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editorial
. 2020 Aug 13;56(2):2002108. doi: 10.1183/13993003.02108-2020

COVID-19 and COPD

Janice M Leung 1,2, Masahiro Niikura 3, Cheng Wei Tony Yang 1, Don D Sin 1,2,✉
PMCID: PMC7424116  PMID: 32817205

As of 11 July, 2020, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus responsible for the coronavirus disease 2019 (COVID-19) pandemic has infected over 12.7 million people around the world and caused more than 560,000 deaths [1]. Given the devastating impact that COVID-19 can have on the lung, it is natural to fear for patients with underlying COPD. Estimating their excess risk for contracting COVID-19 and, in particular, its more severe respiratory manifestations has been a challenging exercise in this pandemic for various reasons. First, the reporting on cases has concentrated on hospitalised and intensive care unit (ICU) patients, rather than on mild, outpatient cases. This is in part also due to the variability in testing strategies across the world, where some nations with stricter testing requirements and scarce testing resources have focused on testing only those requiring hospitalisation.

Short abstract

COPD patients have increased risk of severe pneumonia and poor outcomes when they develop COVID-19. This may be related to poor underlying lung reserves or increased expression of ACE-2 receptor in small airways. https://bit.ly/37dSB8l

Is COPD a risk factor for COVID-19?

As of 11 July, 2020, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus responsible for the coronavirus disease 2019 (COVID-19) pandemic has infected over 12.7 million people around the world and caused more than 560,000 deaths [1]. Given the devastating impact that COVID-19 can have on the lung, it is natural to fear for patients with underlying COPD. Estimating their excess risk for contracting COVID-19 and, in particular, its more severe respiratory manifestations has been a challenging exercise in this pandemic for various reasons. First, the reporting on cases has concentrated on hospitalised and intensive care unit (ICU) patients, rather than on mild, outpatient cases. This is in part also due to the variability in testing strategies across the world, where some nations with stricter testing requirements and scarce testing resources have focused on testing only those requiring hospitalisation. We have also not yet quantified how many COPD patients might have chosen never to present to a hospital in this pandemic, only to subsequently appear in the statistics for excess mortality during this time [2, 3]. Second, the underestimation of COPD in the general population is a problem that predates the COVID-19 era [4–6] and one that is likely to be exacerbated in overburdened hospitals where the precise ascertainment of comorbidities may be overlooked and spirometry cannot be performed. Moreover, how the diagnosis of COPD has been adjudicated in these studies has not been clearly delineated, possibly giving rise to variability in prevalence across the world.

Due to the earlier time course of infections there, our most thorough snapshot of COPD in COVID-19 is from China, where the background rate of COPD is 13.6% in adults aged >40 years [7]. The vast majority of these studies have centred on hospitalised patients, with only one to date including both hospitalised patients and outpatients (of which only 1.1% carried a diagnosis of COPD [8]) and one considering asymptomatic patients (of which only 1.6% had COPD [9]). For cohorts in China reporting on hospitalised patients, the prevalence of COPD has ranged from 0 to 10% (table 1) [10–41]. As data from other nations have trickled in, the figures for COPD amongst hospitalised COVID-19 patients appear to be similar, with estimates in New York City ranging from 2.4 to 14% [42–45] and in Italy ranging from 5.6 to 9.2% [46–48]. Data from ICU-only cohorts, however, have been more variable. One cohort in Italy totalling 1591 ICU patients [49] and one in Seattle with 24 ICU patients noted COPD rates of 4% in each [50]. Much higher prevalence has been reported in a Spanish ICU of 48 patients, of which 38% had COPD [51], and in another Seattle ICU of 21 patients, where 33% had COPD [52], although the small size of these studies must be kept in mind. To provide context, the prevalence of COPD in northern Italy, Spain, New York state, and Washington state is 11.7% [53], 10.2% [54], 5.8% [55], and 4.1% [56], respectively. Other cohorts that have reported more broadly on chronic pulmonary diseases without necessarily specifying COPD still show considerable variability. These numbers have ranged from as low as 2.0% in a Shanghai cohort of 249 hospitalised patients, to up to 17.7% of 20 133 hospitalised patients in the UK. Still, these numbers are less than those reported for other comorbidities, such as hypertension and diabetes.

TABLE 1.

COPD and smoking prevalence in coronavirus disease 2019 patients

Study [ref.] Location Subjects n Age# Female Type of patient Smoking rate COPD rate COPD prevalence by outcome p-value
Guan [8] China 1099 47.0 41.9% Hospitalised and outpatients Current 12.6%; former 1.9% 1.1% Severe 3.5% NA
Non-severe 0.6%
Met primary endpoint 10.4% NA
Did not meet primary endpoint 0.5%
Wang [10] China 138 56 45.7% Hospitalised NA 2.9% ICU 8.3% 0.054
Non-ICU 1.0%
Zhou [11] China 191 56.0 38% Hospitalised Current 6% 3% Survivor 7% 0.047
Non-survivor 1%
Huang [12] China 41 49.0 27% Hospitalised Current 7% 2% ICU 8% 0.14
Non-ICU 0
Guan [13] China 1590 48.9 42.7% Hospitalised Current and former 7% 1.5% Severe 62.5% NA
Non-severe 15.3%
ICU 29%
Non-ICU 5.9%
Mechanical ventilation 20.8%
No mechanical ventilation 2.9%
Survivor 25%
Non-survivor 2.8%
Zhang [14] China 140 57 49.3% Hospitalised Current 1.4%; former 5.0% 1.4% Severe 3.4% 0.170
Non-severe 0
Liu [15] China 78 38 50.0% Hospitalised Current and former 6.4% 10% Progression 9.1% 0.264
Improvement 1.5%
Feng [16] China 476 53 43.1% Hospitalised 9.7%+ 4.6% Critical 15.7% <0.001
Severe 5.6%
Moderate 2.3%
Li [17] China 548 60 49.1% Hospitalised Current 7.5%; former 9.4% 3.1% Severe 4.8% 0.026
Non-severe 1.4%
Wang [18] China 85 59.4 47.1% Hospitalised NA 5.9% Severe 10.3% 0.265
Non-severe 2.2%
Yan [19] China 1004 62§; 68ƒ 50.9% Hospitalised 46.0%+ 0.8% Survivors 0.8% 0.563
Non-survivors 0
Xiong [20] China 421 52 49.2% Hospitalised NA 4.3% Severe 1.7% 0.478
Recovered 4.7%
Lv [21] China 354 62 50.56% Hospitalised NA 1.69% Critical 1.19% NA
Severe 1.94%
Mild 1.74%
Zheng [90] China 34 66 32.4% ICU NA 5.9% Intubated 6.7% 1.00
Non-intubated 5.3%
Cai [22] China 383 61##; 44.5¶¶ 36.3%##; 57.2%¶¶ Hospitalised NA 8.4% Severe 14.3% 0.03
Non-severe 6.51%
Chen [23] China 548 56.0 42.9% Hospitalised Ever 5.8% 1.3% Survivors 0.4% NA
Non-survivors 4.9%
Shi [24] China 671 63 52% Hospitalised NA 3.4% Survivors 3.4% 1.00
Non-survivors 3.2%
Zou [25] China 154 60.68 56.49% Hospitalised 8.44%+ 5.84% Survivors 2.94% 0.074
Non-survivors 11.54%
Hu [26] China 323 61 48.6% Hospitalised 11.8%+ 1.9% Critical 3.8% 0.033
Severe 3.4%
Non-severe 0
Zhang [27] China 111 38.0 65% Hospitalised NA 2.7% Deterioration 5.6% 0.415
Discharge 2.2%
Chu [91] China 33 65.2 33.3% ICU NA 3.0% ECMO 14.3% 0.21
No ECMO 0
Wang [28] China 107 51.0 46.7% Hospitalised NA 2.8% Survivors 2.3% 0.447
Non-survivors 5.3%
Lagi [46] Italy 84 62 34.5% Hospitalised Current 7.1%; former 22.6% 5.6% ICU 18.8% 0.045
Non-ICU hospitalisation 2.9%
Tomlins [92] UK 95 75 37% Hospitalised NA 11% Survivors 8% 0.2
Non-survivors 20%
Israelsen [93] Denmark 175 71 51.4% Hospitalised Ever 55.8%
Never 44.2%		 6.3% ICU 7.4% 1.00
Non-ICU hospitalisation 6.1%
Auld [94] Atlanta, GA, USA 217 64 45.2% ICU NA 9.7% Survivors 9.5% 0.737
Non-survivors 8.1%
Buckner [95] Seattle, WA, USA 105 69 50% Hospitalised Ever 26% 10% Severe 14% NA
Non-severe 7%
Javanian [96] Iran 100 60.12 49% Hospitalised NA 12% Survivors 8.64% 0.032
Non-survivors 26.31%
Itelman [97] Israel 162 52 35.2 Hospitalised 8.9%+ 1.2% Severe 3.8% 0.364
Moderate 0
Mild 1.1%
Lian [29] China 788 68 57.4% Hospitalised Current 5.88% 2.2% NA
Liu [30] China 137 57 55.5% Hospitalised NA 1.5% NA
Wu [31] China 80 44 48% Hospitalised NA 4% NA
Xu [32] China 90 50 57% Hospitalised NA 1% NA
Zhu [33] China 32 46 53% Emergency room 19%+ 6% NA
Huang [34] China 34 56.2 58.8% Hospitalised NA 8.8% NA
Wang [9] China 63 39.3 46% Asymptomatic NA 1.6% NA
Zhang [35] China 326 51 47.54% Hospitalised NA 0.61% NA
Liu [36] China 238 55.0 42.0% Hospitalised NA 1.3% NA
Lian [37] China 465 45 47.7% Hospitalised NA 0 NA
Hong [38] China 75 46.37 45% Hospitalised NA 0 NA
Ji [39] China 101 51.0 52% Hospitalised 5%+ 2% NA
Qiu [40] China 104 43 52.88% Hospitalised 3.85%+ 0.96% NA
Wei [41] China 101 49 46.5% Hospitalised 7.9%+ 1.0% NA
Grasselli [49] Italy 1591 63 19% ICU NA 4% NA
Cecconi [47] Italy 239 63.9 29.3% Hospitalised NA 9.2% NA
Inciardi [48] Italy 99 67 19% Hospitalised 20%+ 9% NA
de Abajo [98] Spain 1139 69.1 39.0% Hospitalised NA 10.5% NA
Barrasa [51] Spain 48 63.2 43% ICU 19%+ 38% NA
Szekely [99] Israel 100 66.1 37% Hospitalised 8%+ 4% NA
Richardson [42] NYC 5700 63 39.7% Hospitalised 15.6%+ 5.4% NA
Goyal [43] NYC 393 62.2 39.4% Hospitalised NA 5.1% NA
Kuno [44] NYC 8438 59 46.1% Hospitalised and outpatients NA 2.4% NA
Palaiodimos [45] NYC 200 64 51% Hospitalised Current and former 32.5% 14.0% NA
Arentz [52] Washington state, USA 21 70 48% ICU NA 33.3% NA
Bhatraju [50] Seattle, WA, USA 24 64 38% ICU NA 4% NA
Price-Haywood [100] Louisiana, USA 3481 55.5++; 53.6§§ 60% Hospitalised and outpatients NA 2.3% NA
Ferguson [101] California, USA 72 60.4 47.2% Hospitalised Ever 27.4% 4.2% NA
Gold [102] Georgia, USA 305 60 50.5% Hospitalised Current 5.2% 5.2% NA
Rentsch (preprint) [103] USA 585 66.1 4.6% Hospitalised and outpatients Current 27.2%; former 30.6%; never 36.9% 15.4% NA
Mitra [104] Canada 117 69 32.5% ICU Current and former 13.7% 6.8% NA
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NYC: New York City, NY, USA. #: median or mean ages, years; : ICU, mechanical ventilation or death; +: smoking status (i.e. current or former) not specified; §: age for survivors; ƒ: age for non-survivors; ##: severe cases; ¶¶: non-severe cases; ++: age for white patients; §§: age for black patients. NA: not available.

Nonetheless, there is increasing evidence that COPD may be a risk factor for more severe COVID-19 disease [57]. An analysis of comorbidities in 1590 COVID-19 patients across China found that COPD carried an odds ratio of 2.681 (95% CI 1.424–5.048; p=0.002) for ICU admission, mechanical ventilation or death, even after adjustment for age and smoking [13]; 62.5% of severe cases had a history of COPD (compared with only 15.3% in non-severe cases) and 25% of those who died were COPD patients (compared with only 2.8% in those who survived). In a multicentre Chinese study, COPD patients made up 15.7% of the critically ill patients, but only 2.3% of moderately ill patients (p<0.001) [16]. Other studies have found similar, if statistically weaker, differences in COPD rates between ICU admissions and non-ICU admissions (8.3% versus 1.0%; p=0.054) [10], severe and non-severe cases (4.8% versus 1.4%; p=0.026) [17], and between non-survivors and survivors (7% versus 1%; p=0.047) [11].

The COPD airway in COVID-19

Why COPD patients appear to suffer worse outcomes upon contracting COVID-19 (even if their risk of contracting to begin with may not be high) is worth some speculation. First, recent evidence that COPD patients and smokers may display the machinery required for SARS-CoV-2 cellular entry differently has come to light. Similar to SARS-CoV (which was responsible for the 2002–2003 SARS pandemic) [58], SARS-CoV-2 bears an envelope spike protein that is primed by the cellular serine protease TMPRSS2 to facilitate fusion of the virus with the cell's angiotensin-converting enzyme 2 (ACE-2) receptor and subsequent cell entry (figure 1) [59–62]. Our group has recently demonstrated that in three separate cohorts with available gene expression profiles from bronchial epithelial cells, ACE-2 expression was significantly elevated in COPD patients compared to control subjects [63]. Current smoking was also associated with higher ACE-2 expression compared with former and never smokers, an observation which has subsequently been validated by other groups in separate cohorts of lung tissue and airway epithelial samples [64–66] and supported by additional evidence linking ACE-2 expression with nicotine exposure [67, 68]. It is important to note, though, that ACE-2 expression alone has not been shown yet to confer increased susceptibility or increased severity of disease. Moreover, the relatively low expression of ACE-2 in the bronchial epithelium in comparison to the nasal epithelium [69] has unclear implications for disease susceptibility in patients with predominantly small airways pathology.

FIGURE 1.

FIGURE 1

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Schematic representation of a) severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) binding to the angiotensin-converting enzyme 2 (ACE-2) receptor following activation of the spike protein (s) by transmembrane serine protease 2 (TMPRSS2), which leads to endocytosis and infection. b) Human organs that have been reported by Zou et al. [105] to show ACE2 expression, with the respiratory system highlighted in red. c) The renin–angiotensin system (RAS) and the proposed SARS-CoV-2 action. The generation of angiotensin II from angiotensin I by angiotensin-converting enzyme (ACE) induces vasoconstriction of blood vessels and pro-inflammatory effects through the binding of angiotensin II receptor type 1 (AT1R), while the receptor type 2 (AT2R) may negatively regulate this pathway. ACE inhibitors (ACEi) and angiotensin II receptor blockers (ARBs) are very successful anti-hypertensives by promoting vasodilation of blood vessels. ACE-2 inhibits the activity of angiotensin II by converting angiotensin I to angiotensin 1–9 and angiotensin II to angiotensin 1–7, which binds to the MAS1 proto-oncogene (Mas) receptor with anti-inflammatory effects. Upon SARS-CoV-2 binding to ACE-2, there is a shift in the ACE/ACE-2 balance towards a predominance of ACE, resulting in increased pro-inflammatory effects and tissue damage.

The management of COPD patients during the COVID-19 pandemic

Two challenges of clinical care in COPD have emerged during this pandemic: 1) whether the usual algorithms of pharmaceutical management in COPD still apply and 2) how to weather the dramatic curtailments in non-pharmaceutical interventions this pandemic has wrought. Although our understanding of COVID-19 has substantially increased in a short period of time, these problems have largely been the domain of expert opinion rather than being guided by rigorous scientific evidence.

Questions remain about the effects of common respiratory medications used by our COPD patients such as inhaled (ICS) and systemic corticosteroids, short- and long-acting β2-agonists, and short- and long-acting muscarinic antagonists in either mitigating or exacerbating COVID-19 infections. The epidemiological data emerging from China and other early epicentres have not yet provided the necessary granularity required to determine whether these medications are harmful or beneficial in COVID-19 patients with COPD. Peters et al. [70], however, have recently shown that ACE-2 expression in airway epithelial cells obtained from asthmatic patients was decreased in those taking ICS compared to those who were not on ICS, raising the possibility that ICS exposure could decrease viral entry. Whether the same relationship holds true in the COPD airway, in which the predisposition to pneumonia following ICS use is well-documented, has not yet been established. For now, in the absence of data demonstrating definitive harm or benefit, ICS and other long-acting inhalers should not be routinely withdrawn nor should their use be escalated as a preventative measure for COPD patients during this pandemic [71].

Of greater concern is the use of systemic corticosteroids, the backbone of COPD exacerbation treatment. On balance, the historical evidence for systemic corticosteroids in viral pandemics has not been entirely favourable. Lessons from the SARS and Middle East respiratory syndrome (MERS) pandemics suggest potential harm, in fact. In SARS, while the majority of studies were inconclusive, four studies showed harm, including delayed viral clearance and increased rates of psychosis [72]. In MERS, corticosteroid use was associated with increased mortality [73] and delayed viral clearance [74]. So far, the most promising preliminary data on corticosteroids and COVID-19 are from a randomised controlled trial of dexamethasone (RECOVERY) performed in the UK, which demonstrated a one-third reduction in mortality [75]. Published data, however, are derived from small retrospective studies and appear mixed, with two studies showing no benefit [76, 77] and two studies showing improvements in rates of death and escalation of care [78, 79]. Because of the results of the RECOVERY trial, however, it is likely that dexamethasone will become standard of care treatment for COVID-19 patients including those with COPD.

The impact of the pandemic has been keenly felt by COPD patients in myriad aspects of their lives. Face-to-face clinic visits with their physicians have been curtailed, as have pulmonary rehabilitation sessions and COPD home visit programmes. Patients who may have normally presented to the hospital during an exacerbation might choose to stay home for fear of exposure, resulting in delayed care, as has occurred in other conditions like myocardial infarction [80, 81]. The long-term effects of this pause in routine care have yet to be measured. For now, healthcare systems have had to adapt to these conditions by augmenting telehealth and virtual visits. Fortunately, multiple randomised controlled trials assessing telehealth for COPD patients have demonstrated its feasibility and at least non-inferiority to usual care when it comes to exacerbations, hospitalisations and quality of life [82–86]. Moreover, online pulmonary rehabilitation programmes appear to be as effective as in-person sessions [87–89]. In the event that social distancing measures remain in place for many more months, we advocate for the establishment of these virtual programmes to ensure our patient population can continue to receive optimal care.

Directions for COVID-19 and COPD research

Specifically, we will have to address the following questions on COVID-19 as they pertain to COPD:

  • Does the burden of disease, clinical manifestations, and outcomes of COVID-19 in COPD patients differ from the general population and if so, how?

  • Given the multiple phenotypes associated with the term “COPD” (i.e. frequent exacerbators, emphysema-predominant, eosinophilic-predominant, asthma overlap), does COVID-19 infection in each of these phenotypes present and behave differently?

  • Are routine medications used in COPD such as inhaled and systemic corticosteroids, β2-agonists, muscarinic antagonists and chronic azithromycin protective or harmful in the setting of COVID-19 infection?

  • What will the impact of post-COVID-19 infection disability be in COPD patients and what resources will be required to adequately support the transition of COPD patients from the hospital to home after COVID-19?

  • How can we manipulate the unique airway pathology of COPD patients and the ACE-2 system to identify novel therapeutics?

  • What is the role of inhaled substances (e.g. tobacco, cannabis and e-cigarettes) and air pollution in increasing the susceptibility of COPD patients to COVID-19?

  • What can we learn from the experience of virtual care to COPD patients during this pandemic that can be applied in future scenarios to reach isolated patient populations and resource limited settings?

These research questions can best be answered by developing standards for transparent data reporting across the globe and harnessing the power of international networks that can quickly collate the data of COVID-19 COPD patients. Similarly, the efforts of translational research scientists at the laboratory bench who are working to characterise the pathophysiology of COVID-19 infections in the airway are critical to developing new therapies for a world in which there are currently very few.

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Acknowledgement

The authors would like to thank Irving Ding and Chun Hong Tao for their financial support of the SPF COVID-19 Response Fund. D.D. Sin holds a Tier 1 Canada Research Chair in COPD and the de Lazzari Family Chair at the Centre for Heart Lung Innovation. J.M. Leung is supported by the Michael Smith Foundation for Health Research (MSFHR)/Providence Health Care Health Professional Investigator (HPI) Award and by the Canadian Institutes of Health Research (CIHR)/AstraZeneca Early Career Investigator Award.

Footnotes

Conflict of interest: J.M. Leung has nothing to disclose.

Conflict of interest: M. Niikura has nothing to disclose.

Conflict of interest: C.W.T. Yang has nothing to disclose.

Conflict of interest: D.D. Sin reports grants from Merck, personal fees for advisory board work from Sanofi-Aventis and Regeneron, grants and personal fees for lectures from Boehringer Ingelheim and AstraZeneca, personal fees for lectures and advisory board work from Novartis, outside the submitted work.

Support statement: This work was supported by the St. Paul's Foundation (SPF) COVID-19 Response Fund.

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