Introduction

The Egyptian government has taken successful measures to control Hepatitis C Virus (HCV) as a public health threat, with a high potential for eliminating this disease before 2030. Efforts for achieving this goal should not be limited to testing and treatment only, but should also target the level of behavioral development that is still defective.

The World Health Organization (WHO) has recently formulated the ‘Global Health Sector Strategy on Viral Hepatitis, 2016–2021 with service coverage targeting to eliminate HCV as a public health threat by 2030 [1, 2]. Action to combat viral hepatitis has now been integrated into the United Nations’ 2030 Agenda for Sustainable Development [3].

One of the countries that was most affected by hepatitis C virus (HCV) is Egypt. According to the data of the Egyptian Health Issues Survey (EIHS), 14.7% of the people aged 15–59 years had an active hepatitis infection in 2009 [4], which decreased to 7% in 2015 [5] and was substantially higher than global levels [6]. To face this challenge, Egypt developed a national strategy for HCV control and established HCV prevention and treatment programs. This strategy covers six main components of prevention and control: surveillance, infection control, improving blood safety, hepatitis B vaccination, health education to providers and communities, and care and treatment [7, 8].

Scientific research clearly shows that personal health behaviors played a major role in endemicity of hepatitis, mainly hepatitis C in Egypt [9–12].

Prevention is the only safeguard against epidemics of viral hepatitis. Knowing facts, having proper attitudes and adopting certain behaviors are critical in preventing the spread of HCV in Egypt [13]. However, little is known about the extent to which Egyptians are participating in practices that limit the spread of HCV and their level of awareness. There have been very few attempts to evaluate the Knowledge, Attitudes and Practice (KAP) regarding HCV infection [14].

Communication for development (C4D) approach was designed to help meet national development goals aiming at promoting and solving health problems. C4D goes beyond collecting information about people to understand their beliefs, social and cultural norms to communicate with them at best. C4D is a two-way process for using the gained information to set strategies, take actions and implement programs that empower individuals and communities to improve their lives [15, 16].

The current study was a national formative research survey aiming at assessing the dominance of risk practices associated with HCV endemicity in Egypt to decide which practices could be targeted and identify the behavioral development level concerning different aspects of HCV risk behaviors with respect to age and gender. The survey highlights the most cost-effective strategies that could accelerate HCV elimination in Egypt.

Methods

Results

Our study population consisted of 43.9% males and 56.1% females with a mean age of 33.9±16.5 years and an age range between 10 and 85 years. One quarter (25.4%) of the participants were adolescents while three quarters (74.6%) were adults. About two thirds of the studied population (62.2%) were married. Regarding education, the highest percentage of the studied individuals were illiterate, could read and write (33.3%) which is nearly equivalent to those with secondary or equivalent education (29.5%). Those who had university or higher education were the least percentage (13.3%). About two thirds of the studied population were unemployed (Table 1).

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Table 1. Socio-demographic characteristics of the surveyed participants (n = 3780).

https://doi.org/10.1371/journal.pone.0242257.t001

Regarding misconceptions about the methods of HCV transmission, more than 50% of the participants incorrectly believed that contaminated food (59.3%) and water (65.7%), sharing food utilities (59.1%), schistosomiasis (54.7%) and mosquitoes (50.7%) might lead to HCV transmission. Females had significantly more misconceptions as compared to males (p<0.001) (Table 2).

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Table 2. Misconceptions about practices leading to HCV transmission.

https://doi.org/10.1371/journal.pone.0242257.t002

The six domains concerning the continuum of behavioral development level are shown in Table 3. Regarding the mean scores of the six levels of behavioral development, the awareness score, the perceived risk score and the motivation score were high (60.9±27.5, 65.8±31.9 and 65.7±30.4 respectively). The mean score was <40% regarding rejection, followed by adoption, and the least was the trial (7.7±13.3). However, the mean score of the adoption was only 31.5±28.6. Meanwhile, the awareness score, the perceived risk score and the motivation score were significantly higher among adults, employed, married, Lower Egypt governorates and university educated participants (p<0.001) (Table 3).

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Table 3. Comparison of mean scores of the six domains of behavior development level of participants based on socio-demographic characteristics.

https://doi.org/10.1371/journal.pone.0242257.t003

Table 4 presented community level of practice to certain selected behaviors. The highest self-reported behavior that was rejected by >60% of the participants was not sharing nail cutters (73.8%) followed by not sharing sponges for personal cleaning (63.1%). Regarding adoption, <40% adopted the assessed recommended behaviors. The highest self-reported adopted safe behavior by males was using their own shaving instruments at the barber (67.1%), and by females was not sharing scarves pins (36.9%). In the trial stage, the highest self-reported behavior was asking the barber to change shaving tools by males followed by not sharing toothbrushes. The highest undetermined behaviors to seeking trial were asking barbers to change shaving tools (72.5%) followed by not sharing shaving tools (65.7%). Generally, adults and females significantly show more adoption of most of the safe behaviors when compared to adolescents and males respectively.

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Table 4. Assessment of the level of practice according to certain selected community behaviors.

https://doi.org/10.1371/journal.pone.0242257.t004

Around two thirds (65.2%) of the participants were motivated with the intention to follow up to 4 or 5 out of the 6 recommended behaviors for limiting the HCV problem. Meanwhile, the adoption was observed among only 12.6% of the participants versus 32% who rejected almost half of the recommended safe behaviors (Fig 1). There were no significant differences between genders in most of the levels of behavior development (Fig 2). Adults’ scores of awareness, perceived risk of HCV, motivation towards practicing safe behaviors and adoption were significantly higher than that of adolescents (p<0.001). More than two thirds (68.3%) of the adults were significantly motivated to practice more than 75% of the recommended behaviors versus 59.4% of the adolescents (Fig 3).

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Fig 1. Grading scores per level of behavior development.

https://doi.org/10.1371/journal.pone.0242257.g001

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Fig 2. Gender differences in grading scores of behavior development levels.

https://doi.org/10.1371/journal.pone.0242257.g002

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Fig 3. Differences between adults and adolescents in grading scores of levels of behavior development.

https://doi.org/10.1371/journal.pone.0242257.g003

Table 5 provided suggested strategies to accelerate HCV elimination according to the level of behavioral development stage. Giving a high level of awareness, perceived risk, and motivation to change of participants in the current survey, strategies enhancing trial and adoption of the recommended safe behaviors are needed. Strategies towards the elimination of HCV should be directed to addressing traditional beliefs and false rumors, reinforcing safe behaviors through confidence building, and solving problems that hinder its adoption. HCV public health messages should be effectively disseminated to the target population. Media should disseminate messages that motivate adopting risk-reduction behaviors for hepatitis with special emphasis on poor and neutral behavior (< 75%) to improve the level of this behavior to be good (> 75%). Encouraging and mobilizing the community to try the recommended behaviors is required in order to engage approximately 40% of the participants in trying the recommended behaviors. This could be accelerated by identifying misbeliefs and practices to reinforce ideal ones and to adjust negative ones. Strategy of confidence building so that individuals feel and perceive that not only the community supports the recommended behavior but also the social norms and culture. At this stage multimedia channels are required e.g communities can use supportive statements and messages of respected leaders from each beneficiary and/or use of satisfied acceptors and/or individual counseling.

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Table 5. Suggested strategies to accelerate HCV elimination according to the level of behavioral development stage.

https://doi.org/10.1371/journal.pone.0242257.t005

Strategy of problem solving and creating opportunities to continue and sustain the recommended behaviors to decrease the chance of rejection have to be implemented. Availability of resources to monitor and reinforce recommended behaviors, skills and practices have to be ensured. Individual counseling and psychological rewarding of the recommended behaviors have to be used to sustain the change to the safe practices. Local community members serve as support groups, providing both information about the virus and emotional support.

Discussion

Egypt has had the highest prevalence of HCV infection worldwide for years but has taken the largest step towards the elimination of the disease so far, with the highest treatment campaigns in the world using highly effective regimens of the direct-acting antiviral therapy resulting in mass treatment of nearly two and a half millions of Egyptian HCV patients [21].

More than 2 million individuals have been treated between 2014 and 2017. However, finding individuals unaware of their HCV infection remained a challenge. This pool of undiagnosed individuals, if untreated, are at risk of progressive disease and a potential source for infection [22]. This led eventually to a country state-sponsored mass screening campaign initiative that targeted the whole adult population. Between October 2018 and April 2019 almost 50 million of the population were tested and those positive for HCV were referred to treatment [23]. However, an essential step in elimination of HCV and its sustainability is prevention of transmission largely related to vigilant infection control practices which necessitates awareness, attitude, and adoption of safe practices.

In recent years, there has been increased an interest in application of behavior change theories in the areas of health, education, criminology, energy and international development with the hope that understanding behavioral change will improve services offered in these areas. These theories generally aim at understanding and changing a given behavior [24]. The most prevalent are learning theories), social cognitive theory, theories of reasoned action and planned behavior, trans-theoretical model of behavior change, the health action process approach and the health belief model of behavior change [25].

Success in achieving global developmental goals was dependent largely on the extent to which national planning processes are informed by all sectors of its citizens [26]. The current study applied the process of C4D which starts with informative research for determining the level of behavioral development; including rich and underprivileged, marginalized people, and those with different levels of education. Therefore, C4D could be seen as a supporting tool that can be applied to accelerate and enhance the HCV elimination.

Regarding misconceptions about exposures and practices that could lead to HCV transmission, the participants had some incorrect beliefs about HCV infection and disease, probably from former misperceived messages. More than 60% of the participants believed that virus C is a food-borne and water-borne virus, whereas more than 40% believed that the virus could be transmitted by mosquitoes. These percentages were slightly higher than a similar previous study in Egypt where participants were surveyed about their health beliefs regarding HCV [9] but much higher than a study from Pakistan where less than 15% of the participants stated that water, food, and mosquitoes were methods of transmission [27]. This may be explained by that one third of the population (33.3%) were either illiterate or just read and write. Other misconceptions that could transmit HCV in the current study included sharing food utilities among 55.2% of females and 62.2% of males. In another study, sharing food utilities was wrongly believed as a route of HCV transmission by more than 80% of participants but was reduced to less than 10% after educational campaigns to raise awareness were conducted [14]. More than one-third of the current participants wrongly believed that coughing and sneezing could transmit HCV. The Public health association in Canada stated that Hepatitis C cannot be spread by natural contact, such as kissing, hugging, or by being with someone who is coughing or sneezing. The virus is not present in food or water [28]. Combating misconceptions about HCV is important. Otherwise, dissemination of wrong information about HCV may lead to unnecessary isolation, which may lead to social stigma and depression in infected patients.

One-third (33.3%) of the participants in the current survey were either illiterate or could read and write where more than 50% of the illiterates were from Egypt upper governorates, and only 13.3% had university level of education where more than two thirds (69.6%) were from Middle and Lower governorates. However, it was found that the awareness, perceived risk and the motivation mean scores were more than 60%. Good awareness and high motivation of the current participants is most probably related to the previous community based educational programs [14] and TV mass media awareness campaign in Egypt over several years, complementing the national program for control of viral hepatitis established in 2006 [29]. On the other hand, studies done in China [30], Korea [31], Turkey [32], and Spain [33] showed poor knowledge in the community regarding HCV transmission.

Although, the awareness score, the perceived risk score and the attitude score were high (60.9±27.5, 65.8±31.9 and 65.7±30.4 respectively), the mean score of the adoption was only 31.5±28.6. This is most probably because most of the studied population were socially underprivileged. Hence, they could not afford many of the personal hygienic products. The reality of low income is that it restricts people’s options, leaving them caught between eat or be clean. So low adoption of the safe recommended behaviors in the presence of high awareness and positive attitude is most probably because of not being able to buy a private toothbrush, toothpaste or shaving tools. Therefore, they prefer to share these tools to save money.

Adults’ scores of awareness, perceived risk of HCV, motivation and adoption were significantly higher than that of adolescents (p<0.001). This is most probably due to past educational campaigns [28]. These findings suggest that adolescents may not be aware of the risk of HCV infection and highlight the urgent need for HCV behavioral interventions to reduce ongoing high-risk behavior that perpetuates the risk of HCV transmission. At the same time, for most of the behavioral development levels, males and females were similar. This could be explained by being direct relatives or close neighbors or married. Besides being living in the same environment, they are of a similar socioeconomic standard, hold close levels of education and culture, and are exposed to the same external influences.

The results of the current study were different from another study done in Egypt by Metwally et al., [9] where the percentage of those who tried and adopted the recommended behaviors was statistically higher than those who rejected these behaviors. Also, the percentage of those who rejected the safe behavior of not sharing nail cutters (73.8%) was much higher than another study done by Metwally et al., [10] where only 26.5% of HCV-ve contacts and 29.3% of HCV+ve cases reported sharing nail cutters. The differences are because the old study was conducted on HCV patients who took precise information from doctors and nurses about the importance of following and adopting the recommended behaviors that counteract HCV transmission.

Shaving at the barbershops is a well-known risk factor for HCV infection [34]. Barbers in resource-limited countries are usually unaware of the concept of blood-borne transmission, and razors and scissors are used repeatedly for different customers without intervening sterilization [35]. In the current study, only 4.5% of the males adopted the safe behavior of asking the barber to change shaving tools in front of them. This might be explained by the fact that 67.1% of the males used their own shaving instruments at the barber which is good. Meanwhile, legislations are required to enforce the sterilization of barbers’ equipment.

Toothbrushes are essential to maintain oral hygiene and health [36]. However, sharing toothbrushes may carry a risk of infection [37, 38]. The presence of injuries in the oral cavity associated with the absence of biosafety practices and the presence of contaminated blood during dental treatment could also be a risk factor for HCV transmission [39]. However, the present study showed an alarming situation where nearly half of the participants did not determine whether they would or wouldn’t share toothbrushes and only 53.3% checked the use of sterilized tools at dental clinics in spite of their high awareness and motivation score.

Regarding certain community practices, the results of this survey showed that the highest percentage for those who did not try the recommended behaviors was observed regarding asking the barber to change the shaving tools in front of them (72.5%) and not sharing shaving tools (65.7%). Surprisingly, the study done by Shiha and his colleagues [14] reported that the percentage of participants who were using their own shaving instruments at the barber shop and not sharing shaving tools increased to 75% or more as a result of behavioral intervention, indicating the powerful role of communication for behavioral change. Therefore, the behavior of not asking the barber to change shaving tools in front of them in the current study can be substituted by the behavior of using the persons own shaving instruments at the barber shop as a modified good behavior. The highest percentage that is still at the trial stage was observed for asking the barber to change shaving tools in front of them (16.3%) indicating that this behavior needs supportive strategies for engaging people to try and support its adoption.

A very low level of behavioral adoption indicators (< 25%) was observed regarding not sharing personal tools (nail cutters and shaving tools (24.3% and 23.9% respectively). The highest rejection was observed for some of the family behaviors like not sharing nail cutters (73.8%), not sharing sponges (63.1%), not sharing scarves’ pins for females (53.9%) and for checking the use of sterilized tools at dental clinics (40.5%). In the current study, we focused on behaviors like sharing scarves pins and sponges for personal cleaning among the community. These behaviors were uncovered during the group discussions in a recent study [10] and considered new emerging behaviors carrying a potential risk for HCV infection. They are also culturally sensitive to the Egyptian people and might be behind HCV endemicity. Sharing scarves’ pins by veiled women, which might be contaminated with the blood of HCV infected women, might expose the non-infected women to HCV infection on piercing the scalp or skin. Also sharing the sponge for personal cleaning might expose the non-HCV infected person to infection if the used sponge was contaminated with HCV-infected blood and penetrated any injured skin especially in rural areas with an inadequate amount of water [10].

The current study provides a cost-effective model through which behavioral related problems within low and low-middle-income communities should be tackled. The suggestions emerging from this survey can support the national program in accelerating elimination of HCV and may provide a model for other resource-limited settings with high infection rates. The suggested strategies will result in shifting the level of behavioral development for the low indicators to be neutral i.e. from < 50% to be 50%-75% and the neutral ones to be good (more than 75%).

The suggested strategies are focus on identifying misconceptions and wrong practices, to reinforce ideal ones and to adjust negative ones. Wrong beliefs essentially addressed and corrected included that virus C infection is a food-borne virus that could be transmitted by mosquitoes, could be caused by bilharziasis and could be treated by herbs. This strategy will prevent stigmatization of infected populations, thus they will not miss the opportunities for prevention, testing and treatment which will limit the endemicity of HCV. This will not happen unless misconceptions are corrected. This could be achieved by using focus groups to tackle misconceptions and reinforce social support. Also the use of multimedia could be useful in disseminating detailed information about HCV in order to modify public behavior, dispel rumors, counter myths, and correct misinformation.

Generally speaking, tackling wrong traditional beliefs has to be a prime target in any health intervention program to have a positive impact on the population. Community-based studies provide accessibility to local resources to monitor and reinforce recommended behaviors, skills, and practices. Accordingly, this is should be a way to tackle behavioral related problems within low-income communities. Many community-based studies that were dependent on communication for behavioral development and initially determined communities’ levels of behavioral development were done in Egypt. They were very successful in creating behavior changes aiming at counteracting wrong believes not only for HCV related behaviors [14] but providing support for many other health problems. Successful models of Egyptian studies range from hygiene promotion [40–42], promoting school and breastfeeding [43, 44] promoting safe motherhood and reducing maternal mortality [45, 46], supporting child psychosocial development [47, 48] alleviating health problems like diabetes [49], HBV and vaccination [50, 51], and supporting end-stage renal disease Egyptian patients [52]. Such approach was also successful for sensitive issues like accepting organ donation and resulted in shifting the attitude of almost half of the participants who were refusing posthumous organ donation to become an acceptable issue [53]. A worthy note is that all through stages, services like testing, treatment and care have to be affordable, available and accessible as recommended by patient groups studies from 25 studied countries [54]. In addition, the people offering services have to be competent, approachable and welcoming. Focusing on the social acceptability of some recommended behaviors has to be promoted; for example, using one’s own instruments at the barber/hairdresser and emphasis on the availability sterilized equipment for dental treatment or using one’s own toothbrushes, shaving brushes, and syringes. If the problem is due to unavailability of facilities, it is advisable to provide the missing equipment and devices to improve adoption and decrease rejection level of the recommended behaviors. The recommended behavior has to be rewarded (self-rewarded or externally rewarded) temporarily to sustain safe behaviors (e.g school campaigns and provision of low cost or free personal tools e.g toothbrushes, toothpaste, shaving tools, nail cutters and scarves pins). A study by Michie and colleagues concluded that recognizing the nature of what motivates persons and the economic and social pressures that act upon them will help improve public health behaviors [55].

In conclusion, it is clear that new therapies will not control the disease unless accompanied by increasing levels of behavior development. The current study demonstrated that our participants are concerned about the HCV problem. Health messages about HCV appear to have largely been received and remembered by the adult population. There is some deficit among adolescents reflecting that they have not been effectively exposed to detailed HCV public health messages. Furthermore, misconceptions about HCV transmission is obvious among all shared participants irrespective of gender and age. However, they acquired knowledge and were motivated to try out the majority of the recommended behaviors. Awareness, perceived risk and attitude mean scores were high. On the contrary, trial and adoption of the recommended safe behaviors mean scores were low with considerable high level of rejection of almost half of the recommended behaviors. On the other hand, almost one third of the participants did not try any.

Whereas, much emphasis should be put on the poor indicators for creating messages for inducement of action for improvement, strengthening of the neutral indicators to be shifted to the good ones and maintaining the good ones should be priority actions.

With the availability of an enabling environment in Egypt, the implementation of the recommended strategies to achieve behavioral change is achievable and hence accelerate and sustain the elimination of HCV. In the light of the mass screening, diagnosis, and treatment by competent, approachable, and welcoming health personnel who are offering these services, strategies to reinforce optimizing behaviors or modify negative ones could be implemented.

Supporting information

Acknowledgments

We are deeply grateful to the Ministry of Health and Population (MOHP) staff who contributed to the successful completion of this project especially, head and staff of the epidemiology, gastroenterology and Hepatology departments within the National Treatment Reference Centers of MOHP along six governorates of Egypt: Benisuef and Assuit as representative to urban and rural upper Egypt, Dakhlya and Gharbya as representative to urban and rural lower Egypt, Cairo as representative to middle Egypt and Ismailia as representative to canal region, and to the National Committee for the Control of Viral Hepatitis. Special thanks to all patients for their willing participation and cooperation.