Epidemiology of sylvatic trichinellosis in north-western Italy

Rev. sci. tech. Off. int. Epiz., 1992,11 (4), 1039-1046
Epidemiology of sylvatic trichinellosis in
north-western Italy
L. ROSSI *, E. POZIO **, W. MIGNONE ***, C. ERCOLINI *** and V. DINI ****
Summary: Muscle samples from 7,142 wild boars (Sus scrofa), 80 free-ranging
hogs, 1,462 red foxes (Vulpes vulpes), 90 mustelids, 15 Alpine
marmots
(Marmota marmota), 873 rodents and 92 insectivores were examined for
Trichinella Railliet, 1895. A wild boar, a badger (Meles meles) and 30 foxes
(2.1%) were found to be infected. Eleven vulpine isolates and the wild boar
isolate were identified as Trichinella britovi. These results show that the wild
boar has little significance as a reservoir of T. britovi in the area under study.
A vulpine isolate resulted in low infectivity in experimentally-infected
swine.
The prevalence of trichinellosis in the vulpine population is higher in the
mountains than in lowland areas and indicates the key role played by this
carnivore in the epidemiology of T. britovi. Preliminary results from four field
trials seem to demonstrate that differences in attitudes towards cannibalism exist
between mountain and lowland foxes.
KEYWORDS: Cannibalism - Fox - Italy - Trichinella britovi - Wild boar.
INTRODUCTION
Recent taxonomic contributions to the knowledge of the genus Trichinella Railliet,
1895 have resulted in the recognition of five species and three different gene pools on
the world scale (10,24), the epidemiology of which needs to be carefully redefined. The
aetiological agent of trichinellosis in Italy has b e e n identified recently as Trichinella
britovi (T3), a Trichinella species of the south-west Palearctic region, originally
considered as Trichinella nelsoni by Soviet a u t h o r s (29). T h e domestic species,
T. spiralis sensu stricto ( T l ) , has occasionally b e e n i m p o r t e d into Italy (22). In the
present paper, the authors report on the epidemiology of T. britovi in the north-west of
Italy and make reference to both unpublished and published data (9,25,26).
MATERIALS AND METHODS
Research carried out to date has attempted to answer the following questions:
- D o wild swine play a role of epidemiological significance?
- A r e foxes the main or only reservoir of T. britovi,
indicator of the prevalence of this parasite?
or are they merely a good
* Facoltà di Medicina Veterinaria, Via Nizza 52,10126 Turin, Italy.
** Istituto Superiore di Sanità, Viale Regina Elena 299,00161 Rome, Italy.
*** Istituto Zooprofilattici Sperimentale (Piemonte, Liguria e Valle d'Aosta), Via Bologna 148,
Turin, Italy.
**** Unità Socio-Sanitaria Locale 6, Via del Collegio 18, Carcare (Savona), Italy.
1040
Muscle samples (principally tongue and diaphragm) from 7,142 wild boars were
collected during five consecutive hunting seasons (from 1986/1987 to 1990/1991).
Diaphragms of 80 free-ranging hogs were also collected in 1991. The origin of samples is
reported in Tables I and II. Parasitic larvae were detected by means of trichinelloscopy
(54 cells per sample) and the peptic digestion technique (6) on samples of 5-10 g each. In
addition, three 60-day-old nematode-free piglets were fed, over a 24-hour period, with
the raw meat of a fox naturally-infected with T. britovi. Each piglet received a dose of
approximately 75, 750 or 7,500 larvae, respectively; one piglet was used as an
uninoculated control. T h e animals w e r e e u t h a n i s e d on day 50 post-infection and
examined for Trichinella larvae, as indicated above, in 10 g samples of tongue, masseter,
a b d o m i n a l muscle and d i a p h r a g m . B l o o d sera withdrawn on days 0 and 50 post­
infection were tested for specific antibodies by immunofluorescence (23).
TABLE I
Geographic origin of wild boars, mustelids and foxes sampled for Trichinella spp.
and prevalence of infection in foxes
Province
Total No.
Alessandria
Aosta
Asti
Cuneo
Imperia
La Spezia
Savona
Turin
Vercelli
Total
53
62
235
642
1,567
4,009
1,370
604
152
8,694
Wild
boars
Mustelids
20
8
2
--
-
59
1,484**
3,802
1,324
453
17*
10
5
2
46
-
-
7,142
90
Foxes
No.
No.
examined positive
25
60
235
566
73
202
44
105
152
1,462
1
7
1
5
4
0
0
12
0
30
%
4.0
11.6
0.4
0.9
5.5
0.0
0.0
11.4
0.0
2.1
* one positive badger
one positive wild boar
TABLE II
Eco-geographic
origin of wild boars, mustelids and foxes sampled for Trichinella spp.
and prevalence of infection in foxes
Habitat
Plains
Hills
Pre-Alps/Apennines
Alps
* one positive badger
* one positive wild boar
Total No.
382
1,889
4,859
1,563
Wild
boars
95
1,215
4,440
1,391 *
Mustelids
7
16
25
42**
Foxes
No.
No.
examined positive
280
658
394
130
0
1
.3
26
%
0.0
0.1
0.7
20.0
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Muscle samples (usually d i a p h r a g m and/or tibialis cranialis) from 1,462 foxes,
58 stone m a r t e n s (Martes foina), 15 badgers (Meles meles), 3 pine m a r t e n s (Martes
martes), 4 stoats (Mustela erminea), 5 weasels (Mustela nivalis) and 5 polecats (Mustela
putorius) w e r e examined as above. In an a t t e m p t to explain the differences in
prevalence of infection between mountain and lowland foxes:
- pooled hind-leg tissue from 965 small mammals (Table III) and the diaphragm of
15 Alpine marmots (Marmota marmota), collected close to places where infected foxes
had been shot or found dead, were examined for Trichinella larvae by peptic digestion
(6);
TABLE III
Small mammals examined for Trichinella spp. and their eco-geographic
Origin of samples
Pre-Alpine/
Alpine habitats
Apennine habitats
Species
Apodemus spp.
Clethrionomys glareolus
Microtus nivalis
Mus musculus
Sorex araneus
Sorex minutus
Rattus rattus
Eliomys quercinus
Crocidura russula
Talpa europaea
Rattus norvegicus
Erinaceus europaeus
Sciurus vulgaris
Total
294
262
63
158
23
-
42
3
13
2
2
1
18
Total
452
285
63
42
39
24
13
5
2
3
1
24
12
965
-
36
24
5
1
6
12
703
origin
262
- during winter and early spring, fox carcasses were laid out in one lowland and
three mountain areas, and their consumption by scavengers was observed over four
weeks by means of snow tracks and feeding signs (Table IV).
Biochemical identification was carried out for 27 allozymes (12) on
isolates from eleven foxes and one wild boar.
Trichinella
TABLE IV
Field trials aimed at testing the cannibalistic behaviour of foxes under natural
conditions
Fox carcasses
Trial
Habitat
Month
1
2
3
4
Plains
Mountainous
Mountainous
Mountainous
February
January
February
March
Laid out
Visited by
foxes
Taken away
and/or eaten
16
5
19
5
10
5
4
4
0
5
3
3
1042
RESULTS
Epidemiological significance of wild swine
A wild boar (wounded adult male from the Ligurian Alps) was found to be naturallyinfected with T. britovi (120 larvae per g in diaphragm tissue).
E x p e r i m e n t a l infection was successful in the piglet which had b e e n given
7,500 larvae, but only 0.2 larvae per g were observed in the diaphragm tissue and none in
the other samples. Seroconversion was detected in two of the infected piglets (750 and
7,500 larvae) on day 50 post-infection.
Epidemiological significance of red foxes
Thirty foxes (2.1%) and one badger (an adult female from the Maritime Alps) were
positive; the mean density of larvae in the vulpine diaphragms was 29.7 per g of tissue
(range = 0.5 to 125 larvae per g). No other mammal was positive. The origin of infected
foxes is reported in Tables I and II. Eleven vulpine isolates were identified as belonging
to T. britovi.
Results of field trials with fox carcasses are r e p o r t e d in Table IV. Cannibalistic
behaviour was fairly common in mountain foxes, whereas lowland foxes refrained from
feeding on the carcasses. In the lowland area, the carcasses were laid out for 65 days
without being t a k e n away by any land scavengers; only buzzards and crows were
responsible for some consumption.
DISCUSSION
Nine autochthonous outbreaks of human trichinellosis have been recorded in Italy
since 1961: infected wild boars were the source for five of these (3, 23), while freeranging hogs (7, 28) and foxes (18,23) accounted for only two each. Data showed that
wild boars and free-ranging hogs were not significant reservoirs of T. britovi in the areas
studied. The sample size supports this conclusion, as the number of animals examined
was 20% higher than the average yearly hunting bag for north-west Italy (25). These
results parallel those of other surveys carried out in northern and central Italy, where
n a t u r a l infection of wild b o a r s was either absent (8, 13, 20) or sporadic (21, 27).
F u r t h e r m o r e , results of the experimental infection performed offer a r e a s o n a b l e
explanation for both this situation and the presence of specific antibodies in 7.2% of 803
wild boar sera tested so far in Italy (13, 21, 23). The dose-dependent success of piglet
infection and the minimum infective dose are consistent with similar trials using strains
of fox origin from central Italy (2,16,19).
In the area studied, the red fox is the only host species in which T. britovi is frequent
r a t h e r than sporadic. Significant variability in the prevalence of infection has been
observed between foxes of different eco-geographic origin, with optimum conditions for
the spreading of this parasite existing at relatively high altitudes (above 800-1,000 m). A
similar observation, though not expressly stated, emerges from the analysis of other sets
of epidemiological d a t a (4, 6, 15). T h e authors have considered t h r e e possible
explanations for this, as follows:
1043
a) different levels of predation on other T. britovi reservoirs
b) different opportunities for cannibalism
c) different attitudes towards cannibalism.
H y p o t h e s i s b) can b e eliminated at once; although higher n a t u r a l mortality is
expected in mountain habitats due to harsh environmental conditions, a much higher
"anthropogenic" mortality is actually recorded in the lowlands due to road casualties,
hunting wounds, agricultural poisoning, etc., making fox carcasses m o r e frequently
accessible to conspecifics.
The negative findings in small mammals and Alpine marmots, which are among the
most c o m m o n prey of foxes in the n o r t h - w e s t e r n Alps (11), t e n d to discredit
hypothesis a). The same conclusion arises from previous data on 1,222 small mammals
from mountain areas of northern and central Italy where fox trichinellosis is endemic
(2,5,18).
A s regards hypothesis c), preliminary evidence shows that fox carcasses, though
regularly consumed by mountain foxes, do not represent an attractive food source for
their lowland kin. The abundance of other food resources in lowland areas may account
for this behaviour. On the other hand, it is generally accepted that, in temperate zones,
food quantity is a limiting factor for fox p o p u l a t i o n s living in the most selective
e n v i r o n m e n t s ; much larger " h o m e r a n g e s " and strictly individual b e h a v i o u r in
mountain foxes indirectly confirm this (1).
T h e epidemiological significance of mustelids a p p e a r s negligible, even t h o u g h
sample size was limited in this case. Sporadic infections in a badger (17) and a stone
marten (7) have been reported in the literature in Italy. The lack of infection in highly
efficient mouse-eaters (Martes spp. and Mustela spp.) from areas with endemic fox
trichinellosis may be further evidence against hypothesis a); however, nothing is known
about the infectivity of T. britovi for these hosts.
CONCLUSIONS
The results indicate the dominant and perhaps unique role played by the red fox in
maintaining the sylvatic cycle of T. britovi. If further field trials should confirm the
observations m a d e to date on cannibalism, the eco-ethology of the red fox would
emerge as the key factor in the epidemiology of this parasite. The recent demographic
explosion of wild boar in Italy and the increased consumption of meat from this animal
have drawn the infection risk a little closer to humans without "changing the rules of the
game", which were already perceived thirty years ago (14), when the wild boar was still
rare in the western Alps. Interaction of public health education and wild boar meat
inspection is likely to minimise this risk in Italy. A fitting example is the positive wild
boar r e p o r t e d h e r e , the c o n s u m p t i o n of which would have probably resulted in an
outbreak in the human population.
* *
1044
ÉPIDÉMIOLOGIE D E LA TRICHINELLOSE SYLVATIQUE DANS LE NORDOUEST DE L'ITALIE. - L. Rossi, E. Pozio, W. Mignone, C. Ercolini et V. Dini.
Résumé : Les prélèvements musculaires effectués sur 7 142 sangliers (Sus
scrofa), 80 porcs sauvages, 1 462 renards roux (Vulpes vulpes), 90 mustélidés,
15 marmottes alpines (Marmota marmota), 873 rongeurs et 92 insectivores ont
été examinés en vue d'y rechercher Trichinella Railliet, 1895. Un sanglier, un
blaireau (Meles meles) et trente renards (2,1 %) étaient infectés. Onze souches
isolées chez les renards et la souche trouvée chez le sanglier appartenaient à
l'espèce Trichinella britovi. Ces résultats indiquent que le sanglier n'est pas un
réservoir important de T. britovi dans la région étudiée. Une souche isolée chez
les renards a révélé un faible pouvoir infestant chez des porcs inoculés
expérimentalement.
La prévalence de la trichinellose dans la population
vulpine est plus élevée en montagne qu'en plaine. Les chiffres reflètent le rôle
clé joué par ce carnivore dans l'épidémiologie des infections à T. britovi. Les
résultats préliminaires de quatre essais sur le terrain semblent montrer qu'il
n'existe pas le même type de cannibalisme chez les renards selon qu'ils vivent en
montagne ou en plaine.
MOTS-CLÉS : Cannibalisme - Italie - Renard roux - Sanglier - Trichinella
britovi.
*
EPIDEMIOLOGÍA DE LA TRIQUINELOSIS SELVÁTICA EN EL NOROESTE DE
ITALIA. - L. Rossi, E. Pozio, W. Mignone, C. Ercolini y V. Dini.
Resumen: Se sometieron a examen para la detección de Trichinella Railliet,
1895, muestras musculares procedentes de 7.142 jabalíes (Sus scrofa), 80 cerdos
salvajes, 1.462 zorros rojos (Vulpes vulpes), 90 mustélidos, 15 marmotas
alpinas (Marmota marmota), 873 roedores y 92 insectívoros.
Resultaron
infectados un jabalí, un tejón (Meles meles) y 30 zorros (2,1%). Once de las
cepas aisladas en los zorros así como la cepa aislada en el jabalí pertenecían a la
especie Trichinella britovi. Estos resultados demuestran que el jabalí no es un
reservorio importante de T. britovi en la zona estudiada. Una cepa aislada en
los zorros dio muestras de escasa infectividad en cerdos
inoculados
experimentalmente. La prevalencia de la triquinelosis en la población vulpina
es más alta en la montaña que en la llanura y revela el papel determinante que
desempeña este carnívoro en la epidemiología de las infecciones por T. britovi.
Los resultados preliminares de cuatro ensayos de terreno parecen demostrar
que existen diferencias de canibalismo entre los zorros de montaña y los zorros
de llanura.
PALABRAS CLAVE: Canibalismo - Italia - Jabalí - Trichinella britovi Zorro rojo.
1045
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