Trichinella in Italy and in the European Union

Edoardo Pozio European Union Reference Laboratory for Parasites Istituto Superiore di Sanità Rome, Italy The genus in Europe

• At present, 12 taxa are recognized in the genus Trichinella worldwide • Of them, 4 species are circulating in Europe – T. spiralis – T. nativa – T. britovi – T. pseudospiralis The Trichinella genus in Europe

• At present, 12 taxa are recognized in the genus Trichinella worldwide • Of them, 4 species are circulating in Europe – T. spiralis – T. nativa – T. britovi – T. pseudospiralis Europeran Trichinella species and their hosts

• T. spiralis • T. nativa • T. britovi • T. pseudospiralis Trichinella spp. circulating in the EU and their hosts

Trichinella spp. Tested isolates Carnivores Suidae Other hosts

T. britovi 1,741 (48.3%) 64% 35.4% 0.6% (horses, rodents)

T. spiralis 1,699 (47.1%) 8.6% 87.9% 3.5% (horses, rodents)

T. nativa 124 (3.4%) 98.5% 1.5% never detected

T. pseudospiralis 43 (1.2%) 20.9% 69.7% 9.3% (rodents, birds)

Total 3,607 38.5% 59.5% 2.0% Trichinella sp. epidemiology

Sylvatic cycle Domestic cycle The sylvatic cycle- 1

• Wild susceptible to Trichinella infection (carnivores and omnivores) are the Trichinella reservoirs • The Trichinella biomass is higher in wild than in domestic animals • The poor management of wild and domestic animals favours the Trichinella sp. transmission from the wild to the domestic habitat and viceversa

Trichinella larvae survive for long period in carcasses

• Trichinella larvae of some species can survive for months up to several years in frozen muscles – The survival time is higher between 0°C and -18°C • Encapsulated larvae of Trichinella survive for months in decaying flesh of their hosts: – High humidity – Low temperature • Larvae can survive in the collagen capsule even when the muscle tissues are completely liquefied The subnivium

• The habitat “below snow” provides environmental stability linked to snow duration, density, and depth

Minimum daily temperatures The subnivium climate is characterized - under deep snow (black line) by a stable temperature near freezing - shallow snow (dashed line) because heat released from the soil is - ambient temperature (grey line) trapped by the low thermal conductivity of snow Rearing practices involved in transmission of Trichinella spp. to domestic pigs - 1

• Feed on wild animal carcasses • Hunters who leave animal carcasses in the field after skinning, or remove and discard the entrails, or dispose of in dumps • Hunters who feed pigs with animal carcasses • Road-killed wild animals • Introduction of new pigs on a farm without any information on the farm of origin and previous farming conditions Rearing practices involved in transmission of Trichinella spp. to domestic pigs - 2 • Cannibalism due to a high mortality rate • Feed on garbage containing or wild animal scraps • Feed on pork scraps from pigs slaughtered at the farm • Feed on carcasses or scraps from farmed fur animals • Feed on rats, which can play the role of Trichinella spp. ‘vector’ from one farm to another • Feed origin and correct daily feed intake not always controlled Pigs at risk for Trichinella transmission Trichinella sp. in domestic pigs and wildlife Trichinellosis in humans in the EU 1986-2009

Country Period N. of cases Average incidence x 100.000 inhabitants Bulgaria 1990-06 4108 2.4. 2.9 Czech Rep. 1986-09 31 0.01 *most from Estonia 1986-09 91 0.0-2.9 imported France 1986-89 1261* 0.005-0.006 horse meat Germany 1986-09 185 0.005 Greece 2009 1 0.008 Hungary 1986-09 158 0.18-0.027 Ireland 2007 2** 0.04 Italy 1986-09 1181* 0.0-0.9 ** from Latvia 1986-09 636 0.07-0.38 imported pork Lithuania 1990-04 3979 0.4–21.8 Poland 1986-07 3084 0.05-1.5 Romania 1986-07 28564 1.7-16.1 Slovakia 1986-08 440 0.0-6.2 Slovenia 1989-06 203 0.00-10.5 Spain 1986-09 1684 0.0-0.4 UK 1999 7** 0.01 TOTAL 45.615 Trichinellosis in humans in the EU 2010-2015

Country N. of cases Average incidence x 100.000 inhabitants Austria 6 (imported) 0.07 Belgium 18 (imported meat) 0.14 Bulgaria 234 2.9 Croatia 6 0.07 Estonia 3 0.07 Finland 1 (imported) Germany 31 0.02 Greece 4 0.03 Italy 80 0.07 Latvia 150 7.3 Lithuania 219 6.2 Poland 93 0.17 Romania 1083 (2 deaths) 4.97 Spain 69 (1 death) 0.14 Sweden 2 (imported) 0.01 TOTAL EU 2,005 0.07 0.7 cases per million inhabitants mortality rate 0.15% Trichinella spp. in Italy

• From 1985 to 2016, 354 Trichinella sp. isolates from animals (both domestic and wild) living in Italy, have been identified at the species level: • 342 T. britovi (97.5%) – 4 cats, 5 dogs, 5 brown rats, 1 black rat, 163 red foxes, 106 wolves, 1 brown bear, 30 wild boars, 18 pigs, 8 stone martens, and 2 badgers; • 8 T. pseudospiralis (2.2%) – 1 tawny owl, 1 little owl, 1 red fox, and 5 wild boars; • 2 T. spiralis (0.3%) (1991, 2016) – red foxes Foci of Trichinella species in Italy

T. pseudospiralis T. spiralis T. britovi T. britovi +++

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+ 500 m asl

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200 m asl Indirect versus direct detection methods of Trichinella spp. infection in

Tested wild boar: 1,462

Seroprevalence of 2.2% in muscle juices (95% C.I 1.55-3.07; 32/1,462)

Prevalence by digestion: 0.07% (95%C.I. 0.01-0.39; 1/1,462) Trichinella britovi larvae

From 2006 to 2012, a prevalence of 0.017% was detected by muscle digestion in wild boar hunted in the whole Italian territory Hunting dogs as sentinel animals for monitoring infections with Trichinella spp. in wildlife

Out of 384 tested hunting dogs, 56 tested positive by serology. All positive dogs hunt in mountain areas Trichinellosis outbreaks in Italy from 1948 to 2016

Source of infection free Source of infection hunted Source of infection ranging or backyard pigs wild boar ( ), foxes ( ) imported horse meat Trichinellosis in Italy from 1948 to 2015 by source Source No. of No. of infected foci persons (%) Domestic swine 13 180 (11.9) Hunted wild boar 11 288 (19.0)

Hunted foxes 2 11 (0.7)

Imported horses 7 1038 (68.4) Total 33 1517 1000 Horse Pig Wild boar 100

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1 1975 1977 1979 1981 1983 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 2005 2007 2009 2011 2013 2015 Conclusions

• of the genus Trichinella are parasites of wild animals • These parasites are transmitted from wildlife to domestic animals when humans do not properly manage – game offal and scraps – backyard and free-ranging pigs – fur animals – horses • Pigs reared under controlled housing conditions are exempted from these parasites • Public health and veterinary services should invest funds into the education of consumers, farmers, and hunters Thank you for your attention