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The Seroprevalence of Cystic Echinococcosis in a Rural Normal Population,

Southwestern Iran

Article · February 2018

DOI: 10.2174/1871526518666180213165306

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Infectious Disorders - Drug Targets, 2018, 18, 000-000 1

RESEARCH REPORT

The Seroprevalence of Cystic Echinococcosis in a Rural Normal

Population, Southwestern Iran
Abdollah Rafiei1,2, Esmat Panabad2 and Molouk Beiromvand1,2,*

1Infectiousand Tropical Disease Research Center, Health Research Institute, Ahvaz Jundishapur
University of Medical Sciences, Ahvaz, Iran and 2Department of Parasitology, School of Medicine,
Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

Abstract: Introduction: Cystic echinococcosis is a neglected zoonotic disease with

ARTICLE HISTORY
Received: September 17, 2017
Revised: January 27, 2018
Accepted: February 12, 2018
DOI:
10.2174/1871526518666180213165306
worldwide distribution, which occurs mainly in pastoral regions. Echinococcus granu-
losus sensu stricto, is the main agent of human infection. Although Iran is an endemic
area for CE in the Middle East, lack of data regarding the disease among rural inhabit-
ants of Khuzestan province in recent years, persuaded us to perform the current study.
Methodology: This cross–sectional study was conducted in 2016 using simple random
sampling method in 15 villages of Shushtar County, southwestern Iran. Three hundred
and fourteen rural inhabitants were examined using AgB- ELISA test for CE.
Results: From 314 patients included in the study, females and males were 244 (77.7%)
and 70 (22.3%), respectively. Of these, 227 (72.3%) were in close contact with dogs,
out of which 173 (70.9%) of them were females and 54 (29.1%) were males. ELISA de-
tected three (1%) seropositive cases among investigated population. All three positive
cases were females and in close contact with dogs. Furthermore, the positive cases were
in the age range of 21-50. None of the 70 examined males were positive.
Conclusion: This study is the first report of CE in rural areas of Shushtar, Southwest
Iran, which indicated seroprevalence of CE among rural areas with a high prevalence
rate of infection among females. It seems that the rural population of the region are at
the risk of exposure to E. granulosus eggs. Therefore, more studies are required to eval-
uate the human CE in all parts of the province using serological and ultrasound meth-
ods.

Keywords: Cystic echinococcosis, Iran, Khuzestan.

1. INTRODUCTION
Cystic echinococcosis (CE) is a zoonotic dis-
ease caused by the larval stages of Echinococcus
granulosus, the dog tapeworm [1]. Two mammali-
an hosts are involved in the life cycle of the ces
*Address correspondence to this author at the Infectious and Tropi-
cal Disease Research Center, Health Research Institute, Ahvaz Jun-
dishapur University of Medical Sciences, Ahvaz, Iran, P.O. Box
61357–15794 Ahvaz Iran; Tel: +98 61 33367543; Fax: +98 61
33367547, E-mail: Beiromvand-m@ajums.ac.ir
tode. Dogs and other canids play the role of final
hosts, whereas ungulates are intermediate hosts
[1]. Human, the dead-end intermediate host, ac-
quires infection by accidental ingestion of Echino-
coccus eggs through contaminated food and vege-
tables [1]. Although the metacestode (hydatid cyst)
develops in many anatomic sites, mainly infections
occur in the liver [1-2].
The disease has medical, economical, veteri-
nary, and public health importance [1]. The World
Health Organization (WHO) has considered CE as

1871-5265/18 $58.00+.00 © 2018 Bentham Science Publishers

2 Infectious Disorders - Drug Targets, 2018, Vol. 18, No. 00
neglected tropical disease (NTD) and neglected
zoonotic disease (NZD) [3]. It has a worldwide
distribution, particularly in rural communities
which, due to close contact with dogs, are more at
risk [4].
Based on molecular studies, 10 genotypes (G1–
10) have been identified, among which the most
common strain is sheep strain (G1) [5]. The G1
genotype is responsible for most of the human
cases of CE [4]. It is estimated that more than 270
million people are at the risk of infection in Cen-
tral Asia, including Afghanistan, Pakistan and Iran
[6]. Most human cases are asymptomatic and di-
agnosed accidentally by imaging techniques, par-
ticularly ultrasonography [2]. Experimental studies
show that immunoglobulin (Ig) G appears in re-
sponse to hydatid cyst fluid (HF) antigens after 2-
11 weeks [7]. Hydatid cyst fluid is a complex of
proteins that some of their components are highly
immunogenic. Serological tests, such as enzyme-
linked immunosorbent assay (ELISA) and the im-
munoblotting (IB) have been developed based on
the antigenic components for immunodiagnosis of
human CE [8].
CE has been reported from different parts of
Iran, especially northern and western rural areas
[6]. Khuzestan province is one of the endemic foci
of CE in the southwest Iran [9]. The annual rec-
orded surgical incidence of CE has been reported
to be 1.33/100,000 in south western Iran [10]. It
seems that farmers and housewives are at the
higher risk of infection in this area [6]. Epidemio-
logical studies on CE are few [9-10] despite the
fact that the disease is endemic in the province.
Furthermore, the high population of dogs, espe-
cially stray dogs, lack of programs, such as con-
trolling and monitoring local slaughterhouses, and
anthelminthic treatment of dogs, low awareness of
zoonotic diseases among rural inhabitants, and the
lifestyle in Khuzestan villages where people keep
dogs in their homes are important, however, ne-
glected factors affect the disease.
Shushtar County is one of the 23 counties of
Khuzestan province, located in the north of the
province and southwest Iran. Most people who
live in Shushtar villages are farmers or ranchers.
Rural inhabitants, like other parts of the country,
keep dogs as the companions and guards of their
properties and livestock. Therefore, the chance of
dog-transmitted diseases, particularly CE, might
Rafiei et al.
be increased in this region. The aim of the current
study was to evaluate the human CE among nor-
mal population of rural areas in 2016 using indi-
rect ELISA.
2. MATERIALS AND METHODS
2.1. Ethics Statement
The protocol of this study was reviewed and
approved by the Ethics Committee of Ahvaz Jun-
dishapur University of Medical Sciences (Approv-
al No IR.AJUMS.REC.2016-622).
2.2. Study Area
Shushtar County, one of the counties of
Khuzestan province, is located in the southwest
Iran and at the foot of the Zagros Mountains (32°
02′ N 48° 51′ E). The center of the county is
Shushtar with a population of 192,028 (census
2016) and an area of 2436 km2 is located in the
north of Khuzestan province. Old Shushtar, an an-
cient pre-Islamic town, is a part of Shushtar city
now. The climate is hot semi-arid in summers and
mild in winters. The precipitation is 600 mm per
year.
2.3. Sampling
This cross-sectional study was conducted
among rural inhabitants in 2016. Three hundred
and fourteen of rural inhabitants from 15 villages
of Shushtar County, who were in contact with
dogs, were included in the present study. Prior to
collecting the patients' sera, the required infor-
mation regarding the study was provided to all
participants, and the assigned verbal consent was
obtained from each participant. The designed
questionnaire contained items regarding close con-
tact with animals, particularly dogs. Moreover, the
participants filled in the questionnaire items con-
cerning their medical history. The collected sera
were stored at −20°C until further examinations.
2.4. Antigen Purification
Hydatid cyst fluid (HCF) was aspirated under
sterile conditions from fertile cysts obtained from
sheep slaughtered at local slaughterhouse. The hy-
datid fluid was transferred to 50 mL falcon tubes,
and then was centrifuged at 5000 ×g for 30 min (at
4°C) to remove protoscoleces and solid materials.
100 ml of obtained HCF was dialyzed against
Cystic Echinococcosis in a Rural Normal Population Infectious Disorders - Drug Targets, 2018, Vol. 18, No. 00 3

0.005 M acetate buffer (pH 5) at 4°C overnight, Three hundred and fourteen participants aged
and centrifuged at 50 000 × g for 30 min. After between 15 to over 70 years old from 15 villages
discarding the supernatant, 10 ml phosphate- of Shushtar County voluntarily participated in this
buffered saline (PBS; pH 8) was added to the pel- study. The participants were grouped in the age
let and carefully mixed using a vortex to dissolve ranges of 15-20 (9), 21-30 (69), 31-40 (80), 41-50
completely. After boiling at 100°C in water bath (51), 51-60 (57), 61-70 (23), and >70 (25) (Table
for 15 min, it was centrifuged at 50 000 × g for 60 1). Out of the 314 participants, 244 (77.7%) were
min. Finally, the supernatant was transferred to 2 females and 70 (22.3%) were males. Among them,
ml tubes and stored at 20°C until next examination 227 (72.3%) were in close contact with animals,
[11]. The protein concentration was assayed by particularly with dogs. From these, 173 (70.9%)
Bradford method. were females and 54 (29.1%) were males. ELISA
test detected three (1%) seropositive cases among
2.5. ELISA the participants (Table 2). All three positive cases
ELISA test was conducted using 96 SPL maxi were females and were in close contact with dogs.
binding plates (SPL, Korea). The plates were coat- Two of them were in the age range of 21-30, and
ed with 100 µl (5 µg/ml) of purified antigen in one was in 41-50 age group. None of the 70 exam-
coating buffer (0.1 M carbonate/bicarbonate buff- ined males was positive. The obtained data in
er, pH 9.6), and then incubated at 4°C overnight. terms of studied villages and seropositive cases are
The plates were washed four times with phosphate presented in Table 3.
buffered saline 0.1% Tween 20 (PBS/T) and Table 1. ELISA results by gender and age groups of the
blocked with 300 µl of skimmed milk at room participants.
temperature (RT) for 1-2 hrs. After four times
washing with PBS/T, 100 µl of sera diluted 1:100 Positive by ELISA
in PBS was added to each well and incubated at Age groups (Year) No. (%)
RT for 60 min. The plates were then washed four Female Male
times with PBS/T, and 100 µl of diluted 1:3000 in 15-20 9 (2.9) 0/8 0/1
PBS-T anti-human IgG antibody (whole molecule)
conjugated to alkaline phosphatase produced in 21-30 69 (22.0) 2/60 0/9
goat (Sigma Aldrich, Saint Louis, USA) was add- 31-40 80 (25.5) 0/69 0/11
ed. After five times washing, 100 µl/well of p-
Nitrophenyl Phosphate, Disodium Salt, Hexahy- 41-50 51 (16.2) 1/40 0/11
drate substrate in 0.05 M carbonate/bicarbonate 51-60 57 (18.2) 0/37 0/20
buffer (pH 9.8) was added and kept in a dark envi-
61-70 23 (7.3) 0/15 0/8
ronment at RT for 20 min, and the plates were read
at 405 nm with an ELISA reader [9]. Positive sera >70 25 (8.0) 0/15 0/10
from patients with surgically and pathologically Total 314 (100) 3/244 0/70
confirmed liver CE at Ahvaz hospitals, and nega-
tive sera from healthy blood donors were used as
positive and negative controls, respectively. The
cut-off-values were taken using the mean +2 SD of Table 2. Number (%) of seropositive cases by gender
the negative sera, which were included in all using ELISA.
plates.
Genus
2.6. Statistical Analyses Result Total (%)
Female (%) Male (%)
The Chi-Square test and Fisher's Exact test
were used to evaluate the differences between the Negative 241 (99.0) 70 (100.0) 311 (99.0)
groups of seropositive patients. A P value<0.05 Positive 3 (1.0) 0 (0.0) 3 (1.0)
was considered statistically significant. The ob-
Total 244 70 314 (100)
tained data were analyzed using SPSS version 16.
Table 3. Seroprevalence (%) of cystic echinococcosis
3. RESULTS based on villages and dog's contact.
4 Infectious Disorders - Drug Targets, 2018, Vol. 18, No. 00 Rafiei et al.

Contact with [13-16]. In a study by Reiterova et al., the sensitiv-

Village dog (%) Negative Positive Total ity and specificity of AgB-ELISA in detecting
(%) (%) (%) cystic echinococcosis were reported to be 96.4%
Yes No
and 97.2%, respectively [17]. Based on seroepi-
Sherafat
38 14
52 (16.6) 0
52 demiological studies, human CE rate is reported to
(73.1) (26.9) (16.6) range from 1.2 % in Ilam province to 21.4% in
1 Chaharmahal and Bakhtiari province, southwest
Colahjaz 7 (87.5) 8 (2.5) 0 8 (2.5)
(12.5) Iran [18]. Human CE has been studied in different
14 5 parts of Iran, using native AgB-ELISA, but the
Darbkhazyneh 19 (6.1) 0 19 (6.1) disease has not been studied in the Khuzestan
(73.7) (26.3)
3
province widely, and the only available data is re-
Deilam 5 (62.5)
(37.5)
8 (2.5) 0 8 (2.5) stricted to the study by Rafiei et al.in 2007 [9].
The previous study reported 13.8% seropositive
14 3
Shoaybiyeh 17 (5.4) 0 17 (5.4) rate of CE in some parts of the province, but no
(82.4) (17.6)
actual data was available in Shushtar County. In
28 16 the present study, 1 % seropositivity of CE in rural
Gavmishabad 43 (13.7) 1 (0.31) 44 (14)
(63.6) (36.4) inhabitants of Shushtar County was identified by
Konarpeer 8 (80) 2 (20) 10 (3.2) 0 10 (3.2) ELISA. Although our results showed a sharp de-
10
crease in the CE rate in comparison with the study
Pirdalou 1 (9.1) 11 (3.5) 0 11 (3.5) by Rafiei et al., but this research confirmed ende-
(90.9)
micity of CE in the region. The low prevalence
24 10 34
Arabhasan
(70.6) (29.4)
34 (10.8) 0
(10.8)
observed in the current study may be because this
study was conducted in a rural normal population,
14 9 but the previous study was performed on nomadic
Noormohamadi 22 (7) 1 (0.31) 23 (7.3)
(60.9) (39.1)
population who are at high risk of infection.
13 2
Zoyeh 15 (4.8) 0 15 (4.8) The data showed that women within the age
(86.7) (13.3)
group of 21-50 revealed higher infection than oth-
24 7
Sardarabad
(77.4) (22.6)
30 (9.5) 1 (0.31) 31 (9.9) er age groups (Table 1). It seems that higher infec-
tion in this age group is due to more exposure to
12 7 the agents of the infection. Therefore, our data are
Mahdiabad 19 (6.1) 0 19 (6.1)
(63.2) (36.8)
in agreement with the earlier studies [18-20]. The
Gooriyeh 5 (62.5)
3
8 (2.5) 0 8 (2.5) results also indicated some difference between
(37.5) males and females (Table 2). Our findings are sim-
11 4 ilar to those previous studies showing that house-
Abgarmak 15 (4.8) 0 15 (4.8)
(73.3) (26.7) wives are more at risk of having CE in Iran [18].
227 87 314 Although this seropositivity rate of infection is
Total 311 (99) 3 (1) lower than previously reported (13.8%) in
(72.3) (27.7) (100)
Khuzestan province [9], the observed prevalence
4. DISCUSSION among people who were not suspected to hydati-
dosis is considerable. Another reason for higher
Cystic echinococcosis is a serious threat for prevalence in the previous study is most probably
both humans and farm animals, therefore, its early that it was conducted only on nomadic population
diagnosis is important. Imaging techniques, partic- [9]. It is clear that more exposure to risk factors,
ularly ultrasound (US) as reliable diagnostic meth- such as close contact with infected dogs, could in-
ods, are crucial, and are the first choice in the early crease the chance of infection. The data confirmed
diagnosis, that is, staging and management of the another part of southwestern Iran as an endemic
diseases [2, 12]. However, doubtful cases must be area for the diseases; thus, close contact of inhab-
confirmed serologically [12]. Among serological itants with dogs may represent a serious health
tests, AgB-ELISA (antigen B) is a reliable test threat in villages. In rural areas of Iran, people are
with acceptable sensitivity ranging from 60% to in close contact with dogs, but their knowledge
85% [8], which is used in many epidemiological about zoonotic diseases and their transmission
studies in order to detect cystic echinococcosis
Cystic Echinococcosis in a Rural Normal Population
routs is less than that of the people living in devel-
oped countries. Subsequently, poor hygiene, low
level of education, eating contaminated food and
vegetables, and contact with soil can complicate
the issue.
CONCLUSION
In recent years, several studies provided more
information about the endemicity of human CE in
Iran [21-23]. However, increasing number of hos-
pitals and slaughterhouses reports and uncon-
trolled population dogs, particularly stray dogs, are
public health problems in Khuzestan province.
Thus, our findings suggest that a comprehensive
program of hygiene education and anthelmintic
prophylaxis as well as the control of stray and feral
dog populations should be implemented. Moreo-
ver, ultrasound screening programs should be
planned in all villages of Khuzestan.
ETHICS APPROVAL AND CONSENT TO
PARTICIPATE
The protocol of this study was reviewed and
approved by the Ethics Committee of Ahvaz Jun-
dishapur University of Medical Sciences (Approv-
al No IR.AJUMS.REC.2016-622).
HUMAN AND ANIMAL RIGHTS
In the current study, informed written consents
were obtained from all of the participants.
CONSENT FOR PUBLICATION
Not applicable.
CONFLICT OF INTEREST
The authors declare no conflict of interest, fi-
nancial or otherwise.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the inhab-
itants of villages for their help in sampling. This
project was supported by Infectious and Tropical
Disease Research Center, Health Research Insti-
tute, Ahvaz Jundishapur University of Medical
Sciences grant OG-95134.
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