INTRODUCTION
Viral hepatitis is a public health problem in Brazil and worldwide. According to the World Health Organization (WHO), 2 billion people have had contact with the hepatitis B virus (HBV); approximately 5% of these individuals are considered carriers (11. European Association for the Study of Liver. EASL Clinical practice guidelines: management of chronic hepatitis J Hepatol. 2009;50(2):227-42.).
The risk of chronicity after infection is 90% in the newborns of mothers with positive hepatitis B early antigen (HBeAg), 25 to 30% in children under 5 years of age, and less than 5% in adults (22. Daruich J, Gadano A, Fainboim H, Pessoa M, Cheinquer H. Guía Latinoamericana de tratamiento de la hepatitis crónica B. Acta Gastroenterol Latinoam. 2007;37(3):168-77.). Chronic carriers have an increased risk (15 to 40%) of developing cirrhosis, hepatic decompensation, and hepatocellular carcinoma, resulting in 1 million deaths each year (33. McMahon BJ. Natural history of chronic hepatitis B - clinical implications. Medscape J Med. 2008;10(4):91.).
The most effective hepatitis B preventive measure is vaccination. Since 1998, a policy of
universal vaccination has been implemented for children younger than 1 year in Brazil. The policy
was subsequently extended to people younger than 20 years (44. Ministério da Saúde (Brasil). Programa Nacional de Imunizações: 30 anos.
Brasília: Ministério da Saúde. 2003. [acesso em 2010 Fev.] Disponível em: http://www.scribd.com/doc/27663002/Ministerio-Da-Saude.
http://www.scribd.com/doc/27663002/Minis...
). Vaccination was also extended to vulnerable populations (e.g., injected drug users or
healthcare workers) in 2001 and to people up to 29 years of age in 2010 (55. Ministério da Saúde (Brasil). Nota Técnica 89/2010 CGPNI/DEVEP/SVS/MS. Ministério
da Saúde em05/08/2010.). It is estimated that 75% of the under-29 population is vaccinated (66. Ministério da Saúde (Brasil). Portal Brasil. Disponível em: http://www.brasil.gov.br/noticias/arquivos/2012/07/24.
http://www.brasil.gov.br/noticias/arquiv...
).
Because HBV carriers are the source of infection and chronic hepatitis B is a major cause of
cirrhosis and hepatocellular carcinoma, it is important to understand the incidence, prevalence, and
chronification associated with HBV infection (77. Hyams KC. Risks of chronicity following acute hepatitis B virus infection: a
review. Clin Infect Dis. 1995;20(4):992-1000,
http://dx.doi.org/10.1093/clinids/20.4.992.
http://dx.doi.org/10.1093/clinids/20.4.9...
).
The objective of this study was to describe the clinical outcomes of patients with confirmed acute hepatitis B (AHB) in the South region of Brazil in the city of Porto Alegre from 1999 to 2007.
PATIENTS AND METHODS
This retrospective-prospective cohort study was based on secondary data (retrospective data) obtained from the Information System for Notifiable Diseases (SINAN) and primary data collected from patients who completed structured and semi-structured questionnaires (prospective data).
A case was defined as any individual reported to SINAN in Porto Alegre, a city of 1.5 million inhabitants, from January 1999 to December 2007, and who had positive HBsAg and positive immunoglobulin M antibody to the hepatitis B core antigen (anti-HBc IgM). The patients were contacted at their addresses and phone numbers, and the records of individuals whom we were unable to find were checked through the Mortality Information System or the Health Care Unit registers.
After signing informed consent forms, the patients answered questionnaires evaluating epidemiologic data, the risk factors for hepatitis B acquisition and their participation in consultation and preventive measurements (i.e., vaccination). They were asked to supply copies of laboratory tests performed at least 6 months after their AHB diagnoses. If no information could be obtained, serological tests were performed in a Public Health Service unit.
Patients were considered to have resolved hepatitis B if they had negative HBsAg and positive antibodies to the hepatitis B surface antigen (anti-HBs) after 6 months and, in cases of chronic carriers, if they presented with positive HBsAg in the same period (88. Lok AS, Mcmahon BJ. AASLD Practice guideline update. Chronic Hepatitis B: Update 2009. Hepatology. 2009;50:1-36.).
To determine the number of coinfected patients, the authors examined notification forms with information related to coinfection with hepatitis C virus (HCV) and human immunodeficiency virus (HIV).
This study was approved by the Ethics Committee of the Universidade Federal de Ciências da Saúde de Porto Alegre.
In the statistical analysis, Pearson's Chi-squared test was used, with a 5% level of significance.
RESULTS
Between 1999 and 2007, 103 confirmed cases of AHB were reported to SINAN in Porto Alegre: 67 (65%) patients were male, and 77 (74.8%) were aged between 20 and 49 years.
Of the 103 eligible patients, it was possible to identify outcomes in 78 (75.7%) cases: 56 (71.8%) were considered resolved; 11 (14.1%) became chronic carriers; and 11 (14.1%) died. Four (36.4%) of the 11 deaths (5.1% of the 78 evaluated patients) resulted from fulminant hepatitis.
Hepatitis became chronic in patients older than 22 years: 8 of these patients (72.7%) were between 20- and 49-years-old, and 3 (27.3%) were over 50-years-old. The Caucasian race was prevalent, and female patients became chronic carriers more often than males.
Seventeen (16.5%) of the 103 reported patients had associated coinfections: 12 (70.6%) had HIV; 4 (23.5%) had HIV/HCV; and 1 (5.9%) had HCV. There was no association between the type of coinfection and patient outcomes, chronicity, resolutions or deaths (p=0.747). Two of the patients who became chronic carriers were coinfected, 1 with HIV and 1 with HIV/HCV.
DISCUSSION
Since the early 70s, several published studies have evaluated the chronicity of AHB in adult
patients (Table 1) and shown an evolution to chronicity of
up to 12% (99. Barker LF, Murray R. Acquisition of hepatitis-associated antigen. Clinical
features in young adults. JAMA. 1971;216(12):1970-6,
http://dx.doi.org/10.1001/jama.1971.03180380028006.
http://dx.doi.org/10.1001/jama.1971.0318...
10. Beasley RP, Hwang LY, Lin CC, Ko YC, Twu SJ. Incidence of hepatitis among
students at a university in Taiwan. Am J Epidemiol. 1983;117(2):213-22.
11. Ferraz MLG, Yoradjian A, Barbieri A, Figueiredo V, Lopes Neto E, Cruz CN, et al.
Epidemiology of acute hepatitis B in a university hospital in São Paulo. Brazil: retrospective study
of two five-year periods. Sao Paulo Med J. 1998;116(3):1695-9.
12. Gimeno V, Escudero A, Gonzalez R, Serra MA, Del Olmo JA, Wassel A, et al. Acute
hepatitis in heroin addicts: etiologic and follow-up study of 110 cases. Rev Clin Esp.
1989;184(7):360-3.
13. Hoofnagle JH, Seeff LB, Bales ZB, Zimmerman HJ. Type B hepatitis after
transfusion with blood containing antibody to hepatitis B core antigen. N Engl J Med.
1978;298(25):1379-83.
14. Kent GP, Brondum J, Keenlyside RA, LaFazia LM, Scott HD. A large outbreak of
acupuncture-associated hepatitis B. Am J Epidemiol. 1988;127(3):591-8.
15. Kuruüzüm Z, Ozgenç O, Havuk A, Coşkuner A, Ari A, Celenkoğlu N. Rate of
chronicity and time of disappearance of HBsAg following acute hepatitis B. Hepatogastroenterol.
2009;56(90):466-9.
16. Lavarini C, Farci P, Chiaberge E, Veglio V, Giacobbi D, Bedarida G, et al. IgM
antibody against hepatitis B core antigen (IgM anti-HBc): diagnostic and prognostic significance in
acute HBsAg positive hepatitis. Br Med J (Clin Res Ed). 1983;287(6401):1254-6,
http://dx.doi.org/10.1136/bmj.287.6401.1254.
http://dx.doi.org/10.1136/bmj.287.6401.1...
17. McMahon BJ, Alward WL, Hall DB, Heyward WL, Bender TR, Francis DP, et al. Acute
hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent
development of the carrier state. J Infect Dis. 1985;151(4):599-603,
http://dx.doi.org/10.1093/infdis/151.4.599.
http://dx.doi.org/10.1093/infdis/151.4.5...
18. Rinker J, Galambos JT. Prospective study of hepatitis B in thirty-two
inadvertently infected people. Gastroenterology. 1981;81(4):686-91.
19. Roumeliotou A, Tassopoulos N, Richardson SC, Kalafatas P, Papaevangelou G. How
often does chronic liver disease follow acute hepatitis B in adults? Infection. 1985;13(4):174-6,
http://dx.doi.org/10.1007/BF01642806.
http://dx.doi.org/10.1007/BF01642806...
20. Roumeliotou A, Papaevangelou G. Chronic liver disease rarely follows acute
hepatitis B in non-immunocompromised adults. Infection. 1992;20(4):221-3,
http://dx.doi.org/10.1007/BF02033063.
http://dx.doi.org/10.1007/BF02033063...
21. Schomerus H, Wiedmann KH, Dölle W, Peerenboom H, Strohmeyer G, Balzer K, et al.
(+)∼Cyanidanol-3 in the treatment of acute viral hepatitis: a randomized controlled trial.
Hepatology. 1984;4(2):331-5, http://dx.doi.org/10.1002/hep.1840040226.
http://dx.doi.org/10.1002/hep.1840040226...
22. Wiedmann KH, Brating NW, Diao GD, Schomerus H, Dolle W, Berg PA. Serum
inhibitory factors (SIF) are of prognostic value in acute viral hepatitis. Lancet.
1985;1(8424):309-12, http://dx.doi.org/10.1016/S0140-6736(85)91083-9.
http://dx.doi.org/10.1016/S0140-6736(85)...
23. Tassopoulos NC, Papaevangelou GJ, Roumeliotou-Karayannis A, Ticehurst JR,
Feinstone SM, Purcell RH. Search for hepatitis B virus DNA in sera from patients with acute type B
or non-A. non-B hepatitis. J Hepatol. 1986;2(3):410-8,
http://dx.doi.org/10.1016/S0168-8278(86)80052-6.
http://dx.doi.org/10.1016/S0168-8278(86)...
24. Tassopoulos NC, Papaevangelou GJ, Sjogren MH, Roumeliotou-Karayannis A, Gerin
JL, Purcell RH. Natural history of acute hepatitis B surface antigen-positive hepatitis in Greek
adults. Gastroenterology. 1987;92(6):1844-50.-2525. Wands JR, Walker JA, Davis TT, Waterbury LA, Owens AH, Carpenter CC. Hepatitis B
in an oncology unit. N Engl J Med. 1974;291(26):1371-5.). A
meta-analysis of 10 studies with adult heterogeneous populations, without adjusting for potential
differences between them, showed that the risk of chronicity was higher than 10% in 2 studies, 5% in
1 and less than 5% in 7 (77. Hyams KC. Risks of chronicity following acute hepatitis B virus infection: a
review. Clin Infect Dis. 1995;20(4):992-1000,
http://dx.doi.org/10.1093/clinids/20.4.992.
http://dx.doi.org/10.1093/clinids/20.4.9...
).
Note that the chronicity in this study was high (14.1%) compared to the literature. This
discrepancy could most likely be explained by the fact that the evolution to chronicity is inversely
proportional to the age at which infection occurs (1616. Lavarini C, Farci P, Chiaberge E, Veglio V, Giacobbi D, Bedarida G, et al. IgM
antibody against hepatitis B core antigen (IgM anti-HBc): diagnostic and prognostic significance in
acute HBsAg positive hepatitis. Br Med J (Clin Res Ed). 1983;287(6401):1254-6,
http://dx.doi.org/10.1136/bmj.287.6401.1254.
http://dx.doi.org/10.1136/bmj.287.6401.1...
). For
example, some authors have reported that approximately 10% of patients who become infected with HBV
as adults would not clear HBsAg after 6 months (2121. Schomerus H, Wiedmann KH, Dölle W, Peerenboom H, Strohmeyer G, Balzer K, et al.
(+)∼Cyanidanol-3 in the treatment of acute viral hepatitis: a randomized controlled trial.
Hepatology. 1984;4(2):331-5, http://dx.doi.org/10.1002/hep.1840040226.
http://dx.doi.org/10.1002/hep.1840040226...
). As shown
in our sample, all the patients were older than 22 years, which could justify a higher chronicity.
Note that other studies have also observed high frequencies of chronicity (1010. Beasley RP, Hwang LY, Lin CC, Ko YC, Twu SJ. Incidence of hepatitis among
students at a university in Taiwan. Am J Epidemiol. 1983;117(2):213-22.,1515. Kuruüzüm Z, Ozgenç O, Havuk A, Coşkuner A, Ari A, Celenkoğlu N. Rate of
chronicity and time of disappearance of HBsAg following acute hepatitis B. Hepatogastroenterol.
2009;56(90):466-9.,1717. McMahon BJ, Alward WL, Hall DB, Heyward WL, Bender TR, Francis DP, et al. Acute
hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent
development of the carrier state. J Infect Dis. 1985;151(4):599-603,
http://dx.doi.org/10.1093/infdis/151.4.599.
http://dx.doi.org/10.1093/infdis/151.4.5...
). Several factors are associated with the increased risk of chronic HBV infection,
including male gender, various causes of immune deficiency, genome variations, and genetic, hormonal
and nutritional factors (77. Hyams KC. Risks of chronicity following acute hepatitis B virus infection: a
review. Clin Infect Dis. 1995;20(4):992-1000,
http://dx.doi.org/10.1093/clinids/20.4.992.
http://dx.doi.org/10.1093/clinids/20.4.9...
).
Differences in chronicity can also be explained by the manner in which it was calculated. In the
present study, the evolution to chronicity was calculated based on patients who had complete
follow-ups, similar to other studies (1515. Kuruüzüm Z, Ozgenç O, Havuk A, Coşkuner A, Ari A, Celenkoğlu N. Rate of
chronicity and time of disappearance of HBsAg following acute hepatitis B. Hepatogastroenterol.
2009;56(90):466-9.,2424. Tassopoulos NC, Papaevangelou GJ, Sjogren MH, Roumeliotou-Karayannis A, Gerin
JL, Purcell RH. Natural history of acute hepatitis B surface antigen-positive hepatitis in Greek
adults. Gastroenterology. 1987;92(6):1844-50.). However, some authors did not specify whether there were
losses in the follow-up (1717. McMahon BJ, Alward WL, Hall DB, Heyward WL, Bender TR, Francis DP, et al. Acute
hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent
development of the carrier state. J Infect Dis. 1985;151(4):599-603,
http://dx.doi.org/10.1093/infdis/151.4.599.
http://dx.doi.org/10.1093/infdis/151.4.5...
) or if they calculated the
progression to chronicity based on the total number of patients or only those with completed
follow-ups (1111. Ferraz MLG, Yoradjian A, Barbieri A, Figueiredo V, Lopes Neto E, Cruz CN, et al.
Epidemiology of acute hepatitis B in a university hospital in São Paulo. Brazil: retrospective study
of two five-year periods. Sao Paulo Med J. 1998;116(3):1695-9.). The results of the present study could be
overestimated because some patients were lost to follow-up.
Regarding deaths, it is relevant that 5.1% of patients (4 of 78) died of causes related to fulminant hepatitis. Clearly, this result is most likely overestimated by the under-reporting of AHB.
Implementing the HBV vaccination over the last 30 years in several countries, such as the United
States in 1981, Taiwan in 1984 and Brazil in 1998, has promoted a change in patient outcomes (1313. Hoofnagle JH, Seeff LB, Bales ZB, Zimmerman HJ. Type B hepatitis after
transfusion with blood containing antibody to hepatitis B core antigen. N Engl J Med.
1978;298(25):1379-83.,1818. Rinker J, Galambos JT. Prospective study of hepatitis B in thirty-two
inadvertently infected people. Gastroenterology. 1981;81(4):686-91.,2626. Kao JH, Chen DS. Global control hepatitis B virus infection. Lancet Infect Dis.
2002;2(7):395-403, http://dx.doi.org/10.1016/S1473-3099(02)00315-8.
http://dx.doi.org/10.1016/S1473-3099(02)...
,2727. Daniels D, Grytdal S, Wasley A. Centers for Disease Control and Prevention CDC.
Surveillance for acute viral hepatitis - United States. 2007. MMWR Surveill Summ.
2009;58(3):1-27.).
Of the AHB patients, 77 (74.8%) were aged between 20 and 49 years; this age range is not included in the National Immunization Program. Our findings suggest the importance of revising the inclusion criteria used in the vaccination schedule currently used in Brazil.
Regarding ethnicity, the Caucasian race was prevalent. Regarding gender, female patients were
more likely to become chronic carriers, although this difference was not statistically significant.
This result was not in alignment with other studies, which have reported a higher evolution to
chronicity in male individuals (2828. Kim WR, Benson JT, Therneau TM. Torgerson HA, Yawn BP, Melton LJ. Changing
epidemiology of hepatitis B in a U.S. community. Hepatology. 2004;39(3):811-6,
http://dx.doi.org/10.1002/hep.20098.
http://dx.doi.org/10.1002/hep.20098...
,2929. Meffre C, Le Strat Y, Delarocque-Astagneau E, Dubois F, Antona D, Lemasson JM,
et al. Prevalence of hepatitis B and hepatitis C virus infections in France in 2004: social factors
are important predictors after adjusting for known risk factors. J Med Virol. 2010;82(4):546-55,
http://dx.doi.org/10.1002/jmv.21734.
http://dx.doi.org/10.1002/jmv.21734...
,3030. Taylor BC, Yuan JM, Shamliyan TA, Shaukat A, Kane RL, Wilt TJ. Clinical outcomes
in adults with chronic hepatitis B in association with patient and viral characteristics: a
systematic review of evidence. Hepatology. 2009;49(5 Suppl):S85-95,
http://dx.doi.org/10.1002/hep.22929.
http://dx.doi.org/10.1002/hep.22929...
).
Regarding the 17 coinfected patients, 12 (70.6%) had HIV, 4 had HIV/HCV, and 1 had HCV. HBV/HIV
coinfection occurs in many patients, and it is explained by the common routes of transmission for
these 2 viruses, primarily sexual, parenteral and vertical (3131. Souza MG, Passos ADC, Machado AA, Figueiredo JFC, Esmeraldino LE. Co-infecção
HIV e vírus da hepatite B: prevalência e fatores de risco. Rev Soc Bras Med Trop.
2004;37(5):391-5.). A study conducted in Porto Alegre involving 587 HIV patients showed that 14 of 306
(4.6%) had positive HBsAg (3232. Tovo CV, Santos DE, Mattos AZ, Almeida PRL, Mattos AA, Santos BR. Prevalência
ambulatorial em um hospital geral de marcadores para hepatites B e C em pacientes com infecção pelo
vírus da imunodeficiência humana. Arq Gastroenterol. 2006;43(2):73-6,
http://dx.doi.org/10.1590/S0004-28032006000200002.
http://dx.doi.org/10.1590/S0004-28032006...
).
Note that 2 patients who became chronic carriers were coinfected. Literature reports suggest that
worse outcomes are more frequent in coinfected patients (3333. Sherman M. Strategies for managing coinfection with hepatitis B virus and HIV.
Cleve Clin J Med. 2009;76 Suppl 3:S30-3, http://dx.doi.org/10.3949/ccjm.76.s3.07.
http://dx.doi.org/10.3949/ccjm.76.s3.07...
).
The abovementioned results suggest the utmost importance of control measures and epidemiological assessments of HBV patients because in the evaluated population, there were high levels of chronicity and mortality related to liver injury. Effective actions, such as universal vaccination, break the transmission chain of HBV. The appropriate follow-up of patients and their contacts (home and/or sexual) is essential for improving the well-being of our population.
REFERENCES
-
1European Association for the Study of Liver. EASL Clinical practice guidelines: management of chronic hepatitis J Hepatol. 2009;50(2):227-42.
-
2Daruich J, Gadano A, Fainboim H, Pessoa M, Cheinquer H. Guía Latinoamericana de tratamiento de la hepatitis crónica B. Acta Gastroenterol Latinoam. 2007;37(3):168-77.
-
3McMahon BJ. Natural history of chronic hepatitis B - clinical implications. Medscape J Med. 2008;10(4):91.
-
4Ministério da Saúde (Brasil). Programa Nacional de Imunizações: 30 anos. Brasília: Ministério da Saúde. 2003. [acesso em 2010 Fev.] Disponível em: http://www.scribd.com/doc/27663002/Ministerio-Da-Saude
» http://www.scribd.com/doc/27663002/Ministerio-Da-Saude -
5Ministério da Saúde (Brasil). Nota Técnica 89/2010 CGPNI/DEVEP/SVS/MS. Ministério da Saúde em05/08/2010.
-
6Ministério da Saúde (Brasil). Portal Brasil. Disponível em: http://www.brasil.gov.br/noticias/arquivos/2012/07/24
» http://www.brasil.gov.br/noticias/arquivos/2012/07/24 -
7Hyams KC. Risks of chronicity following acute hepatitis B virus infection: a review. Clin Infect Dis. 1995;20(4):992-1000, http://dx.doi.org/10.1093/clinids/20.4.992.
» http://dx.doi.org/10.1093/clinids/20.4.992 -
8Lok AS, Mcmahon BJ. AASLD Practice guideline update. Chronic Hepatitis B: Update 2009. Hepatology. 2009;50:1-36.
-
9Barker LF, Murray R. Acquisition of hepatitis-associated antigen. Clinical features in young adults. JAMA. 1971;216(12):1970-6, http://dx.doi.org/10.1001/jama.1971.03180380028006.
» http://dx.doi.org/10.1001/jama.1971.03180380028006 -
10Beasley RP, Hwang LY, Lin CC, Ko YC, Twu SJ. Incidence of hepatitis among students at a university in Taiwan. Am J Epidemiol. 1983;117(2):213-22.
-
11Ferraz MLG, Yoradjian A, Barbieri A, Figueiredo V, Lopes Neto E, Cruz CN, et al. Epidemiology of acute hepatitis B in a university hospital in São Paulo. Brazil: retrospective study of two five-year periods. Sao Paulo Med J. 1998;116(3):1695-9.
-
12Gimeno V, Escudero A, Gonzalez R, Serra MA, Del Olmo JA, Wassel A, et al. Acute hepatitis in heroin addicts: etiologic and follow-up study of 110 cases. Rev Clin Esp. 1989;184(7):360-3.
-
13Hoofnagle JH, Seeff LB, Bales ZB, Zimmerman HJ. Type B hepatitis after transfusion with blood containing antibody to hepatitis B core antigen. N Engl J Med. 1978;298(25):1379-83.
-
14Kent GP, Brondum J, Keenlyside RA, LaFazia LM, Scott HD. A large outbreak of acupuncture-associated hepatitis B. Am J Epidemiol. 1988;127(3):591-8.
-
15Kuruüzüm Z, Ozgenç O, Havuk A, Coşkuner A, Ari A, Celenkoğlu N. Rate of chronicity and time of disappearance of HBsAg following acute hepatitis B. Hepatogastroenterol. 2009;56(90):466-9.
-
16Lavarini C, Farci P, Chiaberge E, Veglio V, Giacobbi D, Bedarida G, et al. IgM antibody against hepatitis B core antigen (IgM anti-HBc): diagnostic and prognostic significance in acute HBsAg positive hepatitis. Br Med J (Clin Res Ed). 1983;287(6401):1254-6, http://dx.doi.org/10.1136/bmj.287.6401.1254.
» http://dx.doi.org/10.1136/bmj.287.6401.1254 -
17McMahon BJ, Alward WL, Hall DB, Heyward WL, Bender TR, Francis DP, et al. Acute hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent development of the carrier state. J Infect Dis. 1985;151(4):599-603, http://dx.doi.org/10.1093/infdis/151.4.599.
» http://dx.doi.org/10.1093/infdis/151.4.599 -
18Rinker J, Galambos JT. Prospective study of hepatitis B in thirty-two inadvertently infected people. Gastroenterology. 1981;81(4):686-91.
-
19Roumeliotou A, Tassopoulos N, Richardson SC, Kalafatas P, Papaevangelou G. How often does chronic liver disease follow acute hepatitis B in adults? Infection. 1985;13(4):174-6, http://dx.doi.org/10.1007/BF01642806.
» http://dx.doi.org/10.1007/BF01642806 -
20Roumeliotou A, Papaevangelou G. Chronic liver disease rarely follows acute hepatitis B in non-immunocompromised adults. Infection. 1992;20(4):221-3, http://dx.doi.org/10.1007/BF02033063.
» http://dx.doi.org/10.1007/BF02033063 -
21Schomerus H, Wiedmann KH, Dölle W, Peerenboom H, Strohmeyer G, Balzer K, et al. (+)∼Cyanidanol-3 in the treatment of acute viral hepatitis: a randomized controlled trial. Hepatology. 1984;4(2):331-5, http://dx.doi.org/10.1002/hep.1840040226.
» http://dx.doi.org/10.1002/hep.1840040226 -
22Wiedmann KH, Brating NW, Diao GD, Schomerus H, Dolle W, Berg PA. Serum inhibitory factors (SIF) are of prognostic value in acute viral hepatitis. Lancet. 1985;1(8424):309-12, http://dx.doi.org/10.1016/S0140-6736(85)91083-9.
» http://dx.doi.org/10.1016/S0140-6736(85)91083-9 -
23Tassopoulos NC, Papaevangelou GJ, Roumeliotou-Karayannis A, Ticehurst JR, Feinstone SM, Purcell RH. Search for hepatitis B virus DNA in sera from patients with acute type B or non-A. non-B hepatitis. J Hepatol. 1986;2(3):410-8, http://dx.doi.org/10.1016/S0168-8278(86)80052-6.
» http://dx.doi.org/10.1016/S0168-8278(86)80052-6 -
24Tassopoulos NC, Papaevangelou GJ, Sjogren MH, Roumeliotou-Karayannis A, Gerin JL, Purcell RH. Natural history of acute hepatitis B surface antigen-positive hepatitis in Greek adults. Gastroenterology. 1987;92(6):1844-50.
-
25Wands JR, Walker JA, Davis TT, Waterbury LA, Owens AH, Carpenter CC. Hepatitis B in an oncology unit. N Engl J Med. 1974;291(26):1371-5.
-
26Kao JH, Chen DS. Global control hepatitis B virus infection. Lancet Infect Dis. 2002;2(7):395-403, http://dx.doi.org/10.1016/S1473-3099(02)00315-8.
» http://dx.doi.org/10.1016/S1473-3099(02)00315-8 -
27Daniels D, Grytdal S, Wasley A. Centers for Disease Control and Prevention CDC. Surveillance for acute viral hepatitis - United States. 2007. MMWR Surveill Summ. 2009;58(3):1-27.
-
28Kim WR, Benson JT, Therneau TM. Torgerson HA, Yawn BP, Melton LJ. Changing epidemiology of hepatitis B in a U.S. community. Hepatology. 2004;39(3):811-6, http://dx.doi.org/10.1002/hep.20098.
» http://dx.doi.org/10.1002/hep.20098 -
29Meffre C, Le Strat Y, Delarocque-Astagneau E, Dubois F, Antona D, Lemasson JM, et al. Prevalence of hepatitis B and hepatitis C virus infections in France in 2004: social factors are important predictors after adjusting for known risk factors. J Med Virol. 2010;82(4):546-55, http://dx.doi.org/10.1002/jmv.21734.
» http://dx.doi.org/10.1002/jmv.21734 -
30Taylor BC, Yuan JM, Shamliyan TA, Shaukat A, Kane RL, Wilt TJ. Clinical outcomes in adults with chronic hepatitis B in association with patient and viral characteristics: a systematic review of evidence. Hepatology. 2009;49(5 Suppl):S85-95, http://dx.doi.org/10.1002/hep.22929.
» http://dx.doi.org/10.1002/hep.22929 -
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No potential conflict of interest was reported.
Publication Dates
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Publication in this collection
May 2013
History
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Received
15 Aug 2012 -
Reviewed
1 Oct 2012 -
Accepted
7 Jan 2013