Abstract
Objective
The aims of this study were twofold — to determine the impact of a health education intervention led by a hospital pharmacy department on influenza vaccination take-up in patients diagnosed with immune-mediated diseases. Patients were receiving treatment with biological medicines. Secondly, to compare those rates with the vaccination percentages of another hospital pharmacy with similar characteristics in which no educational intervention was conducted.
Methods
This was a retrospective cohort study of adult patients with immune-mediated diseases receiving treatment with biological medicines. The medicines were dispensed by the hospital pharmacy departments of two hospitals between 1 January 2019 and 31 December 2020. In Cohort A (intervention group), a health education strategy was implemented with regards to influenza vaccination. Cohort B acted as a control group. The influenza vaccination rates obtained in both cohorts during 2019 and 2020 were compared.
Result
A total of 355 patients took part in the study — 148 (41.7%) in Cohort A and 207 (58.3%) in Cohort B. The hospital pharmacy department in Cohort A implemented a health education strategy after which the vaccination percentage during the 2020 campaign increased by 38 patients (45.7%), compared with a 10 patient (5.8%) increase in Cohort B (p<0.001).
Conclusions
The health intervention by the pharmacy department had a positive impact. This included an opportunity to improve vaccination take-up and is a strategy to consider when implementing a vaccination programme. Health education is a fundamental objective of healthcare. In our case it led to an increase in vaccination and had a positive impact on public health. It also provides opportunities for pharmacists to work in a multidisciplinary way with other healthcare professionals.
Keywords: EDUCATION, PHARMACY; PHARMACY SERVICE, HOSPITAL; Education, Pharmacy, Continuing; CLINICAL MEDICINE; COVID-19
Introduction
Seasonal influenza can coexist with SARS-CoV-2, the virus that causes Coronavirus (COVID-19). During autumn and winter months, this means that influenza vaccination coverage rates must be improved in the patient groups at risk of both infections.1
The COVID-19 pandemic has had a significant impact on the management of chronic diseases. The pandemic has shown we need to reorganise the healthcare system to focus on multi-disciplinary collaboration and to incorporate a transdisciplinary approach in healthcare teams.
It is therefore essential to ensure the healthcare system has the capacity to care for patients with influenza and respiratory infections due to SARS-CoV-2. This can help to reduce the number of visits to emergency care departments, hospitalisations and deaths, while continuing to provide appropriate care for patients who have other types of disease.1 It is fundamental, therefore, to combine different strategies that include all healthcare professionals (nurses, pharmacists and physicians, among others)2 to work in a coordinated manner to ensure the message reaches the entire population.
Patients with immune-mediated diseases are at increased risk of having infections — primarily respiratory infections. Various factors contribute to this increased risk, including the impact on the functioning of the immune system due to the disease itself, immunosuppressive treatment and associated comorbidities.3 Studies in patients with rheumatoid arthritis have shown an increase in the incidence of influenza, while the complications arising from it in these patients are greater, particularly in the over 70s. Moreover, anti-tumour necrosis factor (TNF) therapies are independently associated with a greater likelihood of experiencing influenza symptoms.4
Therefore, various scientific societies issue recommendations on administering the influenza vaccine to patients receiving biological therapies. More specifically, annual influenza vaccination is recommended in moderate-severe psoriasis.5 In turn, the EULAR (European League Against Rheumatism)6 recommendations include the need for this vaccine to be administered in most patients. In the case of inflammatory bowel disease, Guidelines from the European Crohn's and Colitis Organisation (ECCO) recommend annual influenza vaccination to help prevent, diagnose and manage of infections linked to Crohn's and Colitis.7
With regards to the habitual vaccination circuit, these patients are referred by their medical practice to the preventive medicine practice before the start of treatment with these drugs.
In terms of the role of pharmacists in Spain, unlike some other countries, pharmacists are not responsible for administering vaccinations. However, access to pharmacists as healthcare professionals is high making them an important link as patient advisers and educators. Indeed, pharmacists can work with patients to promote health and prevent illness.8
The objective of this study was to determine the impact of a hospital pharmacy-led health education intervention on the increase in the percentage of influenza vaccination in patients diagnosed with immune-mediated diseases. All patients in the study were receiving treatment with biological medicines. The study compared the results of patients who received health education with results from a control group of patients with similar characteristics but no health education. The aim was to ascertain the possible differences or similarities between these two populations.
Method
This was a retrospective cohort study that included all adult patients diagnosed with immune-mediated diseases treated with biological medicines dispensed by the pharmacy departments of two first-rate hospitals between 1 January 2019 and 31 December 2020.
Cohort A (intervention group) contained patients whose prescriptions were dispensed by the Pharmacy Department at Monforte de Lemos Public Hospital (Lugo, Spain).
The intervention was performed by the pharmacists and nursing staff in the department who, within their healthcare activity and as a result of restrictions imposed due to the COVID-19 pandemic, made a telephone call to each patient to provide health education. Specifically, they talked to patients about the importance of influenza vaccination, gave campaign dates, and directions on how to arrange an appointment for the vaccine to be administered. Whether the influenza vaccine had been received during the 2019 campaign was also recorded.
To perform the intervention on Cohort A, two pharmacists and two nurses from the pharmacy department divided telephone calls to 148 patients. Each patient received one health education telephone call. Each healthcare professional made a total of 37 calls between September and October 2020 ahead of the 2020–2021 influenza vaccination campaign.
Cohort B (control group) contained adult patients with immune-mediated diseases receiving treatment with biological medicines dispensed by the Pharmacy Department at Da Mariña Public Hospital (Lugo, Spain) during the same study period. A record was kept of the influenza vaccination results from 2019 and 2020, with no education intervention by the pharmacy department.
At both sites, patients visited the pharmaceutical care clinic every 2 months and visited the specialist physician’s practice every 3–6 months. The vaccination circuit in both hospitals is the same: patients are referred by the specialist physician’s practice to the preventive medicine practice before the start of their biological therapy. This means they can receive their influenza vaccination at the preventive medicine practice if they are referred during the influenza vaccination campaign, which this year was from October to December. Alternatively, patients can arrange an appointment for the vaccine to be administered at their primary care centre if their treatment begins outside these dates. Once treatment has begun, they must arrange an annual appointment with their primary care centre for vaccination.
The vaccination records kept by the specialist care area of preventive medicine and by the primary care health centre are included in the electronic medical record programme (IANUS). Part of the Galician Health Service, IANUS is a centralised programme that includes the record of vaccinations administered to each patient in the Autonomous Community of Galicia.
We consulted the vaccination records included in the IANUS programme for information on the vaccination results at both sites during the 2019 and 2020 campaign.
In terms of the sample size, if the study included 140 and 180 patients in Cohorts A and B, respectively, we could obtain a 95% chance of detecting differences in the vaccination percentages of the two cohorts using a bilateral chi-squared test for two independent samples. We considered that the significance level was 5% and assumed that the increased proportion in the intervention group was 25%. The increased proportion in the control group was estimated to be 10%.
The continuous variables were described with mean and standard deviation (SD) and the categorical variables in absolute and relative frequencies. The chi-squared test was used to compare the differences in vaccination percentages between the groups being studied. We analysed the data collected using R statistical analysis software (version 3.6.2).
The study was performed following a favourable opinion from the Drug Research Ethics Committee of Galicia (ethics approval number: 2021/196).
Results
A total of 355 patients participated in the study, 148 (41.7%) belonging to Cohort A and 207 (58.3%) to Cohort B. The average age of patients was 52.9 years (SD 14.5), 176 (46%) were male and 179 (54%) female. The biological medicines most commonly prescribed in both cohorts were: adalimumab in 89 patients (25%) and etanercept in 81 patients (22.8%). The main immune-mediated diseases were: 86 rheumatoid arthritis (24.2%), 68 psoriatic arthritis (19.1%) and 67 psoriasis (18.9%). The main characteristics of the patients included in each cohort are summarised in table 1.
Table 1.
Characteristics of the patients included in each cohort
| Variable | Cohort A (148) | Cohort B (207) |
| Gender (male) | 79 (53.3) | 97 (46.8) |
| Age (>65) | 30 (20.2) | 31 (14.9) |
| Disease | ||
| Psoriatic arthritis | 15 (10.1) | 53 (25.6) |
| Rheumatoid arthritis | 35 (23.6) | 51 (24.6) |
| Crohn’s disease | 16 (10.8) | 34 (16.4) |
| Ulcerative colitis | 16 (10.8) | 6 (2.9) |
| Ankylosing spondylitis | 23 (15.5) | 39 (18.8) |
| Psoriasis | 43 (29.0) | 24 (11.6) |
| Medication | ||
| Abatacept | 5 (3.3) | 12 (5.7) |
| Adalimumab | 28 (18.9) | 61 (29.4) |
| Apremilast | 6 (4.0) | 4 (1.9) |
| Baricitinib | 1 (0.6) | 0 (0.0) |
| Brodalumab | 0 (0.0) | 1 (0.5) |
| Certolizumab | 10 (6.7) | 14 (6.7) |
| Etanercept | 34 (22.9) | 47 (22.7) |
| Golimumab | 12 (8.1) | 21 (10.1) |
| Guselkumab | 1 (0.6) | 1 (0.5) |
| Infliximab | 24 (16.2) | 2 (1.0) |
| Ixekizumab | 2 (1.3) | 1 (0.5) |
| Sarilumab | 1 (0.6) | 1 (0.5) |
| Secukinumab | 7 (4.7) | 15 (7.2) |
| Tocilizumab | 1 (0.6) | 1 (0.5) |
| Tofacitinib | 4 (2.7) | 5 (2.4) |
| Ustekinumab | 10 (6.7) | 19 (9.1) |
| Vedolizumab | 2 (1.3) | 2 (1.0) |
Values in absolute cases and percentages in brackets.
During the 2020 campaign, there was an increase of 38 (45.7%) vaccinated patients in Cohort A after the intervention compared with an increase of 10 patients (5.8%) (p<0.001) in Cohort B (table 2).
Table 2.
Results per site.
| Variable | Cohort A (148) | Cohort B (207) | p-value |
| 2019 vaccination | 83 (56.1) | 172 (83.1) | <0.001 |
| 2020 vaccination | 121 (81.7) | 182 (87.9) | 0.105 |
| Vaccination increase (%) | 45.7 | 5.8 | <0.001 |
| Vaccination | |||
| Vaccinated in 2019, not in 2020 | 6 (4.0) | 9 (4.3) | <0.001 |
| Not vaccinated in 2019 or 2020 | 21 (14.2) | 16 (7.7) | |
| Vaccinated in 2019 and 2020 | 77 (52.0) | 163 (78.7) | |
| Not vaccinated in 2019, vaccinated in 2020 | 44 (29.7) | 19 (9.1) |
*Values in absolute cases and percentages in brackets. p-value calculated using the chi-squared test.
On analysing the results by subgroup, there were no statistically significant differences between the increase in vaccination in 2020 compared with 2019 at both sites according to gender, which stood at 20.5% in the case of males and 15.1% in females (p=0.137).
In terms of age, 294 patients (82.81%) in both cohorts were below the age of 65 and 61 (17.19 %) above the age of 65. A statistically significant increase of 20.7% was observed in the vaccination percentage in 2020 in patients above the age of 65 at both sites, and of 3.3% in those over the age of 65 (p<0.001).
Discussion
Health education offered by the hospital pharmacy departments, which focuses on the pharmacist as part of the healthcare team, is a promising tool for ensuring an increase in overall vaccination rates. The intervention led to a significant increase in the vaccination rate and chimes with results described in literature.9 10
Other studies which offered no pharmaceutical intervention yielded improvable results in influenza vaccination rates. In an Italian study of 266 patients with multiple sclerosis, for whom the most commonly prescribed treatments were dimethyl fumarate, natalizumab, teriflunomide and interferon-beta, the percentage of vaccinated patients was 58.2% higher in those treated with natalizumab. The higher percentage was attributed to the increased proximity of health professionals and more frequent clinical evaluations for these patients.11
In a study that included 162 patients treated with pembrolizumab, most with a melanoma diagnosis, 56.8% had not received the influenza vaccination while they were being treated.12 In another reference in which the prescribed treatments were not specified, the vaccination rates stood at 64% of a total of 5053 onco-haematological patients.13
In the United Kingdom, the vaccination results in high-risk individuals aged between 16 and 64, including patients undergoing immunosuppressive treatment, were much lower than recommended by the Public Health England’s National Infection Service.14
The 2020—2021 influenza vaccination campaign objectives set by the Ministry of Health, Consumer Affairs and Social Welfare, were reached in our study. We achieved more than 75% coverage in the population aged 65 or over. This achievement of objectives does not occur on comparing the results of our study with the overall rates of the Autonomous Community of Galicia (71.66 %) and the overall data for Spain (67.7 %).15 In addition, vaccination coverage in 60% of people with risk conditions was achieved, which is a result that is in line with the new objectives included in the 2021–2022 campaign.16
A by no means negligible percentage of patients who were not vaccinated during either of the two campaigns prevails: 21 (14.2%) in Cohort A and 16 (7.7%) in Cohort B, indicating that there is still a target population susceptible to intervention.
To this end, health professionals form the group with the greatest capacity to have a positive or negative impact on the health-related knowledge, attitudes and behaviour of the population. Frequent contact in the medical practice, the confidence they provide, and the demand for assistance often required by patients visiting the medical practice are all factors favouring this effectiveness. Provision of the verbal information in writing may be of use when implementing an educational intervention. A study performed in Japan by community pharmacists showed that health education in the medical practice is of greater use than written messages, the latter being an ideal addition to the verbal intervention.17
With regards to age groups, the intervention achieved better results in those under the age of 65. This could be based on the fact that those over the age of 65 are included in the vaccination campaigns as an at-risk population group in which the vaccination rates are already high.
Therefore, health education strategies should be designed and personalised to target different age groups. For example, these interventions must be continued to ensure those below the age of 65 maintain the high level of awareness that they achieved during the pandemic.
Another aspect to consider in the case of patients of working age is the fact that absenteeism from work occurring during an episode of influenza (estimated at between<1 and 4.3 days in a pharmacoeconomic review from 2008)9 is often combined with patients having to request an additional day off work to be vaccinated. At both sites, direct referral from the specialist’s practice to the preventive medicine practice means that vaccination is possible on the same day. This strategy guarantees to reduce the loss of productivity by individuals in active employment and it could be an intervention that helps increase the percentage of overall vaccination, although studies to confirm this hypothesis are required.
The analysis performed offers information on the needs of our population and enables us to adapt our work circuits to permanently provide and improve our intervention. The drawing up of protocols for this is key, as the information conveyed to the patient must remain homogeneous throughout the healthcare journey.18
To this end, the health education provided by the medical practice at both sites leads us to believe that, by modifying the circuit to include the support of pharmacists and nursing staff from the pharmacy department in reinforcing the information provided at the medical practice, this might lead to vaccination percentages of almost 100% sustained over time.
The pharmacist becomes a key link in the comprehensive management of patient drug therapy, due to the trust established with them at the pharmaceutical care clinic. Their inclusion in the health teams would therefore promote the primary prevention of illness.
This is a pilot project that included two hospitals, an increase in the number of sites in the near future might be of further interest.
In terms of the limitations of the study, in addition to those of a retrospective study, there is a bias related to the COVID-19 pandemic which is that patients might be more aware of the importance of vaccination and have more information on the risks of not being vaccinated. The percentage of people vaccinated increases as a result, and so is not only in response to the intervention performed.
Conclusion
Chronicity and pandemic are two elements that generate debate as to the need to plan actions that favour the willingness of the population to be vaccinated. With regards to attitudes towards vaccination, the perception of patients as to its importance is an influential factor. Therefore, the role of health professionals in promoting health through health education becomes a cornerstone in meeting this objective. At this point, given our training, skills and proximity to the patient, pharmacists are required to convey truthful, proven information adapted to the patient's clinical and psychosocial situation, solving any doubts that may arise when healthcare is being provided.
Key messages.
What is already known on this topic
Vaccination is a fundamental strategy for primary prevention of infectious diseases. It acquires even more importance, in the current situation of COVID-19 pandemic. There is little evidence about the impact of pharmaceutical interventions on influenza vaccination rates in the population.
What this study adds
Pharmaceutical intervention, carried out by pharmacists from a hospital pharmacy service and nursing staff as part of a multidisciplinary team, resulted in a significant increase in the percentage of high-risk patients treated with biological medicines, who were vaccinated against influenza.
How this study might affect research, practice or policy
The health education offered by pharmacy departments, which focuses on the pharmacist as part of the healthcare team, is a promising tool for ensuring an increase in overall vaccination rates.
ejhpharm-2021-003175supp001.pdf (163.3KB, pdf)
Footnotes
Twitter: @lvilpin1, @anaipin
Contributors: LVP designed the study and made primary contributions to data collection. ABH made data analysis. AICP, YMTG, PNB, LAF, MVL, CC and JVAB assisted with data collection. Guarantor: LVP.
Funding: The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests: None declared.
Provenance and peer review: Not commissioned; externally peer reviewed.
Supplemental material: This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.
Data availability statement
No data are available. Not applicable.
Ethics statements
Patient consent for publication
Not applicable.
Ethics approval
A favourable opinion from the Drug Research Ethics Committee of Galicia was obtained to perform this study (ethics approval number: 2021/196).
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
ejhpharm-2021-003175supp001.pdf (163.3KB, pdf)
Data Availability Statement
No data are available. Not applicable.