Introduction
Camel (Caemelus
dromedarius) is a multiuse animal in semi-arid and arid zones of the world.
Camel provides meat, milk and byproducts which is the good useful addition to
the food chain (Hussain
et al. 2016; Qureshi et al. 2019). In Pakistan, there are 21 breeds of camels reared for different
purposes. However, the major types of camels are mountainous and riverine,
which are mostly reared by pastoral nomads (Ali et
al. 2009; Marghazani 2018). Hydatidosis (also known as cystic
echinococcosis) in ruminants is caused by the larval stage of dog tapeworm “Echinococcus
granulosus”. It is one of the major parasitic problems in camel that
effects the production potential of camel because of the development of many cysts in different organs, known as “Hydatid
Cyst”. The cyst is slow growing, and severity of infection depends on the size
of cyst. When cyst gains full size, it creates pressure on tissues or organs,
followed by necrosis and organ disruption. Most of the meat animals are
slaughtered before these cysts getting full size. However, the life span of camel is 40 to 50 years which is four times more
than other domestic animals so the chances of developing full sized hydatid cyst are more in camel as
compared to other domestic animals (Ahmadi and
Dalimi 2006; Ijaz et al. 2018).
It is also considered as Top
Neglected Tropical Zoonotic Disease, which has been reported in many hosts,
including humans, round the globe (Jenkins 2005;
Hüttner et al. 2008; Liao et al. 2016; Khan et al. 2018). Dogs are definitive host for this parasite while food
animals such as sheep, goats, cattle and camels are likely to act as
intermediate hosts (Torgerson and Budke 2003).
In humans, cystic echinococcosis is listed as most severe parasitic
disease by the World Health Organization. The hydatid cysts develop in liver
and lungs of humans, leading to organ dysfunction (Brunetti and Junghanss 2009). G1 and G3 strains of E. granulosus are most commonly
prevalent species in Humans. However, recent studies have shown that the E. granulosus strain G6 commonly
occurring in camels are also prevalent in humans, indicating that camel may
play a significant role in transmission of this parasite to humans (Kinkar et al. 2018; Laurimäe et
al. 2018).
Infection can be diagnosed
through conventional, serological and molecular techniques. However,
serological diagnosis has been preferred over conventional approaches due to
their high specificity and sensitivity (Abdybekova and Torgerson 2012;
Elmajdoub and Rahman 2015). Molecular
diagnosis may be an option but requires more expertise and instrumentation.
Serological methods standardized for detection of specific antibodies in sera of infected animals are indirect
haemagglutination (IHA) and enzyme linked immunosorbent assay (ELISA) (Latif et al. 2010; Sazmand et al. 2013;
Liao et al. 2016).
In Pakistan, hydatidosis with high prevalence in
domestic animals has been reported by some epidemiologists in some regions (Mirani et al. 2000; Latif et al. 2010;
Ehsan et al. 2017). However, no study has been carried out
regarding occurrence of this disease in camels which are main source of income
for nomads in Balochistan. Importantly, in pastoralist farming, the
camel herd is accompanied by dogs for security purposes which are main host for
this parasite, indicating that the camel in Balochistan may be suffering from
hydatidosis with a possibility of reduced production. Therefore, the current
study was designed to investigate the sero-prevalence of hydatidosis in camel population of
Balochistan, Pakistan.
Material and Methods
Study area
This study was conducted in geographically and
ecologically four different camel raising districts of Balochistan, Pakistan i.e., Barkhan, Musakhel, Loralai and Zhob. The Latitude and
Longitude of Balochistan is 28.49 and 65.09, respectively. Balochistan contains
44% land mass of Pakistan. The four districts are located at northern side of Balochistan
and are hilly areas with high monsoon rain fall. The following prevailing
conditions in the study districts may favour the growth and development of this
parasite: pastoralist pattern grazing, mix herds, keeping dogs with herds, high
population of Wolf, Fox, Jekale and Hyena in mountains.
Estimation of
sample size
For sample size calculation, statistical formula was
used by keeping expected prevalence as 50% with CI as 95% and desired absolute
precision as 6% (Thrusfield 2007).
Multistage cluster sampling was done for selection of camels in the study area.
According to cluster sampling, primary units along with secondary and tertiary
units were selected as union councils, number of farms and camels,
respectively. The secondary units were selected based on number of camels per
herd (>20) with no history of anti-parasitic medication for last one year.
Based on above statistical methods and criteria, 334 camels from 11 herds in 16
union councils were screened for cystic echinococcosis.
Sample
collection and processing
From each animal, approximately 5 mL blood sample was
aseptically collected from jugular vein using 21.5-gauge sterile needle in a
gel-clot activator vacutainer (Improvacuter, Germany). All samples were
transported to laboratory and centrifuged at 4000 rpm for 5 min. Then, the serum
was separated in cryovial tubes and stored at -20oC until further experiment. From herds’ owners, complete
information regarding possible risk factors, including previous medication,
age, sex and breed were collected on pre-designed questionnaire.
Serological analysis
For detection of hydatidosis in camel, an indirect enzyme linked immunosorbent assay
(iELISA) was performed using antigen B (EgAgB) of hydatid cyst by following the
steps and conditions described by Al-Kitani et
al. (2017). The EgAgB was kindly provided by Animal Health Research
Centre, Ministry of Agriculture & Fisheries, Oman (Al-Kitani et al. 2017).
Statistical analysis
The relationship between each
factor (age, sex, breed, study districts, season) and seroprevalence of hydatidosis was
computed using both the univariate analysis through chi-square test and
multivariate analysis through binary logistic regression model with backward
step approach (Thrusfield 2007). The risk factors were further
divided into two categories, including individual level model (age, breed,
gender) and herd level model (districts, season). The evaluation of model
fitness and classification of outliers
was performed at 0.5 cut off point. The 95% CI for all these tests were also
computed. All the analyses were performed at 0.5% level of significance using S.P.S.S.
software (IBM S.P.S.S. Statistics
for Windows, Version 20.0) (Urdaz-Rodriguez
et al. 2009).
Results
Table 1: Univariate and multivariate
analyses for assessment of association of risk factors with the occurrence of hydatidosis
in camels in Balochistan Province, Pakistan
|
Category |
Variable |
Prevalence (%) (Positive/ total samples) |
95%CI |
Univariate analysis |
Multivariate analysis |
||
|
Chi-square |
P Value |
OR |
P value |
||||
|
Gender |
Female |
41.43 (104/251) |
33.9-50.8 |
χ2=14.27 |
P=0.013 |
2.96 |
0.0004 |
|
Male |
19.27 (16/83) |
15.3-20.5 |
- |
- |
|||
|
Age |
>10 years |
61.25 (49/80) |
55.5-68.9 |
χ2=34.36 |
P=0.014 |
8.34 |
0.0001 |
|
5-10 years |
37.58 (53/141) |
31.8-44.2 |
3.18 |
0.0002 |
|||
|
<5 years |
15.93 (18/113) |
13.4-16.5 |
- |
- |
|||
|
Breed |
Raigi |
32.04 (33/103) |
25.4-41.1 |
χ2=5.66 |
P=0.010 |
2.33 |
0.0079 |
|
Pahwal |
62.26 (66/106) |
57.6-68.9 |
8.17 |
0.0001 |
|||
|
Kohi |
16.80 (21/125) |
12.3-20.8 |
- |
- |
|||
|
Herd Region |
Musakheil |
40.00 (52/130) |
36.4-44.7 |
χ2=0.06 |
P=0.014 |
1.56 |
0.0016 |
|
Lorallai |
32.08 (17/53) |
28.3-34.7 |
1.10 |
0.0085 |
|||
|
Zhob |
37.04 (30/81) |
35.2-41.2 |
1.37 |
0.0036 |
|||
|
Barkhan |
30.00 (21/70) |
24.4-32.5 |
- |
- |
|||
|
Season |
Spring |
44.00 (44/100) |
39.8-48.9 |
χ2=1.44 |
P=0.016 |
3.45 |
0.0008 |
|
Summer |
24.44 (22/90) |
22.1-27.4 |
1.41 |
0.0037 |
|||
|
Winter |
55.41 (41/74) |
51.2-60.8 |
5.45 |
0.0001 |
|||
|
Autumn |
18.57 (13/70) |
14.9-21.1 |
- |
- |
|||
Antibodies against cyst form of E. granulosus were detected in camels belonging to all study areas
of Balochistan with varied prevalence. The
overall prevalence of hydatidosis in camel population in study districts was
35.92% (120/334), as determined through iELISA. The univariate analysis
indicated that various factors influenced the prevalence of hydatidosis in
camels in the study area. The higher prevalence of the disease was observed in
district Musakhel (40.00%, χ2=7.12, P=0.010)
as compared to those in Zhob (37.04%), Loralai (32.08) and Barkhan (30.00%). Gender-wise
prevalence of hydatidosis was higher in female camels (41.43%, χ2=14.27, P=0.003) as compared to those of males
(19.27%). Among different breeds, the higher prevalence of hydatidosis was
observed in Pahwal breed (62.26%, χ2=5.66, P=0.001), followed in decreasing order by Raigi (32.04%) and Kohi
breeds of camels (16.80%). Age-wise prevalence was higher in >10 years age
group (61.25%, χ2=34.36, P=0.014),
as compared to those of 5–10 years (37.58%) and <5 years age groups (15.93%)
in decreasing order. According to seasons, the prevalence of hydatidosis was
significantly higher (χ2=1.44, P=0.016)
in Winter (55.41%) and lower in Autumn (18.57%). However, no significant
difference in the prevalence of hydatidosis was observed during Summer (24.44%)
and Autumn (18.57%). The details regarding number of samples and confidence
intervals have been mentioned in Table 1.
The multivariate model using
binary logistic regression was applied for the determination of association of
different risk factors with prevalence of hydatidosis at both individual (age,
breed, gender) and herd level (Districts, seasons) (Table 1). The model fitness
tests, including Lemeshow and Hosmer Test (χ2=14.08, df=2, P=0.001) and Nagelkerke R Square
(0.038), indicated that binary regression model is a weak model to investigate
the association of individual level factors with the prevalence of hydatidosis. However, similar to the
statistical findings of univariate analysis, the prevalence of hydatidosis was higher (P < 0.05) in females (OR=2.96), Pahwal
breed (OR=8.17) and above than 10 years age group (OR=8.34) as compared to
those of respective variables in each of these categories. At herd level,
Lemeshow and Hosmer Test (χ2=0.732, df=2, P = 0.583) and Nagelkerke R Square (0.038) indicated that binary
logistic regression model is best fitted to investigate the association of risk
factors with the prevalence of hydatidosis
at herd level. In contrast to the results of univariable analysis, the
prevalence of hydatidosis was
found significantly different among different seasons (P < 0.05), being higher prevalence in Winter (OR=5.45), followed
in decreasing order by Spring (OR=3.45), Summer (OR=1.41) and Autumn. However,
among study districts, the prevalence of hydatidosis
was higher in Musakhel district (OR=1.56, P<0.05),
followed in decreasing order by Zhob (OR=1.37), Loralai (OR=1.10)
and Barkhan, as indicated by univariate analysis. The detailed information
regarding association of risk factors with prevalence of hydatidosis along with confidence
intervals, Odds’ ratios and P values through univariate and multivariate
analyses has been mentioned in Table 1.
Discussion
The
prevalence of hydatidosis in Pakistan has been reported in wide range of host
in many areas such as 8.85% in Sheep, 6.21% in Goat (Iqbal et al. 2012), 7.19% in cattle and
7.52% in buffalo (Latif et al. 2010)
in various areas on Punjab Province. Although, a few studies have been
conducted to ascertain the occurrence of this disease in camels (Latif et al. 2010). However, the
epidemiological data of hydatidosis
in camels in Balochistan is not collected so far, which is having largest
population of this animal in Pakistan. Interestingly, a higher prevalence of
hydatidosis has been reported in sheep (46.74%) in Quetta district of
Balochistan (Ahmed et al. 2006),
highlighting the occurrence of this diseases in camel in the province.
Therefore, the present study was designed to investigate the sero-prevalence of
cyst form of E. granulosus in four
districts of Balochistan province, including Barkhan, Musakhel, Loralai and
Zhob, which have high camel population in the province.
In the present study, 35.92% camels were sero-positive
for hydatidosis, including
30.00% in Barkhan, 40% in Musakhel, 32.08% in Loralai and 37.04% in Zhob
district. Though, in another province of Pakistan, namely Punjab, a report
published in 2012 indicated the prevalence of this disease in camels as 17.29% (Latif et al. 2010), which is lower than
that of present study. This higher prevalence of this disease in camels in
Balochistan may be due to following reasons: (1) the camels in the province are
generally kept in pastoralist conditions, including utilization of large
grazing areas receiving wide range of animal species which may favor the
disease spread, (2) Likewise, poor diet and draught stress weaken their
resistance to disease, (3) Deployment of large population of dogs (definitive
host) which are main reservoir of this parasite. Another factor is the lack of
implementation of quarantine measures in the
province for camels coming from neighboring countries. As for example,
Balochistan share its border with Afghanistan and Iran, where a high prevalence
of this disease in camel (60%) has been reported (Ahmadi 2005).
The hydatidosis has been reported in camels in many
countries, although lower than that of present study, such as 12.54% prevalence
in Libya (Elmajdoub and Rahman 2015),
32.85% in Saudi Arabia (Ibrahim 2010),
1.28% in Oman (Idris et al. 1999).
In contrast, a higher prevalence of hydatidosis in camel (60%) has been
documented in some areas of Iran (Ahmadi 2005). This varied prevalence of hydatidosis in camel among
different countries may be due to different climatic conditions, farming
system, on-farm management and housing practices of that area and sample size
in each study.
With
respect to animal gender, it has largely been reported that the occurrence of
parasitic infections is higher in females as compared to those of males, as the
growth and development of parasite larval stages increased due to
immunosuppression in pregnancy and parturition stress. Moreover, the prolonged
keeping of females for several years for breeding and milking purpose make them
more exposed to parasites as compared to males which are slaughtered at young
ages for meat purpose (Hussen et al.
2019). Accordingly, various studies have shown a higher prevalence of hydatidosis
in females as compared to those of males (Salih et
al. 2011; Pour et al. 2012; Khan et al. 2013).
Similarly, in the present study, females had higher prevalence of this disease
(41.43%) than those of males (19.27%). Apart from the above reasons, male
animals in the study area are kept at farm due to aggressive behavior, while,
female animals mostly graze in a pasture which may increase the chances of
ingestion of infective stage of this parasite through contaminated vegetation
(Personal observation).
Age of the animals is another reported factor
influencing the prevalence of many parasitic infections (Brunetti and Junghanss 2009). In the present study, highest
prevalence of hydatidosis was recorded in older animals (>10 years old age
group), followed in decreasing order by 5–10 years old and <5 years old age
groups. However, there is dearth of knowledge regarding association of age with
transmission dynamics of this parasite in camels. The possible reasons of this
higher seroprevalence in older animal may include, (1) weaken immune system
against pathogens (Varcasia et al. 2007),
(2) persistence of antibodies due to prolonged survival of hydatid cyst on
organs of host for many years (Liao et al.
2016), (3) higher population of female animals in this age group, which
were more infected in the present study (Personal observation). Nevertheless,
various scientists in other regions documented higher prevalence of this disease
in old age groups of other animal species (Lahmar
et al. 1999; Capuano et al. 2006; Ibrahim et al. 2008;
Rinaldi et al. 2008).
Among various
breeds of camel, the highest prevalence of hydatidosis was recorded in Pahwal
breed as compared to those of Raigi and Kohi. This varied prevalence of the
disease among various breeds may be linked with feeding habits of these breeds,
as Pahwal breed graze in pastures and Kohi breed browse leaves of trees, herbs
and shrubs (Raziq et al. 2010).
Moreover, Kohi and Raigi are local breeds of the study area, which are well
adapted to harsh and drought conditions of Balochistan and presumed to be
resistant to parasitic infections (Raziq et
al. 2010).
The highest prevalence of hydatidosis
was documented in camels in District Musakhel than those of other districts.
The higher prevalence of hydatidosis in camels in this district may be due to
following reasons: (1) highest population of camels, including large number of
females, (2) presence of large number of wild animals, including Wolf, Fox, Jackal
and Hyena which are definitive host of this parasite, further contaminating the
pasture through feces, (3) existence of pastoral system.
According to seasons, a higher prevalence of hydatidosis
was observed during Winter and Spring as compared to Autumn and Summer. In Winter,
due to cold and dry climatic conditions, less fodder and fewer grazing areas
are available for camels in Balochistan, where pastoralist farming system is
prevailing. Consequently, the animals may become malnourished with weakened
immunity; and they start licking bones and faeces on the ground which may
increase the likelihood of transmission of this parasite through feco-oral
route (Personal observation). On the other hand, the higher prevalence of hydatidosis in camels of study area
in Spring may be due to rainy period increasing the spread of infective stage
of this parasite from one area to surroundings.
Conclusion
The overall prevalence of hydatidosis was 35.92% in four districts of Balochistan. The
animals having age more than 10 years had more prevalence as compared to
younger animals. In female camels, the prevalence of hydatidosis was
higher as compared to those of male animals. Among different breeds of camel,
the prevalence of hydatidosis was higher in Pahwal breed as compared to those
of Kohi and Raigi. Nevertheless, this high
prevalence of hydatidosis in camel is also highlighting that the human
population linked with camel farming in the study area may be at risk of getting
this infection, as evident by previous studies showing high prevalence of camel
Echinococcus strains in humans.
Acknowledgment
Special thanks to Dr. Muhammad Saqib (Associate
Professor, Department of Clinical Medicine and Surgery, Faculty of veterinary
science, University of Agriculture Faisalabad, Pakistan) for provision of EgAgB
antigens from Animal Health Research Centre, Ministry of Agriculture &
Fisheries, Oman.
References
Abdybekova A, P Torgerson (2012).
Frequency distributions of helminths of wolves in Kazakhstan. Vet Parasitol
184:348‒351
Ahmadi N (2005). Hydatidosis in camels (Camelus dromedarius) and their potential
role in the epidemiology of Echinococcus
granulosus in Iran. J Helminthol 79:119‒125
Ahmadi N, A Dalimi (2006).
Characterization of Echinococcus
granulosus isolates from human, sheep and camel in Iran. Infect Genet
Evol 6:85‒90
Ahmed S, M Nawaz, R Gul, M Zakir, A Razzaq
(2006). Some epidemiological aspects of hydatidosis of lungs and livers of
sheep and goats in Quetta, Pakistan. Pak J Zool 38:1–6
Al-Kitani FA, MK Mansoor, MH Hussain, AH
Al Rawahi, M Saqib, MG Al Maawali (2017). Sero-epidemiology of cystic
echinococcosis (Echinococcus granulosus)
in the livestock of Oman. Vet Parasitol 8:21‒27
Ali I, MS Chaudhry, U Farooq (2009). Camel
rearing in Cholistan desert of Pakistan. Pak Vet J 29:85‒92
Brunetti E, T Junghanss (2009). Update on
cystic hydatid disease. Curr Opin Infect Dis 22:497‒502
Capuano F, L Rinaldi, M Maurelli, A
Perugini, V Veneziano, G Garippa, C Genchi, V Musella, G Cringoli (2006).
Cystic echinococcosis in water buffaloes: epidemiological survey and molecular
evidence of ovine (G1) and buffalo (G3) strains. Vet Parasitol 137:262‒268
Ehsan M, N Akhter, B Bhutto, A Arijo, JA
Gadahi (2017). Prevalence and genotypic characterization of bovine Echinococcus granulosus isolates by
using cytochrome oxidase 1 (CO1) gene in Hyderabad, Pakistan. Vet Parasitol
239:80‒85
Elmajdoub LO, WA Rahman (2015). Prevalence
of hydatid cysts in slaughtered animals from different areas of Libya. Open
J Vet Med 5:1
Hussain R, A Khan, RZ Abbas, A Ghaffar, G
Abbas, TU Rahman, F Ali (2016). Clinico-hematological and biochemical studies
on naturally infected camels with trypanosomiasis. Pak J Zool 48:311‒316
Hussen J, T Shawaf, AIA Al-Mubarak, NAA
Humam, F Almathen, HJ Schuberth (2019). Leukocytes immunophenotype and
phagocytosis activity in pregnant and nonpregnant dromedary she camels. Pak Vet J 2019:1-5 (http://dx.doi.org/10.29261/pakvetj/2019.117)
Hüttner M, M Nakao, T Wassermann, L
Siefert, JD Boomker, A Dinkel, Y Sako, U Mackenstedt, T Romig, A Ito (2008).
Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Intl
J Parasitol 38:861‒868
Ibrahim MM (2010). Study of cystic
echinococcosis in slaughtered animals in Al Baha region, Saudi Arabia:
interaction between some biotic and abiotic factors. Acta Trop 113:26‒33
Ibrahim MM, M Ghamdi, M Gahmdi (2008).
Helminths community of veterinary importance of livestock in relation to some
ecological and biological factors. Turk Parazitol Derg 32:42‒47
Idris M, A Ruppel, H Gehrig-Feistel, A
Alansari, A Al-Rejaibi, M Tageldin, K El-Sinary (1999). The seroprevalence of
cystic hydatidosis in Oman. Ann Trop Med Parasitol 93:259‒263
Ijaz
M, MA Zaman, F Mariam, SH Farooqi, AI Aqib, S Saleem, A Ghaffar, A Ali, R
Akhtar (2018). Prevalence, hematology and chemotherapy of gastrointestinal
helminths in camels. Pak Vet J 38:81‒85
Iqbal H, A Maqbool, M Lateef, M Khan, A
Riaz, A Mahmood, F Atif, Z Ali, M Ahmad (2012). Studies on hydatidosis in sheep
and goats at Lahore, Pakistan. J Anim Plant Sci 22:894‒897
Jenkins DJ (2005). Hydatid control in
Australia: where it began, what we have achieved and where to from here. Intl
J Parasitol 35:733‒740
Khan A, S Simsek, H Ahmed (2018).
Molecular epidemiology of Echinococcus species in Pakistan. Asian Pac J Trop Med 11:36–36
Khan AM, M Gazi, S Bashir (2013). Seasonal
prevalence of hydatidosis in buffaloes–A retrospective study. Vet World
6:647‒650
Kinkar L, T Laurimäe, G Acosta-Jamett, V
Andresiuk, I Balkaya, A Casulli, RB Gasser, JVD Giessen, LM González, KL Haag (2018).
Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto
genotype G1. Intl J Parasitol 48:729‒742
Lahmar S, M Kilani, P Torgerson, M Gemmell
(1999). Echinococcus granulosus
larvae in the livers of sheep in Tunisia: the effects of host age. Ann Trop
Med Parasit 93:75‒81
Latif AA, A Tanveer, A Maqbool, N Siddiqi,
M Kyaw-Tanner, RJ Traub (2010). Morphological and molecular characterisation of
Echinococcus granulosus in livestock
and humans in Punjab, Pakistan. Vet Parasitol 170:44‒49
Laurimäe T, L Kinkar, E Moks, T Romig, RA
Omer, A Casulli, G Umhang, G Bagrade, M Irshadullah, M Sharbatkhori (2018).
Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato
genotypes G6/G7 and G8/G10 can be regarded as two distinct species. Parasitol
145:1929‒1937
Liao S, C Liu, Z Chen, D Shi, N Qi, J Li,
J Zhang, M Xie, M Lv, C Wu (2016). Seroprevalence of Echinococcus granulosus in dogs in Southern China. Intl Res J Environ
Publ Health 3:91‒95
Marghazani IB (2018). The Camels in
Balochistan: Status, farming practices and camel centered measures. Pure
Appl Biol 8:503‒508
Mirani A, N Akthar, M Brohe, S Bughio, F
Oad (2000). Hydatidosis in buffaloes at Larkana slaughter house (Pakistan). Pak
J Biol Sci 3:1311‒1312
Pour AA, S Hosseini, P Shayan (2012). The
prevalence and fertility of hydatid cysts in buffaloes from Iran. J
Helminthol 86:373‒377
Qureshi AS, S Rehan, M Usman, K Hayat, Z
Umar, A Sarfraz (2019). Quantitative evaluation of age-related anatomical
characteristics of selected digestive organs of dromedary camel. Pak Vet J 2019:1–6
Raziq A, KD Verdier, M Younas (2010).
Ethnoveterinary treatments by dromedary camel herders in the Suleiman
Mountainous Region in Pakistan: an observation and questionnaire study. J
Ethnobiol Ethnomed 6:16–28
Rinaldi L, M Maurelli, F Capuano, A
Perugini, V Veneziano, S Cringoli (2008). Molecular update on cystic
echinococcosis in cattle and water buffaloes of southern Italy. Zoonoses. Publ
Health 55:119‒123
Salih M, H Degefu, M Yohannes (2011).
Infection rates, cyst fertility and larval viability of hydatid disease in
camels (Camelus dromedarius) from
Borena, Kereyu and Harar areas of Ethiopia. Prevalence 10:21–26
Sazmand A, MR Jalali, S Hekmatimoghaddam,
Z Asadollahi (2013). Seroprevalence of hydatidosis in camels of Yazd Province,
Iran. J Vet Lab Res 5:121‒128
Thrusfield M (2007). Veterinary
Epidemiology, 3rd edition. Blackwell Publishing, UK
Torgerson P, C Budke (2003).
Echinococcosis–an international public health challenge. Res Vet Sci
74:191‒202
Urdaz-Rodriguez J, G Fosgate, A Alleman, D
Rae, G Donovan, P Melendez (2009). Seroprevalence estimation and management
factors associated with high herd seropositivity for Anaplasma marginale in commercial dairy farms of Puerto Rico. Trop
Anim Health Prod 41:1439‒1448
Varcasia A, S Canu, A Kogkos, AP Pipia, A Scala, G
Garippa, A Seimenis (2007). Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece.
Parasitol Res 101:1135‒1139