Association between Schistosomiasis mansoni and hepatitis C: systematic review

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

doi:10.1590/S0034-910.2013047004247

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Review • Rev. Saúde Públ. 47 (2) • June 2013 • https://doi.org/10.1590/S0034-910.2013047004247 copy

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

Authorship SCIMAGO INSTITUTIONS RANKINGS

OBJECTIVE:

To perform a systematic review of the prevalence of the HCV/ S. mansonico-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

Faculdade de Saúde Pública da Universidade de São Paulo Avenida Dr. Arnaldo, 715, 01246-904 São Paulo SP Brazil, Tel./Fax: +55 11 3061-7985 - São Paulo - SP - Brazil
E-mail: revsp@usp.br

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[1] The authors declare that there are no conflicts of interests.

Author	Country	Type of study	Objective

Silva JLA et al⁴⁵ (2008)	Brazil	Cross-sectional	To obtain the serological prevalence for HCV in SM patients
Mudawi HM et al^36,a (2007)	Sudan	Cross-sectional	To determine the prevalence of HCV and identify the most common genotype in patients with HSS
Mudawi HM et al^37,a (2007)	Sudan	Population based cross-sectional	To determine the HCV prevalence and the risk factors associated, in a population living in SM endemic area
Berthe N et al⁸ (2007)	Ethiopia	Population based cross-sectional	To elucidate determinants of morbidity in SM
Blanton RE et al⁹ (2002)	Egypt and Kenya	Population based cross-sectional	To compare the severity of hepatic lesions and morbidity in co-infection in two populations with different epidemiological patterns for SM and hepatitis C
Pereira LMMB et al^40,a (2001)	Brazil	Cross-sectional with an external control group	To analyze the frequency of HBV and HCV markers and to correlate this with severity of hepatic lesions in co-infected patients
Kamal S et al^29,a (2000)	Egypt	Cross-sectional	To investigate the influence of SM on chronic hepatitis C with respect to the natural course of the disease and others parameters
Aquino RTR et al⁶ (2000)	Brazil	Retrospective cases series	To evaluate the frequency and the consequences of the co-infection of hepatitis B and C in patients with HSS
El-Sayed HF et al^19,a (1997)	Egypt	Cross-sectional	To determine the prevalence of HBV and HCV in a endemic area for SM and the risk factors associated with co-infection
Pereira LM et al³⁹ (1995)	Brazil	Cross-sectional with an external control group	To investigate the HCV participation in severity of hepatic lesions in SM patients
Abdel-Wahab MF et al² (1994)	Egypt	Prospective cases series	To estimate the prevalence and magnitude of HCV infection in Egypt
Kamel MA et al³⁰ (1994)	Egypt	Population based cross-sectional	To determine the epidemiological relationship between SM and HBV and HCV serologic markers
Lacerda CM et al^32,a (1993)	Brazil	Cases series with an external control group	To study the HBV and HCV serologic markers in 50 patients with HSS and compare the results with 50 controls

Population size	Population characteristics	HCV diagnosis	SM diagnosis	Prevalence of Association

184 subjects⁴⁵	41.3% male	Anti-HCV ELISA 3^rd generation	Not mentioned	11.9%
176 subjects³⁶	81.3% male Mean age = 41.4	Anti-HCV ELISA 3^rd generation HCV RNA PCR and genotype	Clinical and history examinations Ultrasonography (US) with periportal fibrosis (PPF)	4.5% for anti-HCV 2.3% for HCV RNA PCR
410 subjects³⁷	45% male Mean age = 35 91% have SM infection	Questionnaire Anti-HCV ELISA 3^rd generation HCV RNA PCR	Presence of ova in stool samples Epidemiological history	2.2%
2.451 subjects⁸ 1.615 SM infected	52.1% male Mean age = 18.8	Anti-HCV 3^rd generation	Kato-Katz Questionnaire US	21-30 years old = 1.6% 31-40 = 0.8% > 40 = 1%
237 Kenyans⁹ 112 Egyptians	Mean age Kenyans: 33.1 Mean age Egyptians: 34	Anti-HCV ELISA 3^rd generation RT-PCR	Parasitological exams US	Egyptians: 39.7% Kenyans: 11.3%
234 subjects⁴⁰ 50 controls	Mean age: 39 55.1% male; 44.9% female	Anti-HCV HCV RNA PCR	Clinical examination Presence of eggs in stools or rectal biopsy	20% for anti-HCV 12.4% for HCV RNA PCR
126 subjects²⁹	84 men (66.6%) Mean age = 43 Group A (n = 33): HCV infection; mean age = 44.2 Group B (n = 30): Schistosomiasis; mean age = 38.2 Group C (n = 63): co-infection; mean age = 41.5	Anti-HCV ELISA 2^nd generation HCV RNA PCR	Presence of eggs in stool or rectal biopsy Epidemiological history	50%
101 HSS patients⁶	Mean age: 40.31 42.6% male 75.8% Caucasian; 8.1% black; 16.2% mixed ethnicity	Anti-HCV HCV RNA PCR	History and clinical examinations Medical records	12.9%
506 subjects¹⁹	Mean age: 20 52% male; 48% female	Anti-HCV ELISA 2^nd generation	Kato-Katz technique US	10.3% 28% in people more than 40 years old
215 patients³⁹ 50 controls	SM: 43 with HIS 173 with HSS 115 male (53.4%) Mean age = 38 Controls: 21 male (42%) Mean age = 45	Anti-HCV ELISA anti-core and NS3/NS4 Nested PCR	History examination Presence of Schistosomaeggs in stools or rectal biopsy Liver biopsy	22% in patients 2% in controls
354 adults²	Patients admitted to Kasr El Aini Hospital, in Cairo, for chronic hepatic diseases evaluation	Liver function tests, liver biopsies Anti-HCV ELISA 2^nd generation	History examination Liver function tests US Liver biopsies	32.9% 77% were male
1,550 subjects³⁰	Mean age = 20.2	Anti-HCV ELISA 2nd generation in duplicate samples	Kato-Katz US compatible with PPF	15.3%
50 HSS patients (G1)³² 50 controls (G2)	G 1: SM patients, 46% male; mean age = 41 G 2: 42% male; mean age = 44.4	Anti-HCV ELISA 1^st generation	Medical records	20%

Risk factors for HCV	Results	Conclusion

Blood transfusion⁴⁵ Digestive endoscopy	90.5% of co-infected had HSS form 54.5% received blood transfusion	Blood transfusion and endoscopy history are associated with the increase of HCV prevalence in HSS form.
No risk factor^36,a	Genotype 4 was the most prevalent in HS patients. The parenteral therapy was not associated with co-infection	The HCV prevalence in HS patients is considered low (4.5%) and the genotype 4 is the most common in Sudan.
No risk factor^37,a	91% had SM 11.2% had anti-HCV+, only 2.2% were HCV RNA PCR+ Between 21 and 40 years old, the anti-HCV reactivity was 7.8%	HCV infection has low prevalence in Sudan and the anti-SM parenteral therapy cannot be associated with co-infection.
No risk factor⁸	65.9% were positive for SM 1.3% subjects with SM were positive for HCV The highest prevalence was found among children	It is necessary to integrate helminth control targeting school-aged children to reduce the risk of PPF in future.
Age older⁹ Genetic background	OPG mean was higher among the Kenyans than Egyptians The PPF pattern was higher among Egyptians Hepatitis C is 3 times more prevalent among Egyptians	Geographical differences are observed in relation to PPF patterns among the two populations. HCV is associated with active infection only among Egyptians, who present more severity and morbidity for co-infection.
Blood transfusion^40,a	57% were positive for HBV or HCV or both	HCV infection may contribute to severity of liver damage when the subject has the HSS form.
Anti-SM therapy (76%)^29,a Blood transfusion (22.2%) Nosocomial exposure	The mortality in group C was 48% after 6 years in comparison with group A (12%) and B (3%). HCC is most frequent in co-infected (33%) patients than mono-infected. Mortality was not affected by age, HCV RNA titer or genotype virus	Patients co-infected are characterized by more advanced liver disease, higher HCV RNA titers, predominance of HCV genotype 4, higher inflammatory activity, incidence of cirrhosis and HCC with much higher mortality rate.
Blood transfusion⁶	84.6% of anti-HCV+ had HCV RNA PCR+ with high aminotransferases, more cell decompensation and high rate of chronic hepatitis	The rate of hepatitis B and C markers in HSS patients is higher than control group and it is responsible for a high frequency of liver damage.
History of surgeries^19,a Anti-SM parenteral treatment	Anti-HCV was positive in 10.3% of subjects and 5% was positive for anti-HBV and anti-HCV	Hepatitis B and C are the major public health problems in Egypt. Studies about epidemiology, natural history, risk factors and modes of transmission are necessary.
No significance between groups was found for blood transfusion³⁹	The HCV prevalence in co-infected group was higher (22%) than in control group (2%). 61.7% of co-infected had HCV-RNA circulating with high levels of liver enzymes, especially in HSS decompensated form	Co-infection is a major factor contributing to the severity of liver disease in chronic SM and active replication of the virus in the liver or at extra-hepatic sites is strongly associated with severe liver disease.
Blood transfusions² Hemodialysis Anti-SM parenteral treatment	The prevalence of anti-HCV was 46% in renal chronic patients, 22.1% in soldiers and 47.2% in chronic hepatic diseases	HCV infection prevalence is high in Egypt, especially among patients with liver disorders. More studies are necessary to confirm this transmission route.
No risk factors³⁰	About 1550 samples examined by Kato-Katz technique, 49.1% were positive for SM. The anti-HCV was + in 15,9%, and increases with age	No relationship among HBV or HCV and S. mansoniinfection is found in those living in endemic area for SM, with statistical significance.
Blood transfusion^32,a Sporadic contamination	Prevalence of HCV serologic marker was 20% in group 1 and 4% in group 2. Among 10 HSS patients, 7 had received blood transfusion	A high prevalence for anti-HCV markers is found in SM patients in comparison with healthy people.