key: cord-0807767-79cd6p3d
authors: Sohn, Minji; Koo, Bo Kyung; Yoon, Ho Il; Song, Kyoung-Ho; Kim, Eu Suk; Kim, Hong Bin; Lim, Soo
title: Impact of COVID-19 and Associated Preventive Measures on Cardiometabolic Risk Factors in South Korea
date: 2021-09-30
journal: J Obes Metab Syndr
DOI: 10.7570/jomes21046
sha: e91ca098254e0a8f0a303814582ae69372494fc5
doc_id: 807767
cord_uid: 79cd6p3d

BACKGROUND: During the coronavirus disease 2019 (COVID-19) pandemic, preventive measures mandated by government policies have included the closure of exercise facilities and movement restriction, which can lead to an unhealthy lifestyle. We investigated the effect of these preventive measures on metabolic parameters in individuals with cardiometabolic disorders. METHODS: In this retrospective, observational study of patients who visited the hospital at least twice a year for the past 4 years, changes in cardiometabolic factors during the COVID-19 pandemic (2019-2020) were compared with changes in the same cohort at the same annual time points during the previous seasons of 2016-2019. RESULTS: A total of 1,485 individuals with a mean age of 61.8±11.7 years were included in the analyses. During the COVID-19 pandemic, the number of patients whose metabolic syndrome worsened increased significantly by 21% compared with the 2018-2019 season. Body mass index increased by 0.09±1.16 kg/m(2) in the 2019-2020 pandemic period, whereas it decreased by -0.39±3.03 kg/m(2) in 2018-2019 and by -0.34±2.18 kg/m(2) in 2017-2018 (both P<0.05). Systolic blood pressure increased by 2.6±18.2 mmHg in the COVID-19 pandemic period, while it decreased in the three antecedent seasons (all P<0.05). Lipid profiles worsened in the pandemic period compared with the previous years. Framingham coronary heart disease risk score also increased significantly. CONCLUSION: Nationwide strategies to maintain cardiometabolic health are necessary during contagious disease pandemics like COVID-19 to mitigate the adverse health effects of pandemic-preventative strategies.

riod of the COVID-19 outbreak compared with before the outbreak based on mobile big data. 4 Thanks to these preventive measures and cooperation from the general public, the number of daily new domestic infections in South Korea fell dramatically.

In the early days following the introduction of these measures, people were cautious and made lifestyle changes, but became less cautious over time. The infection rate dropped from 441 to 47 per day as of October 15, 2020-although it has risen to 621 per day as of February 17, 2021. 5 The Korean government has again raised the crisis alert level, which means stricter observation of social distancing, and a ban on staying in public places and in indoor health facilities, cafes, bars, and any places where people gather together.

Large-scale gatherings are also prohibited (see http://ncov.mohw.

go.kr/en/).

Several groups, including ours, have reported that old age, diabetes mellitus (DM), cardiovascular disease, hypertension, metabolic syndrome, and obesity are risk factors for fatal outcomes of COV-ID-19. 6 People with coronary heart disease (CHD) or DM have a higher chance of being admitted to intensive care units, needing mechanical ventilation, or of dying due to SARS-CoV-2 infection. 7 Because elevated glucose levels directly promote SARS-CoV-2 replication, which essentially requires glycolysis in the host, 8 patients with uncontrolled DM are expected to experience more rapid progression of COVID-19. 6 Moreover, metabolic syndrome induces host immune dysregulation and a proinflammatory milieu, leading to increased severity and mortality when infected with SARS-CoV-2 via vasculopathy, thrombosis, and coagulopathy. 9 Conversely, inactivity associated with social and physical distancing to prevent the spread of COVID-19 might impair metabolic control. 10 

The Korean government reinforced the national public health emergency response by emphasizing the need to maintain social distancing on February 29, 2020. Therefore, we divided clinical data according to date of examination as follows: (1) from Septem- The use of medications for DM, hypertension, and dyslipidemia was also investigated.

Anthropometric and biochemical parameters were measured in SNUBH as reported previously. 14 (5) BMI ≥ 23 kg/m 2 and/or taking anti-obesity agents. Patients with HbA1c ≥ 6.5% and/or taking antidiabetic agents were classified according to the status of DM treatment.

Ten-year CHD risk was calculated using the Framingham risk score (FRS). 17 The correlation of calculated CHD risk with actual 10-year CHD was shown to be stronger when using total cholesterol levels than when using LDL-C scoring in Korean subjects. 18 Therefore, FRS in this study was calculated using TC level.

All data were obtained for the same subjects in all four periods/ seasons. Continuous variables are summarized as mean ± SD and categorical variables are shown as numbers and percentages of subjects. Normality of data distributions were evaluated using the Shapiro-Wilk test and by histograms; all variables were found to be normally distributed with bell-shaped symmetric graphs. Student ttest was used to assess the significance of differences in continuous variables between groups while the chi-square test was used to as- have complete test results. 19 Imputed data were used to analyze changes in values. Relative risk (RR) was calculated as the number of patients who showed worse metabolic syndrome components in 

A total of 1,485 patients with a mean age of 61.8 ± 11.7 years in September 2016 were included in this study. The proportions of men and women were almost equal (male: n = 757, 51.0%). All patients had at least one chronic cardiometabolic impairment such as (Table 1) . In addition, various public health interventions including staying at home, refraining from nonessential social activities, and school closures limit access to healthy food options. 10 These foods are more obesogenic than homemade foods. 24 More specifically, Korean-style fast foods are popular in South Korea because they are less expensive and easier to order regardless of household income level and residential location. 25 Of particular concern, Korean-style fast foods contain high-carbohydrate ingredients such as white flour, white rice, and cornstarch. Increased consumption of these foods is associated with increased energy density and high glycemic load. 26 Some previous studies have shown that increased consumption of fast food and sugar-containing drinks is associated with an increased risk of obesity, metabolic syndrome, and DM. 26, 27 From a sociological context, the COVID-19 pandemic has produced economic disruption and many households are suffering financial distress, limiting their access to healthy foods. In addition, a decrease in outdoor activities and an increase in time spent using the Internet and social network services, playing online games, and watching TV may have also had a negative impact on diet. 28 In the current analysis, body weight, blood pressure, and lipid levels decreased in spring except during the 2019-2020 COVID-19 pandemic season. This is a similar finding to those reported in previous studies. 29 Limited access to exercise facilities and disruption of human relationships also increase psychological stress levels, which likely contributes to elevations in blood pressure and dysregulation of glucose homeostasis as a result of the release of stress hormones such as cortisol and catecholamines by activation of the hypothalamicpituitary-adrenal axis. 34 In fact, the sympathetic system produces increased levels of catecholamines after catastrophic events, which influence the heart and blood vessels negatively. 35 In a dysregulated metabolic status, the renin-angiotensin system is inappropriately activated, which also leads to increased production of angiotensinogen (up to 30% of circulating angiotensinogen) and elevated plasma renin activity, which in turn contributes to an increase in blood pressure and impaired glucose metabolism. 36 Although the effects of this pandemic may not be evident in the short term, its long-term impacts on cardiometabolic risk cannot be ignored. 12 In the current study, males had a significantly increased risk of metabolic syndrome and low HDL-C during the COVID-19 pandemic compared with previous seasons. In general, middle-aged men are more involved in economic activities than women or elderly populations in Korea, 37 and may therefore have been more affected by current preventive measure than females, which could explain the above findings.

Considering the deterioration in cardiometabolic profiles during the COVID-19 pandemic, physicians should focus on patients with metabolic impairment to prevent future adverse cardiovascular events. Elevated release of cytokines in metabolic syndrome status is likely to provoke a "cytokine storm" in those individuals infected with SARS-CoV-2, which may lead to multiorgan failure. 38 Governments and medical institutions must promote physical ac-tivity, healthy eating, and mental health care during such pandemics. Social media or web-based programs can help patients maintain healthy lifestyles. Active counseling to help people with metabolic dysregulation cope with barriers to healthier lifestyles would be helpful in this critical situation. 39 One strength of this study is that we focused exclusively on regularly attending outpatients who were followed-up for 4 years to reduce bias. Nonetheless, the study population was from a single center and only individuals who visited at least twice a year during 2016-2020 were included. Thus, the results reported might not be representative of the broader population in Korea. We did not investigate changes in physical activity or dietary habits in the study subjects. Moreover, it was not possible to observe the actual occurrence of CHD given the short observation period. Instead, we used

10-year CHD risk based on the FRS, but this is a well-established tool that has been used widely for this purpose. 17 In conclusion, we found that the COVID-19 pandemic and its preventive measures had a negative influence on cardiometabolic profiles in subjects with metabolic impairments. This might be because of decreased physical activity and unhealthy dietary patterns linked to preventive measures such as social distancing and lockdown. Movement of individuals decreased in many countries during the COVID-19 pandemic, thus we expect that a similar aggravation in cardiometabolic risks will be found in other countries affected by the pandemic. From a long-term perspective, encouraging home exercise and healthy homemade meals is strongly recommended to mitigate the unfavorable impact of COVID-19 and related government preventive policies on cardiometabolic risk.

Editor of the journal. However, they were not involved in the peer reviewer selection, evaluation, or decision process of this article.

Otherwise, no other potential conflicts of interest relevant to this article were reported.

This research was funded by Yuhan Corporation through a subcontract with Seoul National University Bundang Hospital. The funding agency had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

activity for cardiovascular disease prevention in adults without known cardiovascular disease risk factors: updated evi-dence report and systematic review for the US preventive services task force. JAMA 2017;318:175-93.

TNF-α and inflammatory cytokines and risk of type 2 diabetes: a systematic review and meta-analysis

Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention

Stronger social distancing for 15 days, starting with the government

Stepwise strategy of social distancing in Korea

Sympathetic activation: a potential link between comorbidities and COVID-19

COVID-19 and diabetes mellitus: from pathophysiology to clinical management

Clinical characteristics of coronavirus disease 2019 in China

Elevated glucose levels favor SARS-CoV-2 infection and monocyte response through a HIF-1α/glycolysis-dependent axis

Metabolic syndrome and COVID 19: endocrine-immune-vascular interactions shapes clinical course

Collateral damage of the COVID-19 pandemic on nutritional quality and physical activity: perspective from South Korea

Eating habits and lifestyle changes during COVID-19 lockdown: an Italian survey

COVID-19 pandemic: the effects of quarantine on cardiovascular risk

Seoul National University Bundang Hospital's electronic system for total care

Glycemic efficacy and metabolic consequences of an empagliflozin addon versus conventional dose-increasing strategy in patients with type 2 diabetes inadequately controlled by metformin and sulfonylurea

Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP)

And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III)

World Health Organization, Regional Office for the Western

COVID-19 Preventive Measures and Metabolic Syndrome

The Asia-Pacific perspective: redefining obesity and its treatment. Sydney: Health Communications Australia

Prediction of coronary heart disease using risk factor categories

The assessment of Framingham risk score and 10 year CHD risk according to application of LDL cholesterol or total cholesterol

Mice: multivariate imputation by chained equations in R

Interaction revisited: the difference between two estimates

Self-quarantine and weight gain related risk factors during the COVID-19 pandemic

Metabolic impacts of confinement during the COVID-19 pandemic due to modified diet and physical activity habits

Food price trends in South Korea through time series analysis

A systematic review of fast food access studies

Trends in fast-food and sugar-sweetened beverage consumption and their association with social environmental status in South Korea

Fast-food habits, weight gain, and insulin resistance (the CARDIA study): 15-year prospective analysis

Popkin BM. Differential associations of fast food and restaurant food consumption with 3-y change in body mass index: the Coronary Artery Risk Development in Young Adults Study

Sedentary behavior and dietary intake in children, adolescents, and adults: a systematic review

Time trends (1993-1997) and seasonal variation in body mass index and waist circumference in the Netherlands

Seasonal variation in home blood pressure and its relationship with room temperature in patients with type 2 diabetes

Seasonal variation in serum cholesterol levels: treatment implications and possible mechanisms

COVID-19 and mental health: a review of the existing literature

COVID-19 outbreak: impact of the quarantine-induced stress on cardiovascular disease risk burden

Stress and the HPA axis: role of glucocorticoids in alcohol dependence

Quarantine during COVID-19 outbreak: changes in diet and physical activity increase the risk of cardiovascular disease

The renin angiotensin aldosterone system in obesity and hypertension: roles in the cardiorenal metabolic syndrome

Gender differences in leisure-time physical activity

SARS-CoV-2 infection and obesity: common inflammatory and metabolic aspects

Behavioral counseling to promote a healthful diet and physical

COVID-19 Preventive Measures and Metabolic Syndrome