Table 1 Prevalence values (%) of extraintestinal helminths found with necroscopic examination of red foxes (Vulpes vulpes) in Italy (2013-1983)
Reference This
study
Ferrantelli et al. 2010
Magi et al.
2009a
Ferroglio et al.
2008
Manfredi et al.
2003
Stancampiano et al. 1998
Marconcini et al. 1996
Poli and Biraghi
1994
Guberti and Poglayen
1991
Iori et al. 1990 Cancrini 1986
Leoni et al.
1986
Polidori et al.
1985
Poli et al.
1984 Rossi et al.
1983
Region of study LIG SIC TUS PIEM TREN VEN TUS TUS EM R LOM VEN TREN LAZ LAZ SAR SAR TUS PIEM
N of examined foxes 165 55 129 608 42 98 523 355 153 93 28 29 182 182 85 35 180 33
Cardiopulmonary nematodes Angiostrongylus vasorum
78.2 7 0.0 18.5 0.0 6.3 0.0 15.3 23.8 0.0
Eucoleus aerophilus 41.8 7 14.6 28.0 0.0 3.6 10.7 0.0 1.2 51.5
Eucoleus boehmi posa -- 0.0 0.0
Crenosoma vulpis 15.8 14.7 17.3 25.6 0.0 20.7 13.1 0.0 0.0 9
Filaroides spp. 4.8 0.0 0.0 0.0 0.0 0.0 0.0
Filarial nematodes
Dirofilaria immitis 0.0 6.2 0.0 0.0 9.6a 8.3 0.0 0.0 0.0 0.0 0.0 0.0 1.2 0.0
Dirofilaria repens 0.0 0.7 1.1 0.0 0.0 0.0 0.0 0.0 0.0
Acanthocheilonema reconditum
0.0 9.3 10.9 38.5 0.0 0.0 0.0 0.0 0.0 0.0
Acanthocheilonema dracunculoides
0.0 2.3 18.9 0.0 0.0 0.0 3.8 10.4 0.0
Gastric nematodes
Spirocerca lupi 23.5 9.2 0.0 0.0 0.0 0.0 68.2 80 0.0
Physaloptera spp. 2.5 2.6 0.0 0.0 0.0 0.0 0.0
Aonchothecha putorii
8.6
Spirura rytipleures 0.0 0.5
Olullanus trichuspis 0.0 0.5
Cyathospirura sp. 0.0 0.49
Urinary tract nematodes
Pearsonema plica 56.8 21.4 27.6 14.0 45.4
Liver nematodes
Opistorchis felineus 0.0 0.5
a 9.6% positivity for adults in the heart, 0.4% positivity for microfilariae. EM R: Emilia Romagna; LAZ: Latium; LIG: Liguria; LOM: Lombardy; PIEM: Piedmont; SAR: Sardinia; SIC: Sicily; TREN:
Trentino Alto Adige; TUS: Tuscany; VEN: Veneto.
Table 2 Prevalence values (%) of extraintestinal helminths of red foxes (Vulpes vulpes) in Europe according to comparable surveys (2013-1993)
Reference This
study
Lalosevic et al.
2013
Bružinskaitė et al. 2011
Gerrikagoitia et al., 2010
Morgan
et al.
2008
Martinez- Carrasco et al. 2007
Davidson et al.
2006 Eira et al.
2006 Saeed
et al.
2006
Manas et al.
2005
Segovia et al.
2004
Sréter et al.
2003
Shimalov and Shimalov
2002
Gortázar et al.
1998
Lassnig et al.
1998
Simpson et al.
1996
Wolff and Bucklar
1995
Steinbach et al. 1994
Gortázar et al.
1994
Country IT SRB LTU ES GB ES NORW PT DK ES ES HUNG BYEL ES AUST GB CH
LIEC
DE ES
N° of foxes 165 70 104 48 546 55 181 62 1040 251 399 100 94 161 516 12 405 400 433
Cardiorespiratory nematodes Angiostrongylus vasorum
78.2 33.3 7.3 1.8 0.0 16.1 48.6b 22.7 17.5 5.0 0.0 20.7 0.0 41.6 0.0
Eucoleus aerophilus 41.8 84.3 97.1 39.0 5.4 88.3 4.8 74.1 58.9 48.1 64.0 9.6 34.8 43.9 77.8
Eucoleus boehmi Pos 90 a 50.6 8.0
Crenosoma vulpis 15.8 53.8 2.0 0.0 58.0 3.2 17.4 33.9 20.3 24.0 5.3 2.5 24.9 4.2
Filaroides spp. 4.8 Filarial nematodes
Dirofilaria immitis 0.0 0.0 0.0 0.0 3.2 0.0 0.4 0.2 0.0 0.0 12.7 11
Dirofilaria repens 0.0 0.0
Acanthocheilonema reconditum
0.0 0.0
Acanthocheilonema dracunculoides
0.0 0.0
Gastric nematodes
Spirocerca lupi 23.5 0.0 12.9 7.0 2.1 2.5
Physaloptera spp. 2.5 0.0 0.0 11.5 0.0 0.0
Aonchotheca putorii 8.6 Vigisospirura
potekhinae
0.2
Mastophorus muris 1.5 1.5
Ollullanus trichuspis 2.1
Urinary tract nematodes
Pearsonema plica 56.8 93.3 52.6 1.6 80.5 40.3 52.0 21.3 27.3 35.6 59.0 98.3
Liver nematodes Pseudamphistomum truncatum
3.2 2.2 2.1
Metorchis sp. 0.5 3.2 13.2
Opistorchis felineus 2.9 0.2 3.2
aout of 10 foxes examined; bonly from the endemic area of New Zealand with 436 foxes examined. AUST: Austria; BYEL: Byelorussia; CH: Switzerland; DE: Germany; DK: Denmark; ES: Spain; GB:
Great Britain; HUNG: Hungary; IT:Italy; LIECH: Liechtenstein; NORW: Norway; PT: Portugal.
Table 3 Prevalence values (%) of intestinal helminths of red foxes (Vulpes vulpes) in Italy according to comparable surveys (2013-1983) (part 1)
Reference This
study
Magi et al.
2009a
Di Cerbo et al.
2008
Di Cerbo et al.
2008
Manfredi et al. 2005
Manfredi et al.
2003
Capelli et al. 2003 Stancampiano et al. 1998
Poli and Biraghi
1994
Guberti and Poglayen
1991
Iori et al. 1990 Leoni et al. 1986
Poglayen et al.
1985
Rossi et al. 1983
Region of study area LIG TUS AO, LOM, TREN,
VEN
TREN, VEN
TREN, VEN, AO, LOM,
LIG
TREN VEN TUS EM R
VEN TUS EM R LOM VEN TREN LAZ SAR EM R PIEM
N° of foxes 165 129 645 260 1446 42 89 100 109 98 335 153 93 28 29 182 85 103 33
Nematodes Uncinaria stenocephala
68.5 39.1 51.3 52.3 Pos 51.2 74 41 11 72.9 75.8 11.8 63.4 28.6 48.3 43.4 91.7 14.6 81.8
Ancylostoma caninum 0.0 2 3.9 12.1
Toxocara canis 24.3 9.1 54.4 48.5 Pos 56.1 66 32 70 56.1 13.6 46.4 54.8 46.4 48.3 31.9 3.5 45.6 45.4
Toxascaris leonina 26.7 5.4 1 1.6
Trichuris vulpis 20.6 0.2 0.4 Pos 12.2 9 1 4 9.0 3.3 28.6 48.3 5.9 2.9 18.1
Molineus legerae 24.2 2.9 5.8 Pos 9.8
Molineus patens Pterygodermatites affinis
4.8 19.4 24.2 Pos 17.1 8 0 0 7.3 21.5 17.8 6.9
Aonchotecha putorii 8.5 17.1 3.4 1.1
Capillaria sp. 0.3 0.4 Pos 2.7 12.1
Oxynema crassispiculum
0.2 0.4 Pos
Cestodes 48.5 53.1
Echinococcus multilocularis
0.0 0.8b Posb
Echinococcus granulosus
0.0 1.18
Taenia sp. 5.5 24.2 19.1 17.0 6.8
Taenia crassiceps 28.9 Pos 9 0 9 9.2 2.0 3.2 37.9 2.9 30.3
Taenia hydatigena 0.3 Pos 3.3 12.6
Taenia polyacantha 24.4 20 0 0 20.9 11.8 3.6 27.6 1.6 3.0
Taenia taeniaeformis 3.4 Pos
Taenia pisiformis 8.6 3.6 45.5
AO: Aosta Valley; EM R: Emilia Romagna; LAZ: Latium; LIG: Liguria; LOM: Lombardy; PIEM: Piedmont; SAR: Sardinia; SIC: Sicily; TREN: Trentino Alto Adige; TUS: Tuscany; VEN: Veneto.
Table 3 Prevalence values (%) of intestinal helminths of red foxes (Vulpes vulpes) in Italy according to comparable surveys (2013-1983) (part 2)
Reference This
study
Magi et al.
2009a
Di Cerbo et al.
2008
Di Cerbo et al.
2008
Manfredi et al. 2005
Manfredi et al.
2003
Capelli et al. 2003 Stancampiano et al. 1998
Poli and Biraghi
1994
Guberti and Poglayen
1991
Iori et al. 1990 Leoni et al. 1986
Poglayen et al.
1985
Rossi et al. 1983
Region of study area LIG TUS AO, LOM, TREN,
VEN
TREN, VEN
TREN, VEN, AO, LOM,
LIG
TREN VEN TUS EM R
VEN TUS EM R LOM VEN TREN LAZ SAR EM R PIEM
N° of foxes 165 129 645 260 1446 42 89 100 109 98 335 153 93 28 29 182 85 103 33
Cestodes 48.5 53.1
Mesocestoides spp. 82.4 45.4 Pos 4.9 0 37 1 60 9.7
Mesocestoides lineatus 27.4 27.7 11.1
Mesocestiodes litteratus
21.5 7.1 10.3 14.3
Dilepididae 27.3 57.3 0 4 3 2.6 2.9
Joyeuxiella echinorhynchoides
15.9
Joyeuxiella spp. 48.2
Diplopylidium spp. 2.4
Spirometra erinacei europei
0 0 10
Trematodes 1.4a 0.7
Alaria alata Ascocotyle longa Pseudamphistomum truncatum
Pharingostomum cordatum
Pos Pos 2.4
Metorchis vulpis Pos 0.8 Pos
Plagiorchis elegans Pos 0.8 Pos
AO: Aosta Valley; EM R: Emilia Romagna; LAZ: Latium; LIG: Liguria; LOM: Lombardy; PIEM: Piedmont; SAR: Sardinia; SIC: Sicily; TREN: Trentino Alto Adige; TUS: Tuscany; VEN: Veneto.
Table 4 Prevalence values (%) of intestinal helminths of red foxes (Vulpes vulpes) in Europe according to comparable surveys (2013-1993) (part 1)
Reference This
study
Bružinskaitė et al. 2011
Sikó et al.
2010 Borecka
et al.
2009
Martinez- Carrasco et al.
2007 Eira et al.
2006 Saeed
et al.
2006 Letková
et al.
2006
Vervaeke et al.
2005
Segovia et al.
2004 Smith
et al.
2003 Shimalov
and Shimalov
2002
Rajković- Janje et al. 2002
Wolfe et al.
2001 Luty et al.
2001 Hofer et al.
2000 Gortazar
et al.
1998 Lassnig
et al.
1998
Papadopoulos et al. 1997
Pavlovic et al.
1997 Pfeiffer
et al.
1997 a,b
Willingham et al.1996
Richards et al.
1995
Steinbach et al.1994**
Wessbecher et al. 1994
Country IT LTU ROM PL ES PT DK SVK BE ES GB BYEL HVR IE PL CH ES AUST EL SRB DE DK GB DE DE
N° of foxes examined
165 269 561 639 55 62 1040 302 219 399 588 94 85 77 92 388 81 516 314 532 1300 21 843 400 801
Nematodes Uncinaria stenocephala
68.5 76.9 15.0 35.8 1.8 77.4 68.6 2.0 31.5 71.2 41.3 40.4 25.9 92.2 66.8 30.9 43.0 43.9 40 15.9 85.7 67.9 24.3
Ancylostoma caninum
18.2 0.6 5.6 0.5 3.2 5.1 6 81.0 1.1
Toxocara canis 24.8 40.5 29.4 19.1 45.5 37.1 59.4 25.8 47.9
29.3 61.6 25.5 28.2 37.7 16.3 47.4 6.2 46.8 28.6 50 26.5 55.9 56.6 30.2
Toxascaris leonina 26.7 4.6 5.4 0.6 17.5 19.3 0.3 18.1 66.7 0.6 2.5 10.5 1.5 4.5 2.0
Toxocara cati 1.8 0.2 3.2
Trichuris vulpis 20.6 27.2 9.1 8.1 0.5 6.9 8.3 0.3 3.2 12.3 0.2 8 0.47
Molineus legerae 24.2 2.0
Molineus patens 4.8 2.3 3.2
Pterygodermatites affinis
4.8 54.4 3.2 22.3 23.4
Aonchotheca putorii
8.5 29.4 1.2 5.3
Fam. Spiruridae 3.90
Rictularia sp. 6.4 17.5
Strongyloides vulpis
2.1
Trichostrongylus sp.
0.6
Oxynema crassispiculum
5.4
Cestodes Echinococcus multilocularis
58.7 4.8 13.9 0.3 10.6 1.8 7.5 44.3 3.6 0.3 -- 11.5
Echinococcus granulosus
0.2 0.1
Taenia spp. 5.5 29.7 21.5 20.9 2.7 2.3 20.7 24.7 0.09 8.4 17.4 1.6 9.2 38.1
Taenia taeniformis
3.7 2.6 1.6 1.0 0.2 3.2 0.2 0.7
Taenia pisiformis 12.0 7.3 3.2 0.3 6.3 2.0 12.8 4.9 0.2 22 0.1 13.8
Taenia polyacantha
61.7 5.3 10.3 17.0 0.5 3.7 6.8 16 11.9 7.0
Taenia hydatigena 8.2 0.4 2.0 5.3 0.9 2 2.5
Taenia multiceps 4.6 1.2
Taenia serialis 0.9 0.1
Taenia crassiceps 26.4 5.0 0.2 4.3 27.7 7.6 14.6 0.3 51 17.7 19.9
Taenia ovis 3.7
AUST: Austria; BE: Belgium; BYEL: Byelorussia; CH: Switzerland; DE: Germany; DK: Denmark; EL: Greece; ES: Spain; GB: Great Britain; HUNG: Hungary; HVR: Croatia; IE: Ireland; IT: Italy; LTU:
Lithuania; NORW: Norway; PL: Poland; PT: Portugal; ROM: Romania; SRB: Serbia; SVK: Slovakia.
Table 4 Prevalence values (%) of intestinal helminths of red foxes (Vulpes vulpes) in Europe according to comparable surveys (2013-1993) (part 2)
Reference This
study
Bružinskaitė et al. 2011
Sikó et al.
2010 Borecka
et al.
2009
Martinez- Carrasco et al.
2007 Eira et al.
2006 Saeed et al.
2006 Letková
et al.
2006
Vervaeke et al.
2005 Segovia
et al.
2004 Smith et al.
2003 Shimalov
and Shimalov
2002
Rajković- Janje et al. 2002
Wolfe et al.
2001 Luty et al.
2001 Hofer et al.
2000 Gortazar
et al.
1998 Lassnig
et al.
1998
Papadopoulos et al. 1997
Pavlovic et al.
1997 Pfeiffer
et al.
1997 a,b
Willingham et al.1996
Richards et al.
1995
Steinbach et al.1994**
Wessbecher et al. 1994
Country IT LTU ROM PL ES PT DK SVK BE ES GB BYEL HVR IE PL CH ES AUST EL SRB DE DK GB DE DE
N° of foxes examined 165 269 561 639 55 62 1040 302 219 399 588 94 85 77 92 388 81 516 314 532 1300 21 843 400 801
Cestodes
Mesocestoides sp. 82.4 78.4 71.2 30.6 35.6 61.2 28.8 4.4 71.6 15.8 73.2 54.1
Mesocestoides lineatus
28.7 56.4 13.8 62 23.8
Mesocestoides litteratus
5.4
Fam. Dilepididae 27.3 0.5
Dipylidium caninum 14.7 1.8 2.0 0.9 0.7 4.3 1.2 3.2 3.8 0.5
Joyeuxiella pasqualei 34.6 2.8 1.2
Joyeuxiella echinorhynchoides
6.0 24.5
Hymenolepis sp. 0.1
Diplopylidium noelleri 0.2
Diphyllobothrium latum
Spirometra spp. 3.2 0.3
Trematodes 0.9
Alaria alata 94.8 15.0 56.7 27.4 15.4 2.0 42.6 4.7 27.3 2.1 1.6 65
Apophallus donicum 1.1
Ascocotyle longa 24.2
Brachylaima spp. 1.5 2.8
Cryptocotyle lingua 23.8 2.2
Echinochasmus perfoliatus
1.3 1.1
Isthmiophora melis 17.0
Echinostomatidae 1.5 0.9
Acantocephalans Macracanthorhynchus catulinus
27.6 1.6 1.0 3.2 7.4 0.1
Centrorhynchus sp. 1.6
Polymorphus sp. 1.2 9.5
Oncicola canis 0.3
Pachysentis sp. 14.6
Prosthorhynchus transversus
0.7
AUST: Austria; BE: Belgium; BYEL: Byelorussia; CH: Switzerland; DE: Germany; DK: Denmark; EL: Greece; ES: Spain; GB: Great Britain; HUNG: Hungary; HVR: Croatia; IE: Ireland; IT: Italy; LTU:
Lithuania; NORW: Norway; PL: Poland; PT: Portugal; ROM: Romania; SRB: Serbia; SVK: Slovakia.
NB: Comparing the prevalence of helminths of red foxes reported in European (and Italian) surveys (Table s 3 and 4) should be done with caution, since techniques used to recover intestinal helminths may have a significant influence on prevalence estimates (Vervaeke et al. 2005). The intestinal sedimentation and counting technique (SCT), and the intestinal scraping technique (IST) are considered to be the most reliable techniques (Eckert et al.
2001), while the faecal flotation technique is known to severely underestimate the prevalence of gastrointestinal helminths in carnivores (Lalosević et al. 2013; Wolfe et al. 2001; Hofer et al. 2000; Eckert et al. 2001; Rodriguez and Carbonell 1998). Thus only data from surveys conducted with SCT or IST were included in the Tables. Furthermore, not to overestimate the presence of some species, only works which investigated the whole intestinal helminth-fauna were included, whereas studies dedicated to specific species are discussed in relation to the single species in the discussion.
Table 5 Recent (2013-2000) surveys on filarial infections in dogs in Italy
Year References Techniques Study area Dogs (n) Dirofilaria
immitis
Dirofilaria repens
Acanthocheilonema reconditum
2013 This study Kn+HS+Ag+PCR Liguria (Imperia and Savona) 365 0.5% 1.4% 7.9%
2012 Rinaldi et al. 2012 Kn Campania 415 1.7% 1.9%
2012 Giangaspero et al. 2012 Apulia (Foggia) 308 3.6% 1.9%
2012 Solinas et al. 2012 Kn Sardinia (all provinces) 591 8.3% 8.3% 14%
2012 Brianti et al. 2012 Kn Sicily (Messina) 152 -- -- 11.2-13.3%
2011 Magi et al. 2012b Kn+HS+Ag Tuscany (all provinces) 630 12.5% 12.1% 1.9%
2010 Traversa et al. 2010b Kn+Ag+PCR Abruzzo 300 2.3% 5.6% 0
2008 Mortarino et al. 2008
Kn+Ag
Tuscany (Arezzo) 11 27% 0 0
Umbria (Perugia) 272 6% 4% 0
2008 Otranto et al. 2008 Kn+Ag Puglia and Calabria 1447 1.2% 0.1% 0
2008 Paoletti et al. 2008 Kn+PCR Abruzzo 504 0.2% 1.4% --
2007 Giannetto et al. 2007 Kn Sicily (all provinces) 2512 1% 5% 5%
2007 Genchi et al. 2007 Kn+Ag Lombardy (Milan 301 32.9% 12.6% 0
2007 Di Tommaso and Di Giulio 2007 necropsy Abruzzo (Pescara) C.rep. 2 0 0
2005 Scaramozzino et al. 2005 Kn+PCR Lazio (all provinces) 972 0 2% 0
2004 Scala et al. 2004 Kn Sardinia (all provinces) 974 3.8% 2.6% 7.4%
2003 Piergili Fioretti et al. 2003 Kn+Ag Umbria (all provinces) 2406 14% 6% 0
2003 Tarello 2003 Kn+Ag Aosta Valley C. rep. -- 5 --
2001 Cringoli et al. 2001 Kn+HS Campania (Mt. Vesuvius) 351 0.6% 2% 16.5%
2001 Petruschke et al. 2001 Kn+Ag Lombardy (Varese, Como) 308 14.6% 5.5% 0
n = number of sampled dogs; C.rep.=case report; Techniques: Kn= Knott’s method, HS = histochemical staining; Ag = ELISA for D. immitis’ antigens