Abstract
Purpose
This study aimed to evaluate clinical pharmacist’s contribution to the pneumococcal vaccination rate by providing education to cancer patients in hospital settings.
Methods
This study was conducted in 2 tertiary-care hospitals’ medical oncology outpatient clinics. Patients over 18 years of age and diagnosed with cancer for less than 2 years, in remission stage, and have not previously received the pneumococcal vaccine were included. Patients were randomized to intervention and control groups. The intervention group was provided vaccination education and recommended to receive the PCV13 vaccine. The control group received routine care.
Patients’ knowledge about pneumonia/pneumococcal vaccine, Vaccine Attitude Examination Scale (VAX) score, and vaccination rates were evaluated at baseline and 3 months after the education.
Results
A total of 235 patients (intervention: 117, control: 118) were included. The mean age ± SD was 57.86 ± 11.88 years in the control and 60.68 ± 11.18 years in the intervention groups. The numbers of correct answers about pneumonia/pneumococcal vaccine (p = 0.482) and VAX scores (p = 0.244) of the groups were similar at baseline. After the intervention, the median (IQR) number of correct answers in intervention group [10(3)] was higher than control group [8(4)] (p < 0.001). After the education, the total VAX score (mean ± SD) was less in intervention group (33.09 ± 7.018) than the control group (36.07 ± 6.548) (p = 0.007). Three months after the education, 20.2% of the patients in the intervention and 6.1% in the control groups were vaccinated with pneumococcal vaccine (p = 0.003).
Conclusions
The pneumococcal vaccination rate in cancer patients has increased significantly by the education provided by a clinical pharmacist in hospital settings.
Supplementary Information
The online version contains supplementary material available at 10.1007/s00520-023-07652-3.
Keywords: Cancer patients, Clinical pharmacist, Patient education, Pneumococcal vaccine, Vaccination rates
Introduction
Immunosuppressive treatments lead cancer patients to become vulnerable to infections. Among the infections, pneumococcal diseases caused by Streptococcus pneumonia have shown high morbidity and mortality rates, in which invasive pneumococcal disease is seen 23–38 times more frequently in cancer patients than healthy individuals [1, 2]. Pneumonia causes hospitalization in 10% of cancer patients and the risk exceeds 30% during cancer treatment, particularly with hematological malignancies [2]. The Infectious Diseases Society of America (IDSA) and the Advisory Committee on Immunization Practices (ACIP) recommend pneumococcal vaccines for cancer patients to prevent pneumococcal diseases [3, 4].
Thirteen-valent pneumococcal conjugate vaccine (PCV13) and 23-valent polysaccharide pneumococcal vaccine (PSV23) have been successfully used in childhood vaccination programs in many countries within the framework of World Health Organization (WHO)’s immunization policies; however, the intended targets for vaccination rates in adults, including patients with cancer, have not been reached yet [5–7]. A study conducted in the USA indicated that only 4.8% of 216,658 cancer patients had been vaccinated with the pneumococcal vaccine in 2007 [6]. Another study that included patients over 75 years with a diagnosis of cancer has shown the rate of vaccination with pneumococcal vaccine as 5.5% [8]. Similar vaccination rates for the pneumococcal vaccine have been reported as 4.2–7.4% in patients with cancer in Turkey [9, 10].
Pharmacists, mainly those who work in community settings, have an essential role in increasing adult vaccination rates. Community pharmacists are authorized to administer vaccines in the USA, Europe, and Australia, and the implementation of vaccination in pharmacies has increased adult vaccination rates [11]. In countries where pharmacists are not authorized to vaccinate, studies have shown that vaccination rates can be increased through the provision of education and information by pharmacists to the public [12, 13].
This study aimed to evaluate a clinical pharmacist’s contribution to the pneumococcal vaccination rate by providing education and information to patients with cancer in hospital settings.
The main outcome measures were changes in the patients’ knowledge about pneumonia and the pneumococcal vaccine, patients’ VAX Scale scores, and vaccination rates after the provision of education. The secondary outcome was to determine the factors affecting pneumococcal vaccination behavior in patients.
Material and methods
Design and settings
This study was conducted in 2 tertiary-care hospitals’ medical oncology outpatient clinics between July 2019 and February 2021. One hospital is in the capital city and has a 160-bed capacity with 80,000 admissions annually. The other hospital is in the eastern part of the country and serves as a regional hospital, with 217 beds. The study was approved by the University Non-Clinical Trials Ethics Committee (GO-19–681).
Randomization
Patients who met the inclusion criteria were assigned to the intervention group (provided face-to-face education on the vaccine) and the control group (received standard care) using a simple randomization method by a clinical pharmacist. The patients with an even number of medical files were assigned to the intervention group and the patients with an odd number of medical files were assigned to the control group. After randomization, a clinical pharmacist administered the questionnaires to the patients in both groups for baseline assessments.
Patients
An equal number of patients were recruited from each hospital. The patients who attend medical oncology outpatient clinics, are over 18 years of age and diagnosed with cancer for less than 2 years, in remission stage (which is confirmed by a medical oncologist), and have not previously received the pneumococcal vaccine were included in the study. Patients who could not communicate in Turkish, were illiterate, had visual/auditory/cognitive impairments, had previously received a pneumococcal vaccine recommendation, and did not know their pneumococcal immunization status were excluded. All patients who volunteered to participate in the study have signed an informed consent form. The demographics and medical information were obtained from the patients’ medical files and hospital information systems. The patients were invited to participate in the study by a clinical pharmacist after consulting with a medical oncologist at routine outpatient visits. Medical oncologists referred eligible patients to be interviewed with a clinical pharmacist in a private room.
Study sample
The pneumococcal vaccination rate was previously found to be 7.4% in cancer patients who attend a medical oncology clinic in Turkey [9]. Therefore, this study considered a twofold increase in vaccination rates for the target (15% increase in vaccination rates compared to the control group). The sample size was calculated with a 90% power and 5% error level and was led to have a minimum of 114 patients per group.
The tools used for the evaluation
Two questionnaires were developed for this study. The patients’ vaccination status was assessed by the Vaccination Status Questionnaire (VSQ) (that consists of 17 questions with multiple choices; supplement-1), and patients’ knowledge on pneumonia and pneumococcal vaccine were evaluated by the Vaccination Knowledge Questionnaire (VKQ) (that consists of 13 questions to be answered as “yes/no/unknown”; Table 3). The researchers created these structured questionnaires based on previous studies in the literature and tested their content validity on 20 patients who attended medical oncology outpatient clinics prior to the study.
Table 3.
Patients’ knowledge about vaccines before and after the education [control (n = 114) and intervention (n = 114)]
| Baseline, n (%) | After education, n (%) | |||||
|---|---|---|---|---|---|---|
| Control group | Intervention group | p value | Control group | Intervention group | p value | |
| 1. Vaccine is a solution containing weakened or killed disease microbe, protecting the person from infectious diseases | 0.790 | 0.004 | ||||
|
True False Do not know |
63(55.26) 0 (0.00) 51(44.74) |
65 (57.02) 0 (0.00) 49 (42.98) |
69 (60.53) 0 (0.00) 45 (39.47) |
89 (78.07) 0 (0.00) 25 (21.93) |
||
| 2. An adult younger than 65 years old with diabetes does not need a pneumococcal vaccine | 0.575 | 0.003 | ||||
|
True False Do not know |
8 (7.02) 20 (17.54) 86 (75.44) |
12 (10.53) 22 (19.30) 80 (70.17) |
9 (7.89) 23 (20.18) 82 (71.93) |
4 (3.51) 46 (40.35) 64 (56.14) |
||
| 3. Those with chronic heart, lung, liver disease, and diabetes are not at risk in terms of being infected with pneumonia | 0.137 | 0.021 | ||||
|
True False Do not know |
11 (9.65) 55 (48.25) 48 (42.10) |
6 (5.26) 69 (60.53) 39 (34.21) |
11 (9.65) 72 (63.16) 31 (27.19) |
6 (5.26) 91 (79.82) 17 (14.91) |
||
| 4. 65 years and older is a risky group in terms of being infected with pneumonia | 0.388 | 0.002 | ||||
|
True False Do not know |
78 (68.42) 7 (6.14) 29 (25.44) |
84 (73.68) 3 (2.63) 27 (23.69) |
91 (79.83) 7 (6.14) 6 (5.26) |
106 (92.98) 0 (0.00) 8 (7.02) |
||
| 5. Those whose immune system is suppressed are a risky group in terms of being infected with pneumonia | 0.280 | 0.046 | ||||
|
True False Do not know |
77 (67.54) 6 (5.26) 31 (27.2) |
75 (65.79) 2 (1.75) 37 (33.26) |
91 (79.82) 2 (1.75) 19 (18.43) |
103 (90.35) 0 (0.00) 11 (9.65) |
||
| 6. Pneumococcal vaccine is administered only to individuals aged 65 and over | 0.533 | 0.030 | ||||
|
True False Do not know |
2 (1.75) 55 (48.25) 57 (50.00) |
55 (4.39) 6 (49.12) 53 (46.49) |
4 (3.51) 62 (54.39) 48 (42.10) |
2 (1.75) 81 (71.05) 34 (27.20) |
||
| 7. Pneumonia is a vaccine preventable disease | 0.273 | <0.001 | ||||
|
True False Do not know |
46 (40.35) 14 (12.28) 54 (47.37) |
48 (42.11) 7 (6.14) 59 (51.75) |
67 (58.77) 7 (6.14) 40 (35.09) |
94 (82.46) 1 (0.88) 19 (16.66) |
||
| 8. Pneumonia is a serious disease | 0.895 | 1.000 | ||||
|
True False Do not know |
109 (95.61) 2 (1.75) 3 (2.64) |
107 (93.87) 2 (1.75) 5 (4.38) |
110 (96.49) 1 (0.88) 3 (2.63) |
111 (97.37) 0 (0.00) 3 (2.63) |
||
| 9. Pneumonia is transmitted by sneezing and coughing | 0.405 | <0.001 | ||||
|
True False Do not know |
56 (49.12) 23 (20.18) 35 (30.70 |
66 (57.89) 20 (17.54) 28 (24.57) |
56 (49.12) 29 (25.44) 29 (25.44) |
85 (74.56) 17 (14.91) 12 (10.53) |
||
| 10. A person with asthma cannot be vaccinated | 1.00 | 0.354 | ||||
|
True False Do not know |
9 (7.89) 25 (21.93) 80 (70.18) |
9 (7.89) 25 (21.93) 80 (70.18) |
5 (4.39) 32 (28.07) 77 (67.54) |
8 (7.02) 39 (34.21) 67 (58.77) |
||
| 11. Mild side effects such as pain, swelling, and redness may occur at injection site of the vaccine | 0.788 | 0.007 | ||||
|
True False Do not know |
93 (81.58) 6 (5.26) 15 (13.16) |
97 (85.09) 1 (0.88) 16 (14.03) |
93 (81.58) 6 (5.26) 15 (13.16) |
108 (94.74) 1 (0.88) 5 (4.38) |
||
| 12. Vaccines have serious side effects | 0.319 | 0.008 | ||||
|
True False Do not know |
34 (29.82) 22 (19.30) 58 (50.88) |
34 (29.82) 31 (27.19) 49 (57.01) |
29 (25.44) 29 (25.44) 56 (49.12) |
19 (16,67) 51(44.74) 44 (38.59) |
||
| 13. Flu vaccine (influenza vaccine) and pneumococcal vaccine are free of charge for those over the age of 65, those with chronic diseases, and those with suppressed immune systems | 0.364 | <0.001 | ||||
|
True False Do not know |
44 (38.60) 8 (7.02) 62 (54.39) |
35 (30.70) 12 (10.53) 67 (41.23) |
47 (41.23) 11 (9.65) 56 (49.12) |
81 (71.05) 5 (4.38) 28 (24.57) |
||
The Vaccination Attitudes Examination Scale
The scale was developed to evaluate the general vaccination attitudes of the patients by Martin et al. [14], and the Turkish validity and reliability studies were conducted by Yildiz et al. [15] (Cronbach alpha = 0.818). This scale consists of 12 items and four subgroups (mistrust of vaccine benefit, worries about unforeseen future effects, concerns about commercial profiteering, and preference for natural immunity) to be responded on a 6-point Likert scale, and the total score ranges between 12 and 72. The higher scores indicate the anti-vaccination attitudes of the patients. The Vaccination Attitudes Examination (VAX) Scale is categorized according to the total score as 12–31 (low negative attitude), 32–51 (moderate negative attitude), and 52–72 (high negative attitude), and according to the subgroups score as 3–7 (low negative attitude), 8–12 (moderate negative attitude), and 13–18 (high negative attitude), respectively. Two questionnaires and the scale were administered to the patients in the control and intervention groups before and 3 months after education provision.
Provision of education by a clinical pharmacist (intervention)
The educational content was developed based on literature and expert perspectives and included general information about immunization, pneumonia, pneumococcal vaccines, and misconceptions about vaccines. This information was first provided verbally, and booklets containing the same information were given to the patients in the intervention group afterward. The PCV13 vaccine was recommended to the patients based on IDSA, ACIP, and national adult immunization guidelines. Patients in the intervention group were followed up by telephone call 3 months after the education and asked about their vaccination status, and the VKQ and VAX Scale were administered.
The control group did not receive verbal or written information from a clinical pharmacist at baseline; however, they received routine information and counseling by a medical oncologist and were followed by a clinical pharmacist on the phone to identify vaccination status, to administer VKQ and VAX Scale at 3 months.
After completing the randomized controlled phase of the study, the clinical pharmacist called the unvaccinated patients in the intervention group monthly to remind them to get the vaccine (two reminder calls). The control group’s unvaccinated patients were given education over the phone (with the same content of the face-to-face education). Their vaccination status was questioned 3 months after the education provided on the telephone. The control group received two reminder calls at monthly intervals as well.
Statistical analysis
Data were analyzed using IBM SPSS Statistics for MacOS, version 26.0 (IBM Corp., Armonk, NY, USA). Categorical variables were presented as numbers and percentages, whereas continuous variables were presented as median with an interquartile range (IQR) or mean with standard deviation (SD) according to the data distribution. Pearson chi-square, Fisher exact test, and Yates continuity correction tests were used to compare categorical variables. For continuous variables, if the data are normally distributed independent t-test was used to compare the means of two independent groups; if not, the Mann–Whitney U test or Kruskal–Wallis test was used. A p-value of < 0.05 was considered statistically significant. Cronbach’s alpha coefficient was calculated for the reliability analysis of the VAX Scale. For logistic regression, variables with a p-value of < 0.25 were included in the model.
Results
A total of 235 patients (intervention group: 117, control group: 118) were included in the study (Fig. 1). Four patients in the control group and three in the intervention group could not be reached after 3 months of follow-up; therefore, 228 patients were included and analyzed. The mean age ± SD was 57.86 ± 11.88 years in the control group and 60.68 ± 11.18 years in the intervention group (p = 0.067). The common types of cancer in the control/intervention groups were breast (35.95% and 46.49%), lung (14.04% and 14.91%), and colon (14.04% and 10.53%), respectively (Table 1).
Fig. 1.
Flow diagram of the study (CONSORT 2010)
Table 1.
Characteristics of the patients (n = 228)
| n (%) | |||
|---|---|---|---|
| Control group | Intervention group | p value | |
| Gender | 0.683 | ||
|
Female Male |
69 (60.53) 45 (39.47) |
72 (63.16) 42 (36.84) |
|
| Educational status | 0.322 | ||
|
Literate Primary school Secondary school High school Bachelor degree/Master degree |
11 (9.65) 47 (41.23) 15 (13.16) 21 (18.42) 20 (17.54) |
18 (15.79) 49 (42.98) 12 (10.53) 18 (15.79) 17 (14.91) |
|
| Monthly income (€) | 0.865 | ||
|
< 203 204–254 255–356 357–509 > 510 |
39 (34.21) 25 (21.93) 16 (14.04) 21 (18.42) 13 (11.40) |
40 (35.09) 25 (21.93) 21 (18.42) 17 (14.91) 11 (9.65) |
|
| Area of living | 0.766 | ||
|
Province District Rural |
78 (68.42) 21 (18.42) 15 (13.16) |
78 (68.42) 24 (21.05) 12 (10.53) |
|
| Smoking status | 0.353 | ||
|
Smoker Non-smoker |
20 (17.54) 94 (82.46) |
14 (12.28) 100 (87.72) |
|
| Alcohol use | 0.106 | ||
|
Yes No |
8 (7.02) 106 (92.98) |
2 (1.75) 112 (98.25) |
|
| Cancer diagnosis | 0.739 | ||
|
Breast Lung Colon Stomach Lymphoma Rectum Others |
41(35.95) 16 (14.04) 16 (14.04) 8 (7.02) 7 (6.14) 3 (2.63) 23 (20.18) |
53 (46.49) 17 (14.91) 12 (10.53) 7 (6.14) 6 (5.26) 3 (2.63) 16 (14.04) |
|
| Have received chemotherapy | 0.601 | ||
|
Yes No |
92 (80.70) 22 (19.30) |
96 (84.21) 18 (15.79) |
|
| Have received radiotherapy | 0.033 | ||
|
Yes No |
44 (38.60) 70 (61.40) |
60 (52.63) 54 (47.37) |
|
| Have previous oncological surgery | 0.577 | ||
|
Yes No |
95 (83.33) 19 (16.67) |
99 (86.84) 15 (13.16) |
|
| Comorbidities | 0.106 | ||
|
Yes No |
61(53.51) 53 (46.49) |
74 (64.91) 40 (35.09) |
|
| Presence of risk factors in the family* | 1.000 | ||
|
Yes No |
82 (71.93) 32 (28.07) |
82 (71.93) 32 (28.07) |
|
| Presence of chronic diseases for indication of pneumococcal vaccine | (n = 61) | (n = 74) | 0.309 |
|
Yes No |
43 (70.49) 18 (29.51) |
44 (59.46) 30 (40.54) |
|
*The definition of risk indicates that people who are likely to be infected with respiratory tract infections: such as newborn, < 5 years old child, immunocompromised person, person with chronic disease, or aged > 65 years
There was no difference between the groups of patients at baseline in terms of demographics and past medical histories, except having the previous radiotherapy.
Patients’ general opinions on vaccination in intervention and control groups were not different (p > 0.05). Almost half of the patients in both the intervention group (n = 51, 44.74%) and the control group (n = 50, 43.86%) had previously encountered anti-vaccine attitudes. Only 42.11% (n = 48) of patients in the intervention group and 41.23% (n = 47) in the control group were previously recommended to be vaccinated with any vaccine. Sixty-four (56.14%) patients in the intervention group and 71 (62.28%) patients in the control group had been vaccinated with at least one vaccine during adult life. Only 14.91% (n = 17) of patients in the intervention group and 16.67% (n = 19) in the control group had been vaccinated with influenza vaccine in the previous influenza season.
In the construct validity analyzes for the Vaccine Attitude Scale, CMIN/DF value was calculated as 2.437, CFI value 0.912, NFI value 0.862, GFI value 0.913, and RMSEA value 0.08. It was found that the model showed a good fit. VAX Scale’s Cronbach’s alpha value was 0.717 (good reliability) and the intraclass correlation coefficient of the test–retest analysis was found to be 0.91 (high reliability). The baseline total scores [median (IQR)] of the scale were 36 (8) in the control group and 36 (10) in the intervention group (p = 0.244). Three months after the educational intervention, the total score (mean ± SD) was 36.07 ± 6.548 in the control group and 33.09 ± 7.018 in the intervention group (p = 0.007).
Degree of negative attitudes (categorized as low, moderate, and high, respectively) identified by the total score of VAX Scale was not changed after the provision of education in the intervention (before: 24.56%, 71.93%, 3.51%; after: 34.21%, 65.79%, and 0%) and control groups (before: 21.05%, 77.19%, 1.76%; after: 22.81%, 76.32%, and 0.87%) (p = 0.106). Table 2 shows the degree of negative attitudes indicated by VAX Scale subgroups for the intervention and control groups before and after the education. There was a difference in the “preference for natural immunity” subgroup between the intervention and control groups before the education provided (p = 0.034). Following the education, there was a significant difference in the subgroups of “worries about unforeseen future effects” between the intervention and control groups (p = 0.001).
Table 2.
Degree of attitudes identified by the VAX Scale subgroups among the patients before and after the education
| Baseline, n (%) | After education, n (%) | |||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Intervention group | Control group | p value | Intervention group | Control group | p value | |||||||||
| Scale subgroups | Low | Moderate | High | Low | Moderate | High | Low | Moderate | High | Low | Moderate | High | ||
| Mistrust of vaccine benefit | 84 (73.68) | 24 (21.05) | 6 (5.27) | 82 (71.92) | 26 (22.81) | 6 (5.27) | 0.888 | 91 (79.82) | 21 (18.42) | 2 (1.76) | 83 (72.81) | 23 (20.17) | 8 (7.02) | 0.223 |
| Worries about unforeseen future effects | 5 (4.39) | 71 (62.28) | 38 (33.33) | 6 (5.27) | 71 (62.28) | 37 (32.45) | 0.949 | 5 (4.39) | 91 (79.82) | 18 (15.79) | 5 (4.39) | 67 (58.77) | 42 (36.84) | 0.001 |
| Concerns about commercial profiteering | 62 (54.39) | 42 (36.84) | 10 (8.77) | 68 (59.65) | 37 (32.46) | 9 (7.89) | 0.724 | 75 (65.79) | 38 (33.33) | 1 (0.88) | 65 (57.02) | 45 (39.47) | 4 (3.51) | 0.212 |
| Preference for natural immunity | 27 (23.69) | 42 (36.84) | 45 (39.47) | 17 (14.91) | 61 (53.51) | 36 (31.58) | 0.034 | 30 (26.32) | 56 (49.12) | 28 (24.56) | 17 (14.91) | 68 (59.65) | 29 (25.44) | 0.088 |
No difference was observed in the mean ± SD numbers of correct answers in the VKQ between the patients in the control (6.54 ± 2.63) and the intervention (6.83 ± 2.75) groups at baseline (p = 0.482). After the provision of education, the median (IQR) number of the correct answers in the intervention group [10 (3)] was higher compared to the control group [8 (4)] (p < 0.001) (Table 3).
Regarding the vaccination rates, 20.2% (n = 23) and 6.1% (n = 7) of the patients in the intervention and the control group were vaccinated with the PCV13 vaccine at 3-month follow-up, respectively (p = 0.003). After the education provided by telephone, 14.1% of unvaccinated patients (n = 14) in the control group were vaccinated. Patients who received face-to-face education (intervention group) had a higher vaccination rate (20.2%) than patients who received telephone education (14.1% in the control group), and this difference was statistically significant (p = 0.004).
After face-to-face education and two reminder calls (n = 114), 46.49% of the patients were vaccinated (4.39% were not reached, 49.12% were not vaccinated). After telephone education and two reminder calls (n = 107), 50.47% of the patients were vaccinated (11.21% were not reached, 38.32% were not vaccinated). The vaccination rates (46.49% vs 50.47%) were found not different between the ways of provision of education (p = 0.241).
Fifty-six (49.12%) patients in the intervention group (n = 114) reported that they were still not vaccinated after the education and two reminder calls. The reasons for not being vaccinated (n, %) were indicated as not being able to go to the health facility due to COVID-19 (16, 29.09%), do not believe that the vaccine is necessary (15, 27.27%), lack of access to the vaccine/not in stock at healthcare centers (12, 21.82%), indecision about getting vaccinated (6, 10.71%), not believing that the vaccine is necessary (5, 8.93%), fear of side effects (2, 3.57%), not having time to go to the family physician (2, 3.57%), physician did not recommend the vaccine (2, 3.57%), and initiation of a new chemotherapy protocol (1, 1.79%).
Pneumococcal vaccination were more likely to be received by patients being in the vaccine-education group (p = 0.003), had lung cancer (p = 0.012), had influenza vaccine in the previous season (p = 0.002), wanted to be vaccinated (p = 0.020), had higher number of correct answers on the VKQ (p = 0.002), and had lower score of VAX Scale (p < 0.001). Once the logistic regression analysis was performed, it was found that not having influenza vaccine in the previous season (OR: 2.846, 95% CI: 1.102–7.352, p = 0.031), and higher VAX Scale scores (OR: 1.176, 95% CI: 1.095–1.263, p < 0.001) were the factors affecting the vaccination behavior in patients.
Discussion
This study investigated the impact of the education provided by a clinical pharmacist on pneumococcal vaccination rates in cancer patients. This study showed that the pneumococcal vaccination rate in patients with cancer is increased to 20.2% after the education given by a clinical pharmacist (compared to the rate of 6.1% in the control group). Moreover, the provision of education yield to an increased knowledge among the patients, which was confirmed by the increased number of correct answers on the vaccine and the decreased scores on anti-vaccine attitudes in the intervention group.
The number of studies focused on the interventions to increase pneumococcal vaccination rates in cancer patients is limited [16–18]. These studies have been evaluated the effect of physician-led interventions or the implementation of vaccination guidelines on the pneumococcal and influenza vaccination rates in patients with particular cancers. It has been reported that the pneumococcal vaccination rate in patients with cancer is increased to 85% after the physician’s recommendation [17].
The previous studies have also evaluated the impact of community pharmacists’ interventions on vaccination rates in adults not having cancer diagnoses [19–23] and found that activities such as motivational interviews, patient education, telephone calls for reminders, sending mobile messages, and patients’ referrals to the vaccination unit increase the vaccination coverage in the population.
According to a meta-analysis that investigated the influence of pharmacist interventions on immunization rates, patients exposed to pharmacist intervention are 24% more likely to get vaccinated than patients who receive standard care [24].
Regarding the rate of vaccination after the provision of education by a pharmacist, a previous study showed that 14.9% of the patients in the intervention group and 0.5% of patients in the control group were vaccinated (p < 0.005) [25], which is consistent with the results of this study (20.2% in the intervention and 6.1% in the control group).
Vaccination rates are closely related to the vaccination attitudes of patients. A negative attitude is known as a significant obstacle to vaccination. This highlights the importance of interactions with the patients, as patients with negative attitudes may have influenced others, resulting in a cumulative risk for anti-vaccine attitude. This study also found that patients in the intervention and the control groups had a moderate negative attitude at baseline. In a study conducted by Shacham et al. that evaluated the general population’s hesitancy about general and COVID-19 vaccinations found that the mean VAX score for vaccines (other than COVID-19 vaccines) was 27.48 [26]. Compared to the study of Shacham et al., cancer patients have a more negative attitude towards vaccines compared to the general population. This may be because cancer patients are being more vulnerable due to exhausting disease and treatment processes, and more concerned about vaccinations’ harmful effects on cancer treatment.
After providing education to the intervention group, a statistical decrease in the total score of the VAX Scale was seen. However, the degree of negative vaccination attitudes after the education was not different in control and intervention groups.
Patients in this study exhibited a negative attitude toward the vaccine’s side effects or unknown effects and the producers’ commercial gain rather than the vaccine’s benefits. Patients both in control and intervention groups had high confidence in the vaccine’s benefit; however, mostly preferred natural immunity at baseline. Patients in both groups were most concerned about the unforeseen effects of the vaccine in the future, and this was scored the highest negative attitude among the vaccine attitude scale subgroups. The degree of negative attitude in unforeseen effects of the vaccine showed a significant decrease in the intervention group compared to the control group. These data suggest that counseling by healthcare providers can lower total VAX Scale scores and patients’ fears about unknown or side effects of vaccines.
In studies that evaluated negative vaccine attitudes towards COVID-19 vaccine and general vaccines in the literature, high negative attitudes were observed mainly in the worries about unforeseen future effects (16.3–51.8%) of vaccine and preference for natural immunity (8.5–22.2%) [27, 28]. Compared to those studies, cancer patients seem to have a higher negative attitude towards vaccines than the general population. Since our study did not evaluate the negative attitude towards the COVID-19 vaccine, a comparison could not be made in terms of the COVID-19 vaccine.
Healthcare professionals’ attitudes also affect the patients’ willingness to have vaccines and vaccination coverage. It was demonstrated that only one third of family physicians recommended any vaccine to cancer patients [29], whereas 72% of medical oncologists recommended the pneumococcal vaccination to the patients [30]. In the present study, it was found that two thirds of the patients (in both the control and intervention groups) had not previously been recommended any vaccine by their healthcare providers.
Potential factors that affect vaccination attitudes and behaviors of patients have been previously identified as financial barriers, health status, lifestyle, age, and health literacy [31, 32]. Age, gender, educational level, monthly income, and having chemotherapy or radiotherapy were found to have no effect on vaccination behavior; however, having influenza vaccination in the previous season and a lower VAX Scale score were found to have a positive effect on patients’ vaccination behavior in the present study. It was observed that vaccination behavior is also affected by extraordinary situations such as pandemics. Although patients received vaccination education and wanted to be vaccinated in the present study, 14% could not go to the healthcare centers for vaccination due to COVID-19 curfew or fear of disease transmission.
After the completion of randomized controlled phase in this study, the control group was provided education via telephone to not be disadvantaged against the intervention group. When comparing face-to-face education to telephone education, it was found that face-to-face education raised immunization rates more. However, once the education was supplemented by two reminders, there was no difference in total vaccination rates between face-to-face and telephone education. These findings imply that, regardless of how information is delivered, reminder calls can help raise immunization rates.
Adult vaccination rates are still lower than predicted for various reasons, including patients’ lack of awareness of the risks of vaccine-preventable diseases, a lack of reliable vaccine information, and misbeliefs about the vaccine’s efficacy and safety [33]. According to the National Vaccine Advisory Committee’s Recommendations for Adult Immunization study published in 2014, one of the primary impediments to vaccination is adults’ lack of knowledge about vaccines [34]. In this study, it was observed that about half of the patients know the definition of the vaccine, transmission route of the pneumonia, and that of disease is vaccine-preventable. Most patients knew that pneumonia is a severe disease, and people aged over 65 years and in those immune system is suppressed are at risk for pneumonia. Very few people knew that individuals with diseases such as diabetes, asthma, chronic lung, kidney, and heart diseases are at the risk of developing the pneumonia. These findings highlight the need for patient-specific (individualized) information during counseling with patients about vaccines.
Limitations
Although the major strengths of this study were being a randomized controlled design and conducted in two different health centers, limitations are inevitable. Self-reported vaccination status through telephone interviews with patients may have underestimated or overestimated the actual number of pneumococcal vaccinated patients. The questionnaire used in this study to evaluate the patients’ knowledge on pneumococcal vaccine and pneumonia does not quantify the level of knowledge, but provides an overview for patients’ knowledge and awareness; therefore, a potential change in the level of knowledge could not be determined. Furthermore, the COVID-19 pandemic, which was first discovered in the country in March 2020 and coincided with the study period, may have influenced the patients’ vaccination preferences and attitudes.
Conclusion
The education provided by a clinical pharmacist in hospital settings has considerably raised the pneumococcal vaccination rate in cancer patients. Although more patients get vaccinated after receiving face-to-face information, vaccination rates were unaffected by methods of education augmented with reminder calls. Pneumococcal vaccination behavior was influenced by characteristics such as receiving influenza vaccine and having a less anti-vaccination attitude. Pharmacists can play an important role in the cancer treatment process by participating in immunization programs and giving information and patient monitoring to identify vulnerable patients and eliminate misconceptions about the vaccines in patients with cancer.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
The authors want to thank all patients participating in the study and pharmacist Elif Aras-Atik for her contribution during data collection.
This study is registered with the NCT05229081 registration number and the title of “Impact of Pharmacist-led Educational Intervention on Pneumococcal Vaccination Rates in Cancer Patients” on the ClinicalTrials.gov website. The full protocol is available at ClinicalTrials.gov.
Author contribution
All authors contributed to the study conception and design. Data collection and analysis were performed by Nesligul Ozdemir, Burak Yasin Akdas, and Ahmet Gulmez. The first draft of the manuscript was written by Nesligul Ozdemir, Burak Yasin Akdas, and Aygin Bayraktar-Ekincioglu and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Declarations
Conflict of interest
The authors declare no competing interests.
Footnotes
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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