key: cord-0991045-h8at8x03
authors: Liu, Shuang; Cao, Yang; Du, Tian; Zhi, Yuxiang
title: Prevalence of comorbid asthma and related outcomes in COVID-19: a systematic review and meta-analysis
date: 2020-12-09
journal: J Allergy Clin Immunol Pract
DOI: 10.1016/j.jaip.2020.11.054
sha: 4b8d29c50d8c9e8ce3662b21d0dfcd951c369e8a
doc_id: 991045
cord_uid: h8at8x03

Background The impact of asthma on COVID-19 remains largely unknown. Objective To investigate the asthma prevalence among COVID-19 patients and compare outcomes between asthma and non-asthma patients. Methods In this systematic review and meta-analysis, we searched PubMed, Embase, Web of Science, Biorxiv and Medrxiv for studies reporting asthma prevalence in general COVID-19 patients or comparing outcomes between asthma and non-asthma patients, and excluded duplicate publications, reviews, editorials, comments, single case reports or small case series (<10 cases). We determined the pooled estimates of effect using random-effect-model. Results Based on 131 studies (410382 patients), we found great variability in the prevalence of comorbid asthma among COVID-19 patients in different countries or regions ranging from 1.1% to 16.9%. No significant difference in asthma prevalence was found between hospitalized and non-hospitalized (RR: 1.15, 95% confidence interval: 0.92-1.43), severe and non-severe (RR: 1.21, 95% confidence interval: 0.92-1.57), ICU and non-ICU (RR: 1.19, 95% confidence interval: 0.92-1.54,), dead and survived (RR: 0.90, 95% confidence interval: 0.73-1.11), intubated/mechanically ventilated and non-intubated/mechanically ventilated (RR: 0.91, 95% confidence interval: 0.71-1.17) COVID-19 patients. Asthmatic patients have a lower risk of death compared with non-asthmatic patients (RR: 0.65, 95% confidence interval: 0.43-0.98). Asthma is not associated with higher risk of intubation or mechanical ventilation (RR: 1.03, 95% confidence interval: 0.72-1.46). Conclusions There is great variability in asthma prevalence among COVID-19 patients in different countries or regions. Asthma is not associated with higher COVID-19 severity or worse prognosis, and asthmatic patients are found to have lower risk of death compared with non-asthmatic patients.

intubation/mechanical ventilation (RR: 0.91, 95% CI: 0.71-1.17, p=0.42, I 2 =46.9%, 221 Figure 3e ). These findings suggest that asthma was not more prevalent among 222 COVID-19 patients with more severe disease courses. No significant publication bias 223 was detected by contour-enhanced funnel-plot and Egger test. 224

In addition, a comparison of clinical outcomes between asthmatic and non-asthmatic 226 patients, could provide better information on the relationship between comorbid 227 asthma and COVID-19 mortality. By combining 6 studies reporting the outcome of 228 death among asthma and non-asthma COVID-19 patients, we found that the death risk 229 was even lower in asthmatic COVID-19 patients (RR: 0.65, 95% CI: 0.43-0.98, 230 p=0.04, I 2 =0.0%, Figure 4a ) than the non-asthmatic COVID-19 patients. We also 231 found that asthma patients were not associated with significantly higher risk of 232 intubation or mechanical ventilation (RR: 1.03, 95% CI: 0.72-1.46, p=0.83, I 2 =0.0%, 233 Figure 4b ) based on 4 studies reporting relevant outcomes. No significant publication 234 bias was detected by contour-enhanced funnel-plot and Egger test. Table 2 lists the 235 reported COVID-19 outcomes in asthma and non-asthma patients. No significant 236 difference in asthma prevalence was reported in terms of length of hospitalization, 237 ICU admission and severity rate. Currently, meta-analysis focusing on the relationship between COVID-19 and asthma 242 is lacking. To the best of our knowledge, this meta-analysis is the first to produce a 243 pooled estimate of asthma comorbidity rate and related outcomes based on a large 244 COVID-19 population (over 400,000 patients). To identify the most comprehensive 245 original studies, we performed systematic literature search in both databases and 246 preprint websites, and updated the search during the analysis. Our results revealed 247 great variability in the prevalence of comorbid asthma among COVID-19 patients in 248 different countries or regions. We also found that the prevalence of asthma was not 249 higher in COVID-19 patients who need more intensive treatment (hospitalization, 250 ICU admission, intubation or mechanical ventilation), with higher clinical severity, or 251 have worse outcome (death). When compared with non-asthmatics, a lower risk of 252 death was found in asthmatic COVID-19 patients. No significant difference was 253 reported in terms of other clinical outcomes between these two groups of patients. 254

Altogether, our results suggest that asthma is not associated with more severe 255 COVID-19 phenotypes. 256 257 From the perspective of pathophysiology, it is reasonable to anticipate asthma as a 258 risk factor for higher susceptibility to COVID-19. First, asthmatic patients are known 259 to have deficient antiviral immune response that may predispose them to elevated 260 susceptibility to viral infection 6 . Interferon responses, which play a central role in 261 antiviral immune response, are deficient in asthmatic patients due to impaired 262 J o u r n a l P r e -p r o o f 14 production 18-21 and damping effect of immunoglobulin (Ig) E cross-linking 21 . Second, 263 asthmatic patients have a tendency for exacerbation elicited by common respiratory 264 viruses, and are associated with severe adverse outcomes 22 . Based on these theoretical 265 associations, current Centers for Disease Control guidelines warned that patients with 266 moderate to severe asthma may be at increased risk for more severe disease course 267 with COVID-19 23 . However, this theoretical association was not validated by 268 real-world observations. The results based on currently available data showed high 269 variable asthma comorbidity rates, and most of the original studies failed to 270 distinguish physician-diagnosed from self-reported asthma, making it hard to 271 determine whether asthma plays a predisposing or protective role in susceptibility. 273

Despite the concern that patients with asthma might suffer more severe 275 the current analyses did not indicate that asthma aggravates COVID-19 disease course. 276

We firstly reported that asthma was not more prevalent among COVID-19 patients 277 with more severe disease courses. Then by comparing the clinical outcomes between 278 asthmatic and non-asthmatic patients, we further found that asthma did not increase 279 the risk of intubation or mechanical ventilation, and might even be associated with 280 lowered death risk. The above findings are consistent in suggesting that asthma is not 281 associated with elevated death risk of COVID-19, which is against the previous public 282

concern. The theoretical mechanisms may include the role of type 2 immune response 283 and other physiological changes associated with the asthmatic state, asthma 284 medications, and behavioral aspects. As stated in our previous review article 24 , certain 285 aspects of type 2 immune response have the potential to provide protection against 286 COVID-19 to some extent. Some type 2 cytokines (interleukin (IL)-4, 287 etc.) have inhibitory effects on the production of pro-inflammatory cytokines 288 tumor necrosis factor-α, etc.), the over-activation of which is proposed to be a 289 potential pathological mechanism for COVID-19 progression. Recruitment and 290 activation of effector cells, including mast cells, eosinophils, and basophils, may also 291 modulate the immune response against SARS-CoV-2. Local eosinophilia, which is 292 characteristic of asthma, may also act on viral clearance by releasing ribonucleases, 293 although the association between eosinophil and COVID-19 disease course is 294 inconclusive 25 . In addition, mucus over-produced during the type 2 immune response 295 may also serve as a physical barrier against viral invasion 26 . Respiratory allergy and 296 controlled allergen exposures are associated with reduced expression of 297 angiotensin-converting enzyme (ACE Ⅱ 2), which is the entry receptor for 298 SARS-CoV-2 associated with in vitro susceptibility 27 . Another consideration is the 299 role of asthma medication, including inhaled corticosteroids, allergen immunotherapy, 300 and biological agents (anti-IgE monoclonal antibody, anti-IL-5 monoclonal antibody), 301 which might also be beneficial through alleviating inflammation or enhancing 302 antiviral defense. In addition, warned of the increased risk since the beginning of the 303 pandemic, asthmatic patients may better observe recommendations such as social 304 J o u r n a l P r e -p r o o f 16 distancing, personal protection and hygiene rules, which are also supposed to have 305 potential protective effects. However, the question whether asthma is associated with 306 lowered death risk of COVID-19 should be answered with great caution in case of 307 giving misleading information. Our results provided potential clues; however, 308

considering the relative small number of available studies (n=6), further evidence is 309 stilled needed to confirm the observed association. 310

There is also evidence that severe asthmatic patients did not tend to develop into more 312 severe types of COVID-19. In a large cohort study based on the Severe Asthma 313

Network in Italy, an infrequent rate of confirmed or highly-suspected COVID-19 314 (26/1504, 1.73%) is reported, which coincides with the under-reported asthma cases 315 among COVID-19 patients 28 . In the abovementioned cohort, the COVID-19 related 316 mortality rate was 7.7%, which was lower than that of the general population in Italy, 317 indicating that severe asthma does not increase the risk of SARS-CoV-2 infection and 318 disease severity. In another follow-up study in Spain, 3 of 80 (3.8%) severe asthmatic 319 patients had confirmed COVID-19 28 but no patient developed cytokine storm, acute 320 respiratory distress syndrome 29 . In addition, no increase in exacerbation of severe 321 asthma due to COVID-19 was observed during the study period 29 COPD, but case mortality rate was found to be only weakly correlated with asthma 337 (r=0.28) 32 . 338

The above articles have provided valuable information on the relationship between 340 asthma and COVID-19. However, our manuscript also provides additional 341 information regarding this issue. First, to explore the association between asthma 342 comorbidity and COVID-19 severity, we performed several subgroup analyses rather 343 than only compare whether severe COVID-19 disease was associated with increased 344 risk of asthma. Our results revealed with the risk of asthma was not increased in 345 patients requiring hospitalization compared to those not requiring hospitalization, as 346 well as in patients needing ICU admission VS no ICU admission, in patients having 347 severe diseases VS non-severe diseases, in patients with outcomes of death VS 348 survive, in patients requiring intubation/mechanical ventilation VS not requiring those 349 measures. Therefore, our manuscript provided more detailed evidence to support the 350 previous conclusion. Second, by incorporating more available studies, we found that 351 asthmatic patients had lower death risk than non-asthmatic patients, which was never 352

proposed by previous studies. Third, our analyses are based on a larger population. 353

For analysis on the association of COVID-19 severity and asthma risk, we employed 354 data from 64 articles of 308775 participants. For analysis on the asthma comorbidity 355 and COVID-19 clinical outcomes, we used data from 6 articles representing 694 356 asthmatic patients and 4306 nonasthmatic patients. Therefore, although new articles 357 are emerging in this quickly-moving field, our manuscript could still provide new 358 perspectives for readers. 359 360 This study has several potential limitations. First, since available COVID-19 patients' 361 data does not represent the proportion of population in each country, a pooled asthma 362 prevalence based on meta-analysis is not directly comparable to the global asthma 363 prevalence. In this sense, it is almost impossible to know the exact asthma 364 comorbidity rate among COVID-19 patients, and to know the difference between 365 asthma prevalence among COVID-19 patients and the general population. Therefore, 366

we only calculated country-specific and regional prevalence of comorbid asthma. 367 databases were searched on July 21, 2020 for articles published since January 1, 2020. 522

Another search was performed on August 18, 2020 to include eligible articles that 523 were published between the two searches. 524 difference in asthma comorbidity rate is visualized as a colored world map, in which a 526 darkening color represents higher prevalence. The asthma comorbidity rate was 527 calculated as follows: for countries with 2 or more studies reporting the prevalence of 528 asthma in COVID-19 patients, a meta-analysis was performed to estimate the pooled 529 prevalence; for countries with only 1 studies on asthma prevalence in COVID-19 530 patients, asthma prevalence was calculated as (total COVID-19 patients with 531 asthma)/(total COVID-19 patients). 532 Table 1 . The prevalence of asthma in COVID-19 patients in different countries or regions. For each country/region with 2 or more studies reporting the prevalence of asthma in COVID-19 patients, a meta-analysis was performed to estimate the pooled prevalence. For country or region with only 1 available study reporting asthma prevalence in COVID-19 patients, asthma prevalence was calculated as (total COVID-19 patients with asthma)/(total COVID-19 patients). Table E1 A. Quality Assessment for observational cohort and cross-sectional studies. The National Institutes of Health (NIH) Quality Assessment Tool for observational cohort and cross-sectional studies was used to rate the quality of included studies. Answers to 14 basic questions and an overall quality rating (Good, fair or poor) were listed for each study.

Criteria for observational cohort and cross-sectional studies (Yes, No, Other-CD/NR/NA) CD: cannot determine, NR: not reported, NA: not applicable Q1: Was the research question or objective in this paper clearly stated? Q2: Was the study population clearly specified and defined? Q3: Was the participation rate of eligible persons at least 50%? Q4: Were all the subjects selected or recruited from the same or similar populations (including the same time period)? Were inclusion and exclusion criteria for being in the study prespecified and applied uniformly to all participants? Q5: Was a sample size justification, power description, or variance and effect estimates provided? Q6: For the analyses in this paper, were the exposure(s) of interest measured prior to the outcome(s) being measured? Q7: Was the timeframe sufficient so that one could reasonably expect to see an association between exposure and outcome if it existed? Q8: For exposures that can vary in amount or level, did the study examine different levels of the exposure as related to the outcome (e.g., categories of exposure, or exposure measured as continuous variable)? Q9: Were the exposure measures (independent variables) clearly defined, valid, reliable, and implemented consistently across all study participants? Q10: Was the exposure(s) assessed more than once over time? Q11: Were the outcome measures (dependent variables) clearly defined, valid, reliable, and implemented consistently across all study participants? Q12: Were the outcome assessors blinded to the exposure status of participants? Q13: Was loss to follow-up after baseline 20% or less? Q14: Were key potential confounding variables measured and adjusted statistically for their impact on the relationship between exposure(s) and outcome(s)? Table E1 . C. Quality Assessment for case-control studies. The National Institutes of Health (NIH) Quality Assessment Tool for case-control studies was used to rate the quality of included studies. Answers to 12 basic questions and an overall quality rating (Good, fair or poor) were listed for each study.

CD: cannot determine, NR: not reported, NA: not applicable Q1: Was the research question or objective in this paper clearly stated and appropriate?Q2: Was the study population clearly and fully described, including a case definition? Q2: Was the study population clearly specified and defined? Q3: Did the authors include a sample size justification? Q4: Were controls selected or recruited from the same or similar population that gave rise to the cases (including the same timeframe)? Q5: Were the definitions, inclusion and exclusion criteria, algorithms or processes used to identify or select cases and controls valid, reliable, and implemented consistently across all study participants? Q6: Were the cases clearly defined and differentiated from controls? Q7: If less than 100 percent of eligible cases and/or controls were selected for the study, were the cases and/or controls randomly selected from those eligible? Q8: Was there use of concurrent controls? Q9: Were the investigators able to confirm that the exposure/risk occurred prior to the development of the condition or event that defined a participant as a case? Q10: Were the measures of exposure/risk clearly defined, valid, reliable, and implemented consistently (including the same time period) across all study participants? Q11: Were the assessors of exposure/risk blinded to the case or control status of participants? Q12: Were key potential confounding variables measured and adjusted statistically in the analyses? If matching was used, did the investigators account for matching during study analysis? J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f 

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OR "retrospective studies

OR "control group

OR longitudinal studies[mesh:noexp] OR follow-up studies[mesh:noexp] OR prospective studies[mesh:noexp] OR retrospective studies

OR cross-sectional

OR "clinical trials, phase i as topic

Epidemiologic Studies

13# 7# OR 8# OR 9# OR 10# OR 11# OR 12#

Heterogeneity: I 2 = 99.2%, τ 2 = 0.0213, p = 0 

Arjun S. Yadaw (153) 2  44  190  6  74  42  5321  280  18  17  36  230  109  146  2  180  9  6  2  249  1  1229  19  39  274  38  13   Total   236765   63  308  4635  46  634  626  185075  1372  190  75  301  2884  1001  2988  60  4043  245  104  108  3286  445  6710  293  1077  19768 276 152

Heterogeneity: I 2 = 0.0%, t 2 = 0, p = 0.80