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\begin{document}

\title{HBV, HCV and HIV Seroprevalence in Syrian Refugee Patient Population
Undergoing Preoperative Anaesthetic Assessment: A 10-Year Survey in a
Tertiary Teaching Hospital}



\author[1]{Mehmet Çömez}%
\author[2]{Tayibe Bal}%
\author[3]{Mehmet Çabalak}%
\affil[1]{Hatay Mustafa Kemal University}%
\affil[2]{Mustafa Kemal Universitesi Tayfur Ata Sokmen Tip Fakultesi}%
\affil[3]{Affiliation not available}%


\vspace{-1em}



  
  \date{May 15, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Objective: Migration can lead to a change in the demographic dynamics of
host populations in terms of communicable diseases in destination
countries. This is a potential public health challenge for health
authorities. HBV and HCV infections can lead to the development of
chronic liver diseases, cirrhosis and hepatocellular carcinoma, and HIV
infection can lead to the development of serious opportunistic diseases.
The aim of this study is to evaluate the seroprevalence of HBV, HCV and
HIV in Syrian refugees and Turkish patients who were evaluated
preoperatively in our hospital. Materials and methods: HBsAg, Anti-HBs,
Anti-HBc, Anti-HCV and Anti-HIV results of Syrian refugee and Turkish
patients who applied to surgical clinics between 2011-2021 were
retrospectively reviewed. Results: The study is comprised of 54446
patients: Turkish patient group (n=20569) and Syrian refugee patient
group (n=33877). The Syrian refugee patients had a significantly higher
HBsAg seropositivity rate and a significantly lower anti-HBs
seropositivity rate than the Turkish patients (p=0.002 and
p\textless{}0.001, respectively). The anti-HCV and anti-HIV
seropositivity rates were similar. The annual preoperative prevalance of
HBsAg seropositivity in the Syrian refugee patients tended to
significantly decrease gradually from year 2011 to year 2021
(p\textless{}0.001 for [?]30 and p=0.001 for \textgreater{}30 years old).
Conclusion: As a result, although HBV seroprevalence gradually decreases
and HCV and HIV seroprevalence is low; screening, information and
treatment programs should be given due importance because of the serious
disease potential and preventable conditions with precautions. In
addition, preoperative screening of refugee patients coming for major
surgery may be important for the safety of healthcare professionals.%
\end{abstract}%



\sloppy


\textbf{Introduction}

Migration is recognized as an independent social determinant of health.
Large-scale migration can contribute to a change in the demographic
dynamics of host populations in terms of communicable diseases in
destination countries. Current mass movement from high or medium
prevalence regions is a potential public health challenge for health
authorities in countries with low prevalence of infectious diseases
{[}1{]}.

The Syrian civil war, which has been ongoing since 2011, led to the
biggest refugee crisis since World War II. 3.658 million refugees were
reported in Turkey in September 2019 {[}2, 3{]}. Refugees bring many
infectious diseases that endanger the health of both themselves and the
host population {[}4{]}. Infections caused by hepatitis B virus (HBV)
and hepatitis C vir\selectlanguage{ngerman}üs (HCV) lead to the development of chronic liver
diseases, cirrhosis and hepatocellular carcinoma, while human
immunodeficiency virus (HIV) infection can lead to the development of
serious opportunistic infections. According to the World Health
Organization (WHO), an estimated number of 500 million people live with
chronic viral hepatitis, making HBV and HCV one of the most virulent
infectious diseases worldwide {[}5, 6{]}. At least 1.3 million deaths
per year can be attributed to chronic liver disease caused by HBV and
HCV {[}6, 7{]}. Also, viral hepatitis is largely responsible for the
global increase in liver cancer.

More than 90\% of the Syrian refugee population live in the community
and mostly in big provinces such as Istanbul, Gaziantep, Hatay and
Sanliurfa. Hatay province hosts 435,953 Syrian refugees {[}8{]}. Our
city, which is close to the war zone, is at a higher risk of infectious
diseases compared to other regions, as there are many applications for
emergency and elective operations to our institution, which is a third
level training and research hospital. In order to minimize the risk of
occupational contamination, every patient may be potentially infected
and there is a need to take protective measures accordingly. In
addition, it is important to know the current prevalence of these
diseases in establishing appropriate health policies for refugees. The
aim of this study is to evaluate the HBV, HCV and HIV seroprevalence of
Syrian refugee patients who were evaluated preoperatively in our
hospital and to compare them with the results of Turkish patients.

\textbf{Materials and methods}

This study was approved by the Non-Interventional Clinical Research
Ethics Committee of XXXXXXXXXXXXX (approval number: 22/04 / 2021-05).
hepatitis B surfage antigen (HBsAg), hepatitis B surfage antibody
(Anti-HBs), hepatitis B core antibody (Anti-HBc), hepatitis C virüs
antibody (Anti-HCV) and human immunodeficiency virüs antibody (Anti-HIV)
results of Syrian refugees and Turkish patients of all age groups who
applied to XXXXXXXXXXXX Hospital between 2011-2021 to be operated in
surgical clinics were retrospectively screened and a comparison was made
between the two groups. Serum samples were tested for HBsAg, anti-HCV,
anti- HIV, total anti-HBc, and anti-hepatitis B surface antibody (HBs)
using commercial immunoenzymatic assays (Abbott Architect i2000SR,
Illinois, USA). Anti-HIV reactivity was always confirmed by a western
blot assay, which identifies both HIV-1 and HIV-2 strains. The
demographic data of the patients were analyzed retrospectively from the
hospital electronic information system and patient files. Duplicate
records were removed.

Patient characteristics were determined as age, gender, race and year of
admission to the hospital. Patients with positive HBs Ag but with normal
ALT and AST levels and negative HBV DNA were accepted as HBV carriers.
Patients with Hbs Ag and Anti-HBc IgG negative but positive for Anti-HBs
were considered vaccinated. Detection of anti-HBc IgG positivity alone
was accepted as isolated Anti-HBc IgG positivity. Patients who were
found to be negative for all three parameters (HBs Ag, Anti HBs and Anti
HBc) were considered to have never encountered hepatitis B. All analyses
were carried out using SPSS, version 23 software (SPSS Inc, Chicago IL,
USA). The Shapiro Wilk normality test was used to examine normality of
distribution. Categorical variables were presented as frequencies
(percentages) and compared with Chi-square test (or Fisher's exact test,
where appropriate). Non-normally distributed continuous variables were
presented as median with interquartile range (IQR, 25th and 75th
percentiles) and compared with the Mann-Whitney U test between the
groups.

\textbf{Results}

The study is comprised of 54446 patients, divided into two groups:
Turkish patient group (n=20569) and Syrian refugee patient group
(n=33877). The median age of the patients was 41 (28-59) years and
44.8\% (n=24396) were male. The epidemiological characteristics and
preoperative seroprevalance of HBV, HCV, HIV serological markers in the
Syrian refugee and Turkish patients are shown in Table 1.

Although the Syrian refugee patients were significantly younger than the
Turkish patients, Syrian refugee patients had a significantly higher
HBsAg seropositivity rate and a significantly lower anti-HBs
seropositivity rate than the Turkish patients (p\textless{}0.001,
p=0.002 and p\textless{}0.001, respectively). The anti-HBc, anti-HCV and
anti-HIV seropositivity rates were similar between the two groups
(p=0.258, p=0.457 and p=1.000, respectively) (Table 1).

The comparisons of seropositivity of HBV markers between two groups
according to age are shown in Table 2. Syrian refugee patients
15-year-old or younger and in the 16-30 age group had a significantly
higher rate of HBsAg seropositivity than the Turkish patients in the
same age groups (p=0.007 and p=0.002, respectively). However, the rates
of HBsAg seropositivity between two groups were similar in other age
groups (Table 2).

The annual preoperative prevalance of HBsAg seropositivity in the Syrian
patients (both in 30-year-old or younger and in over 30-year-old
patients) tended to significantly decrease gradually from year 2011 to
year 2021 (p\textless{}0.001 and p=0.001, respectively). However, no
significant changes were seen in the prevalance of HBsAg seropositivity
in the Turkish patients in the same age groups (p=0.910 and p=0.483,
respectively) (Figure 1). Although anti HCV seropositivity was similar
between Syrian refugee and Turkish patients in \textless{}15, 16-30,
46-60 and \textgreater{} 60 age groups, it was significantly higher in
Syrian refugee patients in the 31-45 age group (p:0.037) (Table 3).

\textbf{Discussion}

Millions of people around the world emigrate from their homeland due to
economic, political and war reasons. Our border city, Hatay, received
significant immigration due to the Syrian civil war that started in
2011, and many people who were injured in the war applied to our
hospital due to the need for urgent surgical operation. It is important
to determine the infectious disease prevalence of our city due to
migration and patient transfers. According to our latest information,
this is the first preoperative hepatitis serology study conducted in
Syrian refugee patients.

According to the HBV carrier rate, the world is divided into 3 regions
with high, medium and low endemics. The Center for Disease Control and
Prevention in Atlanta, USA recommends screening for HBV infection in
people from countries with an HBsAg prevalence greater than 2\%. Turkey
is a moderately endemic country for HBV with a prevalence of 4\% (2-8\%)
{[}9{]}. Vaccination against HBV in Turkey started in 1998 and
vaccination rates reached 98\% in 2016 {[}10{]}. Vaccination against HBV
in Syria started in 1991 and the pre-war vaccination rate reached 83\%
in 2008 {[}11, 12{]}. Also, Syria is one of the middle endemic countries
for HBV {[}13{]}.

In this study, the Syrian refugee patient population was 33877 and the
Turkish patient population was 20569. The average age was significantly
lower in Syrian patients compared to Turkish patients. However, there
was no gender difference between the groups (p\textless{}0.001 and
p=0.360, respectively). There was a significantly higher HBsAg
seropositivity rates in Syrian refugee patients (2.3\%) compared to
Turkish patients (1.9\%) (p= 0.002). In a study conducted in Karabük,
A\selectlanguage{polish}ş\selectlanguage{english}k\selectlanguage{polish}ı\selectlanguage{english}n et al. {[}14{]} reported HBsAg seropositivity as 2.3\% in the
general patient population of Syrian refugees. In a study conducted in
Kahramanmara\selectlanguage{polish}ş, \selectlanguage{english}Ozkaya et al. {[}15{]} reported HBsAg seropositivity as
3.6\% in the general patient population of Syrian refugees. In a study
conducted in Ankara, T\selectlanguage{ngerman}ümtürk et al. {[}16{]} reported that HBsAg
seropositivity was 5.7\% in the general patient population of Syrian
refugees. When evaluated according to age groups, HBsAg seropositivity
was significantly higher in Syrian refugee patients under the age of 15
and in the 15-30 age group. There was no difference in other age groups.
This may be due to the fact that refugee children who came to Turkey
missed a large number of vaccination periods due to the collapse of the
vaccination system in their country of origin {[}17, 18{]}.

The annual preoperative prevalence of HBsAg seropositivity in Syrian
refugee patients (both \selectlanguage{english}[?]30 and \textgreater{}30 years old) tended to
gradually decline significantly from 2011 to 2021 (p \textless{}0.001
and p = 0.001, respectively). However, there was no significant change
in the prevalence of HBsAg seropositivity in Turkish patients in the
same age group (p = 0.910 and p = 0.483, respectively). This may be due
to the collapse of the vaccination system in the country of origin
during the first period of war and migration and more crowded living
environments such as camps. In the later period, it can be attributed to
the inclusion of all Syrian refugee children in the national vaccination
program and the improvement of socioeconomic conditions (such as free
access to health and treatment, children's education, work permits and
free access to vocational training) {[}17, 19, 20{]}.

Anti HBs seropositivity was significantly lower in Syrian refugee
patients (40.8\%) compared to Turkish patients (42.5\%)
(p\textless{}0.001). No difference was found between Syrian refugee and
Turkish patients in terms of anti-HBs seropositivity under the age of 15
(p\textless{}0.001). This may be due to the fact that all Syrian refugee
children who arrived in Turkey are included in the national vaccination
program {[}19{]}. According to the data of the Turkish Ministry of
Health, the number of Syrian refugee children vaccinated was reported as
59743 in 2014, 100244 in 2015, 148172 in 2016 and 269085 in 2017
{[}19{]}. Anti HBs seropositivity was lower in Syrian refugee patients
compared to Turkish patients in the 16-30 age (p \textless{}0.01) and
31-45 age (p: 0.013) groups. This was attributed to the poor
socioeconomic conditions in the war zone and the absence of vaccination
tracking {[}17, 18{]}. No significant difference was found between
Syrian refugee and Turkish patients over the age of 46. In accordance
with this study, Ozkaya et al. {[}15{]} found a significant difference
in anti-HBs seropositivity between Syrian refugees (34.9\%) and Turkish
patients (43.4\%).

According to WHO data, Syria is among endemic areas with a low anti-HCV
seropositivity rate {[}21{]}. Consistent with this, anti HCV
seropositivity was 1.2\% in Syrian refugee patients and 1.1\% in Turkish
patients in this study. There was no significant difference between
Syrian refugee and Turkish patients in terms of anti-HCV seropositivity.
Anti-HCV seropositivity was significantly higher in Syrian refugee
patients aged 31-45 (p:0.037). However, it was similar to Turkish
patients in other age groups. Consistent with this study, Ozkaya et al.
{[}15{]} reported 1.8\% anti-HCV seropositivity. In another study, A\selectlanguage{polish}ş\selectlanguage{english}g\selectlanguage{polish}ı\selectlanguage{english}n
et al. {[}14{]} reported it as 1\%. T\selectlanguage{ngerman}ümtürk et al. {[}16{]} found 2.46\%
in a study they conducted on a small population (244 Syrian refugees).
In a meta-analysis, Chemaitelly et al. {[}22{]} reported the anti-HCV
seropositivity rate as 48.8-75\% in hemodialysis patients, 21\% in drug
users and 20.5\% in hemophilia patients in the Syrian population. These
high rates may be due to the presence of serious risk factors in
patients.

Syria has very low HIV prevalence {[}23{]}. In this study, 1 HIV (+)
patient was identified in 33877 Syrian refugee patients and only 1 in
20569 Turkish patients. Inci et al. {[}24{]} did not find any anti HIV
(+) patients among 300 Syrian refugees in their study. In another study
conducted by Tümtürk et al. {[}16{]}, they did not find any anti HIV (+)
patients among 244 Syrian refugees.

We have some limitations in this study. This study was conducted on
Syrian refugee patients, who had a high population, but had preoperative
anesthetic evaluation in a single center. Therefore, multi-center
studies are needed as our results may not reflect the serological data
of all Syrian refugees. Since this study was retrospective, the medical
history and risk factors of the patients could not be obtained.

In this study, information on HBV, HCV and HIV seroprevalence of high
population of Syrian refugees who came for emergency and elective
surgical operations from the ongoing Syrian civil war since 2011 was
presented. In the Syrian refugee population, HBsAg seroprevalence was
high and anti HBsAg seroprevalence was low. However, due to the
vaccination studies conducted in Turkey, especially in the pediatric age
group in Syrian refugees, HBsAg seroprevalence has gradually decreased
and anti-HBs seroprevalence has increased gradually in the 10-year
period. HCV and HIV rates are very low in both Turkish and Syrian
populations.

As a result, although HBV seroprevalence decreases gradually and HCV and
HIV seroprevalence is low, due attention should be paid to screening,
information and treatment programs due to the serious disease potential
and preventable conditions. In addition, healthcare professionals'
strict adherence to standard protection measures, training, vaccination
against HBV and preoperative screening of refugee patients coming for
major surgery may be important for the safety of healthcare
professionals.

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