An Epidemiological updating on cystic echinococcosis in cattle and sheep in Sicily, Italy

Abstract

Cystic echinococcosis (CE) is a zoonotic parasitic
disease caused by larval stage of dog tapeworm
Echinococcus granulosus . Transmission occurs predominantly
in synanthropic cycles, involving sheep,
goats, cattle and pigs as intermediate hosts. In Italy,
according to sheep breeding, the infection rate
increases from north to south regions including
islands. Previous CE prevalence recorded in Sicily in
cattle and sheep were 11.1% and 15.6%, respectively.
The cyst viability, studied in sheep only, was
1,9% (Magliarditi D, Niutta PP, 1995, Atti Associazione
Siciliana di Sanità Veterinaria: 165-167;
Scala A et al. , 2001, 20th International Congress of
Hydatidology, Kusadasi, Turkey: 303). This paper
reports preliminary results on prevalence and viability
of CE in cattle and sheep in Sicily and is part of
a larger research focused on the epidemiological
updating of E. granulosus infection.

Full text

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Parassitologia 46: 423-424, 2004
An epidemiological updating on cystic echinococcosis in
naria e Patologia Animale, University of Bologna, Italy; 3 Dipartimento di Biologia Animale, University of Sassari, Italy;
cattle and sheep in Sicily, Italy
S. Giannetto 1, G. Poglayen 2, E. Brianti 1, C. Sorgi 1, G. Gaglio 1, S. Canu 3, A. Virga 4
l Dipartimento di Sanità Pubblica Veterinaria, University of Messina, Italy; 2 Dipartimento di Sanità Pubblica Veteri­
4 Assessorato alla Sanità della Regione Siciliana, Palermo, Italy.
Cystic echinococcosis (CE) is a zoonotic parasitic
disease caused by larval stage of dog tapeworm
Echinococcus granulosus. Transmission occurs pre­
dominantly in synanthropic cycles, involving sheep,
goats, cattle and pigs as intermediate hosts. In Italy,
according to sheep breeding, the infection rate
increases from north to south regions including
islands. Previous CE prevalence recorded in Sicily in
cattle and sheep were I l.1 % and 15.6%, respec­
tively. The cyst viability, studied in sheep only, was
1,9% (Magliarditi D, Niutta PP, 1995, Atti Associ­
azione Siciliana di Sanità Veterinaria: 165-167;
Scala A et al., 2001, 20th International Congress of
Hydatidology, Kusadasi, Turkey: 303). This paper
reports preliminary results on prevalence and viabil­
ity of CE in cattle and sheep in Sicily and is part of
a larger research focus ed on the epidemiologica l
updating of E. granulosus infection.
Between May 2004 and October 2004, a total of
393 cattle and 41 1 sheep from northeast and mid­
west of the island were examined for CE at local abat­
toirs. Cysts from positive organs were examined for
protoscoleces presence and classified as fertile (with
viable protoscoleces) or sterile (without or with not
viable protoscoleces). Aliquots of viable cysts (germi­
nal layer and protoscoleces), were stored at -20°C in
glass tubes. From these isolates and with the strain
typing purpose, DNA was extracted with a commer­
ciaI kit (High pure PCR template preparation kit,
Roche) and PCR (Dinkel A et al., 2004, Int J Para­
sitol, 34: 645-653) were carried out to discriminate
the various strains (Eckert J et al., 2001, WHO/OIE
Manual on Echinococcosis in Humans and Animals: a
Public Health Problem .of Global Concerno World
Health Organization, Paris, France: 265). The strain
obtained by PCR was confirmed by sequencing COI
and NADH mithocondrial genes (Bowles J, McManus
Dp, 1993, Int J Parasitol, 23: 969-972; Bowles J et al.,
1994, Parasitology, 109: 215-221).
Cyst frequencies from the different organs and
infection frequency in the different host age classes
were compared by chi-squared test. The variances of
CE prevalence within the host age were analyzed
using logistic regression mode!. Statistical analyses
�orresponding author: Salvatore Giannetto, Sezi?ne �i yaras­
dell'Annunziata, 98168 Messina, Italy, Tel/Fax +39 090
355922, e-mail: sgiannetto@unime.it
sttologia e Malattie Parassitarie, Dipartimento dI Samta Pub­
blica Veterinaria, University of Messina. Polo Universitario
were performed with the software SPSS 12.0 for
Windows (Apache Software Foundation, Chicago).
Table 1. Age prevalence of E. granulosus infection in caUle
and sheep.
The overall CE prevalence was 67.1 % (264/393) in
caUle and 57.6% (237/41 1) in sheep. In Table 1 are
showed the infection rates by age classes of caule and
Age (years)
Cattle rate
(infected/examined)
Sheep rate
(infected/examined)
0-1
1-2
2-3
3-4
4-5
5-6
6-7
7-8
8-9
9-10
>10
X2
Total
oa (0/24)
0.33b (3/9)
0.38b (5/13)
0.23b (3/13)
0.5ge (10/17)
0.77e (10/13)
0.58e (7/12)
0.65e (1 1/17)
0.78e (21/27)
0.72e (23/32)
0.7ge (171/216)
91 .64*
67.1 (264/393)
oa (0/6)
OA2b (5/12)
OA3b (12/28)
0.6ge (49/71)
0.56e (89/159)
0.82d (27/33)
0.71e (5/7)
0.86e (6/7)
1 (4/4)
29.16*
60.2 (197**/41 1 )
• The differences in age groups with different letter in the same column
are statistically significant (p < 0.05).
•• Qut of 41 1 sampled sheep only for 197 was possible the age determi­
nation.
sheep. The logistic regression model for generaI trend
of CE age-prevalence showed a positive correlation
with an odds ratio per year of 1.23 (1.16-1.30) and
1.45 (1.19-1.76) for caUle and sheep, respectively.
Additionally, sheep were found to be 2.2 time (1.4-
3.3) more at risk than caUle for CE infection. Distri­
bution of cysts in the internaI organs (Table 2)
showed different paUems .in the 2 animai species.
Table 2. Distribution of E. granulosus cysts in caUle and
sheep.
Infected organs
Cattle (n=264)
Number
Sheep (n=237)
Number
%
%
Liver
Lung
Liver+lung
Liver +Iung+other
X2
32
40
190
12.1a
15.1a
72b
0.7e
88
27
121
37.1a
1 1 .3b
51e
OAd
2
430.38*
204.17*
• The CE percentages among internai organs with different letter in the
same column are statistically significant (p<0.05).

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424
S. Giannetto et al. - An epidemiological updating on cystic echinococcosis in Sicily
G1 PCR
isolates
Table 3. E. granulosus strains found from cattle and sheep.
Species (organ)
Number of
(Dinkel 2004)
Sheep (Iungs)
Sheep (Iiver)
Cattle (Iungs)
Cattle (liver)
13
5
5
6
Positive
Positive
Positive
Positive
While in cattle most infections were characterized by
the presence of cysts both in the liver and the lung
followed by lung only and liver only, in sheep cysts
were found mostly in liver. Overall cysts fertility rate
was 4% (16/393) in cattle and 9.2% (38/41 1) in
sheep. A positive correlation between cysts viability
and sheep ages was found with rates ranging from
2% to 28% in 1-2 years and 8-9 years age classes,
respectively. Furthermore, conceming the site of fer­
tile cysts, signifieant differences were found in sheep
where most viable cysts were found in lung (28/148;
in liver 23/209). Strain typing by PCR and mitho- .
condrial genes NADH and COI sequencing showed
the presence of G 1 or Sheep Strain (Table 3) from
both sheep and cattle isolates.
Although in this paper are presented the prelimi­
nary results, the data have important implications.
The positive trend recorded for CE age-prevalence,
in agreement with other studies, shows that there is
no evidence of parasite-induced host immunity or at
least that the natural immunity response in cattle
and sheep has no efficacy in CE infection control
. (Roberts MG et a!., 1 986, Parasitology, 92: 621-
641 ; Cabrera PA et al., 1996, Int J Parasitol, 25:
807-81 3; Dueger EL, Gilman RH, 200.1, Trans R
SocTrop Med Hyg, 95: 379-383; Torgerson PR et
al., 2003, Vet Parasitol, 1 14: 143-153). Further­
more, the results show that sheep tend to be m'ore
at risk than cattle for CE infection, confirming their
role as most important intermediate host in Sicily.
The high number of positive animals and the cysts
viability rates recorded, especially in old cattle,
showed that these ruminants could act as active
intermediate hosts in E. granulosus infecÌion main­
tenance in the island. Additionally, although the
high number of viable cysts found in sampled cattle
no G5 or cattle strain (Thompson RCA, MacManus
G5/G6/G7 PCR
(Dinkel 2004)
NADH
sequence
COI
sequence
Negative
Negative
Negative
Negative
G1
G1
G1
G1
G1
G1
G1
G1
DP, 2002, Parasitol Today, 18: 452) was found. The
finding of the G 1 strain, only. It suggests that fac­
tors due to the strain type might influence the cyst
viability in cattle. Compared to previous surveys in
Sicily, our data show higher prevalence values. This
could be .as a consequence of several factors such as
the ages of the sampled animals, the differences of
the geographical prevalence and the methods of
study. Thus, conceming the age, in the last survey
carried out on sheep CE (Scala A et al., 2001, 20th
Intemational Congress of Hydatidology, Kusadasi,
Turkey: 303), overall prevalence and viability were
15.50/ 0 and 1 .90/ 0 respectively, but all the sampled
sheep were aged 2-3 year-old. Regarding the differ­
ences in geographic prevalence, Poglayen G et al.
(2003, WAAVP 19th Intemational Conference, New
Orleans, USA: 164) well described the importance
of climatic and environmental factors that could
influence the CE prevalence in Sieily. About the
method of study we preferred to personally check
animals at abattoirs. In fact, it is important to note
that surveys based on records from slaughterhouses
usually showed lower prevalence respect to the real
infection rate (Umur S, 2003, J Vet Med, 50: 247-
252). In conclusion, according with Scala et al.
(2001, 20th Intemational Congress of Hydatidology,
Kusadasi, Turkey: 303) "echinococcosis-hydatidosis
continues to be a public health problem in the 2
biggest Italian islands" and these results, at least for
the Italian endemie regions, should be used to stim­
ulate the requirement of a continuous control pro­
gram of this important parasitie zoonotic disease.
Acknowledgments.
The authars would like to thank Dr Michele Drigo far the help
provided in data statistical analyses. The wark was founded by
MURST (COFIN 2003) Prot. 2003070410_002.