%, p=0.01) as requiring immunization (Table 3).
Table 3. Percentage of medical residents in the USA and Iran correctly recognizing the identified target populations recommended by the CDC to receive the influenza immunization.
| % | p-Value | ||
|---|---|---|---|
| USAa | Iran | ||
| Persons ≥50 years of age | 93 | 73 | 0.003 |
| Households with high-risk patients | 81 | 41 | <0.001 |
| Physicians and nurses | 88 | 53 | <0.001 |
| Long-term care residents | 93 | 62 | <0.001 |
| Patients with: | |||
| Asthma | 86 | 65 | 0.008 |
| Chemotherapy | 81 | 47 | <0.001 |
| HIV/AIDS | 81 | 50 | <0.001 |
| Long-term steroids | 81 | 52 | <0.001 |
| Diabetes | 79 | 51 | 0.01 |
| Congestive heart failure | 77 | 60 | 0.04 |
| Renal failure | 72 | 55 | 0.04 |
| In third trimester of pregnancy | 60 | 18 | <0.001 |
| Anemia | 49 | 39 | 0.23 |
aToy WC, Janosky JE, Laird SB. Influenza immunization of medical residents: knowledge, attitudes, and behaviors. Am J Infect Control 2005;33:473–5. |
The rank order for the reasons cited by medical residents in Iran and the USA for being immunized were significantly different (p=0.001; Table 4). The top three reasons cited by the US medical residents for being immunized included a belief that they were at risk due to the nature of their work (80%), that immunization reduces the risk of transmission to patients (68%), and that the influenza vaccine is generally safe (56%). The second and third top reasons cited by medical residents in Iran included influenza vaccine is effective (67%) and influenza is a serious disease (67%). None of the Iranian medical residents were immunized because it reduces the risk of transmission to their patients (68% vs. 0%, p=0.05).
Table 4. Reasons for and against immunization cited by the medical residents of Iran and the USA.
| USAa % (n/N) | Iran % (n/N) | Rank order p-value | |
|---|---|---|---|
| Reasons for being immunized: | p=0.001 | ||
| Belief in being at risk because of nature of their work | 80 (20/25) | 67 (2/3) | |
| Reducing risk of transmission to patients | 68 (15/25) | 0 (0/3) | |
| Influenza vaccine generally safe | 56 (14/25) | 33 (1/3) | |
| Influenza vaccine is effective | 36 (9/25) | 67 (2/3) | |
| Flu is a serious disease | 28 (7/25) | 67 (2/3) | |
| Encouraged by other employees | 24 (6/25) | 0 (0/3) | |
| Chronic illness | 4 (1/25) | 0 (0/3) | |
| Reasons for not being immunized: | p=0.001 | ||
| Procrastinated/forgot | 44 (8/18) | 9 (13/149) | |
| Not interested | 17 (3/18) | 11 (16/149) | |
| Not in high-risk group | 17 (3/18) | 20 (30/149) | |
| Not likely to get the flu | 17 (3/18) | 7 (11/149) | |
| Vaccine is not effective | 11 (2/18) | 10 (15/149) | |
| Do not like needles | 11 (2/18) | 5 (7/149) | |
| Concerns about adverse effects | 11 (2/18) | 8 (3/149) | |
| Concerns about pain and discomfort | 11 (2/18) | 4 (6/149) | |
| Flu is not a serious disease | 11 (2/18) | 21 (31/149) | |
| Did not know it was available | 6 (1/18) | 31 (46/149) | |
| Allergic to the vaccine | 6 (1/18) | 2 (3/149) | |
aToy WC, Janosky JE, Laird SB. Influenza immunization of medical residents: knowledge, attitudes, and behaviors. Am J Infect Control 2005;33:473–5. |
The reasons given by medical residents in the USA and Iran for not being immunized were significantly (p=0.001) different. Procrastination or forgetting was the primary reason cited by medical residents in the USA (44%), while Iranian medical residents cited unavailability of the vaccine (31%), influenza is not a serious disease (21%), and that they were not in a high risk group (20%) (Table 4).
Results of multiple logistic regression analysis
Six iterations using backward algorithms identified the final model for intention not to be vaccinated against influenza this season. Male clinical staff were 2.9 times (95% CI 1.1–7.5, p=0.031) more likely than female staff to intend not to be vaccinated. Staff who did not intend to be vaccinated next season were 7.6 times (95% CI 2.9–19.7, p=0.000) more likely to not be immunized this season (Table 5).
Table 5. Multiple logistic regression models to identify predictors of non-immunization behavior and predictors of intention to be immunized next season.
| Significant predictors | β | SE (β) | OR | 95% CI | p-Value |
|---|---|---|---|---|---|
| Final model for not being vaccinated this season: | |||||
| Do not intend to be vaccinated next season | 2.03 | 0.484 | 7.6 | 2.9–19.7 | 0.000 |
| Male | 1.05 | 0.489 | 2.9 | 1.1–7.5 | 0.031 |
| Final model for intention to receive a vaccine next season: | |||||
| Received vaccine this season | 1.71 | 0.54 | 5.5 | 1.9–16.1 | 0.002 |
| Recommended vaccine to family and co-workers | 2.28 | 0.24 | 9.8 | 6.1–15.8 | 0.000 |
| Recommended vaccine to patients | 0.88 | 0.20 | 2.4 | 1.6–3.6 | 0.000 |
| Knowledge | 0.02 | 0.01 | 1.01 | 1.0–1.03 | 0.022 |
Five iterations identified the final model for intention to be immunized next season (Table 5); staff who had been immunized this season (OR 5.5, p=0.002), those who recommend the vaccine to family/co-worker (OR 9.8, p=0.000), those who recommend vaccine to patients (OR 2.4, p=0.000), and those with correct knowledge about the target populations for immunization (OR 1.01, p=0.022).
Discussion
A basic lack of knowledge about the benefits and side effects of the vaccine were the main barriers to vaccination. Most HCWs were unaware of the availability of the vaccine (consistent with other studies12, 14), believed they did not need to be immunized, and believed that influenza was not a potentially serious disease to themselves, their co-workers, or their patients. The vaccination rate in our HCWs was lower than the recommended rate in Iran,17 the USA,1 and rates reported elsewhere.11, 12, 13, 14, 15, 16 The rate in medical residents was seriously poorer than the 38%14 to 58%11 reported in medical training placements at higher resourced hospitals, while the rate in nurses was higher than elsewhere.12 Where vaccination has been free, the rate has been high,12, 14 and freely available vaccination given to our nurses in the neonatal intensive care unit and pediatric wards may have facilitated uptake. Knowledge about who should be immunized, marital status, having children <16 years of age, ward type, or shift pattern were not significant predictors of immunization in either our study or others.10, 11, 12
Our finding that HCWs are motivated to be immunized because their work increases their risk of influenza rather than by the need to reduce the risk of transmission to their patients concurs with other studies.11, 12, 13, 14, 15, 16 Procrastination,11 doubt about effectiveness of the vaccine,13 or lack of time14, 16, 18 did not feature prominently.
Males who had not directly related themselves to the benefits of the program failed to be immunized. Improving factors associated with a positive personal experience of immunization is key to uptake. Previously immunized HCWs (possibly those spared from influenza) were nearly six times more likely to intend to be immunized again, nearly 10 times more likely to recommend immunization to family and colleagues, and twice as likely to recommend immunization to their patients. Recommendation of the vaccine to patients will be improved as uptake in HCWs improves. To increase uptake in junior staff we should start with extensive and sustained campaigns aimed at improving senior medical and senior nursing staff understanding of their vulnerability to influenza, the efficacy of the vaccine, and their role in the transmission of influenza to patients.
Acknowledgement
Our study was funded by the Deputy of Research at the Shiraz University of Medical Sciences.
Conflict of interest: No conflict of interest to declare.
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PII: S1201-9712(08)01537-3
doi:10.1016/j.ijid.2008.09.013
© 2008 International Society for Infectious Diseases. Published by Elsevier Inc. All rights reserved.
Volume 13, Issue 4 , Pages 476-482, July 2009
