Efficacy of Neonatal HBV Vaccination on Liver Cancer and Other Liver Diseases over 30-Year Follow-up of the Qidong Hepatitis B Intervention Study: A Cluster Randomized Controlled Trial

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Background:
Neonatal hepatitis B vaccination has been implemented worldwide to prevent hepatitis B virus (HBV) infections. Its long-term protective efficacy on primary liver cancer (PLC) and other liver diseases has not been fully examined.

Methods and Findings:
The Qidong Hepatitis B Intervention Study, a population-based, cluster randomized, controlled trial between 1985 and 1990 in Qidong, China, included 39,292 newborns who were randomly assigned to the vaccination group in which 38,366 participants completed the HBV vaccination series and 34,441 newborns who were randomly assigned to the control group in which the participants received neither a vaccine nor a placebo. However, 23,368 (67.8%) participants in the control group received catch-up vaccination at age 10–14 years. By December 2013, a total of 3,895 (10.2%) in the vaccination group and 3,898 (11.3%) in the control group were lost to follow-up. Information on PLC incidence and liver disease mortality were collected through linkage of all remaining cohort members to a well-established population-based tumor registry until December 31, 2013. Two cross-sectional surveys on HBV surface antigen (HBsAg) seroprevalence were conducted in 1996–2000 and 2008–2012. The participation rates of the two surveys were 57.5% (21,770) and 50.7% (17,204) in the vaccination group and 36.3% (12,184) and 58.6% (17,395) in the control group, respectively. Using intention-to-treat analysis, we found that the incidence rate of PLC and the mortality rates of severe end-stage liver diseases and infant fulminant hepatitis were significantly lower in the vaccination group than the control group with efficacies of 84% (95% CI 23%–97%), 70% (95% CI 15%–89%), and 69% (95% CI 34%–85%), respectively. The estimated efficacy of catch-up vaccination on HBsAg seroprevalence in early adulthood was 21% (95% CI 10%–30%), substantially weaker than that of the neonatal vaccination (72%, 95% CI 68%–75%). Receiving a booster at age 10–14 years decreased HBsAg seroprevalence if participants were born to HBsAg-positive mothers (hazard ratio [HR] = 0.68, 95% CI 0.47–0.97). Limitations to consider in interpreting the study results include the small number of individuals with PLC, participants lost to follow-up, and the large proportion of participants who did not provide serum samples at follow-up.

Conclusions:
Neonatal HBV vaccination was found to significantly decrease HBsAg seroprevalence in childhood through young adulthood and subsequently reduce the risk of PLC and other liver diseases in young adults in rural China. The findings underscore the importance of neonatal HBV vaccination. Our results also suggest that an adolescence booster should be considered in individuals born to HBsAg-positive mothers and who have completed the HBV neonatal vaccination series.

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Vyšlo v časopise: Efficacy of Neonatal HBV Vaccination on Liver Cancer and Other Liver Diseases over 30-Year Follow-up of the Qidong Hepatitis B Intervention Study: A Cluster Randomized Controlled Trial. PLoS Med 11(12): e32767. doi:10.1371/journal.pmed.1001774
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1001774

Souhrn

Zdroje

1. HyamsKC (1995) Risks of chronicity following acute hepatitis B virus infection: a review. Clin Infect Dis 20: 992–1000.

2. ChangMH (2007) Hepatitis B virus infection. Semin Fetal Neonatal Med 12: 160–167.

3. Finelli L, Bell BP (2011) Chapter 4: Hepatitis B. VPD survellance manual, 5th edition: 4-1-13.

4. ChangMH, LeeCY, ChenDS, HsuHC, LaiMY (1987) Fulminant hepatitis in children in Taiwan: the important role of hepatitis B virus. J Pediatr 111: 34–39.

5. McMahonBJ (2009) The natural history of chronic hepatitis B virus infection. Hepatology 49: S45–55.

6. JemalA, BrayF, CenterMM, FerlayJ, WardE, et al. (2011) Global cancer statistics. CA Cancer J Clin 61: 69–90.

7. PoonD, AndersonBO, ChenLT, TanakaK, LauWY, et al. (2009) Management of hepatocellular carcinoma in Asia: consensus statement from the Asian Oncology Summit 2009. Lancet Oncol 10: 1111–1118.

8. ChenDS (2009) Hepatitis B vaccination: the key towards elimination and eradication of hepatitis B. J Hepatol 50: 805–816.

9. ZanettiAR, Van DammeP, ShouvalD (2008) The global impact of vaccination against hepatitis B: a historical overview. Vaccine 26: 6266–6273.

10. ZuckermanAJ, SunTT, LinsellA, StjernswardJ (1983) Prevention of primary liver cancer-report on a meeting of a W.H.O. Scientific Group. Lancet 1: 463–465.

11. ChangMH, YouSL, ChenCJ, LiuCJ, LeeCM, et al. (2009) Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: a 20-year follow-up study. J Natl Cancer Inst 101: 1348–1355.

12. ChiangCJ, YangYW, YouSL, LaiMS, ChenCJ (2013) Thirty-year outcomes of the national hepatitis B immunization program in Taiwan. JAMA 310: 974–976.

13. ChienYC, JanCF, ChiangCJ, KuoHS, YouSL, et al. (2014) Incomplete hepatitis B immunization, maternal carrier status, and increased risk of liver diseases: a 20-year cohort study of 3.8 million vaccinees. Hepatology 60: 125–132.

14. McMahonBJ, BulkowLR, SingletonRJ, WilliamsJ, SnowballM, et al. (2011) Elimination of hepatocellular carcinoma and acute hepatitis B in children 25 years after a hepatitis B newborn and catch-up immunization program. Hepatology 54: 801–807.

15. GwackJ, ParkSK, LeeEH, ParkB, ChoiY, et al. (2011) Hepatitis B vaccination and liver cancer mortality reduction in Korean children and adolescents. Asian Pac J Cancer Prev 12: 2205–2208.

16. WuQJ, VogtmannE, ZhangW, XieL, YangWS, et al. (2012) Cancer incidence among adolescents and young adults in urban Shanghai, 1973-2005. PLoS One 7: e42607.

17. SunZ, ChenT, ThorgeirssonSS, ZhanQ, ChenJ, et al. (2013) Dramatic reduction of liver cancer incidence in young adults: 28 year follow-up of etiological interventions in an endemic area of China. Carcinogenesis 34: 1800–1805.

18. ChenJG, KenslerTW (2013) Changing rates for liver and lung cancer in Qidong, China. Chem Res Toxicol 27: 3–6.

19. ChenJG, ZhuJ, ParkinDM, ZhangYH, LuJH, et al. (2006) Trends in the incidence of cancer in Qidong, China, 1978-2002. Int J Cancer 119: 1447–1454.

20. GaoJ, XieL, ChenWQ, ZhangSW, WuQJ, et al. (2013) Rural-urban, sex variations, and time trend of primary liver cancer incidence in China, 1988-2005. Eur J Cancer Prev 22: 448–454.

21. SunZ, MingL, ZhuX, LuJ (2002) Prevention and control of hepatitis B in China. J Med Virol 67: 447–450.

22. SunZ, ZhuY, StjernswardJ, HillemanM, CollinsR, et al. (1991) Design and compliance of HBV vaccination trial on newborns to prevent hepatocellular carcinoma and 5-year results of its pilot study. Cancer Detect Prev 15: 313–318.

23. Chen JG (2013) Qidong Cancer Registration System Cancer Cancer in Qidong, China. Chen JG, editor. Beijing: Military Medical Science Press. pp9-23.

24. Parkin DM, Whelan SL, Ferlay J, Teppo L, Thomas DB (2002) Cancer incidence in five continents, vol. VIII. Sci Publ number 155. Lyon: IARC. pp 212–231.

25. SarinSK, KumarA, AlmeidaJA, ChawlaYK, FanST, et al. (2009) Acute-on-chronic liver failure: consensus recommendations of the Asian Pacific Association for the study of the liver (APASL). Hepatol Int 3: 269–282.

26. Wu M, Shen F (2010) Liver cancer. 3rd edition.. Beijing: Peking University Medical Press pp.327.

27. WiwanitkitV (2005) Hepatitis virus B is not a risk factor in hepatoblastoma patients. Asian Pac J Cancer Prev 6: 213–214.

28. ChangMH, ShauWY, ChenCJ, WuTC, KongMS, et al. (2000) Hepatitis B vaccination and hepatocellular carcinoma rates in boys and girls. JAMA 284: 3040–3042.

29. KenslerTW, QianGS, ChenJG, GroopmanJD (2003) Translational strategies for cancer prevention in liver. Nat Rev Cancer 3: 321–329.

30. XiaGL, LiuCB, CaoHL, BiSL, ZhanMY, et al. (1996) Prevalence of hepatitis B and C virus infections in the general Chinese population: results from a nationwide cross-sectional seroepidemiologic study of hepatitis A, B,C, D and E virus infections in China, 1992. Int Hepatol Commun 5: 12.

31. ZhangHW, YinJH, LiYT, LiCZ, RenH, et al. (2008) Risk factors for acute hepatitis B and its progression to chronic hepatitis in Shanghai, China. Gut 57: 1713–1720.

32. HuttonDW, SoSK, BrandeauML (2010) Cost-effectiveness of nationwide hepatitis B catch-up vaccination among children and adolescents in China. Hepatology 51: 405–414.

33. HarpazR, McMahonBJ, MargolisHS, ShapiroCN, HavronD, et al. (2000) Elimination of new chronic hepatitis B virus infections: results of the Alaska immunization program. J Infect Dis 181: 413–418.

34. ChuCM, LiawYF (2007) HBsAg seroclearance in asymptomatic carriers of high endemic areas: appreciably high rates during a long-term follow-up. Hepatology 45: 1187–1192.

35. LiuJ, YangHI, LeeMH, LuSN, JenCL, et al. (2010) Incidence and determinants of spontaneous hepatitis B surface antigen seroclearance: a community-based follow-up study. Gastroenterology 139: 474–482.

36. YalcinK, AcarM, DegertekinH (2003) Specific hepatitis B vaccine therapy in inactive HBsAg carriers: a randomized controlled trial. Infection 31: 221–225.

37. LuCY, ChiangBL, ChiWK, ChangMH, NiYH, et al. (2004) Waning immunity to plasma-derived hepatitis B vaccine and the need for boosters 15 years after neonatal vaccination. Hepatology 40: 1415–1420.

38. ZhuCL, LiuP, ChenT, NiZ, LuLL, et al. (2011) Presence of immune memory and immunity to hepatitis B virus in adults after neonatal hepatitis B vaccination. Vaccine 29: 7835–7841.

39. RomanoL, CarsettiR, TozziAE, MeleA, ZanettiAR (2014) Chronic hepatitis B infection in adolescents vaccinated at birth: an alarm bell in favor of the need for a booster? Hepatology 59: 349.

40. NiYH, HuangLM, ChangMH, YenCJ, LuCY, et al. (2007) Two decades of universal hepatitis B vaccination in taiwan: impact and implication for future strategies. Gastroenterology 132: 1287–1293.

41. WenWH, ChangMH, ZhaoLL, NiYH, HsuHY, et al. (2013) Mother-to-infant transmission of hepatitis B virus infection: significance of maternal viral load and strategies for intervention. J Hepatol 59: 24–30.

42. LuL, ChenB, WangJ, WangD, JiY, et al. (2014) Maternal transmission risk and antibody levels against hepatitis B virus e antigen in pregnant women. Int J Infect Dis 28: 41–4.

43. LuFM, ZhuangH (2009) Management of hepatitis B in China. Chin Med J (Engl) 122: 3–4.

44. BeathSV, BoxallEH, WatsonRM, TarlowMJ, KellyDA (1992) Fulminant hepatitis B in infants born to anti-HBe hepatitis B carrier mothers. BMJ 304: 1169–1170.

45. SunZ, LuP, GailMH, PeeD, ZhangQ, et al. (1999) Increased risk of hepatocellular carcinoma in male hepatitis B surface antigen carriers with chronic hepatitis who have detectable urinary aflatoxin metabolite M1. Hepatology 30: 379–383.

46. MingL, ThorgeirssonSS, GailMH, LuP, HarrisCC, et al. (2002) Dominant role of hepatitis B virus and cofactor role of aflatoxin in hepatocarcinogenesis in Qidong, China. Hepatology 36: 1214–1220.

47. ChuangSC, La VecchiaC, BoffettaP (2009) Liver cancer: descriptive epidemiology and risk factors other than HBV and HCV infection. Cancer Lett 286: 9–14.

48. MastEE, MahoneyFJ, AlterMJ, MargolisHS (1998) Progress toward elimination of hepatitis B virus transmission in the United States. Vaccine 16 Suppl: S48-51

49. Ramachandran S, Purdy MA, Xia GL, Campo DS, Dimitrova ZE, et al. (2014) Recent population expansions of hepatitis B virus in the United States. J Virol. In press.

50. ArevaloJA, WashingtonAE (1988) Cost-effectiveness of prenatal screening and immunization for hepatitis B virus. JAMA 259: 365–369.