key: cord-0824650-xtvujuji
authors: Sacks, Lori J; Pham, Cecilia; Fleming, Nicola; Neoh, Sandra L.; I Ekinci, Elif
title: Considerations for people with diabetes during the Coronavirus Disease (COVID-19) Pandemic
date: 2020-07-03
journal: Diabetes Res Clin Pract
DOI: 10.1016/j.diabres.2020.108296
sha: 88f6956b2328a6023f28314b86e36d07374b1082
doc_id: 824650
cord_uid: xtvujuji

Abstract Introduction The severe acute respiratory syndrome corona virus 2 (SARS-CoV-2) continues to cause havoc globally, resulting in unprecedented healthcare, societal and economic disruption. People with diabetes have been shown to be at higher risk of complications and death when exposed to pneumonia, influenza and other coronaviruses. Despite pandemic scale infection, there is currently limited understanding on the potential impact of SARS-CoV-2 on people with diabetes. Aims (1) To characterise the outcomes of SARS-CoV-2 for people with diabetes and (2) add value to current recommendations for healthcare providers and people with diabetes to encourage optimal management. Methods A search of PubMed, Embase and MEDLINE to March 2020 was undertaken, using search terms pertaining to diabetes, coronavirus and acute respiratory distress syndrome (ARDS). We briefly reviewed the epidemiology and pathophysiology of SARS-CoV in the context of diabetes. Conclusion People with diabetes are at greater risk of severe infection and death with COVID-19. COVID-19 has significantly impacted the daily lives of individuals living with diabetes through financial implications, food and medication scarcity and its burden on mental health. In Australia, delivery of medical care has been adapted to reduce the risk of transmission, with a particular emphasis on telehealth and remote monitoring.

The novel coronavirus (SARS-Cov-2) originating in Wuhan, China has spread rapidly around the world. On March 11 th 2020, the World Health Organisation (WHO) declared the coronavirus disease (COVID-19) a pandemic (1). This virus has had devastating consequences on a global scale (2) . People with diabetes are more susceptible to adverse outcomes and death from respiratory tract infections (3) , influenza A (H1N1) (4), severe acute respiratory syndrome coronavirus 1 (SARS-CoV-1) (5) , and the Middle East respiratory syndrome coronavirus (MERS-CoV) infection (6) . Diabetes, particularly in patients aged 70 years or older, has been strongly associated with an increased risk of infection and complications (7, 8) . It is unclear if susceptibility to infection in people with diabetes is due to a chronic inflammatory state with associated alterations in glucose metabolism and dysregulation of the immune system or due to the renal, vascular and cardiovascular complications frequently associated with diabetes and increasing age (9) .

Our understanding of the health impact of COVID-19 in people with diabetes is evolving. It is clear that community management of diabetes has been directly and indirectly impacted by COVID- 19 . In order to minimise the transmission risk between healthcare workers and their patients or consumers, public health policies have focussed on early detection, self-isolation of positive cases, infection control precautions and minimising face to face contact through the use of telemedicine (10) .

We aimed to review the impact of COVID-19 on people living with diabetes in Australia. We provide practical recommendations for the management of diabetes in the outpatient setting.

We undertook a search of PubMed, MEDLINE, EMBASE, Google Scholar using the key words "diabetes", "coronavirus", "SARS", "MERS" and "management". Studies with full text English versions were included. We reviewed the literature on the epidemiology and pathophysiology of COVID-19, which are relevant for people with diabetes.

Recommendations were summarised in addition to expert guidance based on the following topic areas: diabetes specific, general prevention and logistical considerations.

The 2019 severe-acute-respiratory-syndrome coronavirus (SARS-CoV-2) outbreak is believed to have originated from a zoonotic source in the Huanan wholesale seafood market, in Wuhan City, China (11). Highly contagious, SARS-CoV-2 has rapidly spread throughout China and worldwide, with person-to-person spread the main mode of transmission (12) .

Since initial detection, there have been over 1 million laboratory confirmed cases globally, with the largest burden of morbidity and mortality arising in European cities and the United States (2) .

Whilst all ages are susceptible, children are significantly less affected, with 2-3% of reported cases occurring in individuals under age 19 years (11). The majority of cases (87%) appear to affect individuals between 30 and 79 years. Disease severity appears to worsen with age and underlying comorbid conditions (13, 14) . The incidence of diabetes in COVID-19 cases in China has varied from 5% to 20% however large-scale data suggest incidence may be in the order of 5.3-7.4% (15-21) (refer to Appendix 3). These discrepancies may be attributed to incomplete data due to lack of testing and comorbid analysis of cases of death. In comparison, diabetes was reported in approximately 10.9% of the Chinese population prior to COVID-19 (22, 23) . Therefore based on early prevalence studies in China, it appears that people with diabetes are not significantly more likely to be infected with COVID-19.

People with diabetes are at increased risk of severe infection (13, 24) 

In a large China cohort study of 1590 individuals, mortality rate of patients with diabetes was significantly higher than people without diabetes (10% vs 2.5% respectively; p<0.001 2 ) (14).

Mortality is further increased in people with more than one coexisting comorbid condition (14) , an important consideration, given that diabetes is commonly associated with multiple organ systems, including renal and cardiovascular complications. From 55,924 laboratory confirmed cases in China in February 2020, mortality was highest in people over 80 years (case fatality rate (CFR) of 21%) and those with comorbidities (CFR for cardiovascular disease 13%, diabetes 9.2%, hypertension 8.4%, chronic respiratory disease 8.0% and cancer 7.6% vs patients with no comorbid condition CFR 1.4%) (11). Additionally, population based data by the England National Health Service has revealed that diabetes was prevalent in one in four (26%) patients who had died in hospital and tested positive for COVID-19 (29)".

As of the 19th of April 2020, 6606 cumulative confirmed cases and a total of 69 deaths have been reported in Australia (30) . Of total cases, 12% were admitted to hospital and a further 17% of those admitted patients required intensive care unit (ICU) admission for ventilatory support. Diabetes was the most prevalent comorbidity among hospitalised cases admitted to an ICU followed by cardiovascular disease at in 24% and 22% of patients respectively. Diabetes was also the most commonly reported comorbid condition among SARS-CoV-2 associated death, with 33% of fatalities having diabetes (30) . The median age of SARS-CoV-2 deaths was 79 years (interquartile range: 74 -84 years) indicating that frailty was associated with increased severity of infection and mortality (30) which is consistent with international reports (11). However, stringent social distancing measures and expanded testing criteria by the federal government has led to a sharp decrease in the incidence of new COVID-19 cases in Australia since the beginning of April 2020 (see Figure 1 ).

(Insert Figure 1 here) 

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV2) is an enveloped, single stranded, positive-sense RNA virus, which is believed to be in the same subgenus as SARS-CoV-1, and distantly related to MERS-CoV (31) . Coronaviruses have the largest genome out of all RNA viruses with typically 27 to 32 kilobases enclosed within a nucleocapsid (32) . Bound to the coronavirus envelope are spike glycoproteins which give the virus its distinctive "halo" appearance under electron microscope (33, 34) . Aside from giving coronavirus its characteristic name, spike glycoprotein receptor binding domains (RBDs) bind to angiotensinconverting-enzyme 2 (ACE2) surface receptors with high affinity, mediating viral entry into the host cell and enhancing the pathogenicity of SARS-CoV2 (32, 34) (figure 2). Upon binding to ACE2, SARS-CoV2 invades the host cell through endocytosis, leading to the subsequent down regulation of surface ACE2 receptor (35) .

ACE2 is a type I membrane bound receptor with a single active site and is abundant in mucosal epithelial cells within lung alveolar tissue, as well as the heart, kidney, intestine and blood vessels (36, 37) ACE2 is also an endogenous inhibitor of the renin-angiotensin system (RAS) through degradation of angiotensin II into angiotensin 1-7 (38) (figure 1). Angiotensin 1-7 subsequently binds to the protein-coupled receptor Mas and exerts vasodilatory, antithrombotic, antiproliferative and antioxidative effects (39) (see figure 2 ).

(Insert Figure 2 here)

5.1 ACE2 and inhibition of the renin-angiotensin system. In healthy individuals, circulating ACE2 is low (40) . However, circulating ACE2 is increased in individuals with diabetes, hypertension and nephropathy (38, 41) . This has been ascribed to a compensatory mechanism to account for overactivity of angiotensin II and the RAS in people with diabetes (43) . Importantly there is currently no clinical data in humans to indicate that a change in ACE2 activity alters susceptibility to SARS-CoV-2 infection.

Many people with cardiovascular complications and nephropathy due to diabetes are prescribed ACE inhibitors (ACEi) or angiotensin II receptor blockers (ARBs) for cardiovascular (42) and renoprotective effects (43, 44) . Recently there has been speculation that the use of ACEi and ARBs may upregulate ACE2 (45) . Through the binding of angiotensin II to angiotensin type I (AT 1 ) receptor, MAP kinase-phosphotase signalling pathways are activated to reduce ACE2 mRNA gene expression and activity (46) . By inhibiting the formation of angiotensin II, ACEi blocks this negative feedback loop, resulting in increased ACE2 (see figure 2 ). Others suggest that angiotensin II binds to the AT 1 receptor, which mediates internalisation of ACE2 and degradation by lysosomes. This process was inhibited by the ARB, Losartan (47) .

Whilst some animal studies have demonstrated upregulation of ACE2 gene expression in response to ACE inhibition (48, 49) , normotensive models were used and these studies failed to investigate whether increased ACE2 gene expression correlated with increased ACE2 activity. Other animal studies have contradictorily shown no increase in ACE2 gene expression or activity levels with ACEi or ARBs (50, 51) . To date, human studies have shown no evidence of upregulation of ACE2 activity in patients on ACEi or ARBs (38, 52) . Thus the ongoing use of usual ACE inhibitors for blood pressure management in patients with diabetes continues to be supported by the Australian Diabetes Society (ADS) as well as other international bodies (53).

characterised by a chronic low-grade inflammatory state induced by excess adipose tissue (54) . Elevated levels of tumour necrosis factor (TNF)-a, interleukin (IL)-6, C-reactive protein, plasminogen activator inhibitor and reactive oxygen species (ROS) have been demonstrated in adipose tissue of obese mice (55, 56) . These inflammatory cytokines are believed to inhibit insulin signalling by serine phosphorylation of insulin receptor substrate via activation of Iҡβα kinase β (IKKβ) and c-Jun N-terminal kinase I (JNK1) mediators (57) . Activated IKKβ also results in transcription of various other inflammatory genes (57) . In addition to the pathogenesis of insulin resistance and type 2 diabetes, increased proinflammatory macrophages, cytokines, chemokines and proteases contribute to the development of diabetes related retinopathy, nephropathy, neuropathy and cardiovascular disease (58) .

Individuals with diabetes are at increased risk of infection due to dysregulation of the innate and humoral immune system. Previous studies demonstrated that hyperglycaemia upregulates adhesion molecules (intracellular cell adhesion molecule-1, vascular cell adhesion molecule-1 and E-selectin and CD11b) on endothelial cells and neutrophils (59, 60) , which is believed to diminish neutrophil chemotaxis at sites of infection (1). Acute hyperglycaemia also impairs neutrophil phagocytosis and bactericidal activity (59, 61, 62) , respiratory burst capacity (63, 64) and formation of granular elastase and myeloperoxidase extracellular traps leading to susceptibility to infection (65) . Acute hyperglycaemia has also been associated with reduced complement fixation and opsonization of microorganisms (66) .

isolated from individuals with diabetes has been reported (57) . These inflammatory mediators are important for inducing the adaptive immune response, and therefore may explain the increased susceptibility to invading pathogens in people with diabetes (67).

Further evidence suggests that insulin treatment may restore immune function by improving chemotaxis, phagocytosis and bactericidal capacities of neutrophils (9, 68) and thereby supporting the importance of adequate blood glucose management during COVID-19.

Zhu et al utilized a retrospective longitudinal multi-centered cohort study to investigate the relationship between plasma glucose levels and COVID-19 outcome in 952 patients with diabetes (69) . They found inpatient plasma glucose levels more than 10mmol/L were associated with adverse outcomes and death from COVID-19. The hazard ratio (HR), adjusted for age, gender, comorbidities, and site effect, of the all-cause mortality in the well managed type 2 diabetes mellitus (T2DM) group (blood glucose <10mmol/L) compared to the suboptimally managed T2DM group (blood glucose >10mmol/L) was 0.13 (95%CI, 0.04-0.44; p < 0.001) (69) . The prevalence of acute respiratory distress syndrome and acute heart injury were also lower in the well managed T2DM group, HR 0.41 (95% CI, 0.25-0.66, p < 0.001) and 0.21 (95% CI, 0.07-0.59, p = 0.003) respectively (69) . However, authors did not have access to pre-hospital data and therefore were unable to determine the associations between prehospital glycemic status on the natural history of COVID-19, nor investigate if active inpatient management of hyperglycaemia improved COVID-19 adverse outcomes.

Patients with stress hyperglycaemia, without a previous history of diabetes, is associated with an increase in COVID-19 disease severity and mortality as seen in those with established diabetes (70) . Additionally, in these individuals, increased levels of raised inflammatory biomarkers, hypercoagulopathy as well as leukocytosis and neutrophilia were also comparable to those seen in patients with established diabetes (70, 71) , suggesting that perhaps hyperglycaemia may reflect consequences of a counter-regulatory state during severe COVID-19 infection (71). Similar outcomes have been observed in retrospective studies in the USA. Among hospitalized patients with COVID-19, those with diabetes and/or uncontrolled hyperglycaemia had a four-fold increase mortality rate than those without (28% vs 6.2%, P<0.001). Patients with diabetes and/or uncontrolled hyperglycaemia who survived and were discharged from hospital, had a significant increase length of stay compared to their counterparts (median 5.7 vs 4.3 days, P < .001) (72) .

glucose index (TyG) with severity and mortality of COVID-19 (73) . They found that TyG index levels were significantly higher in the severe cases and death group after controlling for confounding variables. The TyG index has been positively associated with arterial stiffness, nephric microvascular damage and coronary artery disease, however is not a direct marker of metabolic control (73) .

Whilst there is substantial evidence to suggest a strong association between hyperglycaemia, irrespective of diabetes status, and poorer prognosis, it is difficult to prove cause and effect based on the available observational studies. Further interventional studies are required to draw definitive conclusions.

has projected the global economy to contract sharply by approximately three percent, surpassing that of the 2008 global financial crisis (74) . In Australia, unemployment rates are expected to rise to 10%, almost doubled from rates in February this year (75) . The Australian government has responded quickly with stimulus packages of almost $320 billion dollars, providing financial support to businesses and employees, education providers and other community services including the "JobKeeper" and "JobSeeker" packages (76).

According to the Department of Agriculture, approximately 90% of Australia's' food supply is sourced locally with Australia producing substantially more food than it consumes (77). Despite this, uncertainties around the impacts of COVID-19 initially triggered panic buying and stockpiling of staple goods resulting in temporary disruption in supermarket supply (77). It is unclear what the impact of social isolation, home schooling and financial instability will have on healthy eating behaviours and glycaemia management. The disruption to work, school and social routine may lead to "stress and emotional eating" of high-calorie and high glycaemic index foods (78). Legislative changes have also been introduced to legalise electronic prescriptions and home delivery of medications for vulnerable patients and those in isolation (84).

Hospitals have converted the majority of face to face outpatient appointments to telehealth consultations, with the main provider of telehealth consultations reporting increased usage from 400 consultations to over 10,000 a day (85) . The use of telehealth in the management of diabetes prior to the pandemic has been well documented with evidence to support improved glycaemic management (86, 87) and patient satisfaction (88) compared to conventional health services. Although long-term outcomes from telehealth are lacking, short to intermediate term improvement in hyperglycaemia and patient engagement makes telehealth a viable way to deliver health care during periods of pandemic and natural disasters. There are however potential barriers to telehealth such as internet connectivity, age, fear and lack of support to use technology, access to devices, patient preference for faceto-face encounters and patients with hearing and/or vision impairments (89). With the increasing use of insulin pump therapy and CGM devices, telemonitoring of diabetes management can be improved to help support individuals with diabetes and avoid prolong hyperglycaemia and its complications. This increase in technology will also greatly complement telehealth by providing invaluable, real-time data and improve patient engagement and contact through the COVID-19 pandemic and beyond. Clinicians can access the uploaded reports remotely and assist people with diabetes remotely leading to collaborative decision making to improve outcomes including reducing hypo and hyperglycaemia (92).

People with diabetes are more likely to experience severe infection and death from COVID-19. Frailty, pre-existing comorbid conditions and underlying immune system dysfunction may contribute to poorer outcomes. We suggest the continuation of usual care for people with diabetes incorporating telehealth, with a larger focus on sick day management, early detection and testing for SARS-CoV-2 where permissible and increased blood glucose testing to account for changes in daily routine, diet and mental health. Health  Have enough household items and groceries on hand so that you will be prepared if required to quarantine for a period of time  Write down the phone numbers of your doctor, diabetes educator and local pharmacy.  Write down a list of your usual medications and doses.  You should have a 30-day supply of insulin and other diabetes medications, in the unlikely event that you are quarantined.  Ensure you have supply of insulin pump consumables and continuous glucose monitoring device.  All patients with type 1 diabetes should have sufficient supply of ketone testing strips (and glucagon if prescribed by your doctor).

 Engage with your diabetes team and your pump supplier and learn how to upload pump data to your diabetes nurse educator, endocrinologist or doctor while in isolation  Continue to monitor your blood glucose level (BGL). If your glucose management is unsatisfactory (BGLs consistently more than 12 mmol/l, or less than 5 mmol/l) speak to your doctor or diabetes nurse educator for assistance with medication adjustments.  Ketone levels should be checked every 1-2 hours when BGLs are more than 15 mmol/l. Call your doctor immediately if you have raised ketones.  If you experience a hypo (BGL less than 4 mmol/l), eat 15 g of simple carbohydrates (5 jelly beans or ½ can of full strength soft drink) and recheck your BGL in 15 minutes to ensure your levels are rising.  Develop a "sick day management plan" with your doctor or diabetes nurse educator People with type 2 diabetes  Continue to monitor your blood glucose level (BGL). If your glucose control is unsatisfactory (BGLs consistently more than 12 mmol/l, or less than 5 mmol/l) speak to your doctor or diabetes nurse educator for assistance with medication adjustments.  If you experience a hypo (BGL less than 4 mmol/l), eat 15 g of simple carbohydrates (5 jelly beans or ½ can of full strength soft drink) and recheck your BGL in 15 minutes to ensure your levels are rising.  Continue taking your usual oral medications and insulin as prescribed by your doctor.  If you are unwell with nausea and vomiting, or unable to tolerate oral intake, stop taking your SGLT inhibitor (empagliflozin, dapagliflozin, ertugliflozin) to prevent ketoacidosis.  Develop a "sick day management plan" with your doctor or diabetes nurse educator information system)

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