Abstract
Background
Asthma is one of the most common respiratory diseases worldwide. 1 In the United States, improving asthma control is a high priority for many health organizations. According to the Centers for Disease Control and Prevention, there are nearly 25 million Americans diagnosed with asthma. 2 Out of these patients, over 4.6 million are under the age of 18 years old. In 2021, 39% of asthma patients reported having at least 1 asthma attack. In 2020, 36% of American children with asthma required emergency department treatment for their asthma. This illustrates a need for improvements in pediatric asthma control with appropriate medication therapy, which pharmacists may help to provide. Therapy for asthma is complex due to the need to manage acute rescue medications as well as controlling symptoms and reducing exacerbations with maintenance medications. The high complexity of available medications makes pharmacists beneficial resources in the management of asthma.
The 2023 GINA guidelines highlight the role of pharmacists in the care of asthma patients. 1 Specifically, they endorse the ability of pharmacists to educate patients about asthma and asthma inhaler technique. Given that the committee for the GINA guidelines recommend assessment of asthma inhaler technique before consideration of therapy adjustments, pharmacists should play a key role in decision making for asthma therapy. Ambulatory care pharmacists are in a position to make care for asthma patients more accessible, and with consult agreements in place are able to both educate the patient and make therapy adjustments if needed.
There are many published studies which suggest that pharmacists can have a measurable impact on pediatric asthma control. Inpatient pharmacy asthma counseling programs have reduced hospital admissions 3 and reported improvement in quality of life. 4 A clinic-based pharmacist service has shown reductions in oral steroid use, emergency department visits, and hospital admissions. 5 A retail pharmacy team with a collaborative service between a health system helped to provide asthma therapy recommendations based on retail pharmacist assessment. 6 However, there has been limited documentation of pharmacist impact on the asthma control test (ACT) and childhood asthma control test (C-ACT) from studies conducted in the United States. Pharmacists in Jordan successfully improved the ACT scores in pediatric asthma patients after intervention, with 1 publication demonstrating benefits from simple corrections in the inhaler use process.7,8 Additionally, a school-based clinic showed an average increase in the ACT of 3 points, which is considered a clinically significant impact based on association with frequency of rescue inhaler use and frequency of exacerbations.9,10 The impact of pharmacists on the ACT and C-ACT have yet to be published from an outpatient pediatric medical clinic perspective.
The use of technology to aid the care of patients with asthma is becoming more popular, especially in the post-COVID era. 1 Biofeedback devices, mobile apps for tracking symptoms and adherence, and virtual visits are a few examples of tools that pharmacists are currently utilizing to improve patient care. One example of a useful biofeedback device is the Vitalograph Aerosol Inhalation Monitor (AIM®). Vitalograph AIM® is a biofeedback device that has been approved for use since 1989. 11 It visually shows patients correct inhaler technique using placebo inhalers and a display device. Measured areas of inhaler technique include device actuation, inhalation rate, inhalation time, and breath hold time. Placebo devices are available for metered dose inhalers (MDI) with and without a spacer as well as dry powder inhalers (DPI). There are very few published studies demonstrating the value of counseling using a Vitalograph AIM® device in pediatric patients, although there are studies in adults with asthma. Blum et al utilized the AIM device for counseling and adjusting therapy in a group of 44 adult patients in a hospital-based outpatient pulmonary clinic, with significant improvements seen in ACT or COPD assessment test (CAT) scores after 4 weeks. 12 Based on experiences from our own clinic, improvements in symptom control can be seen after counseling with this device even when therapy is not changed. 13 Although the adult data with the Vitalograph AIM® are encouraging, additional data with pediatric patients is needed to demonstrate the full benefit of the device. This study was conducted in part to fill this gap in the use of beneficial asthma technology. As advancements in medical technology continue to progress, pharmacists have a key role in implementing technology into patient care within their practice and providing increased evidence of the benefits associated with its use. More research is needed to clearly show the benefit of utilizing technology in pediatric patients with asthma, as well as the benefits of pharmacist interactions using validated surveys such as the ACT.
Objectives
The primary objective of this study is to determine whether outpatient pharmacist visits in pediatric patients with asthma result in a measurable difference in asthma control, utilizing the validated ACT and C-ACT scoring tools.
The secondary objective of this study is to describe the benefits of using biofeedback technology to assist in asthma counseling.
Methods
Practice Setting
This single-center, prospective, pre-post cohort study analyzed the control of pediatric asthma at baseline and after implementation of an ambulatory care pharmacist into the patient’s care team. The study was conducted at an outpatient primary care clinic. The primary care clinic has 8 pediatricians, and the availability of 3 ambulatory care pharmacists and an ambulatory care pharmacy resident who also work with the adult family medicine providers in the clinic. The ambulatory care pharmacists have a consult practice agreement for adult patients with asthma but are also asked to assist with the pediatric asthma patients, in which case recommendations are made to the provider prior to any changes in patient therapy. There is currently a plan to expand the pharmacist consult agreement to include pediatric patients.
Inclusion and Consent Process
Inclusion criteria consisted of patients between 6 and 17 years of age, with a diagnosis of asthma confirmed by their pediatrician. Patients were excluded from the study if they had another respiratory condition which could be contributing to illness, including cystic fibrosis or tracheostomy, and if they declined to consent to participate in the study. Patients and their caregivers agreed to the consent and assent documents as appropriate for the age of the patient. The study was approved by the Institutional Review Board and the Pediatric Research Compliance Committee prior to the start of data collection. Patients were enrolled between November 15th, 2023 and April 5th, 2024.
Visit Schedule
Patients enrolled in the study had an initial visit with the clinical pharmacist on the same day as the pediatrician visit which was already scheduled. The initial visit consisted of consent and assent to the study; medication reconciliation; a preliminary ACT if the patient was 12 years or older or C-ACT if the patient was 6 years to 11 years old; a brief patient history of asthma including steroid use, emergency department visits, hospital admissions, and smoking exposure; an aerosol inhalation monitor, (Vitalograph AIM® assessment) if the patient was agreeable; an inhaler technique review; an adherence assessment; and initial recommendations to the pediatrician or managing specialist. The initial visits took place in-person at the pediatrician office and took 30 to 60 minutes to complete. Patients then completed at least 1 but preferably 2 follow-up visits. The first follow-up visit was scheduled approximately 4 weeks after the initial visit and the second follow-up visit was scheduled approximately 12 weeks after the initial visit. These follow-up times were chosen to closely reflect the similar study conducted by Padden-Elliott et al 9 and to allow sufficient time for patients to incorporate recommended adjustments. This is a similar follow-up structure to the usual practice within our clinic. Follow-up visits were permitted to be over phone or in-person in the primary care office, and consisted of repeated medication reconciliation, verbal inhaler technique review, ACT or C-ACT assessments, and additional recommendations to the pediatrician. Follow-up visits took 10-30 minutes to complete. The patient’s final visit was considered the last date which the pharmacist met with the patient either in person or by phone, which could have been either the 4-week or 12-week scheduled visit as the protocol for the study required only 1 follow-up visit for patient to be included in the study.
Inhaler Technique Assessment
During the aerosol inhalation monitor portion of the initial visits, all patients were asked to demonstrate technique using a metered-dose inhaler placebo device and a metered-dose inhaler plus spacer placebo device. Patients with a dry powder inhaler in their existing or proposed regimen were asked to demonstrate technique with a dry powder inhaler placebo device. Patients were observed using the inhaler device once and instructed on how to improve their technique between each trial of the aerosol inhalation monitor. Patients completed the trials of each inhaler type at least 1 time, and up to 3 times if improvements in technique were required. If the patient had their own inhaler device present, they were asked to use the device to demonstrate their usual technique. If patients did not have their inhalers with them, they were asked to verbally describe steps they would take to use the inhaler and were brought an equivalent demonstration inhaler to physically show the pharmacist their actions. If patients were unable to demonstrate correct inhaler technique on their device or with the aerosol inhalation monitor, a change in therapy was recommended involving a switch to a device that the patient was able to use appropriately. If no inhalers could be used effectively by the patient, nebulized medications were recommended.
Adherence Assessment
Adherence was monitored using dose counters on inhalers when present, parent and patient reports, and dispense reports provided in the patient’s electronic medical record. All methods of adherence tracking were used whenever possible. Adherence was calculated using patient-reported missed doses as well as fill history reported through the electronic health record, utilizing reported doses taken per week vs expected doses taken. Patients with only as-needed therapy were considered to be adherent as they had no scheduled dose times. If discrepancies existed between adherence tracking methods, the patient and their caregivers were asked for potential explanations such as hospital stays, samples provided to the patient, or an existing home supply from previous early fills. When no explanation was able to appropriately reflect differences in reported adherence, the device and fill history as seen on the electronic medical record were considered the most reliable methods of adherence tracking and were recorded for adherence tracking purposes. If adherence problems were suspected, the importance of adherence was addressed with the patient and their caregivers along with a review of the mechanism of action of the medication. If patients or their family mentioned cost issues, coupons or patient assistance programs for an equivalent medication were found and recommended for the patient to use.
Outcomes
The primary outcome of the study was change in ACT or C-ACT score from the initial visit to the final follow-up visit. Secondary outcomes included Vitalograph AIM® data, recommendations made and accepted from the clinical pharmacists, adherence rates, and change in oral steroid use, emergency department visits, and hospital admissions from 6 months prior to study enrollment to 1 to 3 months after the final study visit, depending on patient enrollment date. Emergency department visits and hospital admissions recorded for the purposes of this research study were limited to those related to asthma, including exacerbations or respiratory tract infections. The timing of 3 months after the final visit was chosen to include a time frame of 6 months from the patient enrollment into the study if all proposed visits were completed, and was intended to mimic the 6 month time period reviewed prior to the patient’s enrollment. These visits were reviewed using the electronic medical record.
Statistical Analysis
Descriptive statistics were used to describe the baseline characteristics of the patients, including age, sex assigned at birth, race, and smoking exposure. Descriptive statistics were also reported for Vitalograph AIM® data and pharmacist recommendations. Categorical variables were described using frequency and proportion. McNemar’s test for paired comparisons was used for any change in categorical variables. Continuous variables were described as mean with standard deviation if normally distributed, or median with interquartile range if not normally distributed. Primary outcome data was analyzed using the Wilcoxon signed-rank test. All data was analyzed using Stata/MP 16.1 (StataCorp, College Station, TX). Statistical significance was set as a priori alpha of 0.05. To attain 80% power and detect a 3-point difference in the ACT test, an estimated population of 15 patients was calculated.
Results
Patient Demographics
Patient Demographics.
Abbreviations: ICS, inhaled corticosteroid; SABA, short-acting beta agonist; LABA, long-acting beta agonist. Dose classifications of inhaler potency included in the table are based on the definitions provided in the 2023 GINA guidelines. Given steps of GINA therapy differ between age groups, this is not differentiated within the table.
Primary Outcome
Asthma Control Test.
Data is expressed as median (IQR) and n (%). All data was compared to baseline visit to calculate P-values. *Final visit is the last visit in which a patient was seen (7 patients at 12 weeks, 6 patients at 4 weeks). **The Wilcoxon signed-rank test was used for the ACT and ***McNemar’s test was used for control status.
Inhaler Technique
Vitalograph AIM®.
Abbreviations: MDI, metered dose inhaler; DPI, dry powder inhaler. *Patients successful refers to the number of patients with a good AIM result within 3 attempts of device. **Breakdown of incorrect breathing strategies indicates the number of patients making a single type of mistake on each attempt. Patients may have more than 1 type of error on each attempt.
Adherence
Adherence improved throughout the duration of the study. At baseline, 44% of patients met at least an 80% adherence rate to their asthma medications. By the final study visit, adherence rates of 80% or higher were reported in 85% of patients (P = 0.0365).
Pharmacist Recommendations
Throughout all visits, 100% of pharmacist recommendations were accepted by the patient’s pediatrician. A total of 15 recommendations were made to the providers throughout the duration of the study, with patients having between zero recommendations and 3 recommendations each. Of note, recommendations to the patient on improving technique were not included in the count of recommendations to the provider. Most recommendations made by the pharmacist that required a physician’s approval were for the provision of a spacer or a physician note permitting the use of a rescue medication at school rather than a change to the inhaler therapy. Four inhaler adjustments were recommended throughout the duration of the study. Of these recommendations, 2 patients required a change in inhaler directions, which in both cases was increased frequency of inhaler use. One patient required a higher potency inhaled corticosteroid to be prescribed. Finally, 1 patient required the addition of a controller inhaler to therapy.
Emergent Interventions
Emergent Interventions for Asthma.
Discussion
In this study, we demonstrated that clinical pharmacists are able to make improvements to pediatric asthma control. Improved ACT scores, improved adherence rates, and fewer emergent interventions for asthma were achieved in enrolled patients after outpatient pharmacist counseling and recommendations. Most patients included in the study followed up at the 4-week visit interval, which showed a statistically significant median improvement of 3 points in the asthma control test, consistent with the median final study visit findings. Although a trend was seen towards greater improvement at week 12, with a median difference of 5 points compared to baseline scores, statistical significance was not achieved when isolating this visit. This may be due to the greater loss of follow-up, with 7 patients completing a 12-week visit compared to thirteen patients following up at a minimum of 1 visit. Another possible confounding factor in the 12-week visit is that more than half of the patients were originally scored as controlled, leaving a smaller possible margin for the improvement in their score.
This study also highlights the benefit of having a Vitalograph AIM® device to counsel patients on inhaler use. Although this device has been available for decades, few clinics have published data about the use of the device for inhaler recommendations and patient counseling. There are also limited studies currently published which assess Vitalograph AIM® use in pediatric patients. The data collected using this device demonstrates that by visually assessing patient inhaler technique and discussing areas of improvement, patients are able to improve their technique during the same study visit. It is important to note that there were a variety of mistakes detected for patients using the Vitalograph AIM® device, which highlights the importance of individualized technique assessment instead of generalized key counseling points. For many patients, technique counseling was the only change that was required to see clinical improvements.
The results of our study are similar to previous findings that have demonstrated pharmacist impacts in pediatric asthma care. Almomani et al found a significant difference in a randomized control trial when assessing the group assigned to pharmacist counseling vs no counseling, with 40% of patients in the control group achieving an ACT score of 20 or greater vs 80% of patients in the intervention group. 7 Padden-Elliott et al found that asthma control as measured by ACT improved from about 52% controlled tests at baseline to nearly 90% after 3 months of pharmacist care. 9 In our study, all patients had controlled asthma control test scores at their final visit, compared to only half of the patient population at baseline. This improvement is clinically significant, although the ability to achieve 100% controlled scores may be due in part to the small population included in the trial. It is not possible to determine if patients lost to follow-up had similar improvements in asthma control.
Patients enrolled in this study had a variety of baseline control status and a variety of ICS potency needs. In the previous trial conducted by Padden-Elliott et al, nearly 43% of patients were considered to have intermittent asthma. 9 Similarly to our trial, trends toward improvement were seen despite a large population of patients requiring only as needed therapy. This highlights the impact that understanding of asthma and the treatment of asthma can have on patients, even if controlled at baseline. The results of our trial and the Padden-Elliott trial are remarkably similar, with a baseline median ACT score of 20 and final score of 23 in each trial. 3
There were several limitations to our study. First, our study does have a small sample size pulled from a single outpatient office, which may limit generalizability to other populations of patients. It was also conducted in a short period of time, which did limit enrollment potential. Due to the short duration of review, not all patients were able to be screened for a full 3 months after their final visit date for an exact 6-month period comparable to the period the chart was reviewed prior to enrollment. Due to the variable nature of asthma triggers throughout times of year, it is possible that there were confounding variables in the control of some patients. It is also possible that patients were counseled at outside health systems or retail pharmacies independently of their study participation. Most patients did not have their home inhalers present at the initial visit, which limited the pharmacist’s ability to track used doses of inhaler compared to expected use for the best possible adherence tracking. The drop-out rate may have skewed adherence data, as patients who did not follow up may have decreased adherence compared to patients who did follow up. The patients who were lost to follow up also had a large number of emergent events before the study which were not tracked at the conclusion. This may highlight that patients with non-adherent behaviors are more likely to be uncontrolled, but cannot be considered conclusive given the short timeline of the study. Patients may have reported appropriate inhaler technique with telephone follow-up visits while continuing to have flaws in technique which are difficult to ascertain without visually seeing the patient use the inhaler device. There was no control group of patients outside of the patient’s previous experiences due to difficulty of appropriately matching patient criteria in a small patient population, as well as the difference in reporting styles between pharmacist and provider notes within the clinic.
Strengths of this study include the prospective nature of the trial, the use of Vitalograph AIM® to counsel patients, and similar findings to previous literature. Future studies are needed to confirm the benefits of pharmacist implementation in outpatient asthma clinics. It would be valuable to conduct larger studies of longer duration to confirm that benefits of pharmacist counseling are lasting in this patient population. It would also be beneficial to look at populations of several clinics to increase the generalizability of these findings.
Conclusion
Asthma is one of the most common pediatric disease states and uncontrolled asthma has been a key health issue in the United States. Pharmacists are one of the most accessible health professionals. This pilot study supports the potential role of pharmacist interventions in the improvement in pediatric asthma control.
Footnotes
Author Contributions
Lauren Anthony: Conceptualization, methodology, validation, formal analysis, investigation, writing- original draft, visualization, project administration. Sandra Axtell: Conceptualization, methodology, supervision, validation, writing- review and editing. Bianca Nixon: Conceptualization, methodology, supervision, validation, writing- review and editing.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
