Building Effective Quality Improvement Programs for Liver Disease: A Systematic Review of Quality Improvement Initiatives

Accepted Manuscript Building Effective Quality Improvement Programs in Liver Disease: A Systematic Review of Quality Improvement Initiatives Elliot B. Tapper, MD.

PII: DOI: Reference:

S1542-3565(16)30081-7 10.1016/j.cgh.2016.04.020 YJCGH 54723

To appear in: Clinical Gastroenterology and Hepatology Accepted Date: 11 April 2016 Please cite this article as: Tapper EB, Building Effective Quality Improvement Programs in Liver Disease: A Systematic Review of Quality Improvement Initiatives, Clinical Gastroenterology and Hepatology (2016), doi: 10.1016/j.cgh.2016.04.020. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Building Effective Quality Improvement Programs in Liver Disease: A Systematic Review of Quality Improvement Initiatives

Elliot B. Tapper, MD.

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Liver Center, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA

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Keywords: Hepatocellular Carcinoma, Vaccination, Readmissions, Paracentesis, Hepatic Encephalopathy, Cirrhosis Roles: Tapper (study concept and design; acquisition of data; analysis and interpretation of data; drafting of the manuscript; statistical analysis)

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Abbreviations: quality improvement (QI), spontaneous bacterial peritonitis (SBP), gastrointestinal bleeding (GIB), acute variceal hemorrhage (AVH), hepatocellular carcinoma (HCC), hepatitis A (HAV), hepatitis B (HBV), veterans administration (VA), hepatitis c (HCV), hepatic encephalopathy (HE)

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Disclosures: No funding was provided for the conduct of this research. Conflicts: No conflicts of interest to declare Writing assistance: None

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Word count: abstract 220, body 4,626, 1,070 references, legends 76 (Total 5,980)

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Address for Correspondence: Elliot B. Tapper, MD Beth Israel Deaconess Medical Center Deaconess 309 330 Brookline Avenue Boston, MA 02215 Phone: 617-632-5587 Fax: 617-632-8261 Email: [email protected]

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Abstract:

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Background: Quality indicators are the measurable components of clinical standards. Data are limited the design and impact of interventions to improve quality indicators for patients with chronic liver disease.

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Methods: A systematic review of PubMed, Web of Science and conference proceedings was performed to find reports of quality improvement (QI) interventions. Data regarding the several indicators was collected. The search focused on vaccination against hepatitis A or hepatitis B virus, management of spontaneous bacterial peritonitis (SBP), screening for varices, management of acute variceal hemorrhage, hepatocellular carcinoma (HCC) screening and 30-day readmissions.

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Results: Fifteen studies reported on the results of QI interventions. Nine focused on specific quality indicators (1 specific to vaccination, 2 SBP, 3 gastrointestinal bleeding, and 4 HCC screening); 5 focused on clinical outcomes. Most studies employed a pre-post study design. Interventions included checklists, educational conferences, electronic decision supports, nurse coordinators and systematic changes to facilitate specialist co-management. Successful interventions optimized clinical workflow, closed knowledge gaps among frontline providers, created forced-functions in the electronic ordering system, added dedicated staff to manage specific indicators and provided viable alternatives to hospitalization in order to reduce readmission. Unsuccessful interventions included case-management, phone-calls and home-visits to reduce readmissions, checklists and educational programs. Conclusion: Past experience with QI provides generalizable rules for successful future interventions aimed at improve quality indicator adherence and patient outcomes. 2

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Introduction

As clinicians, we seek to provide the best care for our patients. Simultaneously, we are

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required by our regulators to define and measure our care’s quality. These dual and reinforcing aims motivate the development of quality improvement (QI) programs.1 QI plays an increasingly

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important role in virtually every clinical activity. Further, QI has driven the development of electronic health records,2 shaped society recommendations for our procedures,3 and changed the

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tenor of our divisional conferences.4

Above all, QI, as a discipline, bridges the gap between guidelines and practice. Whereas

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guidelines have always defined the standard of care, only recently have these standards been

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articulated by into explicitly measurable activities. In their seminal paper, Kanwal and colleagues translated many key standards for the care of patients with liver disease into measurable ‘quality

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indicators.’5 QI is the step further from indicator to implementation. Thoughtful QI, in turn, requires that we must develop and assess the efficacy of clinical or administrative mechanisms to ensure the delivery of widely available, high quality care. However, guidance regarding the design of successful QI programs is limited. Herein, this review systematically assesses the literature on existing QI interventions for patients with chronic liver disease.

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Methods

A systematic review of the literature was performed by searching MEDLINE, Web of

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Science and the conference proceedings for AASLD, AGA and ACG. As a first step, set of

search terms was employed that reflected the explicit quality indicators delineated by Kanwal et

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al5 and the recent interest in hospital readmissions: ( "Liver Transplant"[Mesh] OR "Liver Cirrhosis"[Mesh] or "Cirrhosis"[TIAB]) AND ("Quality Improvement"[Mesh] OR "Quality Indicators, Health Care"[Mesh] or "Health Services Research"[Mesh] OR "paracentesis"[Mesh] or "vaccine"[Mesh] or "readmissions"[TIAB] or "Early Detection of Cancer"[mesh] or

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“Esophageal and Gastric Varices”[MESH] or “variceal hemorrhage" or "variceal bleeding" or

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"variceal bleed” or “spontaneous bacterial peritonitis”). References were searched within the ‘MELD era’ (> 2001) for generalizability and conference proceedings were searched from 2012-

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2015 to capture programs in development by the time of the search end-date (February 1, 2016). All titles and abstracts were reviewed for appropriateness. The reference list as well as the list of

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citing articles for each reviewed article was searched for relevant papers. Authors were contacted for missing data. A flow-chart of the literature search is available in the online supplement (Supplementary figure 1).

The primary aim of this review was to assemble the available data regarding interventions to improve quality and outcomes for patients with chronic liver disease. QI interventions were defined as a deliberate change in practice implemented with the aim of improved outcomes or adherence to quality indicators. A secondary aim was to describe the 4

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pooled statistics for each major quality indicator addressed by the included trials. Statistical

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analyses were performed using Comprehensive Meta-Analysis version 3 (Biostat, Englewood, NJ, USA). If significant heterogeneity among included studies was present ((I2 statistic >50%),

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a random-effects model was employed.

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Results

A total of 15 studies reported on the results of QI interventions; 10 focused on specific quality indicators (1 specific to vaccination, 2 spontaneous bacterial peritonitis (SBP), 3

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gastrointestinal bleeding (GIB) and acute variceal hemorrhage (AVH), and 4 hepatocellular

carcinoma (HCC) screening) while 5 focused on outcomes. Overall, 9 papers reported pre-post

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study designs and 4 described controlled trials (including 2 randomized-controlled trials). Most (9) studies came from the US while 3 came from Australia, and 1 from the UK, Denmark and

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Italy.

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Observational studies describing rates of quality indicators

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Vaccination for Hepatitis A and B Virus

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Acute viral super-infection can be life threatening for patients with pre-existing liver

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disease.6 Accordingly, protecting patients with chronic liver disease with or without cirrhosis from the risk of acute viral hepatitis A or B (HAV, HBV) through vaccination is a widely held quality indicator.5 Ten studies have previously assessed adherence to this recommendation (Supplementary table 1). The pooled rates of HAV and HBV vaccination for susceptible patients were 28.9% 95% CI (18.1-42.8, I2 99.5) and 31.1% 95% CI (18.5 - 47.2, I2 99.9). According to

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the largest study from the national VA database, vaccination rates were highly variable between

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facilities: 22.5%-87.3% for HBV and 9.6%-82.9% for HAV.7

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Intervention studies describing quality improvement

Masson and her colleagues report the results of the sole intervention study aimed at vaccination.(Table 1)8 489 patients enrolled in a methadone clinic (~60% hepatitis c (HCV) antibody positive) were randomized to receive either usual care (education regarding Human Immunodeficiency Virus prevention and off-site referral for hepatitis evaluation and vaccinations) or an intervention consisting of case-management, on-site serological testing, vaccination and motivational interviewing. Patients in the intervention group were far more likely to complete a 3-dose vaccine schedule than those in the control, 78.0% vs 9.3%. 7

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Observational studies describing rates of quality indicators

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Management of potential SBP

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The management of SBP touches upon multiple quality indicators. These include timely paracentesis, appropriate assessment of ascitic fluid for cell count and culture as well as timely

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treatment of SBP with appropriate antibiotics and albumin co-therapy for renal protection.5 Owing to the morbidity and mortality of delayed treatment for SBP, routine paracentesis for patients admitted with ascites, particularly early paracentesis, has been associated with reduced risk of death in multiple studies.9-11 Among all inpatients with ascites assessed in 5 studies,

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56.7% 95% CI (48.4 – 64.7, I2 93.9) received a paracentesis during their admission.

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(Supplementary Table 2)

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Intervention studies describing quality improvement

Two interventions aimed at improving the management of SBP have been published (Table 1). Desai and colleagues retrospectively reviewed their experience with SBP management before and after changes in the structure of cirrhosis care at an academic transplant center.12 The intervention entailed a shift from on-demand hepatology consultation by housestaff teams located anywhere in the hospital to a model where patients with cirrhosis were admitted to a geographical unit under the care of hospitalists and mid-level practitioners who round daily with a hepatologist. Their small study (26 patients with SBP before and 30 after protocol initiation),

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saw several quality indicators improve without changes in outcomes (length of stay, readmission,

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mortality) or cost. Specifically, the rate of early (< 24 hour) paracentesis (100% vs 79%),

albumin co-therapy (97% vs 65%) and use of secondary SBP prophylaxis on discharge (91% vs

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32%) were all improved.

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Rawson et al reviewed all ascitic fluid samples for the ‘time to tap’ from admission, tests ordered and labelling of bottles for the appropriate indication before and after an educational intervention.(Table 1) Data was available for 34 housestaff (and 33 of their patients) prior to the intervention and 26 housestaff (54 patients) afterward. The educational intervention entailed a 1-

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hour talk by a senior resident and a 20-page booklet summarizing the definition,

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pathophysiology, clinical presentation and treatment of SBP. The intervention was associated with significantly better performance on a quiz provided before and after the clinical rotation.

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day).

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Furthermore, the authors observed significant reductions in the time to tap (median of 2 days to 1

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Observational studies describing rates of quality indicators

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Varices Care

Quality indicators for the care of patients with varices reflect adequate screening and

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prophylaxis as well as optimal treatment of AVH.5, 13 Screening patients with cirrhosis for

varices identifies candidates for primary AVH prophylaxis13 and improves survival in a cost-

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effective fashion.14 Four studies have examined the rate of screening endoscopy among patients with newly identified cirrhosis. These included reports from a single center,15 a three center collaboration,16 a large commercial database,17 and the VA national database.18 The pooled

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screening rate among these studies was 26.8% 95% CI (19.5 – 35.8, I2 99.3).

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Ten studies have examined the quality process measures for patients with AVH.(Supplementary table 3) All studies agree that timely endoscopy, vasoactive medications,

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prophylactic antibiotics and endoscopic interventions are quality indicators with the specific

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timeframe for each therapy varying with reference to differing consensus statements.5, 13 The pooled rates of prophylactic antibiotics, octreotide infusion, band ligation or sclerotherapy and timely (< 24 hour) endoscopy were: 35.0% 95% CI (25.8 – 45.5, I2 92.2), 76.1% 95% CI (61.5 – 86.3, I2 96.5), 79.8% 95% CI (68.8 – 87.6, I2 94.0) and 77.9% 95% CI (66.8 – 86.1, I2 91.7)

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Intervention studies describing quality improvement

Four studies have assessed the role of interventions to improve the quality of care

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provided to patients with cirrhosis who present with GIB.(Tables 1-2) Johnson et al deployed a program of clinician education (an hour-long powerpoint-based didactic) and a standardized

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paper order set in order to promote AASLD guideline-based care for patients with chronic liver disease and upper GIB.19(Table 1) The order set included standard labs, diagnostic tests and provided recommendations on therapeutic medications and procedures. The authors assessed their program using a pre-post study design that examined 59 admissions (48 unique patients)

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prior to and 55 admissions (51 unique patients) after the program’s implementation. More

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patients received prophylactic antibiotics and octreotide while equal numbers received protonpump inhibitors after the protocol. Overall, 66% received all three measures after and 41%

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beforehand. The intervention was associated with decreased 30-day readmissions (13% vs 41%),

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including readmissions for GIB (5% vs 22%).

Mayorga extended these data by implementing an electronic order set and confirming similar findings with respect to improved process measures.20(Table 1) The authors performed a prospective observational study at large safety-net hospital over the course of 1 year with the intention of increasing the provision of and decreasing the time to octreotide and antibiotics. The order-set cued clinicians to provide the correct medications and doses along with free-text education regarding the underlying rationale. Order set utilization was variable. Of the 123 patients admitted with cirrhosis and bleeding over the study period, 61 (49.6%) patients received 11

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the order set and 62 did not. However, there were no significant differences in the demographic

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or clinical characteristics between these patients. This intervention was associated with

significantly increased antibiotic (100% vs 89%) but not octreotide (98% vs 94%) utilization.

The time to both measures, however, was significantly decreased. The authors did not observe

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any differences with respect to units of blood, length of stay, rebleeding or mortality.

Ghaoui et al evaluated many different process measures following the implementation of mandatory GI consults for patients with cirrhosis.21(Table 2) Using a pre-post study design, the authors compared adherence to quality indicators and outcomes after initiating a program where

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two staff gastroenterologists manually reviewed all admissions to their center for the presence of

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decompensated cirrhosis in order to contact and request admitting teams to consult gastroenterology. Of note, no specific protocol was employed and the consult responsibilities

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were shared by four general gastroenterology groups. The authors then compared 379 admissions prior to the intervention (including 76 with GIB) to 316 thereafter (57 with GIB). Patients in the

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mandatory consult period had a higher frequency of endoscopy within 24 hours (91.2% vs 76.9%) and statistically similar banding rates (93.8% vs 87.0%), antibiotics (44.8% vs 39.1%) and octreotide (84.5% vs 76.6%).

Finally, Wundke and colleagues attempted an education-based intervention before hiring a dedicated nurse to coordinate varices care.22(Table 1) The authors conducted a pre-post study to determine the impact of a QI intervention on both rates of screening for varices in patients with cirrhosis (n = 250) and optimal care for a small cohort (n = 46) presenting with AVH. At 12

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baseline prior to the intervention the authors found that roughly 10% of patients with cirrhosis

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were being screened for varices and of those with bleeding, 15% received antibiotics, > 90% received octreotide and 9% received adequate endoscopic eradication of varices. The

intervention’s first iteration included lectures and posted guidelines to promote quality

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indicators; it failed to improve adherence. Thereafter, the authors deployed a dedicated nurse coordinator to facilitate varices care for all patients referred to the center. The nurse operated

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independently, fielding referrals from clinicians for new patients, assuming responsibility for their care and proactively coordinating management according to protocol. In addition, all patients were entered into database with an automated recall for procedures. The result was increased rates of screening for varices (>90% for 3 years in a row). For a post-intervention

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cohort of 46 patients with AVH, rates of prophylactic antibiotics rose to 90% while octreotide

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use remained stable and the rate of variceal eradication rose to 100%.

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HCC Screening

Semiannual screening of patients with cirrhosis for HCC improves overall survival likely

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by fostering early detection in the setting of effective locoregional therapies and liver

transplantation.23 In their systematic review of studies including 17,286 patients, Singal and

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colleagues identified that the pooled imaging-based surveillance rate for patients with cirrhosis was 18.4%.24

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Intervention studies describing quality improvement

Four studies have evaluated interventions aimed at increasing the rate HCC

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screening.(Table 1)25-28 Frueland et al presented an abstract describing an intervention wherein

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Danish clinicians at a single center caring for patients with HBV or HCV cirrhosis were prompted to complete a quality assurance module through the electronic health record.(Table 1) Among a cohort of 51 patients, the screening rate increased, but non-significantly, from 63% to 84%.27 The authors cited difficulty in the use and implementation of the platform.

Two interventions with positive results employed nurses dedicated to ensuring HCC screening and care coordination.25, 28(Table 1) Kennedy et al studied the impact of their program in a pre-post design for 114 Australian patients with viral hepatitis (84% with HCV cirrhosis) followed longitudinally at a single center.28 Their intervention was multimodal, including 14

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physician and patient education as well as a dedicated ‘viral hepatitis nurse’ with responsibility

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for facilitating HCC screening aided by a patient database with an automated reminder/recall

function. By the conclusion of the study, the rate of biannual screening rose from 46% to 92%. Aberra et al evaluated a larger (N = 355) American cohort of patients with cirrhosis from a single

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center.25 Patients were enrolled from clinic after their physician indicated on a check-out form that the patient was cirrhotic. Thereafter each patient was entered into a database which alerted

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both clinicians and nursing staff when patients were due or delinquent for a screening test. In a pre-post design comparing the HCC screening rate to a historical age, sex and race matched

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cohort, the authors observed a statistically significant 19% increase.

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The largest trial to date was reported by Beste.26(Table 1) The authors prospectively assessed a point-of-care electronic reminder wherein the electronic ordering system would

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prompt clinicians to order HCC screening for patients with cirrhosis during a clinical encounter. The intervention was deployed in a quasi-experimental fashion at one facility while 7 VA centers

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were followed as contemporaneous controls. For clinicians at the intervention site, a clinical reminder would appear upon opening the electronic health record of any patient with cirrhosis who had not received an ultrasound or multiphasic cross-sectional abdominal imaging within the preceding 6 months. The reminder provided the clinician with a brief statement regarding screening rationale as well as check-boxes to order tests or provide opt-out reasons. This intervention was displayed to all providers caring for patients with cirrhosis, whether in specialty or primary care clinics. HCC screening rates increased by 51% at the intervention site (albeit with a low absolute improvement from 27.6% vs 18.2%) but not at the controls (16.1% vs 17.5%). 15

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Observational studies describing rates of quality indicators

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Hospital Readmissions

Readmissions are independently associated with mortality, frequently un-reimbursed by

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payors and potentially linked to broad financial disincentives.1, 29 Unfortunately, readmissions for patients with cirrhosis are common. To date, 8 studies have examined readmissions and identified a pooled 25.8% 95%CI (23.8 – 28.0, I2 90.3) 30-day readmission rate (Supplementary Table 4). In addition, Bajaj et al recently identified a 53% 90-day readmission rate for a

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multicenter cohort of patients with decompensated cirrhosis (most of whom had nosocomial

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infections).30

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Intervention studies describing quality improvement

Two intervention studies have taken specific aim at 30-day readmissions.(Table 2) Li et al have reported in an abstract the results of small study of two peridischarge interventions for patients with chronic hepatic encephalopathy (HE) – a medication reconciliation program and a post-discharge phone call.31 From a cohort of 312 patients with HE, 18 patients received one of the two interventions. Phone calls were not associated with changes in readmission risk while the medication reconciliation program was associated with increased readmission risk. Tapper et al examined a broad QI intervention aimed at reducing 30-day readmissions on a closed liver unit.29 16

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This study took place in three phases: a pre-intervention control, a paper-checklist phase that was

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performed on daily work-rounds with housestaff and electronic phase that incorporated the checklist elements into the electronic health record. The intervention sought to decreased

practice variation, standardize the management of HE and universalize prophylactic measures.

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The protocol consisted of daily medication reconciliation, high dose/frequency lactulose for overt HE, and prophylactic measures for HE (universal rifaximin for a history of overt HE),

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variceal hemorrhage, SBP and deep vein thrombosis. The electronic phase prompted prophylactic medication orders on admission, defaulted the protocol’s dose/frequency of lactulose and further reinforced each element with a templated note for all patients admitted to the liver service. In a pre-post design, readmissions were reduced from 37.9% to 26.6% after the

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electronic phase. Additionally, the protocol was associated with decreased length of stay for

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patients with overt HE.

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Interventions aimed at outcomes

Three studies have evaluated broad protocols designed to improve patient care with the

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goal of reducing or predicting all-cause hospitalizations or improving survival and quality of life.(Table 2) Ghaoui and his colleagues examined a cohort of 316 hospitalized patients with

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decompensated cirrhosis who received a mandatory gastroenterology consult for co-management and compared quality indicators to a pre-intervention control of 379 patients.21 Though no difference in clinical outcomes was observed, the authors found an increase in the rate of paracentesis (82.2% vs 39.9%), ascitic cell count assessment (75.8% vs 14.4%), salt restriction

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for patients with ascites (66.4% vs 30.6%), and timely endoscopy for bleeding within 24 hours

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(91.2% vs 76.9%).

Finally, Wigg and Morando both reported on comprehensive interventions that aimed to

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create new models of care for patients with cirrhosis.32, 33(Table 2) Wigg employed casemanagers and dedicated hepatology nurses.33 Following hospital discharge, nurses performed one home-visit and, thereafter, routine phone calls. All patients were provided a standard guideline for symptoms that would prompt evaluation as well as reminders for the best practices to avoid symptomatic ascites or HE. Morando, in addition to outreach programs, created day hospitals where procedures could be performed and arranged multidisciplinary outpatient evaluations that lasted between 5-9 hours depending on the needs of the patient.32 The available procedures included imaging, same-day endoscopy, and psychometric testing and electroencephalograms for the diagnosis of covert HE. Both studies are small. Wigg randomized 18

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a total of 60 patients with a recent admission for a complication of decompensated cirrhosis; 40

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received the intervention and 20 were controls. Morando evaluated 100 consecutive patients who were discharged after an admission for a complication of decompensated cirrhosis; 60 controls and 40 who received the intervention, their results illustrate critically important themes. The

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Wigg study demonstrated improved clinic attendance but no difference in mortality or hospital readmission rate. Conversely, Morando’s study, although non-randomized, demonstrated

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improved survival as well as reduced readmissions and cost.

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Discussion Taken together, these studies speak to the mechanisms by which QI proceeds from quality indicator to implementation. Five generalizable trends emerge from the results of these

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interventions (Figure 1):

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1. Successful programs understand and manage clinical workflow

Many quality indicators involve the performance of tasks by busy clinicians. A successful QI intervention’s design involves sensitivity to the manner in which clinicians and patients

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accomplish their goals. Masson’s vaccination trial, for example, streamlined the process by which clinicians at a methadone clinic could determine and care for candidates for vaccination

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against viral hepatitis.8 Since the primary aim of that clinic is the safe provision of methadone,

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each additional step required to accomplish unrelated tasks such as preventative health makes them less likely to be performed in the context of busy practice. Masson therefore brought

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phlebotomy, nursing and vaccine storage on site. The advantages provided by this intervention are highlighted by problems observed elsewhere. Jacobs et al found that variable vaccination rates across clinics were dependent on the physical availability vaccines at the point of care.34 Further, Thudi and colleagues showed in a retrospective cohort study that vaccination ‘reminders’ through electronic health record flags which were not linked to the resources needed to complete the task were not associated with increased vaccinations.35 The same rule applies to patients. For many patients, additional trips to a clinic for blood tests or additional vaccines in a series are not realistic. Two studies have indicated that between 31% and 64% of patients are lost to follow up after their first visit and thus unable to complete a vaccination series.36, 37 20

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Timely paracentesis has been shown to be a potentially life-saving procedure.9-11 Like any

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aspect of care that exists outside usual workflow, it too is at risk for delay or deferral. For

frontline clinicians, admitting patients is a routine that involves taking and writing histories and physical exams; paracentesis is often a departure from routine that may make its performance

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less likely. Rawson was successful in part by compelling early paracentesis through education regarding its importance to relevant patient outcomes.38 However, the long-term effects of this

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strategy are uncertain, particularly where housestaff rotate on and off service. Complicating workflow, furthermore, the devices needed for paracentesis may take time to assemble and in many centers housestaff require supervision for the safe performance of paracentesis. One response, as provided by Desai,12 is to restructure the clinical service, bringing to the frontline

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clinicians with familiarity to the specific needs of patients with cirrhosis and the ability to

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perform procedures. An unaddressed additional issue was raised in a study using the National Inpatient Sample where decreased utilization of paracentesis was observed during weekends.11

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In this case, hospital staffing may play a role either as a function of decreased time allotted per

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patient on weekends or limited interventional radiology services.

2. Interventions operated by dedicated staff achieve goals

Trials which employ dedicated staff, often nurses, who are empowered to independently coordinate directed aspects of patient care yield consistently positive findings. Wundke reported how, for an admittedly small cohort of patients with AVH (n = 46) and a larger cohort of patients needing variceal screening (n = 250), a nurse coordinator effected nearly perfect adherence with

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quality care guidelines.22 A similar strategy was described by the same group who also employed

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a ‘viral hepatitis nurse’ to facilitate HCC screening.28 Aberra modified this protocol for their

HCC screening program by using nursing staff as a backstop for overdue screening tests through electronic notifications of delinquency.25 Finally, as above, Masson demonstrated the success of

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embedding nursing staff in the clinic to coordinate vaccination following visits for unrelated

reasons.8 Though this strategy is consistently found to be effective, there may be two drawbacks.

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First, hiring trained and specialized staff is costly. Second, effect sizes often fall when smaller interventions based on hiring additional staff are scaled up. Positive results in small trials can be

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related to the effect of a specific, exceptional nurse.1

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3. Efforts to close knowledge gaps are key to achieving many quality indicators

Many clinicians are unaware of the specific needs of patients with cirrhosis. While quality

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indicators have been defined for many aspects of care by guidelines, their dissemination to frontline clinicians is often limited. Multiple trials have described educational interventions. Rawson described positive, albeit short-term, effects on the time to paracentesis performed by housestaff from an educational seminar and booklet.38 Similarly, Johnson improved the management of upper GIB by educating housestaff with a powerpoint presentation before deploying a paper checklist.19 Education is most useful as one component of an intervention but less so alone. Unfortunately, educational initiatives often have short-lived effects,1 a problem which is compounded when depending on rotating housestaff. They are also associated with

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mixed results. Wundke increased varices screening only after transitioning from an educational

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program to a nurse-led intervention.22

An alternative solution is to modify the delivery of care so that all patients are at least co-

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managed by experts. After observing incomplete adherence to quality indicators in the context of housestaff-led patient care, Desai restructured their inpatient service.12 Multiple quality

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indicators improved after moving all cirrhosis admissions to a service staffed by hospitalists and a consistent group of midlevel practitioners who rounded daily with a hepatologist. Mandatory gastroenterology consultation is another option. As described in Ghaoui et al,21 though it was a laborious process, this can be achieved by having staff gastroenterologists survey each admission daily to prompt consults for patients with decompensated cirrhosis. Notably, however, in the

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adherence persisted.

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absence of a predefined protocol for the consultants, practice variation and incomplete indicator

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4. Voluntary interventions are less likely to be completed than forced-functions.

When the aim of QI is to standardize care, facilitating consistent adherence to quality indicators, many investigators create checklists.1, 19, 29 Johnson19 and Tapper29 both report on paper checklist-based interventions. While Johnson’s results were positive, the study was shortterm and affected a small population (n = 99). Tapper et al, on the other hand, found negative results owing to poor adherence in a larger patient series (n = 470). Instead of a paper checklist, Mayorga implemented an electronic order set for their GIB protocol.20 Unfortunately, while order set use was associated with a measurable impact, the very study design reported – 23

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comparing results for patients who did or did not receive the order set – was based on the

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observed < 50% protocol adherence rate. Beste at al used a pop-up flag in the health record to promote HCC screening and also observed low uptake of their intervention; 3 of 4 patients with cirrhosis remained unscreened.26 Clinicians receive many ‘reminders’ and may simply close

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them out before reading carefully.

It is generally difficult to achieve adherence to any new measure that requires voluntary action. For this reason, the results of checklist-based interventions are inconsistent or demonstrate early improvements that fade over time.1 Published alternatives include automatic

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orders to nursing staff as studied by Aberra (to arrange forgotten HCC screening),25 modifying

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the way medications are ordered in the electronic health record to set a specific treatment protocol as a default order,29 or, as studied by Wundke and Kennedy, assigning responsibility for

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a task to staff who can act independently.22, 28

5. Interventions seeking to reduce readmission should consider providing alternatives

Readmissions are an increasing focus of QI initiatives. However, given the tenuous clinical status of many patients with decompensated cirrhosis, rehospitalization remains an effective solution for urgent symptoms. Post-discharge phone calls have been studied among patients with and without cirrhosis but do not reduce readmissions.1, 22, 31 Instead, these calls are best viewed as a way to capture decompensations early. For example, Thomson et al demonstrated how an automated telephone system that periodically queries patients could 24

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identify patient-reported symptoms, specifically weakness and weight gain > 5 pounds, that

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were highly associated with hospitalization risk.39 Such tools should be paired with resources for symptom management without readmission. Otherwise, clinicians alerted to their patients’ illness will struggle to arrange solutions (e.g. urgent paracentesis or evaluation).1, 31 Indeed, of the two

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most comprehensive trials aiming to improve patient outcomes, Wigg et al offered phone calls and failed to reduce readmissions while Morando succeeded.32, 33 Morando created ‘day

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hospitals’ where multidisciplinary management and readily available procedures provided viable alternatives to readmission. While the feasibility and safety of such programs in other settings deserves further study, observation and therapy before referral to the hospital for selected

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patients with fluid overload or even HE could be a promising approach.

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In conclusion, efforts to raise the quality of care provided to patients with cirrhosis will

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be repaid with improved outcomes. They will also benefit from an understanding of what has or what hasn’t worked previously. Moving forward, initiatives are needed to reduce practice variability, standardize care and translate best practices from the guidelines to the bedside. Further research comparing strategies for healthcare delivery are needed.

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Figure 1: Generalizable Trends from the Results of QI Intervention Studies

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Quality improvement (QI) is the process by which programs are implemented to address predefined quality indicators. Five generalizable trends governing the success of QI programs are presented with examples of the indicators addressed (left) and the programs implemented (right).

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Table 1: Protocols aimed at condition-specific quality indicators

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Domain

Stated Aim

Intervention

Study Design

Population; (n)

Process Measures

Improved adherence?

Masson 20138

Vaccination

Improve vaccination rates

Case-management, counselling, on-site vaccines

Randomized controlled trial

Methadone users; 489

Rates of hepatitis A and B vaccination

Yes

Improve primary prevention and treatment of AVH

Education, dedicated nurse coordinator

Pre-Post

Cirrhosis; 250 primary prevention, 46 with bleeding

Prophylactic endoscopy; antibiotics, octreotide and correct ward placement

Not with education; yes with nurse coordinator

Improve GIB management

Paper order set, clinician education

Pre-Post

Cirrhosis; 48 pre, 51 post

Rate of prophylactic antibiotics, octreotide

Yes

Observational

Cirrhosis; 61 used order set, 62 did not

Mayorga 201320

Improve GIB management

Aberra 201325

Improve HCC screening

Kennedy 201328

Improve HCC screening

Frueland 201327*

HCC

Electronic order set; clinicians free to use or not use Dedicated nurse, automated reminders Education, dedicated nurse, patient database

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Varices

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Johnson 201119

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Wundke 201022

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Paper (Ref)

Rate/time to prophylactic antibiotics, octreotide, endoscopy Utilization of HCC screening

Yes

Pre-Post

Cirrhosis; 160 pre, 355 post

Pre-Post

Viral hepatitis; 114

Rate of HCC screening in past 6 and 24 months

Yes

Yes

Educational module

Pre-Post

Cirrhosis; 51

Rate of ultrasound use for screening

No (not significant)

Beste 201526

Improve HCC screening

Point-of-care electronic reminder

Controlled, trial

Cirrhosis; 790 intervention, 2094 control

Adequate 6-month HCC surveillance

Yes

Desai 201412

Improve SBP care

Mandatory GI comanagement

Pre-Post

Patients with SBP; 30 pre, 26 post

Early paracentesis, albumin use, secondary prophylaxis

Yes

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Improve HCC screening

Ascites

Improve SBP Patients with ascites; Rawson Educational booklet Pre-Post Early paracentesis Yes 38 care 33 pre, 54 post 2015 AVH = acute variceal hemorrhage, GI = gastroenterology, GIB = gastrointestinal bleeding, HCC = hepatocellular carcinoma, SBP = spontaneous bacterial peritonitis. *Abstract

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Table 2: Protocols Aimed at Clinical Outcomes Domain Aim

Intervention

Wigg 201333

Reduce hospital-days, improve quality of life

Morando 201332

Determine efficacy of a new model of care

Casemanagement, dedicated nursing and education Comprehensive multidisciplinary outpatient evaluation; “day hospital”

Improved clinical outcomes?

Randomized, controlled trial

Decompensated cirrhosis; 40 intervention, 20 control

Clinic attendance, HCC screening, vaccination rates

No

Controlled, nonrandomized trial

Decompensated cirrhosis; 40 intervention, 60 control

-

Improved survival, reduced readmissions and cost

Pre-Post

Decompensated cirrhosis; 379 pre, 316 post

Many. E.g. diagnostic paracentesis, timely endoscopy for bleeding

No

-

No

Dose of lactulose, rifaximin use, SBP/DVT prophylaxis

40% fewer readmissions with electronic intervention

Mandatory GI consult

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Improve overall inpatient care quality

Process Measures

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Ghaoui 201521

Multiple outcomes

Population

Study Design

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Paper (Ref)

Retrospective, observational cohort

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Reduce readmissions

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Hepatic encephalopathy; Li 2014 18 intervention, 294 control 30-day readmissions Cirrhosis; 626 Paper checklist, Reduce pre, 470 Tapper electronic Pre-Post readmissions checklist, 624 201529 decision support electronic phase DVT = deep vein thrombosis, GI = gastroenterology, SBP = spontaneous bacterial peritonitis 31

Medication reconciliation and post-discharge calls

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References

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7. 8.

9.

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Tapper EB. Challenge accepted: Confronting readmissions for our patients with cirrhosis. Hepatology 2016. Bates DW, Ebell M, Gotlieb E, et al. A proposal for electronic medical records in US primary care. Journal of the American Medical Informatics Association 2003;10:1-10. Rex DK, Bond JH, Winawer S, et al. Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the US MultiSociety Task Force on Colorectal Cancer. Am j gastroenterol 2002;97:1296-1308. Tapper EB, Leffler DA. The Morbidity and Mortality Conference in Gastroenterology and Hepatology: An Important Cornerstone of Patient Safety and Optimal Care. Gastroenterology 2016;150:19-23. Kanwal F, Kramer J, Asch SM, et al. An explicit quality indicator set for measurement of quality of care in patients with cirrhosis. Clin Gastroenterol Hepatol 2010;8:709-17. Sagnelli E, Coppola N, Pisaturo M, et al. HBV superinfection in HCV chronic carriers: a disease that is frequently severe but associated with the eradication of HCV. Hepatology 2009;49:10901097. Kramer JR, Hachem CY, Kanwal F, et al. Meeting vaccination quality measures for hepatitis A and B virus in patients with chronic hepatitis C infection. Hepatology 2011;53:42-52. Masson CL, Delucchi KL, McKnight C, et al. A randomized trial of a hepatitis care coordination model in methadone maintenance treatment. American journal of public health 2013;103:e81e88. Kim JJ, Tsukamoto MM, Mathur AK, et al. Delayed paracentesis is associated with increased inhospital mortality in patients with spontaneous bacterial peritonitis. Am J Gastroenterol 2014;109:1436-42. Le S, Spelman T, Chong C-P, et al. Could Adherence to Quality of Care Indicators for Hospitalized Patients With Cirrhosis-Related Ascites Improve Clinical Outcomes&quest. The American journal of gastroenterology 2016. Orman ES, Hayashi PH, Bataller R, et al. Paracentesis is associated with reduced mortality in patients hospitalized with cirrhosis and ascites. Clinical Gastroenterology and Hepatology 2014;12:496-503. e1. Desai AP, Satoskar R, Appannagari A, et al. Co-management between hospitalist and hepatologist improves the quality of care of inpatients with chronic liver disease. Journal of clinical gastroenterology 2014;48:e30-e36. de Franchis R, Faculty BV. Expanding consensus in portal hypertension: Report of the Baveno VI Consensus Workshop: Stratifying risk and individualizing care for portal hypertension. Journal of hepatology 2015;63:743-752. Arguedas MR, Heudebert GR, Eloubeidi MA, et al. Cost-effectiveness of screening, surveillance, and primary prophylaxis strategies for esophageal varices. The American journal of gastroenterology 2002;97:2441-2452. Moodley J, Lopez R, Carey W. Compliance with practice guidelines and risk of a first esophageal variceal hemorrhage in patients with cirrhosis. Clinical Gastroenterology and Hepatology 2010;8:703-708. Buchanan PM, Kramer JR, El-Serag HB, et al. The quality of care provided to patients with varices in the department of veterans affairs. Am J Gastroenterol 2014;109:934-40. Waghray A WN, Kyprianou A, Menon N. Variceal Screening in Cirrhotic Patients. Hepatology 2014;60:1594A.

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Flemming JA, Saxena V, Shen H, et al. Facility-and Patient-Level Factors Associated with Esophageal Variceal Screening in the USA. Digestive Diseases and Sciences 2016;61:62-69. Johnson EA, Spier BJ, Leff JA, et al. Optimising the care of patients with cirrhosis and gastrointestinal haemorrhage: a quality improvement study. Aliment Pharmacol Ther 2011;34:76-82. Mayorga CA, Rockey DC. Clinical utility of a standardized electronic order set for the management of acute upper gastrointestinal hemorrhage in patients with cirrhosis. Clinical Gastroenterology and Hepatology 2013;11:1342-1348. Ghaoui R, Friderici J, Desilets DJ, et al. Outcomes Associated With a Mandatory Gastroenterology Consultation to Improve the Quality of Care of Patients Hospitalized With Decompensated Cirrhosis. Journal of Hospital Medicine 2015;10:236-241. Wundke R, Altus R, Sandford J, et al. Improving management of oesophageal varices in patients with cirrhosis. Quality and Safety in Health Care 2010;19:536-541. Singal AG, Pillai A, Tiro J. Early detection, curative treatment, and survival rates for hepatocellular carcinoma surveillance in patients with cirrhosis: a meta-analysis. PLoS Med 2014;11:e1001624. Singal AG, Yopp A, Skinner CS, et al. Utilization of hepatocellular carcinoma surveillance among American patients: a systematic review. Journal of general internal medicine 2012;27:861-867. Aberra FB, Essenmacher M, Fisher N, et al. Quality improvement measures lead to higher surveillance rates for hepatocellular carcinoma in patients with cirrhosis. Dig Dis Sci 2013;58:1157-60. Beste LA, Ioannou GN, Yang Y, et al. Improved Surveillance for Hepatocellular Carcinoma With a Primary Care–Oriented Clinical Reminder. Clinical Gastroenterology and Hepatology 2015;13:172-179. Fruelund P, Larsen CS, Erlandsen M, et al. Improving Performance of Hepatocellular Carcinoma Screening of Cirrhotic Patients with Chronic Viral Hepatitis B and C using a Combined Clinical Decision-Support and Quality Assurance System. HEPATOLOGY 2013;58:1211A-1211A. Kennedy N, Rodgers A, Altus R, et al. Optimisation of hepatocellular carcinoma surveillance in patients with viral hepatitis: a quality improvement study. Internal medicine journal 2013;43:772-777. Tapper EB, Finkelstein D, Mittleman MA, et al. A Quality Improvement Initiative Reduces 30-Day Rate of Readmission for Patients With Cirrhosis. Clin Gastroenterol Hepatol 2015. Bajaj JS, Reddy KR, Tandon P, et al. The Three-Month Readmission Rate Remains Unacceptably High in a Large North American Cohort of Cirrhotic Patients. Hepatology 2015. Li R, Tierney A, Carr R. The Impact of Peri-discharge Interventions on 30-Day Readmission and 90-Day Mortality Rates for Patients Admitted With Hepatic Encephalopathy. Am J Gastroenterol 2014;109:S131-S131. Morando F, Maresio G, Piano S, et al. How to improve care in outpatients with cirrhosis and ascites: a new model of care coordination by consultant hepatologists. Journal of hepatology 2013;59:257-264. Wigg AJ, McCormick R, Wundke R, et al. Efficacy of a chronic disease management model for patients with chronic liver failure. Clinical Gastroenterology and Hepatology 2013;11:850-858. e4. Jacobs RJ, Meyerhoff AS, Saab S. Immunization needs of chronic liver disease patients seen in primary care versus specialist settings. Dig Dis Sci 2005;50:1525-31. Thudi K, Yadav D, Sweeney K, et al. Physicians infrequently adhere to hepatitis vaccination guidelines for chronic liver disease. 2013.

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Hernandez B, Hasson NK, Cheung R. Hepatitis C Performance Measure on Hepatitis A and B Vaccination: Missed Opportunities&quest. The American journal of gastroenterology 2009;104:1961-1967. Scaglione SJ, Shepard K, Adams W, et al. Preventative Care Quality Indicator Adherence and Factors Affecting Quality Care Measurement in Patients with Cirrhosis: A Single-centered Study. HEPATOLOGY 2014;60:958A-959A. Rawson TM, Bouri S, Allen C, et al. Improving the management of spontaneous bacterial peritonitis in cirrhotic patients: assessment of an intervention in trainee doctors. Clinical Medicine 2015;15:426-430. Thomson M, Volk M, Kim HM, et al. An Automated Telephone Monitoring System to Identify Patients with Cirrhosis at Risk of Re-hospitalization. Digestive diseases and sciences 2015;60:3563-3569.

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VA; single center

Jacobs 2005(3) Shim 2005(4)

Kramer 2011(8)

VA; national database VA; national database

Thudi 2013(9)

Single center

Kanwal 2010(7)

Chronic HCV

-

Cirrhosis

26.3% (76)

Chronic liver disease

22.6% (598)

33.1% (565)

Chronic HCV

10.5% (870)

-

Chronic HCV

6.6% (5,825)

6.7% (5,832)

Chronic HCV

52.5% (1,837)

58.6% (2,186)

Chronic HCV

21.5% (8,167)

26.0 (8,167)

Chronic HCV

45.5% (40,288)

57.0% (50,442)

52.1% (497)

50.6% (443)

Chronic liver disease

8.5% (118)

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Scaglione 2014 Single center Cirrhosis 56% (445) (10)* HCV = hepatitis C, VA = Veteran’s administration. * - abstract

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Hepatitis B Vaccination % (N)

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Hernandez 2009(6)

Arguedas 2002(2)

Hepatitis A Vaccination % (N)

25.8% (89)

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Hachem 2008(5)

Single liver center Single transplant center Multiple primary care and specialist practices VA; 2 centers VA; single center

Wong 1996 (1)

Patients

Setting

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Paper (Reference)

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Supplementary Table 1: Studies Assessing Vaccination rate

46% (445)

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Setting

Kanwal 2012(11) Abed 2013 (12)*

VA; 3 centers Single center

Brooling 2014(13)

Single center

Paracentesis during admission % (N) 57.6% (535) 42.9% (70)

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Paper (Reference)

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Supplementary Table 2: Studies Assessing Paracentesis Performance Among Hospitalized Patients with Ascites

41% (193); 29.0% < 1 day

National 60.7% (17,711); 36.6% < 1 day inpatient sample Australian 75% (302) Le 2016(15) single center VA = Veteran’s administration. * - abstract

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Orman 2014(14)

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Supplementary Table 3: Studies Assessing the Quality of Acute Variceal Hemorrhage Management

Antibiotics % (N)

Octreotide % (N)

Timely endoscopy % (N)

Nine Korean centers

Acutely bleeding, cirrhotic

77.9% (403)

49.4% (403)

87.6% (403)

-

Singh 2007(16)

Canadian Single center

Acutely bleeding, cirrhotic

82% (81); 56.8% prior to endoscopy (81)

58% (81; 6 hours) 97% (81;24 hours)

Cheung 2009(17)

Two Canadian centers

Hsu 2009(18)

Single center, Taiwan

Holboth 2010

Two centers, Denmark

Bassett 2011(20)

Single center

Buchanan 2014(21)

VA, three centers

Ghaoui 2014(22)

Single center

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Jairath 2014(23)

National, UK

Acutely bleeding, cirrhotic

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Single center

43.2% (81)

64% (210; 12 hours)

90% (210)

22% (210)

70% (210)

89.7% (311)

14.8% (311)

97.4% (311)

83.3% (311; 24 hours))

-

76% (26)

76% (26)

94% (26; 24 hours)

44.6% (177)

74.2% (177)

93.2% (177; 24 hours)

59% (76)

-

-

46% (76); 24 hours

63.5% (63)

37.7% (114)

59.3% (113)

74.8% 24hours (119)

39.1% (69)

76.8% (69)

76.9% (78), 24 hours

44.1% (569)

66% (569; 24 hours). 20%; 12 hours

81.5% (177)

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Kijsirichareanchai

Stable, acutely bleeding, cirrhotic Acutely bleeding, cirrhotic Acutely bleeding, cirrhotic Acutely bleeding, cirrhotic Acutely bleeding, cirrhotic Acutely bleeding, cirrhotic Acutely bleeding, cirrhotic

87% (69)*

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Seo 2007

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Setting

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Patients

Band ligation or sclerotherapy % (N)

Paper (Ref)

87.0% (46)

64% (569)

27% (144)

UK = United Kingdom, VA = Veteran’s administration. * Not that definitions change across studies: Timely endoscopy varies from 12-24 hours; timely antibiotics or octreotide for actively bleeding patients varices from being provided prior to the endoscopy to any time during the admission; and appropriate variceal treatment is variably described as band ligation or sclerotherapy within 1 week, banding or sclerotherapy during the index endoscopy or banding, not sclerotherapy, during the index procedure.

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VA, single center Two centers Single center

30-day readmissions % (N) 19.7% (197) 20.0% (554) 37% (402)

Singal 201342

Single center

27% (1,291)

Setting

Ghaoui 201443 Siddiqui 201444* Tapper 201545

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Paper (Ref) Bini 200140 Berman 201141 Volk 201233

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Table 4: Studies Assessing Early Readmissions after Hospitalization

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Single center 6.3% (128) California state 26% (90,326) database Single center 26.6% (1,358) 14 North American 53% (1,013) – 90-day readmits Bajaj 201534 centers VA = Veteran’s administration. *Abstract

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Supplementary Figure 1: Search strategy yield

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References

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1. Wong V, Wreghitt TG, Alexander G. Prospective study of hepatitis B vaccination in patients with chronic hepatitis C. BMJ: British Medical Journal 1996;312:1336. 2. Arguedas MR, McGuire BM, Fallon MB. Implementation of vaccination in patients with cirrhosis. Dig Dis Sci 2002;47:384-387. 3. Jacobs RJ, Meyerhoff AS, Saab S. Immunization needs of chronic liver disease patients seen in primary care versus specialist settings. Dig Dis Sci 2005;50:1525-1531. 4. Shim M, Khaykis I, Park J, Bini EJ. Susceptibility to hepatitis A in patients with chronic liver disease due to hepatitis C virus infection: missed opportunities for vaccination. Hepatology 2005;42:688695. 5. Hachem CY, Kramer JR, Kanwal F, El-Serag HB. Hepatitis vaccination in patients with hepatitis C: practice and validation of codes at a large Veterans Administration Medical Centre. Aliment Pharmacol Ther 2008;28:1078-1087. 6. Hernandez B, Hasson NK, Cheung R. Hepatitis C Performance Measure on Hepatitis A and B Vaccination: Missed Opportunities&quest. The American journal of gastroenterology 2009;104:19611967. 7. Kanwal F, Schnitzler MS, Bacon BR, Hoang T, Buchanan PM, Asch SM. Quality of care in patients with chronic hepatitis C virus infection: a cohort study. Ann Intern Med 2010;153:231-239. 8. Kramer JR, Hachem CY, Kanwal F, Mei M, El-Serag HB. Meeting vaccination quality measures for hepatitis A and B virus in patients with chronic hepatitis C infection. Hepatology 2011;53:42-52. 9. Thudi K, Yadav D, Sweeney K, Behari J. Physicians infrequently adhere to hepatitis vaccination guidelines for chronic liver disease. 2013. 10. Scaglione SJ, Shepard K, Adams W, Pappano E, Ali AM, Cheung A, Naravadi VVR, et al. Preventative Care Quality Indicator Adherence and Factors Affecting Quality Care Measurement in Patients with Cirrhosis: A Single-centered Study. In: HEPATOLOGY; 2014: WILEY-BLACKWELL 111 RIVER ST, HOBOKEN 07030-5774, NJ USA; 2014. p. 958A-959A. 11. Kanwal F, Kramer JR, Buchanan P, Asch SM, Assioun Y, Bacon BR, Li J, et al. The quality of care provided to patients with cirrhosis and ascites in the Department of Veterans Affairs. Gastroenterology 2012;143:70-77. 12. Abed J, Mankal P, Hussain S, Agrawal N, Asaad A, Munot K, Aristy J, et al. QI Project: Management of Ascites to Rule Out Spontaneous Bacterial Peritonitis (SBP) in Cirrhotic Patients at St. Luke's-Roosevelt Hospital. In: AMERICAN JOURNAL OF GASTROENTEROLOGY; 2013: NATURE PUBLISHING GROUP 75 VARICK ST, 9TH FLR, NEW YORK, NY 10013-1917 USA; 2013. p. S116-S117. 13. Brooling J, Ghaoui R, Lindenauer PK, Friderici J, Lagu T. Use of paracentesis in hospitalized patients with decompensated cirrhosis and ascites: opportunities for quality improvement. J Hosp Med 2014;9:797-799. 14. Orman ES, Hayashi PH, Bataller R, Barritt AS. Paracentesis is associated with reduced mortality in patients hospitalized with cirrhosis and ascites. Clinical Gastroenterology and Hepatology 2014;12:496503. e491. 15. Le S, Spelman T, Chong C-P, Ha P, Sahhar L, Lim J, He T, et al. Could Adherence to Quality of Care Indicators for Hospitalized Patients With Cirrhosis-Related Ascites Improve Clinical Outcomes&quest. The American journal of gastroenterology 2016. 16. Singh H, Targownik L, Ward G, Minuk G, Bernstein C. An assessment of endoscopic and concomitant management of acute variceal bleeding at a tertiary care centre. Canadian journal of gastroenterology 2007;21:85.

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17. Cheung J, Soo I, Bastiampillai R, Zhu Q, Ma M. Urgent vs. non-urgent endoscopy in stable acute variceal bleeding. The American journal of gastroenterology 2009;104:1125-1129. 18. Hsu YC, Chung CS, Tseng CH, Lin TL, Liou JM, Wu MS, Hu FC, et al. Delayed endoscopy as a risk factor for in-hospital mortality in cirrhotic patients with acute variceal hemorrhage. Journal of gastroenterology and hepatology 2009;24:1294-1299. 19. Kijsirichareanchai K, Ngamruengphong S, Rakvit A, Nugent K, Parupudi S. The utilization of standardized order sets using AASLD guidelines for patients with suspected cirrhosis and acute gastrointestinal bleeding. Quality Management in Healthcare 2013;22:146-151. 20. Bassett JT, Volk ML. Can Quality of Care for Patients with Cirrhosis Be Measured? Digestive Diseases and Sciences 2011;56:3488-3491. 21. Buchanan PM, Kramer JR, El-Serag HB, Asch SM, Assioun Y, Bacon BR, Kanwal F. The quality of care provided to patients with varices in the department of veterans affairs. Am J Gastroenterol 2014;109:934-940. 22. Ghaoui R, Friderici J, Visintainer P, Lindenauer PK, Lagu T, Desilets D. Measurement of the quality of care of patients admitted with decompensated cirrhosis. Liver Int 2014;34:204-210. 23. Jairath V, Rehal S, Logan R, Kahan B, Hearnshaw S, Stanworth S, Travis S, et al. Acute variceal haemorrhage in the United Kingdom: patient characteristics, management and outcomes in a nationwide audit. Digestive and Liver Disease 2014;46:419-426.