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COVID-19: Health Care Implications

Synopsis The coronavirus disease 2019 (COVID-19) pandemic has challenged the capacity of healthcare systems around the world, including substantial disruptions to cardiovascular care across key areas of healthcare delivery. In this narrative review, we examine implications of the COVID-19 pandemic for cardiovascular healthcare, including excess cardiovascular mortality, acute and elective cardiovascular care, and disease prevention. Additionally, we consider the long-term public health consequences of disruptions to cardiovascular care across both primary and secondary care settings. Finally, we review healthcare inequalities and their driving factors, as highlighted by the pandemic, and consider their importance in the context of cardiovascular healthcare.


Introduction
The coronavirus disease 2019 (COVID-19) pandemic has placed immense pressures on healthcare services, necessitating reorganisation and reprioritisation of resources and changes in models of healthcare delivery. The large number of COVID-19 inpatient admissions has required restructuring of hospital services and redeployment of staff for provision of acute clinical care. Furthermore, many governments have postponed non-urgent elective work, due to both staff and infrastructure limitations, as well as concerns around exposure of potentially vulnerable patients to infection. These service pressures have been further compounded by staff shortages related to COVID-19 infection or contact exposure requiring isolation.
There have also been changes in the public's pattern of healthcare utilisation, owing, in part, to altered risk perceptions and health seeking behaviours 1 . Such behavioural changes have perhaps been influenced by national "lockdowns" or "stay at home" public health recommendations. Thus, delayed service provision due to resource-constrained healthcare delivery systems has been augmented by patients' hesitance to access healthcare.
Indeed, growing evidence indicates significant decline in use of healthcare services across multiple key areas. In the UK, emergency department (ED) visits declined by 49% and out-of-hours general practice consultations fell by 11% during the peak pandemic period in 2020 compared to the preceding year 1 . In the USA, there was a 42% decline in ED visits 2 . Similar trends were seen across Europe and globally. A study of 27 European nations reported significant reduction in healthcare utilisation after the first COVID-19 outbreak 3 . Whilst reports from China 4 , Singapore 5 , and Taiwan 6 indicate declines in utilisation of both inpatient and outpatient services.
Available evidence suggests major disruptions to delivery and utilisation of cardiovascular services during the pandemic, with important clinical consequences. Cardiovascular diseases are the most common cause of morbidity and mortality worldwide 7 . Their management requires a combination J o u r n a l P r e -p r o o f of preventive medicine, acute care, and chronic disease management. The longer-term impact of service disruptions during the pandemic on population cardiovascular health is likely significant and not yet fully appreciated.
In this narrative review, we examine implications of the COVID-19 pandemic for cardiovascular healthcare, including excess cardiovascular mortality, acute and elective cardiovascular care, and disease prevention. Additionally, we consider the long-term public health consequences of disruptions to cardiovascular care across both primary and secondary care settings. Finally, we review healthcare inequalities and their driving factors, as highlighted by the pandemic, and consider their importance in the context of cardiovascular healthcare.

Acute cardiovascular care (Figure 1)
The COVID-19 pandemic has resulted in excess premature mortality across many countries worldwide 8,9 . Cardiovascular disease and its risk factors have been linked to higher risk of adverse COVID-19 outcomes, including more severe disease manifestations and higher risk of death 10-12 . In a meta-analysis of 51 studies including a total of 48,317 patients, Bae et al. 10 identified pre-existing cardiovascular risk factors (hypertension, diabetes) and CVD itself as independent predictors of mortality amongst patients with COVID-19 across all age groups. A large nationwide study from Korea similarly reports significant associations of diabetes, hypertension, and heart failure with critical illness amongst patients hospitalised with COVID-19 11 . Accordingly, Wu et al. 13 report an 8% increase in acute cardiovascular deaths in England during the pandemic period. However, the excess cardiovascular deaths are not fully attributed to direct COVID-19 effects. Whilst a proportion of these deaths were related to COVID-19 (5.1%), the most frequent primary causes of death were stroke (35.6%), acute coronary syndrome (ACS, 24.5%), and heart failure (23.4%) 13 .
These observations may reflect reduced access to emergency services for these conditions, compounded by hesitance of patients to seek medical care during the pandemic. In the UK, public health messaging during the early stages of the COVID-19 pandemic centred around the slogan of "stay home, protect the NHS, save lives", with similar variations in other nations, which may have increased the reticence of patients to seek medical attention for acute cardiovascular events. Others have pointed out J o u r n a l P r e -p r o o f confusion around hospital protocols as a key reason for delays in seeking treatment for non-COVID illnesses during the pandemic 14 . Wu et al. 13 demonstrate a translocation in the place of death, with substantial increases in cardiovascular deaths at home (+35%) and in care homes or hospices (+32%), with more modest increase in hospital deaths. Mafham et al. 15 , also report a significant decline in the number of patients hospitalised with ACS per week in England at the end of March 2020 compared to weekly pre-pandemic averages. Braiteh et al. 16 report similar trends from the USA with 40.7% reduction in total hospital admission for ACS. There is also evidence that patients who did seek medical help waited significantly longer to do so compared to the pre-pandemic period. In a study from Switzerland, longer-term impact of these missed care opportunities is yet to be fully appreciated, but likely will comprise increase in both premature deaths and disability. In the clinical setting, it is important to remain vigilant to such potential late presentations of previously undetected acute events and to initiate appropriate therapies in order to minimise subsequent risks.

Elective activity
As with acute care, there have been declines in elective procedures. Whilst these procedures do not carry the same immediate urgency as the previously discussed acute conditions, substantial delays in their delivery leads to significantly poorer health outcomes. In this context, patients with severe aortic stenosis (AS) are a particular at-risk group; these patients have an extremely poor prognosis in the absence of valvular intervention with a mortality rate of more than 50% at two years 31 . In a study of UK procedural registry data, Martin et al. 32 report a rapid and significant reduction in surgical aortic valve replacement (SAVR) and transcatheter aortic valve replacement (TAVR) procedures following the COVID-19 pandemic. The authors estimate that almost 5,000 patients with severe aortic stenosis had not received appropriate procedural intervention in the months following the start of the pandemic (November to March 2020). These notable treatment delays are expected to translate to poorer outcomes in this patient population, including higher risk of death and presentations with acute cardiovascular decompensation. Indeed, in a study of 22,876 patients with severe AS, Albassam et al. 33 report association of greater wait time for valve intervention with higher risk of death and hospitalisation for heart failure whilst on the waiting list. Thus, there is urgent need to address strategies for service provision which may ameliorate these procedural backlog and treatment deficits.
The decline in elective work was observed across all cardiac interventions. In a study considering a wide range of cardiac procedures from the UK, Mohamed et al. 34 report a total deficit of over 45,000 procedures over the COVID-19 period (March to May 2020) compared with previous years. In a study of over half a million patients referred for elective cardiovascular procedures from Canada, Tam et al. 35 report a significant decline in the number of coronary revascularisation procedures performed during the pandemic compared to the pre-pandemic period. Importantly, the authors also J o u r n a l P r e -p r o o f observed increased risk of all-cause death whilst waiting for coronary revascularisation for referrals made during the pandemic. There was also evidence of change in choice of procedural strategy.
Amongst patients with left main coronary artery stenosis in the UK, there was observation of both a reduction in revascularisation procedures and greater use of PCI over coronary artery bypass grafting 36 .
The pandemic has also had dramatic impact on cardiovascular imaging services with reduced activity due to redeployment of staff and fewer referrals from both primary and secondary care.
Cardiovascular imaging is central to accurate diagnosis of many CVDs. In a survey of 909 centres covering 108 European centres, Williams et al. 37 report that total cardiac imaging reduced by 45% in March 2020 and by 69% in April 2020, compared to pre-pandemic levels. The authors demonstrate geographic variation in these trends with greater reductions observed in Southern European nations compared to elsewhere 37 . Consistent with these observations, in a study of 52 Italian centres, Dondi et al. 38 report reduction in imaging volumes of 67% in March 2020 and 77% in April 2020, compared to the preceding year. These disruptions to clinical care raise concerns about the large number of patients with delayed or missed diagnoses and the potential adverse impact of this on long term risk of cardiovascular morbidity and mortality.

Impact on primary care
The adverse impact of COVID-19 has extended to primary care, the key setting for primary prevention strategies and management of patients with stable chronic cardiovascular diseases. A UK report from NHS Digital 39 , indicated a near 30% reduction in appointments recorded in general practice systems in mid-March 2020, compared to pre-pandemic averages. In an analysis of nationwide general practice prescribing trends, Dale and Takhar et al. 40  additional strokes 40 . In a study of over 600,000 UK patients, Carr et al. 41 report near 50% reduction in measurement of blood pressure in general practice and 22% reduction in prescription of new antihypertensive medications during the first year of the COVID-19 pandemic. An earlier nationwide J o u r n a l P r e -p r o o f study of patients with type 2 diabetes in the UK demonstrated 31% reduction in glycated haemoglobin A1c (HbA1c) testing, 20% reduction in starting new metformin prescriptions, and 5% reduction in initiation of insulin therapy 42 . These missed diagnosis and treatment optimisation opportunities are concerning and have significant and sustained implications for population cardiovascular health. There is need for dedicated efforts to address missed opportunities for primary and secondary prevention to alleviate future population burden of cardiovascular disease.

Inequities of CV care
The COVID-19 pandemic has highlighted the impact of social inequalities on health. Black Asian and Minority Ethnic (BAME) communities experienced higher infection and mortality related to COVID-19 compared to the White population [43][44][45][46][47][48] . Geography, deprivation, occupation, living arrangements, and health conditions such as cardiovascular disease and vascular risk factors account for some, but not all, of the excess mortality risk of COVID-19 in BAME populations 46,49 . As well as experiencing more severe outcomes from COVID-19, BAME cohorts also had disproportionately poorer cardiovascular outcomes during the pandemic. For instance, Kwok et al. 20 report the decline in PCI procedures to be more marked amongst BAME patients, whilst Rashid et al. 23 found that BAME individuals were more likely to suffer out of hospital cardiac arrest during the pandemic. In a multisource linked cohort study, Rashid et al. 50 demonstrate that BAME individuals with acute myocardial infarction were less likely to receive guideline directed therapies and had higher early mortality than White ethnicities, and, importantly, that these disparities appeared wider during the COVID-19 period compared to the prepandemic period. These poorer health experiences also extended to women and those from more deprived background. For instance, Carr et al. 41 found that individuals with the highest levels of socioeconomic deprivation experienced the greatest decline in general practice health checks for key cardiovascular risk factors. Similarly, Hartnett et al. 2 report significant decline in ED visits of 42% during the early pandemic period and found that the steepest decreases were amongst women. These social inequalities were further exacerbated by the economic impact of the pandemic, which also disproportionately affected the most vulnerable in society. In a study including 27 European countries, J o u r n a l P r e -p r o o f Jiskrova et al. 3 report that job losses during the pandemic were significantly more likely amongst women, those with lower educational level, and lower household income.
Social and economic disadvantage are key determinants of health outcomes. The disproportionate impact of the pandemic on the most vulnerable in society mirrors the effect of other catastrophic natural disasters, where, consistently, the most devestating impacts are experienced by communities who are already disadvantaged and underserved 51 . COVID-19 has highlighted social inequalities and emphasised the urgent need for dedicated interventions to prevent and manage ill health in the most vulnerable populations. There is need for high quality data to understand the social and healthcare needs of deprived groups and to permit development and tracking of appropriately targeted strategies by policy makers and healthcare professionals.

Summary
The COVID-19 pandemic has adversely disrupted cardiovascular care across key areas of healthcare delivery including acute and chronic disease management and preventive interventions. The reduction in access to guideline-directed therapies and procedures in the acute setting have likely driven early observations of excess cardiovascular disease mortality. The substantial decline in elective cardiovascular procedures and significant related backlog, if not promptly addressed, is expected to translate into excess death and disability in the medium term. Meanwhile, treatment deficits in primary and secondary disease prevention are expected to have a wider longer-term impact in adversely impacting population cardiovascular health. The pandemic has shone a light on healthcare inequalities, which has been observed both in direct relation to COVID-19 and in the context of cardiovascular care during the pandemic. There is need for concerted efforts from policy makers and clinicians to identify