key: cord-0908491-lbe6hiwf
authors: Vepa, Abhinav; Bae, Joseph P.; Ahmed, Faheem; Pareek, Manish; Khunti, Kamlesh
title: Diabetes & Metabolic Syndrome: Clinical Research & Reviews COVID-19 and Ethnicity: A Novel Pathophysiological Role for Inflammation
date: 2020-06-30
journal: Diabetes Metab Syndr
DOI: 10.1016/j.dsx.2020.06.056
sha: 3ef2cedfe1a931f4d94cef3cec55a62f80a590d8
doc_id: 908491
cord_uid: lbe6hiwf

INTRODUCTION: There have been recent mounting concerns regarding multiple reports stating a significantly elevated relative-risk of COVID-19 mortality amongst the Black and Minority Ethnic (BAME) population. An urgent national enquiry investigating the possible reasons for this phenomenon has been issued in the UK. Inflammation is at the forefront of COVID-19 research as disease severity appears to correlate with pro-inflammatory cytokine dysregulation. This narrative review aims to shed light on the novel, pathophysiological role of inflammation in contributing towards the increased COVID-19 mortality risk amongst the BAME population. METHODS: Searches in PubMed, Medline, Scopus, medRxiv and Google Scholar were performed to identify articles published in English from inception to 18(th) June 2020. These databases were searched using keywords including: ‘COVID-19’ or ‘Black and Minority Ethnic’ or ‘Inflammation’. A narrative review was synthesized using these included articles. RESULTS: We suggest a novel pathophysiological mechanism by which acute inflammation from COVID-19 may augment existing chronic inflammation, in order to potentiate a ‘cytokine storm’ and thus the more severe disease phenotype observed in the BAME population. Obesity, insulin resistance, cardiovascular disease, psychological stress, chronic infections and genetic predispositions are all relevant factors which may be contributing to elevated chronic systemic inflammation amongst the BAME population. CONCLUSION: Overall, this review provides early insights and directions for ongoing research regarding the pathophysiological mechanisms that may explain the severe COVID-19 disease phenotype observed amongst the BAME population. We suggest ‘personalization’ of chronic disease management, which can be used with other interventions, in order to tackle this.

COVID-19 is the term used to describe the disease caused by Severe Acute Respiratory Syndrome Coronavirus-2 (SARS CoV-2). It originated in December 2019 from Wuhan, Hubei province in China, and owing to its ability to be transmitted between humans via respiratory droplets 1 , has since spread globally. Within the United Kingdom (UK), there have been mounting concerns regarding multiple reports of an elevated relativerisk of COVID-19 mortality amongst the Black and Minority Ethnic (BAME) population 2-5 .

After adjusting for socio-demographic characteristics and self-reported comorbidity/disability, the Office for National Statistics (ONS) estimates that Indian females are 1.43 times, Pakistani and Bangladeshi males are 1.8 times, and Black males and females 1.9 times, more likely to die from COVID-19 relative to their White counterparts 2 . This pattern has broadly been reflected in UK critical care admission and outcome data from the Intensive Care National Audit and Research Centre report 6 , as well as data from the United States of America (USA) 7 . An urgent national enquiry into the possible reasons for this phenomenon has thus been issued.

SARS CoV-2 is a positive-sense, enveloped, single-stranded RNA virus which can bind to the angiotensin converting enzyme 2 (ACE2) receptor in humans 1, 8 . ACE2 receptors are expressed widely throughout the body but it is believed that SARS CoV-2 uses ACE2 receptors expressed on respiratory epithelial cells to gain entry into the host 8 . After entering the respiratory epithelium, it can replicate to cause pyroptosis and thus the release of pathogen associated molecular patterns (PAMPs) and damage associated molecular patterns (DAMPs) 9 . DAMPs and PAMPs are recognised by the pattern recognition receptors of surrounding epithelial cells, alveolar macrophages and vascular endothelial cells, which respond by releasing a wide array of pro-inflammatory cytokines such as C-X-C motif chemokine-10 (CXCL-10), interleukin-6 (IL-6), macrophage inflammatory protein 1α (MIP1α), macrophage inflammatory protein 1α (MIP1β) and monocyte chemoattractant protein 1 (MCP1). These inflammatory cytokines and chemokines can then recruit monocytes, macrophages and T-cells to the local tissue which all release further pro-inflammatory cytokines in a positive feedback loop mechanism resulting in a 'cytokine storm' 8 . Evidence to support this was confirmed by the levels of various inflammatory cytokines such as IL-2, IL-7, IL-10, granulocyte colony-stimulating factor (G-CSF), CXCL-10, MCP1, MIP1α and tumour necrosis factor- (TNF-), being elevated in severe COVID-19 patients who required critical care admission, usually after the initial phase of viral infection 10 .

One of the major complications of COVID-19 is acute respiratory distress syndrome (ARDS), which can lead to death by respiratory failure, and is indeed associated with systemic inflammation 11 . The aforementioned 'cytokine storm' can also lead to sepsis and multi-organ failure 12, 13 . Another emerging frequently fatal complication of COVID-19 are venous thrombo-embolisms (VTE), namely pulmonary embolisms (PE), which are hypothesized to arise due to the pro-inflammatory and hypercoagulable state described extensively in the literature 14 . Peak IL-6 levels have now been directly associated with COVID-19 disease severity 15 and tocilizumab, an IL-6 inhibitor, is amongst many other promising anti-inflammatory drugs undergoing clinical trials to treat COVID-19 16, 17 . Inflammation is thus at the forefront of COVID-19 research 18 and it is postulated that disease severity and outcomes correlate with pro-inflammatory cytokine dysregulation 19, 20 . We therefore undertook the synthesis of a narrative review, which aims to shed light on the novel, acute-on-chronic, pathophysiological role of inflammation in contributing towards the increased mortality risk of COVID-19 amongst the BAME population. We propose that the BAME population may be subjected to elevated levels of chronic, systemic inflammation, due to various reasons discussed, which may augment the acute COVID-19 'cytokine storm'

described, to potentiate multi-organ failure and death. OR 'Genetic'. The reference list of each study identified in the initial database search, and the library of each co-author, was also reviewed to identify any potentially relevant studies.

Study Selection: Titles, abstracts, and key words of the studies identified in the electronic search were screened for eligibility to be included in this narrative review. All studies deemed relevant were retrieved. A standardized checklist was then used to determine the eligibility for inclusion in the review based on information within the full article. Original research articles were selected to participate in this study if they were relevant to our study hypothesis and contained the highest quality of evidence pertaining a given subject; systematic reviews were used preferentially where possible. Studies confined to local indigenous populations, or published before the year 2000, were excluded. Key epidemiological data was also extracted from government reports.

Synthesis: A narrative review was synthesized using the included articles in order to summarize key information, hypothesize pathophysiological mechanisms, draw inferences and suggest recommendations for public health policy. 29 . This suggests that from childhood itself, metabolic risk in the BAME population is higher, and indeed, there is evidence to suggest a genetic predisposition to metabolic syndrome amongst the BAME population 30 42 . OSA has been associated with an exacerbation of metabolic syndrome [43] [44] [45] , increased intubation risks 46 and respiratory failure 47 . Furthermore, obesity can contribute to nonalcoholic fatty liver disease (NAFLD), which is more commonly found in ethnic minorities 48, 49 . Thus, during a COVID-19 'cytokine storm', patients with NAFLD, may be more prone to acute-on-chronic liver failure 50 .

Obesity, and insulin resistance, can both also contribute to a chronic inflammatory state which may potentiate a 'cytokine storm' within the context of an acute COVID-19 infection. Excess fat, in particular visceral fat which is broadly measured by waist circumference, has been associated with chronic systemic inflammation 51 and COVID-19 severity 36 Furthermore, densely populated urban areas such as London suffered the most deaths from COVID-19 and, likewise, the population of London also comprises of over 40% BAME 100 . Not only does overcrowded housing and inner-city living pose a huge impediment for social distancing, but they are also both associated with psychological stress, mental health disorder and inflammation [101] [102] [103] .

Finally, whilst 63% of COVID-19 related deaths amongst NHS frontline staff were BAME 104 , only 20.8% of the NHS workforce are BAME 105 . This highlights an enormous relative risk which is greater than that of the general BAME population, raising questions regarding occupational hazard. This may partially be explained by the fact that frontline NHS workers are more likely to be exposed to higher viral loads of COVID-19. However, healthcare workers can often experience psychological stress and burn-out 106 and there is now emerging evidence that BAME NHS staff may encounter greater work-related psychological stress 107 .

Amongst the non-medical NHS workforce, a hierarchal correlation can be observed whereby the prevalence of White staff positively, and BAME staff negatively, correlate with seniority 105 . Indeed, a 'lack of decision making' has been identified as a potent source of occupation-related psychological stress 108, 109 . Similarly, various other occupations such as chefs, taxi drivers and security guards, have all also encountered a disproportionately higher number of COVID-19 related deaths 110 . These occupations not only contain higher representations of minority ethnics amongst staff 111 , but may also involve less decision making, as well as more night shifts, sedentary work and viral load exposure.

Overall, the mechanism as to how psychological stress can contribute to chronic inflammation is yet to be fully elucidated, but there are two mechanisms that have been described 

In addition to the well evidenced pathophysiological mechanisms discussed above, there may also be a smaller role played by chronic infections such as Tuberculosis (TB), chronic hepatitis, and Human Immunodeficiency Virus (HIV), which are more prevalent in migrants from developing countries [124] [125] [126] [127] . TB is known to contribute to various chronic lung changes such as cavitation, fibrosis, bronchiectasis and impairment in lung function, all of which may contribute to impaired pulmonary immunity 128 

Based on the pathophysiological mechanisms identified in this review, as well as the surrounding literature, suggested multi-disciplinary interventions to reduce the health inequalities highlighted by the COVID-19 pandemic have been summarized in Table 1 below.

Income inequalities for younger generations can be targeted by further investing in the education of deprived populations. Inner-city Schools and Universities can be given more subsidies and grants to facilitate this with awareness of these government schemes should also be addressed by diversifying advertising platforms, for example, via social media. Housing inequalities can be addressed by allocating housing benefit claimants to council properties throughout the country rather than in specific inner-city areas. The barriers preventing elderly BAME individuals from utilizing care homes should be tackled to reduce overcrowded housing. Certain populations, containing more BAME, may be excluded from receiving high quality healthcare. Firstly, in prisons, where Blacks are overrepresented, the Lammy review identifies that there is scope for improvement in the mental health awareness and health literacy amongst prison staff as they can often be the first point of contact for prisoners seeking medical attention 93 . Additionally, improving staffing levels in prisons would help overcome the added barrier of escort requirements when prisoners require secondary care. Secondly, undocumented migrants may not be entitled to non-emergency, healthcare which may delay their presentation to healthcare services due to deportation fears. The government should supportively work with these populations to prevent resultant health impairments by introducing crossborder health and social care. The BAME population are at increased risks of unhealthy behaviours such as physical inactivity, and high-fat, high-sugar diets [38] [39] [40] . Dietary advice should be offered, in multiple languages, focussing on healthy food interventions for all cuisines, rather than just Western cuisines. The importance and benefits of healthy eating and exercise should be taught in schools, social media, and certain occupations which suffered disproportionate COVID-19 deaths, for example, taxi drivers. Councils in areas which suffered higher levels of COVID-19 deaths should be given subsidies to focus on health promotion. This could involve supermarket food stamps for healthy food, discounted gym memberships, more cycle lanes and cycle-to-work schemes, subsidies to convert fast-food restaurants into health food restaurants, and the delivery of healthy-lifestyle talks at community gatherings, places of worship and Gypsy communities. The BAME population are at elevated risks of various diseases which could be contributing to their more severe COVID-19 phenotype. Guidelines should reflect this by incorporating ethnicity as a relevant risk factor to assist in determining when to initiate treatment. This may involve starting oral hypoglycaemic agents at lower HbA1c levels, the NHS provision of bariatric surgery at a lower BMI threshold, or perhaps the use of statins, aspirin and percutaneous coronary intervention at lower cardiovascular risk thresholds for BAME individuals. Non-English speakers may lack the confidence to use NHS 111 services. It is thus imperative to increase the provision of translators and multi-lingual NHS services. Language barriers may also reduce the effectiveness of talking therapies such as cognitive behavioural therapy. For this reason, the NHS provision of evidence-based, non-verbal psychotherapies such as yoga, tai-chi, dance movement psychotherapy, and music therapy may thus be of benefit. Cultural barriers can often influence the interaction between BAME individuals and healthcare services. For example, the stigma associated with mental health disorder is often higher amongst the BAME population.

Healthcare staff, such as community mental health teams, should be equipped to deal with such stigmas as well as other cultural barriers. Furthermore, the use of alternative medicine may be more prevalent amongst the BAME population 143 . Where possible, evidence based alternative therapies such as acupuncture, mindfulness and fasting should be considered by health professionals. Various drugs such as dexamethasone, convalescent plasma, tocilizumab, and remdesivir are undergoing clinical trials to assess their efficacy in treating COVID-19 144 . It is important to increase the BAME individuals participating in these studies, or even to conduct separate studies focussed on the BAME population. The recognition and reporting of ethnicity as a crucial demographic risk factor, like age and gender, should also be encouraged amongst healthcare research.

The mechanisms discussed throughout this review have been summarized in Figure 1 below. Figure 1 : Illustrating the complex, acute-on-chronic interplay between social determinants of health, acute COVID-19 pathophysiology and the chronic diseases discussed in this review, which are more prevalent in the Black and Minority Ethnic (BAME) population. Chronic diseases, and disease processes, that could be contributing to the more severe COVID-19 phenotype observed in the BAME population include Metabolic Syndrome ( 

This review aims to shed light on the ongoing, national enquiry investigating the disproportionate effect of COVID-19 on the BAME population. For the first time, inflammation has been discussed in a common framework with regards to COVID-19 and ethnicity. We suggest a novel, pathophysiological mechanism by which acute inflammation, arising from COVID-19, may augment existing chronic inflammation secondary to medical co-morbidity, in order to potentiate a 'cytokine storm' and thus the more severe disease phenotype observed in the BAME population. Obesity, insulin resistance, cardiovascular disease, psychological stress, chronic infections and genetic predispositions are all relevant factors which may be contributing to elevated chronic, systemic inflammation amongst the BAME population. We suggest various interventions to reduce the prevalence of the severe COVID-19 disease phenotype amongst the BAME population. Subsequent Systemic Immune Response Syndrome (SIRS) and multi-organ failure secondary to COVID-19 can manifest as acute coronary syndrome (ACS), myocarditis, Venous Thrombo-Embolism (VTE), acute liver failure, respiratory failure, and acute renal injury, all of which can be directly potentiated by the aforementioned, pre-existing co-morbidities. 

There are no relevant conflicts of interest to declare.

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There is no funding to declare.

Please wait... If this message is not eventually replaced by the proper contents of the document, your PDF viewer may not be able to display this type of document.You can upgrade to the latest version of Adobe Reader for Windows®, Mac, or Linux® by visiting http://www.adobe.com/go/reader_download. For more assistance with Adobe Reader visit http://www.adobe.com/go/acrreader. Windows is either a registered trademark or a trademark of Microsoft Corporation in the United States and/or other countries. Mac is a trademark of Apple Inc., registered in the United States and other countries. Linux is the registered trademark of Linus Torvalds in the U.S. and other countries. Table 1 Intervention Explanation Reducing Socioeconomic Inequalities Income inequalities for younger generations can be targeted by further investing in the education of deprived populations. Inner-city Schools and Universities can be given more subsidies and grants to facilitate this with scholarships, as well as career mentorship programmes. For the current working population, adult-learner courses can be further subsidized. The awareness of these government schemes should also be addressed by diversifying advertising platforms, for example, via social media. Housing inequalities can be addressed by allocating housing benefit claimants to council properties throughout the country rather than in specific inner-city areas. The barriers preventing elderly BAME individuals from utilizing care homes should be tackled to reduce overcrowded housing. Improving Access to Healthcare in specific 'at-risk' populations Certain populations, containing more BAME, may be excluded from receiving high quality healthcare. Firstly, in prisons, where Blacks are overrepresented, the Lammy review identifies that there is scope for improvement in the mental health awareness and health literacy amongst prison staff as they can often be the first point of contact for prisoners seeking medical attention 93 . Additionally, improving staffing levels in prisons would help overcome the added barrier of escort requirements when prisoners require secondary care. Secondly, undocumented migrants may not be entitled to non-emergency, healthcare which may delay their presentation to healthcare services due to deportation fears. The government should supportively work with these populations to prevent resultant health impairments by introducing crossborder health and social care. Improving Health LiteracyThe BAME population are at increased risks of unhealthy behaviours such as physical inactivity, and high-fat, high-sugar diets [38] [39] [40] . Dietary advice should be offered, in multiple languages, focussing on healthy food interventions for all cuisines, rather than just Western cuisines. The importance and benefits of healthy eating and exercise should be taught in schools, social media, and certain occupations which suffered disproportionate COVID-19 deaths, for example, taxi drivers. Communitydirected health promotion Councils in areas which suffered higher levels of COVID-19 deaths should be given subsidies to focus on health promotion. This could involve supermarket food stamps for healthy food, discounted gym memberships, more cycle lanes and cycle-to-work schemes, subsidies to convert fast-food restaurants into health food restaurants, and the delivery of healthy-lifestyle talks at community gatherings, places of worship and Gypsy communities. Personalizing chronic disease managementThe BAME population are at elevated risks of various diseases which could be contributing to their more severe COVID-19 phenotype. Guidelines should reflect this by incorporating ethnicity as a relevant risk factor to assist in determining when to initiate treatment. This may involve starting oral hypoglycaemic agents at lower HbA1c levels, the NHS provision of bariatric surgery at a lower BMI threshold, or perhaps the use of statins, aspirin and percutaneous coronary intervention at lower cardiovascular risk thresholds for BAME individuals. OvercomingNon-English speakers may lack the confidence to use NHS 111 services. It is Language Barriers thus imperative to increase the provision of translators and multi-lingual NHS services. Language barriers may also reduce the effectiveness of talking therapies such as cognitive behavioural therapy. For this reason, the NHS provision of evidence-based, non-verbal psychotherapies such as yoga, tai-chi, dance movement psychotherapy, and music therapy may thus be of benefit. Improving Cultural AwarenessCultural barriers can often influence the interaction between BAME individuals and healthcare services. For example, the stigma associated with mental health disorder is often higher amongst the BAME population. Healthcare staff, such as community mental health teams, should be equipped to deal with such stigmas as well as other cultural barriers. Furthermore, the use of alternative medicine may be more prevalent amongst the BAME population 143 . Where possible, evidence based alternative therapies such as acupuncture, mindfulness and fasting should be considered by health professionals. BAME-targeted Healthcare ResearchVarious drugs such as dexamethasone, convalescent plasma, tocilizumab, and remdesivir are undergoing clinical trials to assess their efficacy in treating COVID-19 144 . It is important to increase the BAME individuals participating in these studies, or even to conduct separate studies focussed on the BAME population. The recognition and reporting of ethnicity as a crucial demographic risk factor, like age and gender, should also be encouraged amongst healthcare research.