Abstract
The association between thromboembolic events (TE) and COVID-19 infection is not completely understood at the population level in the United States. We examined their association using a large US healthcare database. We analyzed data from the Premier Healthcare Database Special COVID-19 Release and conducted a case–control study. The study population consisted of men and non-pregnant women aged ≥ 18 years with (cases) or without (controls) an inpatient ICD-10-CM diagnosis of TE between 3/1/2020 and 6/30/2021. Using multivariable logistic regression, we assessed the association between TE occurrence and COVID-19 diagnosis, adjusting for demographic factors and comorbidities. Among 227,343 cases, 15.2% had a concurrent or prior COVID-19 diagnosis within 30 days of their index TE. Multivariable regression analysis showed a statistically significant association between a COVID-19 diagnosis and TE among cases when compared to controls (adjusted odds ratio [aOR] 1.75, 95% CI 1.72–1.78). The association was more substantial if a COVID-19 diagnosis occurred 1–30 days prior to index hospitalization (aOR 3.00, 95% CI 2.88–3.13) compared to the same encounter as the index hospitalization. Our findings suggest an increased risk of TE among persons within 30 days of being diagnosed COVID-19, highlighting the need for careful consideration of the thrombotic risk among COVID-19 patients, particularly during the first month following diagnosis.
Supplementary Information
The online version contains supplementary material available at 10.1007/s11239-022-02735-0.
Keywords: COVID-19, Thromboembolic events, Case–control study, Healthcare database
Highlights
A strong association was found between thromboembolic events and COVID-19 diagnoses in a large U.S. healthcare database.
The association was particularly pronounced for a COVID-19 diagnosis identified in a previous hospitalization
Our findings suggest opportunity for better screening and medical interventions to prevent thromboembolic events and subsequent admission among COVID-19 patients
Background
Numerous reports have described the occurrence of coagulation events, including venous thromboembolism, among people with SARS-CoV-2 infection [1–5]. However, the association between thromboembolic events and COVID-19 infection is not completely understood at the population level in the United States. Using a large U.S. healthcare database, we examined the association between thromboembolic events and a COVID-19 diagnosis.
Methods
A case–control study was conducted using March 2020–June 2021 data from the Premier Healthcare Database Special COVID-19 Release (PHD-SR). The PHD-SR is an extensive hospital-based administrative all-payer database, which includes longitudinal patient data from > 900 facilities in the United States, representing approximately 20% of U.S. hospital admissions. Thromboembolic events (hereafter referred to as TE) were defined as the occurrence of any of the following: venous thromboembolism (deep vein thrombosis and/or pulmonary embolism), cerebral venous thrombosis, and portal vein thrombosis. The study population consisted of men and non-pregnant women ≥ 18 years of age. Further, cases were defined as persons with an inpatient ICD-10-CM diagnosis of TE between 3/1/2020 and 6/30/2021. Controls were inpatients without TE and matched 2:1 to the cases by sex, age (± 2 years), admission month, and facility; if there were more than two potential controls matching to a case, two were randomly selected (Supplementary Table 1 and 2). The index healthcare related encounter (hereafter referred to as encounter) date was defined as the date of the initial TE healthcare encounter for cases or a patient’s first matched encounter during the matching month (if a matched control had more than one encounter during that month) for controls. We compared the proportion of both cases and controls who had concurrent or prior COVID-19 diagnosis during either inpatient or non-hospital (including emergency department and other type of non-inpatient services, such as clinics, or rehabilitation/skilled nursing/hospice settings) encounters within 30 days of their index TE/non-TE encounter date; we also observed the distributions of timing and encounter type of the COVID-19 diagnosis. Using multivariable logistic regression, we assessed the association between TE occurrence and COVID-19 diagnosis, adjusting for sex, age groups, race/ethnicity, insurance type, urban vs rural location of the facility, U.S. Census region of the facility, and comorbidities associated with TE, which occurred within 6 months prior to the index hospitalization [6]. We also performed separate models to assess the effect of the timing of the COVID-19 diagnosis (concurrent with vs prior to TE); and the combination effect of the timing and the encounter type of the COVID-19 diagnosis (inpatient vs non-hospital encounter type). All ICD-10 and CPT codes used in this study are listed in Supplementary Table 3. All analyses were performed using SAS 9.4 (SAS Institute, Cary NC). Because of the use of secondary data, patient consent was not required for this study. This study was among those using PHD data determined by a CDC review to be research not involving human subjects.
Results
Among 227,343 cases and 454,686 controls, 34,500 (15.2%) cases and 47,021 (10.3%) controls had a concurrent or prior COVID-19 diagnosis within 30 days of their index TE or non-TE inpatient encounter (Table 1). Among 34,500 cases with a COVID-19 diagnosis, 83.1% were diagnosed with COVID-19 during the same encounter as their TE diagnosis, while 16.9% were diagnosed during a separate encounter up to 30 days prior. Among cases with a concurrent or prior COVID-19 diagnosis, 91.8% of the COVID-19 diagnoses occurred during inpatient encounters and 8.2% occurred during non-hospital encounters.
Table 1.
Number and percentage of COVID-19 diagnosis among cases and controls*, by timing and encounter type, Premier Healthcare Database Special COVID-19 Release, March 2020–June 2021
| TE cases (n = 227,343) | Non-TE controls (n = 454,686) | |||
|---|---|---|---|---|
| n | (%) | n | (%) | |
| Had concurrent or prior COVID-19 diagnosis within 30 days of TE or non-TE encounter | ||||
| Yes | 34,500 | (15.2) | 47,021 | (10.3) |
| No | 192,156 | (84.5) | 407,665 | (89.7) |
| Among those with COVID-19 diagnosis within 30 days of TE or non-TE encounter | ||||
| Timing of the COVID-19 diagnosis | ||||
| Same encounter as TE or non-TE | 28,684 | (83.1) | 42,293 | (89.9) |
| Encounter 1–30 days prior to TE or non-TE encounter | 5,816 | (16.9) | 4728 | (10.1) |
| Encounter type of the COVID-19 diagnosis | ||||
| Inpatient or observation encounters | 31,664 | (91.8) | 42,597 | (90.6) |
| Non-hospital* encounters | 2,836 | (8.2) | 4424 | (9.4) |
| Encounter type and timing of the COVID-19 diagnosis | ||||
| Inpatient/observation encounters of COVID-19 diagnosis same encounter as TE or non-TE | 28,684 | (83.1) | 42,293 | (89.9) |
| Inpatient/observation encounters of COVID-19 diagnosis 1–30 days prior to TE or non-TE encounter | 2,980 | (8.6) | 304 | (0.7) |
| Non-hospital* encounters of COVID-19 diagnosis 1–30 days prior to TE or non-TE encounter | 2,836 | (8.2) | 4424 | (9.4) |
TE thromboembolic events defined as the occurrence of any of the following: venous thromboembolism (deep vein thrombosis and/or pulmonary embolism), cerebral venous thrombosis, and portal vein thrombosis
*Non-hospital encounters included emergency department and other type of non-inpatient services, such as clinics, or rehabilitation/skilled nursing/hospice settings
Multivariable regression analysis showed a statistically significant association between a COVID-19 diagnosis and TE among cases compared to controls (adjusted odds ratio [aOR] 1.75, 95% CI 1.72–1.78; Table 2, Model 1). The association was more substantial if a COVID-19 diagnosis occurred 1–30 days prior to index hospitalization (aOR 3.00, 95% CI 2.88–3.13; Table 2, Model 2) compared to the same encounter as the index hospitalization. When considering both timing and encounter type, a COVID-19 diagnosis from a prior inpatient encounter showed a remarkedly strong association of TE occurrence compared to controls (aOR 21.77, 95% CI 19.31–24.55; Table 2, Model 3). Several covariates showed significant positive associations with TE, including female sex, age ≥ 85 years, non-Hispanic black race/ethnicity, and most comorbidities.
Table 2.
Multivariable analysis of demographic and clinical characteristics associated with occurrence of thromboembolic events, premier healthcare database special COVID-19 release, March 2020–June 2021 (n = 609,441)
| Model 1 | Model 2 | Model 3 | |||||||
|---|---|---|---|---|---|---|---|---|---|
| aOR | (95% CI) | p–value | aOR | (95% CI) | p–value | aOR | (95% CI) | p–value | |
| Had concurrent or prior COVID-19 diagnosis within 30 days of TE or non-TE encounter | |||||||||
| Yes | 1.75 | (1.72–1.78) | < .0001 | ||||||
| No | Reference | ||||||||
| Timing of the COVID-19 diagnosis | |||||||||
| No COVID-19 diagnosis | Reference | ||||||||
| COVID-19 diagnosed during same encounter as TE or non-TE | 1.61 | (1.59–1.64) | < .0001 | ||||||
| COVID-19 diagnosed1-30 days prior to TE or non-TE encounter | 3.00 | (2.88–3.13) | < .0001 | ||||||
| Encounter type and timing of the COVID-19 diagnosis | |||||||||
| No COVID-19 diagnosis | Reference | ||||||||
| Inpatient/observation encounters of COVID-19 diagnosis same encounter as TE or non-TE | 1.61 | (1.59–1.64) | < .0001 | ||||||
| Inpatient/observation encounters of COVID-19 diagnosis 1–30 days prior to TE or non-TE encounter | 21.77 | (19.31–24.55) | < .0001 | ||||||
| Non-hospital* encounters of COVID-19 diagnosis 1–30 days prior to TE or non-TE encounter | 1.64 | (1.56–1.73) | < .0001 | ||||||
| Sex | |||||||||
| Male | 0.96 | (0.95–0.97) | < .0001 | 0.96 | (0.95–0.97) | < .0001 | 0.96 | (0.95–0.97) | < .0001 |
| Female | Reference | Reference | Reference | ||||||
| Age group (years) | |||||||||
| 18–49 | Reference | Reference | Reference | ||||||
| 50–64 | 0.92 | (0.90–0.93) | < .0001 | 0.92 | (0.91–0.94) | < .0001 | 0.92 | (0.90–0.93) | < .0001 |
| 65–74 | 0.97 | (0.95–0.99) | 0.0068 | 0.97 | (0.95–0.99) | 0.0124 | 0.97 | (0.95–0.99) | < .0001 |
| 75–84 | 1.00 | (0.98–1.02) | 0.9826 | 1.00 | (0.98–1.03) | 0.8399 | 1.00 | (0.98–1.02) | 0.8593 |
| ≥ 85 | 1.08 | (1.06–1.11) | < .0001 | 1.09 | (1.06–1.21) | < .0001 | 1.08 | (1.05–1.11) | < .0001 |
| Race/ethnicity | |||||||||
| Asian, non-Hispanic | 0.79 | (0.76–0.83) | < .0001 | 0.79 | (0.76–0.83) | < .0001 | 0.79 | (0.76–0.83) | < .0001 |
| Black, non-Hispanic | 1.21 | (1.20–1.23) | < .0001 | 1.21 | (1.20–1.23) | < .0001 | 1.21 | (1.20–1.23) | < .0001 |
| Hispanic | 0.94 | (0.92–0.96) | < .0001 | 0.94 | (0.92–0.95) | < .0001 | 0.94 | (0.92–0.96) | < .0001 |
| White, non-Hispanic | Reference | Reference | Reference | ||||||
| Other | 1.01 | (0.98–1.04) | 0.4265 | 1.01 | (0.99–1.04) | 0.3412 | 1.02 | (0.99–1.04) | 0.2747 |
| Unknown | 1.28 | (1.24–1.33) | < .0001 | 1.28 | (1.24–1.34) | < .0001 | 1.29 | (1.24–1.34) | < .0001 |
| Insurance type | |||||||||
| Medicare | 0.86 | (0.83–0.88) | < .0001 | 0.86 | (0.84–0.88) | < .0001 | 0.86 | (0.83–0.88) | < .0001 |
| Medicaid | 0.93 | (0.91–0.96) | < .0001 | 0.94 | (0.91–0.96) | < .0001 | 0.93 | (0.91–0.96) | < .0001 |
| Managed care | 0.99 | (0.97–1.02) | 0.6446 | 0.99 | (0.97–1.02) | 0.6495 | 1.00 | (0.97–1.02) | 0.6760 |
| Commercial | Reference | Reference | Reference | ||||||
| Self-pay | 1.00 | (0.96–1.04) | 0.9818 | 1.00 | (0.97–1.04) | 0.8828 | 1.00 | (0.96–1.04) | 0.9791 |
| Other | 0.91 | (0.88–0.94) | < .0001 | 0.91 | (0.88–0.94) | < .0001 | 0.91 | (0.87–0.94) | < .0001 |
| Facility urbanicity | |||||||||
| Urban | 0.94 | (0.92–0.95) | < .0001 | 0.94 | (0.92–0.96) | < .0001 | 0.94 | (0.92–0.95) | < .0001 |
| Rural | Reference | Reference | Reference | ||||||
| Facility region | |||||||||
| Midwest | Reference | Reference | Reference | ||||||
| Northeast | 1.03 | (1.01–1.05) | 0.0006 | 1.04 | (1.02–1.05) | 0.0001 | 1.03 | (1.02–1.05) | 0.0002 |
| South | 1.01 | (0.99–1.02) | 0.2682 | 1.01 | (1.00–1.02) | 0.2181 | 1.01 | (1.00–1.02) | 0.1950 |
| West | 1.05 | (1.03–1.07) | < .0001 | 1.05 | (1.03–1.07) | < .0001 | 1.05 | (1.03–1.07) | < .0001 |
| Comorbidities associated with TE** | |||||||||
| Thrombocytopenia | 1.60 | (1.57–1.63) | < .0001 | 1.60 | (1.57–1.63) | < .0001 | 1.59 | (1.57–1.62) | < .0001 |
| Hemorrhagic stroke | 2.30 | (2.21–2.40) | < .0001 | 2.30 | (2.21–2.40) | < .0001 | 2.31 | (2.21–2.40) | < .0001 |
| Ischemic stroke | 0.99 | (0.97–1.01) | 0.4075 | 0.99 | (0.97–1.01) | 0.4240 | 0.99 | (0.97–1.01) | 0.3703 |
| Myocardial infarction | 1.25 | (1.22–1.28) | < .0001 | 1.25 | (1.23–1.28) | < .0001 | 1.25 | (1.22–1.28) | < .0001 |
| Other arterial thrombosis | 2.79 | (2.66–2.94) | < .0001 | 2.79 | (2.66–2.94) | < .0001 | 2.79 | (2.66–2.94) | < .0001 |
| Meningitis, encephalitis, or other CNS | 2.22 | (2.07–2.37) | < .0001 | 2.22 | (2.08–2.37) | < .0001 | 2.22 | (2.07–2.37) | < .0001 |
| Head or neck infection | 1.41 | (1.36–1.46) | < .0001 | 1.40 | (1.35–1.45) | < .0001 | 1.39 | (1.35–1.45) | < .0001 |
| Prior venous thromboembolism | 3.55 | (3.50–3.61) | < .0001 | 3.55 | (3.49–3.60) | < .0001 | 3.55 | (3.49–3.60) | < .0001 |
| Thrombophilia | 3.48 | (3.36–3.60) | < .0001 | 3.48 | (3.37–3.60) | < .0001 | 3.47 | (3.36–3.60) | < .0001 |
| Malignancy | 1.77 | (1.74–1.79) | < .0001 | 1.77 | (1.74–1.79) | < .0001 | 1.77 | (1.74–1.79) | < .0001 |
| Head injury | 1.11 | (1.07–1.15) | < .0001 | 1.11 | (1.08–1.15) | < .0001 | 1.11 | (1.07–1.15) | < .0001 |
| Thyroid disorder | 0.98 | (0.96–0.99) | 0.0006 | 0.97 | (0.96–0.99) | 0.0005 | 0.97 | (0.96–0.99) | 0.0003 |
| Cardiovascular disease | 1.26 | (1.24–1.27) | < .0001 | 1.26 | (1.24–1.27) | < .0001 | 1.26 | (1.24–1.27) | < .0001 |
| Hypertension | 0.83 | (0.82–0.84) | < .0001 | 0.83 | (0.82–0.84) | < .0001 | 0.83 | (0.82–0.84) | < .0001 |
| Obesity | 1.30 | (1.29–1.32) | < .0001 | 1.30 | (1.29–1.32) | < .0001 | 1.30 | (1.29–1.32) | < .0001 |
| Type 2 diabetes | 0.86 | (0.85–0.87) | < .0001 | 0.86 | (0.85–0.87) | < .0001 | 0.86 | (0.85–0.87) | < .0001 |
| Hemorrhagic disorder | 1.68 | (1.63–1.73) | < .0001 | 1.68 | (1.63–1.74) | < .0001 | 1.68 | (1.63–1.73) | < .0001 |
| Systemic lupus | 1.11 | (1.07–1.16) | < .0001 | 1.11 | (1.06–1.15) | < .0001 | 1.11 | (1.06–1.15) | < .0001 |
| Renal disease | 1.32 | (1.31–1.34) | < .0001 | 1.33 | (1.31–1.34) | < .0001 | 1.32 | (1.31–1.34) | < .0001 |
| Liver disease | 1.48 | (1.46–1.51) | < .0001 | 1.48 | (1.46–1.51) | < .0001 | 1.48 | (1.46–1.51) | < .0001 |
aOR adjusted odds ratio, CI confidence interval, CNS central nervous system
Model 1 included cases and controls assessing the association of concurrent or prior COVID-19 diagnosis (exposure) and occurrence of thromboembolic events (outcome) adjusting for covariates. Model 2 included cases and controls assessing the association of timing of COVID-19 diagnosis to index encounter and occurrence of thromboembolic events adjusting for covariates. Model 3 included cases and controls assessing the association of the encounter type and timing of COVID-19 diagnosis and occurrence of thromboembolic events adjusting for covariates. Covariates adjusted for in all three models included sex, age group, race/ethnicity, insurance type, urban vs rural location of the facility, U.S. Census region of the facility, thrombocytopenia, hemorrhagic stroke, ischemic stroke, myocardial infarction, other arterial thrombosis, meningitis, encephalitis, other CNS conditions, head or neck infection, prior venous thromboembolism, thrombophilia, malignancy, head injury, thyroid disorder, cardiovascular disease, hypertension, obesity, type 2 diabetes, hemorrhagic disorder, systemic lupus erythematosus (SLE) or other connective tissue disorder, renal disease, and liver disease
*Non-hospital encounters included emergency department and other type of services not considered as inpatient services
**Comorbidities were identified within 6 months prior to the admission of interest
Discussion
This case–control study using a large U.S. hospital-based data source demonstrated a strong association between TE and prior (within 30 days) or concurrent COVID-19 diagnoses, consistent with data from other studies [3, 7–9]. The association was particularly pronounced for a COVID-19 diagnosis identified in a previous hospitalization. Although in the majority of cases in our study a COVID-19 diagnosis and TE occurred during the same encounter, about 9% of the TE hospitalizations were among patients who were previously admitted with a COVID-19 diagnosis, representing an opportunity for better screening and medical intervention to prevent TE and subsequent readmission. As another consideration, the potential benefits of prolonged TE prophylaxis for selected patients hospitalized with COVID-19 could be assessed. Additionally, patients seen in non-hospital settings with a COVID-19 diagnosis and subsequently admitted to hospital may need additional clinical considerations related to TE prevention based on the potential additional risk that the COVID-19 infection may have conferred. Future studies could assess the relationship between the use and timing of anticoagulation therapy and risk for subsequent TE.
We also observed that the association between COVID-19 and TE was higher among non-Hispanic black people than other racial/ethnical groups, a finding also seen in other studies [8, 9]. Racial disparities in thrombotic risk were found in the pre-COVID-19 era, and COVID-19 infection may have aggravated the gap [10]. Racial differences in the prevalence and severity of COVID-19 have been documented in the United States, possibly due to a higher rate of comorbidities and social disparities in access to health care in black populations [11, 12]. It is important to note that higher ORs among non-Hispanic black persons were found even after controlling for several comorbidities associated with TE. While comorbidities associated with TE were controlled for in our analysis, further confirmatory investigation to better understand other conditions not controlled for is warranted. The adjusted ORs for TE were slightly lower among Medicare and Medicaid patients in this study. We are not sure why this may be; however, the finding merits further investigation.
This study has limitations. First, COVID-19 and TE were defined by ICD-10 diagnosis codes, and some may have been misclassified. Second, our generalizability is limited as our study population was primarily patients diagnosed with COVID-19 during hospitalization prior to or concurrent with the TE admission; the relationship between potentially less severe COVID-19 disease (e.g., patients not requiring hospitalization) and TE risk could be assessed further. Third, although we stratified the associations between TE and COVID-19 by hospital vs non-hospital encounter type, we didn’t quantify the risk based on COVID-19 severity of disease or inflammatory markers. Future cohort studies are needed to understand what factors predispose hospitalized COVID-19 patients to develop TE and thus could benefit from preventive measures. Finally, causality between COVID-19 diagnosis and TE cannot be inferred from our findings due to the case–control design. The strengths of this study are that it is one of the largest U.S.-based studies on this topic that included > 225,000 patients who experienced a thromboembolic event and twice as many controls who were matched based on several characteristics. This study also controlled for several comorbidities known to increase the risk of TE.
In conclusion, our study suggests an increased risk of TE among persons within 30 days of being diagnosed COVID-19. These findings highlight the need for careful consideration of the thrombotic risk among COVID-19 patients, particularly during the first month following diagnosis, as coagulation events can result in worse outcomes. It is essential to implement evidence-based public health prevention strategies, including COVID-19 vaccination, to reduce the risk of COVID-19 and associated morbidity and mortality, as well as measures to prevent TE among patients hospitalized with COVID-19. In this context, it is also important to note that in January of 2022, the Advisory Committee for Immunization Practices (ACIP) recommended that primary and booster doses of COVID-19 vaccinations among persons ≥ 18 years of age be administered preferentially using mRNA vaccines. As more patients have been vaccinated, future studies could assess the effect of vaccination on reducing the TE from COVID-19 infection.
Supplementary Information
Below is the link to the electronic supplementary material.
Funding
No funding external to the Centers for Disease Control and Prevention was provided for this study.
Declarations
Conflict of interest
No conflicts of interest were reported by any authors.
Disclaimer
The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
Footnotes
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