A Cross-Sectional Study of Viral Hepatitis Perception among Residents from Southeast and North Regions of Brazil

Few data are available regarding viral hepatitis perception among the general global population. The present study aims to estimate the perception of viral hepatitis in a cohort of individuals living in two geographical regions of Brazil: North (Manaus city (MA)) and Southeast (Rio de Janeiro city (RJ)). A cross-sectional, descriptive study was carried out among 287 subjects recruited in MA (134) and RJ (153). All individuals answered a questionnaire assessing socio-demographic characteristics and viral hepatitis awareness. Participants’ responses were scored and divided using interquartile values. Associations between socio-demographic characteristics and knowledge were also evaluated. Interquartile analysis scored 0–21 correct answers as “Very Weak”; 22–27 as “Weak”; 28–31 as “Intermediate”; and 32–47 as “Desirable”. Mean ± standard deviations (SD) of correct responses were weak in both MA (24.1 ± 7.0) and RJ (26.3 ± 7.3). Bivariate analysis showed an association between viral hepatitis awareness and both education level (p < 0.001) and family income (p < 0.01). Desirable scores were more common in female participants (61%), those aged between 21–30 years (40%), those with a secondary education (51.7%), those who received high income (31.6%), and those from RJ (70.0%). Health education campaigns in these cities are recommended to increase knowledge and reduce the transmission of these viruses.


Introduction
A group of viruses known as hepatitis A-E (HAV, HBV HCV, HDV, and HEV) cause viral hepatitis. HAV and HEV are transmitted by ingestion of contaminated food or water while HBV, HCV, and HDV are usually transmitted as a result of parenteral contact with infected bodily fluids, such as during transfusion of contaminated blood or blood products, invasive medical procedures using contaminated equipment, sexual intercourse, and horizontal and vertical transmission [1][2][3].
Viral hepatitis is the eighth primary cause of mortality worldwide, resulting in 1.44 million deaths in 2010 [2]. In Brazil, the prevalences of HAV, HBV, and HCV are low [4][5][6]. The incidence of cases per 100,000 inhabitants in 2016 of HAV, HBV, and HCV were 0.7, 14.0, and 10.8, respectively, in Manaus (MA) and 0.3, 3.3, and 13.4, respectively, in Rio de Janeiro (RJ) [4]. The confirmed cases of HAV, HBV, HCV, and HDV represent 25.8%, 14.2%, 3.1% and 76.8% of all cases in the North region of Brazil, respectively, and 16.4%, 35.4%, 62.2% and 9.8% in the Southern areas of Brazil, respectively, in 2016. Regarding HEV infection, Brazil is considered a moderate endemicity region where HEV prevalence varies from 1% in pregnant women to 17.7% in women at risk for HIV [7].

Study Population
A cross-sectional, descriptive study was carried out to determine viral hepatitis perception among Brazilian individuals living in two cities from North and Southeast Brazil (MA and RJ, respectively). Interviews were conducted in RJ in June 2009 and in MA from July to August 2009 during public health campaigns for infectious disease prevention, such as poliovirus vaccination. All individuals were from the metropolitan region of Rio de Janeiro and North and South-Central regions of Manaus city.
RJ city is situated in the Southern region of Brazil and has 6,453,682 residents, while MA city is located in the Northern region of the country and has 2,020,301 residents. RJ and MA are the second and the seventh most populous cities in Brazil, respectively [16].
The group of participants comprised both genders and inclusion criteria required participants to be 18 years of age and provide signed, informed consent. A sample size of 100 individuals for each location was targeted. Assuming a response rate of 75-80%, 75 completed questionnaires would yield a power of 80% with a 5% type 1 error rate to detect a 16% difference when comparing dichotomous variables between two groups of equal size. The final sample was made up of 287 individuals. No incentive was given to these individuals to participate in this study. The local ethical committee approved the study (protocol 0086.0.317.000-08).

Questionnaire
A specific questionnaire was developed to determine viral hepatitis perception. This instrument was composed of two topics: demographic characteristics and viral hepatitis perception.
Sociodemographic data included gender, age, education, and monthly family income. Monthly family income was determined according to the Brazilian minimum salary (US $276.00). In this fashion, individuals who receive <US $276.00 were grouped as "low family income", individuals who received US $276.00 to US $828.00 were grouped as "intermediate family income", and individuals who receive more than US $828.00 were grouped as "high family income".
Participants' understanding of some viral hepatitis aspects, such as general information, diagnosis, clinical manifestation, transmission, risk factors, complications, and prevention, were assessed. This section of the questionnaire consisted of 3 questions requiring one or more responses and a further 16 questions with the following options: "yes/correct", "no/incorrect", or "do not know". In five questions, individuals were required to inform the type of hepatitis viruses related to their responses (items 4-7, 13) ( Figure 1). Sociodemographic data included gender, age, education, and monthly family income. Monthly family income was determined according to the Brazilian minimum salary (US $276.00). In this fashion, individuals who receive <US $276.00 were grouped as "low family income", individuals who received US $276.00 to US $828.00 were grouped as "intermediate family income", and individuals who receive more than US $828.00 were grouped as "high family income".
Participants' understanding of some viral hepatitis aspects, such as general information, diagnosis, clinical manifestation, transmission, risk factors, complications, and prevention, were assessed. This section of the questionnaire consisted of 3 questions requiring one or more responses and a further 16 questions with the following options: "yes/correct", "no/incorrect", or "do not know". In five questions, individuals were required to inform the type of hepatitis viruses related to their responses (items 4-7, 13) ( Figure 1).  The authors developed this questionnaire following a review of the literature on viral hepatitis aspects [1]. A total of 47 correct answers could be achieved. The questionnaire was standardized by applying it to a set of individuals characteristically representative of but not included in the study population (data not shown and statistical analysis not conducted). Interviewers administrated the questionnaire to the participants as a face-to-face interview in a confidential setting. At the end of the interview, the correct answers were shown to each volunteer. Authors asked for participants in the recruitment setting not to reveal the answers of this interview to other potential participants.
Descriptive statistics were generated for the responses and a chi-squared test for independence or trend was used to compare categorical and continuous variables, respectively, among the perception score groups. The Kruskal-Wallis test was used to evaluate the relationship between nominal and ordinal variables and a p-value < 0.05 was considered statistically significant. A viral hepatitis perception score was created based on all participants' responses according to interquartile values. The 1-4 quartiles were considered very weak, weak, intermediate, and desirable, respectively. Associations between socio-demographic characteristics and perception were also evaluated. All analyses were performed using the Statistical Package for the Social Sciences (SPSS for Windows, release 20.0, SPSS, Chicago, IL, USA). The authors developed this questionnaire following a review of the literature on viral hepatitis aspects [1]. A total of 47 correct answers could be achieved. The questionnaire was standardized by applying it to a set of individuals characteristically representative of but not included in the study population (data not shown and statistical analysis not conducted). Interviewers administrated the questionnaire to the participants as a face-to-face interview in a confidential setting. At the end of the interview, the correct answers were shown to each volunteer. Authors asked for participants in the recruitment setting not to reveal the answers of this interview to other potential participants.
Descriptive statistics were generated for the responses and a chi-squared test for independence or trend was used to compare categorical and continuous variables, respectively, among the perception score groups. The Kruskal-Wallis test was used to evaluate the relationship between nominal and ordinal variables and a p-value < 0.05 was considered statistically significant. A viral hepatitis perception score was created based on all participants' responses according to interquartile values. The 1-4 quartiles were considered very weak, weak, intermediate, and desirable, respectively. Associations between socio-demographic characteristics and perception were also evaluated. All analyses were performed using the Statistical Package for the Social Sciences (SPSS for Windows, release 20.0, SPSS, Chicago, IL, USA).

Demographic Characteristics
A total of 287 individuals were recruited-134 from MA and 153 from RJ. Most participants were female, had a secondary education, were aged between 21-30 years, and had a low monthly family income. Main socio-demographic characteristics are shown in Table 1.

Viral Hepatitis Perception in Manaus City
In MA city, most respondents (>70%) were aware of the existence of hepatitis A-C. However, more than 50% considered hepatitis D and E to be nonexistent. Furthermore, most individuals were unaware that hepatitis can be cured, that individuals cannot have the same form of hepatitis more than once, that there are vaccines for viral hepatitis, and of the differences between acute and chronic hepatitis (Table 2).  Most of the individuals declared that they could collaborate to control hepatitis by "teaching what you learned about the disease to the people who frequent the same places you were infected" (96.3%) and "informing family and colleagues to search for a health service" (93.3%) ( Table 2). It is important to recognize that the information about viral hepatitis should be transmitted to other individuals to help in prevention and control.
Most of the participants claimed that a blood test can be used for diagnosis (91.8%) and that jaundice and fever are symptoms of hepatitis infection (91.0% and 76.1%, respectively) ( Table 2). Regarding transmission, most participants responded that blood (79.9%), sexual contact (70.1%), and water or vegetables without treatment could transmit hepatitis (62.7%), but a minority of participants recognized seafood (26.1%) as a vehicle of transmission. Also, most participants were unable to identify precisely the virus transmitted by seafood, blood, sexual intercourse, or ingestion of untreated water or vegetables (percentages varied from 76.9 to 91.8%) ( Table 3).  A majority of respondents recognized healthcare workers in hospitals and clinical analysis laboratories as groups at risk of acquiring hepatitis (87.3% and 88.1%, respectively). Additionally, most individuals were able to identify cirrhosis (85.8%) and cancer (79.9%) as complications of hepatitis infection (Table 3).
Regarding hepatitis prevention, more than 78% of individuals affirmed that septic tanks, sewage systems, piped water, screening of blood donors, and the use of condoms are means of transmission prevention ( Table 3). Half of the participants cited the existence of viral hepatitis vaccines, but 85% of them did not know the forms of hepatitis against which the vaccines were active (Table 2) and more than 70% claimed that the measles, mumps, and rubella (MMR) vaccine can prevent viral hepatitis (Table 3).

Viral Hepatitis Perception in Rio de Janeiro City
A majority of individuals from RJ (>74%) knew of the existence of hepatitis A-C. Also, most individuals (60.8%) affirmed that hepatitis could be cured and more than 67% did not believe that hepatitis D and E exist ( Table 2).
Most of the participants declared that the population could collaborate to control hepatitis by "teaching what you learned about the disease to the people who frequent the same places you were infected" (78.4%), and "informing family and colleagues to search for a health service" (83.0%) ( Table 2).
Most individuals cited blood tests (95.4%) and biopsies (65.5%) as diagnostic tools for viral hepatitis and more than 65% of individuals recognized jaundice (76.5%) and fever (66.0%) as clinical manifestations of infection (Table 2). Most participants also recognized blood (88.2%), untreated water or vegetables (83.7%), and sexual intercourse (75.8%) as vehicles for hepatitis transmission, and less than 40% of individuals identified seafood as a mode of transmission. Additionally, most of the participants did not know precisely the virus transmitted by seafood, blood, sexual intercourse, or untreated water or vegetables (Table 3).
A majority of individuals cited individuals working in clinical analysis laboratories (85.0%) or hospitals (78.4%), those with tattoos or piercings (76.5%), and drug users (71.9%) as those more vulnerable to hepatitis infection. Cirrhosis (68%) and cancer (58.2) were identified as hepatitis complications ( Table 3).
Most of the participants cited the use of condoms (73.9%), screening of blood donors (70.6%), piped water (69.3%), and septic tanks and sewage systems (64.4%) as effective measures in the prevention of hepatitis transmission (Table 3). Among the participants, 72.5%% were aware of viral hepatitis vaccines, but 75.8% did not know the type of virus prevented by vaccination (Table 2) and 46.4% of individuals believed that the MMR vaccine can prevent viral hepatitis (Table 3).
Females and individuals aged between 31-40 years presented a high mean of correct answers, although it was not significant. Perception was associated with education (p < 0.001), family income (p = 0.001), and city of residence (p = 0.001) in bivariate analysis (Table 4). Desirable scores were more common among females (61%), subjects aged between 21-30 years (40%), those presenting secondary school education (51.7%), and residents from RJ (70.0%). "Very weak" and "weak" perception was more common among individuals who had low family income (71.2% and 85.3%, respectively) ( Table 4).

Discussion
In this study, a poor public perception regarding viral hepatitis was observed in North and Southeast regions of Brazil (average score of 25.3 ± 7.2 correct answers), and knowledge level was significantly associated with family income, level of education, and city of residence.
Most of the individuals answered more than 50% of the questions correctly, but some wrong answers occurred in all sections of the questionnaire (general information, diagnosis, clinical manifestations, transmission, risk factors, complications, and prevention). Saleh et al. [17] found that absence of knowledge among different groups and levels of literacy is not unique to HCV but can also be observed for other forms of hepatitis.
Although the subjects recognized the existence of viral hepatitis, they were unable to identify which hepatitis viruses are transmitted by seafood, blood, sexual contact, or water or vegetables without treatment. Strong et al. (2015) [14] affirmed that misunderstanding of the transmission route may strengthen the stigma against individuals with HBV. The inability to recognize the transmission pathways of different viruses can influence the prevention of these diseases.
Several individuals did not recognize the existence of hepatitis D and E, claimed that blood in the stool can be a complication of viral hepatitis, and did not know that a biopsy could be used for diagnosis. Also, more than half of subjects from both cities did not recognize the differences between the acute and chronic forms of the disease and did not know that the same form of hepatitis cannot be acquired more than once. The difficulty participants had with some general questions about hepatitis demonstrates the importance of health education programs to increase viral hepatitis awareness.
Low knowledge of HEV could be related to the absence of routine, specific HEV diagnosis in central laboratories [7]. This situation could lead to potential cases being unreported. Additionally, while vertical transmission is less common, the mortality of children born to HEV-infected mothers is high [18]. As such, both under-reporting and a lack of prenatal testing of HEV pose both a threat to those at risk and an under-checked source of transmission.
Some questions of this survey could have had more than one answer, such as "can viral hepatitis be cured?". In HBV and HDV infections, there is no cure for chronic infections. This imprecision may have influenced the evaluation of the knowledge of this question; however, as mentioned previously, most of the participants did not recognize the differences between the acute and chronic form and this unfamiliarity could also influence this evaluation.
The majority of respondents recognized the vehicles of transmission as the same as those observed by hairdressers regarding HCV transmission [19]. On the other hand, 81% of participants from a rural village of Egypt did not recognize the routes of HCV transmission and 38% of barbers from Pakistan did not know the transmission routes of HBV and HCV [17,20,21].
In the present study, seafood was not recognized as a source of viral hepatitis transmission, although ingestion of seafood can transmit HAV and HEV [22,23]. This situation could increase the transmission of viruses through this route if individuals are not cognizant of cleaning and disinfection of seafood as viable means of reducing their vulnerability to infection.
Most of the individuals recognized that viral hepatitis diagnosis is made using blood samples, but in MA city, many subjects did not identify biopsies as a method for hepatitis diagnosis. Biopsies are an additional method that allow the prediction of the evolution of the disease. In MA city almost half of the participants reported that urine could diagnose viral hepatitis. Viral hepatitis markers are detected in urine and other biological fluids such as saliva, semen, breast milk, pancreatic secretions, bile and vaginal, tears, menstrual, pleural, and nasopharyngeal [9,24], but the efficiency of detection in fluids like urine is not ideal for diagnosis of all types of hepatitis viruses [25][26][27].
More than 50% of individuals from both cities recognized clinical manifestations of viral hepatitis, but many of them did not know that these symptoms could appear years after the establishment of infection or may not manifest at all. Saleh et al. [17] showed that 45% of the participants did not know about the clinical manifestations of HCV.
The existence of a viral hepatitis vaccine was correctly reported by 50.0% of subjects from MA and 72.5% from RJ. However, 85.1% of respondents from MA and 75.8% from RJ did not know whether or not there were vaccines for HAV and HBV. Unfamiliarity with the existence of HAV and HBV vaccines is an alarming situation since vaccines for HAV and HBV are available in Brazilian Immunization Programs, and would reduce the burden of these infections in our setting. The HAV vaccine was included in the National Immunization Program and has been available in public health clinics for children under two years of age since 2014. HBV vaccination began in 1989 in the Brazilian Amazon region. In 1992, it was offered to all Brazilian children under two years of age and since 1998 it has been recommended in Brazil for all children at birth.
Among the confirmed cases of HDV in Brazil from 1999 to 2016, 78.6% occurred in the North region, and, among these, 50.8% in the Amazonas state [4]. Although the individuals interviewed in MA belong to this state and region, almost 60% of the participants did not know about HDV. These findings, together with the low knowledge about the HBV vaccine-which is a form of HDV prevention-demonstrates a lack of access to information in the North region about this infection and the need for better knowledge regarding measures of HDV prevention. Viral hepatitis perception was associated with education level and monthly family income. A desirable perception was observed among those who have at least completed secondary school and very weak perception among individuals with low family income. Amodio et al. [19] also saw low awareness of viral hepatitis in hairdressers with low education in Italy. These results demonstrate the role of formal education in the dissemination of infectious disease perception and the absence of knowledge in poor communities.
The present study has some limitations: (i) absence of information regarding the neighborhood of each participant; (ii) high diversity of occupations reported by each in this sample; (iii) lack of control for confounding factors and multivariate analysis model; (iv) the study was conducted in 2009 and several measures by public health authorities in Brazil have since been conducted. These measures included the publication of clinical guidelines for therapy of Hepatitis B and C, Brazilian seroprevalence studies for Hepatitis A-C, the inclusion of rapid tests for diagnosis, the distribution of HBV vaccines to all individuals, and the inclusion of new direct antiviral agents for HCV treatment. Despite these limitations, few data are available regarding the knowledge of hepatitis and the present study is important in showing the concepts about these viruses in this period. The data observed is pertinent to the improvement of methods for assessing the public knowledge of viral hepatitis.

Conclusions
In conclusion, a weak level of perception about viral hepatitis was observed in both cities. Knowledge levels were associated with education and family income. It is necessary to conduct health education campaigns to increase viral hepatitis awareness in these cities so that the transmission of these viruses might be reduced.