Association between Schistosomiasis mansoni and hepatitis C: systematic review

Associação entre esquistossomose mansônica e hepatite C: revisão sistemática

Asociación entre esquistosomiasis mansoni y hepatitis C: revisión sistemática

Daniele Silva de Moraes Van-Lume Maria de Fátima Pessoa Militão de Albuquerque Alexandre Ignácio de Souza Ana Lúcia Coutinho Domingues Edmundo Pessoa de Almeida Lopes Clarice Neuenschwander Lins de Morais Silvia Maria Lucena Montenegro About the authors

Abstracts

OBJECTIVE:

To perform a systematic review of the prevalence of the HCV/ S. mansoni co-infection and associated factors in Schistosoma mansoni -infected populations.

METHODS:

The bibliographic search was carried out using the Medline, Lilacs, SciELO, Cochrane Library and Ibecs databases. The criteria for the studies' selection and the extraction data were based on systematic review methods. Forty five studies were found, with nine being excluded in a first screening. Thirteen articles were used for data extraction.

RESULTS:

The HCV infection rates in schistosomiasis populations range from 1% in Ethiopia to 50% in Egypt. Several studies had poorly defined methodologies, even in areas characterized by an association between hepatitis C and schistosomiasis, such as Brazil and Egypt, which meant conclusions were inconsistent. HCV infection rates in schistosomotic populations were heterogeneous and risk factors for acquiring the virus varied widely.

CONCLUSIONS:

Despite the limitations, this review may help to identify regions with higher rates of hepatitis C and schistosomiasis association. However, more studies are necessary for the development of public health policies on prevention and control of both diseases.

Comorbidity; Hepatitis C, epidemiology; Schistosomiasis, epidemiology; Review


OBJETIVO:

Realizar revisão sistemática sobre a prevalência da confecção do vírus da hepatite C e Schistosoma mansoni e os fatores de risco associados a indivíduos com esquistossomose.

MÉTODOS:

Revisão realizada nas bases de dados Medline, Lilacs, SciELO, Biblioteca Cochrane e Ibecs. Os critérios de seleção e a obtenção dos dados foram baseados em métodos de revisão sistemática. Foram encontradas 45 referências relevantes, das quais nove foram excluídas na primeira triagem, 14 na leitura dos resumos e nove na leitura completa. Treze artigos foram selecionados para análise.

RESULTADOS:

A prevalência da associação entre vírus da hepatite C e Schistosoma mansoni variou de 1% na Etiópia a 50% no Egito. Alguns estudos apresentam metodologias pouco definidas, mesmo em áreas caracterizadas pela associação entre vírus da hepatite C e S. mansoni , como Brasil e Egito, o que não permitiu conclusões consistentes. As taxas de infecção pelo VHC em populações esquistossomáticas foram heterogêneas e os fatores de risco para adquirir o vírus foram variáveis.

CONCLUSÕES:

Apesar das limitações, esta análise pode ajudar a identificar regiões com maiores taxas dessa associação. Outros estudos serão necessários para o desenvolvimento de políticas públicas de prevenção e controle dessas doenças.

Comorbidade; Hepatite C, epidemiologia; Esquistossomose, epidemiologia; Revisão


OBJETIVO:

Realizar revisión sistemática sobre la prevalencia de la co-infección del virus de la hepatitis C y Schistosoma mansoni y los factores de riesgo asociados a individuos con esquistosomosis.

MÉTODOS:

Revisión realizada en las bases de datos MEDLINE, LILACS, SciELO, Biblioteca Cochrane e IBECS. Los criterios de selección y la obtención de los datos fueron basados en métodos de revisión sistemática.

RESULTADOS:

Fueron encontradas 45 referencias relevantes, de las cuales, nueve fueron excluidas en la primera selección, 14 en la lectura de los resúmenes y nueve en la lectura completa. Trece artículos fueron seleccionados para análisis. La prevalencia de la asociación entre virus de la hepatitis C y Schistosoma mansoni varió de 1% en Etiopia, a 50% en Egipto. Algunos estudios presentan metodologías poco definidas, inclusive en áreas caracterizadas por la asociación entre el virus de la hepatitis C y S. mansoni, como Brasil y Egipto, lo que no permitió conclusiones consistentes. Los cocientes de infección por el VHC en poblaciones esquistosómicas fueron heterogéneos y los factores de riesgo para adquirir el virus fueron variables.

CONCLUSIONES:

A pesar de las limitaciones, este análisis pudo ayudar a identificar regiones con mayores cocientes de esa asociación. Otros estudios serán necesarios para el desarrollo de políticas públicas de prevención y control de estas enfermedades.

Comorbilidad; Hepatitis C, epidemiologia; Esquistosomiasis, epidemiologia; Revisión


INTRODUCTION

Schistosomiasis is the second most important parasitic infection after malaria and affects more than 200 million people in 74 countries. 5656. WHO Expert Committee. Prevention and Control of Schistosomiasis and Soil-Transmitted Helminthiasis. World Health Organ Tech Rep Ser.2002;912:i-vi,1-57. It is endemic, with high prevalence and morbidity rates in many countries, especially those in Africa, such as Egypt, 1818. El-Khoby T, Galal N, Fenwick A, Barakat R, El-Hawey A, Nooman Z, et al. The epidemiology of schistosomiasis in Egypt: summary findings in nine governorates. Am J Trop Med Hyg. 2000;62(2Supll):88-99. Kenya 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
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and Sudan, 2727. Homeida M, Ahmed S, Dafalla A, Suliman S, Elton I, Nash T, et al. Morbidity associated with Schistosoma mansoni infection as determined by ultrasound: a study in Geriza, Sudan. Am J Trop Med Hyg. 1988;39(2):196-201. , 4444. Richter J, Monteiro E, Braz RM, Abdalla M, Abdel-Rahim IM, Fano U, et al. Sonografic organometry in Brazilian and Sudanese patients with hepatosplenic schistosomiasis mansoni and its relation to the risk of bleeding from oesophageal varices. Acta Trop. 1992;51(3-4):281-90. DOI: http://dx.doi.org/10.1016/0001-706X(92)90046-Z
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and in South America, mainly Brazil.38, a a Maciel RCR. Enzimas caniculares na forma hepatoesplênica da esquistossomose mansoni [dissertação de mestrado]. Recife: Universidade Federal de Pernambuco; 2006.

The prevalence of schistosomiasis ranged from 15 to 45% in Egypt and Brazil.18,38, a a Maciel RCR. Enzimas caniculares na forma hepatoesplênica da esquistossomose mansoni [dissertação de mestrado]. Recife: Universidade Federal de Pernambuco; 2006. In this country, six to eight million people are infected with Schistosoma mansoni and about 30 million people live under risk of infection. a a Maciel RCR. Enzimas caniculares na forma hepatoesplênica da esquistossomose mansoni [dissertação de mestrado]. Recife: Universidade Federal de Pernambuco; 2006. The prevalence of Schistosomiasis mansoni (SM) can reach up to 27% of the population in some areas of Northeastern Brazil, 3838. Palmeira DCC, Carvalho AG, Rodrigues K, Couto, JLA. Prevalência da infecção pelo Schistosoma mansoni em dois municípios do Estado de Alagoas. Rev Soc Bras Med Trop. 2010;43(3):313-7. DOI: http://dx.doi.org/10.1590/S0037-86822010000300020
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turning this country into a major schistosomiasis endemic area in the world.

The diverse clinical patterns observed for this disease depend on many factors, including parasite strain, host genetic background, host nutritional and immunological state, and co-infections. 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
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, 1010. Boisier P, Ramarokoto CE, Ravoniarimbinina P, Rabarijaona L, Ravaoalimalala VE. Geographic diffrerences in hepatosplenic complications of schistosomiasis mansoni and explanatory factors of morbidity. Trop Med Int Health. 2001;6(9):699-706. DOI: http://dx.doi.org/10.1046/j.1365-3156.2001.00781.x
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, 1616. Dessein AJ, Hillaire D, Elwali NE, Marquet S, Mohamed-Ali Q, Mirghani A, et al. Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene. Am J Hum Genet. 1999;65(3):709-21. DOI: http://dx.doi.org/10.1086/302526
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, 3131. King CH, Magak P, Abdel-Salam E, Ouma JH, Kariuki HC, Blanton E. Measuring morbidity in schistosomiasis mansoni: relationship between image pattern, portal vein diameter and portal branch thickness in large-scale surveys using new WHO coding guidelines for ultrasound in schistosomiais. Trop Med Int Health. 2003;8(2):109-17. DOI: http://dx.doi.org/10.1046/j.1365-3156.2003.00994.x
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, 3535. Mohamed-Ali Q, Elwali NE, Abdelhameed AA, Mergani A, Rahoud S, Elagib KE, et al. Susceptibility to periportal (Symmers) fibrosis in human Schistosoma mansoni infections: evidence that intensity and duration of infection, gender and inherited factors are critical in disease progression. J Infect Dis. 1999;180(4):1298-306. DOI: http://dx.doi.org/10.1086/314999
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Schistosomiasis may progress to the most advanced stage of disease, the hepatosplenic form (HS). This clinical form is observed in endemic areas and is characterized by portal hypertension that may cause digestive hemorrhage. 2828. Jordan P, Webbe G, Sturrock RF, editors. Human schistosomiasis. Wallingford: CAB International; 1993. , 4242. Raia S, Silva LC, Gayotto LCC, Forster SC, Fukushima J, Strauss E. Portal hypertension in schistosomiasis a long-term follow-up of a randomized trial comparing three types of surgery. Hepatol. 1994; 20(2):398-403. DOI: http://dx.doi.org/10.1002/hep.1840200220
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, 4848. Strickland GT. Gastrointestinal manifestations of schistosomiasis. Gut. 1994; 35(10):1334-7. DOI: http://dx.doi.org/10.1136/gut.35.10.1334
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When SM comes combined with other hepatic disease, especially the Hepatitis C Virus (HCV) infection, the progression of hepatic fibrosis into cirrhosis and hepatocellular carcinoma (HCC) can occur within a few years. 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
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, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. Concomitant SM and HCV infection is observed with high frequency in Egypt 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 77. Bassily S, Hyams KC, El-Marsry NA, Hassan NF, Watts DM. Hepatitis C virus infection and hepatosplenic schistosomiasis. Scand J Infect Dis. 1992;24(5):687-8. DOI: http://dx.doi.org/10.3109/00365549209054660
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, 4747. Strickland GT, Elhefni H, Salman T, Waked I, Abdel-Hamid M, Mikhail N, et al. Role of hepatitis C infection in chronic liver disease in Egypt. Am J Trop Med Hyg. 2002;67(4):436-42. and Brazil. 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...

Hepatitis C is also considered an important public health issue throughout the world, with approximately 3% of people (about 170 million) being infected with the HCV. 11. Abbas OM, Omar NA, Zaghla HE, Faramawi MF. Schistosoma mansoni coinfection could have a protective effect against mixed cryoglobulinemia in hepatitis C patients. Liver Int. 2009;29(7):1065-70. DOI: http://dx.doi.org/10.1111/j.1478-3231.2009.01970.x
http://dx.doi.org/10.1111/j.1478-3231.20...
, 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. It is also the most important cause of liver disease and HCC in developed countries, including the United Kingdom and USA, 55. Alter MJ, Margolis HS, Krawczynsky K, Judson FN, Mares A, Alexander WJ, et al. The natural history of community acquired hepatitis C in the United States. N Engl J Med. 1992;327(27):1899-905. DOI: http://dx.doi.org/10.1056/NEJM199212313272702
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, 4141. Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. Lancet. 1997;349(9055):825-32. DOI: http://dx.doi.org/10.1016/S0140-6736(96)07642-8
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, 5353. Thomson BJ, Finch RG. Hepatitis C virus infection. Clin Microbiol Infect. 2005;11(2):86-94. DOI: http://dx.doi.org/10.1111/j.1469-0691.2004.01061.x
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, 5454. Tong MJ, el-Farra NS, Reikes AR, Co RL. Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med. 1995;332(22):1463-6. DOI: http://dx.doi.org/10.1056/NEJM199506013322202
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and in developing countries, such as Egypt 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 2525. Hassan MM, Zaghloul AS, El-Serag HB, Soliman O, Patt YZ, Chappell CL, et al. The role of hepatitis C in hepatocelullar carcinoma: a case control study among Egyptians patients. J Clin Gastroenterol. 2001;33(2):123-6. DOI: http://dx.doi.org/10.1097/00004836-200108000-00006
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, 2626. Heintges T, Wands J. Hepatitis C virus: Epidemiology and transmission. Hepatology. 1997;26(3):521-6. DOI: http://dx.doi.org/10.1002/hep.510260338
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and Brazil. 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
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, 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32.

In Egypt, eight to ten million are infected and 68 million people have been exposed to HCV 5252. Thomas S, Elhefni H, Salman T, Walked I, Abdel-Hamid M, Mikhail NN, et al. Role of hepatitis C infection in chronic liver disease in Egypt. Am J Trop Med Hyg. 2002;67(4):436-42. (a prevalence of 10 to 60%), mainly in rural areas. 1515. Darwish MA, Raouf TA, Rushdy P, Constantine NT, Rao M, Edelman R. Risk factors associated with high seroprevalence of hepatitis C virus infection in Egyptian blood donors. Am J Trop Med Hyg. 1993;49(4):440-7. , 1717. El-Gohary A, Hassan A, Nooman Z, Lavanchy D, Mayerat C, El Ayat A, et al. High prevalence of hepatitis C virus among urban and rural population groups in Egypt. Acta Trop. 1995;59(2):155-61. DOI: http://dx.doi.org/10.1016/0001-706X(95)00075-P
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, 2121. Frank C, Mohamed MK, Strickland GT, Lavanchy D, Arthur RR, Magder LS. The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet. 2000;355(9207):887-91.DOI: http://dx.doi.org/10.1016/S0140-6736(99)06527-7
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The prevalence of HCV infection is lower in Brazil than in Egypt and varies from 2.5% to 4.9%, corresponding to approximately 3.9 to 7.6 million people. 1111. Brandão A, Fuchs SC. Risk factor for hepatitis C virus infection among blood donors in southern Brazil: a case-control study. BMC Gastroenterol.2002;2(18):1-8.

HCV may be implicated as a factor influencing the severity of schistosomiasis in developing countries. Likewise, an influence of SM on HCV severity has been suggested by some authors. 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3333. Mohamed A, Elsheikh A, Ghandour Z, Al Karawi M. Impact of hepatitis C virus infection on schistosomal liver disease. Hepatogastroenterology. 1998;45(23):1492-6. , 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...

There are many contradictory data about the prevalence of HCV/S. mansoni co-infection in SM endemic areas and the risk factors associated with increased susceptibility for HCV infection in a S. mansoni-infected person, especially in the HS form. 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 44. Al-Faleh FZ, Ramia S, Arif M, Ayoola EA, Al-Rashed RS, Al-Jefry M, et al. Profile of hepatitis C virus and the possible modes of transmission of the virus in the Gizan area of Saudi Arabia: a community based study. An Trop Med Parasitol. 1995;89(4):431-7. , 77. Bassily S, Hyams KC, El-Marsry NA, Hassan NF, Watts DM. Hepatitis C virus infection and hepatosplenic schistosomiasis. Scand J Infect Dis. 1992;24(5):687-8. DOI: http://dx.doi.org/10.3109/00365549209054660
http://dx.doi.org/10.3109/00365549209054...
, 4949. Tavares-Neto J, Prata A, Paraná R, Valente VB, Vitvitski L, Figueiredo FC. Very low prevalence of hepatitis C virus infection in rural communities of northeastern Brazil with a high prevalence of schistosomiasis mansoni. Rev Soc Bras Med Trop. 2005;38(4):290-3. DOI: http://dx.doi.org/10.1590/S0037-86822005000400002
http://dx.doi.org/10.1590/S0037-86822005...

The worldwide relevance of the hepatitis C and schistosomiasis association as a public health issue is mainly due to the severe clinical patterns and high morbidity associated with it, especially in developing countries. This study aimed to perform a systematic review of the prevalence of the HCV/S. mansoni co-infection in SM-infected population living in endemic areas and associated factors.

METHODS

The bibliographic search was performed through a systematic search covering the 1990s and up to May 2011. The terms “Schistosomiasis mansoni” and “Hepatitis C” were utilized to search the Medline, Lilacs, SciELO, Cochrane Library and IBECS databases. These databases fulfill the minimum criteria search to conduct a systematic review, in accordance with the literature. 2222. Green S. Systematic reviews and analysis. Singapore Med J. 2005;46(6):270-4.

Forty-five publications were obtained through the website search described and a first screening was performed. The criteria adopted for inclusion were:

• Studies in scientific article formats published on or after 1989, the year in which HCV was discovered;

• Titles published in English, Spanish or Portuguese with available abstracts;

• Studies performed with human populations.

Nine studies were excluded because they utilized experimental models, were presented as thesis or monograph or were redundant in different databases (Figure).

Figure.
Flowchart of the systematic review results of selected publications.

A second screening was done by analyzing the 36 selected abstracts. Fourteen studies were excluded because they did not contain information about the prevalence of HCV/ S. mansoni association or the risk factors associated with HCV infection in a schistosomiasis population (Figure).

A total of 22 articles were selected for complete reading. This step was carried out by a pair of reviewers where each one, independently, filled a table with the criteria relevant to the articles selected for data extraction. 1414. Crowther M, Lim W, Crowther MA. Systematic review and analysis methodology. Blood. 2010;116(17):3140-6. DOI: http://dx.doi.org/10.1182/blood-2010-05-280883
http://dx.doi.org/10.1182/blood-2010-05-...
, 2222. Green S. Systematic reviews and analysis. Singapore Med J. 2005;46(6):270-4. There was no discordance between the two reviewers in regard to the articles selected, with kappa index = 1 (p < 0.05). The inclusion criteria adopted in this step were:

• Population: subjects of both sexes infected by S. mansoni and living in endemic areas;

• Age group: > 18 years old;

• Measurement of HCV/ S. mansoni association: studies that described the methods utilized to measure the prevalence of HCV and S. mansoni infections;

• Risk factors: studies that reported the risk factors associated with HCV infection and if there is a correlation with schistosomiasis.

Studies that used only serologic methods to evaluate the prevalence of S. mansoni infection were excluded because the distinction between past and present infection is not possible, raising doubts about the confirmed SM diagnosis. 2020. Farid A, Al-Sherbiny M, Mohamed N, Saad A, Shata MT, Lee DH, et al. Schistosoma infection inhibits cellular immune responses to core HCV peptides. Parasite Immunol. 2005;27(5):189-96. DOI: http://dx.doi.org/10.1111/j.1365-3024.2005.00762.x
http://dx.doi.org/10.1111/j.1365-3024.20...

Of the 22 articles selected for the last step, 13 filled all inclusion criteria and offered data required to analyze the prevalence of hepatitis C and schistosomiasis association in SM endemic areas. The exclusion of the nine articles in the last screening are described in Figure. 11. Abbas OM, Omar NA, Zaghla HE, Faramawi MF. Schistosoma mansoni coinfection could have a protective effect against mixed cryoglobulinemia in hepatitis C patients. Liver Int. 2009;29(7):1065-70. DOI: http://dx.doi.org/10.1111/j.1478-3231.2009.01970.x
http://dx.doi.org/10.1111/j.1478-3231.20...
, 33. Agha S, El-Mashad N, El-Malky M, El-Shony H, El-Sherif M, El-Hasan MA, et al. Prevalence of low positive anti-HCV antibodies in blood donors: Schistosoma mansoni co-infection and possible role of auto-antibodies. Microbiol Immunol. 2006;50(6):447-52. , 2020. Farid A, Al-Sherbiny M, Mohamed N, Saad A, Shata MT, Lee DH, et al. Schistosoma infection inhibits cellular immune responses to core HCV peptides. Parasite Immunol. 2005;27(5):189-96. DOI: http://dx.doi.org/10.1111/j.1365-3024.2005.00762.x
http://dx.doi.org/10.1111/j.1365-3024.20...
, 2424. Halim AB, Garry RF, Dash S, Gerber M. Effect of schistosomiasis and hepatitis on liver disease. Am J Trop Med Hyg. 1999;60(6):915-20. , 2525. Hassan MM, Zaghloul AS, El-Serag HB, Soliman O, Patt YZ, Chappell CL, et al. The role of hepatitis C in hepatocelullar carcinoma: a case control study among Egyptians patients. J Clin Gastroenterol. 2001;33(2):123-6. DOI: http://dx.doi.org/10.1097/00004836-200108000-00006
http://dx.doi.org/10.1097/00004836-20010...
, 3434. Mohamed MK, Bakr I, El-Hoseiny M, Arafa N, Hassan A, Ismail S, et al. HCV-related morbidity in a rural community of Egypt. J Med Virol. 2006;78(9):1185-9. DOI: http://dx.doi.org/10.1002/jmv.20679
http://dx.doi.org/10.1002/jmv.20679...
, 4949. Tavares-Neto J, Prata A, Paraná R, Valente VB, Vitvitski L, Figueiredo FC. Very low prevalence of hepatitis C virus infection in rural communities of northeastern Brazil with a high prevalence of schistosomiasis mansoni. Rev Soc Bras Med Trop. 2005;38(4):290-3. DOI: http://dx.doi.org/10.1590/S0037-86822005000400002
http://dx.doi.org/10.1590/S0037-86822005...
5151. Helal TE, Danial MF, Ahmed HF. The relationship between hepatitis C virus and Schistosomiasis: histopathologic evaluation of liver biopsy specimens. Human Pathol. 1998;29(7):743-9. DOI: http://dx.doi.org/10.1016/S0046-8177(98)90285-4
http://dx.doi.org/10.1016/S0046-8177(98)...

RESULTS

Table 1 , 2 and 3 list the 13 articles that were analyzed.

Table 1.
Authors, type of studies and their objectives.
Table 2.
Systematic review of results of Hepatitis C Virus and Schistosoma mansoni diagnosis and prevalence of Hepatitis C Virus/ mansoni association.
Table 3.
Risk factors, results and conclusion of studies selected.

The prevalence of HCV/ S. mansoni association ranged from 0.8 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
to 50.0% among the studies, with the highest ranges in Egypt (10 to 50%). 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9.

Among the 13 articles included in the final step of the review, ten were cross-sectional studies, 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. one was a retrospective cases series, 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
one was a prospective cases series 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. and the other was a cases series with an external control group. 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. Five studies 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. were conducted in Brazil, five in Egypt, 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. two in Sudan, 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
one in Ethiopia 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. and one in Kenya. 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
A higher prevalence of HCV infection was found in the SM population of Egypt, compared to the other countries ( Table 1 ).

Eight studies 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. sought to determine the serologic prevalence of HCV infection in an SM population and one study proposed to verify any epidemiologic relationship of schistosomiasis and HBV and HCV serologic markers. 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. Six studies 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. aimed to evaluate the severity of hepatic lesions and morbidity of hepatitis C when associated with SM and to correlate this with serologic markers. The mean age of humans enrolled in these studies was 33.7 years and in four articles subjects were > 40 years 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
( Table 2 ).

The inclusion criteria used by the authors to choose subjects with schistosomiasis were mainly: people living in endemic areas with positive parasitological exams confirmed by the presence of S. mansoni eggs in stool samples or rectal biopsies (eight studies) and/or ultrasonography (US) compatible with periportal fibrosis (PPF) (six studies). The epidemiological history was considered in seven studies to compose diagnosis when in conjunction with one or both criteria mentioned above.

The main exclusion criteria adopted for the selected studies was if the person did not live at the study site. People with no history of contaminated water contact and/or with liver disease caused by alcohol consumption, autoimmune disorders or by Hepatitis viruses A, B, D or with others etiologies were also excluded from these studies. Six studies did not mention the exclusion criteria adopted. 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. , 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...

The most commonly chosen technique of HCV diagnosis was 3rd generation anti-HCV ELISA, utilized in five studies. 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. Four other studies utilized 2nd generation anti-HCV ELISA. 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. The quantification of the viral titers was performed by HCV RNA PCR in seven studies. 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7.

Six studies made appropriate epidemiologic and statistical analyses to confirm the correlation between risk factors associated and HCV infection in SM patients. 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. The other articles suggested possible risk factors without any statistical correlation found ( Table 3 ).

Blood transfusion was cited by seven of them as a risk factor for HCV contamination. 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. The second most observed risk factor described in three studies was the antischistosomal mass treatment, due to the use of syringes and nosocomial equipments without proper sterilization. 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
Surgical procedures, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
digestive endoscopy, 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. old age, 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
genetic background 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
and hemodialysis 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. were also cited as risk factors for HCV acquisition. Four studies did not find any association between SM infection and an increased risk of acquiring HCV. 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. , 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...

DISCUSSION

Schistosomiasis is an important public health issue associated with poverty and poor sanitary conditions. 1313. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Trop. 2000;77(1):41-51. DOI: http://dx.doi.org/10.1016/S0001-706X(00)00122-4
http://dx.doi.org/10.1016/S0001-706X(00)...
All studies described were conducted in developing countries since the 1970s, especially in Egypt, Sudan, Ethiopia, Kenya and Brazil, confirming the impact of this disease in these countries. 1313. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Trop. 2000;77(1):41-51. DOI: http://dx.doi.org/10.1016/S0001-706X(00)00122-4
http://dx.doi.org/10.1016/S0001-706X(00)...
The association between schistosomiasis and hepatitis C has been studied by many authors, showing the importance of research into this condition worldwide ( Tables 1 , 2 and 3 ).

The majority of articles were cross-sectional studies ( Table 1 ) and aimed to determine the prevalence of HCV infection in a confirmed SM population. Cross-sectional studies are important in identifying regions in developing countries that need more attention from the government authorities for the implementation of public health policies in regards to treatment and control for both hepatitis C and SM. On this point, this review may help to identify regions where the association of these diseases and the risk factors associated with HCV infection are relevant, and to aid the implementation of prevention and control actions.

A few studies pointed to a correlation between diseases with morbidity patterns, progression of liver damage 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
and risk factors 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. in acquiring HCV. It could be useful to understand the clinical course of this particular condition and for treatment choices ( Tables 2 and 3 ). When schistosomiasis and hepatitis C association is established, the clinical course develops into severe hepatocellular damage. Viral persistence and hepatic cirrhosis can develop faster than in mono-infected people. 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...

The high percentage of HCV infection in schistosomiasis populations of different countries caught the attention of the scientific community for the variable prevalence of disease association rates. 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. , 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. The rates ranged from 10 to 50% in Egypt, 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3030. Kamel MA, Miller FD, Masry AG, Zakaria S, Khattab M, Essmat G, et al. The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. An Trop Med Parasitol. 1994;88(5):501-9. mainly due the mass treatment of the schistosomiasis infected population in the 1970s. This public policy was not adopted in other countries and similar prevalence rates cannot be observed. 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
There is a lack of a relationship between the high prevalence of HCV infection in schistosomiasis endemic areas and risk factors, although many of them were.

Disease association rates in Brazil, although not as high as in Egypt, can be considered relevant due to the high morbidity when HCV is present. When the study was conducted with hospital patients in Brazil, disease association rates were up to 20%. 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. Conflicting results among studies on HCV /S. mansoni association in Brazil,6,40,45,46, b b Morais CNL. Avaliação da relação entre marcadores biológicos com os graus de fibrose no complexo hepatite C e esquistossomose [tese de doutorado]. Recife: Centro de Pesquisas Aggeu Magalhães da Fiocruz; 2007. reinforce the need for further studies of this condition, especially with appropriate methodologies for prevalence and risk factor evaluations. Methodological issues are the main problem of the majority of studies worldwide, suggesting the inadequacy of study designs.

The serologic method was the most commonly used method of evaluating HCV infections, including recently developed techniques adapted from the older versions. The 3rd generation ELISA is performed by many research groups, since it is a fast and relatively cheap technique. 88. Berthe N, Myrvang B, Gundersen SG. Intensity os Schistosoma mansoni, hepatitis B, age and sex predict levels of hepatic periportal thickening/fibrosis (PPT/F): a large-scale community-based study in Ethiopia. Am J Trop Med Hyg. 2007;77(6):1079-86. , 99. Blanton RE, Salam EA, Kariuki HC, Magak P, Silva L, Michiri EM, et al. Population-based differences in Schistosomiasis mansoni and hepatitis C induced disease. J Infect Dis. 2002;1859(11):1644-9. DOI: http://dx.doi.org/10.1086/340574
http://dx.doi.org/10.1086/340574...
, 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. Some authors reject this method because, in S. mansoni, infection could produce auto-antibodies against HCV epitopes, mimicking HCV infection. 33. Agha S, El-Mashad N, El-Malky M, El-Shony H, El-Sherif M, El-Hasan MA, et al. Prevalence of low positive anti-HCV antibodies in blood donors: Schistosoma mansoni co-infection and possible role of auto-antibodies. Microbiol Immunol. 2006;50(6):447-52. However, this immunoglobulin (Ig) production is not well defined in the literature and the auto-Ig’s ratios are low, which can be differentiated from HCV infection by increasing the cut-off point. As for schistosomiasis diagnosis, the method of choice continues being Kato-Katz test, based on the presence of S. mansoni eggs in stool samples or in rectal biopsies, and US patterns to evaluate the periportal fibrosis. 4343. Rey L. Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na áfrica. 3. ed. Rio de Janeiro: Guanabara Koogan; 2001. , 5555. World Health Organization. Ultrasound in schistosomiasis. A practical guide to the standardized use of ultrasonography for the assessment of schistosomiasis-related morbidity. Second International Workshop October 22 - 26, 1996, Niamey, Niger. Geneva; 2000. This review confirms that no significant diagnosis methods have been developed for either disease over the last decades.

The current systematic review also considered risk factors associated with an increased chance of acquiring HCV infection when the subject has SM. 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3636. Mudawi HMY, Smith HM, Fletcher IA, Fedail SS. Prevalence and common genotypes of HCV infection in Sudanese patients with hepatosplenic schistosomiasis. J Med Virol. 2007;79(9):1322-4. DOI: http://dx.doi.org/10.1002/jmv.20865
http://dx.doi.org/10.1002/jmv.20865...
, 3737. Mudawi HMY, Smith HM, Rahoud SA, Fletcher IA, Babikir AM, Saeed OK, et al. Epidemiology of HCV infection in Geriza State of Central Sudan. J Med Virol. 2007;79(4):383-5. DOI: http://dx.doi.org/10.1002/jmv.20780
http://dx.doi.org/10.1002/jmv.20780...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. These data may be useful to direct monitoring and treatment campaigns for both diseases and may contribute to lower prevalence and morbidity rates in the future.

Blood transfusion was the risk factor most cited 66. Aquino RTR, Chieffi PP, Catunda SM, Araújo MF, Ribeiro MCSA, Taddeo EF, et al. Hepatitis B and C virus markers among patients with hepatosplenic mansonic schistosomiasis. Rev Inst Med Trop S Paulo. 2000;42(6):313-20. DOI: http://dx.doi.org/10.1590/S0036-46652000000600003
http://dx.doi.org/10.1590/S0036-46652000...
, 3232. Lacerda CM, Ramos H, Melo IS, Machado IS. Prevalência do anti-HCV e de marcadores do vírus B na esquistossomose hepatesplênica. An Fac Med Univ Fed Pernamb. 1993;38(1):30-2. , 3939. Pereira LM, Melo MC, Saleh MG, Massarolo P, Koskinas J, Domingues AL, et al. Hepatitis C virus infection in schistosomiasis mansoni in Brazil. J Med Virol. 1995; 45(4):423-8. DOI: http://dx.doi.org/10.1002/jmv.1890450412
http://dx.doi.org/10.1002/jmv.1890450412...
, 4040. Pereira LMMB, Spinelli V, Lacerda C, Mies S, Massarolo PCB, McFarlane IG. Hepatite B e C na esquistossomose mansoni. GED Gastroenterol Endosc Dig. 2001;20(3):71-7. , 4545. Silva JLA, Coelho MRCD, Souza VSB, Domingues ALC. Soroprevalência da hepatite C em pacientes com esquistossomose. Rev Para Med. 2008;22(1):27-32. in Brazil and the anti-schistosomiasis parenteral mass therapy, 22. Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994;51(5):563-7. , 1919. El-Sayed HF, Abaza SM, Mehanna S, Winch PJ. The prevalence of hepatitis B and C in fections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997;68(2):229-37. DOI: http://dx.doi.org/10.1016/S0001-706X(97)00097-1
http://dx.doi.org/10.1016/S0001-706X(97)...
, 2929. Kamal S, Madwar M, Bianchi L, Tawil AEL, Fawzy R, Peters T, et al. Clinical, virological and histopathological features: long-term follow-up in patients with chronic hepatitis C co-infected with S. mansoni. Liver Int. 2000;20(4):281-9. DOI: http://dx.doi.org/10.1034/j.1600-0676.2000.020004281.x
http://dx.doi.org/10.1034/j.1600-0676.20...
in Egypt. Poorly sterilized syringes and equipment used during these campaigns 2121. Frank C, Mohamed MK, Strickland GT, Lavanchy D, Arthur RR, Magder LS. The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet. 2000;355(9207):887-91.DOI: http://dx.doi.org/10.1016/S0140-6736(99)06527-7
http://dx.doi.org/10.1016/S0140-6736(99)...
, 2626. Heintges T, Wands J. Hepatitis C virus: Epidemiology and transmission. Hepatology. 1997;26(3):521-6. DOI: http://dx.doi.org/10.1002/hep.510260338
http://dx.doi.org/10.1002/hep.510260338...
may be the key to increased chances of acquiring HCV.

In the HS schistosomiasis form, common in endemic areas, the subject presents esophageal varices in most cases as a consequence of periportal hypertension and disease severity in SM. 4343. Rey L. Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na áfrica. 3. ed. Rio de Janeiro: Guanabara Koogan; 2001. Disruption of these veins can cause digestive bleeding and blood transfusion may be required for patient survival. b b Morais CNL. Avaliação da relação entre marcadores biológicos com os graus de fibrose no complexo hepatite C e esquistossomose [tese de doutorado]. Recife: Centro de Pesquisas Aggeu Magalhães da Fiocruz; 2007.

The serological screening in Brazilian blood banks did not include anti-HCV markers before 1993, in spite of the recent discovery of HCV. Blood transfusion before this year can be considered as a risk factor for HCV acquisition. 1212. Carrazzone CFV, Brito AM, Gomes YM. Importância da avaliação sorológica pré-transfusional em receptores de sangue. Rev Bras Hematol Hemoter. 2004;26(2):93-8. DOI: http://dx.doi.org/10.1590/S1516-84842004000200005
http://dx.doi.org/10.1590/S1516-84842004...
The lack of proper sterilization of equipment and reused syringes during anti-schistosomiasis parenteral mass therapy 2121. Frank C, Mohamed MK, Strickland GT, Lavanchy D, Arthur RR, Magder LS. The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet. 2000;355(9207):887-91.DOI: http://dx.doi.org/10.1016/S0140-6736(99)06527-7
http://dx.doi.org/10.1016/S0140-6736(99)...
, 2323. Habib M, Mostafa K, Abdel-Aziz F, Magder LS, Abdel-Hamid M, Gamil F, et al. Hepatitis C virus infection in a community in the Nile delta: risk factors for seropositivity. Hepatol. 2001;33(1):248-53.DOI: http://dx.doi.org/10.1053/jhep.2001.20797
http://dx.doi.org/10.1053/jhep.2001.2079...
increases the chance of HCV infection in SM patients in Egypt. The causes of HCV infection are different among the countries and in most cases the public policies are adopted as a reflex.

In most articles, the risk factors were based on patient reports and epidemiological history, without significant statistical analyses. More studies are needed to clarify HCV transmission routes and risk factors for HCV/ S. mansoni association. The last study on this issue was published in 2008, pointing to the lack of research in this area.

In conclusion, this revision shows the lack of well-designed studies with appropriate methodology for evaluating the prevalence of this condition in areas of endemic schistosomiasis. Despite the limitations of this study, the results may help to identify regions with higher HCV/ S. mansoni association rates. New public health policies attempting to reduce the current high prevalence and morbidity rates observed in hepatitis C and schistosomiasis could be proposed, especially in SM endemic regions.

ACKNOWLEDGMENTS

To the researchers Sinval Pinto Brandão Filho and Zulma Maria de Medeiros of the Centro de Pesquisas Aggeu Magalhães/FIOCRUZ-PE, for their important guidance.

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  • a
    Maciel RCR. Enzimas caniculares na forma hepatoesplênica da esquistossomose mansoni [dissertação de mestrado]. Recife: Universidade Federal de Pernambuco; 2006.
  • b
    Morais CNL. Avaliação da relação entre marcadores biológicos com os graus de fibrose no complexo hepatite C e esquistossomose [tese de doutorado]. Recife: Centro de Pesquisas Aggeu Magalhães da Fiocruz; 2007.
  • Research parcially supported by fellowship of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES. Post Graduation Program in Public Health of the Centro de Pesquisas Aggeu Magalhães/FIOCRUZ-PE to the PhD thesis of Daniele Silva de Moraes Van-Lume.

History

  • Received
    7 Mar 2012
  • Accepted
    15 July 2012
  • Publication
    June 2013
Faculdade de Saúde Pública da Universidade de São Paulo São Paulo - SP - Brazil
E-mail: revsp@org.usp.br