SciELO - Scientific Electronic Library Online

 
vol.37 issue2Incidence and characterization of colorectal adenomas in the area of influence of a specialized institutionColo-umbilical enterocutaneous fistula as a rare complication of diverticulitis of the sigmoid colon author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Revista colombiana de Gastroenterología

Print version ISSN 0120-9957On-line version ISSN 2500-7440

Rev. colomb. Gastroenterol. vol.37 no.2 Bogotá Jan./June 2022  Epub Aug 24, 2022

https://doi.org/10.22516/25007440.853 

Original article

The behavior of liver diseases in a cohort of Colombian patients with COVID-19

Santiago Sánchez-Pardo1  * 
http://orcid.org/0000-0003-3869-6907

Nathaly Garzón-Orjuela2 
http://orcid.org/0000-0001-6181-8154

Robin Germán Prieto-Ortiz3 
http://orcid.org/0000-0001-7605-760X

Javier Eslava-Schmalbach4 
http://orcid.org/0000-0003-1502-2918

Jhon Edison Prieto-Ortiz.5 
http://orcid.org/0000-0002-8009-5999

1MD, Internal Medicine Specialist, Infectious Diseases Fellow, Universidad Javeriana. Bogotá, Colombia.

2ND, MSc in Clinical Epidemiology. Researcher associated with the Equidad en Salud Group of the Medicine School. Universidad Nacional de Colombia. Hospital Universitario Nacional de Colombia. Bogotá, Colombia.

3MD, General Surgery and Gastroenterology Specialist (CEHYD). Hospital Central de la Policía (HOCEN). Bogotá, Colombia.

4MD, MSc, PhD in Public Health. Leader of the Equidad en Salud Group, Medicine School, Universidad Nacional de Colombia. Hospital Universitario Nacional de Colombia. Bogotá, Colombia.

5MD, Internal Medicine, Gastroenterology, and Hepatology Specialist. Centro de enfermedades hepáticas y digestivas (CEHYD). Bogotá, Colombia.


Abstract

Introduction:

Severe acute respiratory syndrome type 2 coronavirus infection (SARS-CoV-2) is receiving the most attention now. The asymptomatic elevation of transaminases is typical in the liver, and liver involvement varies from 14 % to 78 %. The assessment of liver comorbidities is scarce, with prevalence ranging between 2 % and 11 %.

Aim:

To describe the behavior of a cohort of patients with liver diseases who fell ill with coronavirus disease 2019 (COVID-19).

Materials and methods:

This retrospective observational study analyzed the behavior of a cohort of patients with liver diseases who fell ill with COVID-19.

Results:

543 patients became ill with COVID-19, of which 300 were women (55.3 %). The median age at diagnosis of liver disease was 52 years. The leading causes of liver disease were nonalcoholic steatohepatitis (49.5 %), cholestatic disease (7.7 %), and hepatitis C and B viruses (6.3 %). Alanine aminotransferase (ALT) had a median of 52 U/L (interquartile range [IQR]: 30-98) and aspartate aminotransferase (AST) 32 U/L (IQR: 23-62). Mortality due to viral infection was 5.7 %, with an incidence rate of 2.9 (95 % confidence interval [CI]: 2-4.2).

Conclusions:

It is a retrospective study but, until the preparation of the manuscript, it had been the first cohort in Colombia to describe the behavior of liver diseases in patients who become ill with COVID-19. No statistically significant differences were found between the causes of liver disease that confer a higher risk of mortality; however, having decompensated cirrhosis is the only condition related to mortality.

Keywords: Fatty liver; SARS virus; cirrhosis of the liver; mortality

Resumen

Introducción:

la infección por coronavirus del síndrome respiratorio agudo grave de tipo 2 (SARS-CoV-2) concentra la mayor atención en el momento. En el hígado es frecuente la elevación asintomática de transaminasas y la afectación hepática varía del 14 % al 78 %. La evaluación de las comorbilidades hepáticas es escasa, con prevalencias que oscilan entre el 2 % y el 11 %.

Objetivo:

describir el comportamiento de una cohorte de pacientes con enfermedades hepáticas que presentaron el coronavirus de 2019 (COVID-19).

Materiales y métodos:

estudio observacional retrospectivo que analizó el comportamiento de una cohorte de pacientes con hepatopatías que enfermaron por COVID-19.

Resultados:

543 pacientes padecieron por COVID-19, de los cuales 300 fueron mujeres (55,3 %). La mediana de edad al diagnóstico de la enfermedad hepática fue de 52 años. Las principales causas de las hepatopatías fueron esteatohepatitis no alcohólica (49,5 %), enfermedad colestásica (7,7 %), virus de la hepatitis C y B (6,3 %). La alanina-aminotransferasa (ALT) presentó una mediana de 52 U/L (rango intercuartílico [RIC]: 30-98) y aspartato-aminotransferasa (AST) 32 U/L (RIC: 23-62). La mortalidad por la infección viral fue del 5,7 % con una tasa de incidencia de 2,9 (intervalo de confianza [IC] 95 %: 2-4,2).

Conclusiones:

es un estudio de carácter retrospectivo; sin embargo, hasta la elaboración del manuscrito es la primera cohorte en Colombia en describir el comportamiento de las enfermedades hepáticas en pacientes que enferman de COVID-19. No se encontraron diferencias estadísticamente significativas entre las causas de hepatopatía que confieran un mayor riesgo de mortalidad; sin embargo, tener una descompensación de cirrosis es la única condición que tiene una relación con la mortalidad.

Palabras clave: Hígado graso; virus del SARS; cirrosis hepática; mortalidad

Introduction

Infection by the severe acute respiratory syndrome coronavirus type 2 (SARS-CoV-2) called COVID-19 pandemic infection (from the English novel coronavirus disease 2019) is receiving the most attention now, and liver involvement is not alien to the viral infection. Asymptomatic elevation of transaminases is typical, and liver injury varies from 14% to 78%1-5. Gastrointestinal manifestations such as nausea, vomiting, abdominal pain, diarrhea, loss of appetite, dysgeusia, and liver chemical changes are increasingly being reported, especially in hospitalized patients4,5.

In the meta-analysis by Dorrell et al5, 62 studies were found that reported transaminase alterations with average alanine aminotransferase (ALT) of 34.8 (+/-16.1 U/L) and aspartate aminotransferase (AST) 39.0 U/L (+/-17.3) among all patients with coronavirus disease 2019 (COVID-19), with a weighted average AST:ALT ratio of 1.15 (+/-0.20).

Liver damage may be directly caused by virus-induced cytopathic effects, considering that SARS-CoV-2 binds to the angiotensin-converting enzyme 2 (ACE-2) receptor to enter its target cells6,7. Data from two independent cohorts revealed a significant enrichment of ACE-2 expression in cholangiocytes (59.7% of cells) compared to hepatocytes (2.6% of cells), suggesting that SARS-CoV-2 could bind directly to ACE-2-positive cholangiocytes and produce alterations in liver function8-10.

Among the liver diseases described and associated with severe cases of COVID-19, the main one was chronic hepatitis B infection, with 2.4% of severe cases. AST elevation is observed in approximately 18.2% of non-severe cases and 39.4% of severe cases, and ALT elevation in 19.8% of non-severe cases and 28.1% of severe cases.

Few studies have depicted hepatic manifestations, with one study in Wuhan, China, where the origin of the virus was initially described in a series of 99 patients. A decrease in albumin was observed in 98% of patients. At the same time, serum levels of AST, ALT, and bilirubin were elevated in 35%, 28%, and 18% of patients, respectively11. Similarly, in an analysis of 1,099 patients, elevated AST levels were noted in 18.2% of patients with non-severe disease and 39.4% of patients with severe disease12.

Therefore, considering that the description of the hepatic manifestations of COVID-19 is scarce and that there is no record thereof in Colombia, the present study aims to explain the behavior of a cohort of patients with liver diseases who suffered from COVID-19.

Materials and methods

A retrospective observational study was conducted with a review of medical records that analyzed the behavior of a cohort of patients with liver disease who became ill with COVID-19.

Only patients older than 18 years who were under follow-up for liver disease at the Center for Liver and Digestive Diseases (CEHYD) from March 2020 to June 2021 were included. Pregnant patients and those under 18 years of age were excluded.

Statistical analysis

The variables of interest were compared with a description of the sociodemographic variables through frequency and central tendency measures. The variables with normal distribution were compared using the chi-square test, while the variables with abnormal distribution were analyzed using the Mann-Whitney test. Survival analysis was performed by comparing the variables related to mortality represented in Kaplan-Meier graphs and using the log-rank test. Results were presented as tables or graphs using Stata 13.0.

Results

We reviewed a total of 1,937 medical records of patients under follow-up for liver disease with suspected SARS-CoV-2 infection, confirming the diagnosis by molecular tests (real-time polymerase chain reaction [RT-PCR] or antigens) in 543 patients, of whom 300 were women (55.3%).

The median age at diagnosis of liver disease was 52 years (interquartile range [IQR]: 40-61). The main associated comorbidities were high blood pressure (HBP) (23%), dyslipidemia (20.1%), and obesity (17.6%), and the leading causes of liver disease were, in order, non-alcoholic steatohepatitis (NASH; 49.5%), cholestatic disease (7.7%), hepatitis C and B virus (6.3%), and alcohol (4%), with a significant difference between them. Sociodemographic characteristics are shown in Table 1.

Table 1 Sociodemographic characteristics and laboratory variables in all patients 

Variable Total n = 543 n (%) Women n = 300 (55.3 %) n (%) Men n = 243 (44.7 %) n (%) P-value
Sociodemographic characteristics
- Age at diagnosis Median (IQR) 52 (40-61) 53 (40-61) 51 (39-62) 0.628*
Background
- DM 67 (13.3) 39 (13.8) 28 (12.6) 0.7ç
- Dyslipidemia 103 (20.1) 52 (18.1) 51 (22.6) 0.2ç
- Obesity 90 (17.6) 45 (15.6) 45 (20.0) 0.2ç
- Alcohol use 204 (37.5) 60 (20) 144 (59.2) <0.001+
- HBP 118 (23.0) 66 (23.0) 52 (23.1) 0.976ç
- Coronary heart disease 26 (5.0) 15 (5.2) 11 (4.8) 0.863ç
- BMI Me (IQR) 26.5 (24.29.4) 26 (23-29) 27 (24.9-30) 0.002*
Laboratories (n = 151) Median (IQR)
- Leukocytes Me (IQR) 5950 (5000-7230) 5905 (4762-7157) 6190 (5070-7295) 0.2352*
- Neutrophils 54 (47-60) 54 (48-61) 52 (46-59) 0.0621*
- Lymphocytes 34 (27-39) 33 (28-39) 34 (26-41) 0.2057*
- ESR (mL/h) 7 (3-15) 8 (5-20) 5 (2-8) <0.0001*
- Hb 15 (14-16) 14 (13-15) 16 (15-17) <0.0001*
- HCT 45 (42-48) 43 (41-46) 48 (45-50) <0.0001*
- Platelets 242000 (192 x103-288 X103) 260000 (207 x103-307x103) 218000 (178 x103-262 x 103) <0.0001*
- Glycemia 94 (86-102) 91 (84-100) 96 (89-104) <0.0001*
- Creatinine 0.8 (0.7-1) 0.7 (0.6-0.8) 0.9 (0.8-1.1) <0.0001*
- Total cholesterol 193 (160-224) 196 (166-229) 188 (153-222) 0.0319*
- Triglycerides 143 (104-194) 138 (93-184) 147 (113-204) 0.0106*
- TSH 2.5 (1.5-3.6) 2.5 (1.5- 3.6) 2.4 (1.6-3.7) 0.7767*
Liver function
- AST 35 (23-62) 33 (21-63) 35.5 (26-61) 0.1763*
- ALT 52 (30-98) 49 (23-101) 58 (36-95) 0.0064*
- Alkaline phosphatase 96 (74-136) 101 (77-142) 91 (72-134) 0.0279*
- Total bilirubin 0.7 (0.4-1.1) 0.6 (0.4-1) 0.7 (0.5-1.3) <0.0001*
- Albumin 4.4 (4.1-4.7) 4.4 (4.1-4.6) 4.5 (4.2-4.8) 0.0007*
- AFP 2.5 (1.7-3.9) 2.3 (1.6-3.6) 2.7 (1.7-4.3) 0.0882*
Cause of liver disease <0.001+
- Fatty liver 269 (49.5) 135 (45) 134 (55.1)
- Alcohol 22 (4.1) 3 (1) 19 (7.8)
- Virus 34 (6.3) 19 (6.3) 15 (6.1)
- Cholestatic 42 (7.7) 36 (12) 6 (4.5)
- Mixed (three or more) 14 (2.6) 7 (2.3) 7 (2.8)
- Other 162 (29.8) 100 (33.3) 62 (25.5)

çChi-square. *Mann-Whitney test. +Fisher’s test. AFP: Alpha-fetoprotein; DM: Diabetes mellitus; Hb: Hemoglobin; HCT: Hematocrit; Me: Median; TSH: Thyrotropin; ESR: Erythrocyte sedimentation rate.

One hundred fifty-two patients (27.9%) were diagnosed with cirrhosis with statistically significant differences (p < 0.001), together with coronary heart disease (p < 0.015) for mortality.

The leading cause of cirrhosis was again NASH in 36.8% (n = 42), and 28.2% had a history of decompensation, and the most frequent were ascites (40%), followed by variceal bleeding (20 %).

Transaminases had higher values ​​for ALT, showing a median of 52 U/L (IQR: 30-98), and for AST, there was a slightly elevated value with a median of 32 U/L (IQR: 23-62). Laboratory variables were taken before a diagnosis of SARS-CoV-2 infection.

Despite not having statistically significant differences in mortality, a higher proportion of DM, dyslipidemia, and obesity stands out in patients who survived, as shown in Table 2.

Table 2 Variables related to mortality from COVID-19 in patients with liver disease 

Variable Total n = 543 n (%) Alive n = 512 (94.3) n (%) Deceased n = 31 (5.7) n (%) P-value
Clinical features
- Women 300 (55.3) 283 (55.2) 229 (44.7) 0.962ç
- Diabetes (n = 503) 67 (13.3) 63 (13.3) 4 (12.9) 1+
- Dyslipidemia (n = 512) 103 (20.1) 99 (20.5) 4 (12.9)  
- Obesity (n = 511) 90 (17.6) 87 (18.1) 3 (9.6)  
Alcohol use 204 (37.5) 188(36.7) 16 (51.6) 0.001
- Does not use 302 (59.6) 287 (60.4) 15 (48.3)  
- HBP 118 (23.0) 111 (23.0) 7 (22.5) 0.949ç
- Coronary heart disease 26 (5.0) 21 (4.3) 5 (16.1) 0.015+
- Cirrhosis 152 (100) 74 (100) 78 (100) <0.001ç
Cause of cirrhosis 0.274+
- NASH 42 (36.8) 29 (39.1) 20 (25.6)  
- NASH + alcohol 10 (8.7) 1 (1.3) 16 (20.5)  
- Hepatitis C virus 8 (7.0) 16 (21.6) 5 (6.4)  
- Autoimmune 8 (7.0) 6 (8.1) 1 (1.2)  
- Alcohol 7 (6.1) 1 (1.3) 23 (29.4)  
- Other causes 20 (15.6) 8 (10.8) 12 (8.9)  
Decompensation 0.005+
- Ascites 12 (20.3) 6 (13.6) 6 (40.0)  
- Variceal bleeding 8 (13.5) 5 (11.3) 3 (20.0)  
- Encephalopathy 3 (5.0) 1 (2.2) 2 (13.3)  
- HCC 2 (3.3) 1 (2.2) 1 (6.6)  
- Jaundice 7 (11.8) 6 (13.6) 1 (6.6)  
- Coagulopathy 3 (5.0) 2 (4.5) 1 (6.6)  

çChi square. *Mann-Whitney test. +Fisher’s test. HCC: Hepatocarcinoma.

Mortality from COVID-19 was 5.7% (n = 31), with an incidence rate of 2.9 (95% confidence interval [CI]: 2-4.2) and a median survival of 18 days (IQR: 12-32). The only variable related to liver disease with statistically significant differences in mortality was cirrhosis decompensation (p < 0.005), as shown in Table 2.

In the survival analysis, no statistically significant differences were found between survival curves by sex, cause of HCC, diagnosis or not of cirrhosis, etiology of cirrhosis due to NAFLD, or alcohol use, as shown in Table 3 and Figures 1,2,3,4 y5.

Tabla 3 Survival analysis 

Incidence rate * 100 (95%CI) Median survival (days) Percentile 25% - percentile 75% (days)
Positive diagnosis 2.9 (2 a 4.2) 18 12-32

Figure 1 Survival analysis for the gender variable. Prepared by the authors. 

Figure 2 Survival analysis for the cirrhosis variable. Prepared by the authors 

Figure 3 Survival analysis for the NASH variable. Prepared by the authors 

Figure 4 Survival analysis for the alcohol variable. Prepared by the authors 

Figure 5 Survival analysis for the alcohol-NASH variable. Prepared by the authors 

Discussion

We recognize the weaknesses of the study for being retrospective; however, until the writing of the manuscript, it is the first cohort in Colombia to describe the behavior of liver diseases in patients who become ill with COVID-19.

Similarities to other studies are found in which liver diseases have not posed an increased risk of SARS-CoV-2 infection. The descriptive studies published so far found that only a small number of patients with the condition (approximately 3%) have underlying chronic liver disease, and no statistically significant association between chronic liver disease and severity of COVID-19 or outcomes regarding mortality or severity of infection has been established11,13-15. The preceding is reflected in the incidence rate of 2.9, even considering that this study is based on those patients who already have chronic liver disease. Furthermore, it reveals that mortality in this series is probably related to other factors and in those patients having advanced disease with decompensated cirrhosis from the perspective of liver disease.

No statistically significant differences were found between the causes of liver disease that represent a higher risk of mortality from SARS-CoV-2 infection in this series, contrary to what has been described in other latitudes. It has been shown that chronic diseases such as hepatitis B and C occupy the first places12, even considering non-negligible rates of hepatitis C infection of 7% in the present study.

We ignore the transaminase behavior from the point of view of liver involvement, considering that baseline paraclinical tests are before infection. However, they show a slight elevation of ALT and AST. Other studies5,11,12 show liver enzyme elevations with SARS-CoV-2.

Compared to global reports of patients with liver disease who develop COVID-19, such as SECURE-Cirrhosis and COVID-HEP. Mortality was similar at 13.8% for SECURE-Cirrhosis, but with a difference from COVID-HEP, in which 36.5% of deaths were found among patients with chronic liver disease and liver transplants16,17.

Only one report of a transplanted patient was found, leaving the door open for research in this group of patients, who already have a higher risk of mortality from any cause because they are immunosuppressed patients. Nonetheless, this reinforces the concept of protection with immunization since this group of patients has a lower immunogenic response (approximately 50%), unlike those immunocompetent with responses close to 94%18,19.

As it was a study conducted in an outpatient center, the primary liver disease was NAFLD associated with obesity and dyslipidemia, which until now has been briefly described in a few observational studies20,21. These found that mainly young patients and those with NAFLD have a higher risk of severe disease and a longer viral shedding time. However, fatty liver is frequently associated with other comorbidities such as diabetes or cardiovascular disease, which are also established risk factors for severe COVID-19 and could contribute to worse outcomes in these patients. Thus, there is a need for an adequate diagnosis of NAFLD to adequately define if it represents a cardiovascular risk factor in addition to chronic comorbidities, such as arterial hypertension or diabetes, once again reinforcing the concept of early vaccination in this population deemed a risk group.

Conditions of causality could not be established due to the characteristics of the study. Long-term observations are required to define the impact of liver diseases in severe cases of SARS-CoV-2 illness and determine potential therapeutic interventions in those patients with chronic liver diseases. Until now, there are discordant results as to whether or not they are a factor of more significant mortality from COVID-1922,23.

Conclusion

Despite being a retrospective study, it is probably the first cohort of patients with liver diseases affected by SARS-CoV-2. Similarities and differences with other studies are found, but prospective studies are needed to assess the impact of chronic liver diseases on SARS-CoV-2 infection.

Acknowledgments

We thank our patients for being the subjects of our study and the health staff who have been closely affected by COVID-19.

Referencias

1. Perisetti A, Gajendran M, Mann R, Elhanafi S, Goyal H. COVID-19 extrapulmonary illness - special gastrointestinal and hepatic considerations. Dis Mon. 2020;66(9):101064. https://doi.org/10.1016/j.disamonth.2020.101064Links ]

2. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497-506. https://doi.org/10.1016/S0140-6736(20)30183-5Links ]

3. Jin X, Lian JS, Hu JH, Gao J, Zheng L, Zhang YM, et al. Epidemiological, clinical and virological characteristics of 74 cases of coronavirus-infected disease 2019 (COVID-19) with gastrointestinal symptoms. Gut. 2020;69(6):1002-1009. https://doi.org/10.1136/gutjnl-2020-320926Links ]

4. Fan Z, Chen L, Li J, Cheng X, Yang J, Tian C, et al. Clinical Features of COVID-19-Related Liver Functional Abnormality. Clin Gastroenterol Hepatol. 2020;18(7):1561-1566. https://doi.org/10.1016/j.cgh.2020.04.002Links ]

5. Dorrell RD, Dougherty MK, Barash EL, Lichtig AE, Clayton SB, Jensen ET. Gastrointestinal and hepatic manifestations of COVID-19: A systematic review and meta-analysis. JGH Open. 2020;5(1):107-115. https://doi.org/10.1002/jgh3.12456Links ]

6. Musa S. Hepatic and gastrointestinal involvement in coronavirus disease 2019 (COVID-19): What do we know till now? Arab J Gastroenterol. 2020;21(1):3-8. https://doi.org/10.1016/j.ajg.2020.03.002Links ]

7. Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell. 2020;181(2):271-280.e8. https://doi.org/10.1016/j.cell.2020.02.052Links ]

8. Chai X, Hu L, Zhang Y, Han W, Lu Z, Ke A, et al. Specific ACE2 expression in cholangiocytes may cause liver damage after 2019-nCoV infection. bioRxiv. 2020. https://doi.org/10.1101/2020.02.03.931766Links ]

9. Zhang C, Shi L, Wang FS. Liver injury in COVID-19: management and challenges. Lancet Gastroenterol Hepatol. 2020;5(5):428-430. https://doi.org/10.1016/S2468-1253(20)30057-1Links ]

10. Kim KD, Zhao J, Auh S, Yang X, Du P, Tang H, et al. Adaptive immune cells temper initial innate responses. Nat Med. 2007;13(10):1248-52. https://doi.org/10.1038/nm1633Links ]

11. Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395(10223):507-513.https://doi.org/10.1016/S0140-6736(20)30211-7Links ]

12. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382(18):1708-1720. https://doi.org/10.1056/NEJMoa2002032Links ]

13. Shi H, Han X, Jiang N, Cao Y, Alwalid O, Gu J,et al. Radiological findings from 81 patients with COVID-19 pneumonia in Wuhan, China: a descriptive study. Lancet Infect Dis. 2020;20(4):425-434. https://doi.org/10.1016/S1473-3099(20)30086-4Links ]

14. Zhang JJ, Dong X, Cao YY, Yuan YD, Yang YB, Yan YQ, et al. Clinical characteristics of 140 patients infected with SARS-CoV-2 in Wuhan, China. Allergy. 2020;75(7):1730-1741. https://doi.org/10.1111/all.14238Links ]

15. Arentz M, Yim E, Klaff L, Lokhandwala S, Riedo FX, Chong M, et al. Characteristics and Outcomes of 21 Critically Ill Patients With COVID-19 in Washington State. JAMA. 2020;323(16):1612-1614. https://doi.org/10.1001/jama.2020.4326Links ]

16. Surveillance Epidemiology of Coronavirus (COVID-19) Under Research Exclusion [internet]. Secure Cirrhosis; 2020 [consultado el 5 de abril de 2022]. Disponible en: Disponible en: https://covidcirrhosis.web.unc.edu/wp-content/uploads/sites/22503/2020/03/SECURE-CIRRHOSIS_Case-Report-Form_3-24-20.pdfLinks ]

17. COVID-Hep.net: Coronavirus (COVID-19) in liver disease reporting registry [internet]. COVID-Hep; 2020 [consultado el 5 de abril de 2022]. Disponible en: Disponible en: https://covid-hep.net/Links ]

18. Calleri A, Saracco M, Pittaluga F, Cavallo R, Romagnoli R, Martini S. Seroconversion After Coronavirus Disease 2019 Vaccination in Patients Awaiting Liver Transplantation: Fact or Fancy?. Liver Transpl. 2022;28(2):180-187. https://doi.org/10.1002/lt.26312Links ]

19. Rabinowich L, Grupper A, Baruch R, Ben-Yehoyada M, Halperin T, et al. Low immunogenicity to SARS-CoV-2 vaccination among liver transplant recipients. J Hepatol. 2021;75(2):435-8. https://doi.org/10.1016/j.jhep.2021.04.020Links ]

20. Ji D, Qin E, Xu J, Zhang D, Cheng G, Wang Y, et al. Non-alcoholic fatty liver diseases in patients with COVID-19: A retrospective study. J Hepatol. 2020;73(2):451-453. https://doi.org/10.1016/j.jhep.2020.03.044Links ]

21. Zhou YJ, Zheng KI, Wang XB, Yan HD, Sun QF, Pan KH, et al. Younger patients with MAFLD are at increased risk of severe COVID-19 illness: A multicenter preliminary analysis. J Hepatol. 2020;73(3):719-721. https://doi.org/10.1016/j.jhep.2020.04.027Links ]

22. Ponziani FR, Del Zompo F, Nesci A, Santopaolo F, Ianiro G, Pompili M, et al. Liver involvement is not associated with mortality: results from a large cohort of SARS-CoV-2-positive patients. Aliment Pharmacol Ther. 2020;52(6):1060-1068. https://doi.org/10.1111/apt.15996Links ]

23. Singh S, Khan A. Clinical Characteristics and Outcomes of Coronavirus Disease 2019 Among Patients With Preexisting Liver Disease in the United States: A Multicenter Research Network Study. Gastroenterology. 2020;159(2):768-771.e3. https://doi.org/10.1053/j. gastro.2020.04.064Links ]

Citation: Sánchez-Pardo S, Garzón-Orjuela N, Prieto-Ortiz RG, Eslava-Schmalbach J, Prieto-Ortiz J. The behavior of liver diseases in a cohort of Colombian patients with COVID-19. Rev Colomb Gastroenterol. 2022;37(2):193-200. https://doi.org/10.22516/25007440.853

Sources of funding This study was carried out with the authors’ resources

Received: November 29, 2021; Accepted: April 25, 2022

*Correspondence: Santiago Sánchez-Pardo. sasanchez21@hotmail.com

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License