Severe acute respiratory syndrome coronavirus 2 caused a worldwide outbreak. Its associated disease, coronaviruses disease 2019 (COVID-19), causes respiratory, gastrointestinal (GI), inflammatory, and neurologic symptoms.1 In the United States, minorities such as African Americans (AA) and Hispanics (HSP) have shown a higher incidence of the disease.2 , 3. However, no detailed characterization of the disease’s features in these populations has been performed.4
Although the initial focus was on saving lives and developing and delivering vaccines and therapeutics, the focus is shifting toward an assessment of specific features of the disease in different patient groups, variables that affect outcome, and, more importantly, factors that correlate with persistent and recurring symptoms.5 In this study we describe the demographics, clinical features, and GI symptoms of hospitalized minority patients with confirmed severe acute respiratory syndrome coronavirus 2 infection at a tertiary hospital located in Washington, DC. We also sought to determine how these features relate to outcomes and which can be considered for prognosis assessment.
Methods
Patient Selection
A list of 447 hospitalized adult (March to September 2020 at Howard University Hospital) COVID-19 patients was obtained. This study was approved by the Institutional Review Board. Demographics, clinical values, comorbidities, laboratory test results, and treatment data were collected from patient charts.
Statistical Analysis
Patient demographics, symptoms, comorbidities, treatment, and clinical values in relation to outcome was assessed in the overall cohort and in a subgroup analysis of AA, whites (CAU), and HSP. Correlation coefficients were calculated together with a multivariate binary logistic regression analysis to establish associations with death as an outcome. SPSS version 26 (SPSS Inc, Chicago, IL) was used for these analyses.
Results
Overall Features of the Cohort
Our cohort consisted of 447 patients, with 309 AA (69.1%), 27 CAU (6%), and 111 HSP (24.8%) with 71 deaths overall (15.5%). AA and CAU had similar death rates, 18.1% and 18.5%, respectively, whereas HSP had 7.3% deaths. The overall age was 56.1 years, with 53.9 years for survivors vs 68.6 years for those who died. HSP were the youngest, at 44.9 years, whereas CAU were the oldest, at 61.1 years. There were more men (51.1%) than women (48.9%). Our cohort had an average body mass index of 30.6 kg/m2, with HSP having lowest BMI (27.4 kg/m2) vs AA with the highest (31.6 kg/m2) (Table 1 ).
Table 1.
Demography, Clinical Manifestations, and Comorbidities of COVID-19 Patients
| AA | P | CAU | P | HSP | P | Overall | P | |
|---|---|---|---|---|---|---|---|---|
| Total no. of cases | 309 (69.1) | 27 (6) | 111 (24.8) | 447 (100) | ||||
| Deceased | 56 (18.1) | 5 (18.5) | 8 (7.3) | 71 (15.5) | .023a | |||
| Average age, y | 59.7 | <.001 | 61.1 | .021 | 44.9 | .009 | 56.1 | <.001 |
| Survivors | 57.6 | 57.7 | 43.8 | 53.9 | ||||
| Deceased | 69.2 | 76.2 | 60.1 | 68.6 | ||||
| Sex | .53 | .825 | .479 | .41 | ||||
| Men | 157 (50.8) | 15 (55.6) | 54 (49.5) | 227 (51) | ||||
| Survivors | 122 (77.7) | 12 (80) | 50 (90.9) | 184 (81.1) | ||||
| Deceased | 35 (22.3) | 3 (20) | 5 (9.1) | 43 (18.9) | ||||
| Women | 152 (49.2) | 12 (44.4) | 55 (50.5) | 218 (49) | ||||
| Survivors | 131 (86.2) | 10 (83.3) | 51 (94.4) | 192 (88.1) | ||||
| Deceased | 21 (13.8) | 2 (16.7) | 3 (5.6) | 26 (11.9) | ||||
| Mean body mass index, kg/m2 | 31.6 | .155 | 30.5 | .216 | 27.4 | .288 | 30.6 | .223 |
| Normal | 127 (31.2) | |||||||
| Survivors | 65 (76.5) | 6 (75) | 31 (91.2) | 102 (80.3) | ||||
| Deceased | 20 (23.5) | 2 (25) | 3 (8.8) | 25 (19.7) | ||||
| Overweight | 0.450 | 0.640 | 0.658 | 126 (31.4) | .552 | |||
| Survivors | 68 (81.9) | 6 (75) | 33 (94.3) | 107 (84.9) | ||||
| Deceased | 15 (18.1) | 2 (25) | 2 (5.7) | 19 (15.1) | ||||
| Obese | 154 (37.8) | |||||||
| Survivors | 100 (83.3) | 9 (90) | 21 (87.5) | 130 (84.4) | ||||
| Deceased | 20 (16.7) | 1 (10) | 3 (12.5) | 24 (15.6) | ||||
| Fever | 171 (56.4) | 16 (59.2) | 55 (52.9) | 242 (55.8) | ||||
| Survivors | 139 (81.3) | .773 | 14 (87.5) | .332 | 49 (89.1) | .192 | 202 (83.5) | .580 |
| Deceased | 32 (18.7) | 2 (12.5) | 6 (10.9) | 40 (16.5) | ||||
| Cough | 196 (65.7) | 18 (66.6) | 57 (57) | 271 (63.8) | ||||
| Survivors | 162 (82.7) | .631 | 15 (83.3) | .726 | 52 (91.2) | .743 | 229 (84.5) | .841 |
| Deceased | 34 (17.3) | 3 (16.7) | 5 (8.8) | 42 (15.5) | ||||
| Shortness of breath | 198 (65.7) | 16 (61.5) | 57 (55.3) | 271 (63) | ||||
| Survivors | 155 (78.3) | .032 | 13 (81.3) | .937 | 49 (86) | .008 | 217 (80.1) | .002 |
| Deceased | 43 (21.7) | 3 (18.8) | 8 (14) | 54 (19.9) | ||||
| Abdominal pain | 43 (15.4) | 3 (13) | 17 (17.3) | 63 (15.8) | ||||
| Survivors | 40 (93) | .75 | 3 (100) | .328 | 16 (94.1) | .824 | 59 (93.7) | .050 |
| Deceased | 3 (7) | 0 (0) | 1 (5.9) | 4 (6.3) | ||||
| Diarrhea | 67 (22.4) | 6 (23) | 10 (9.7) | 83 (19.4) | ||||
| Survivors | 56 (83.6) | .681 | 5 (83.3) | .856 | 9 (90) | .781 | 70 (84.3) | .994 |
| Deceased | 11 (16.4) | 1 (16.7) | 1 (10) | 13 (15.7) | ||||
| Nausea | 41 (14.2) | 2 (8.3) | 12 (12) | 55 (13.3) | ||||
| Survivors | 35 (85.4) | .661 | 2 (100) | .449 | 12 (100) | .311 | 49 (89.1) | .382 |
| Deceased | 6 (14.6) | 0 (0) | 0 (0) | 6 (10.9) | ||||
| Vomiting | 38 (12.9) | 3 (11.5) | 11 (10.6) | 52 (12.3) | ||||
| Survivors | 33 (86.8) | .465 | 3 (100) | .369 | 11 (100) | .311 | 47 (90.4) | .239 |
| Deceased | 5 (13.2) | 0 (0) | 0 (0) | 5 (9.6) | ||||
| Fatigue | 94 (47.4) | 11 (50) | 25 (35.2) | 130 (44.7) | ||||
| Survivors | 81 (86.2) | .782 | 9 (81.8) | .534 | 22 (88) | .428 | 112 (86.2) | .391 |
| Deceased | 13 (13.8) | 2 (18.2) | 3 (12) | 18 (13.8) | ||||
| Loss of appetite | 86 (33.8) | 1 (4.7) | 19 (20.9) | 106 (29) | ||||
| Survivors | 143 (85.1) | .445 | 1 (100) | .567 | 18 (94.7) | .793 | 89 (84) | .522 |
| Deceased | 25 (14.9) | 0 (0) | 1 (5.3) | 17 (16) | ||||
| Loss of taste | 19 (8) | 2 (9) | 7 (8.1) | 28 (8.1) | ||||
| Survivors | 17 (89.5) | .463 | 2 (100) | .421 | 7 (100) | .450 | 26 (92.9) | .247 |
| Deceased | 2 (10.5) | 0 (0) | 0 (0) | 2 (7.1) | ||||
| GI bleed | 17 (5.6) | 1 (3.7) | 1 (1) | 19 (4.4) | ||||
| Survivors | 11 (64.7) | .057 | 1 (100) | .627 | 0 (0) | .001 | 12 (63.2) | .009 |
| Deceased | 6 (35.3) | 0 (0) | 1 (100) | 7 (36.8) | ||||
| Pancreatitis | 3 (1) | 0 (0) | 1 (1) | 4 (0.9) | ||||
| Survivors | 2 (66.7) | .477 | 0 (0) | N/A | 1 (100) | .769 | 3 (75) | .594 |
| Deceased | 1 (33.3) | 0 (0) | 0 (0) | 1 (25) | ||||
| Cholecystitis | 6 (1.9) | 0 (0) | 1 (1) | 7 (1.6) | ||||
| Survivors | 5 (83.3) | .918 | 0 (0) | N/A | 1 (100) | .769 | 6 (85.7) | .911 |
| Deceased | 1 (16.7) | 0 (0) | 0 (0) | 1 (14.3) | ||||
| Cardiac disease | 71 (24) | 9 (34.6) | 5 (5.1) | 85 (20.2) | ||||
| Survivors | 55 (77.5) | .334 | 6 (66.7) | .184 | 5 (100) | .496 | 66 (77.6) | .084 |
| Deceased | 16 (22.5) | 3 (33.3) | 0 (0) | 19 (22.4) | ||||
| Diabetes mellitus | 128 (43.1) | 9 (34.6) | 25 (25.3) | 162 (38.4) | ||||
| Survivors | 102 (79.7) | .576 | 5 (55.6) | .018 | 20 (80) | .11 | 127 (78.4) | .021 |
| Deceased | 26 (20.3) | 4 (44.4) | 5 (20) | 35 (21.6) | ||||
| Hypertension | 188 (63.3) | 16 (61.5) | 29 (29.3) | 233 (55.2) | ||||
| Survivors | 154 (81.9) | .656 | 11 (68.8) | .049 | 24 (82.8) | .031 | 189 (81.1) | .118 |
| Deceased | 34 (18.1) | 5 (31.2) | 5 (17.2) | 44 (18.9) | ||||
| History of liver disease | 14 (4.7) | 1 (3.8) | 3 (3) | 18 (4.3) | ||||
| Survivors | 9 (64.3) | .095 | 1 (100) | .619 | 3 (100) | .606 | 13 (72.2) | .171 |
| Deceased | 5 (35.7) | 0 (0) | 0 (0) | 5 (27.8) | ||||
| History of inflammatory bowel disease | 4 (1.3) | 0 (0) | 1 (1) | 5 (1.2) | ||||
| Survivors | 3 (75) | .742 | 0 (0) | N/A | 1 (100) | .768 | 4 (80) | .812 |
| Deceased | 1 (25) | 0 (0) | 0 (0) | 1 (20) | ||||
| History of gastroesophageal reflux disease/peptic ulcer disease | 33 (11.1) | 4 (15.3) | 5 (5) | 42 (10) | ||||
| Survivors | 28 (84.8) | .585 | 3 (75) | .750 | 5 (100) | .501 | 36 (85.7) | .734 |
| Deceased | 5 (15.2) | 1 (25) | 0 (0) | 6 (14.3) | ||||
| Immunocompromised | 22 (7.2) | 2 (8) | 4 (3.8) | 28 (6.5) | ||||
| Survivors | 15 (68.2) | .096 | 2 (100) | .461 | 3 (75) | .182 | 20 (71.4) | .060 |
| Deceased | 7 (31.8) | 0 (0) | 1 (25) | 8 (28.6) | ||||
| Alcohol use | 45 (19.9) | 6 (27.2) | 12 (15.4) | 63 (19.3) | ||||
| Survivors | 42 (93.3) | .079 | 5 (83.3) | .910 | 11 (91.7) | .933 | 58 (92.1) | .133 |
| Deceased | 3 (6.7) | 1 (16.7) | 1 (14.3) | 5 (7.9) | ||||
| Elevated ferritin | 166 (61.2) | 14 (66.6) | 47 (62.7) | 227 (61.9) | ||||
| Survivors | 125 (75.3) | .004 | 10 (71.4) | .469 | 41 (87.2) | .445 | 176 (77.5) | .02 |
| Deceased | 41 (24.7) | 4 (28.6) | 6 (12.8) | 51 (22.5) | ||||
| Elevated D-dimer | 244 (90) | 18 (85.7) | 62 (86.1) | 324 (89) | ||||
| Survivors | 193 (79.1) | .031 | 13 (72.2) | .296 | 55 (88.7) | .263 | 261 (80.6) | .008 |
| Deceased | 51 (20.9) | 5 (27.8) | 7 (11.3) | 63 (19.4) | ||||
| Elevated C-reactive protein | 148 (58.4) | 14 (70) | 47 (62.7) | 210 (60) | ||||
| Survivors | 109 (73.2) | <.001 | 10 (71.4) | .573 | 40 (85.11) | .124 | 159 (75.7) | <.001 |
| Deceased | 40 (26.8) | 4 (28.6) | 7 (14.9) | 51 (24.3) | ||||
| Elevated procalcitonin | 98 (38.5) | 7 (31.8) | 20 (29.4) | 125 (36.3) | ||||
| Survivors | 56 (57.1) | <.001 | 3 (42.9) | .009 | 14 (70) | .003 | 73 (58.4) | <.001 |
| Deceased | 42 (52.9) | 4 (57.1) | 6 (30) | 52 (41.6) | ||||
| Mean elevated creatinine | 55.5 | 34.6 | 23.4 | 48.7 | ||||
| Survivors | 0.46 | <.001 | 0.19 | 0.002 | 0.18 | <.001 | 0.37 | <.001 |
| Deceased | 0.96 | 1.00 | 0.87 | 0.95 | ||||
| Elevated IL-6 | 93 (98.9) | 8 (100) | 28 (100) | 129 (99.2) | ||||
| Survivors | 71 (76.3) | .77 | 5 (62.5) | N/A | 27 (96.4) | N/A | 103 (79.8) | .800 |
| Deceased | 22 (23.7) | 3 (37.5) | 1 (3.6) | 26 (20.2) | ||||
| Abnormal platelet count | 35.3 (109) | .18 | 22.2 (6) | .571 | 31 (27.9) | .360 | Low 146 (32.9) | .02 |
| 23.6 (73) | 25.9 (7) | 22 (19.8) | Elevated 102 (23.1) | |||||
| Abnormal lymphocyte count | 1 (3) | .582 | 1 (3.7) | .782 | 106 (95.5) | .814 | Low 1.3 (6) | .628 |
| 295 (95.1) | 25 (92.6) | 2 (1.8) | Elevated 95.3 (434) | |||||
| Elevated cholesterol | 5 (6) | 1 (9) | 0 (0) | 6 (5.2) | ||||
| Survivors | 5 (100) | .166 | 1 (100) | .621 | 0 (0) | N/A | 6 (100) | .174 |
| Deceased | 0 (0) | 0 (0) | 0 (0) | 0 (0) | ||||
| Elevated low-density lipoprotein | 4 (1.3) | 1 (3.7) | 0 (0) | 5 (4.4) | ||||
| Survivors | 4 (100) | .210 | 1 (100) | .621 | 0 (0) | N/A | 5 (100) | .208 |
| Deceased | 0 (0) | 0 (0) | 0 (0) | 0 (0) | ||||
| Elevated high-density lipoprotein | 1 (1.2) | 0 (0) | 0 (0) | 1 (0.9) | ||||
| Survivors | 1 (100) | .542 | 0 (0) | N/A | 0 (0) | N/A | 1 (100) | .583 |
| Deceased | 0 (0) | 0 (0) | 0 (0) | 0 (0) | ||||
| Elevated triglycerides | 34 (38.6) | 3 (27.2) | 6 (30) | 43 (36.1) | ||||
| Survivors | 24 (70.6) | .721 | 2 (66.7) | .425 | 3 (50) | .004 | 29 (67.4) | .118 |
| Deceased | 10 (29.4) | 1 (33.3) | 3 (50) | 14 (32.6) | ||||
| Elevated liver function test values on admission | 107 (37) | 12 (52.1) | 44 (51.2) | 163 (41) | ||||
| Survivors | 72 (67.3) | <.001 | 8 (66.7) | .159 | 41 (93.2) | .417 | 121 (74.2) | <.001 |
| Deceased | 35 (32.7) | 4 (33.3) | 3(6.8) | 42 (25.8) | ||||
| Mean elevated alanine aminotransferase peak | 25 (78.1) | 1 (33.3) | 11 (84.6) | 37 (77.1) | ||||
| Survivors | 60.1 | .258 | 65.6 | .386 | 58.8 | .326 | 60.1 | .878 |
| Deceased | 113.3 | 51.2 | 703.3 | 180.1 | ||||
| Mean elevated aspartate aminotransferase peak | 15 (46.9) | 2 (66.7) | 7 (53.8) | 24 (50) | ||||
| Survivors | 75.5 | .228 | 74.2 | .386 | 56.3 | .612 | 70.6 | .121 |
| Deceased | 246.8 | 77.2 | 1518.5 | 388.1 | ||||
| Pneumonia | 255 (84.4) | 23 (85.1) | 71 (68.9) | 349 (80.8) | ||||
| Survivors | 202 (79.2) | .007 | 18 (78.3) | .302 | 63 (88.7) | .048 | 283 (81.1) | <.001 |
| Deceased | 53 (20.8) | 5 (21.7) | 8 (11.3) | 66 (18.9) |
Values are n (%) unless otherwise defined. N/A, Chi square statistical test is not applicable.
Comparing mortality rate between ethnicities.
Overall, diarrhea was the most common GI symptom (19.4%) followed by abdominal pain (15.8%). GI bleeding was reported in 4.4%, pancreatitis in 0.9%, and cholecystitis in 1.6%. Diarrhea frequency was highest in AA (22.4%), whereas abdominal pain was highest in HSP (17.3%). Of note, 24% of the overall cohort presented these GI manifestations after admission.
The most common comorbidities in our study were hypertension (55.2%) followed by diabetes (38.4%) and cardiac disease (20.2%). With respect to GI comorbidities, the most common was history of liver disease (4.3%) and history of gastroesophageal reflux disease (10%). HSP had the lowest level of pre-existing liver disease, whereas CAU had the highest rate of gastroesophageal reflux disease/peptic ulcer disease history (15.3%), and only 1.3% of AA had a previous diagnosis of inflammatory bowel disease (Table 1).
Overall, 41% of our cohort had abnormal levels in their liver function test panel. CAU had the highest proportion of such patients (52.1%). Elevated alanine aminotransferase was reported in 77.1% of tested patients; this rate was the lowest in CAU (33.3%). Elevated aspartate aminotransferase was reported in 50% and was highest in CAU (66.7%). Other abnormal test results were elevated D-dimer in 89%, abnormal IL-6 in 99.2%, and elevated ferritin in 61.9% (Table 1).
Variable Correlations With Death as an Outcome
Older age (P < .001), shortness of breath (P < .001), abdominal pain (P = .050), GI bleeding (P = .009), diabetes (P = .021), elevated ferritin (P = .02), D-dimer (P = .008), C-reactive protein (P < .001), elevated procalcitonin (P < .001), elevated creatinine (P < .001), altered platelet (P = .002), high liver function test values on admission (P < .001), pneumonia (P < .001), intensive care unit admission/transfer (P ≤ .001), sepsis (P ≤ .001), vasopressors (P < .001), and mechanical ventilation (P < .001) were statistically associated with death in the overall cohort (Supplementary Table 1). For AA, shortness of breath (P = .032), elevated ferritin (P = .004), D-dimer (P = .031), C-reactive protein (P < .001), procalcitonin (P < .001), liver function test values on admission (P < .001), pneumonia (P = .007), intensive care unit admission (P ≤ .001), intensive care unit transfer (P < .001), sepsis (P < .001), vasopressors (P < .001), and mechanical ventilation (P = .020) were significantly associated with death (Supplementary Table 1). For HSP, shortness of breath (P = .008), GI bleeding (P = .001), hypertension (P = .031), elevated procalcitonin (P = .003), elevated triglycerides (P = .004), pneumonia (P = .048), intensive care unit admission (P = .004), intensive care unit transfer (P < .001), sepsis (P = .004), extracorporeal membrane oxygenation (P = .020), vasopressors (P < .001), Remdesivir (P = .043), and mechanical ventilation (P < .001) were associated with death as an outcome (Supplementary Table 1). For CAU, only associated with death were diabetes (P = .018), hypertension (P = .049), elevated procalcitonin (P = .009), mechanical ventilation (P = .023), and vasopressors (P = .033; Supplementary Table 1).
Discussion
In the overall cohort analysis, age was a major effector of outcome. This was further confirmed in subgroup analyses. Indeed, HSP, the youngest group, had the lowest death rate, whereas CAU, the oldest group, had the highest death rate. Respiratory issues such as shortness of breath and pneumonia requiring intensive care unit care and mechanical ventilation were strongly associated with poor outcome in our patients, regardless of race. Elevated procalcitonin was also a common risk factor. Procalcitonin is primarily increased in response to bacterial-triggered inflammation, pointing to potential opportunistic pathogen activity in the course of COVID-19. Vasopressor use in critically ill patients was also associated with poor outcome, attesting to unstable hemodynamics independent of race.6
The association of diabetes with poor outcome was noted in CAU only, whereas hypertension was common with HSP. This finding reflects the weight of metabolic syndrome in CAU that were the oldest group in our cohort. The small number of CAU in our cohort is a limitation of the study. Within HSP, high triglyceride level was a risk factor reflecting the negative impact of blood fat in coronary artery disease and outcome. Although HSP had a lower body mass index compared with AA, the cumulative effects of high triglyceride levels and hypertension point to the impact of the metabolic syndrome in this group, even though it was the youngest. GI bleeding was reported as a risk factor in HSP as well. Whether this symptom is a cause or consequence risk of hemodynamic instability remains to be explored. Indeed, such cases were reported in patients with thromboembolism.7 Elevated ferritin, D-dimer, and C-reactive protein were major and unique risk factors to AA in the subgroup analysis, highlighting the prevalence of systemic inflammation and coagulopathies in this group.
Of note, elevated liver function test values on admission were significantly associated with poor outcome in our study cohort. A study reported that patients with chronic liver disease were more likely to develop severe COVID-19.8 However, liver function alterations were also reported as a result of COVID-19 or antiviral treatment during hospitalization. Diarrhea frequency and abdominal pain were highest in AA and HSP, respectively. They are likely to affect postdischarge patient condition because the virus persists longer in the GI tract after clearance from the respiratory system.
Acknowledgments
CRediT Authorship Contributions
Hassan Ashktorab, PhD (Conceptualization: Lead; Funding acquisition: Lead; Supervision: Lead; Writing – review & editing: Lead). Antonio Pizuorno, MD (Data curation: Equal; Writing – review & editing: Supporting). Farshad Aduli, MD (Writing – review & editing: Equal). Adeyinka O Laiyemo, MD (Writing – review & editing: Equal). Gholamreza Oskrochi, PhD (Formal analysis: Lead). Hassan Brim, PhD (Conceptualization: Equal; Writing – review & editing: Equal).
Footnotes
Conflicts of interest The authors disclose no conflicts.
Funding This project was supported in part by the National Institute on Minority Health and Health Disparities of the National Institutes of Health under Award Number G12MD007597. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Note: To access the supplementary material accompanying this article, visit the online version of Gastroenterology at www.gastrojournal.org and at 10.1053/j.gastro.2021.03.043.
Supplementary Material
Association between treatment and death as an outcome.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Association between treatment and death as an outcome.