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Review Article| Volume 364, ISSUE 3, P257-263, September 2022

Hyperlipidemia, COVID-19 and acute pancreatitis: A tale of three entities

  • Author Footnotes
    † Qiuyi Tang and Lin Gao contributed equally to this work.
    Qiuyi Tang
    Footnotes
    † Qiuyi Tang and Lin Gao contributed equally to this work.
    Affiliations
    Medical School, Southeast University, Nanjing, Jiangsu, China

    Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Nanjing, Jiangsu, China
    Search for articles by this author
  • Author Footnotes
    † Qiuyi Tang and Lin Gao contributed equally to this work.
    Lin Gao
    Footnotes
    † Qiuyi Tang and Lin Gao contributed equally to this work.
    Affiliations
    Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Nanjing, Jiangsu, China
    Search for articles by this author
  • Zhihui Tong
    Correspondence
    Corresponding authors at: Weiqin Li, MD, Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Medical School of Southeast University, Nanjing, Jiangsu, China. Zhihui Tong, MD, Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Nanjing, Jiangsu, China
    Affiliations
    Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Nanjing, Jiangsu, China
    Search for articles by this author
  • Weiqin Li
    Correspondence
    Corresponding authors at: Weiqin Li, MD, Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Medical School of Southeast University, Nanjing, Jiangsu, China. Zhihui Tong, MD, Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Nanjing, Jiangsu, China
    Affiliations
    Medical School, Southeast University, Nanjing, Jiangsu, China

    Center of Severe Acute Pancreatitis (CSAP), Department of Intensive Care Unit, Jinling Hospital, Nanjing, Jiangsu, China
    Search for articles by this author
  • Author Footnotes
    † Qiuyi Tang and Lin Gao contributed equally to this work.
Published:April 02, 2022DOI:https://doi.org/10.1016/j.amjms.2022.03.007
Hyperlipidemia, COVID-19 and acute pancreatitis: A tale of three entities
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      Abstract

      Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) caused the ongoing pandemic of coronavirus disease 2019 (COVID-19), which presented as not only respiratory symptoms, but various digestive manifestations including pancreatic injury and acute pancreatitis (AP). The underlying mechanism is still unclear. Hypertriglyceridemia has become one of the leading causes of AP in recent years and hyperlipidemia is highly reported in COVID-19 cases. The current narrative review aimed to explore the associations between AP, COVID-19 and hyperlipidemia. Substantial cases of COVID-19 patients complicated with AP were reported, while the incidence of AP in the COVID-19 population was relatively low. Hyperlipidemia was common in COVID-19 patients with a pooled incidence of 32.98%. Hyperlipidemia could be a mediating factor in the pathogenesis of AP in COVID-19 patients. Further studies are warranted to clarify the relationship among AP, lipid metabolism disorders and COVID-19.

      Key Indexing Terms

      Introduction

      The ongoing pandemic of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection-induced coronavirus disease 2019 (COVID-19) has led to over 164 million infected cases and 3 million deaths worldwide by May 20, 2021. Although most of the infected adults have self-limited disease courses, about 5% of infections may progress to critical illness, featured as severe acute respiratory distress syndrome (ARDS), thrombosis complications, myocardial dysfunction, acute kidney injury, gastrointestinal symptoms, hyperlipidemia, and even multiple organ dysfunction syndrome (MODS).
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      TABLE 1Reported cases of COVID-19 patients with acute pancreatitis.
      AuthorAgeGenderTGBMIOutcome
      Wifi, M. N.72F81mg/dL33.14Discharged
      Tollard, C.32FNormal40.4Died
      Sandhu, H.25FDischarged
      Samies, N. L.15M34.4Discharged
      Samies, N. L.11M251 mg/dL29.5Discharged
      Samies, N. L.16FNormal18.7Discharged
      Narang, K.20FNormal36.1Discharged
      Mohammadi Arbati, M.28M122 mg/dLDischarged
      Maalouf, R. G.62MNormalDischarged
      Bouali, M.60F24Died
      Bineshfar, N.14MDischarged
      Ali, E.53M1.4 mmol/LDied
      AlHarmi, R. A. R.52F3.4 mmol/LDischarged
      Abraham, G.61FDischarged
      Abbas, M.14M5.5 mmol/L21.6Discharged
      Zielecki, P.38MDischarged
      Wang, K.42M3.2 mmol/LDied
      Wang, K.35M3.97 mmol/LDischarged
      Szatmary, P.29M2.7 mmol/L32.9Discharged
      Szatmary, P.41M2.7mmol/L35.8Discharged
      Szatmary, P.42M2.7mmol/L29.7Discharged
      Szatmary, P.47M2.7mmol/L25.7Discharged
      Szatmary, P.53M2.7mmol/L30Discharged
      Simou, E. M.672.40 mmol/L34Died
      Shinohara, T.58MNormalDischarged
      Rabice, S. R.36F44Discharged
      Purayil, N.58MDischarged
      Pinte, L.47MDischarged
      Patnaik, R. N. K.29M84 mg/dLDischarged
      Miao, Y.26FNormalDischarged
      Meyers, M. H.67MNormalDischarged
      Meireles, P. A.36FTC:119 mg/dLDischarged
      Mazrouei, S. S. A.24MDischarged
      Lakshmanan, S.68MDischarged
      Kurihara, Y.55M185 mg/dLDischarged
      Kumaran, N. K.67F27.5Discharged
      Kataria, S.49FDischarged
      Karimzadeh, S.65F80 mg/dLDischarged
      Kandasamy, S.45FDischarged
      Hassani, A. H.78FDied
      Hadi, A.47FNormalDischarged
      Hadi, A.68FNormalDischarged
      Gonzalo-Voltas, A.76FDischarged
      Gadiparthi, C.40M4245 mg/dL38.8Discharged
      Cheung, S.38MNormalDischarged
      Brikman, S.61M3.18mmol/LDischarged
      Bokhari, S.32M150 mg/dLDischarged
      Anand, E. R.59FDischarged
      Alwaeli, H.30M133 mg/dL21.4Discharged
      Alves, A. M.56F209 mg/dLDischarged
      Alloway, B. C.7FDischarged
      Abbreviations: TC, total cholesterol; TG, total glycerides
      Given the considerable presence of hyperlipidemia in COVID-19 cases, we postulated that hyperlipidemia might play a potential role between COVID-19 and AP. Hence, this narrative review aimed to accumulate evidence on the incidence of hyperlipidemia and AP in the COVID-19 population, and demonstrate whether hyperlipidemia acted as a mediating factor in COVID-19 patients combined with AP.

      The correlation between AP and COVID-19

      We used “COVID-19” and “acute pancreatitis” as search terms to retrieve related articles in PubMed database. The results of different studies were controversial. An epidemiological study from Spain including 63,822 COVID-19 patients showed that the incidence of AP in COVID-19 patients was 0.71% compared with 1.59% in the non-COVID-19 population (OR 0.44, 95% CI 0.33–0.60).
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      In another study which included 74,814 COVID-19 patients, 54 patients were complicated with AP (0.72%) and the incidence rate was lower than that in the non-COVID-19 population (1.61%).
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      A case-control emergency department-based analysis of acute pancreatitis in COVID-19: results of the UMC-19-S(6).
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      However, a case-control study that included 112 COVID-19 children and 8047 non-COVID-19 children came to the opposite conclusion, the incidences of AP in two groups were 1.8% and 0.14%, respectively.
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      In addition, another study reported that 1.25% of 398 pediatric COVID-19 patients were complicated with AP.
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      It seems that AP was more prevalent in pediatric COVID-19 patients than in adult patients. It was shown in one study that almost no AP occurred in COVID-19 patients with mild disease courses, while most of AP cases were present in critically ill COVID-19 patients.
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      Association between acute pancreatitis and COVID-19: could pancreatitis be the missing piece of the puzzle about increased mortality rates?.
      J Invest Surg. 2020; : 1-7https://doi.org/10.1080/08941939.2020.1833263
      For AP patients, the coexistence of COVID-19 could lead to a worse prognosis of AP. A prospective multicenter cohort study compared the outcomes of AP patients with or without COVID-19, with the results showing that AP patients infected by SARS-CoV-2 were more likely to develop local complications, persistent organ failure, have prolonged hospital stay, higher 30-day mortality, and require ICU admission.
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      SARS-CoV-2 infection in acute pancreatitis increases disease severity and 30-day mortality: COVID PAN collaborative study.
      Gut. 2021; 70: 1061-1069https://doi.org/10.1136/gutjnl-2020-323364
      A retrospective observational study included 189 AP cases, 32 of them were COVID-19 positive and these patients required more mechanical ventilation and had a longer length of hospital stay (OR=5.65, 3.22, respectively).
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      Prevalence, risk factors, and outcomes of hospitalized patients with coronavirus disease 2019 presenting as acute pancreatitis.
      Gastroenterology. 2020; 159: 2226-2228https://doi.org/10.1053/j.gastro.2020.08.044

      The correlation between hyperlipidemia and COVID-19

      We used “COVID-19” and “hyperlipidemia” as search terms to retrieve related articles in PubMed database. Thirty-four papers were reviewed after screening, which reported the incidence of hyperlipidemia in COVID-19 patients (Table 2).
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      TABLE 2Incidence of hyperlipidemia in Covid-19 patients in different studies.
      AuthorSpecific PopulationTotalHyperlipidemiaRate
      Wu, B.COVID-199822630964.23%
      Wang, D.COVID-19 patients in Fangcang hospital349329.17%
      Tzur Bitan, D.COVID-19 with schizophrenia255391098143.00%
      Spoulou, V.Newborns with COVID-1914642.86%
      Qureshi, A.I.COVID-19 with stroke7709261333.90%
      Pérez-García, C.N.COVID-19 died in hospital32418757.72%
      Pareek, M.COVID-1958622638.57%
      Moftakhar, L.COVID-19 with diabetes16391490.30%
      Karimi, F.COVID-19 with AIDS2524919.44%
      Mirzaei, H.COVID-19164106.10%
      Giannis, D.COVID-19 with venous thrombosis1462114.38%
      Chetboun, M.COVID-19146142328.95%
      Aldhaeefi, M.COVID-1953020438.49%
      Xu, H.COVID-19 with pulmonary embolism1013231.68%
      Wong, K.COVID-19 with pneumothorax752432.00%
      Wei, Z.Y.COVID-19 with myocardial injury400112.75%
      Wang, B.COVID-19 with multiple myeloma583662.07%
      Tee, L.Y.COVID-19 in immigrant workers240114.58%
      Tan, W.Y.T.COVID-1971715621.76%
      Shady, A.COVID-19 admitted in community hospital37110227.49%
      Rameez, F.COVID-19 with stroke11981.82%
      Piazza, G.COVID-19111431928.64%
      Palaiodimos, L.COVID-192009246.00%
      Nimkar, A.COVID-19 with AKI32711434.86%
      Newton, S.COVID-1999122422.60%
      Nakanishi, H.COVID-19601321.67%
      Mori, S.COVID-1945817.78%
      Kenes, M.T.COVID-19 with propofol infusion27933.33%
      He, S.COVID-194204510.71%
      Gómez Antúnez, M.COVID-19 with COPD10385407139.20%
      Fernandes, N.D.COVID-19371540.54%
      Ebert, T.J.COVID-19955355.79%
      Dashti, H.T.COVID-194140153036.96%
      Best, J.H.COVID-19347156616.31%
      Miguel León SanzARDS-COVID-19 receiving parental nutrition873236.78%
      Abbreviations: AKI, acute kidney injury; ARDS, acute respiratory distress syndrome; COPD, chronic obstructive pulmonary disease.
      Hyperlipidemia was commonly presented in critically ill COVID-19 patients and the potential causes for it could be: hemophagocytic lymphohistiocytosis, medication and acute liver injury.
      • Thomas C.M.
      • Vicent M.
      • Moore S.
      • Ali F.
      • Wooten L.
      • Louzon P.R.
      Treatment of severe hypertriglyceridemia with insulin infusions in severe COVID-19: a case series.
      J Pharm Pract. 2021; 8971900211010473https://doi.org/10.1177/08971900211010473
      For instance, some studies suggested that ARDS patients with COVID-19 experienced a higher rate of propofol-associated hypertriglyceridemia than non-COVID-19 induced ARDS patients, even after adjusting for propofol administration doses.
      • Kenes M.T.
      • McSparron J.I.
      • Marshall V.D.
      • Renius K.
      • Hyzy R.C.
      Propofol-associated hypertriglyceridemia in coronavirus disease 2019 versus noncoronavirus disease 2019 acute respiratory distress syndrome.
      Crit Care Explor. 2020; 2: e0303https://doi.org/10.1097/cce.0000000000000303
      It was reported that the incidence of propofol-associated hypertriglyceridemia was 18%-45% in the non-COVID-19 population, but could be as high as 56.6% in COVID-19 patients.
      • Kovacevic M.P.
      • Dube K.M.
      • Lupi K.E.
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      • DeGrado J.R.
      Evaluation of hypertriglyceridemia in critically Ill patients with coronavirus disease 2019 receiving propofol.
      Crit Care Explor. 2021; 3: e0330https://doi.org/10.1097/cce.0000000000000330
      Besides, there was a case report presenting 2 cases of tocilizumab-induced hypertriglyceridemia during the treatment of COVID-19, and one of them developed into AP in the later disease course.
      It is unclear whether hyperlipidemia leads to deterioration of disease course and prognosis of COVID-19 patients. Previous research has showed that patients older than 50 were prone to have hyperlipidemia,
      • Palaiodimos L.
      • Kokkinidis D.G.
      • Li W.
      • et al.
      Severe obesity, increasing age and male sex are independently associated with worse in-hospital outcomes, and higher in-hospital mortality, in a cohort of patients with COVID-19 in the Bronx, New York.
      Metabolism. 2020; 108154262https://doi.org/10.1016/j.metabol.2020.154262
      which led to an increased risk of hospital admission (OR=1.8)
      • Newton S.
      • Zollinger B.
      • Freeman J.
      • et al.
      Factors associated with clinical severity in emergency department patients presenting with symptomatic SARS-CoV-2 infection.
      medRxiv. 2020; https://doi.org/10.1101/2020.12.08.20246017
      and disease deterioration (OR=2.15).
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      Association of overlapped and un-overlapped comorbidities with COVID-19 severity and treatment outcomes: a retrospective cohort study from nine provinces in China.
      Biomed Environ Sci. 2020; 33: 893-905https://doi.org/10.3967/bes2020.123
      In addition, previous reviews suggested that patients with hypercholesterolemia had increased risk for COVID-19 and the related complications.
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      Familial hypercholesterolaemia and COVID-19: a two-hit scenario for endothelial dysfunction amenable to treatment.
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      Possible mechanisms of cholesterol elevation aggravating COVID-19.
      Int J Med Sci. 2021; 18: 3533-3543https://doi.org/10.7150/ijms.62021
      However, one study compared between two cohorts, namely COVID-19 patients discharged alive and those that died, and multiple regression analysis showed that hyperlipidemia had a protective effect on reducing the likelihood of death (OR=0.75).
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      Identifying patients at greatest risk of mortality due to COVID-19: a New England Perspective.
      West J Emerg Med. 2020; 21: 785-789https://doi.org/10.5811/westjem.2020.6.47957
      Another study carried out cluster analysis in a large cohort of 12,066 COVID-19 patients, and the results showed that hyperlipidemia had no significant effects on COVID-19 prognosis.
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      Predicting clinical outcome with phenotypic clusters in COVID-19 pneumonia: an analysis of 12,066 Hospitalized patients from the Spanish registry SEMI-COVID-19.
      J Clin Med. 2020; 9https://doi.org/10.3390/jcm9113488

      The correlation between acute pancreatitis and hyperlipidemia

      In the general population

      It is widely acknowledged that gallstones and alcohol intake are two major causes of AP followed by hypertriglyceridemia (HTG) and others. HTG has been a major cause of AP over the last decade and accounts for about 10% of total AP worldwide.
      • Carr R.A.
      • Rejowski B.J.
      • Cote G.A.
      • Pitt H.A.
      • Zyromski N.J.
      Systematic review of hypertriglyceridemia-induced acute pancreatitis: a more virulent etiology?.
      Pancreatol Off J Int Assoc Pancreatol(IAP) [et al]. 2016; 16: 469-476https://doi.org/10.1016/j.pan.2016.02.011
      ,
      • Valdivielso P.
      • Ramírez-Bueno A.
      • Ewald N.
      Current knowledge of hypertriglyceridemic pancreatitis.
      Eur J Int Med. 2014; 25: 689-694https://doi.org/10.1016/j.ejim.2014.08.008
      Especially in East Asia, HTG has become the second leading cause of total AP and the incidence of HTG-AP could reach up to 15–25%.
      • Huang Y.X.
      • Jia L.
      • Jiang S.M.
      • Wang S.B.
      • Li M.X.
      • Yang B.H.
      Incidence and clinical features of hyperlipidemic acute pancreatitis from Guangdong, China: a retrospective multicenter study.
      Pancreas. 2014; 43: 548-552https://doi.org/10.1097/mpa.0000000000000069
      , 
      • Yin G.
      • Cang X.
      • Yu G.
      • et al.
      Different clinical presentations of hyperlipidemic acute pancreatitis: a retrospective study.
      Pancreas. 2015; 44: 1105-1110https://doi.org/10.1097/mpa.0000000000000403
      , 
      • Zhu Y.
      • Pan X.
      • Zeng H.
      • et al.
      A study on the etiology, severity, and mortality of 3260 patients with acute pancreatitis according to the revised atlanta classification in jiangxi, china over an 8-year period.
      Pancreas. 2017; 46: 504-509https://doi.org/10.1097/mpa.0000000000000776
      HTG is one of the predominant subtypes of hyperlipidemia, and it has been reported to deteriorate disease severity, progression, and outcomes of AP. A meta-analysis of 15 studies compared 1,564 HTG-AP patients to 5,721 AP cases with other etiologies, the results showed that the occurrence of renal failure, respiratory failure, shock, and mortality was significantly higher in HTG-AP patients.
      • Wang Q.
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      • Liu C.
      Elevated serum triglycerides in the prognostic assessment of acute pancreatitis: a systematic review and meta-analysis of observational studies.
      J Clin Gastroenterol. 2017; 51: 586-593https://doi.org/10.1097/mcg.0000000000000846
      A retrospective study classified AP patients into a normal triglyceride group or mild HTG (<200 mg/dL) group, a moderate HTG (200-749 mg/dL) group, and a severe HTG (>750 mg/dL) group, and demonstrated that higher serum triglyceride level was independently associated with a more severe disease course of AP.
      • Pascual I.
      • Sanahuja A.
      • García N.
      • et al.
      Association of elevated serum triglyceride levels with a more severe course of acute pancreatitis: cohort analysis of 1457 patients.
      Pancreatology. 2019; 19: 623-629https://doi.org/10.1016/j.pan.2019.06.006
      Previous studies suggested that the potential mechanisms of the deteriorating effects of HTG on AP may lie in the accumulation of free fatty acid and thereafter, activation of inflammatory response in the pancreas.
      • Yang A.L.
      • McNabb-Baltar J.
      Hypertriglyceridemia and acute pancreatitis.
      Pancreatology. 2020; 20: 795-800https://doi.org/10.1016/j.pan.2020.06.005
      Free fatty acid has been reported to cause the increase in the levels of inflammatory mediators, such as TNF-alpha, interleukin-6, interleukin-10, which might strengthen the systemic inflammatory response and local pancreatic injury. Moreover, in vitro experiments also presented that free fatty acid had direct cytotoxic effects on acinar cells and vascular endothelial cells.

      In the COVID-19 population

      When it comes to the causes of AP in the COVID-19 population, some studies suggested that SARS-CoV-2 could cause pancreatic injury and AP directly. Angiotensin-converting enzyme 2 (ACE2) is widely expressed in human vascular endothelium, respiratory endothelium, and other cell types, which is thought to be a primary mechanism of SARS-CoV-2 entry and infection.
      • Amraei R.
      • Rahimi N.
      COVID-19, renin-angiotensin system and endothelial dysfunction.
      Cells. 2020; 9https://doi.org/10.3390/cells9071652
      An inflamed/injured endothelium promotes neutrophilia and systemic inflammatory cascades, leading to involvement of multi-organs. A review concerning the role of endothelium in COVID-19 suggested that endothelial cells were a crucial link between SARS-CoV-2 and host immune responses and thus may serve many roles in determining the disease severity and mortality in COVID-19.
      • Kaur S.
      • Tripathi D.M.
      • Yadav A.
      The enigma of endothelium in COVID-19.
      Front Physiol. 2020; 11: 989https://doi.org/10.3389/fphys.2020.00989
      Receptor proteins of SARS-CoV-2 including ACE2 were also highly expressed in the epithelial cells of gastrointestinal tract, so do the pancreatic duct epithelium, pancreatic acinar cell, and islet cell. SARS-CoV-2 could infect the gastrointestinal epithelial cells through the gastrointestinal tract and spread into the pancreas. This hypothesis was supported by a few studies, one study showed the existence of SARS-CoV-2 in gastrointestinal tract epithelium, and RNA of the virus could be detected by real-time reverse transcriptase polymerase chain reaction from feces.
      • Xiao F.
      • Tang M.
      • Zheng X.
      • Liu Y.
      • Li X.
      • Shan H.
      Evidence for gastrointestinal infection of SARS-CoV-2.
      Gastroenterology. 2020; 158: 1831-1833https://doi.org/10.1053/j.gastro.2020.02.055
      Furthermore, SARS-CoV-2 was also isolated from pancreatic pseudocyst tissue.
      • Schepis T.
      • Larghi A.
      • Papa A.
      • et al.
      SARS-CoV2 RNA detection in a pancreatic pseudocyst sample.
      Pancreatology. 2020; 20: 1011-1012https://doi.org/10.1016/j.pan.2020.05.016
      However, this hypothesis was not validated by robust evidence and it is unable to explain the relatively low incidence of AP in COVID-19 patient in some large epidemiological researches.
      • Miró Ò.
      • Llorens P.
      • Jiménez S.
      • et al.
      Frequency of five unusual presentations in patients with COVID-19: results of the UMC-19-S(1).
      Epidemiol Infect. 2020; 148: e189https://doi.org/10.1017/s0950268820001910
      ,
      • Miró Ò.
      • Llorens P.
      • Jiménez S.
      • et al.
      A case-control emergency department-based analysis of acute pancreatitis in COVID-19: results of the UMC-19-S(6).
      J Hepatobiliary Pancreat Sci. 2021; 28: 953-966https://doi.org/10.1002/jhbp.873
      Taking into consideration of the high incidence of hyperlipidemia in COVID-19 patients, we hypothesized that hyperlipidemia could also be a mediator in the pathogenesis of pancreatic injury and AP in COVID-19 patients besides direct virus infection. The detrimental effects of HTG mentioned above should also exist in COVID-19 patients combined with AP. To support the hypothesis, we wondered whether the incidence of AP was higher in patients with hyperlipidemia compared to patients without hyperlipidemia in the COVID-19 population. However, no well-designed study has yet to report the related data, we thereby retrospectively collected the information of all case reports of AP with COVID-19 (Table 1). From the retrospective analysis, the levels of total triglycerides and total cholesterol increased slightly in COVID-19 patients complicated with AP, which suggested that hyperlipidemia may be the reason for the occurrence of AP.

      Concluding remarks

      • (1)
        A small portion of COVID-19 patients presented with acute pancreatitis, but the underlying mechanism was still unknown.
      • (2)
        The occurrence of hyperlipidemia was high in the COVID-19 population.
      • (3)
        In general population, hyperlipidemia has become one of the major causes of AP. And in the COVID-19 population, presuming the detrimental effects of hyperlipidemia still exist, hyperlipidemia could also be a mediating factor in the pathogenesis of pancreatic injury and AP.
      • (4)
        Further studies are warranted to clarify the relationship between AP, hyperlipidemia, and COVID-19.

      Source of funding

      This study was supported by National Natural Science Foundation of China (No. 82070669).

      CRediT authorship contribution statement

      Qiuyi Tang: Conceptualization, Visualization, Data curation, Formal analysis, Writing – review & editing. Lin Gao: Conceptualization, Visualization, Writing – original draft, Writing – review & editing. Zhihui Tong: Writing – review & editing. Weiqin Li: Writing – review & editing.

      Declaration of Competing Interest

      The authors declare that there is no conflict of interest regarding the research, authorship, and/or publication of this paper.

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      Article info

      Publication history

      Published online: April 02, 2022
      Accepted: March 30, 2022
      Received: September 20, 2021

      Identification

      DOI: https://doi.org/10.1016/j.amjms.2022.03.007

      Copyright

      © 2022 Southern Society for Clinical Investigation. Published by Elsevier Inc. All rights reserved.

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