The global spread of severe acute respiratory syndrome coronavirus 2 has resulted in more than a million deaths to date despite many strategies implemented to limit transmission, such as social distancing, wearing a face mask, quarantining and isolation.1 , 2 These strategies were also applied in health care facilities, including recommendations for minimizing face-to-face meetings in allergy and immunology clinics and taking necessary precautions to minimize the risk of transmission.3
Discontinuing subcutaneous immunotherapy (SCIT) is not recommended in patients who do not have coronavirus disease 2019 (COVID-19) or were previously infected. It is also recommended that the interval between doses can be extended to 2 weeks in the build-up phase and up to 6 weeks in the maintenance phase.3, 4, 5
A recent study found that the anxiety levels of the parents of children hospitalized during the COVID-19 pandemic were higher than those of parents whose children were hospitalized before the pandemic.6 Patients receiving SCIT and their parents must continue to come to the hospital for SCIT during the pandemic. We aimed to evaluate the effect of patient and parental anxiety on adherence to SCIT during the COVID-19 pandemic.
Patients who underwent venom and aeroallergen SCIT in our pediatric allergy and immunology hospital clinic during the COVID-19 pandemic between May 1, 2020, and September 1, 2020, and their parents were included in our study. The patients' age, sex, SCIT type, phase and duration, and adherence to SCIT since the start of the pandemic were recorded. The study was approved by the ethics review committee of Ankara City Hospital and by the Turkish Ministry of Health. Written informed consent was obtained from the patients' parents.
Per the recommendations, the interval between doses was extended to 2 weeks in the build-up phase and 6 weeks in the maintenance phase; the patients were informed. The patients were classified as adherent (patients who continued SCIT according to schedule during the pandemic), nonadherent (patients who continued SCIT during the pandemic but with between-dose intervals longer than 2 weeks in the build-up phase and 6 weeks in the maintenance phase), or discontinued treatment (patients who did not present for SCIT at all since the pandemic started).
The anxiety levels of our patients were assessed using the State-Trait Anxiety Inventory (STAI) for children, which is a tool to evaluate the state and trait anxiety in children aged 8 to 18 years.7, 8 Patients older than 18 years and the parents were assessed using the STAI.9 Similar to the STAI for children, the STAI consists of the state anxiety scale and the trait anxiety scale with higher scores reflecting higher anxiety levels.
Statistical analyses were performed using Statistical Package for the Social Sciences software version 22.0 for Windows (International Business Machines Corporation, Armonk, New York). The χ2 square test was used to compare nonparametric data; the Mann-Whitney U test was used for comparisons among non–normally distributed continuous variables and independent samples t test for normally distributed continuous variables. A value of P < .05 was considered statistically significant.
The study included 78 patients (62.8% male) who started SCIT (8 patients for venom, 70 patients for aeroallergen) in our hospital clinic and attended treatment regularly before the pandemic. The mean (±SD) age of the patients was 14.87 (±3.48) (minimum-maximum [min-max]: 8-23.5) years. After the start of the pandemic, 39 (50%) patients continued SCIT regularly (adherent group), 23 patients continued treatment with extended dose intervals (nonadherent group), and 16 patients discontinued treatment.
Of the 16 patients (68.8% male) who discontinued treatment, 10 patients were in the build-up phase and 6 were in the maintenance phase. When asked the reason for SCIT discontinuation, 16 patients cited fear of COVID-19 transmission. Significantly more patients who discontinued treatment were in the build-up phase compared with patients who continued SCIT (P = .006) (Table 1 ).
Table 1.
Demographic Characteristics and State-Trait Anxiety Inventory Scores of Patients Receiving Subcutaneous Immunotherapy and Their Parents
| Characteristic | Continued SCIT, adherent (n = 39) | Continued SCIT, nonadherent (n = 23) | Discontinued SCIT (n = 16) | P valuea (adherent vs nonadherent) | P valueb (continued vs discontinued) |
|---|---|---|---|---|---|
| Patient sex, n (%) | |||||
| Female | 24 (61.5) | 14 (60.8) | 11 (68.7) | .85 | .58 |
| Male | 15 (38.5) | 9 (39.2) | 5 (31.3) | ||
| Patient age (y) | |||||
| Mean ± SD | 14.4 ± 3.6 | 15.5 ± 3.38 | 14.9 ± 3.32 | .25 | .90 |
| Parental age (y) | |||||
| Mean ± SD | 42.5 ± 5.8 | 43.35 ± 6.65 | NA | .63 | — |
| Phase of SCIT, n (%) | |||||
| Build-up phase | 16 (41) | 0 (0) | 10 (62.5) | <.001 | .006 |
| Maintenance phase | 23(59) | 23 (100) | 6 (37.5) | ||
| Patient state anxiety score | |||||
| Mean ± SD | 33.24 ± 7.08 | 35.5 ± 8.38 | NA | .33 | — |
| Patient trait anxiety score | |||||
| Mean ± SD | 34.39 ± 7.38 | 39.5 ± 8.5 | NA | .02 | — |
| Parental state anxiety score | |||||
| Mean ± SD | 36.89 ± 9.86 | 39.11 ± 8.10 | NA | .40 | — |
| Parental trait anxiety score | |||||
| Mean ± SD | 40.37 ± 7.87 | 42.84 ± 7.47 | NA | .26 | — |
Abbreviations: NA, not applicable; SCIT, subcutaneous immunotherapy.
P values in the 5th column refer to the comparisons between adherent and nonadherent patients using the chi square and student t-test.
P values in the last column refer to the comparisons between continued and discontinued patients using the chi square and student t-test.
A total of 23 patients exceeded the recommended between-dose intervals. When asked regarding the reason for SCIT nonadherence, 22 patients cited fear of COVID-19 transmission and 1 patient had to extend the dosing interval owing to quarantine (because his father had a confirmed COVID-19 infection).
Among the patients who continued treatment, the mean state anxiety score was 35.6 (±8.3) (min-max: 20-54) and the mean trait anxiety score was 33.7 (±7.5) (min-max: 23-52). Among the parents, the mean state and trait anxiety scores were 36.6 (±9) (min-max: 21-54) and 40.9 (±7.6) (min-max: 25–58), respectively. A comparison of patients who continued to adhere to the SCIT dose schedule during the pandemic and those who continued treatment but with nonadherence revealed no statistically significant difference in patient state anxiety score or parental state and trait anxiety scores (P =.33; .04; .26 respectively), whereas trait anxiety score was higher among nonadherent patients compared with adherent patients (P = .02) (Table 1).
It is recommended to continue treatment with extended dose intervals for patients already receiving SCIT.8 All of our patients started SCIT before the pandemic. Patients in the build-up phase accounted for a significant proportion of patients who discontinued treatment. Patients in the build-up phase had only been receiving treatment for a few months and had to come every 2 weeks until this phase was complete. In contrast, patients in the maintenance phase had been visiting our hospital clinic for treatment for years and needed to come every 6 weeks during the pandemic. The higher rate of treatment cessation during the build-up phase may be attributed to the fact that these patients had invested less time in treatment before the pandemic and were being required to visit a hospital clinic more frequently.
Yuan et al6 reported that anxiety was more pronounced in the parents of children hospitalized during the pandemic. Our patients were present in the hospital for approximately 1 hour to receive SCIT. Our evaluation revealed that there was no difference in patient or parental state anxiety and parental trait anxiety between the adherent and nonadherent groups, whereas trait anxiety was higher among nonadherent patients. The patients in our sample were predominantly adolescents. Our findings are consistent with the data from studies indicating that in this age group, the patients themselves have a greater effect on treatment processes.10
In conclusion, half of our patients were fully adherent to SCIT during the pandemic. The trait anxiety level of the patients was the only patient or parental anxiety factor associated with poorer SCIT adherence. Therefore, we believe that treatment adherence may be improved if allergists refer the patients who were observed to be particularly anxious for child psychiatric evaluation.
Acknowledgments
The authors thank the following members of the Division of Allergy and Immunology, Department of Pediatrics, Ankara City Hospital, Ankara, Turkey, for their assistance with this article: Muge Toyran, MD, Ersoy Civelek, MD, and Betul Karaatmaca, MD. The authors also thank Esra Cop, MD (Department of Child and Adolescent Psychiatry, Ankara City Hospital, Ankara, Turkey) for her help in the interpretation of anxiety inventory scales of our patients and their parents.
Footnotes
Disclosures: The authors have no conflicts of interest to report.
Funding: The authors have no funding sources to report.
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