ABSTRACT During June 2002 and February 2003 1,800 blood samples were collected from 5 slaughtering plants located in Campania region (Italy) which were supplied by 21 rabbitries situated in central and southern Italian regions, such as Campania, Lazio, Basilicata, Molise, Calabria. The aims of this study were to use the Carbon Immunoassay (India ink) test (CIA) and FC test to determine respectively the prevalence of specific zoonotic agents such as E. cuniculi, T. gondii and Chlamydia psittaci in fattening rabbits. For E. cuniculi of the total number of 1,800 sera examined, 490 were positive and they represented 27.2%. All supplying breeding farms were positive with a percentage from 10% (4/40) to 57.5% (23/40) of total sera collected from each slaughtered batch. Sera resulted less positive for T. gondii: of 1,800 sera only 50 (2.7%) were positive; these date were relative to 6/21 breeding farms. Serological Chlamydia screening resulted totally negative

Baiano A

Bartoli M

Carlo E De

Cerrone A

Ciabrelli M

Fioretti A

Galiero G

Mariani F

CiteSeerX

 
 498 
PARASITOLOGICAL ZOONOSIS IN RABBIT MEAT: 
RESULTS OF SEROEPIDEMIOLOGICAL SURVEY FOR THE INVESTIGATION OF 
ENCEPHALITOZOON CUNICULI, TOXOPLASMA GONDII AND 
CHLAMYDIA PSITTACI  IN ITALIAN RABBITRIES 
 
CERRONE A.1, MARIANI F.1, CIABRELLI M.1, GALIERO G.2, DE CARLO E.2, FIORETTI A.3, 
BAIANO A.3, BARTOLI M. 1 
 
1Istituto Zooprofilattico Sperimentale del Mezzogiorno,  
Via Salute 2, 80055 Portici (NA), Italy,  
annacerr@tin.it, m.bartoli@izsmportici.it  
2Istituto Zooprofilattico Sperimentale del Mezzogiorno. Sezione di Salerno, S.S. 18 Via 
delle Calabrie, 27, 84132 Fuorni (SA), Italy.  
salerno.izsm@tin.it  
3 Dipartimento di Patologia e Sanità Animale. Università degli Studi di Napoli Federico II. 
Facoltà di Medicina Veterinaria. Via F. Delpino, 80100 Napoli, Italy.  
fioretti@unina.it 
 
 
ABSTRACT 
 
During June 2002 and February 2003 1,800 blood samples were collected from 5 
slaughtering plants located in Campania region (Italy) which were  supplied by 21 
rabbitries situated in central and southern Italian regions, such as Campania, Lazio, 
Basilicata, Molise, Calabria. The aims of this study were to use the Carbon 
Immunoassay (India ink) test (CIA) and FC test to determine respectively the prevalence 
of specific zoonotic agents such as E. cuniculi, T. gondii and Chlamydia psittaci in 
fattening rabbits. For E. cuniculi of the total number of 1,800 sera examined, 490 were 
positive and they represented 27.2%. All supplying breeding farms were positive with a 
percentage from 10% (4/40) to 57.5% (23/40) of total sera collected from each 
slaughtered batch. Sera resulted less positive for T. gondii: of 1,800 sera only 50 (2.7%) 
were positive; these date were relative to 6/21 breeding farms. Serological Chlamydia 
screening resulted totally negative. 
 
Key words: Encephalitozoon cunicoli, Toxoplasma gondii, Chlamydia psittaci, zoonosis, 
Carbon Immunoassay. 
 
 
INTRODUCTION 
 
Encephalitozoon cunicoli is one of the mammalian microsporidian pathogens that can 
affect a number of different species of animals as well as humans (X IAO et al. 2001). 
Microsporidia are ubiquitous obligate intracellular sporeforming, small pathogens that 
caused significant agricultural losses and interference with biomedical research. In 1922 
Wright and Craighead reported the first mammalian microsporidial infection in rabbits, 
while microsporidial infection in human beings was first diagnosed by Magarinos Torres 
in 1927. In general, however, microsporidia were not routinely diagnosed. Natural ways 
Proceedings - 8th World Rabbit Congress –September 7-10, 2004 – Puebla, Mexico
 
 499 
of infection transmission are not well known. It is believed that the disease spreads 
horizontally by the oro-fecal route in large breeding farms with the presence of many 
animals, but above all, along the oro-urinal pathway (HALÁNOVÁ et al. 2003). But a key 
role in epidemiology and pathogenesis is also due to vertical, transplacental 
transmission of infection (BANEUX, POGNAN 2003; HALÁNOVÁ et al. 2003). As concerns 
the diffusion of some microsporidial species such as E. cunicoli in human beings, they 
have a zoonotic character, above all in immunocompromised individuals (THOMAS et al. 
1997; SCHOTTELIUS et al. 2000; HALÁNOVÁ et al. 2003). The human clinical pictures 
include diarrhoea, keratitis, sinusitis myositis, pneumonitis and cerebral lesions (ROSSI et 
al. 1998).  
The prevalence of antibodies to E. cuniculi in domestic and laboratory rabbits has been 
found to range from 7.5% to 76% in clinically normal animals, with higher prevalence in 
rabbits suffering from other infections (THOMAS et al. 1997). In industrial animals, and in 
particular in rabbits reared for meat, the infection may cause considerable financial 
losses due to mortality (up to 15%), to increased number of rejected animals and to 
reduced carcass weight (LAVAZZA et al. 1996). 
Another parasitological zoonosis is toxoplasmosis, caused by the protozoan 
Toxoplasma gondii (WALLER, BERGQUIST 1982). Even in this case the risk of an infection 
from rabbit to man is scarce, as rabbit is an intermediate host (TANTINÀ M. et al. 2000). In 
rabbits there is a high level of seroprevalence. Seropositive rabbits have cysts in their 
tissues and most of them remain healthy. In some circumstances illness and death 
among pregnant and nursing does is registered. Rabbits are frequently infected by 
eating feed contaminated by cat faeces containing oocysts of T. gondii (OKERMAN 1994). 
A serological screening for Chlamydia psittaci was done. 
The aims of this study were to use the Carbon Immunoassay (India ink) test (CIA) and 
FC test to determine respectively the prevalence of specific zoonotic agents such as E. 
cuniculi, T. gondii and Chlamydia psittaci in fattening rabbits coming from rabbitries 
located in different Italian regions. 
 
 
MATERIALS AND METHODS 
 
Collection of samples 
 
During June 2002 and February 2003 1,800 blood samples were collected from 5 
slaughtering plants located in Campania region (Italy) which were supplied by 21 
rabbitries situated in central and southern Italian regions, such as Campania, Lazio, 
Basilicata, Molise, Calabria (Table 1). All breeding farms were controlled from twice to 
four times, except for breeding farms 1,9,13,19 and 21 which did not supply rabbits 
anymore to slaughtering plants, so that further samples were not collected.  
 
Isolation and detection 
 
For serological investigations of Encephalitozoon cuniculi and Toxoplasma gondii the 
sera were preserved at –20°C until they were examined. The seropositive rabbits were 
determined by the Carbon Immunoassay (India ink) test (CIA), (WALLER, BERGQUIST 
1982) using a commercial kit produced and distributed by Medicago AB, Uppsala 
Proceedings - 8th World Rabbit Congress –September 7-10, 2004 – Puebla, Mexico
 
 500 
(Sweden). The serological test used to detect chlamydial complement-fixing antibodies 
in animals was the CF test with a commercial antigen (Dade BEHRING MARBURG 
Gmbh from tissutal cultures infected by Chlamydia psittaci and lyophilized after 
inactivation and addiction of stabilizer). 
 
 
Table 1. Examined sera in rabbitries 
 
Range related to 
slaughtering capacity 
Monitored supplying 
breeding farms  Batches Region of origin of animals  Total slaughtered rabbits Total sera 
A) AVELLINO 
3000/day 
2000–3000 animals 
3 
(5, 8, 16) 7 
5), 16) Campania 
8) Calabria 8,350 280 
B) Benevento 
2000/day 
1000–2000 animals 
5 
(6, 13, 14, 15, 19) 9 
6) Molise 
13), 14), 15) Basilicata 
19) Campania 
17,900 360 
C) CASERTA  
1500/day 
1000 –2000 animals 
5 
(1, 3, 4, 7, 12) 10 
1), 3), 4), 7) Campania 
12) Lazio 7,247 400 
D) NAPLES  
600/day 
500 – 1000 animals 
5 
(9, 10, 11, 17, 21) 9 
9), 10), 11) Lazio 
17) Campania 
21) Unknown 
5,100 360 
E)  SALERNO 
300/day 
500 – 1000 animals 
3 
(2, 18, 20) 10 2), 18), 20) Campania 3,200 400 
TOTAL 21 45  41,797 1,800 
 
 
 
RESULTS AND DISCUSSION 
 
Table 2 shows the results obtained during serological monitoring in each farm. In the 
case of a positive immunological reaction to the presence of antibodies against E. 
cuniculi in the serum, this antigen will be stained greyish-black within 5 minutes. Of the 
total number of 1,800 sera examined, 490 were positive and they represented 27.2%. 
All supplying breeding farms were positive with a percentage from 10% (4/40) to 57.5% 
(23/40) of total sera collected from each slaughtered batch. Sera resulted less positive 
for T. gondii: of 1,800 sera only 50 (2.7%) were positive; these date were relative to 6/21 
breeding farms. Serological Chlamydia screening resulted totally negative. This confirms 
the hypothesis that Chlamydiosis mainly involves the does during the first and the last 
week of pregnancy and the young rabbits during the first week of life (BURATTO , COLIN, 
1992). 
Proceedings - 8th World Rabbit Congress –September 7-10, 2004 – Puebla, Mexico
 
 501 
 
Table 2. Serological results from 21 rabbitries 
 
SEROLOGICAL TEST 
PATOGENI 
ENCEPHALITOZOON CUNICULI 
(E)  
TOXOPLASMA GONDII  
(T) 
CHLAMYDIA PSITTACI  
© FARM 
LOCATION 
BREEDING 
FARM 
DATE OF 
COLLECTING 
N° 
POSITIVE 
BATCHES  T
O
TA
L 
A
N
IM
A
LS
 O
F 
TH
E
 
S
LA
U
G
H
TE
R
E
D
 
B
A
TC
H
 
POSITIVE/40 
(N°)  
POSITIVE/40 
(%) 
POSITIVE/40  
(N°)  
POSITIVE/40 
(%) 
POSITIVE/40  
(N°)  
POSITIVE/40 
(%) 
AVELLINO 1 16/10/02 1 (E) 700 15 37.5 --- --- --- --- 
03/07/02 300 4 10 ---  --- --- 
05/11/02 300 12 30 4 10 --- --- 2 
10/12/02 400 20 50 ---  --- --- 
17/07/02 1000 15 37.5 ---  --- --- 
04/11/02 913 4 10 ---  --- --- 3 
25/11/02 600 7 17.5 ---  --- --- 
01/07/02 360 23 57.5 ---  --- --- 4 
09/12/02 546 9 22.5 ---  --- --- 
01/07/02 700 15 37.5 ---  --- --- 
11/09/02 2000 14 35 ---  --- --- 
BENEVENTO 
5 
13/11/02 
10 (E) 
1 (E, T) 
700 16 40 ---  --- --- 
23/07/02 2200 16 40 ---  --- --- CAMPOBASSO 6 
24/09/02 
2 (E) 
2200 14 35 ---  --- --- 
09/09/02 500 11 27.5 ---  --- --- 
30/09/02 700 8 20 ---  --- --- CASERTA 7 
27/01/03 
2 (E) 
1 (E, T) 
928 21 52.5 16 40 --- --- 
17/07/02 1500 4 10 ---  --- --- COSENZA  8 
18/09/02 
2 (E) 
1000 12 30 ---  --- --- 
FROSINONE  9 07/02/03 1 (E) 450 9 22.5 ---  --- --- 
23/10/02 700 ---  ---  --- --- 10 
28/11/02 800 7 17.5 ---  --- --- 
10/07/02 600 ---  ---  --- --- 11 
14/02/03 410 4 10 ---  --- --- 
LATINA 
12 10/03/03 
3 (E) 
1000 14 35 ---  --- --- 
13 25/06/02 2000 4 10 ---  --- --- 
19/11/02 2800 6 15 4 10 --- --- 14 
10/12/02 1337 ---  ---  --- --- 
05/11/02 2900 12 30 ---  --- --- 
26/11/02 2016 28 70 ---  --- --- 
POTENZA 
15 
11/02/03 
4 (E) 
1 (E, T) 
2400 14 35 ---  --- --- 
08/07/02 1450 23 57.5 ---  --- --- 16 
13/01/03 700 16 40 6  --- --- 
20/02/03 320 3 7.5 ---  --- --- 
27/02/03 330 ---  ---  --- --- 17 
20/11/02 800 5 12.5 ---  --- --- 
18/09/02 400 28 70 12 30 --- --- 
04/09/02 300 6 15 6 15 --- --- 
20/11/02 400 8 20 ---  --- --- 
18 
08/01/03 400 18 45 ---  ---  
19 08/01/03 1455 6 15 8  --- --- 
10/07/02 150 8 20 ---  --- --- 
07/10/02 200 15 37.5 ---  --- --- 
SALERNO 
20 
28/01/03 
8 (E) 
4 (E, T) 
300 16 40 ---  --- --- 
UNKNOWN  21 05/12/02 1 (E) 332 15 37.5 --- --- --- --- 
Total positive sera/1,800 tested sera 490 27.2% 50 2.7% 0 0 
 
 
 
Proceedings - 8th World Rabbit Congress –September 7-10, 2004 – Puebla, Mexico
 
 502 
CONCLUSIONS 
 
Immunodiagnosis has proved to be a more reliable method to detect the infection in vivo 
(VARGA, HORVÁTH 1988). For verifying the extent of E. cuniculi in groups of rabbits the 
CIA test is quick and easy to use (LAVAZZA et al. 1996). The same test was found to be a 
rapid and realiable method for identifying rabbits that were seropositive for T. gondii 
(WALLER, BERGQUIST 1982). Fattening rabbits resulted highly positive for E. cunicoli and 
this confirms the necessity of monitoring programmes to control the spread of this 
zoonosis (LAVAZZA et al. 1996) and to control this parasite. Any attempt to reduce the 
infection level can succeed only if the best hygienic conditions are ensured (VIRÁG et al. 
1986). The scarce seroprevalence registered during our research, according to other 
Authors, confirms that rabbit is not a carrier animal of Toxoplasmosis to human beings 
and that there is no zoonotic risk from this animal. 
 
 
ACKNOWLEDGEMENTS 
 
Research supported by funds from the Italian Health Ministry (cod. IZSM CB 211801). 
 
 
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Proceedings - 8th World Rabbit Congress –September 7-10, 2004 – Puebla, Mexico


PARASITOLOGICAL ZOONOSIS IN RABBIT MEAT: RESULTS OF SEROEPIDEMIOLOGICAL SURVEY FOR THE INVESTIGATION OF ENCEPHALITOZOON CUNICULI, TOXOPLASMA GONDII AND CHLAMYDIA PSITTACI IN ITALIAN RABBITRIES

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PARASITOLOGICAL ZOONOSIS IN RABBIT MEAT: RESULTS OF SEROEPIDEMIOLOGICAL SURVEY FOR THE INVESTIGATION OF ENCEPHALITOZOON CUNICULI, TOXOPLASMA GONDII AND CHLAMYDIA PSITTACI IN ITALIAN RABBITRIES

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