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Vinutha M, Sharma UR, Swamy G, Rohini S, Vada S, Janandri S, Haribabu T, Taj N, Gayathri SV, Jyotsna SK, Mudagal MP. COVID-19-related liver injury: Mechanisms, diagnosis, management; its impact on pre-existing conditions, cancer and liver transplant: A comprehensive review. Life Sci 2024; 356:123022. [PMID: 39214285 DOI: 10.1016/j.lfs.2024.123022] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/19/2024] [Revised: 08/20/2024] [Accepted: 08/25/2024] [Indexed: 09/04/2024]
Abstract
AIMS This review explores the mechanisms, diagnostic approaches, and management strategies for COVID-19-induced liver injury, with a focus on its impact on patients with pre-existing liver conditions, liver cancer, and those undergoing liver transplantation. MATERIALS AND METHODS A comprehensive literature review included studies on clinical manifestations of liver injury due to COVID-19. Key areas examined were direct viral effects, drug-induced liver injury, cytokine storms, and impacts on individuals with chronic liver diseases, liver transplants, and the role of vaccination. Data were collected from clinical trials, observational studies, case reports, and review literature. KEY FINDINGS COVID-19 can cause a spectrum of liver injuries, from mild enzyme elevations to severe hepatic dysfunction. Injury mechanisms include direct viral invasion, immune response alterations, drug toxicity, and hypoxia-reperfusion injury. Patients with chronic liver conditions (such as alcohol-related liver disease, nonalcoholic fatty liver disease, cirrhosis, and hepatocellular carcinoma) face increased risks of severe outcomes. The pandemic has worsened pre-existing liver conditions, disrupted cancer treatments, and complicated liver transplantation. Vaccination remains crucial for reducing severe disease, particularly in chronic liver patients and transplant recipients. Telemedicine has been beneficial in managing patients and reducing cross-infection risks. SIGNIFICANCE This review discusses the importance of improved diagnostic methods and management strategies for liver injury caused by COVID-19. It emphasizes the need for close monitoring and customized treatment for high-risk groups, advocating for future research to explore long-term effects, novel therapies, and evidence-based approaches to improve liver health during and after the pandemic.
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Affiliation(s)
- M Vinutha
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - Uday Raj Sharma
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India.
| | - Gurubasvaraja Swamy
- Department of Pharmaceutical Chemistry, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - S Rohini
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - Surendra Vada
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - Suresh Janandri
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - T Haribabu
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - Nageena Taj
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - S V Gayathri
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - S K Jyotsna
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
| | - Manjunatha P Mudagal
- Department of Pharmacology, Acharya & BM Reddy College of Pharmacy, Acharya Dr. Sarvepalli Radhakrishna Road, Achit Nagar (Post), Soldevanahalli, Bengaluru, India
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Antar SA, Ashour NA, Hamouda AO, Noreddin AM, Al-Karmalawy AA. Recent advances in COVID-19-induced liver injury: causes, diagnosis, and management. Inflammopharmacology 2024:10.1007/s10787-024-01535-7. [PMID: 39126569 DOI: 10.1007/s10787-024-01535-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/14/2023] [Accepted: 03/29/2024] [Indexed: 08/12/2024]
Abstract
Since the start of the pandemic, considerable advancements have been made in our understanding of the effects of SARS-CoV-2 infection and the associated COVID-19 on the hepatic system. There is a broad range of clinical symptoms for COVID-19. It affects multiple systems and has a dominant lung illness depending on complications. The progression of COVID-19 in people with pre-existing chronic liver disease (CLD) has also been studied in large multinational groups. Notably, SARS-CoV-2 infection is associated with a higher risk of hepatic decompensation and death in patients with cirrhosis. In this review, the source, composition, mechanisms, transmission characteristics, clinical characteristics, therapy, and prevention of SARS-CoV-2 were clarified and discussed, as well as the evolution and variations of the virus. This review briefly discusses the causes and effects of SARS-CoV-2 infection in patients with CLD. As part of COVID-19, In addition, we assess the potential of liver biochemistry as a diagnostic tool examine the data on direct viral infection of liver cells, and investigate potential pathways driving SARS-CoV-2-related liver damage. Finally, we explore how the pandemic has had a significant impact on patient behaviors and hepatology services, which may increase the prevalence and severity of liver disease in the future. The topics encompassed in this review encompass the intricate relationships between SARS-CoV-2, liver health, and broader health management strategies, providing valuable insights for both current clinical practice and future research directions.
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Affiliation(s)
- Samar A Antar
- Center for Vascular and Heart Research, Fralin Biomedical Research Institute, Virginia Tech, Roanoke, VA, 24016, USA
- Department of Pharmacology, Faculty of Pharmacy, Horus University-Egypt, New Damietta, 34518, Egypt
| | - Nada A Ashour
- Department of Pharmacology and Toxicology, Faculty of Pharmacy, Tanta University, Tanta, 31527, Egypt
| | - Amir O Hamouda
- Department of Biochemistry, Faculty of Pharmacy, Horus University-Egypt, New Damietta, 34518, Egypt
| | - Ayman M Noreddin
- Department of Clinical Pharmacy, Faculty of Pharmacy, Ahram Canadian University, 6Th of October City, Giza, 12566, Egypt
- Department of Internal Medicine, School of Medicine, University of California -Irvine, Irvine, USA
| | - Ahmed A Al-Karmalawy
- Department of Pharmaceutical Chemistry, Faculty of Pharmacy, Horus University-Egypt, New Damietta, New Damietta, 34518, Egypt.
- Pharmaceutical Chemistry Department, Faculty of Pharmacy, Ahram Canadian University, 6Th of October City, Giza, 12566, Egypt.
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Januszewski M, Ziuzia-Januszewska L, Kudan M, Pluta K, Klapaczyński J, Wierzba W, Maciejewski T, Jakimiuk AA, Jakimiuk AJ. Liver damage profile in COVID-19 pregnant patients. Cell Commun Signal 2024; 22:5. [PMID: 38166966 PMCID: PMC10762912 DOI: 10.1186/s12964-023-01285-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/11/2023] [Accepted: 08/19/2023] [Indexed: 01/05/2024] Open
Abstract
INTRODUCTION SARS-CoV-2 unsparingly impacts all areas of medicine. Pregnant women are particularly affected by the pandemic and COVID-19 related liver damage seems to be another threat to maternal and fetal health. The aim of this study is to define liver damage profile including bile acids serum levels in COVID-19 pregnant patients and to determine predictors of disease aggravation and poor obstetrics outcomes. METHODS This study has been carried out in the Obstetrics and Gynecology Department, at the National Medical Institute in Warsaw, Poland between 01.02.2021 and 01.11.2022 The study cohort comprises 148 pregnant patients with COVID-19 and 102 pregnant controls who has been tested negative for SARS-CoV-2. RESULTS COVID-19 pregnant patients presented liver involvement at admission in 41,9%. Hepatotoxic damage accounted for 27 (19.85%), cholestatic type was diagnosed in 11 (8.09%) and mixed type of liver injury was presented in 19 (13.97%) of patients. Higher serum levels of AST, ALT, GGT, total bilirubin and bile acids as well as mixed type of liver injury at admission were correlated with severe form of an illness. AST and ALT above upper reference limit as well as hepatotoxic type of liver damage predisposed pregnant patients with COVID-19 to poor obstetrics outcomes. CONCLUSION Hepatic damage in pregnant women with COVID-19 is a common, mild, transaminase-dominant, or mixed type of injury, and often correlates with elevated inflammatory markers. SARS-CoV-2 test should be performed as a part of differential diagnosis in elevated liver function tests. Although bile acids serum levels were commonly elevated they seems to be clinically irrelevant in terms of pregnancy outcomes. Video Abstract.
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Affiliation(s)
- Marcin Januszewski
- Department of Obstetrics and Gynecology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Laura Ziuzia-Januszewska
- Department of Otolaryngology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Michal Kudan
- Department of Obstetrics and Gynecology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Kamil Pluta
- Department of Obstetrics and Gynecology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Jakub Klapaczyński
- Department of Hepatology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Waldemar Wierzba
- Department of Obstetrics and Gynecology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Tomasz Maciejewski
- Department of Obstetrics and Gynecology, Institute of Mother and Child, Kasprzaka 17a, 01-211, Warsaw, Poland
| | - Alicja A Jakimiuk
- Department of Plastic Surgery, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland
| | - Artur J Jakimiuk
- Department of Obstetrics and Gynecology, National Medical Institute of the Ministry of Interior and Administration, Wołoska 137, 02-507, Warsaw, Poland.
- Center for Reproductive Health, Institute of Mother and Child, Kasprzaka 17a, 01-211, Warsaw, Poland.
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Aktiz Bıçak E, Oğlak SC. Clinical characterisation and management outcome of obstetric patients following intensive care unit admission for COVID-19 pneumonia. J OBSTET GYNAECOL 2023; 43:2218915. [PMID: 37289641 DOI: 10.1080/01443615.2023.2218915] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2022] [Accepted: 05/03/2023] [Indexed: 06/10/2023]
Abstract
This study aims to examine the clinical characteristics and mortality-related factors of obstetric patients, who were taken to the intensive care unit due to Coronavirus Disease 2019 (COVID-19). This study included 31 patients in the peripartum period with COVID-19 pneumonia, followed up in the intensive care unit (ICU) from March 2020 to December 2020. Symptoms, laboratory values, intensive care unit duration of stay, complications, the requirement of non-invasive and invasive mechanical ventilation, and mortality were recorded. The mean age was 30.7 ± 6.2 years and the mean gestational age was 31.1 ± 6.4 weeks. Among the patients, 25.8% had a fever, 87.1% had a cough, 96.8% had dyspnoea and 77.4% had tachypnoea. Seventeen patients (54.8%) had mild, 6 (19.4%) had moderate and 8 (25.8%) had severe pulmonary involvement on computed tomography. Sixteen (51.6%) patients required high-frequency oscillatory ventilation, 6 (19.3%) patients required continuous positive airway pressure, and 5 (16.1%) patients required invasive mechanical ventilation. Sepsis complicated by septic shock and multiorgan failure occurred in 4 patients and all of them died. The ICU duration of stay was 4.9 ± 4.3 days. We have found that older maternal age, obesity, high LDH, AST, ALT, ferritin, leukocyte, CRP, and procalcitonin values, and severe lung involvement were mortality-related factors.Impact statementWhat is already known on this subject? Pregnant women are in the high-risk group for Covid-19 disease and its complications. Although most pregnant women are asymptomatic, severe infection-related hypoxia can cause serious foetal and maternal problems.What do the results of this study add? When we examined the literature, we found that the number of studies on pregnant women with severe Covid-19 infection was limited. For this reason, with our study results, we aim to contribute to the literature by determining the biochemical parameters and patient-related factors associated with severe infection and mortality in pregnant patients with severe Covid-19 infection.What are the implications of these findings for clinical practice and/or further research? With our study results, predisposing factors for the development of severe Covid-19 infection in the pregnant patient population and biochemical parameters that are early indicators of severe infection were determined. In this way, pregnant women in the high-risk group can be followed closely and the necessary treatments can be started quickly so disease-related complications and mortality can be reduced.
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Affiliation(s)
- Esra Aktiz Bıçak
- Department of Anesthesiology and Reanimation, Health Sciences University, Gazi Yaşargil Training and Research Hospital, Diyarbakır, Turkey
| | - Süleyman Cemil Oğlak
- Department of Obstetrics and Gynaecology, Health Sciences University, Gazi Yaşargil Training and Research Hospital, Diyarbakır, Turkey
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Gu Y, Xing Y, Zhu J, Zeng L, Hu X. Post-Coronavirus Disease 2019 (COVID-19) Liver Injury in Pregnant Women: A Retrospective Cohort Study. CLIN EXP OBSTET GYN 2023; 50. [DOI: 10.31083/j.ceog5011248] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/03/2025]
Abstract
Background: Coronavirus Disease 2019 (COVID-19) has risen as a global threat to public health and can cause both respiratory and multisystemic diseases in humans. This study aimed to describe the incidence of abnormal liver function tests (LFTs) in post-COVID-19 pregnant women, and to explore characteristics of pregnant women with abnormal LFTs. Methods: This retrospective cohort study comprised 155 pregnant patients who experienced COVID-19, alongside 76 uninfected pregnant women as a control group. All participants were randomly selected from the Obstetrics outpatient clinic at the Affiliated Maternity and Child Health Care Hospital of Nantong University between December 25 2022 and January 31 2023. Demographic data and laboratory data were collected, and results were statistically analyzed. Results: Of the 155 pregnant women who had experienced COVID-19, 63 (40.6%) showed abnormally raised liver enzymes. In the control group, 9 (11.8%) cases had abnormal LFTs. Differences between the two groups were statistically significant (p < 0.05). Of the 63 post-COVID-19 patients with abnormal LFTs, the median serum level of alanine transaminase (ALT), aspartate transaminase (AST), and alkaline phosphatase (ALP) was: 175 U/L (range, 51–352 U/L), 113 U/L (range, 42–329 U/L), and 123 U/L (range, 35–250 U/L). Median total biliary acid (TBA) was 18.1 µmol/L (range, 1.8–33.5 µmol/L). The patients who developed abnormal LFTs did so within 7–14 days after contracting COVID-19, with a median of 10 days. Subsequently, their liver function returned to normal within 4–26 days, with a median of 12 days. The univariate analysis on factors that may affect abnormal LFTs revealed a statistically significant difference in gestational age and body mass index (BMI) (p < 0.001). Logistic regression analysis found that gestational age (odds ratio (OR): 1.095 [1.021–1.174]) and BMI (OR: 1.169 [1.059–1.289]) remained a significant independent risk factors for liver injury (p < 0.05). Conclusions: Pregnant women are at an increased risk of liver injury after contracting COVID-19. Moreover, with the increase of gestational age and BMI, the risk of liver injury increases.
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Affiliation(s)
- Yannan Gu
- Department of Obstetrics and Gynecology, Affiliated Maternity and Child Health Care Hospital of Nantong University, 226000 Nantong, Jiangsu, China
| | - Ying Xing
- Department of Obstetrics and Gynecology, Affiliated Maternity and Child Health Care Hospital of Nantong University, 226000 Nantong, Jiangsu, China
| | - Jing Zhu
- Department of Obstetrics and Gynecology, Affiliated Maternity and Child Health Care Hospital of Nantong University, 226000 Nantong, Jiangsu, China
| | - Li Zeng
- Department of Obstetrics and Gynecology, Affiliated Maternity and Child Health Care Hospital of Nantong University, 226000 Nantong, Jiangsu, China
| | - Xiaohong Hu
- Department of Obstetrics and Gynecology, Affiliated Maternity and Child Health Care Hospital of Nantong University, 226000 Nantong, Jiangsu, China
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Shi Y, Wang M, Wu L, Li X, Liao Z. COVID-19 associated liver injury: An updated review on the mechanisms and management of risk groups. LIVER RESEARCH 2023; 7:207-215. [PMID: 39958382 PMCID: PMC11792068 DOI: 10.1016/j.livres.2023.07.001] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/13/2022] [Revised: 06/11/2023] [Accepted: 07/09/2023] [Indexed: 09/02/2023]
Abstract
Coronavirus disease 2019 (COVID-19) has been associated with various liver injury cases worldwide. To date, the prevalence, mechanism, clinical manifestations, diagnosis, and outcomes of COVID-19-induced liver injury in various at-risk groups are not well defined. Liver injury may arise in the prevention and treatment of COVID-19 from direct causes such as viral infection and indirect causes such as systemic inflammation, hypoxic changes, and drugs that exacerbate any pre-existing liver disease. Studies have found that patients with underlying liver disease are at higher risk of COVID-19-induced liver injury. Certain condition of cardiopulmonary and metabolic diseases and vulnerable stages in lifespan may also involve in the development of COVID-19-induced liver injury. This review summarized studies of COVID-19-induced liver injury in different at-risk groups regarding their clinical characteristics, parameters, and correlations of the severity with these indicators and signs as well as potential treatment suggestions, to increase attention to physiological and pathological conditions and continue liver function monitoring as they can help in strengthening early supportive treatment and reducing the incidence of adverse outcomes.
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Affiliation(s)
- Yue Shi
- Second Clinical Medical College, Beijing University of Chinese Medicine, Beijing, China
- Graduate School, Beijing University of Chinese Medicine, Beijing, China
| | - Mina Wang
- Graduate School, Beijing University of Chinese Medicine, Beijing, China
- Department of Acupuncture and Moxibustion, Beijing Hospital of Traditional Chinese Medicine, Capital Medical University, Beijing Key Laboratory of Acupuncture Neuromodulation, Beijing, China
| | - Liqun Wu
- Second Clinical Medical College, Beijing University of Chinese Medicine, Beijing, China
| | - Xuexin Li
- Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Solna, Sweden
| | - Zehuan Liao
- School of Biological Sciences, Nanyang Technological University, Singapore, Singapore
- Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institutet, Stockholm, Sweden
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Roshanshad R, Roshanshad A, Fereidooni R, Hosseini-Bensenjan M. COVID-19 and liver injury: Pathophysiology, risk factors, outcome and management in special populations. World J Hepatol 2023; 15:441-459. [PMID: 37206656 PMCID: PMC10190688 DOI: 10.4254/wjh.v15.i4.441] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/28/2022] [Revised: 02/05/2023] [Accepted: 03/20/2023] [Indexed: 04/20/2023] Open
Abstract
The coronavirus disease 2019 (COVID-19) caused by severe acute respiratory syndrome coronavirus-2 is an ongoing health concern. In addition to affecting the respiratory system, COVID-19 can potentially damage other systems in the body, leading to extra-pulmonary manifestations. Hepatic manifestations are among the common consequences of COVID-19. Although the precise mechanism of liver injury is still questionable, several mechanisms have been hypothesized, including direct viral effect, cytokine storm, hypoxic-ischemic injury, hypoxia-reperfusion injury, ferroptosis, and hepatotoxic medications. Risk factors of COVID-19-induced liver injury include severe COVID-19 infection, male gender, advanced age, obesity, and underlying diseases. The presentations of liver involvement comprise abnormalities in liver enzymes and radiologic findings, which can be utilized to predict the prognosis. Increased gamma-glutamyltransferase, aspartate aminotransferase, and alanine aminotransferase levels with hypoalbuminemia can indicate severe liver injury and anticipate the need for intensive care units’ hospitalization. In imaging, a lower liver-to-spleen ratio and liver computed tomography attenuation may indicate a more severe illness. Furthermore, chronic liver disease patients are at a higher risk for severe disease and death from COVID-19. Nonalcoholic fatty liver disease had the highest risk of advanced COVID-19 disease and death, followed by metabolic-associated fatty liver disease and cirrhosis. In addition to COVID-19-induced liver injury, the pandemic has also altered the epidemiology and pattern of some hepatic diseases, such as alcoholic liver disease and hepatitis B. Therefore, it warrants special vigilance and awareness by healthcare professionals to screen and treat COVID-19-associated liver injury accordingly.
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Affiliation(s)
- Romina Roshanshad
- Student Research Committee, School of Medicine, Shiraz University of Medical Sciences, Shiraz 7184731443, Iran
| | | | - Reza Fereidooni
- Health Policy Research Center, Institute of Health, Shiraz University of Medical Sciences, Shiraz 7134814336, Iran
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Sekulovski M, Bogdanova-Petrova S, Peshevska-Sekulovska M, Velikova T, Georgiev T. COVID-19 related liver injuries in pregnancy. World J Clin Cases 2023; 11:1918-1929. [PMID: 36998958 PMCID: PMC10044960 DOI: 10.12998/wjcc.v11.i9.1918] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/22/2022] [Revised: 01/17/2023] [Accepted: 02/21/2023] [Indexed: 03/16/2023] Open
Abstract
While severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) quickly spread across the globe, our understanding of its pathogenic mechanisms evolved. Importantly, coronavirus disease 2019 (COVID-19) is now considered a syndromic multisystem inflammatory disease involving not only the respiratory system but also the cardiovascular, excretory, nervous, musculoskeletal, and gastrointestinal systems. Moreover, a membrane-bound form of angiotensin-converting enzyme 2, the entry receptor for SARS-CoV-2, is expressed on the surface of cholangiocytes and hepatocytes, suggesting the potential of COVID-19 to involve the liver. With the widespread distribution of SARS-CoV-2 throughout the population, infection during pregnancy is no longer a rare occurrence; however, little is known about the course of hepatic injuries and related outcomes in pregnant SARS-CoV-2-positive women. Thus, the understudied topic of COVID-related liver disease during pregnancy poses a great challenge for the consulting gynecologist and hepatologist. In this review, we aim to describe and summarize potential liver injuries in pregnant women with COVID-19.
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Affiliation(s)
- Metodija Sekulovski
- Department of Anesthesiology and Intensive Care, University Hospital Lozenetz, Sofia 1407, Bulgaria
- Medical Faculty, Sofia University St. Kliment Ohridski, Sofia 1407, Bulgaria
| | - Simona Bogdanova-Petrova
- First Department of Internal Medicine, Medical University-Varna, Varna 9010, Bulgaria
- Clinic of Rheumatology, University Hospital “St. Marina”, Varna 9010, Bulgaria
| | - Monika Peshevska-Sekulovska
- Medical Faculty, Sofia University St. Kliment Ohridski, Sofia 1407, Bulgaria
- Department of Gastroenterology, University Hospital Lozenetz, Sofia 1407, Bulgaria
| | - Tsvetelina Velikova
- Medical Faculty, Sofia University St. Kliment Ohridski, Sofia 1407, Bulgaria
- Department of Clinical Immunology, University Hospital Lozenetz, Sofia 1407, Bulgaria
| | - Tsvetoslav Georgiev
- First Department of Internal Medicine, Medical University-Varna, Varna 9010, Bulgaria
- Clinic of Rheumatology, University Hospital “St. Marina”, Varna 9010, Bulgaria
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Bhusal T, Banjade P, Surani S, Sharma M. The Spectrum of COVID-19-Induced Liver Injury in Various Age and Risk Groups. Cureus 2023; 15:e36349. [PMID: 37082482 PMCID: PMC10110415 DOI: 10.7759/cureus.36349] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 03/19/2023] [Indexed: 03/21/2023] Open
Abstract
Coronavirus disease 2019 (COVID-19) has inflicted significant mortality and morbidity worldwide since the virus was first detected towards the end of 2019. Though it primarily affects the respiratory system, COVID-19 has been shown to have a multisystem effect. There have been literature on liver injury associated with COVID-19 in general but liver injury specific to certain risk and age groups needs to be looked into. Thus, we aim to discuss the liver injury associated with COVID-19 in various age and risk groups and revisit pathophysiology, biochemical markers and their correlation with outcomes, and current management recommendations.
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Göklü MR, Oğlak SC, Gedik Özköse Z, Tunç Ş, Bolluk G. The course of infection with the Delta variant of COVID-19 in pregnancy: analysis of clinical, laboratory, and neonatal outcomes. J Turk Ger Gynecol Assoc 2023; 24:33-41. [PMID: 36583294 PMCID: PMC10019012 DOI: 10.4274/jtgga.galenos.2022.2022-6-8] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/31/2022] Open
Abstract
Objective This study aimed to examine the effects of infection with the Delta variant of coronavirus disease-2019 (COVID-19) on the clinical course, laboratory parameters, and neonatal outcome in pregnant women. Material and Methods A total of 96 pregnant women who tested positive for the Delta variant of severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) causing COVID-19 were retrospectively examined. The pregnant women were divided into three groups: Asymptomatic; non-severe; and severe. Age, obstetric history, symptoms and findings, blood tests, medication and vaccination history, clinical course, and perinatal outcome of pregnant women were analyzed. Results Pregnant women who tested positive for the Delta variant of SARS-CoV-2 had an intensive care unit (ICU) admission rate of 9.4% and a mortality rate of 5.2%. Pregnant women in the severe disease group had significantly higher rates of preterm birth and cesarean section compared with the non-severe and asymptomatic group. Pregnant women in the severe group had high C-reactive protein (CRP) levels at the time of admission. White blood cell count (WBC) and procalcitonin levels were increased in clinical follow-up in women in the severe group. Conclusion The Delta variant of SARS-CoV-2 was found to increase mortality rates in pregnant women compared to pre-Delta variants of COVID-19. In pregnant women infected with the Delta variant, advanced gestational age at diagnosis, high CRP, WBC, and procalcitonin levels were significantly correlated with poor prognosis. Pregnant women infected with the Delta variant and with severe COVID-19 had an increased risk for preterm delivery and cesarean section. Although newborns of women with severe disease were found to have significantly higher rates of ICU admission, there was no significant difference in neonatal mortality rates. We recommend close monitoring of CRP, WBC, and procalcitonin levels, in addition to symptoms, in pregnant women infected with the Delta variant of SARS-CoV-2 and diagnosed in the third trimester.
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Affiliation(s)
- Mehmet Rıfat Göklü
- Clinic of Obstetrics and Gynecology, University of Health Sciences Turkey, Gazi Yaşargil Training and Research Hospital, Diyarbakır, Turkey
| | - Süleyman Cemil Oğlak
- Clinic of Obstetrics and Gynecology, University of Health Sciences Turkey, Gazi Yaşargil Training and Research Hospital, Diyarbakır, Turkey
| | - Zeynep Gedik Özköse
- Clinic of Perinatology, University of Health Sciences Turkey, Kanuni Sultan Süleyman Training and Research Hospital, İstanbul, Turkey
| | - Şeyhmus Tunç
- Clinic of Obstetrics and Gynecology, University of Health Sciences Turkey, Gazi Yaşargil Training and Research Hospital, Diyarbakır, Turkey
| | - Gökhan Bolluk
- Clinic of Perinatology, University of Health Sciences Turkey, Başakşehir Çam and Sakura City Hospital, İstanbul, Turkey
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Chourasia P, Maringanti BS, Edwards-Fligner M, Gangu K, Bobba A, Sheikh AB, Shekhar R. Paxlovid (Nirmatrelvir and Ritonavir) Use in Pregnant and Lactating Woman: Current Evidence and Practice Guidelines-A Scoping Review. Vaccines (Basel) 2023; 11:107. [PMID: 36679952 PMCID: PMC9866309 DOI: 10.3390/vaccines11010107] [Citation(s) in RCA: 8] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/01/2022] [Revised: 12/16/2022] [Accepted: 12/23/2022] [Indexed: 01/04/2023] Open
Abstract
COVID-19 virus, since the detection of the first case in Wuhan in 2019, has caused a worldwide pandemic with significant human, economic and social costs. Fortunately, several vaccines and treatments, both IV and oral, are currently approved against the COVID-19 virus. Paxlovid is an oral treatment option for patients with mild-to-moderate disease, and it effectively reduces disease severity in high-risk patients. Paxlovid is an oral antiviral that consists of a combination of nirmatrelvir and ritonavi. As an oral medication suitable for outpatient treatment, it reduces the cost, hospitalization and mortality associated with COVID-19 infection. The pregnant population is a high-risk category for COVID-19 disease. Given their exclusion in clinical trials, there is limited data regarding Paxlovid use in pregnant and lactating women. Indirect evidence from ritonavir use as part of HAART therapy in the pregnant and lactating population with HIV has shown no significant teratogenicity. Moreover, animal studies on the use of nirmatrelvir do not suggest teratogenicity. This article summarizes the available data on ritonavir and nirmatrelvir use during pregnancy and in ongoing clinical trials. We also review the recommendations of major societies worldwide regarding Paxlovid use in pregnant and breastfeeding patients.
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Affiliation(s)
- Prabal Chourasia
- Department of Hospital Medicine, Mary Washington Hospital, Fredericksburg, VA 22401, USA
| | - Babu Sriram Maringanti
- Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87106, USA
| | - Morgan Edwards-Fligner
- Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87106, USA
| | - Karthik Gangu
- Department of Internal Medicine, University of Kansas Medical Center, Kansas City, KS 66160, USA
| | - Aniesh Bobba
- Department of Medicine, John H Stronger Hospital, Cook County, Chicago, IL 60612, USA
| | - Abu Baker Sheikh
- Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87106, USA
| | - Rahul Shekhar
- Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87106, USA
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12
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Cooper KM, Colletta A, Asirwatham AM, Moore Simas TA, Devuni D. COVID-19 associated liver injury: A general review with special consideration of pregnancy and obstetric outcomes. World J Gastroenterol 2022; 28:6017-6033. [PMID: 36405386 PMCID: PMC9669825 DOI: 10.3748/wjg.v28.i42.6017] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/12/2022] [Revised: 10/24/2022] [Accepted: 10/27/2022] [Indexed: 11/15/2022] Open
Abstract
Liver injury is an increasingly recognized extra-pulmonary manifestation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. Coronavirus disease 2019 (COVID-19) associated liver injury (COVALI) is a clinical syndrome encompassing all patients with biochemical liver injury identified in the setting of SARS-CoV-2 infection. Despite profound clinical implications, its pathophysiology is poorly understood. Unfortunately, most information on COVALI is derived from the general population and may not be applicable to individuals under-represented in research, including pregnant individuals. This manuscript reviews: Clinical features of COVALI, leading theories of COVALI, and existing literature on COVALI during pregnancy, a topic not widely explored in the literature. Ultimately, we synthesized data from the general and perinatal populations that demonstrates COVALI to be a hepatocellular transaminitis that is likely induced by systemic inflammation and that is strongly associated with disease severity and poorer clinical outcome, and offered perspective on approaching transaminitis in the potentially COVID-19 positive patient in the obstetric setting.
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Affiliation(s)
- Katherine M. Cooper
- Department of Medicine, University of Massachusetts Chan Medical School, Worcester, MA 01605, United States
| | - Alessandro Colletta
- Department of Medicine, University of Massachusetts Chan Medical School, Worcester, MA 01605, United States
| | - Alison M. Asirwatham
- Department of Obstetrics and Gynecology, University of Massachusetts Chan Medical School, Worcester, MA 01605, United States
| | - Tiffany A. Moore Simas
- Department of Obstetrics and Gynecology, University of Massachusetts Chan Medical School, Worcester, MA 01605, United States
- Departments of Pediatrics, Psychiatry, and Population & Quantitative Health Sciences, University of Massachusetts Chan Medical School, Worcester, MA 01605, United States
| | - Deepika Devuni
- Department of Medicine, University of Massachusetts Chan Medical School, Worcester, MA 01605, United States
- Division of Gastroenterology and Hepatology, University of Massachusetts Chan Medical School, Worcester, MA 1605, United States
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13
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Payus AO, Mohd Noh M, Azizan N, Muthukaruppan Chettiar R. SARS-CoV-2-induced liver injury: A review article on the high-risk populations, manifestations, mechanisms, pathological changes, management, and outcomes. World J Gastroenterol 2022; 28:5723-5730. [PMID: 36338886 PMCID: PMC9627422 DOI: 10.3748/wjg.v28.i39.5723] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/16/2022] [Revised: 08/24/2022] [Accepted: 10/10/2022] [Indexed: 02/06/2023] Open
Abstract
The novel coronavirus disease 2019 is an infection caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and was declared a global pandemic with more than 500 million reported cases and more than 6 million deaths worldwide to date. Although it has transitioned into the endemic phase in many countries, the mortality rate and overall prognosis of the disease are still abysmal and need further improvement. There has been evidence that shows the significance of SARS-CoV-2-related liver injury. Here, we review the literature on the various spectrum of SARS-CoV-2 infection-induced liver injury and the possible mechanisms of damage to the hepatobiliary system. This review aimed to illustrate the latest understanding regarding SARS-CoV-2-induced liver injury including the high-risk populations, the characteristic clinical manifestations, the possible pathogenic mechanism, the pathological changes, the current suggestions for clinical treatment for various spectrum of populations, and the prognosis of the condition. In conclusion, SARS-CoV-2 patients with a liver injury warrant close monitoring as it is associated with the more severe and poorer outcome of the infection.
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Affiliation(s)
- Alvin Oliver Payus
- Department of Medicine, Faculty of Medicine and Health Sciences, Universiti Malaysia Sabah, Kota Kinabalu 88400, Sabah, Malaysia
| | - Malehah Mohd Noh
- Department of Medicine, Faculty of Medicine and Health Sciences, Universiti Malaysia Sabah, Kota Kinabalu 88400, Sabah, Malaysia
| | - Nornazirah Azizan
- Department of Pathobiology and Medical Diagnostic, Faculty of Medicine and Health Sciences, Universiti Malaysia Sabah, Kota Kinabalu 88400, Malaysia
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Djusad S, Irwinda R, Harzif AK, Surya R, Wibowo N, Saroyo YB, Adjie JMS. Determining laboratory parameters in pregnant women with severe COVID-19. SAGE Open Med 2022; 10:20503121221132168. [PMID: 36277440 PMCID: PMC9579820 DOI: 10.1177/20503121221132168] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/03/2022] [Accepted: 09/23/2022] [Indexed: 11/11/2022] Open
Abstract
Objective Coronavirus disease causes a wide spectrum of clinical picture in pregnant women. There are still a few studies concerning laboratory parameters to differentiate the severity of coronavirus disease-19 in pregnant patients. This article aims to identify the cut-off on laboratory parameters between pregnant women with asymptomatic/mild/moderate and severe/critical coronavirus disease-19 illness. Methods All coronavirus disease-19 pregnant women coming to Dr. Cipto Mangunkusumo hospital between January and August 2021 were recruited into this cross-sectional study. All data extracted from medical records were classified into demographic characteristics and laboratory parameters. We defined demographic characteristics as age, parity, systolic, and diastolic blood pressure, heart rate, temperature, respiratory rate, and oxygen saturation. Laboratory parameters measured in this study consisted of complete blood count, renal function test including urea, creatinine, liver function test including aspartate transferase, alanine transferase, infection marker test including procalcitonin, C-reactive protein, interleukin-6, cycle threshold values, ferritin, coagulation test including d-dimer, fibrinogen, random blood glucose, albumin, electrolytes. Data analysis was performed using SPSS statistics. Results There were 159 cases assessed in this study consisting of 130 (81.8%) patients with asymptomatic/mild/moderate illness and 29 (18.2%) patients with severe/critical illness of coronavirus disease-19. Of 28 laboratory parameters, 12 of them were significant statistically; thus, it resulted to make a cut-off using receiver operating characteristic curve and show relative risk, and 95% confidence interval. In multivariate analysis that aspartate transferase, D-dimer, and albumin were laboratory parameters impacted to the severity of coronavirus disease-19 in pregnant women. The area under receiver operating characteristic curve was 0.834 (95% CI 0.736-0.932). Conclusion Of all laboratory parameters, urea, aspartate transferase, alanine transferase, procalcitonin, C-reactive protein, lactate dehydrogenase (LDH), ferritin, D-dimer, random blood glucose, cycle threshold values, albumin, and chloride differs between asymptomatic/mild/moderate, and severe/critical illness coronavirus disease-19 in pregnant women; aspartate transferase, D-dimer, and albumin were laboratory parameters impacted the most to the severity of coronavirus disease-19 in pregnant women.
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Affiliation(s)
- Suskhan Djusad
- Suskhan Djusad, Department of Obstetrics
and Gynecology, Dr. Cipto Mangunkusumo Hospital, Jakarta/Faculty of Medicine,
Universitas Indonesia, Jakarta, DKI Jakarta, Indonesia.
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COVID-19 tanısı konmuş gebe kadınlarda proinflamatuar IL-6 ve antiinflamatuar IL-10 sitokinlerinin etkileri. ANADOLU KLINIĞI TIP BILIMLERI DERGISI 2022. [DOI: 10.21673/anadoluklin.1129488] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022] Open
Abstract
ÖZ
Amaç: Çalışmamızda COVID-19 pozitif gebelerde serum interlökin-6 ve interlökin-10 düzeyleri ile hastalığın seyri arasındaki ilişkinin araştırılması amaçlandı.
Yöntemler: Çalışmamızda 28 üçüncü trimester COVID-19 pozitif gebe ve 30 üçüncü trimester sağlıklı gebede serum IL-6 ve IL-10 düzeyleri ölçüldü. COVID-19 pozitif vakalar, taşıyıcı veya hasta olarak sınıflandırıldı. Çalışma grubundaki gebelerden 13'ü asemptomatik iken veya hafif hastalık nedeniyle takip edilirken; 7'si yoğun bakımda (YBÜ) olmak üzere toplam 15 hamile kadın hastaneye kaldırılarak tedavi altına alındı. COVID-19 pozitif gebe kadınların IL-6 ve IL-10 testleri ilk uygulama sırasında çalışıldı.
Bulgular: COVID-19'lu 7 (%25) hastanın yoğun bakım ünitesine kabul edilmesi gerekti. COVID-19 negatif gebelerde IL-6 düzeyi, COVID-19 taşıyıcısı ve hasta gebelere göre anlamlı derecede düşük bulundu (p=0,01). COVID-19 negatif olan gebelerde IL-10 düzeyi, COVID-19 taşıyıcısı olan gebelere (p=0,002) ve hastalara (p=0,002) göre anlamlı derecede yüksek bulundu.
Sonuç: Şüpheli veya doğrulanmış bir COVID-19 teşhisi ile başvuran hamile kadınlarda olumsuz sonuç riskini en aza indirmek için IL-6 ve IL-10 sitokin düzeylerinin yakından izlenmesi önerilir. Bu şekilde hamile kadınlarda orta-hafif COVID-19'u şiddetli COVID-19'dan ayırt etmek mümkün olabilir.
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Choudhary A, Singh V, Bharadwaj M. Maternal and Neonatal Outcomes in Pregnant Women With SARS-CoV-2 Infection Complicated by Hepatic Dysfunction. Cureus 2022; 14:e25347. [PMID: 35761912 PMCID: PMC9233295 DOI: 10.7759/cureus.25347] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 05/26/2022] [Indexed: 01/09/2023] Open
Abstract
Background and objective The coronavirus disease 2019 (COVID-19) pandemic has caused one of the most devastating healthcare crises in recent times and presented many diagnostic challenges and uncertainties. COVID-19 complicated by acute hepatic dysfunction is a well-described phenomenon, but its impact on maternal and perinatal outcomes is not well documented. In this study, we aimed to evaluate the maternal and neonatal outcomes in pregnant women with COVID-19 complicated by liver dysfunction and compare those with pregnant women with COVID-19 and normal liver function. Methodology This was a retrospective observational cohort study conducted at the Tata Main Hospital, Jamshedpur, a tertiary care hospital in eastern India. All COVID-19-positive pregnant women (n=249) admitted to the hospital from May 15, 2020, to August 15, 2021, were included in this study. Retrospective data collection was done using the medical records of these COVID-19-positive pregnant women and included the baseline characteristics, past medical history, obstetric history, clinical presentation, laboratory results, management modalities, and maternal and neonatal outcomes. Of note, 107 women were found to have acute liver function abnormality on admission and 142 women had normal liver function tests (LFTs). Pregnant women with normal LFTs were classified as group one and those with deranged LFTs as group two. Characteristics such as age, period of gestation, symptoms, associated comorbidities, laboratory results, management, and outcomes were compared across both groups. Results Out of the total 249 pregnant women with COVID-19 admitted during the study period, 42.97% (n=107) women had laboratory findings consistent with liver dysfunction and 142 women (57.03%) had a normal liver function. Significantly higher levels of lactate dehydrogenase (LDH), C-reactive protein (CRP), neutrophil-lymphocyte ratio (NLR), alanine transaminase (ALT), aspartate aminotransferase (AST), and total bilirubin levels were seen in pregnant women with hepatic dysfunction when compared to those with normal liver function. Among the 249 patients, the majority were asymptomatic or had mild disease, 12 women had moderate disease, and six women had severe COVID-19. All women with severe COVID-19 had deranged LFTs. There was no statistical difference in terms of obstetric management between pregnant patients with and without liver dysfunction. Out of the 107 women with deranged liver function, 18 women had a preterm birth, four had intrauterine fetal death, and one had neonatal death. Complications such as postpartum hemorrhage, the need for blood transfusions, sepsis and multiorgan failure, and mortality were more commonly seen in the group of pregnant women with hepatic dysfunction associated with COVID-19. Conclusion COVID-19 in pregnancy may cause deranged LFTs in these women. Pregnant women with COVID-19 complicated by liver dysfunction have been reported to have worse inflammation, higher disease severity, and more morbidity and mortality when compared to those without liver dysfunction. They are also at a higher risk of complications such as postpartum hemorrhage, the need for blood transfusion, sepsis, and multiorgan dysfunction.
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Tofan-Scutaru L, Tcaciuc E, Turcan S. Pregnancy and COVID-19 - liver damage. Med Pharm Rep 2021; 94:S22-S33. [PMID: 38912402 PMCID: PMC11188027 DOI: 10.15386/mpr-2514] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 06/25/2024] Open
Abstract
This review examines information from systematic reviews and meta-analyses, research studies, and case reports to present current knowledge about liver damage in pregnant patients having Covid-19 during pregnancy. Problems with diagnosis and differential diagnosis are examined in the context of the need to rule out other causes of liver dysfunction, including pregnancy-related liver disease. In this paper we give an overview of COVID-19 liver problems during pregnancy. Mechanisms of liver involvement in COVID-19 infection are being examined. An overview of the assessment of abnormal liver biological syndromes in pregnant patients is provided. Differential diagnostic algorithms for primary liver damage established in a pregnant woman in the context of the Covid-19 pandemic are presented. Challenges in diagnosis and etiology assessment methods and customized management options are described. The management of pregnant women with hepatic dysfunction onset on the Covid-19 background and subsequently aggravated is discussed. The importance of anticoagulant therapy as an essential measure of symptomatic management of Covid-19 in pregnant women is emphasized, as both pregnancy and COVID-19 are thrombogenic. Hypercoagulability appears to adversely affect the pregnant women liver with Covid-19 and post Covid-19 and anticoagulant therapy has benefits in the management of liver damage associated with Covid-19. The COVID-19 liver problems in a 33-year-old woman who was not vaccinated for Covid-19, without a history of chronic liver disease, was tested positive for Covid-19 at 33 weeks of gestation is discussed. The report of the diagnostics, differential diagnosis, and management questions in the context of liver dysfunction manifested by a significant increase in alanine aminotransferase cytolysis syndrome. The positive effect of anticoagulant therapy in resolving cytolytic syndrome is emphasized. The good maternal and perinatal result is also mentioned.
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Affiliation(s)
- Liudmila Tofan-Scutaru
- Department of Internal Medicine, Discipline of Gastroenterology, Nicolae Testemitanu State University of Medicine and Pharmacy, Chisinau, Moldova
| | - Eugen Tcaciuc
- Department of Internal Medicine, Discipline of Gastroenterology, Nicolae Testemitanu State University of Medicine and Pharmacy, Chisinau, Moldova
| | - Svetlana Turcan
- Department of Internal Medicine, Discipline of Gastroenterology, Nicolae Testemitanu State University of Medicine and Pharmacy, Chisinau, Moldova
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