Volume 27, Issue 4 (Autumn 2021)                   Intern Med Today 2021, 27(4): 518-533 | Back to browse issues page

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Hajavi J, Mohammadzadeh A, Kianmehr M, Abbasnezhad A, Nasiri M, Alie M, et al . Evaluation of Protective Antibody Titer Against HBs Antigen in Students of Gonabad University of Medical Sciences in 2018. Intern Med Today 2021; 27 (4) :518-533
URL: http://imtj.gmu.ac.ir/article-1-3654-en.html
1- Department of Medical Sciences of Laboratory, Infectious Diseases Research Center, School of Para-Medicine, Gonabad University of Medical Sciences, Gonabad, Iran.
2- Department of Medical Physics, Faculty of Medicine, Gonabad University of Medical Sciences, Gonabad, Iran
3- Department of Physiology, Faculty of Medicine, Gonabad University of Medical Sciences, Gonabad, Iran.
4- Office of Statistics and Information Technology, Gonabad University of Medical Sciences, Gonabad, Iran.
5- Department of Medical Sciences of Laboratory, Infectious Diseases Research Center, School of Para-Medicine, Gonabad University of Medical Sciences, Gonabad, Iran. , hosein.abtahi@gmail.com
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1. Introduction
Infectious diseases constitute a significant health problem in developing and third world countries, and much of the cost of health care and clinical research is spent on diagnosing and treating these diseases [1].
Viral hepatitis is highly prevalent due to inflammation of the liver and various viruses, drugs, alcohol and adipose tissue replacement, and other factors [2]. Hepatitis B infection alone is the most important cause of liver disease and the leading cause of hepatitis mortality in Iran [3]. The importance of hepatitis B results from its high prevalence and hepatic and extrahepatic complications [4].
The prevalence of the hepatitis B virus is more than 2 billion people in the world, of which 400 million are chronic carriers of the virus, and every year about 53000 new cases are reported [1]. Approximately 45% of the world›s population lives in hyperendemic regions (prevalence greater than or equal to 8%), 43% in the mesoendemic areas (prevalence between 2% and 7%), and 12% in hypoendemic regions (prevalence less than 2%) [5].
Factors such as the prevalence of infection, age, sex, weight, genetic structure, individual immune status, underlying diseases, smoking, obesity, differences between vaccines, location and method of vaccine injection, the time elapsed since last vaccine dose, and amount of contact with a positive S antigen is effective in hepatitis [5].
Hepatitis B virus belongs to the hepadnavirus family [6]. The virus has three major types of antigens: s, c, and e. The presence of HBs antigen is the first sign of infection. This antigen can be detected in 90% to 95% of acute cases, and the antibody produced against it has a protective role [6].
HBsAg is the most common indicator used to diagnose hepatitis B. This antigen is present in acute and chronic infections; continued presence and positive HBsAg for at least 6 months indicates the active state of the infection [7].
The ways of transmission of hepatitis B disease are very diverse, and the commonest way is blood transfusion (blood and blood products) [8]. The effective immune response to the hepatitis B virus depends on the response of various components of the cellular immune system, including natural killer (NK) cells, CD+4 helper T cells, CD8+ killer T cells, and regulatory T cells. Studies have shown that CD4 and CTL memory cells are active in the presence of low levels of hepatitis B virus DNA for up to 23 years after primary infection [9, 10].
Prevention is vital because there is no complete and proper cure for HBV infection [11]. HBV vaccination using a recombinant vaccine with HBs antigen particles is the most effective and safe method of prevention. The vaccination strategy against hepatitis B is based on geographical differences and the epidemiology of hepatitis B. Three doses of the hepatitis B vaccine, which consists only of hepatitis B surface antigen, can produce protective antibodies in 85% of healthy individuals [12].
Vaccination of hepatitis B worldwide for infants as well as people with high-risk conditions, especially health workers in Iran, began in 1993, and since 2006, vaccination of adolescents under 18 years (born in 1989) was added to the program. Vaccination against hepatitis surface antigen can induce antibody-protective levels in most vaccinated individuals. Meanwhile, despite the very high efficacy of the vaccine, about 5% to 10% of people cannot produce antibodies at acceptable levels against hepatitis B surface antigen for various reasons, including genetic factors, immunosuppression, and some specific diseases [13].
Over time, in some vaccinated individuals, the antibody titer decreases [141516]. Studies in Iran have shown different results in terms of antibody titer. The study performed among clinical medical students of Islamic Azad University of Mashhad showed that the mean antibody titer was 186.5 with a standard deviation of 114.9 units and 10 patients (6.5%) [17] had no antibody response. Also, in another study, the hepatitis B vaccine was evaluated for immunogenicity in the medical staff of Shahid Madani Hospital in Tabriz. Of the subjects, 32 had no protective titer, 38 had partial protective titer, and 76 had full protective titer [18].
One of the high-risk groups is students who study in health and medical centers who are exposed to this disease due to a lack of sufficient skills in performing treatment processes. On the other hand, reducing the titer of anti-HBs by reducing immunity is associated with hepatitis B, and in practice, vaccination programs will not be effective [1920]. Therefore, measuring the titer of immunogenic antibodies in high-risk groups of the community , such as medical staff and students to estimate their immunogenicity and immunity in high-risk groups is of particular importance. Therefore, this study was performed to evaluate the hepatitis B antibody titer in students of Gonabad University of Medical Sciences in 2018.
2. Materials and Methods
The current study is a descriptive cross-sectional study in which the study population was students of Gonabad University of Medical Sciences who have entered their clinical internship. An available sampling method was used for this study. The purpose of this study was explained to all students participating in the study. Data collection tools were questionnaires and checklists. All students completed the questionnaires.
The questionnaire included questions related to demographic characteristics and dates of vaccination of students, and a checklist containing weight and test results for hepatitis B antibody titer. The questionnaire also includes information, such as educational level, Body Mass Index (BMI), smoking, history of hepatitis in family members, history of corticosteroids, history of radiotherapy, chemotherapy, leukemia, lymphoma, blood transfusion, history of needle contact, history of suspected, unprotected sexual contact, and had a history of kidney and liver failure . The formal validity and content validity of data collection tools were determined by five faculty members. Information about all students was obtained from the administrators of the relevant group. First, for serum analysis, 5 mL of blood samples were taken from each person and then the samples were placed in a centrifuge and their serum was separated. The isolated sera were all frozen at –18°C. To determine the degree of immunity to hepatitis B infection, anti-HBs titration was measured by leading medical laboratory kits in the immunology laboratory of the paramedical school. The amount of hepatitis B antibody titer was quantitatively determined by the ELISA method. If the antibody titer was less than 10 IU/mL, the immunity was weak. If the antibody titer was between 10-100 IU/mL, the immunity was moderate, and when the antibody titer was more than 100 IU/mL , the safety was considered desirable. After data collection, the data were entered SPSS software version 18. Data were analyzed using descriptive statistical methods in the form of frequency distribution tables and analyzed by the Kruskal-Wallis, 2-sample independent t-test, and Chi-square test to determine the relationship between variables. 
3. Results
According to the study population, students from different disciplines were included in the study, which is listed separately in the (Table 1).

Also, individuals were divided into two groups based on vaccine injection: vaccinated and unvaccinated.
Participants in the study were divided into three groups based on hepatitis B antigen-antibody titer: weak (less than 10 IU/mL), moderate (between 10 to 100 IU/mL), and favorable (more than 100 IU/mL). Then, the titer obtained from the antibody assay is calculated based on gender, age, and status of the titer (weak, moderate, and favorable) and is given separately in the Table.
Out of the total students participating in the study, 106 had a favorable status in terms of antibodies against hepatitis B antigen, and also that the optimal status of antibody titer was higher in women than men (Table 2).

The classification of different groups based on age has been done in four age groups, and the most desirable results of antibody titer have been observed in the age group of 18-21 years, and the important point is that the same group in terms of the weakest titer has the most among other age groups and is statistically significant (Table 3).

Participants were also divided into 3 groups based on body mass index, and their titers were categorized as desirable, moderate, and weak. The results of which are given in Table 4 (P=0.723).

Also, the results of analysis based on the titer and body mass index showed the best favorable titer in people with body mass index exists in the category of 20-26 years. As shown in Table 5, Levene’s test was used to check the equality of the variance of the two groups.

The value of P is less than 0.001; therefore, the equality of variances is rejected, but in the mean equality of the two groups, the value of p=0.016 is less than 0.05.
4. Discussion
Hepatitis B virus is one of the most common and important causes of acute and chronic hepatitis, liver cirrhosis, and cancer in the world [20]. One of the main ways to prevent hepatitis B infection is to be vaccinated and develop proper immunity against it. A high level of safety of personnel working in hospitals and health centers can reduce the incidence of infections among these people [21]. Medical students who come to hospitals as interns are exposed to all kinds of patients› secretions; they are exposed to this disease due to not having enough skills in performing treatment processes, so immunization and immunosuppression after vaccination in this group are important. 
The current study was conducted among 416 students studying at Gonabad University of Medical Sciences in 2018. The current study showed that 106 participants in the study have a favorable status in terms of antibody titer against hepatitis B. In the study conducted by Suleiman and associates on 139 personnel working in Farshchian and Army medical centers in Hamedan, 5.1% of the staff had antibody levels below 10 IU/mL but in %51.8 (217 people), the antibody level was below 10 [22]. These differences may be due to differences in the history of vaccination between the two groups. In our study, the interval between vaccination time and antibody titer is higher than the same time in the study of Suleiman et al. Also, in our study, 25.3% (96 people) had antibody levels above 100 IU/mL which was higher than the study of Suleiman and associates with 3.1%. Regarding the difference between those with a titer above 100, it can be said that due to the younger students, they had higher immunogenicity.
In our study, 51.8% of the participants in the study were without the necessary immunity. The study of Suleiman and associates also showed a decrease in the level of safety in one-third of the subjects. A study by Rostami et al. in Tabriz in 100 at-risk hospital staff showed that 11% of antibody titers were less than 10 (unsafe) 14% of antibody titers were between 10 and 100 (relative safety) and 75% had antibody titers greater than 100 (safe) . They were 3 times safer than our study, but 51.8% were unsafe, which is about five times more than the study of Jouneghani et al. [23].
Consistent with the study of Darvish Moghadam et al. andthe study of Amini et al., the current study showed that the level of antibodies decreases over time after vaccination [2425]. The level of immunity of Iranian health center staff in various studies has been reported from 50% to 90%. In the study of Sarkari et al. in Yasuj hospitals, out of 212 hospital staff who were randomly selected, more than 85% had the necessary immunity [21]. In contrast, in our study, immunity was 25.3% and in the study of Momen Heravi and associates which was performed in Shahid Beheshti Hospital in Kashan, 79.8% of people had an acceptable level of safety [26].
In the study of Khodavisi et al., the immune status of hepatitis in the study population indicates that 66% had good immunity, 28% had poor immunity and 6% of students lacked immunity [27]. Contrary to these results, in our study, the immunity status was poor in 51.8%, favorable in 25.3%, and moderate in 22.9%. In total, 48.8% of the subjects had good immunity to hepatitis B in the study. But in the study of Khodavisi et al., Bayas et al. and Janbakhsh, the immunity status was 94%, 97%, and 96.6%, respectively, which were higher and safer than our study [28, 29]. It may depend on the type of vaccine used, for which information is not available.
Our study did not show a significant relationship between gender and immune status against hepatitis, but this relationship was observed between the age of participants in the study and antibody titer so that the most favorable group in terms of antibody titer in the age group of 18-21 was observed (48 people). On the other hand, in this age group, 60 people had a weak immune status which is statistically significant. Consistent with our study, Zamani et al. also showed a significant relationship between age and duration of vaccine with antibody titer [16]. There is conflicting information about the effect of gender on immunosuppression. Consistent with our study, the study of Khodavisi et al. as well as Zamani et al. both in the field of the relationship between gender and the immune response, showed that there is no significant relationship between gender and the immune response [16, 27]. Contrary to our study, Ferraz et al. reported a higher titer of anti-hepatitis antibody in women in their study [30], but Mansouri›s study showed that men responded better to the vaccine [31, 32].
Rostami›s study also showed that antibody titer had a significant relationship with gender and smoking, which was contrary to the results of our study. In addition, the study of Baba Mahmoudi et al . did not show a relationship between age and immune response, although in our study, there were the most immune people in the age group of 21-18 years, this relationship was not significant [33].
The study of Haji Bagheri et al. similarto our research , did not find a relationship between age and weight with serum levels of antibodies against HBs [34]. Similar to our study, Pera et al. did not find a significant relationship between body mass index and antibody titer [35]. But unlike our study, Heidari et al. showed a significant relationship [36].
In the study of Nooshirvanpour et al., a significant relationship was observed between gender and antibody titer and this titer was higher in women, but in our study, no significant relationship was observed between gender and antibody titer [37]. Studies of Izadpanah et al. and Dervishes et al. did not show a relationship between gender and antibody titer [38]. It is possible that the study method, antibody measurement method, sensitivity, and specificity of the kits used can be among the factors for observing different responses and thus comparing them.
5. Conclusion
Prevention is an important issue in public health, and due to the high risk of students, to ensure the effective level of antibodies after childhood vaccination, it is necessary to check the antibody titer against HBsAg before entering different wards of the hospital.

Ethical Considerations
Compliance with ethical guidelines

This study was approved by the Ethics Committee in Biomedical Research of Gonabad University of Medical Sciences (Cde: IR.GMU.REC.1397.106). Ethical considerations for conducting this research have been observed throughout the research process.

This study was conducted with the financial support of the Vice-Chancellor for Research and Technology of Gonabad University of Medical Sciences (Code: 10-1641-A). 

Authors' contributions
The main idea, study design, data collection, and specialized experiments: Seyed Hossein Abtahi and Jafar Hajavi; Data collection and study design: Alireza Mohammadzadeh, Mojbati Kian Mehr, and Abbas Ali Abbasneja; A critical review of the manuscript and final review: Jafar Hajavi, Seyed Hossein Abtahi, Alireza Mohammadzadeh, Mojbati Kian Mehr and Abbas Ali Abbasnejad; Data analysis: Seyed Behnam Mazlum Shahri; Data collection: Mohadeseh Nasiri, Mahnaz Aali, Zohreh Pirzadeh Moghadam, Zohreh Elahi and Zahra Jamali.

Conflicts of interest
The authors declared no conflict of interest.

The authors would like to express their appreciation and gratitude to students and other contributors who cooperate in carrying out this project. 

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Type of Study: Original | Subject: Allergy and Clinical Immunology
Received: 2021/01/29 | Accepted: 2021/06/2 | Published: 2021/10/1

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