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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 5  |  Issue : 2  |  Page : 137-143

Prevalence, risk factors, and outcome of diabetic patients infected with COVID-19 in Saudi Arabia


1 Department of Medicine, King Saud University Medical City, (KSUMC), King Saud University, Riyadh, Saudi Arabia
2 Department of Internal Medicine, King Salman Hospital, Ministry of Health, Riyadh, Saudi Arabia
3 Department of Health Administration, College of Business Administration King Saud University, Riyadh, Saudi Arabia
4 Pharmacy Services Department, King Saud University Medical City (KSUMC), Riyadh, Saudi Arabia
5 General Practitioner, Yanbu General Hospital, Ministry of Health, AlMadinah, Saudi Arabia
6 Internal Medicine Residency Program, Department of Medicine, King Saud University Medical City(KSUMC), Riyadh, Saudi Arabia
7 Internship Program, College of Medicine, King Saud University, Riyadh, Saudi Arabia

Date of Submission28-Mar-2021
Date of Decision18-Oct-2021
Date of Acceptance09-Dec-2021
Date of Web Publication28-Apr-2022

Correspondence Address:
Hadil Abdulkader AlOtair
Department of Medicine, King Saud University Medical city, King Saud University, P O Box 2925(38), Riyadh 11461
Saudi Arabia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jnsm.jnsm_36_21

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  Abstract 


Background: Recent global studies including those coming from Saudi Arabia highlighted the apparent increase in the prevalence and severity of COVID-19 in diabetic patients. Hence, this study was conducted to report the prevalence, clinical outcomes, and risk factors among a cohort of diabetic patients with COVID-19 infection in Saudi Arabia. Research Design and Methods: A retrospective observational case–control study of COVID-19 patients admitted at two major hospitals in Saudi Arabia between April 2020 and July 2020. Electronic charts were retrospectively reviewed, comparing diabetic and nondiabetic patients' demographic, clinical variables, and outcome measures. Results: A total of 564 patients with polymerase chain reaction-confirmed COVID-19 infection were enrolled in the study. Their mean age was 52.3 ± 14.4 years and 254 patients (45%) had diabetes mellitus (DM). Diabetic patients were significantly older compared to patients without DM (P < 0.001) and more likely to have hypertension (P < 0.001), heart failure (P = 0.011), chronic kidney disease (P = 0.002), ischemic heart disease (P = 0.005), and higher D-Dimer level (P = 0.011). Patients with DM had significantly higher risk of acute kidney injury (26.4% vs. 14.8%, P = 0.001) and higher rate of inhospital mortality (25.2% vs. 15.8%, P = 0.006) compared to nondiabetics. The most important independent risk factors in diabetic patients were HbA1c and the average capillary glucose check during admission (P < 0.001). Conclusion: Diabetes is highly prevalent among COVID-19 patients admitted to hospitals in Saudi Arabia. The inhospital mortality rate is increased among diabetic patients of older age group with high HbA1c levels, poor glycemic control during hospitalization, and had multiple comorbid conditions compared to nondiabetics. Early identification of at-risk patients with DM and optimal blood glucose control are extremely important for better clinical outcomes.

Keywords: COVID-19, diabetes mellitus, glucose control, HbA1c, Saudi Arabia


How to cite this article:
AlOtair HA, Sheshah E, AlJuaid MM, AlShaikh MK, AlNajjar FK, AlAshgar LM, Alzeer FA. Prevalence, risk factors, and outcome of diabetic patients infected with COVID-19 in Saudi Arabia. J Nat Sci Med 2022;5:137-43

How to cite this URL:
AlOtair HA, Sheshah E, AlJuaid MM, AlShaikh MK, AlNajjar FK, AlAshgar LM, Alzeer FA. Prevalence, risk factors, and outcome of diabetic patients infected with COVID-19 in Saudi Arabia. J Nat Sci Med [serial online] 2022 [cited 2022 May 21];5:137-43. Available from: https://www.jnsmonline.org/text.asp?2022/5/2/137/344207




  Background Top


The emergence and outbreak of COVID-19 have posed an immense threat to human safety due to its increasing fatal complexion leading to public health crises worldwide. Currently, it has turned into a global pandemic affecting more than 183 million individuals worldwide.[1] In the Kingdom of Saudi Arabia (KSA), 473,112 COVID-19 cases were reported with approximately 7663 deaths, based on the latest report (20 June 2021) from the Saudi Ministry of Health (SMOH) and the Saudi Center of Disease Prevention and Control.[2],[3],[4]

Recent evidences have shown that COVID-19-related mortality and greater risks for hospitalization depend upon several factors including autoimmune conditions specifically patients with diabetes mellitus (DM).[5],[6] A meta-analysis study has demonstrated a 22% prevalence of diabetes among nonsurvivor patients with COVID-19, suggesting diabetes as one of the major risk factors for mortality in COVID-19 patients.[7] Subsequent studies reported that up to half of all admissions of COVID-19 patients to intensive care units (ICUs) had history of DM.[8] The mortality rate of diabetic patients infected with COVID-19 can reach as high as 16%.[9] These studies and others clearly indicate a worse prognosis of COVID-19 among patients with DM.[7],[8],[9]

This represents a major concern for people of KSA due to the higher rate of diabetes prevalence (20% of the total population) and predisposition to risk of COVID-19 infection and related complications.[10],[11],[12] The World Health Organization has ranked Saudi Arabia as having the second-highest rate of DM in the Middle East and seventh highest globally.[13] Two local studies in KSA have recently determined the prevalence of diabetes among patients infected with COVID-19, ranging between 45.7% and 68.3%.[14],[15]

However, the risk factors and possibilities of other comorbidities in relation to the demographic characteristics and laboratory parameters of diabetic patients in Saudi Arabia were not thoroughly explored.

Hence, the present study was aimed to determine the prevalence and possible predictors for the poor outcome in a large cohort of hospitalized patients with DM in Saudi Arabia compared to nondiabetics.


  Research Design and Methods Top


Study design and subject selection

This was a retrospective observational study of patients with COVID-19 who were hospitalized in King Saud University Medical City and King Salman Hospital at Riyadh, Saudi Arabia, from April 2020 to July 2020. Electronic data for demographic details and clinical and laboratory parameters of COVID-19 patients of age 18–80 years were reviewed and analyzed. Pregnant or lactating women, patients diagnosed with cancer or secondary DM, and missing clinical and laboratory data were excluded from this study. All the enrolled patients were categorized into DM and non-DM groups. Patients were confirmed for diabetes having glycosylated hemoglobin, HbA1c value >6.5% on two separate occasions, or received one or more antidiabetic medication.[16]

Methods

Demographic data (e.g., age, sex, and comorbidities), clinical presentation of COVID-19, and medication history were collected from the patients' electronic charts. Baseline of all metrics on admission (blood pressure, body mass index [BMI], (HbA1c), total lipid profile (total cholesterol, high-density lipoprotein, triglycerides and the calculated low-density lipoprotein were recorded. Alanine transaminase (ALT), serum creatinine, D-dimer, complete blood count with differential, serum ferritin, lactate dehydrogenase, and troponin were recorded in the data entry sheet. The average of capillary glucose checks during the days of admission was recorded.

Patient-related outcomes were measured in DM and non-DM groups for proportion of patients with pneumonia, acute respiratory distress syndrome (ARDS) as per Berlin definition,[17] the need for mechanical ventilation, shock, acute kidney injury (AKI), heart failure, ICU admission, length of stay in hospital, viral clearance at day 3, 7, and 14 and inhospital mortality.

AKI was defined as a reduction of renal function within 24 h based on the elevated serum creatinine levels, reduced urine output, need for the renal replacement therapy (dialysis), or the combination of these factors.[18] Acute heart failure was defined as the rapid onset of new or worsening signs and symptoms of heart failure.[19]

Statistical analysis

Demographic and clinical variables were presented using descriptive statistics for the baseline patient characteristics and outcomes. Continuous variables were presented as the means ± standard deviations, while categorical data were expressed as numbers and percentages (%). The continuous data were compared using the independent sample t-test, whereas the categorical variables were analyzed using the Chi-square test. The variables that showed significant differences in the univariate analysis were considered for analysis using binary logistic regression for establishing the association between the independent risk factors and DM. The results were articulated as an odds ratio (OR) and 95% confidence interval (CI). Receiver operating characteristic (ROC) curve was used to assess the discriminative performance of the logistic model. All statistical analyses were performed using the Statistical Package for the Social Sciences software, version 25.0 (SPSS Inc., Chicago, IL, USA). P < 0.05 was considered statistically significant.


  Results Top


Among 564 enrolled COVID-19 patients, 254 (45%) were diabetic and 310 (55%) were nondiabetic with mean age of 52.3 ± 14.4 years [Table 1]. Patients with DM had a significantly higher mean age compared to patients without DM (P < 0.001). The proportion of men was greater (n = 429, 76%) compared to women (n = 135, 24%) with almost 3:1 ratio. The proportion of men in diabetic and nondiabetic groups was not significantly different (44.05% vs. 55.95% respectively, P = 0.405). Overall, non-Saudi individuals (66.1%) were nearly twofolds over Saudi patients (33.9%); however, no significant difference was observed for Saudi participants between diabetic (47.64%) and nondiabetic (52.36%) groups (P = 0.373). The proportion of married patients in diabetic group was significantly lesser compared to nondiabetics (47.97% vs. 52.03, P = 0.003). The average systolic blood pressure (SBP) and diastolic blood pressure on the day of admission were significantly higher in patients with DM compared to non-DM (P = 0.010 and P < 0.001), respectively. No significant change in BMI was observed between the groups (29.6 ± 6.6 vs. 29.7 ± 6.5, P = 0.925).
Table 1: Baseline characteristics of COVID-19 patients with and without diabetes mellitus

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Associated comorbidities

The most common comorbid condition observed in all studied patients was hypertension (35.81%), with a significantly increased proportion in DM (53.9%) compared to nondiabetic (21%) patients (P < 0.001), followed by ischemic heart disease (6.9%), chronic kidney disease (CKD) (5.7%), chronic lung disease (5.5%), heart failure (4.6%), and cerebrovascular accident (4.4%) [Table 1]. All the comorbid conditions, except chronic lung disease, were significantly higher in DM patients compared to non-DM patients (P < 0.05) [Table 1]. Among diabetic COVID-19 patients, the majority of patients (58.7%) had at least one comorbid condition. On the other hand, nondiabetic patients (19.4%) had at least one comorbidity.

Patient-related symptoms

The most common patient-related symptoms were observed for shortness of breath (84.8%) followed by fever (79.3%) and cough (77.3%) [Table 2]. Diabetic patients were more likely to have fever (83.4% vs. 76.4%, P = 0.04) and sputum production (11% vs. 4.8%, P = 0.006) than nondiabetics.
Table 2: The symptoms, medications, laboratory results, and outcomes of COVID-19 patients with and without diabetes mellitus

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Concomitant medications

The most widely prescribed concomitant medications for overall patients were antibiotics (94.5%) followed by steroids (78.9%), azithromycin (78.2%), and hydroxychloroquine (48.2%) [Table 2]. Among all the reported concomitant medications, only angiotensin-converting enzyme (ACE) inhibitors (16.9% vs. 3.9%, P < 0.001) and angiotensin II receptor blockers (ARBs) inhibitors (10.2% vs. 5.2%, P = 0.022) showed significantly increased proportion of diabetic patients taking such medication compared to nondiabetic patients.

Laboratory findings

Analysis of laboratory parameters demonstrated a significant difference in the mean HbA1c between DM and non-DM (9.5 ± 5.9 vs. 6.6 ± 1.8, P < 0.001), D-dimer (3.1 ± 4.2 vs. 2.3 ± 3, P = 0.011), average capillary glucose check during admission (12.1 ± 5.1 vs. 7.2 ± 2.7, P < 0.001), and ALT (55.0 ± 44.8 vs. 77.0 ± 117.1, P = 0.005) [Table 2].

Patient outcome

Patients with DM had significantly higher proportion of developing AKI (26.4% vs. 14.8%, P = 0.001) and higher rate of inhospital mortality (25.2% vs. 15.8%, P = 0.006) compared to nondiabetics [Table 2]. There was a higher percentage of patients with DM who developed ARDS than non-DM; however, this difference did not reach statistical significance (13.8% vs. 9.4%, P = 0.099). All other reported outcome measures did not show significant changes between DM and non-DM groups. Among diabetic COVID-19 patients who died, the majority of them (78%) had at least one or more comorbidities.

Overall association of major risk factors with diabetes mellitus in COVID-19 patients

Overall observation using univariate analysis showed statistically significant variables to enter into a multivariable logistic regression analysis [Table 3]. Hypertension (OR, 3.25; 95% CI, 1.33–7.91; P < 0.05), SBP (OR, 1.03; 95% CI, 1.01–1.06; P < 0.05), HbA1c (OR, 1.03; 95% CI, 1.01–1.06; P < 0.001), and average glucose check during admission (OR, 1.26; 95% CI, 1.12–1.42; P < 0.001) showed significant association with diabetic patients which was also supported with ROC curves [Figure 1]. The area under the ROC curve of 0.851 for HbA1c and 0.812 for average glucose check during admission showed a significant association of these two most important risk factors among patients with DM.
Figure 1: Receiver operating characteristic curves for multivariate logistic regression models of risk fact

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Table 3: Multivariate logistic regression analysis of the risk factors and association with diabetes mellitus

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  Discussion Top


Patients with DM are more susceptible to infections, especially bacteria and viruses affecting the respiratory tract. Hence, diabetic patients have been in the forefront since the advent of COVID-19 pandemic. This study reported 45% of individuals with DM in higher age group who were admitted at two hospitals in Saudi Arabia and showed 25% inhospital mortality among the enrolled diabetic patients with COVID-19. Both hyperglycemia and severe hypoglycemia have been implicated in worsening the overall mortality through cytokine storm, accentuating monocytes, endothelial dysfunction, and multi-organ failure.[20],[21]

Owing to these crucial mechanistic insights of the impact of diabetic conditions, our study identified HbA1c and the average capillary glucose readings during hospitalization as the most important risk factors in diabetic patients. In addition, diabetic patients were more likely to have hypertension (HTN), CKD, and cardiac diseases compared to nondiabetic individuals.

Similar to our findings, a recent multicenter study reported increasing incidence of COVID-19 infection in higher age group (≥65 years) with the most commonly reported conditions such as obesity, diabetes, cardiovascular diseases, hypertension, and chronic lung disease.[22],[23],[24]

Muniyappa and Gubbi described the possible mechanisms by which diabetes enhances COVID-19 related patient morbidity and mortality including (i) enhanced affinity of cellular binding and effective viral entry, (ii) reduced levels of viral clearance, (iii) decreased T-cell activity, and (iv) increased sensitivity to hyperinflammation and cytokine storm.[25]

Several studies have reported heterogeneous nature of COVID-19 related clinical manifestations.[22],[23] We observed hypertension as the foremost clinical manifestation associated with COVID-19-infected diabetic patients (67.83%) followed by ischemic heart disease (6.9%), CKD (5.7%), chronic lung disease (5.5%), heart failure (4.6%), and cerebrovascular accident (4.4%).

The prevalence of DM in our cohort of patients was higher than in earlier studies. A Multicenter study of the weekly hospitalization rate in US hospitals found DM to be one of the most common comorbid conditions reported in 28.3% of COVID-19 adult patients.[26] However, our findings are in agreement with a recent report from SMOH MOH hospital in Riyadh which reported 45.7% of patients with diabetes.[14] This could be in part explained by the high prevalence of DM in the KSA in general.[10] The overall prevalence of abnormal glucose metabolism among patients attending primary health-care centers in Saudi Arabia was reported to be 34.5%.[10] Similar to our study, Alguwaihes et al., reported the prevalence of DM in hospitalized COVID-19 patients to be 68.3%; however, this study included less number of diabetic patients from a single center and did not specifically identify the predictors of mortality among diabetic patients or assessed the associated confounders in diabetic patients.[15]

In this study, the mortality rate among diabetic patients with COVID-19 was high, 25.2%. Guo et al. have reported that the mortality rate of COVID-19 among people with DM was about 16%.[27] Similarly, a large case series conducted by the Chinese Center for Disease Control and Prevention on 44,672 confirmed COVID-19 cases suggested that patients with previous history or underlying cardiovascular condition are at increased risk for developing severe symptoms with high mortality rates representing 10.5% for cardiovascular diseases, 7.3% for diabetes, and 6.0% for hypertension.[5] These studies concur that diabetic patients with COVID-19 infection may have worse outcomes compared to nondiabetics. The higher mortality rate in the present study could be related to the older age and presence of multiple comorbidities in diabetic patients. In addition, patients were recruited from large centers that receive severe cases of COVID-19.

Other possible factors for worse outcome in diabetic patients could be related to the low-grade chronic inflammation related to DM. This might perpetuate the cytokine storm responsible for many of the serious complications of COVID-19.[28] Indeed, it has been reported that different markers of inflammation such as interleukin-6, fibrinogen, C-reactive protein, D-dimer are increased in COVID-19 patients with DM.[28] In the present study, we found that D-dimer levels were significantly higher in diabetic patients compared to nondiabetic.(3.1 ± 4.2 versus 2.3 ± 3, P = 0.011). Another important outcome was reported for AKI in COVID-19 patients with DM. However, possible explanation of its relation with vascular endothelial abnormalities worsened by COVID-19 infection and related thrombophilia remains to be investigated.[14],[20],[29]

In addition, recent studies have demonstrated that SARS-CoV-2 utilizes ACE2 on the surfaces of epithelial cells to bind and gain entry to infected cells. Patients with DM have an increase ACE2 expression on the surface of the cells secondary to the renin–angiotensin system activation.[30] This will no doubt make diabetic patients more susceptible and at risk for severe COVID-19 infection. A higher percentage of patients with DM in our study were using ACE inhibitors or ARBS compared to nondiabetics (27.2% vs. 9.1%, respectively). So far, there is no recommendation by International Societies for ACE inhibitors or ARB discontinuation in patients diagnosed with COVID-19.[31]

Furthermore, binding of ACE2 by SARS-CoV-2 in COVID-19 suggests that prolonged uncontrolled hyperglycemia, and not just a history of DM, may play an important role in the increased complications of COVID-19. An earlier retrospective analysis of 135 patients who died during COVID-19 outbreak in 2006 concluded that a known history of DM, ambient hyperglycemia, and fasting plasma glucose levels were independent predictors for morbidity and mortality.[29] In the present study, HbA1c and the average capillary glucose readings during hospitalization were identified as the most important risk factors in diabetic patients during COVID-19 infection. Similarly, a living systematic review and meta-analysis which was conducted over 22 articles, including 17,687 patients, found “high to moderate” certainty of evidence for associations between older age, preexisting comorbidities (cardiovascular disease, CKD), diabetes treatment, and blood glucose at admission. Patients with a more severe course of diabetes had a poorer prognosis of COVID-19 compared with a milder course of diabetes.[32] This suggests the need for more studies on potential confounders.

Limitations

This study had several limitations of its retrospective design and short duration of data collection. The data collection centers were designated hospitals for severe cases which may lead to high mortality rate, as observed in the study. Further, asymptomatic patients were not tested for COVID-19 infection and remained unreported, thus restricting our analysis to only severe forms of the disease spectrum.

In summary, this study reported increased mortality among diabetic patients of older age group hospitalized with COVID-19 infection and had multiple comorbid conditions compared to nondiabetics. High HbA1c and poor glycemic control during hospitalization were found significantly associated risk factors for increased morbidity and mortality. These findings clearly highlight the need of intensive monitoring and treatment strategies of COVID-19 patients with DM and other comorbidities to abate its devastating effects on outcome measures.

Ethics approval and consent to participate

The research proposal for this study was approved by the Institutional Review Board (IRB) of the King Saud University, Riyadh, Saudi Arabia (IRB Approval Project No. E-204955) for human studies on June 9, 2020. Informed consent was obtained from the subjects or authorized family representatives with strict confidentiality of information gathered.

Availability of data and materials

The datasets used or analyzed during this study are available from the corresponding author upon reasonable request.

Acknowledgments

The authors extend their thanks to the College of Medicine Research Center and Deanship of Scientific Research, King Saud University, Riyadh, Saudi Arabia, for their support and also their deepest gratitude to the Deputyship for Research and Innovation, Ministry of Education, Saudi Arabia, for funding this research work.

Financial support and sponsorship

The authors extend their appreciation to the Deputyship for Research and Innovation, “Ministry of Education” in Saudi Arabia for funding this research work through the project no IFKSURG-247.

Conflicts of interest

There are no conflicts of interest.



 
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