key: cord-0684658-naaj8dt8
authors: Ekström, Sandra; Mogensen, Ida; Georgelis, Antonios; Westman, Marit; Almqvist, Catarina; Melén, Erik; Bergström, Anna; Kull, Inger
title: General stress among young adults with asthma during the COVID-19 pandemic
date: 2021-11-14
journal: J Allergy Clin Immunol Pract
DOI: 10.1016/j.jaip.2021.10.069
sha: 86737b7c1098e2414c4bdd858d7c3b11497f4f00
doc_id: 684658
cord_uid: naaj8dt8

Background The COVID-19 pandemic has profoundly affected the lives of the global population. Objective To explore anxiety and stress in relation to COVID-19 among young adults, and the potential influence of asthma and allergic rhinitis. Methods This cross-sectional study included 1,644 participants from the population-based birth cohort BAMSE, participating in a follow-up at 24 years of age and a COVID-19 follow-up conducted in August-November 2020 (mean age 25.3 years). Anxiety and concern related to COVID-19 were analyzed as general anxiety, concern of own health and health of family members, and contact with online healthcare providers due to concern about COVID-19. Stress was measured with the perceived stress scale (PSS-10). Results Around half of the participants reported increased anxiety due to COVID-19 and this was more common among females (57.0%, compared to 42.6% in males, p<0.001). Young adults with asthma reported more concern about their own health (adjusted odds ratio (adj OR): 1.50, 95% confidence interval (CI): 1.12-2.02) and perceived stress (adjusted regression coefficient (adj β): 1.49 CI: 0.52-2.45) compared to peers without asthma, and this was more pronounced among females and those with uncontrolled asthma. Symptoms of allergic rhinitis were not associated with increased concern or anxiety in relation to COVID-19. Conclusion Young adults with asthma experience more COVID-19 related health concerns, compared to those without asthma; especially females and participants with uncontrolled asthma This needs to be considered in the care of young people with asthma.

The COVID-19 pandemic has profoundly affected the lives of the global population. 48

Objective 49

To explore anxiety and stress in relation to COVID-19 among young adults, and the potential 50 influence of asthma and allergic rhinitis. 51

This cross-sectional study included 1,644 participants from the population-based birth cohort BAMSE, 53 participating in a follow-up at 24 years of age and a COVID-19 follow-up conducted in August-54

November 2020 (mean age 25.3 years). Anxiety and concern related to COVID-19 were analyzed as 55 general anxiety, concern of own health and health of family members, and contact with online 56 healthcare providers due to concern about COVID-19. Stress was measured with the perceived stress 57 scale (PSS-10). 58

Around half of the participants reported increased anxiety due to COVID-19 and this was more 60 common among females (57.0%, compared to 42.6% in males, p<0.001). Young adults with asthma 61

reported more concern about their own health (adjusted odds ratio (adj OR): 1.50, 95% confidence 62 interval (CI): 1.12-2.02) and perceived stress (adjusted regression coefficient (adj β): 1.49 CI: 0.52-63 2.45) compared to peers without asthma, and this was more pronounced among females and those with 64 uncontrolled asthma. Symptoms of allergic rhinitis were not associated with increased concern or 65 anxiety in relation to Conclusion 67

Young adults with asthma experience more COVID-19 related health concerns, compared to those 68 without asthma; especially females and participants with uncontrolled asthma This needs to be 69 considered in the care of young people with asthma. Early adulthood is for most individuals an active period of life, when intensive social interaction with 94 friends, starting a new family, the beginning of a working career and many founding events for the rest 95 of life may take place. The COVID-19, caused by SARS-CoV-2 virus, has profoundly affected the 96 lives of a large part of the global population since it was declared a pandemic by the World Health 97

Organization in March 2020 1 . The measures taken to reduce the spread such as quarantines, travel 98 bans, and restrictions on public gatherings have caused a major impact socially and economically on 99 people in addition to the threat of the disease in itself 2 . In Sweden, in contrast to many other countries, 100 no lock-down has been imposed, although several restrictions (such as closed universities and schools 101 for adolescents, prohibition of larger gatherings and recommendations against visiting people over 70 102 years of age) have been implemented 3 . Still, among young people, often having a large part of their 103 social lives outside the family, these restrictions may have had a major impact on psychological 104

Asthma, the most common respiratory condition among young adults 4 , was early suspected to be a 106 risk factor for severe COVID-19 5 , especially when uncontrolled or undertreated. This was based on 107 the experience that asthma exacerbations and loss of asthma control is commonly triggered by 108 respiratory viral infections and tends to be worse in uncontrolled asthma 6 . Also, allergic rhinitis was 109 early linked to COVID-19 infection and a worse outcome of the disease 7 . However, in the majority of 110 studies performed later, asthma or allergic rhinitis has not been linked to an increased risk of 111 becoming diagnosed with COVID-19 8 or developing a more severe COVID-19 disease 9-12 . 112

There have been several studies observing an increase in anxiety and worse mental health since the 113 onset of the pandemic 13 14 , and female sex has been found to be a risk-factor for COVID-19 related 114 anxiety 13 . One Swedish study of mental health symptoms in adults during the beginning of the 115 pandemic found physical risk factors, including respiratory conditions, to have a significant correlation 116 to anxiety and insomnia 15 . In contrast, a study conducted among university students, also in Sweden, 117 found no increase in levels of stress, anxiety or depression compared to before the onset of the 118 pandemic 16 . However, specific data on increased anxiety and perceived stress in young adults with asthma and allergic disease related to the COVID-19 pandemic are missing. It is important to 120 investigate COVID-19 related anxiety in individuals with asthma, since anxiety previously has been 121 shown to be related to asthma both in childhood and later 17 18 and clinical worsening among middle 122 aged individuals with severe asthma 19 . Uncontrolled asthma has in turn been found to associate with 123 worse quality of life 20 . Allergic rhinitis and atopic diseases have also been reported to associate with 124 increased anxiety 17 21 , however, so far no association between allergic rhinitis and increased levels of 125 anxiety has been established in relation to . 126

The aim of the present study was to describe the prevalence of COVID-19 related anxiety and stress 127 among young adults from a population-based Swedish birth cohort approximately 6 months into the 128 COVID-19 pandemic, and to explore the potential influence of asthma and symptoms of allergic 

The study population includes participants from the population-based prospective birth cohort 134 BAMSE, previously described in detail 23 . The BAMSE cohort originally includes 4,089 participants, In August 2020, a new follow-up of the BAMSE cohort was initiated, focusing on long-term effects of 142 COVID-19 (referred to as the COVID-19 follow-up). All 2270 participants who completed the clinical 143 investigation at the 24-year follow-up study were invited to the study. Starting 11 August 2020, an 144 invitation letter was sent by e-mail with information about the study and a link to a web-questionnaire. 145

The questionnaire was open to answer for 3 months (until 10 November 2020) and covered questions 146 related to the COVID-19 pandemic, including mental health, stress, lifestyle factors and symptoms 147 related to asthma and allergic disease. Out of the 2,270 invited participants, 1,644 (72% of invited) 148 answered the questionnaire and were included in the current study population. The study was 149 approved by the Swedish Ethical Review Authority (approval number 2020-02922). Participants 150 provided written informed consent when answering the questionnaire. 151

Asthma was defined as having a doctor's diagnosis of asthma (ever) in combination with symptoms of 153 wheeze in the last 12 months and/or any asthma medication use in the last 12 months 25 . 154

Uncontrolled asthma was defined based on a modified version of the Global Initiative for Asthma 155 definition 26 as at least one of the following: ≥12 episodes of breathing difficulties in the last 12 156 months, activity limitation due to respiratory symptoms in the last 4 weeks, night time awakening due to respiratory symptoms in the last 4 weeks, regular use of short-acting beta agonists in the last 4 158

Symptoms of allergic rhinitis was defined as having symptoms, from the eyes or nose after exposure 160 to pollen or furred animals without simultaneous common cold or flu in the last 12 months. 161

Anxiety and concern related to COVID-19 were analyzed as general anxiety, concern about the health 163 of own family or close relatives, concern for own health, and contact with online healthcare providers 164 due to concern about COVID-19. The following questions were used to define these outcomes: 165

Have you felt increased concern about the health of your family/close relatives due to Have you felt increased concern about your own health due to Have you been in contact with online healthcare providers due to concerns about COVID-19? question has five answer categories from "never" to "very often" which are given 0 to 4 points 173 depending on the answers (scores are reversed for four questions with positive statements), in total 0-174 40 points. Complete data on the questions included in the PSS-10 score was provided by 1626 of the 175 1644 participants. 176

Information on current occupation, current smoking, and reduction in social activities during the 178 COVID-19 pandemic was collected in the COVID-19 follow-up questionnaire, whereas body mass 179 index (BMI) was calculated based on measured weight and height at the 24-year examination. 180

Occupation was categorized as student, worker, and other (including "parental leave or unpaid leave", 181 "unemployed", "furloughed due to the current pandemic" or "other"). Current smoking was defined as 182 daily or occasional smoking. BMI status was categorized into underweight (<18.5 kg/m 2 ), normal 183 weight (18.5-24.9 kg/m 2 ), overweight (25-29.9 kg/m 2 ) or obesity (≥30 kg/m 2 ) using normal weight as 184 the reference group. 185

Descriptive data are presented as number (n) and percent (%) for categorical variables (background 187 factors, covariates, asthma, asthma control, allergic rhinitis, and anxiety/concern) and as mean and 188 standard deviation (SD) for PSS-score. Differences in background factors between the groups 189 reporting no increased versus increased anxiety due to the COVID-19 pandemic were assessed with 190 chi-squared tests. Differences between sex with regards to anxiety, concern and perceived stress were 191 tested using the chi-squared test for categorical variables and the t-test for PSS-score. 192

Logistic regression analyses were performed to investigate the associations between the exposures 193 (asthma, asthma control, symptoms of allergic rhinitis) and anxiety/concern in relation to 194 in crude models and in models adjusted for sex, current occupation, current smoking, and BMI status 

The study population (n=1,644) consisted of 996 females (60.6%) and 648 males (39.4%). Most of the 203 participants (83.6%) answered the COVID-19 questionnaire in August 2020, at a mean age of 25.3 204 years (SD 0.79). Around half of the participants (51.3%) reported increased anxiety due to COVID-19. 205 Table I shows a description of the study population in relation to reported anxiety due to COVID-19. 206

Among participants who reported increased anxiety, a lower proportion was working (47.3% 207 compared to 55.9% among those with no increased anxiety, p=0.002). The prevalence of smoking was 208 3.7% for daily smoking and 11.0% for occasional smoking, with no significant difference in relation to 209 anxiety. At 24 years, overweight and obesity was present in 17.0% and 4.3% of the participants, 210 respectively, also with no difference in relation to anxiety. Most participants reported that they had 211 reduced their social contacts during the pandemic, and this was more common among participant with 212 increased anxiety (93.8% compared to 78.9% among those with no increased anxiety, p<0.001). 213

A large proportion of the participants (83.9%) reported increased concern about the health of family 215 members and/or close relatives due to COVID-19, whereas 30.5% reported increased concern about 216 their own health due to COVID-19 (Table II) . These aspects of anxiety/concern were more common 217 among females, compared to males (all p<0.05, Table II ). Around 1 in 10 (10.6%) reported that they 218 had been in contact with an online healthcare provider due to worry against COVID-19, with no 219 significant difference with regards to sex. 220 PSS-10 scores ranged from 0-36 points, with a mean of 14.9 (SD 7.2) points and a median of 14 221 points. Females had higher mean PSS-10 scores compared to males (14.9 points vs. 13.1 points, 222 p<0.001, Table II) . 223

The prevalence of asthma according to definition was 14.1% (15.3% in females and 12.2% in males, 224 p=0.08) and the prevalence of symptoms of allergic rhinitis was 43.6% (44.8% in females and 41.7% 225 J o u r n a l P r e -p r o o f in males, p=0.22). Among the participants with asthma at the COVID-19 follow-up (n=231), 29.4% 226 had uncontrolled asthma, 31.6% in females and 25.3% in males, p=0.32. 227

Perceived stress and anxiety/concern due to COVID-19 in relation to asthma and allergic 228 rhinitis 229

Compared to participants without asthma, participants with asthma reported more concern about own 230 health due to COVID-19 (39.4% vs. 29.0%, p=0.001) and more contact with online healthcare due to 231 concerns for COVID-19 (14.7% vs. 10.0%, p=0.03), while there was no difference in increased 232 anxiety (in general) or in increased concern about the health of family or close relatives (Table III) . 233

These associations were confirmed in the adjusted regression models (adj. OR for increased concern 234 about own health: 1.50, 95% CI 1.12-2.02, and adj. OR for contact with online healthcare: 1.52, 95% 235 CI 1.01-2.28). Asthma was also associated with a higher PSS-10 score (16.4 compared to 14.6, adj. β 236 1.49, 95% CI 0.52-2.45). Symptoms of allergic rhinitis was not associated with increased 237 anxiety/concern, but a slightly higher PSS-10 score (15.3 compared to 14.6, p=0.04), significant in the 238 unadjusted model only (Table III) . 239

Since females reported more anxiety and concern than males, Figure 1 shows the prevalence of 240 increased anxiety/concern in relation to COVID-19 by sex and asthma status. This result showed that 241 the increased concern about own health among participants with asthma was statistically significant 242 among females (44.7% among females with asthma compared to 33.3% among females without 243 asthma, p=0.007), but not males (29.1% among males with asthma compared to 22.5% among males 244 without asthma, p=0.20). Additionally, the association between asthma and contact with online 245 healthcare was only present among females while no association was observed among males ( Figure  246 

Perceived stress and anxiety/concern due to COVID-19 in relation to asthma control 248

Among the 231 participants with asthma, uncontrolled asthma was associated with increased concern 249 about own health (OR 1.86, 95% CI 1.05-3.30) and higher PSS-10 score (β 2.35, 95% CI 0.36-4.35) in 250 the unadjusted models (Table IV) . These associations were somewhat attenuated and no longer significant in the adjusted models (adj OR 1.76, 95% CI 0.98-3.18 and adj β 1.83, 95% CI -0.11-3.77, 252 respectively). Uncontrolled asthma was associated with lower concern for family or close relative's 253 health due to COVID-19 in both models (adj OR 0.31, 95% CI 0.14-0.71). There were no significant 254 associations between asthma control and increased anxiety due to COVID-19 (in general) or with 255 contact with online healthcare due to concerns for COVID-19. In the present study, based on data from a population-based cohort, the main aim was to investigate 260 COVID-19 related anxiety and stress in young adults and the potential influence of asthma and 261 symptoms of allergic rhinitis. Around half of the participating young adults reported increased anxiety, 262 and this was more common among females, compared to males. Participants with asthma expressed 263 more COVID-19 related concern about their own health, reported more contact with online healthcare 264 and perceived more stress than participants without asthma, this was more pronounced among females 265 with asthma and in participants with uncontrolled asthma. Participants with symptoms of allergic 266 rhinitis did not report more anxiety or concerns related to COVID-19 than participants without 267 symptoms of allergic rhinitis, although they had a somewhat higher level of perceived stress assessed 268 with the PSS-10 questionnaire. 269

Individuals with respiratory diseases have been identified as a risk group for COVID-19, even if data 270 regarding asthma have pointed towards a low or absent risk increase both to become infected and to 271 become severely ill in COVID-19 7 8 10 28 29 . Still, our data suggest asthma to be associated with more 272 health-related concerns due to COVID-19 also among young, in general healthy, individuals. This 273 confirms that previous findings on an association between anxiety and asthma in children 18 and adults 274 17 are highly relevant also for concerns due to COVID-19. 275

The COVID-19 pandemic has been shown to increase anxiety in the general population in Sweden and 276 elsewhere 15 30-32 . Also younger age, not targeted as a risk factor, has been reported to correlate with 277 poorer mental health related to the COVID-19 pandemic 15 . Female sex has been identified as a risk 278 for more COVID-19 related anxiety symptoms 13 , despite male sex being associated with a higher risk 279 for COVID-19 related death 28 . In the present study, females were also more anxious in relation to 280 COVID-19 in general and about both their own as well as close relatives' health compared to males, 281 and even more so among females with asthma. In contrast obesity, an established risk factor for severe 282 COVID-19 33 , was not found to be more common in the group with increased anxiety. The group with 283 increased anxiety had however, to a higher extent, reduced their social contacts, compared to those who reported no increased anxiety. In line with previous studies 22 , we did however not find increased 285 anxiety due to COVID-19 in participants with symptoms of allergic rhinitis. 286

In the beginning of the pandemic, asthma was hypothesised to be an important risk factor for severe 287 disease and death, which may have impacted on health-related anxiety in individuals with asthma 5 . 288 However, it may be possible that anxiety has lessened in subsequent months of the pandemic since 289 more recent studies indicated that asthma does not increase the risk of severe COVID-19. Another 290 factor possibly increasing the anxiety among asthmatics is the lower access to regular health care 291 during the pandemic. A qualitative British study investigating fears and anxiety related to COVID-19 292 among individuals with chronic respiratory conditions (including asthma) among adults, revealed not 293 only fears for being at higher risk but also for not being prioritized by the health care due to the pre-294 existing condition 34 . In line with these results, we found that participants with uncontrolled asthma 295 experienced more concern about their own health in relation to COVID-19. However, they expressed 296 less concerns about their family or close relatives' health in relation to COVID-19 than participants 297 with controlled asthma. This finding was somewhat unexpected, and possibly reflects that 298 uncontrolled asthma is a highly stressful condition, leaving less room for focus on other concerns. 299

The strengths of the present study include the well characterized study population of young adults 300 from a population-based cohort with information collected recently before and around 6 months after 301 the onset of the COVID-19 pandemic. The population-based design contributes with information on 302 asthma of different severity, in contrast to data from a clinic. The included population is relatively 303 large and has a high response rate. 304

There are however limitations with our study. Due to the population-based design, the group with 305 asthma contains a limited number of individuals, especially when divided in controlled and 306 uncontrolled asthma. Further, the data on health care contacts due to the pandemic are self-reported, 307 however with a low risk of recall bias with questions covering a relatively short period of time (6 308 months). We had no information on anxiety related disorders from before the onset of the pandemic 309 and were not able to adjust for pre-pandemic levels of stress and anxiety potentially higher in 310 individuals with asthma or allergic disease 17 18 2135 However, our study did specifically measure anxiety and concerns related to COVID-19, not general anxiety or health concerns. The higher level of 312 perceived stress found both in participants with asthma and allergic rhinitis was in contrast not asked 313 in relation to COVID-19 and could possibly reflect the generally higher stress level associated to these 314 conditions 36 37 . 315

In conclusion, our results found young people at risk for increased anxiety and perceived stress 316 associated with COVID-19. Looking specifically at the group with asthma, COVID-19 related 317 concerns about their own health was further increased and especially if asthma was uncontrolled. This 318 emphasises the need of awareness in caregivers regarding the risk of increased anxiety in vulnerable 319

individuals not necessarily at higher risk. Table I Table II . Descriptive results on anxiety and concern due to COVID-19, and perceived stress score (PSS-10) in relation to sex (n=1644)

All ( J o u r n a l P r e -p r o o f Table III . Anxiety and concern due to COVID-19, and perceived stress score (PSS-10), in relation to asthma and symptoms of allergic rhinitis (n=1644) Table IV . Anxiety and concern due to COVID-19, and perceived stress score (PSS-10), in relation to asthma control among participants with asthma (n=231) J o u r n a l P r e -p r o o f b) Increased concern for family or close relative's health due to COVID-19 446 c) Increased concern about own health due to COVID-19 447 d) Contact with online healthcare due to concerns for COVID-19, by sex and asthma status at the 448 COVID-19 follow-up. 

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