Skip to main content
Top
Published in: BMC Health Services Research 1/2021

Open Access 01-12-2021 | Hepatitis B | Research article

Cost evaluation of PAGE-B risk score guided HCC surveillance in patients with treated chronic hepatitis B

Authors: Martin F. Sprinzl, Christina Feist, Sandra Koch, Wolfgang M. Kremer, Karl J. Lackner, Arndt Weinmann, Peter R. Galle

Published in: BMC Health Services Research | Issue 1/2021

Login to get access

Abstract

Background

The PAGE-B score (Platelet Age GEnder–HBV) selects chronic hepatitis B (cHB) patients showing no relevant 5-year risk for hepatocellular carcinoma (HCC). We, therefore, explored potential cost reduction following the introduction of a PAGE-B tailored ultrasound screening in a single center cohort of cHB patients receiving stable antiviral therapy.

Methods

cHB patients attending throughout the year 2018 were documented. Patients eligible for PAGE-B score were classified into high (≥18 points), intermediate (10–17 points) and low (≤9 points) HCC risk groups. Patients of the low HCC risk group could postpone HCC screening to reduce HCC screening expenses. Full costs for hepatic ultrasound were assessed.

Results

Throughout the year cHB patients (n = 607) attended our clinic, which included PAGE-B eligible patients (n = 227, 37.4%) of whom n = 94 (15.8%) were allocated to the low HCC risk group. Sonographic HCC screening during a median exam time of 12.4 min (IQR 9.2–17.2) resulted in total costs of 22.82 Euro/exam. Additional opportunistic expenses caused by patient’s lost earnings or productivity were 15.6–17.5 €/exam and 26.7 €/exam, respectively. Following a PAGE-B tailored HCC screening at our institution annual full costs for cHB patients could be reduced by 15.51%, which equals a cost reduction by 1.91% for our total sonography unit. In comparison, 1.35% up to 7.65% of HBV-infected patients of Caucasian descent could postpone HCC screening according to population-based estimates from Germany.

Conclusions

PAGE-B risk score adapted screening for HCC is an efficient and cost neutral tool to reduce costs for sonography in Caucasian patients with chronic hepatitis B receiving antiviral treatment.
Appendix
Available only for authorised users
Literature
1.
go back to reference El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology. 2012;142(6):1264–73 e1261.CrossRef El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology. 2012;142(6):1264–73 e1261.CrossRef
2.
go back to reference Costentin CE, Layese R, Bourcier V, Cagnot C, Marcellin P, Guyader D, et al. Compliance with hepatocellular carcinoma surveillance guidelines associated with increased Lead-time adjusted survival of patients with compensated viral cirrhosis: a multi-center cohort study. Gastroenterology. 2018;155(2):431–42 e410.CrossRef Costentin CE, Layese R, Bourcier V, Cagnot C, Marcellin P, Guyader D, et al. Compliance with hepatocellular carcinoma surveillance guidelines associated with increased Lead-time adjusted survival of patients with compensated viral cirrhosis: a multi-center cohort study. Gastroenterology. 2018;155(2):431–42 e410.CrossRef
3.
go back to reference European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the L: EASL 2017 clinical practice guidelines on the management of hepatitis B virus infection. J Hepatol. 2017;67(2):370–98.CrossRef European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the L: EASL 2017 clinical practice guidelines on the management of hepatitis B virus infection. J Hepatol. 2017;67(2):370–98.CrossRef
4.
go back to reference Cornberg M, Protzer U, Petersen J, Wedemeyer H, Berg T, Jilg W, et al. Prophylaxis, diagnosis and therapy of hepatitis B virus infection - the German guideline. Z Gastroenterol. 2011;49(7):871–930.CrossRef Cornberg M, Protzer U, Petersen J, Wedemeyer H, Berg T, Jilg W, et al. Prophylaxis, diagnosis and therapy of hepatitis B virus infection - the German guideline. Z Gastroenterol. 2011;49(7):871–930.CrossRef
5.
go back to reference Liaw YF, Sung JJ, Chow WC, Farrell G, Lee CZ, Yuen H, et al. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med. 2004;351(15):1521–31.CrossRef Liaw YF, Sung JJ, Chow WC, Farrell G, Lee CZ, Yuen H, et al. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med. 2004;351(15):1521–31.CrossRef
6.
go back to reference Hosaka T, Suzuki F, Kobayashi M, Seko Y, Kawamura Y, Sezaki H, et al. Long-term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology. 2013;58(1):98–107.CrossRef Hosaka T, Suzuki F, Kobayashi M, Seko Y, Kawamura Y, Sezaki H, et al. Long-term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology. 2013;58(1):98–107.CrossRef
7.
go back to reference Cho JY, Paik YH, Sohn W, Cho HC, Gwak GY, Choi MS, et al. Patients with chronic hepatitis B treated with oral antiviral therapy retain a higher risk for HCC compared with patients with inactive stage disease. Gut. 2014;63(12):1943–50.CrossRef Cho JY, Paik YH, Sohn W, Cho HC, Gwak GY, Choi MS, et al. Patients with chronic hepatitis B treated with oral antiviral therapy retain a higher risk for HCC compared with patients with inactive stage disease. Gut. 2014;63(12):1943–50.CrossRef
8.
go back to reference Papatheodoridis G, Dalekos G, Sypsa V, Yurdaydin C, Buti M, Goulis J, et al. PAGE-B predicts the risk of developing hepatocellular carcinoma in Caucasians with chronic hepatitis B on 5-year antiviral therapy. J Hepatol. 2016;64(4):800–6.CrossRef Papatheodoridis G, Dalekos G, Sypsa V, Yurdaydin C, Buti M, Goulis J, et al. PAGE-B predicts the risk of developing hepatocellular carcinoma in Caucasians with chronic hepatitis B on 5-year antiviral therapy. J Hepatol. 2016;64(4):800–6.CrossRef
9.
go back to reference Riveiro-Barciela M, Tabernero D, Calleja JL, Lens S, Manzano ML, Rodriguez FG, et al. Effectiveness and safety of Entecavir or Tenofovir in a Spanish cohort of chronic hepatitis B patients: validation of the page-B score to predict hepatocellular carcinoma. Dig Dis Sci. 2017;62(3):784–93.CrossRef Riveiro-Barciela M, Tabernero D, Calleja JL, Lens S, Manzano ML, Rodriguez FG, et al. Effectiveness and safety of Entecavir or Tenofovir in a Spanish cohort of chronic hepatitis B patients: validation of the page-B score to predict hepatocellular carcinoma. Dig Dis Sci. 2017;62(3):784–93.CrossRef
10.
go back to reference Brouwer WP, van der Meer AJP, Boonstra A, Plompen EPC, Pas SD, de Knegt RJ, et al. Prediction of long-term clinical outcome in a diverse chronic hepatitis B population: role of the PAGE-B score. J Viral Hepat. 2017;24(11):1023–31.CrossRef Brouwer WP, van der Meer AJP, Boonstra A, Plompen EPC, Pas SD, de Knegt RJ, et al. Prediction of long-term clinical outcome in a diverse chronic hepatitis B population: role of the PAGE-B score. J Viral Hepat. 2017;24(11):1023–31.CrossRef
11.
go back to reference European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the L: EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018;69(1):182–236.CrossRef European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the L: EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018;69(1):182–236.CrossRef
15.
go back to reference Johnson RW, Schaner SG. Value of unpaid activities by older americans tops $160 billion per year. In: The retirement project. Vol. 2. Washington: The Urban Institute; 2005. Johnson RW, Schaner SG. Value of unpaid activities by older americans tops $160 billion per year. In: The retirement project. Vol. 2. Washington: The Urban Institute; 2005.
18.
go back to reference Huetter ML, Fuchs M, Hanle MM, Mason RA, Akinli AS, Imhof A, et al. Prevalence of risk factors for liver disease in a random population sample in southern Germany. Z Gastroenterol. 2014;52(6):558–63.CrossRef Huetter ML, Fuchs M, Hanle MM, Mason RA, Akinli AS, Imhof A, et al. Prevalence of risk factors for liver disease in a random population sample in southern Germany. Z Gastroenterol. 2014;52(6):558–63.CrossRef
19.
go back to reference Wolffram I, Petroff D, Batz O, Jedrysiak K, Kramer J, Tenckhoff H, et al. Prevalence of elevated ALT values, HBsAg, and anti-HCV in the primary care setting and evaluation of guideline defined hepatitis risk scenarios. J Hepatol. 2015;62(6):1256–64.CrossRef Wolffram I, Petroff D, Batz O, Jedrysiak K, Kramer J, Tenckhoff H, et al. Prevalence of elevated ALT values, HBsAg, and anti-HCV in the primary care setting and evaluation of guideline defined hepatitis risk scenarios. J Hepatol. 2015;62(6):1256–64.CrossRef
20.
go back to reference Poethko-Muller C, Zimmermann R, Hamouda O, Faber M, Stark K, Ross RS, et al. Epidemiology of hepatitis a, B, and C among adults in Germany: results of the German health interview and examination survey for adults (DEGS1). Bundesgesundheitsbl Gesundheitsforsch Gesundheitsschutz. 2013;56(5–6):707–15.CrossRef Poethko-Muller C, Zimmermann R, Hamouda O, Faber M, Stark K, Ross RS, et al. Epidemiology of hepatitis a, B, and C among adults in Germany: results of the German health interview and examination survey for adults (DEGS1). Bundesgesundheitsbl Gesundheitsforsch Gesundheitsschutz. 2013;56(5–6):707–15.CrossRef
21.
go back to reference Thierfelder W, Hellenbrand W, Meisel H, Schreier E, Dortschy R. Prevalence of markers for hepatitis a, B and C in the German population. Results of the German National Health Interview and examination survey 1998. Eur J Epidemiol. 2001;17(5):429–35.CrossRef Thierfelder W, Hellenbrand W, Meisel H, Schreier E, Dortschy R. Prevalence of markers for hepatitis a, B and C in the German population. Results of the German National Health Interview and examination survey 1998. Eur J Epidemiol. 2001;17(5):429–35.CrossRef
22.
go back to reference Fischer C, Mauss S, Zehnter E, Bokemeyer B, Heyne R, Huppe D. Epidemiology and clinical characteristics of patients with chronic hepatitis B (CHB) in Germany - results of a nationwide cross-sectional study. Z Gastroenterol. 2012;50(1):22–9.CrossRef Fischer C, Mauss S, Zehnter E, Bokemeyer B, Heyne R, Huppe D. Epidemiology and clinical characteristics of patients with chronic hepatitis B (CHB) in Germany - results of a nationwide cross-sectional study. Z Gastroenterol. 2012;50(1):22–9.CrossRef
23.
go back to reference Tan M, Bhadoria AS, Cui F, Tan A, Van Holten J, Easterbrook P, et al. Estimating the proportion of people with chronic hepatitis B virus infection eligible for hepatitis B antiviral treatment worldwide: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2021;6(2):106–19.CrossRef Tan M, Bhadoria AS, Cui F, Tan A, Van Holten J, Easterbrook P, et al. Estimating the proportion of people with chronic hepatitis B virus infection eligible for hepatitis B antiviral treatment worldwide: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2021;6(2):106–19.CrossRef
26.
go back to reference Raffetti E, Fattovich G, Donato F. Incidence of hepatocellular carcinoma in untreated subjects with chronic hepatitis B: a systematic review and meta-analysis. Liver Int. 2016;36(9):1239–51.CrossRef Raffetti E, Fattovich G, Donato F. Incidence of hepatocellular carcinoma in untreated subjects with chronic hepatitis B: a systematic review and meta-analysis. Liver Int. 2016;36(9):1239–51.CrossRef
27.
go back to reference Yip TC, Wong GL, Wong VW, Tse YK, Liang LY, Hui VW, et al. Reassessing the accuracy of PAGE-B-related scores to predict hepatocellular carcinoma development in patients with chronic hepatitis B. J Hepatol. 2020;72(5):847–54.CrossRef Yip TC, Wong GL, Wong VW, Tse YK, Liang LY, Hui VW, et al. Reassessing the accuracy of PAGE-B-related scores to predict hepatocellular carcinoma development in patients with chronic hepatitis B. J Hepatol. 2020;72(5):847–54.CrossRef
28.
go back to reference Zhang BH, Yang BH, Tang ZY. Randomized controlled trial of screening for hepatocellular carcinoma. J Cancer Res Clin Oncol. 2004;130(7):417–22.CrossRef Zhang BH, Yang BH, Tang ZY. Randomized controlled trial of screening for hepatocellular carcinoma. J Cancer Res Clin Oncol. 2004;130(7):417–22.CrossRef
29.
go back to reference Choi DT, Kum HC, Park S, Ohsfeldt RL, Shen Y, Parikh ND, et al. Hepatocellular carcinoma screening is associated with increased survival of patients with cirrhosis. Clin Gastroenterol Hepatol. 2019;17(5):976–87 e974.CrossRef Choi DT, Kum HC, Park S, Ohsfeldt RL, Shen Y, Parikh ND, et al. Hepatocellular carcinoma screening is associated with increased survival of patients with cirrhosis. Clin Gastroenterol Hepatol. 2019;17(5):976–87 e974.CrossRef
30.
go back to reference Yabroff KR, Lawrence WF, Clauser S, Davis WW, Brown ML. Burden of illness in cancer survivors: findings from a population-based national sample. J Natl Cancer Inst. 2004;96(17):1322–30.CrossRef Yabroff KR, Lawrence WF, Clauser S, Davis WW, Brown ML. Burden of illness in cancer survivors: findings from a population-based national sample. J Natl Cancer Inst. 2004;96(17):1322–30.CrossRef
31.
go back to reference Lang K, Danchenko N, Gondek K, Shah S, Thompson D. The burden of illness associated with hepatocellular carcinoma in the United States. J Hepatol. 2009;50(1):89–99.CrossRef Lang K, Danchenko N, Gondek K, Shah S, Thompson D. The burden of illness associated with hepatocellular carcinoma in the United States. J Hepatol. 2009;50(1):89–99.CrossRef
32.
go back to reference Tzartzeva K, Obi J, Rich NE, Parikh ND, Marrero JA, Yopp A, et al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology. 2018;154(6):1706–18 e1701.CrossRef Tzartzeva K, Obi J, Rich NE, Parikh ND, Marrero JA, Yopp A, et al. Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis. Gastroenterology. 2018;154(6):1706–18 e1701.CrossRef
33.
go back to reference Mahajan V, Jin M, Le MH, Nguyen N, Wong CR, Leong J, et al. Tu1672 low rates of antiviral therapy in chronic hepatitis B (CHB) patients and its geographic variation: a systematic review and meta-analysis of 13 studies and 31,342 patients. Gastroenterology. 2016;150(4):S1163–4.CrossRef Mahajan V, Jin M, Le MH, Nguyen N, Wong CR, Leong J, et al. Tu1672 low rates of antiviral therapy in chronic hepatitis B (CHB) patients and its geographic variation: a systematic review and meta-analysis of 13 studies and 31,342 patients. Gastroenterology. 2016;150(4):S1163–4.CrossRef
34.
go back to reference Schuler A, Reuss J, Delorme S, Hagendorff A, Giesel F. Costs of clinical ultrasound examinations - an economical cost calculation and analysis. Ultraschall Med. 2010;31(4):379–86.CrossRef Schuler A, Reuss J, Delorme S, Hagendorff A, Giesel F. Costs of clinical ultrasound examinations - an economical cost calculation and analysis. Ultraschall Med. 2010;31(4):379–86.CrossRef
35.
go back to reference Reuss J, Weiss H, Wanner T, Leser HG. Time requirements of medical and non-medical personnel for ultrasound studies. Ultraschall Med. 1998;19(3):126–9.CrossRef Reuss J, Weiss H, Wanner T, Leser HG. Time requirements of medical and non-medical personnel for ultrasound studies. Ultraschall Med. 1998;19(3):126–9.CrossRef
36.
go back to reference Teichgraber UK, Benter T, Kluhs L, Schroder RJ, Hidajat N, Dorken B, et al. Project graph technique for time management in abdominal ultrasound evaluations. Ultraschall Med. 1999;20(6):236–41.CrossRef Teichgraber UK, Benter T, Kluhs L, Schroder RJ, Hidajat N, Dorken B, et al. Project graph technique for time management in abdominal ultrasound evaluations. Ultraschall Med. 1999;20(6):236–41.CrossRef
37.
go back to reference Glied S. Estimating the indirect cost of illness: an assessment of the forgone earnings approach. Am J Public Health. 1996;86(12):1723–8.CrossRef Glied S. Estimating the indirect cost of illness: an assessment of the forgone earnings approach. Am J Public Health. 1996;86(12):1723–8.CrossRef
39.
go back to reference Bundesamt S: Bevölkerung (Zensus), nach Bundesländer, Stichtag, Nationalität, Altersgruppen. 2018. Bundesamt S: Bevölkerung (Zensus), nach Bundesländer, Stichtag, Nationalität, Altersgruppen. 2018.
40.
go back to reference Bundesamt S. Bevölkerung in Privathaushalten 2017 nach Migrationshintergrund - Nettoeinkommen; 2018. Bundesamt S. Bevölkerung in Privathaushalten 2017 nach Migrationshintergrund - Nettoeinkommen; 2018.
41.
go back to reference Sonneveld MJ, Brouwer WP, de Man RA. Hepatocellular carcinoma risk stratification in HBV cirrhosis: time to turn the page? J Hepatol. 2020;73(3):728–9.CrossRef Sonneveld MJ, Brouwer WP, de Man RA. Hepatocellular carcinoma risk stratification in HBV cirrhosis: time to turn the page? J Hepatol. 2020;73(3):728–9.CrossRef
42.
go back to reference Kim JH, Kim YD, Lee M, Jun BG, Kim TS, Suk KT, et al. Modified PAGE-B score predicts the risk of hepatocellular carcinoma in Asians with chronic hepatitis B on antiviral therapy. J Hepatol. 2018;69(5):1066–73.CrossRef Kim JH, Kim YD, Lee M, Jun BG, Kim TS, Suk KT, et al. Modified PAGE-B score predicts the risk of hepatocellular carcinoma in Asians with chronic hepatitis B on antiviral therapy. J Hepatol. 2018;69(5):1066–73.CrossRef
43.
go back to reference Chayanupatkul M, Omino R, Mittal S, Kramer JR, Richardson P, Thrift AP, et al. Hepatocellular carcinoma in the absence of cirrhosis in patients with chronic hepatitis B virus infection. J Hepatol. 2017;66(2):355–62.CrossRef Chayanupatkul M, Omino R, Mittal S, Kramer JR, Richardson P, Thrift AP, et al. Hepatocellular carcinoma in the absence of cirrhosis in patients with chronic hepatitis B virus infection. J Hepatol. 2017;66(2):355–62.CrossRef
44.
go back to reference Parikh ND, Singal AG, Hutton DW, Tapper EB. Cost-effectiveness of hepatocellular carcinoma surveillance: an assessment of benefits and harms. Am J Gastroenterol. 2020;115(10):1642–9.CrossRef Parikh ND, Singal AG, Hutton DW, Tapper EB. Cost-effectiveness of hepatocellular carcinoma surveillance: an assessment of benefits and harms. Am J Gastroenterol. 2020;115(10):1642–9.CrossRef
45.
go back to reference Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine. 2012;30(12):2212–9.CrossRef Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine. 2012;30(12):2212–9.CrossRef
46.
go back to reference Davila JA, Weston A, Smalley W, El-Serag HB. Utilization of screening for hepatocellular carcinoma in the United States. J Clin Gastroenterol. 2007;41(8):777–82.CrossRef Davila JA, Weston A, Smalley W, El-Serag HB. Utilization of screening for hepatocellular carcinoma in the United States. J Clin Gastroenterol. 2007;41(8):777–82.CrossRef
47.
go back to reference Selvapatt N, House H, Brown A. Hepatocellular carcinoma surveillance: are we utilizing it? J Clin Gastroenterol. 2016;50(1):e8–e12.CrossRef Selvapatt N, House H, Brown A. Hepatocellular carcinoma surveillance: are we utilizing it? J Clin Gastroenterol. 2016;50(1):e8–e12.CrossRef
Metadata
Title
Cost evaluation of PAGE-B risk score guided HCC surveillance in patients with treated chronic hepatitis B
Authors
Martin F. Sprinzl
Christina Feist
Sandra Koch
Wolfgang M. Kremer
Karl J. Lackner
Arndt Weinmann
Peter R. Galle
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Health Services Research / Issue 1/2021
Electronic ISSN: 1472-6963
DOI
https://doi.org/10.1186/s12913-021-06794-6

Other articles of this Issue 1/2021

BMC Health Services Research 1/2021 Go to the issue