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Microbiology and Drug Resistance of Pathogens in Patients Hospitalized at the Nephrology Department in the South of Poland

SÜER, KAYA

GÜVENIR, MERYEM

AYKAÇ, ASLI

ORIGINAL PAPERPolish Journal of Microbiology
2018, Vol. 67, No 4, 525–528
https://doi.org/10.21307/pjm-2018-062
* Corresponding author: M. Güvenir, Vocational School of Health Services, Near East University, Nicosia, Cyprus; 
e-mail: meryemguvenir@hotmail.com
© 2018 Kaya Süer et al.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License (https://creativecommons.
org/licenses/by-nc-nd/4.0/) 
Introduction
Hepatitis E (HEV) infection involves a non-envel-
oped virus belonging to the genus of Orthohepevirus. 
It is a zoonotic pathogen which has spread through 
a number of developing countries (Wu et al. 2016). The 
virus has been designated with the letter E for its trans-
mission via the enteric route (Lapa et al. 2015). Cur-
rently, it is estimated that 20 million individuals world-
wide are infected with HEV, where it is the cause of 
57 000 deaths each year (Lapinski et al. 2016). It is also 
responsible for 3.3 million new symptomatic infections 
with fatal outcomes in 56 600 individuals (Mauceri 
2018). The World Health Organization (WHO) has 
reported that the low endemic regions of HEV epide-
miology are found in the USA and Europe (the UK, 
France, the Netherlands, Austria, Spain, Greece and 
Germany) as well as developed Asian-Pacific coun-
tries (Japan, Taiwan, Korea, Hong Kong, Australia and 
New Zealand) (WHO 2010). High endemic regions are 
found in Central America, Africa and South and Cen-
tral Asia (Melgaco 2018). The prevalence of anti-HEV 
IgG in Africa is between 4.6% and 10.7% and is between 
34.8% and 94% in Asia (Melgaco 2018).
The presence of anti-HEV IgM was conclusive at 
the onset of the infection and increased by the begin-
ning of the fourth week; however, no further increase 
was detected after three months. Anti-HEV IgG anti- 
bodies increase to their peak level by the end of the 
fourth week and can continue for years (El-Tras 
et al. 2013). HEV is generally transmitted by the fecal-
oral route, following transfusion with infected blood 
products, through vertical transmission and also 
through contact with infected animals (Hesamizadeh 
et al. 2016). Individuals considered to be at high risk of 
contracting the virus include employees of slaughter-
houses, people working on pig farms and veterinarians 
(Holt et al. 2016).
A Special Risk Group for Hepatitis E Infection:
The First Record of North Cyprus
KAYA SÜER1, MERYEM GÜVENIR2* and ASLI AYKAÇ3
1 Department of Infectious Diseases and Clinical Microbiology, Faculty of Medicine,
Near East University, Nicosia, Cyprus
2 Vocational School of Health Services, Near East University, Nicosia, Cyprus
3 Department of Biophysics, Faculty of Medicine, Near East University, Nicosia, Cyprus
Submitted 9 July 2018, revised 5 October 2018, accepted 9 October 2018
A b s t r a c t
Hepatitis E virus (HEV) is transmitted by a fecal oral route from animals to humans following exposure to the body fluids of infected ani-
mals. We investigated the seroprevalence of anti-hepatitis E (anti-HEV) antibodies by monitoring IgG and IgM virus antibodies amongst 
employees in the animal industry in North Cyprus through a cross-sectional study. Samples were taken from individuals without occupa-
tional exposure to animals and from those who worked with animals (doing animal husbandry, veterinary work or butchery). Enzyme-
linked immunoassays were used to detect anti-HEV IgG and IgM in the blood samples. The prevalence of anti-HEV IgG antibodies was 
3.0% (12/400), while the prevalence of anti-HEV IgM antibodies was 0.25% (1/400). The prevalence of anti-HEV IgG amongst the samples 
received from females was approximately 2.5-fold higher than samples received from males (2.4%). Anti-HEV IgG was detected amongst 
7% of animal husbandry workers and amongst 2% of veterinarians and butchers. The current findings represent the first records of HEV 
surveillance in Cyprus. We investigated the seroprevalence of anti-HEV by monitoring IgG and IgM virus antibodies amongst employees.
Key words: Cyprus, hepatitis E, seroprevalence, zoonoses, animals, epidemiology
Süer K. et al. 4526
The aim of the study was to determine the health 
risks posed to employees working with animals in 
North Cyprus by monitoring the prevalence of HEV.
Experimental
Materials and Methods
Setting. The present study was a cross-sectional 
survey of animal workers from five regions in North 
Cyprus. The distribution of participants across the dif-
ferent districts in North Cyprus was as follows: Nicosia 
(28.8%), Kyrenia (18%), Omorphou (11%), Famagusta 
(21.7%) and Trikomo (20.5%) according to animal 
workers numbers supplied by Veterinary Office of 
North Cyprus. Since HEV prevalence may be as low 
as 1%, taking α = 0.05 and β = 0.20 one could calculate 
the minimum number of people to be investigated as 
400. Therefore, four hundred persons were selected who 
did not have any clinical findings according to gen-
eral health state. Individuals participating in the study 
were categorized into four groups based on the level of 
interaction each participant had with animals in their 
work life. Group 1 included participants without occu-
pational exposure to animals, while Group 2 consisted 
of participants who worked with animals (animal hus-
bandry). Group 3 included veterinarians, and Group 4 
was composed of butchers. All participants were asked 
by attained healthy worker to complete epidemiologi-
cal questionnaire that included basic demographic and 
epidemiological data such as name, age, sex, how much 
years to spend as animals’ workers.
Laboratory Testing. A total of 400 blood samples 
were collected. Serum samples were separated by cen-
trifugation at 1000 × g for 10 min and were stored at 
–20°C until required for antibody detection. All serum 
samples were tested using a commercially available 
enzyme-linked immunoassay (ELISA) in a kit (Dia Pro, 
Italy), in accordance with the manufacturer’s instruc-
tions. The positive and negative controls were supplied 
in the kit and were included in each antibody screening 
test. Anti-HEV IgG and anti-HEV IgM ELISA tests were 
performed separately. The results from all the samples 
were calculated as a ratio of the individual absorbance to 
the cut-off value (S/CO). The samples with a ratio < 1.0 
were considered as negative, 1.0–1.2 as equivocal and 
> 1.2 as positive. The diagnostic sensitivity of > 98% was 
found according to manufacturer’s instruction.
Ethics Committee Approval. Ethical approval was 
granted by the Institutional Research Ethics Committee 
of the Near East University (No. 179).
Statistical Methods. The software program SPSS 
version 3.0 (SPSS Inc. Chicago, IL, USA) was used for 
the statistical analyses. Student t-tests were used for 
mean differences. Data were expressed as a mean value 
(standard deviation), as a minimum-maximum and as 
a percentage, where appropriate. A p-value of less than 
0.05 was considered statistically significant.
Results
The mean age of participants was 39.4, with the 
youngest being 13 and the eldest being 84 years of 
age (Table I). Three percent of the samples examined 
were positive for anti-HEV IgG (12/400), while 0.25% 
< 30 108 (27.0)
30–40 109 (27.2)
41–50 80 (20.0)
51–60 87 (21.8)
> 61 16 (4.0)
Table I
The socio-demographic characteristics of groups (n = 400).
Age in years N (%)
Female vs. male Female Male p-value Female Male p-value
 4 8 0.115 0 1 0.836
Time spent in contact with animals < 20 years > 20 years p-value < 20 years > 20 years p-value
 2 10 0.001 1 0 0.644
Table II
Prevalence of the Anti-HEV IgG and IgM seropositivity among gender and time spent in contact with animals.
Anti-HEV IgG (+)
Positive
Anti-HEV IgM (+)
Positive
of samples were tested positively for anti-HEV IgM 
antibodies (1/400) as shown in Table II. The 400 par-
ticipants consisted of 334 males and 66 females. The 
prevalence of anti-HEV IgG antibodies was 6.1% (n = 4) 
amongst female participants and 2.4% (n = 8) amongst 
male participants (Table II); however, these differences 
were not statistically significant (p = 0.115). Similarly, 
the anti-HEV IgM seropositivity was not signifi cantly 
associated with gender (p = 0.836). Anti-HEV IgG 
seropositivity was significantly associated with years 
spent working with animals (p = 0.001). Ten cases of 
anti-HEV IgG were found for people who spent more 
A Special Risk Group for Hepatitis E Infection4 527
than 20 years in contact with animals (Table II). Con-
cerning the geographical localization, of the 12 sam-
ples which tested positive for anti-HEV IgG antibodies, 
6.9% (n = 6) were in Famagusta, 2.7% (n = 2) in Kyre-
nia, 0.01% (n = 1) in Nicosia, 4.5% (n = 2) in Morphou 
and 1.2% (n = 1) in Trikomo (Table III). Distribution 
of anti-HEV IgG and IgM were not significantly differ-
ent according to locations (p < 0.05; p = 0.101, p = 0.462, 
respectively) (Table III).
Discussion
Cyprus is in the Mediterranean Sea. Until the cur-
rent study, there has been no surveillance of the sero-
prevalence and epidemic of HEV infections in Cyprus. 
The seroprevalence has been changing, and there 
is a  link to geographical locations between 0.0% to 
0.9% anti-HEV IgM and 1.1% to 14.2% for anti-HEV 
IgG depending of the region of Iran (Taherkhani and 
Farshadpour 2016). Outbreaks of HEV, as such, have 
not occurred and the prevalence of sporadic cases is 
lower than 25% (Mohebbi et al. 2012).
In Europe, HEV seroprevalence is predicted to be 
from 7.5% to 31.9%, with an average of 19.16%. None-
theless, the real seroprevalence could change due to dif-
ferences in test sensitivity and the number of asymp-
tomatic courses of the HEV disease (Mauceri 2018). 
The prevalence rates of anti-HEV in Europe, especially 
in France (17%) and Germany (35%), could again be 
based on the pork consumption (Melgaco 2018). There 
is no published report to allow a comparison with HEV 
seroprevalence in the Cyprus population.
Prevalence of HEV viremia in blood donors ranges 
between 1/762 in the Netherlands and 1/9500 people 
in the United States. Especially immunosuppressed 
reci pients are under the risk of the HEV infection by 
contaminated blood products (Niederhauser 2018). In 
Turkey, the total HEV seroprevalence rate was found 
to be equal to 4.4% (Aydın et al. 2016). In our control 
group which included blood donors, anti-HEV IgG 
seropositivity is 1%. This result indicated that anti-
HEV seroprevalence was low in our general popula-
tion. According to the previous studies, the exposure to 
and more specifically devouring of rare meat products 
are the most important risk factor for HEV transmis-
sion (Melgaco 2018). In North Cyprus, the consump-
tion of rare or raw meat is really low which may be 
a reason that the seroprevalence is lower than in the 
other countries.
El-Tras et al. (2013) reported 26.8% seropositivity in 
males, although the female seropositivity was 50.8% in 
Egypt, and there were significant differences (p = 0.05). 
Altındiş et al. (2000) indicated that female seropositivity 
was 6.7% and male positivity was 3.7% in Turkey. In the 
current study, anti-HEV IgG antibody concentrations 
among females were 2.5-fold higher than those in males 
and this difference was not statistically significant. Our 
prediction found a higher anti-HEV IgG seroprevalence 
in female because females could be more involved in 
activities of supplying animals so that they were more 
often exposed to animals. Interestingly, anti-HEV IgG 
seroprevalence was high in male in our study. The 
majority of the anti-HEV IgG seropositive farmers 
live in Famagusta. Famagusta has a high proportion 
of people whose have own farmers. An association 
to transmission may exists probably through animal 
wastes and other tissues. Our study has some limita-
tions since statistical studies were difficult due to low 
overall seroprevalence for HEV in Cyprus.
The prevalence of HEV ranged from 0 to 12.4% in 
Turkey. The high seroprevalence was detected in agri-
culture workers (35%). Leblebicioğlu and Ozaras (2018) 
suggested that fecal route is not a main way of transmis-
sion to the HEV in Turkey. Also, low socio-economical 
status could be related with the seroprevalence of the 
HEV. The seroprevalence rates were higher for peoples 
which live in camps or work in agriculture and ani-
mal husbandry (Leblebicioğlu and Ozaras 2018). There 
have been a few studies reported the seroprevalence 
of anti-HEV-IgG in agricultural workers as being in 
the range from 4.4% to 34.8%, a 11.5-fold higher than 
the control groups in Turkey (Ceylan et al. 2003). Eker 
et al. (2009) reported that 28.5% of seropositive cases 
were associated with animals such as goats, sheep and 
cattle. Leblebicioğlu and Ozaras (2018) reported that 
Turkey is among the countries where HEV is endemic, 
but there were some limitations to their study since they 
did not cover the entire population. Aydın et al. (2016) 
reported that seroprevalence of HEV in animal work-
ers were 35.9% and most frequent in animal husbandry 
(Aydın et al. 2016). Our results demonstrated a higher 
anti-HEV IgG seroprevalence among those who spent 
over 20 years working with animals as compared to less 
than 20 years. Thus, the time of contact with animals is 
positively correlated with the risk of infection.
Studies which are designed for the surveillance 
of HEV antibodies in both animals and humans will 
Nicosia  1 (0.01%) 0
Kyrenia 2 (2.7%) 0
Morphou 2 (4.5%) 0
Famagusta 6 (6.9%) 1 (1.5%)
Trikomo 1 (1.2%) 0
Table III
Prevalence of the Anti-HEV IgG and IgM seropositivity
in different locations.
Location IgG-positive12 (3%)
IgM-positive
1 (0.25%)
Süer K. et al. 4528
contribute to a better understanding of the seropreva-
lence of HEV. Close monitoring by the government of 
precautions when working with animals, high socio-
economical status and high educational level may 
be important to employees in order to decrease the 
prevalence of the diseases. Currently, there is no data 
recorded within the Health Ministry of Cyprus regard-
ing HEV infections; thus, the current findings represent 
the first record of HEV surveillance in Cyprus.
Acknowledgements
The authors declared that this study was supported by ‘Viral 
Hepatit Savaşım Derneği (VHSD)’.
Conflict of interest
Author does not report any financial or personal connections 
with other persons or organizations, which might negatively affect 
the contents of this publication and/or claim authorship rights to 
this publication.
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A Special Risk Group for Hepatitis E Infection: The First Record of North Cyprus

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