key: cord-0786989-lfztwnzo
authors: Hartl, Lukas; Semmler, Georg; Hofer, Benedikt Silvester; Schirwani, Nawa; Jachs, Mathias; Simbrunner, Benedikt; Bauer, David Josef Maria; Binter, Teresa; Pomej, Katharina; Pinter, Matthias; Trauner, Michael; Mandorfer, Mattias; Reiberger, Thomas; Scheiner, Bernhard
title: COVID‐19‐related downscaling of in‐hospital liver care decreased patient satisfaction and increased liver‐related mortality
date: 2021-05-18
journal: Hepatol Commun
DOI: 10.1002/hep4.1758
sha: 70d77927c93a32f6ce67e6fdfe3c80638b476bd9
doc_id: 786989
cord_uid: lfztwnzo

BACKGROUND&AIMS: The COVID‐19 pandemic necessitated down‐scaling of in‐hospital care to prohibit the spread of severe acute respiratory syndrome‐coronavirus‐2(SARS‐CoV‐2). We (i)assessed patient perceptions on quality of care by tele‐survey(cohort 1) and written questionnaire(cohort 2) and (ii)analyzed trends in elective and non‐elective admissions prior to (12/2019‐02/2020) and during (03/2020‐05/2020) the COVID‐19 pandemic in Austria. METHODS: Two‐hundred seventy‐nine outpatients were recruited into cohort 1 and 138 patients into cohort 2. All admissions from 12/2019 to 05/2020 to the Division of Gastroenterology/Hepatology at the Vienna General Hospital were analyzed. RESULTS: Thirty‐two point six percent (n=91/279) of cohort 1 and 72.5%(n=95/131) of cohort 2 had tele‐medical contact, while 59.5%(n=166/279)and 68.2%(n=90/132) had face‐to‐face visits. 24.1%(n=32/133) needed acute medical help during healthcare restrictions, however, 57.3%(n=51/89) reported that contacting their physician during COVID‐19 was difficult or impossible. Patient‐reported satisfaction with treatment decreased significantly during restrictions in cohort 1 (visual analog scale[VAS] 0‐10:9.0±1.6 to8.6±2.2;p<0.001) and non‐significantly in cohort 2 (VAS0‐10:8.9±1.6 to8.7±2.1;p=0.182). Despite fewer hospital admissions during COVID‐19, the proportion of non‐elective admissions (+6.3%) and ICU‐admissions (+6.7%) increased. Cirrhotic patients with non‐elective admissions during COVID‐19 had significantly higher MELD (25.5[14.2]vs.17.0[IQR:8.8]; p=0.003) and ΔMELD(difference to last MELD;3.9±6.3vs.8.7±6.4;p=0.008), required immediate intensive care more frequently (26.7%vs.5.6%;p=0.034) and had significantly increased 30‐day liver‐related mortality (30.0%vs.8.3%;p=0.028). CONCLUSIONS: The COVID‐19 pandemic impacts on quality of liver care as evident from decreased patient satisfaction, hospitalization of sicker ACLD patients and increased liver‐related mortality. Strategies for improved tele‐medical liver care and preemptive treatment of cirrhosis‐related complications are needed to counteract the COVID‐19‐associated restrictions of in‐hospital care.

Conclusions: The COVID-19 pandemic impacts on quality of liver care as evident from decreased patient satisfaction, hospitalization of sicker ACLD patients and increased liver-related mortality. Strategies for improved tele-medical liver care and preemptive treatment of cirrhosis-related complications are needed to counteract the COVID-19associated restrictions of in-hospital care.

The COVID-19 pandemic caused by the rapid spread of severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) represents a substantial threat for personal and public health (1) . SARS-CoV-2 infection may cause severe illness and death due to disease manifestations in the respiratory, neuronal, hepatic and intestinal systems (2) (3) (4) (5) .

Limiting the spread of SARS-CoV-2 is currently a major public health goal. On the one hand, this goal is globally pursued by physical distancing, protective equipment (6), banning of large gatherings and travel restrictions (7) . On the other hand, restrictions of healthcare contacts in order to minimize the risks of infection by reducing face-to-face visits whenever possible has become common clinical practice (8) . Additionally, reallocation of healthcare resources to respiratory care and intensive care units was especially needed in the beginning of the pandemic in order to ensure sufficient availability of healthcare resources to patients with COVID-19 (9) .

As a consequence of these modifications of healthcare allocations, the management of non-COVID-19 patients with chronic diseases, such as liver disease, was affected. To guide treatment, international societies rapidly published consensus statements on the management of patients with liver disease during COVID-19 (8, 10) . These recommendations emphasize the need for continuation of guideline-compliant treatment.

Additionally, the EASL-ESCMID position paper and AASLD expert panel consensus statement recommend decreasing face-to-face visits by, for example, postponing visits to specialized centers (8) or delaying surveillance visits for hepatocellular carcinoma (HCC) and screening for gastroesophageal varices (8, 10) . Furthermore, these guidelines recommend sending follow-up prescriptions by mail based on routine laboratory testing performed in local laboratories rather than within the centers to further reduce personal contacts. Additionally, the number of patients evaluated for liver transplantation (LT)

should be limited whenever possible (8, 10) . In this context, telemedicine, i.e. contacting patients via telephone or video-calls, has emerged as an essential alternative for personal visits and represents an opportunity to limit personal contacts, but still ensure sufficient follow-up of patients with liver disease (11) . These telemedicine strategies were also encouraged by international consensus statements (8, 10) .

This article is protected by copyright. All rights reserved Despite these ongoing efforts to ensure medical care of patients with liver disease, it is most likely that the COVID-19 pandemic will have a negative impact on the quality of care potentially resulting in an increased rate of emergency decompensations, increased rates of acute-on-chronic liver failure (ACLF), delayed HCC diagnoses, increased LT waitlist morbidity, as well as increased liver-related mortality (12, 13) . In this context, it has already been shown that COVID-19-related healthcare restrictions had a significant negative short-term impact on LT, as for example organ availability significantly decreased in Italy (14) and the LT program was temporarily suspended by many transplant centers in the United States (15 

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In order to evaluate patient perceptions on COVID-19-associated healthcare restrictions, we performed a tele-survey in study cohort 1 (advanced chronic liver disease [ACLD] patients and patients after LT), distributed a specifically designed written questionnaire in study cohort 2 (non-ACLD patients, ACLD patients and patients after LT), and finally assessed trends in non-elective and elective admissions of patients with liver disease (cohort 3).

Cohort 1 included all patients with ACLD or after LT attending regular visits at the Hepatology clinic of the Vienna General Hospital prior to COVID-19-related healthcare restrictions, defined as at least two visits between January 2019 and February 2020. 

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The strategy for liver-disease specific medical care during COVID-19-associated healthcare restrictions consisted of active contacting of patients and offering telemedicine as replacements for cancelled personal visits. Moreover, information concerning COVID-19 and liver disease was provided at the departmental website and by the Austrian society of gastroenterology and hepatology online and via patient advocacy groups. In the context of the tele-survey, patients were also scheduled for future visits, if requested or necessary.

A tele-survey designed with 11 liver-care related questions was conducted in cohort 1 

In patients admitted to the inpatient ward, as well as the intensive care unit, the type of admission (elective/non-elective), underlying liver disease (non-ACLD, ACLD, HCC, LT)

as well as the incidence of (non-)liver-related death during hospitalization were evaluated

This article is protected by copyright. All rights reserved by chart review. Liver-related death was defined as death attributed to underlying liver 

In total, 459 patients with ACLD or a history of LT with regular visits to the Hepatology clinic were considered for the tele-medical survey. Of these, 32(7.0%) patients died during COVID-19-related healthcare restrictions and could therefore not be contacted.

Additionally, no valid contact data was available for 9(2.0%) patients. When comparing cohort 1 patients, who were reached versus those, who could not be contacted, the groups did not differ in sex, age, etiology of ACLD, MELD score,

proportion of decompensated ACLD, HCC, or history of LT ( 

Results of the surveys -ability to contact treating physician ( Table- 2)

The Patient perceptions on tele-medicine ( 

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This article is protected by copyright. All rights reserved p=0.003) and mean CLIF-C AD score (prior:54.0±11.7 vs. during:61.5±11.5points;

p=0.011). Importantly, differences in MELD and CLIF-C AD scores compared to values at the last routine visit were significantly higher during COVID-19 than before [ΔMELD 

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In this study, we present important patient perceptions on liver disease management during COVID-19-associated restriction of in-hospital care. We analyzed data obtained from two large cohorts of patients with liver disease answering a tele-survey (n=279) and a specifically designed questionnaire (n=138 patients). In addition, we collected critical Continuous, state-of-the-art care by specialists is imperative for liver disease patients, as appropriate care improves quality of life, delays complications and likely extends survival (21) (22) (23) (24) (25) (26) (27) . This need for ongoing professional care is exceedingly problematic in the context of the COVID-19 pandemic, since ACLD (28) (29) (30) and LT patients (31, 32) are possibly more susceptible for severe COVID-19. Thus, liver disease-specific care must be maintained at the best possible level, while at the same time minimizing personal contact, in order to protect potentially vulnerable patients and limit the spread of the virus (8, 10).

Tele-medicine is an attractive means for achieving this and tele-medical contacts have been massively expanded throughout the course of COVID-19-related restrictions of healthcare (11, 12) . This could be seen in cohort 2 of our study (72.5% with tele-medical contact), but also in cohort 1, in which 40.8% of patients with cancelled clinical visits had tele-medical contact with their treating physician. Furthermore, the majority of tele-survey patients expressed their openness to tele-medical contact in the future, underscoring the acceptance of these measures (11, (33) (34) (35) . Nevertheless, tele-medicine may come with significant obstacles for specific patient groups like older or socially underprivileged patients and indeed, patients ≥60years of age tended to be more skeptical towards tele-

This article is protected by copyright. All rights reserved medical visits. Consistently, many liver disease patients also expressed their strong desire for personal contact with their treating physician.

Overall, the level of satisfaction with liver disease management was high both prior to and during COVID-19, despite many cancelled visits in the outpatient and/or inpatient clinic. Nevertheless, satisfaction with medical care did decrease during COVID-19-related restrictions, most notably among ACLD patients. ACLD patients also had significantly During COVID-19 related health care restrictions, we observed a relative 20.2% increase in non-electively admitted ACLD patients paralleled by a 21.1% increase of immediate ICU admissions due to liver disease. Importantly, non-electively admitted ACLD patients exhibited not only a significantly higher MELD (38) and CLIF-C AD (19) scores, but also ΔMELD and ΔCLIF-C AD was significantly increased during COVID-19. This indicates a more pronounced worsening of liver function before admission as compared to before COVID-19. Importantly, serum sodium levels were particularly low at admissions during COVID-19, indicating increased circulatory dysfunction (39). Consistently, a significantly higher proportion of emergency ACLD admissions during healthcare restrictions had severe or refractory ascites and one patient even had a perforated umbilical hernia potentially due to non-evacuated large-volume ascites and subsequently died of secondary bacterial peritonitis. Altogether, these results show that especially decompensated patients with ascites tended to be hospitalized later, i.e. in a more advanced stage of decompensation which likely translates into a dismal prognosis.

Elective ACLD admissions also decreased significantly, which may have long-term implications, i.e., further increased rates of emergency decompensations and liver-related deaths in the future (12) .

Additionally, non-electively admitted ACLD patients were more frequently admitted directly to the intensive care unit and liver-related mortality was considerably increased during COVID-19-related restrictions of healthcare. These increases in complications and liver-related deaths during COVID-19 were already predicted (12, 13) , and this scenario Accepted Article might also extend during the continued pandemic. Unfortunately, we can only speculate about the reasons, but patients may be reluctant to contact emergency medical services due to fear of SARS-CoV-2 infection at the hospital, leading to hospitalization at later stages of decompensation. Similar reasons were also speculated to be responsible for the observed 50% decrease of admissions due to myocardial infarctions with a concomitant rise in mortality and complication rates during COVID-19-related shutdown in Italy (40) .

This data indicates the need for simplifying access to in-hospital care, especially for patients with more advanced liver decompensation (i.e. decompensated patients with ascites), and for encouraging patients to timely seek in-hospital care despite the pandemic.

Our study has some limitations: The tele-survey and written questionnaire are assessments of subjective beliefs and feelings and are to be recognized as such.

Furthermore, recall bias cannot be ruled out completely. However, we conducted two different types of standardized surveys/questionnaires using different approaches (via phone and written questionnaires) and in different settings (exclusively outpatients and in-and outpatients combined) and both cohorts yielded similar results. Moreover, despite our efforts to contact all liver disease patients attached to our clinic, a selection bias for cohorts 1 and 2 cannot be completely ruled out. Correspondingly, the negative impact of COVID-19-related healthcare restrictions could in fact be even more severe than shown by our data. While we assume that the changed number of admissions was caused by healthcare-related factors (i.e. healthcare policy, regulation of elective procedures), we cannot completely rule out that death or migration contributed to intrinsic changes within the patient population. The lack of monitoring of the frequency of elective procedures without short-term inpatient stay, such as screening for HCC and varices or large-volume paracentesis in an outpatient setting represents another limitation of our study. Notably, this study did not assess COVID-19-related liver disease and the amount of extra healthcare resources needed for an adequate management of this disease. Further research is required to investigate the incidence of COVID-19-related liver disease and potential long-term consequences.

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In conclusion, the COVID-19 pandemic negatively impacted on patient's perceptions on quality of liver-related care. Additionally, patients often felt insufficiently informed on potential adverse effects of SARS-CoV-2 infections on their liver disease. In terms of clinical outcomes, we observed an increased rate of non-elective hospitalizations of sicker ACLD patients including emergency ICU admissions and higher liver-related mortality. Thus, it is vital to continuously provide patient education and improve efforts for tele-medical liver disease care in order to allow for early treatment of complications of cirrhosis and reduce liver-related mortality during the ongoing COVID-19 pandemic. 

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