Logo-aim
Arch Iran Med. 26(6):316-321. doi: 10.34172/aim.2023.48

Original Article

Epidemiological Features and Outcomes of COVID-19 in Patients With and Without Cardiovascular Disease

Elahe Piraee Validation, Writing – original draft, 1 ORCID logo
Habibollah Azarbakhsh Data curation, Formal analysis, Methodology, 2 ORCID logo
Ghulamraza mohammadyan Resources, Writing – original draft, 3
Leila Moftakhar Conceptualization, Investigation, Supervision, 4, * ORCID logo
Aliasghar Valipour Writing – original draft, Writing – review & editing, 5

Author information:
1Social Determinants of Health Research Center, Yasuj University of Medical Sciences, Yasuj, Iran
2Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
3Department of Biostatistics and Epidemiology, Faculty of Public Health, Kerman University of Medical Sciences, Kerman, Iran
4Abadan University of Medical Sciences, Abadan, Iran
5Department of Public Health, Abadan University of Medical Sciences, Abadan, Iran

*Corresponding Author: Leila Moftakhar, Email: moftakhar_p@yahoo.com

Abstract

Background:

Cardiovascular diseases (CVDs) are known as an important group of risk factor for progression of the Coronavirus-19 disease (COVID-19). The present study compared epidemiological features and outcomes in COVID-19 patients with CVDs versus those without CVDs.

Methods:

This is a retrospective study performed on 1497 patients with CVDs and 26926 patients without CVDs, all of whom were confirmed to have COVID-19. All clinical signs and comorbidities were investigated in the subjects. Mann-Whitney U test and Pearson’s Chi-square test were applied to compare mortality between the groups. Logistic regression was used to identify the predictors of mortality among patients.

Results:

The mean age of COVID-19 patients with underlying CVD was 60 years. Totally, about 5.3% of the individuals under study had CVD. Also, 21.6% of all deaths occurred in COVID-19 patients with CVD. Cough, fever, shortness of breath, muscle pain, and underlying diseases such as diabetes, hypertension, chronic liver and kidney disease, chronic lung disease, and immunodeficiency were significantly higher in patients with CVD than those without CVDs. The odds of death in COVID-19 patients were 1.9 times higher with underlying CVD, 2.1 times with diabetes, 3.4 times with hypertension, 1.9 times with immunodeficiency, and 2.3 times with chronic liver and kidney disease.

Conclusion:

CVDs are a serious threat to COVID-19 patients because they increase mortality among these patients. As a result, preventive and therapeutic strategies must be developed for these vulnerable groups, who will be prone to higher mortality.

Keywords: Cardiovascular disease, COVID-19, Mortality

Copyright and License Information

© 2023 The Author(s).
This is an open-access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Cite this article as: Piraee E, Azarbakhsh H, Mohammadyan G, Moftakhar L, Valipour A. Epidemiological features and outcomes of COVID-19 in patients with and without cardiovascular disease. Arch Iran Med. 2023;26(6):316-321. doi: 10.34172/aim.2023.48


Introduction

The coronavirus-19 disease (COVID-19) is a type of severe acute respiratory syndrome, which is caused by a beta-coronavirus (SARS-CoV-2 virus). This disease was first reported in China in December 2019.1,2 Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) targets the respiratory tract and is clinically similar to severe acute respiratory syndrome of coronavirus (SARS-CoV) and Middle East respiratory syndrome coronavirus (MERS-CoV).3 The most common symptoms of this disease are fever, fatigue, and cough, followed by anorexia, myalgia, shortness of breath, etc.4-8

Patients with COVID-19 show significant differences in length of hospitalization, disease progression, and prognosis.9 Several meta-analyses have shown that COVID-19 patients with cardiovascular diseases (CVDs), hypertension, diabetes, chronic kidney disease, congestive heart failure, and cancer are at higher risk of death compared to those without these diseases.1,2,10,11 Among these diseases, CVDs are the leading cause of death in the world, and account for approximately 17.9 million deaths annually. CVDs are a group of disorders of the heart and blood vessels, including coronary heart disease, rheumatic heart disease, cerebrovascular disease, and others. More than four out of five CVD deaths are due to heart attack and stroke, and one third of these deaths occur prematurely in individuals under 70 years of age.12

In addition, CVDs increase the risk of death among hospitalized COVID-19 patients.13,14 In a study on 44,672 COVID-19-confirmed patients in Wuhan, the mortality rate in patients with CVD was reported as 10.5%, while the overall mortality rate was 2.3%.15

CVD is an important risk factor for rapid progression in COVID-19; hence, more acute medical care and services should be provided to COVID-19 patients with CVD. The present study was conducted to investigate and compare the epidemiological feature and outcomes of COVID-19 patients with CVD versus those without CVD.


Materials and Methods

In this retrospective observational study, we recruited 28 426 patients with COVID-19 who were admitted to the educational hospitals of Abadan University of Medical Sciences, Southwestern Khuzestan, Iran between February, 2020 and December, 2020. The total population in this region was estimated at 627 970 people, according to the national census in 2020. COVID-19 infection should be confirmed by RT-PCR test on nasal and throat swab samples or definite evidence on high resolution computed tomography (HRCT) imaging. Hospitalized patients were those with severe symptoms such as shortness of breath and chest pain, as well as a saturated oxygen levels < 90%. In addition, some patients who had saturated oxygen levels between 90 and 93% were either admitted to hospital or paced in home quarantine, as judged by the physician according to their clinical condition and underlying diseases. In the region under study, there were only two hospitals, and all stages of hospitalization of patients and testing were performed according to the national guidelines of COVID-19 management, similar to other medical centers in the country. The clinical and demographic information of patients, as well as the outcome of each patient, were recorded.

After collecting data, duplicate cases were identified and removed based on the national ID number. Patients were divided into two groups: CVD (n = 1497) and non-CVD (n = 26926). First, demographic features, symptoms and underlying conditions were compared between the two study groups; then, the effect of underlying conditions on mortality was examined. Finally, the subset of deceased subjects from the two study group were compared in terms of clinical signs and underlying conditions. The studied variables were age, gender, job, outcome (death vs. survival), symptoms (i.e. shortness of breath, fever, cough, loss of smell and taste, fatigue, muscle pain, gastrointestinal symptoms, sore throat, headache, dizziness, and bloodshot eyes) as well as underlying diseases (i.e. hypertension, diabetes, CVDs, kidney disease, liver disease, chronic lung disease, immunodeficiency, and thyroid disease).

Statistical Analyses

We used median (interquartile range [IQR]) and frequency (percent) to describe the quantitative and qualitative variables, respectively. Group comparison was carried out using Pearson’s chi-square test and Fisher’s exact test for qualitative variables and Mann-Whitney U test for the quantitative variable (age). The normality of the quantitative variable (age) was assessed by Kolmogorov-Smirnov test. We first performed univariate analysis to determine the factors associated with mortality among patients with COVID-19. Then, variables with P value < 0.2 were entered into multivariate logistic regression. Data analysis was performed using SPSS version 20.0 and Excel spreadsheet 2016. Statistical significance level was also considered at 0.05


Results

During the study period, 28,426 cases of COVID-19 were identified. The median age of patients was 38 [29–50] years, and 56.2% of the subjects were males. Most of the patients (73.2%) mentioned contact with a suspected or definite case of COVID-19. Also, 939 (3.3%) of the patients died, of whom 203 subjects (21.6%) had CVD (Table 1).


Table 1. The Characteristics of COVID-19 Patients with or without Cardiovascular Disease
Variable Total (N=28426) No. (%) Cardiovascular (n=1497) No. (%) Non- Cardiovascular (n=26926) No. (%) P Value
Age, median (IQR) 38 (29-50) 60 (49-70) 37 (29 – 49)  < 0.001
Gender
Male 15970 (56.2) 751 (50.2) 15219 (56.5)  < 0.001
Female 12456 (43.8) 746 (49.8) 11710 (43.4)
Symptoms
Fever 15651 (55.1) 948 (63.3) 14703 (54.6)  < 0.001
Cough 16420 (57.8) 898 (60.0) 15522 (57.6)  < 0.001
Dyspnea 10092 (35.5) 714 (47.7) 9378 (34.8)  < 0.001
Muscular pain 4299 (15.12) 243 (16.2) 4056 (15.1)  < 0.001
Diarrhea 1639 (5.) 90 (6.0) 1549 (5.8)  < 0.001
Runny nose 62 (0.21) 1 (0.1) 61 (0.2) 0.198
Sore throat 685 (2.4) 30 (2.0) 655 (2.4) 0.290
Anorexia 91 (0.3) 3 (0.2) 88 (3) 0.510
Headache/Vertigo 776 (2.7) 42 (2.8) 734 (2.7) 0.805
Fatigue 298 (1.1) 19 (1.3) 279 (1.0) 0.380
Eye redness 16 (0.1) 0 (0.0) 16 (0.1) 0.340
Decreased sense of smell 931 (3.3) 2 (0.1) 929 (3.5)  < 0.001
Decreased sense of taste 863 (3.0) 49 (3.3) 813 (3.0) 0.570
Shiver 1647 (5.8) 61 (4.1) 1586 (5.9) 0.003
Comorbidities
Hypertension 1579 (5.5) 379 (25.3) 1200 (4.5)  < 0.001
diabetes 2288 (8.0) 520 (34.7) 1768 (6.6)  < 0.001
Immunodeficiency 569 (2.0) 88 (5.9) 481 (1.8)  < 0.001
Chronic kidney, liver disease 425 (1.5) 51 (3.4) 374 (1.4)  < 0.001
Chronic pulmonary disease 746 (2.6) 141 (9.4) 605 (2.2)  < 0.001
History of ICU admission 94 (0.3) 19 (1.3) 75 (0.3)  < 0.001
Travel history 60 (0.2) 0 (0) 60 (0.2)  < 0.001
Exposure to disease 20813 (73.2) 1010 (67.5) 19803 (73.5)  < 0.001
Mortality 939 (3.3) 203 (13.6) 736 (2.7)  < 0.001

The most common symptoms were cough (57.8%), fever (55.1%), and shortness of breath (35.5%), muscle pain (15.1%), and gastrointestinal symptoms (5.8%). The most common underlying diseases were diabetes (8%) hypertension (5.6%), CVDs (5.3%), immunodeficiency diseases (including cancers) (2%), chronic lung disease (2.6%), and chronic kidney and liver diseases (1.70%) (Table 1).

In all study participants, 1497 (5.3%) had CVD and 26926 (94.7%) had no CVDs. Compared to non-CVD patients, CVD patients were older (37 [29–49] vs. 60 [49–70] years).

In addition, other underlying diseases were more prevalent in CVD patients than those without CVD: diabetes (520 [34.7%] vs. 1768 [6.6%]), hypertension (379 [25.3%] vs. 1200 [4.5%]), chronic lung disease (141 [9.4%] vs. 605 [2.2%]), chronic liver and kidney diseases (51 [3.4%] vs. 374 [1.4%]), and thyroid disease (17 [1.1%] vs. 158 [0.6%]) (Table 1).

A total of 27,277 patients (95.9%) survived COVID-19. Compared to these patients, deceased patients were significantly older (66 [ 55–76] vs. 37 [29–49] years, P < 0.001), and had a higher prevalence of chronic diseases including diabetes (P < 0.001), hypertension (P< 0.001), CKD (P < 0.001), chronic liver diseases (P < 0.001), chronic pulmonary diseases (P < 0.001), immunodeficiency (P < 0.001), and thyroid disease (P < 0.001) (Table 2).


Table 2. Baseline Characteristics of Survivors and Non-survivors Infected with COVID-19
Variable Total (N=28216)
No. (%)
Survivors (n=27277)
No. (%)
Non-survivors (n=939)
No. (%)
P value
Age, median (IQR) 38 (29-50) 37 (29-49) 66 (55-76)  < 0.001
Gender
Male 15970 (56.2) 15456 (56.7) 514 (54.7) 0.510
Female 12456 (43.8) 12031 (43.3) 425 (45.3)
JOB
Worker 1160 (6.2) 1148 (4.2) 2 (0.7)  < 0.001
Health worker 1974 (10.4) 1958 (7.2) 1 (0.4)
Employee 3706 (19.5) 3675 (13.5) 5 (1.9)
Freelance worker 3772 (19.8) 3724 (13.6) 21 (7.8)
Student, college student 1355 (7.1) 1331 (4.9) 8 (3)
Disabled, elderly 666 (3.5) 616 (2.3) 48 (17.9)
Housekeeper 4835 (25.4) 104 (.4) 4686 (25.2)
Child-neonatal 225 (1.2) 222 (1.2) 1 (0.4)
Retired 499 (2.6) 32 (11.9) 464 (2.5)
Unemployed 704 (3.7) 45 (16.8) 648 (3.5)
Farmer 131 (0.7) 1 (0.4) 130 (0/7)
Comorbidities
Diabetes mellitus 2288 (8.0) 2011 (7.4) 277 (29.5)  < 0.001
Hypertension 1579 (5.5) 1326 (4.9) 253 (26.9)  < 0.001
Thyroid disease 175 (0.6) 160 (0.6) 15 (1.6)  < 0.001
Immunodeficiency 569 (2.0) 486 (1.8) 83 (8.8)  < 0.001
Chronic kidney, liver disease 425 (1.5) 379 (1.4) 46 (4.9)  < 0.001
Chronic pulmonary disease 746 (2.6) 682 (2.5) 64 (6.8)  < 0.001

Moreover, in the CVD group, deceased patients were significantly older than the survivors (69 [61–78] vs. 59 [47–68] years, P < 0.001). Risk of fever (P = 0.020), dyspnea (P < 0.001), muscle pain (P = 0.048), hypertension (P < 0.001), and diabetes (P = 0.010) was higher in deceased patients. Gender, other underlying diseases, and frequency of symptoms showed no significant difference between the two subsets of COVID-19 patients who had CVDs (Table 3).


Table 3. Baseline Characteristics of Survivors and Non-survivors in COVID-19 Patients With Cardiovascular Disease
Variable Total (N=1495)
No. (%)
Survivors (n=1282)
No. (%)
Non-survivors (n=203)
No. (%)
P value
Age, median (IQR) 60 (49-70) 59 (47-68) 69 (61-78)  < 0.001
Sex
Male 751 (50.2) 648 (50.1) 103 (50.7) 0.830
Female 746 (49.8) 646 (49.9) 100 (49.3)
Symptoms
Fever 948 (63.3) 800 (61.8) 148 (72.9) 0.020
Cough 898 (60.0) 761 (58.8) 137 (67.5) 0.180
Dyspnea 714 (47.7) 594 (45.9) 120 (59.1)  < 0.001
Muscular pain 243 (16.2) 224 (17.3) 19 (9.3) 0.048
Gastrointestinal symptoms 90 (6.0) 85 (6.5) 5 (2.5) 0.097
Sore throat 30 (2.0) 24 (1.8) 6 (2.9)  < 0.001
Comorbidities
Hypertension 379 (25.3) 298 (23.0) 81 (39.9)  < 0.001
Diabetes 520 (34.7) 431 (33.3) 89 (43.8) 0.010
Immunodeficiency 88 (5.9) 75 (5.8) 13 (6.4) 0.870
Chronic pulmonary disease 141 (9.4) 113 (8.7) 28 (13.8) 0.070
Chronic liver, kidney disease 51 (3.4) 40 (3.1) 11 (5.4) 0.190
Exposure to disease 1010 (67.5) 889 (68.7) 121 (59.6) 0.002

The result of multivariate logistic regression showed that the odds of death in COVID-19 patients were 1.9 times higher with underlying CVD, 2.1 times with diabetes, 3.4 times with hypertension, 1.9 times with immunodeficiency, and 2.3 times with chronic liver and kidney disease compared to patients without these diseases. In addition, with each year increase in age, the odds of mortality rose by 1.003 times (Table 4).


Table 4. Predictors of Mortality in Patients With COVID-19 Based on the Results of Multiple Logistic Regression.
Variable OR (95% CI) P Value
Age 1.003 (1.001-1.004)  < 0.001
Cardiovascular disease 1.952 (1.339-2.846) 0.001
Diabetes 2.194 (1.557-3.092)  < 0.001
Hypertension 3.453 (2.461-4.846)  < 0.001
Immunodeficiency 1.927 (1.088-3.413) 0.025
Chronic kidney/liver disease 2.307 (1.203-4.425) 0.012

OR, odds ratio.


Discussion

The present study was conducted on 28,426 COVID-19 patients in southwestern Iran, to compare clinical signs and mortality rate amongst patients with and without CVDs. Even though COVID-19 affects all healthy individuals at any age, there is some evidence that some people with underlying diseases, including CVDs, diabetes, hypertension, etc. as well as older people are more likely to develop a more severe medical condition. Many studies have reported that COVID-19 patients with CVD tend to be more infected with higher rates of ICU admission and mortality.6,7,10,15-20

In this study, 5.3% of COVID-19 patients had CVD, which is inconsistent with the results of similar studies. As such, a meta-analysis on 1,576 people, showed a prevalence of heart disease in patients with COVID-19 as high as 8.4%.21 In a meta-analysis by Rodriguez and colleagues, this rate was 14.4%.22 In other similar studies, the rate of CVD in COVID-19 patients was reported at 12%,23 16.4%,24 15%,6 27%25 and 30%.26 The discrepancy among these reports can be due to differences in sample sizes across studies as well as differences in the cultural, economic and health status of the affected areas, which result in different prevalence rates.

In our study, the rate of ICU admission was higher in patients with CVD than those without CVD (1.3% vs. 0.3%). Many other studies have shown that CVD patients with COVID-19 are more likely to have severe medical conditions and more frequently require ICU admission. Accordingly, the rate of ICU admission of COVID-19 patients with CVD was 25% in China,7 21% in Italy,27 and 14% in New York.28 In our study, although only 5.3% of COVID-19 patients had CVD, about one-fifth (21.6%) of mortalities occurred in this group of patients. A study in China also found that although 4.2% of COVID-19 patients had CVD, a higher proportion of mortality (18.3%) was attributed to these patients.29

The results of the present study showed that the oddsof mortality in COVID-19 patients with CVD was about twice as high as patients without CVD. Li et al conducted a meta-analysis and reported that the risk of mortality in COVID-19 patients with CVD was 4.85 times higher than those without it. Also, it was estimated at 21.4 times higher in a Chinese study,17 and even this figure was doubled in a study on 115 patients in Hong Kong.18 Also, the mortality rate of COVID-19 patients with CVD was 10.5% in China.15 However, the reasons for the higher mortality rate among CVD patients are still unclear. Nevertheless, some studies have suggested that in the context of COVID-19, CVD is associated with reduced cardiac function and accelerated myocardial infarction. Also, metabolic demand and myocardial demand are increased, resulting in increased mortality in these patients.30 Also, CVD patients do not have a stable hemodynamic status, hence left/right ventricular dysfunction and cardiogenic shock would be more likely in COVID-19 infection.20 Moreover, inflammatory responses caused by COVID-19 can promote coronary heart disease to acute coronary syndrome, followed by blood clotting and rupture of arteries.20 It should be noted that 48.3% of deaths related to COVID-19 have occurred in patients who had both CVD and diabetes, and 39.9% among COVID-19 patients with CVD and hypertension. Also, diabetes and hypertension alone increased the oddsof death by 2.1 and 3.4 times, respectively. On the other hand, it is also known that both diabetes and hypertension are possible risk factors for CVDs, so these can exacerbate heart disease. Further research is warranted to determine the role of each of these diseases in death amongst patients with COVID-19.

The median age of COVID-19 patients with CVD was higher than COVID-19 patients without CVD (66 years vs. 37 years), which was in accordance with the results of Xie and colleagues who reported a median age of 66 years in COVID-19 patients with CVD and 58 years in non-CVD patients.31 This may be due to the fact that older people usually have a weakened cellular and humoral immune system, which leads to lower antiviral response, and subsequently virus replication in the body and increased risk of heart attack.32 Also, the risk of hypertension and diabetes, which are risk factors for CVD, increases with age,33 and raises the risk of death in these people.

In our study, the incidence of COVID-19 was almost equal in men and women, while the results of chi-square test showed a significant difference. In another study, it was reported that men were more likely to develop this disease and manifest severe complications.34 The results of our study showed that a number of symptoms, such as cough, fever, dyspnea, muscle pain, diarrhea, and sore throat were higher in COVID-19 patients with CVD than those without CVD, which might reflect a more severe form of COVID-19 in patients with CVD.

Although in our study, laboratory and radiologic results of patients were not available, it must be acknowledged that our study was one of the first studies in Iran examining the clinical characteristics of COVID-19 patients with CVD. Our study was conducted on a large sample size, examined several underlying diseases, and included both mild and severe patients, while many in-line studies were limited to patients with the severe form of COVID-19. Our study also identified the role of underlying diseases and the importance of CVD in the death of patients with COVID-19, and thus, it can help to develop hypotheses for future studies and formulate the necessary strategies in this field.

In conclusion, according to the findings of this present study, CVDs are a serious threat to COVID-19 patients because they can increase the mortality rate. However, there are still many unknown issues about COVID-19; for example, the exact link between the disease and CVDs is not well understood. Management of COVID-19 poses a huge challenge. As a result, preventive and therapeutic strategies should be developed for high risk groups, especially those with CVDs. It is also suggested that CVD patients must take preventive measures, such as quarantine in home and social distancing, avoiding unnecessary visits to medical centers, and paying attention to the preventive guidelines developed by the experts of the World Health Organization.


Acknowledgements

We thank the Department of Health of Abadan University of Medical Sciences.


Competing Interests

The authors declare that they have no competing interests.

Data Availability Statement

The data of this study will not be shared publicly.

Ethical Approval

This study was approved by the Ethics Committee of Abadan University of Medical Science (IR.ABADANSUMS.REC.1399,051)

Funding

None.


References

  1. Driggin E, Madhavan MV, Bikdeli B, Chuich T, Laracy J, Biondi-Zoccai G. Cardiovascular considerations for patients, health care workers, and health systems during the COVID-19 pandemic. J Am Coll Cardiol 2020; 75(18):2352-71. doi: 10.1016/j.jacc.2020.03.031 [Crossref] [ Google Scholar]
  2. Zheng YY, Ma YT, Zhang JY, Xie X. COVID-19 and the cardiovascular system. Nat Rev Cardiol 2020; 17(5):259-60. doi: 10.1038/s41569-020-0360-5 [Crossref] [ Google Scholar]
  3. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med 2020; 382(8):727-33. doi: 10.1056/NEJMoa2001017 [Crossref] [ Google Scholar]
  4. Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 2020; 395(10223):507-13. doi: 10.1016/s0140-6736(20)30211-7 [Crossref] [ Google Scholar]
  5. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, et al. Clinical characteristics of 2019 novel coronavirus infection in China. medRxiv [Preprint]. February 9, 2020. Available from: https://www.medrxiv.org/content/10.1101/2020.02.06.20020974v1.
  6. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395(10223):497-506. doi: 10.1016/s0140-6736(20)30183-5 [Crossref] [ Google Scholar]
  7. Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 2020; 323(11):1061-9. doi: 10.1001/jama.2020.1585 [Crossref] [ Google Scholar]
  8. Hui DS, E IA, Madani TA, Ntoumi F, Kock R, Dar O. The continuing 2019-nCoV epidemic threat of novel coronaviruses to global health - the latest 2019 novel coronavirus outbreak in Wuhan, China. Int J Infect Dis 2020; 91:264-6. doi: 10.1016/j.ijid.2020.01.009 [Crossref] [ Google Scholar]
  9. Li M, Dong Y, Wang H, Guo W, Zhou H, Zhang Z. Cardiovascular disease potentially contributes to the progression and poor prognosis of COVID-19. Nutr Metab Cardiovasc Dis 2020; 30(7):1061-7. doi: 10.1016/j.numecd.2020.04.013 [Crossref] [ Google Scholar]
  10. Ruan Q, Yang K, Wang W, Jiang L, Song J. Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med 2020; 46(5):846-8. doi: 10.1007/s00134-020-05991-x [Crossref] [ Google Scholar]
  11. Ssentongo P, Ssentongo AE, Heilbrunn ES, Ba DM, Chinchilli VM. Association of cardiovascular disease and 10 other pre-existing comorbidities with COVID-19 mortality: a systematic review and meta-analysis. PLoS One 2020; 15(8):e0238215. doi: 10.1371/journal.pone.0238215 [Crossref] [ Google Scholar]
  12. WHO. Cardiovascular Diseases. Available from: https://www.who.int/health-topics/cardiovascular-diseases#tab=tab_1.
  13. Mehra MR, Desai SS, Kuy S, Henry TD, Patel AN. Cardiovascular disease, drug therapy, and mortality in COVID-19. N Engl J Med 2020; 382(25):e102. doi: 10.1056/NEJMoa2007621 [Crossref] [ Google Scholar]
  14. Sabatino J, De Rosa S, Di Salvo G, Indolfi C. Impact of cardiovascular risk profile on COVID-19 outcome A meta-analysis. PLoS One 2020; 15(8):e0237131. doi: 10.1371/journal.pone.0237131 [Crossref] [ Google Scholar]
  15. Wu Z, McGoogan JM. 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. JAMA 2020; 323(13):1239-42. doi: 10.1001/jama.2020.2648 [Crossref] [ Google Scholar]
  16. Yang X, Wang J, Chen C. Serum VEGF and Ang-2 levels in infants before and after laser treatment for retinopathy of prematurity. Fetal Pediatr Pathol 2021; 40(5):407-13. doi: 10.1080/15513815.2020.1721625 [Crossref] [ Google Scholar]
  17. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 2020; 395(10229):1054-62. doi: 10.1016/s0140-6736(20)30566-3 [Crossref] [ Google Scholar]
  18. Chan JW, Ng CK, Chan YH, Mok TY, Lee S, Chu SY. Short term outcome and risk factors for adverse clinical outcomes in adults with severe acute respiratory syndrome (SARS). Thorax 2003; 58(8):686-9. doi: 10.1136/thorax.58.8.686 [Crossref] [ Google Scholar]
  19. Levett JY, Raparelli V, Mardigyan V, Eisenberg MJ. Cardiovascular pathophysiology, epidemiology, and treatment considerations of coronavirus disease 2019 (COVID-19): a review. CJC Open 2021; 3(1):28-40. doi: 10.1016/j.cjco.2020.09.003 [Crossref] [ Google Scholar]
  20. Li X, Guan B, Su T, Liu W, Chen M, Bin Waleed K. Impact of cardiovascular disease and cardiac injury on in-hospital mortality in patients with COVID-19: a systematic review and meta-analysis. Heart 2020; 106(15):1142-7. doi: 10.1136/heartjnl-2020-317062 [Crossref] [ Google Scholar]
  21. Yang J, Zheng Y, Gou X, Pu K, Chen Z, Guo Q. Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: a systematic review and meta-analysis. Int J Infect Dis 2020; 94:91-5. doi: 10.1016/j.ijid.2020.03.017 [Crossref] [ Google Scholar]
  22. Rodriguez-Morales AJ, Cardona-Ospina JA, Gutiérrez-Ocampo E, Villamizar-Peña R, Holguin-Rivera Y, Escalera-Antezana JP. Clinical, laboratory and imaging features of COVID-19: a systematic review and meta-analysis. Travel Med Infect Dis 2020; 34:101623. doi: 10.1016/j.tmaid.2020.101623 [Crossref] [ Google Scholar]
  23. Emami A, Javanmardi F, Pirbonyeh N, Akbari A. Prevalence of underlying diseases in hospitalized patients with COVID-19: a systematic review and meta-analysis. Arch Acad Emerg Med 2020; 8(1):e35. [ Google Scholar]
  24. Li B, Yang J, Zhao F, Zhi L, Wang X, Liu L. Prevalence and impact of cardiovascular metabolic diseases on COVID-19 in China. Clin Res Cardiol 2020; 109(5):531-8. doi: 10.1007/s00392-020-01626-9 [Crossref] [ Google Scholar]
  25. Guo T, Fan Y, Chen M, Wu X, Zhang L, He T. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19). JAMA Cardiol 2020; 5(7):811-8. doi: 10.1001/jamacardio.2020.1017 [Crossref] [ Google Scholar]
  26. Capone V, Cuomo V, Esposito R, Canonico ME, Ilardi F, Prastaro M. Epidemiology, prognosis, and clinical manifestation of cardiovascular disease in COVID-19. Expert Rev Cardiovasc Ther 2020; 18(8):531-9. doi: 10.1080/14779072.2020.1797491 [Crossref] [ Google Scholar]
  27. Grasselli G, Zangrillo A, Zanella A, Antonelli M, Cabrini L, Castelli A. Baseline characteristics and outcomes of 1591 patients infected with SARS-CoV-2 admitted to ICUs of the Lombardy Region, Italy. Jama 2020; 323(16):1574-81. doi: 10.1001/jama.2020.5394 [Crossref] [ Google Scholar]
  28. Goyal P, Choi JJ, Pinheiro LC, Schenck EJ, Chen R, Jabri A. Clinical characteristics of COVID-19 in New York City. N Engl J Med 2020; 382(24):2372-4. doi: 10.1056/NEJMc2010419 [Crossref] [ Google Scholar]
  29. Epidemiology Working Group for NCIP Epidemic Response, Chinese Center for Disease Control and Prevention. [The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China]. Zhonghua Liu Xing Bing Xue Za Zhi. 2020;41(2):145-51. 10.3760/cma.j.issn.0254-6450.2020.02.003. [Chinese].
  30. Tan W, Aboulhosn J. The cardiovascular burden of coronavirus disease 2019 (COVID-19) with a focus on congenital heart disease. Int J Cardiol 2020; 309:70-7. doi: 10.1016/j.ijcard.2020.03.063 [Crossref] [ Google Scholar]
  31. Xie Y, You Q, Wu C, Cao S, Qu G, Yan X. Impact of cardiovascular disease on clinical characteristics and outcomes of coronavirus disease 2019 (COVID-19). Circ J 2020; 84(8):1277-83. doi: 10.1253/circj.CJ-20-0348 [Crossref] [ Google Scholar]
  32. Opal SM, Girard TD, Ely EW. The immunopathogenesis of sepsis in elderly patients. Clin Infect Dis 2005; 41 Suppl 7:S504-12. doi: 10.1086/432007 [Crossref] [ Google Scholar]
  33. Boukhris M, Hillani A, Moroni F, Annabi MS, Addad F, Ribeiro MH. Cardiovascular implications of the COVID-19 pandemic: a global perspective. Can J Cardiol 2020; 36(7):1068-80. doi: 10.1016/j.cjca.2020.05.018 [Crossref] [ Google Scholar]
  34. Guzik TJ, Mohiddin SA, Dimarco A, Patel V, Savvatis K, Marelli-Berg FM. COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options. Cardiovasc Res 2020; 116(10):1666-87. doi: 10.1093/cvr/cvaa106 [Crossref] [ Google Scholar]
Submitted: 19 May 2021
Revised: 13 Dec 2021
Accepted: 21 Dec 2021
First published online: 01 Jun 2023
EndNote EndNote

(Enw Format - Win & Mac)

BibTeX BibTeX

(Bib Format - Win & Mac)

Bookends Bookends

(Ris Format - Mac only)

EasyBib EasyBib

(Ris Format - Win & Mac)

Medlars Medlars

(Txt Format - Win & Mac)

Mendeley Web Mendeley Web
Mendeley Mendeley

(Ris Format - Win & Mac)

Papers Papers

(Ris Format - Win & Mac)

ProCite ProCite

(Ris Format - Win & Mac)

Reference Manager Reference Manager

(Ris Format - Win only)

Refworks Refworks

(Refworks Format - Win & Mac)

Zotero Zotero

(Ris Format - FireFox Plugin)

Abstract View: 1318
PDF Download: 601
Full Text View: 49