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Liver Fibrosis in Individuals With Hepatitis C Virus Genotype 1B From Brazilian Eastern Amazon

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23 February 2023

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27 February 2023

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Abstract
INTRODUCTION Hepatitis C virus (HCV) has a high genetic diversity, with seven genotypes with 86 subtypes. This genetic variability confers persistence in the infection and escape of the immune system with evolution to cirrhosis and cancer. Environmental factors can contribute to different disease progression, being essential to assess the viral genotype in the infection and discuss the environmental particularities of Eastern Amazon, and the frequencies of Liver fibrosis between different HCV genotypes in patients living in a region of the Brazilian Eastern Brazilian Amazon. METHODS Consists in an observational cross-sectional study. Sociodemographic and clinical data of 76 individuals diagnosed with Hepatitis C between 2019 and 2020 in public health services were selected. Data collected was tabulated in Microsoft Excel 2010TM spreadsheets and analysed in GraphPad Prism 5.0TM. Liver fibrosis was associated with genetic subtypes. RESULTS Subtype 1b was predominant (42.1%), followed by 1a (13%) and 3a (1.3%). 69.7% of participants had chronic hepatitis, with mild fibrosis (F1/F2) being the most prevalent (38.1%). Severe fibrosis was detected in 75% of individuals infected with the subtype 1b, that is associated with more severe disease. CONCLUSIONS We suggest further studies, to assess other communities in the region, as well as the monitoring of these patients with Liver Elastography to determine the disease evolution and its better management.
Keywords: 
Subject: Biology and Life Sciences  -   Virology

Introduction

Hepatitis C virus (HCV) is a virus with a global infection incidence of 70 million worldwide1. Brazil’s northern region shows highest prevalence rate of this disease, and the states of Pará (Eastern Amazon) and Acre (Western Amazon) have the highest rates of this region, with 2% and 5.9%, respectively14. Complications will be developed by 55 - 85% of infected people. Liver Cirrhosis and hepatocellular carcinoma were responsible for approximately 290,000 deaths associated with the disease in the year of 20192,3,4. Chronic HCV is one of the main health problems globally, with highest rate of complications in comparison to other viral hepatitis.5,6,7.
HCV exhibits a high genetic diversity, with seven genotypes being described, subdivided into 86 subtypes. This genetic variability provides viral persistence, its mechanisms of immune escape, and increase the risk of evolution to cirrhosis and cancer. The determination of the virus genotype is important because it is related to clinical presentation and prognostic8,9,10. The most prevalent HCV genotypes in Amazon region are related with development of Liver fibrosis that are associated with disease complications.
The Amazon population is exposed to environmental factors that would influence the diseases evolution. The effects of rainforest fires or agrobusiness actions directly impact in ecosystem structure, favouring the endemic diseases11; vulnerability of populations with lack access of health services, basic sanitation, and adequate nutrition12; and genetic factors related to miscegenation of brazilian population must be considered. There is epidemiological evidence that the genotype of this virus associated with these environmental, and individual behaviours influence in the disease progression13.
There are few studies associating clinical data of Liver Fibrosis with the viral genotypic classification in Eastern Amazon. This study aimed to identify the degree of liver fibrosis and HCV genotypes in patients from a community located in the Eastern Brazilian Amazon.

Material and Methods

The study was approved by the Research Ethics Committee of Biologic and Health Centre, State of Pará University (opinion nº 4.478,618), being conducted in accordance with Helsinki Declaration for Research with human-beings, the data of participants was accessed from databases after authorization of Health authorities.
This was an observational cross-sectional study with quantitative, descriptive, and analytical characteristics. The sample consisted of patients residing in the city of Abaetetuba, Pará, Eastern Brazilian Amazon, evaluated in the public health services between years 2019 and 2020.
Data were collected from 103 patients aged ≥ 18 years. Twenty-seven patients were excluded from the study due to non-performance of viral load and/or genotyping tests (n=24) and co-infection (n=3): Human Immunodeficience Virus (HIV) (n=1) and Hepatitis B Virus (HBV) (n=2); resulting in a final sample of 76 clinical records analysed.
The clinical and epidemiological data were extracted from the patients’ clinical records of viral hepatitis investigation from Notifiable Diseases Notification System (SINAN) and Sexual transmitted infectious diseases department (CTA/SAE). This database contains (i) the Notification Form for viral hepatitis which contains the sociodemographic data, (ii) the results of viral load tests, (iii) the results of viral genotyping, and (iv) the report of Liver Elastography exam (FibroscanTM, Echosens SA, Paris, France).
The FibroscanTM transient elastography consists in a non-invasive exam that evaluates the hepatic parenchyma at 25-65 mm of the skin in the same intercostal space where the liver biopsy is performed. The patients were classified in the following fibrosis stages: F0 < 7.1 kPa (normal liver), F1 (mild fibrosis), F2 (mild to moderate fibrosis), F3 (severe fibrosis), and F4 (cirrhosis) 31, 32, 33.
The data was organized in Microsoft Excel 2010TM (Microsoft Software Inc., Richmond, USA) spreadsheets and analysed using GraphPad Prism 5.0 software (GraphPad Software Inc., San Diego, USA). Data with normal distribution were analysed using Student’s T-test, while data without normal distribution were evaluated using Chi square or Fisher’s exact test. An alpha-level of 0.05 was adopted to reject the null hypothesis.

Results

Sociodemographic profile of study participants shows an predominance of male patients (67.1%) and those aged ≥ 60 years (53.9%), who are married or in stable union (69.7%), self-declared Dark-skinned (73.7%), residing in the urban area (85.5%). with more than nine years of education (59.2%) (Table 1).
Clinical profiles of the cohort indicated that the degree of fibrosis measured were classified as mild /mild to moderate fibrosis in 38.1% of cases (F1[14, 18.4%] /F2[15, 19.7%]). There are a high prevalence of fibrosis degree classified as cirrhosis [F4(13, 17.1%)]. The most prevalent genotype was genotype 1 (55.3%), followed by genotype 3 (28.9%). The most expressive sub genotype was 1b (42.1%) (Table 2).
Genotypes and sub genotypes of the participants were associated with the degree of fibrosis. There is a difference between the different degrees of fibrosis related to their sub genotypes. Participants without fibrosis had type 1a sub genotype predominantly (3, 60%), while those with severe fibrosis (F3)/ cirrhosis (F4) (15, 75%), and mild (F1)/ mild to moderate (F2) fibrosis (9, 60%) had 1b sub genotype (Figure). There was no significant difference in the genotype of patients according to the different degrees of fibrosis; thus, patients without fibrosis (F0) (5; 62.5%), with mild (F1) / mild to moderate (F2) fibrosis (15; 55.6%), and with severe fibrosis (F3) / cirrhosis (F4) (16; 80%) had mostly type 1 genotype, between individuals infected with subtype 1b (15; 75%) are diagnosed with severe fibrosis (F3)/ cirrhosis (F4) (Table 3).

Discussion

In this study, most individuals with HCV were male and aged ≥ 60 years. 59.2% of the participants had 9 years or more of education. There was a predominance of dark-skinned (73.7%). With regard to transmission, 60.5% of patients stated that it occurred by blood transfusion. Genotype 1 had the highest prevalence rate (55.3%), type 3 was the second most prevalent type (28.9%), followed by type 2 (2.6%).
Men are more vulnerable to the risks of hepatitis C, their biological, social, behavioural, and cultural issues, with turn them more vulnerable to HCV infection. They have a greater intensity of sexual activity and seek for health services with less frequency than women15. In a 2014 study, 50% of the patients had a complete high school education, which was not protective in terms of preventing HCV infection16.
The genetic heterogeneity of population may impact the frequency and distribution of polymorphisms17. Latin American population was composed by native americans, europeans, mostly from Spain and Portugal, and africans, that conferred a predominance of dark-skinned or black people in Brazilian and Amazonian population18. About 30 million people are living in Amazon region, including quilombolas, indigenous people and riverine communities, as well as people of urban centers11. In this region, several people do not have adequate housing and basic sanitation conditions, and access to health services and adequate nutrition12, it creates the conditions to maintenance and spread of infectious diseases, that can potentially modify the development of HCV infection.
The majority of study participants developed the chronic form of the disease. It is known that infection occurs mainly through contact with contaminated blood. Transfusion of blood and blood products was the main risk factor for hepatitis C transmission in the past, which resulted in a 10% risk of acquiring infection16, and the chronic form of the disease are the main clinical form of cases of hepatitis C, with > 60% of cases in almost all age groups analysed4. Furthermore, another factor that may be related to the chronicity of the disease is the occurrence in people with less access to information and health services, as this vulnerability is a risk factor for infection and not early diagnosis19.
The environmental and socioeconomic reality of Amazon region, linked to agrarian economy of region have an influence in evolution of infectious diseases11. The contamination of water, soil, air, and food by mining activity, deforestation, and rainforest fires causes loss of biodiversity, alteration in the structure and function of ecosystem, contributing for climate changes, and impacts in the behaviour of disease-transmitting vectors20. The interaction of population with other endemic infectious diseases, such as Malaria, Dengue, Zika, Chikungunya, Yellow Fever, Chagas Disease, HIV, HTLV, and others, as well as the relationship between these pathogens and HCV would be related with the disease evolution in this population (Figure).
Genotype 1 had the highest prevalence rate (55.3%). Type 3 was the second most prevalent type (28.9%), followed by type 2 (2.6%) in the studied region. This result corroborates other studies conducted in the Brazilian Amazon and Latin American countries. Regarding sub-genotypes, the most prevalent subtype was 1b (42.1%). Studies carried out in other locations corroborate the results of this research, in the Eastern Amazon16, 21,22, 23, Paraguay and Colombia24,25, and recent studies from Northern, Southern and Eastern Europe have also shown the predominance of genotype 126,27,28.
Studies of genotypic distribution is important for a better understanding of the epidemiological profile and the clinical, diagnostic, and therapeutic measures to be adopted. The subtypes 1b and 3a are associated with more severe forms of the disease, including a major risk for development of hepatocellular carcinoma29,30.
80% of the Individuals infected with HCV genotype 1 who had their degree of fibrosis measured were diagnosed with severe fibrosis/cirrhosis (F3/F4), as well as, 75% of the infected with sbtype 1b. It is known that the weighting of the fibrotic degree of the liver in patients with hepatitis C has a high value in terms of diagnosis and prognosis, since approximately 20% of patients with chronic disease can have progression to liver cirrhosis31. Liver fibrosis grade according to the liver elastography test, which is a non-invasive, validated diagnostic method used to identify and classify liver fibrosis, was classified as follows. F0 (without fibrosis) < 7.1 kPa; F1/F2 (mild/ mild to moderate fibrosis) 8.8–9.5; and F3/F4 (severe fibrosis/ cirrhosis) 9.6 to ≥ 12.532, 33, 34.
However, 18.4% (n=14) of the participants did not undergo an examination to verify the degree of fibrosis. These data are worrying, as it is of fundamental importance to determine the degree of fibrosis so that the patient can receive the suitable therapeutic measures and the most appropriate follow-up for their clinical condition. It is known that, even today, the gold standard for this determination is liver biopsy; and despite Liver transient elastography be an efficient non-invasive technique, have a high cost and is less available in public health centres32,35.

Conclusion

The study revealed the high predominance of genotypes 1 and 3 and subtypes 1a, 1b, and 3a among the studied population, with a higher prevalence of severe liver fibrosis (F3) and cirrhosis (F4) between individuals infected with genotype 1, subtype 1b. These HCV genotypes are the most prevalent in the national territory, being associated with more aggressive clinical forms. The results of this study allow us to elucidate the genotypic behaviour of HCV and its association with liver fibrosis and cirrhosis in the Brazilian Eastern Amazon, which is known to be a region of high prevalence for the virus, and with environmental factors that would impacts in the evolution of diseases.

AUTHORS’ CONTRIBUTION

TLS, ARND, JASQ and LFMF conceived the project, wrote and reviewed the manuscript, performed the analysis of data and images. All authors reviewed and approved the article.

CONFLICT OF INTEREST ESTATEMENT

The authors declare that they have no conflict of interest.

ACKNOWLEDGMENT

The authors thank all patients who agreed to voluntarily participate in the study and PAPQ program (UFPA).
  • Tatiane Lobato da Silva.
    Health and Biological Centre, State of Pará University, 2623 Perebebui St,
    Belem, Pará 66087-670, Brazil.
    tatianelobato34@gmail.com
  • Apio Ricardo Nazareth Dias.
    Health and Biological Centre, State of Pará University, 2623 Perebebui St,
    Belem, Pará 66087-670, Brazil.
    apio.dias@uepa.br
  • Juarez Antônio Simões Quaresma.
    Health and Biological Centre, State of Pará University, 2623 Perebebui St,
    Belem, Pará 66087-670, Brazil.
    Tropical Medicine Centre, Federal University of Pará, 92 Generalissimo
    Deodoro Ave, Belém, Pará 66055-240, Brazil
    juarez@ufpa.br
  • Luiz Fábio Magno Falcão
    Health and Biological Centre, State of Pará University, 2623 Perebebui St,
    Belem, Pará 66087-670, Brazil.
    University of São Paulo, 455 Dr Arnaldo Ave, São Paulo, São Paulo 01246-903, Brazil
    fabiofalcao@uepa.br

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Figure. Hepatitis C virus genotypes, environmental factors and Liver fibrosis in Eastern Amazon Legends: Subtype 1b, 1a and 3a are the most prevalent in Eastern Amazon, Subtype 1b is related to Advanced and Mild Liver fibrosis, the individuals with fibrosis have a risk to development of Liver cirrhosis of 20%. Associated to HCV infection, the environmental factors as ethnic diversity, social vulnerability, diversity of pathogens in Amazon region, and the risk behaviors increase the risk of worse prognostic.
Table 1. Sociodemographic profile of patients with hepatitis C, Abaetetuba, Pará, Brazil (2019- 2020).
Table 1. Sociodemographic profile of patients with hepatitis C, Abaetetuba, Pará, Brazil (2019- 2020).
SOCIODEMOGRAPHIC PROFILE n % P-Valor (1)
AGE
Up to 59 years old 35 46.1% 0.491ns
> 60 years old 41 53.9%
Sex
Men 51 67.1% 0.004*
Women 25 32.9%
COLOR/RACE
White 12 15.8% 0.000*
Black 8 10.5%
Dark-skinned 56 73.7%
SCHOOLING
Up to 9 years of study 31 40.8% 0.136ns
> 9 years of study 45 59.2%
Incomplete/complete higher education 0 0.0%
MUNICIPALITY OF RESIDENCE
Abaetetuba 71 93.4% 0.000*
Others 5 6.6%
AREA OF RESIDENCE
Rural area 11 14.5% 0.000*
Urban area 65 85.5%
OCCUPATION
Retired		 29 38.2% 0.051ns
Active work 47 61.8%
MARITAL STATUS
Married / Stable union 53 69.7% 0.001*
Single/ Widower 23 30.3%
POSSIBLE FORM OF TRANSMISSION
Surgical 43 56.6% 0.000*
Blood transfusion (Parenteral route) 46 60.5%
Sexual Route 3 3.9%
Not informed 20 26%
CLINICAL FORM
Acute 4 5.3% 0.000*
Chronicle 53 69.7%
Not filled 19 25.0%
(1) Pearson's Chi-square (Wilks’ G²) test for independence (p-value < 0.05).*Significant Values; ns - Non-Significant Values.
Table 2. Clinical profile of patients with hepatitis C according to the degree of liver fibrosis and the genotype of the hepatitis C virus, Abaetetuba, Pará, Brazil (2019-2020).
Table 2. Clinical profile of patients with hepatitis C according to the degree of liver fibrosis and the genotype of the hepatitis C virus, Abaetetuba, Pará, Brazil (2019-2020).
CLINICAL PROFILE n % p-value (1)
FIBROSIS CLASSIFICATION
F0 8 10.5% 0.140ns
F1 14 18.4%
F2 15 19.7%
F3 8 10.5%
F4 13 17.1%
Exam not performed 14 18.4%
Exam performed/not valid measures 4 5.3%
ELASTOGRAPHY (RESULT IN KPA)
1.2-6.2 11 14.5% 0.000*
6.2-11.2 32 42.1%
11.2-16.2 6 7.9%
16.2 ou mais 9 11.8%
GENOTYPE OF HEPATITIS C VIRUS
1 42 55.3% 0.001*
2 2 2.6%
3 22 28.9%
HEPATITIS C VIRUS SUBGENOTYPE
1a 10 13.2% 0.000*
1b 32 42.1%
3a 1 1.3%
Not Subtyped 10 13.2%
(1) Pearson’s Chi-square (Wilks’ G²) test for independence (p-value < 0.05). *Significant Values; ns - Non-Significant Values.
Table 3. Distribution of patients with hepatitis C according to the genotypes, sub-genotypes, and liver elastography test (Kpa), Abaetetuba, Pará, Brazil (2019-2020).
Table 3. Distribution of patients with hepatitis C according to the genotypes, sub-genotypes, and liver elastography test (Kpa), Abaetetuba, Pará, Brazil (2019-2020).
Genotypes/Subgenotypes F0
(n = 8) 		F1/F2
(n = 27) 		F3/F4
(n = 20) 		p-value (1)
n % n % n %
Hepatitis C virus genotype
1 5 62.5% 15 55.6% 16 80.0% 0.607ns
2 0 0.0% 1* 3.7% 0 0.0%
3 3 37.5% 11 40.7% 4 20.0%
Hepatitis C virus subgenotype F0
(n = 5) 		F1/F2
(n = 15) 		F3/F4
(n = 20)
1a 3 60.0% 4 26.7% 3 15.0% 0.002*
1b 2 40.0% 9 60.0% 15 75.0%
3a 0 0.0% 0 0.0% 1 5.0%
Not subtyped 0 0.0% 2 13.3% 1 5.0%
(1) Pearson’s Chi-square (Wilks’ G²) test for independence (p-value < 0.05). *Significant Values; ns- Non-Significant Values.
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