Toxocara sp. that parasitizes dogs and cats poses a threat to public health because it can cause human disease in types such as visceral toxocariasis, neuro-toxocariasis, ocular toxocariasis and latent toxocariasis (Ursache et al., 2021). The protozoa Cryptosporidium spp. and Giardia duodenalis parasitize in the gastrointestinal tract of humans and other vertebrates (Li et al., 1019). Among the approximately 40 Cryptosporidium species, C. hominis, C. parvum, C. meleagridis, C. canis, and C. felis are the most common in humans (Feng et al., 2018; de Oliveira et al., 2021). So, the potential role of domestic animals as a source of human infection with Giardia spp. is the most debated topic (Bouzid et al., 2015; Mircean et al., 2012; Mravcova et al., 2019; Thompson & Monis, 2004; Thompson et al., 2008). It has been confirmed that genotypes A and B affect many animal species and humans, while genotypes C and D are found in dogs and F in cats and are considered species-specific (Feng and Xiao, 2011; Uiterwijk et al., 2020; Jothikumar et al., 2021). According to the Companion Animal Parasite Council (CAPC), immunocompromised people should limit their exposure to Giardia-infected pets (CAPC guideline, 2019). S. stercoralis is an endemic parasite in tropical and subtropical regions, but recently there have been more confirmed reports of such infections in central and northern Europe, where humans and dogs became infected (Basso et al. 2019; Bourgoin et al. 2018; Cervone et al. 2016; Eydal & Skirnisson 2016; Liberato et al. 2022; Jaleta et al. 2017; Raicevic et al. 2021; Unterkofler et al., 2022). Recently, the scientific community has been interested in determining the role of helminth canine hosts (i.e., S. stercoralis) in the transmission of this infection to humans (Paradies et al., 2017). Data on the epidemiology of canine strongyloidiasis are also limited at this time. Most likely due to the limitations in current diagnostic methods (Paradies et al., 2017).
Humans are infected with zoonotic parasites by consuming contaminated food and water or by direct fecal-oral infection from infected animals (Luis Enrique et al., 2018; Li et al., 1019; Silva et al., 2020). The occurrence of prolonged Giardia invasions or disseminated S. stercoralis or Cryptosporidium spp. infections are likely possible in immunocompromised individuals (Unterkofler et al., 2022; Paradies et al., 2017).
Our work aimed to examine the current situation regarding the prevalence of potentially zoonotic intestinal parasites: Cryptosporidium spp. and Giardia sp., S. stercoralis, and Toxocara sp. in domestic dogs and cats in urban environments, and to establish the frequency of coinfections.
Materials and Methods
Two thousand two hundred eight dogs’ fecal samples were examined in 2018 – 2021. Sampling included 950 animals aged 1 to 12 months and 1258 over 12 months. Meanwhile, one thousand three hundred fifty cats’ fecal samples were examined, where 531 were under the age of 12 months, and 819 were over 12 months of age. The information about the age and likelihood of the animals visiting the outdoor environment was obtained from the animal owners. All examined dogs were kept in apartments and had daily outdoor exposure. Cats were kept solely indoors. In the case of S. stercoralis larvae detection, anamnesis regarding the state of the animal and the defecation type was collected from the pet owners. Finally, all data from the owners were processed after receiving their written or verbal consent.
Collected fecal samples were submitted to the «Pasteur» laboratory in Moscow for endoparasite testing. Samples were sent to the laboratory diagnosis when infection symptoms were present or during the therapy outcome control or routine monitoring. The fecal flotation method using a zinc sulfate solution with a density of 1.24, as described by Zajac A (2012), for detecting intestinal parasites was performed. For larvae detection, direct feces smear microscopy was performed. The microscopy was performed with a Lomo microscope at 100X and 400X magnifications (Joint-stock company Lomo, Russia).
Ethical Approval and Informed Consent
The study protocol was reviewed and approved by the scientific and methodological commission of VNIIP - a branch of the Federal State Budget Scientific Institution “Federal Scientific Center VIEV” (Protocol No. 1 dated January 19, 2018). The procedures used in this study are in line with the principles of the Declaration of Helsinki and the European Convention for the Protection of vertebrate animals used for experimental and other scientific purposes.
Written informed consent was obtained from the owners for the participation of their animals in this study.
Statistics
Data analysis was performed using the statistical package SPSS version 26.0. We assessed the statistical significance of observed differences in the degree of infestation in animals of two age groups using the Chi-square criterion, with a threshold set at 0.05 (p-value).
Results
The results showed that Giardia spp. cysts (Fig. 3) were detected the most frequently (Table 1). The overall prevalence was 10.24 %, with a width of 18.2 % in dogs under 12 months. The infection rates with other parasites were as follows: Cryptosporidium spp. - 5.79 %, T. canis - 3 %, larvae of S. stercoralis (Fig.2) - 2.3 %. The infestation rates in dogs older than 12 months were like this: Giardia spp. - 4.21 %, Cryptosporidium spp. - 0.4 %, T. canis - 1.27 %, and S. stercoralis larvae - 0.24 %. Animals under 12 months of age were infected more than those over 12 months of age (p<0.001).
Prevalence of Cryptosporidium spp., Giardia spp., S. stercoralis and T.canis in dogs.
Type of Infection
2018
2019
2020
2021
2018 – 2021
Dogs (≤ 12) total
104
144
303
399
950
Giardia spp.
N
24
30
55
64
173
%
23.08
20.83
18.15
16.04
18.21
Cryptosporidium spp.
N
5
19
13
18
55
%
4.81
13.19
4.29
4.51
5.79
T. canis
N
4
5
14
6
29
%
3.85
3.47
4.62
1.50
3.05
S. stercoralis
N
3
3
7
9
22
%
2.88
2.08
2.31
2.26
2.32
Dogs (> 12) total
215
285
324
434
1258
Giardia spp.
N
14
12
11
16
53
%
6.51
4.21
3.40
3.69
4.21
Cryptosporidium spp.
N
0
1
2
2
5
%
0.00
0.35
0.62
0.46
0.40
T. canis
N
3
6
3
4
16
%
1.40
2.11
0.93
0.92
1.27
S. stercoralis
N
1
1
1
0
3
%
0.47
0.35
0.31
0.00
0.24
Dogs total
319
429
627
833
2208
Giardia spp.
N
38
42
66
80
226
%
11.91
9.79
10.53
9.60
10.24
Cryptosporidium spp.
N
5
20
15
20
60
%
1.57
4.66
2.39
2.40
2.72
T.canis
N
7
11
17
10
45
%
2.19
2.56
2.71
1.20
2.04
S. stercoralis
N
4
4
8
9
25
%
1.25
0.93
1.28
1.08
1.13
The infection rates in cats were found in this manner (Table 2). Giardia spp. - 8.2 %, Cryptosporidium spp. - 8.6 %, T. cati (Fig.1) - 7.5 %. Cats older than 12 months showed the following prevalences: Giardia spp. - 3.3 %, Cryptosporidium spp. (Fig.4) - 2.3 %, T. cati - 2.3 %. The study revealed that in cats under one year of age, Cryptosporidium spp. and Giardia spp. were detected at the same level; meanwhile, the T. cati eggs were present to a lesser extent. In cats under 12 months of age (p < 0.001), the prevalence was higher when compared with older than 12 months cats.
Fig.1.
Toxocara cati eggs
Fig.2.
Larva of Strongyloides sp. in dog, stage L1.
Fig.3.
Cysts of Giardia spp.
Fig.4.
Oocysts of Cryptosporidium sp. in cat.
Prevalence of Cryptosporidium spp., Giardia spp. and T.cati in cats.
Type of Infection
2018
2019
2020
2021
2018 – 2021
Cats (≤ 12) total
80
98
159
194
531
Giardia spp.
N
10
7
15
12
44
%
12.50
7.14
9.43
6.19
8.29
Cryptosporidium spp.
N
7
10
16
13
46
%
8.75
10.20
10.06
6.70
8.66
T. cati
N
4
5
17
14
40
%
5.00
5.10
10.69
7.22
7.53
Cats (> 12) total
134
198
234
253
819
Giardia spp.
N
2
4
10
11
27
%
1.49
2.02
4.27
4.35
3.30
Cryptosporidium spp.
N
1
4
9
5
19
%
0.75
2.02
3.85
1.98
2.32
T. cati
N
1
3
8
5
19
%
0.75
1.52
3.42
1.58
2.32
Cats total
214
296
393
447
1350
Giardia spp
N
12
11
25
23
71
%
5.61
3.72
6.36
5.15
5.26
Cryptosporidium spp.
N
8
14
25
18
65
%
3.74
4.73
6.36
4.03
4.81
T. cati
N
5
8
25
18
56
%
2.34
2.70
6.36
4.03
4.15
In the analysis of combined infections in dogs, we observed the following (Table 3). Coinfections of Giardia spp. and Cryptosporidium spp. (35.5 %), larvae of S. stercoralis and Giardia spp. (32.3 %), T. canis and Giardia spp. (22.6 %). The combination of T. canis and Cryptosporidium spp. (6.6 %) or T. canis and S. stercoralis (3.2 %) in dogs were observed much less frequently. In cats, only two coinfections were found and were caused by Giardia spp. and Cryptosporidium spp. (58.3 %) or T. cati and Giardia spp. (41,7 %).
Combination mixed infections in dogs and cats.
Type of co-infection
Type of animal
Cats
Dogs
N
%
N
%
Giardia spp +Cryptosporidium spp.
7
58.3
11
35.5
S. stercoralis + Giardia spp
-
-
10
32.3
T.canis + Cryptosporidium spp.
-
-
2
6.5
T. cati/canis + Giardia sppT. canis + S. stercoralis
5
41.7
7
22.6
Total
12
100
31
100
Discussion
Our study was focused on the research of helminths and protozoan prevalence where T. canis/cati, S. stercoralis, Giardia spp., and Cryptosporidium spp. in domestic dogs and cats living represent a potential health threat to humans.
Our study has shown that Giardia spp. cysts were found most frequently in domestic dogs, especially in young animals up to 12 months old (18.2 %), while the other parasites from the studied group were detected less often. Many researchers reported similar results (Bouzid et al., 2015; Geurden et al., 2008; Hussein et al., 2017; Liu et al., 2014; Agresti et al., 2022; Piekara-Stepinska et al., 2021). For example, Bouzid et al. (2015) reported that the overall prevalence of Giardia spp. in dogs and cats is about 15.2 % and 12 %, respectively. Mircea et al. (2012) showed that the prevalence of Giardia spp. in domestic dogs is up to 4.8 %. According to Li et al. (2019), Giardia spp. is found in up to 6.9 % of dogs and 9.4 % of cats. We studied domestic animals, so the prevalence of Giardia spp. and Cryptosporidium was lower than in animals living in the shelters. In shelter dogs, Adeell-Aledon et al. (2018) reported Giardia spp. infestation up to 40.4 %. Tangtrongsup et al. (2020) described the prevalence of Giardia spp. up to 25.5 % in dogs and 27.3 % in cats. Cryptosporidium in dogs was up to 7.6 % and 12.1 % in cats. Silva (2020) reported a 28 % prevalence of Giardia spp. in stray dogs and only 6.2 % in household animals.
Despite the high levels of Giardia spp. in dogs, we noticed a gradual decrease in infestation intensity during the 2019 – 2021 period. This may be due to the growing awareness of veterinarians and pet owners about the spread of giardiasis. When symptoms of giardiasis are present, tests are prescribed to exclude them, or anthelmintics against giardiasis are administered for preventive and treatment purposes.
We detected T. canis in dogs and cats to a lesser extent than Giardia spp. and Cryptosporidium spp. (3 % in dogs under 12 months and 7.5 % in cats). Still, the prevalence remained practically at the same level during the observation period. Our data differ significantly from the results of other researchers, where Genchi et al. (2021) reported a 25.6 % infection rate of Toxocara in cats, while Luis Enrique et al. (2018) reported a 25.3 % detection rate of T. canis in dogs. This is likely related to the region and category of animals studied. Many researchers have reported a higher prevalence of parasites in animals in countries with hot climates and abundant rainfall. (Li et al., 2019; Liberato et al., 2022; Umar et al., 2017). We believe that preventive deworming prescribed by veterinarians affects the rates of T. canis infestation. Thus the infection rate remains low but stable. As Zanzani et al. (2014) and Silva et al. (2020) noted, introducing preventive deworming can significantly reduce the rate and risk of infection and invasion transmission.
Li et al. (2019), Sweet et al. (2021), Genchi et al. (2021), Uiterwijk et al. (2019), and other authors reported that the age of animals, especially if they younger (under 12 months) is a significant infection risk factor. It is valid not only for the Giardia but also for the other parasite species with more pronounced clinical manifestations (Sweet et al., 2020; 2021; Luis Enrique et al., 2018; Silva et al., 2020; Liberato et al., 2022). Our studies are aligned with those data and show that in dogs and cats, T. canis/cati, S. stercoralis larvae (in dogs), Giardia spp., and Cryptosporidium spp. are more frequent in younger animals. In general, parasites detected in older dogs and cats occurred less frequently. The high level of infection in young animals may be due to the immaturity of their immune systems. In addition, in the case of Toxocara canis, the transplacental and transmammary routes of transmission promote its occurrence in puppies (Palmer et al., 2008; Gharekhani, 2014). The detection of S. stercoralis larvae in puppies is of particular interest. Despite the low prevalence of these parasites in dogs, their presence cannot be left unattended. When S. stercoralis larvae are detected, an unformed mucous stool is observed. According to the owners, some puppies were active, but some had prolonged diarrhea associated with loss of appetite and depression. Although the endemicity of the disease has been reported, we should consider its recent spread into temperate areas. (Liberato et al., 2022; Unterkofler et al., 2022). However, the limited reports of its prevalence may indicate the lack of feasible detection in dogs. It is due to the unsuitable diagnostic methods used for this parasite laboratory analysis (Unterkofler et al., 2022; Paradies et al., 2017; Umur et al., 2017).
Detection of combined infestations plays a significant role when studying the prevalence of intestinal parasites. In our study, combined infections of two different parasites were observed most frequently in dogs than in cats. This observation in dogs can probably be explained by contact with the external environment, whereas the cats included in this study lived only in the apartments (Kostopoulou et al., 2017; Ursache et al., 2021, Genchi et al., 2021; Rojekittikhun et al., 2014).
It is quite common to observe intestinal parasites in animals without clinical manifestation. We should remember that even asymptomatic parasite carriage can lead to various intestinal pathologies. (Bilgic et al., 2020; Luis Enrique et al., 2018; Uiterwijk et al., 2019; Stafford et al., 2020; Liberato et al., 2022; Moreira et al., 2008). Asymptomatic carrier animals excrete protozoan cysts, larvae, and helminth eggs with feces for a long time. Consequently, they become a source of infestation for healthy animals and cause risks for environmental contamination (Bilgic et al., 2020).
Current discoveries in the biology, genetics, and taxonomy of Giardia spp., Cryptosporidium spp., and Strongyloides sp. isolates obtained from different hosts and their molecular similarities reflect the zoonotic potential of these parasites. (Unterkofler et al., 2022; Li et al. 2019; Bilgic et al., 2020; Bahramdoost et al., 2021; Agresti et al., 2022).
Our results show the necessity for ongoing surveillance of the prevalence of pet intestinal parasites sharing the same environment as humans. Our research will further study parasites’ genetic identity to understand their zoonotic potential. It will lead to the better implementation of preventive measures against the spread of parasites and improvement of the epizootic situation in the urban environment.
Abere, T., Bogale, B., Melaku, A. (2013): Gastrointestinal helminth parasites of pet and stray dogs as a potential risk for human health in Bahir Dar town, north-western Ethiopia. Vet World, 6(7): 388. DOI: 10.5455/vetworld.2013.388-392AbereT.BogaleB.MelakuA.2013Gastrointestinal helminth parasites of pet and stray dogs as a potential risk for human health in Bahir Dar town, north-western EthiopiaVet World6738810.5455/vetworld.2013.388-392Abierto DOISearch in Google Scholar
Adell-Aledon, M., Köster, P. C., de Lucio, A., Puente, P., Hernandez-de-Mingo, M., Sánchez-Thevenet, P., Dea-Ayuela, M. A., Carmena, D. (2018): Occurrence and molecular epidemiology of Giardia duodenalis infection in dog populations in eastern Spain. Vet Res, 14(1): 26. DOI: 10.1186/s12917-018-1353-zAdell-AledonM.KösterP. C.de LucioA.PuenteP.Hernandez-de-MingoM.Sánchez-ThevenetP.Dea-AyuelaM. A.CarmenaD.2018Occurrence and molecular epidemiology of Giardia duodenalis infection in dog populations in eastern SpainVet Res1412610.1186/s12917-018-1353-zAbierto DOISearch in Google Scholar
Agresti, A., Berrilli, F., Maestrini, M., Guadano Procesi, I., Loretti, E., Vonci, N., Perrucci S. (2021): Prevalence, Risk Factors and Genotypes of Giardia duodenalis in Sheltered Dogs in Tuscany (Central Italy). Pathogens, 11(1): 12. DOI: 10.3390/pathogens11010012AgrestiA.BerrilliF.MaestriniM.Guadano ProcesiI.LorettiE.VonciN.PerrucciS.2021Prevalence, Risk Factors and Genotypes of Giardia duodenalis in Sheltered Dogs in Tuscany (Central Italy)Pathogens1111210.3390/pathogens11010012Abierto DOISearch in Google Scholar
Bahramdoost, Z., Mirjalali, H., Yavari, P., Haghighi, A. (2021): Development of HRM real-time PCR for assemblage characterization of Giardia lamblia. Acta Trop, (224): 106109. DOI: 10.1016/j.actatropica.2021.106109BahramdoostZ.MirjalaliH.YavariP.HaghighiA.2021Development of HRM real-time PCR for assemblage characterization of Giardia lambliaActa Trop22410610910.1016/j.actatropica.2021.106109Abierto DOISearch in Google Scholar
Ballweber, L.R., Xiao, L.H., Bowman, D.D., Kahn, G., Cama, V.A. (2010): Giardiasis in dogs and cats: update on epidemiology and public health significance. Trends Parasitol, 26(4): 180 – 189. DOI: 10.1016/j.pt.2010.02.005BallweberL.R.XiaoL.H.BowmanD.D.KahnG.CamaV.A.2010Giardiasis in dogs and cats: update on epidemiology and public health significanceTrends Parasitol26418018910.1016/j.pt.2010.02.005Abierto DOISearch in Google Scholar
Baneth, G., Thamsborg, S.M., Otranto, D., Guillot, J., Blaga, R., Deplazes, P., Solano-Gallego, L. (2016): Major Parasitic Zoonoses Associated with Dogs and Cats in Europe. J Comp Pathol, 155(1): 54 – 74. DOI: 10.1016/j.jcpa.2015.10.179BanethG.ThamsborgS.M.OtrantoD.GuillotJ.BlagaR.DeplazesP.Solano-GallegoL.2016Major Parasitic Zoonoses Associated with Dogs and Cats in Europe.J Comp Pathol1551547410.1016/j.jcpa.2015.10.179Abierto DOISearch in Google Scholar
Basso, W., Grandt, L., Magnenat, A., Gottstein, B., Campos, M. (2019): Strongyloides stercoralis infection in imported and local dogs in Switzerland: from clinics to molecular genetics. Parasitol Res, 118(1): 255 – 266. DOI: 10.1007/s00436-018-6173-3BassoW.GrandtL.MagnenatA.GottsteinB.CamposM.2019Strongyloides stercoralis infection in imported and local dogs in Switzerland: from clinics to molecular geneticsParasitol Res118125526610.1007/s00436-018-6173-3Abierto DOISearch in Google Scholar
Bilgic, B., Bayrakal, A., Dokuzeylul, B., Dodurka, T. (2020): Zoonotic importance of Giardia spp. infections in asymptomatic Dogs. Van Vet J, 31 (3): 158 – 160. DOI: 10.36483/vanvetj.813479BilgicB.BayrakalA.DokuzeylulB.DodurkaT.2020Zoonotic importance of Giardia spp. infections in asymptomatic DogsVan Vet J31315816010.36483/vanvetj.813479Abierto DOISearch in Google Scholar
Blanciardi, P., Papini, R., Giuliani, G., Cardini, G. (2004): Prevalence of Giardia antigen in stool samples from dogs and cats. Revue Med. Vet., 155 (8–9): 417 – 421BlanciardiP.PapiniR.GiulianiG.CardiniG.2004Prevalence of Giardia antigen in stool samples from dogs and catsRevue Med. Vet.1558–9417421Search in Google Scholar
Bourgoin, G., Jacquet-Viallet, P., Zenner, L. (2018): Fatal strongyloidiasis in a puppy from France. Vet Rec Case Rep, 6(2): e000415. DOI: 10.1136/vetreccr-2016-000415BourgoinG.Jacquet-VialletP.ZennerL.2018Fatal strongyloidiasis in a puppy from FranceVet Rec Case Rep62e00041510.1136/vetreccr-2016-000415Abierto DOISearch in Google Scholar
Bouzid, M., Halai, K., Jeffreys, D., Hunter, P. (2015): The prevalence of Giardia infection in dogs and cats, a systematic review and meta-analysis of prevalence studies from stool samples. Vet Parasitol, 207(3–4): 181 – 202. DOI: 10.1016/j.vetpar.2014.12.011BouzidM.HalaiK.JeffreysD.HunterP.2015The prevalence of Giardia infection in dogs and cats, a systematic review and meta-analysis of prevalence studies from stool samplesVet Parasitol2073–418120210.1016/j.vetpar.2014.12.011Abierto DOISearch in Google Scholar
Burgess, L., Gilchrist, C.A., Lynn, T.C., Petri Jr, W. (2017): Parasitic Protozoa and Interactions with the Host Intestinal Microbiota. Infect Immun, 85(8): e00101–17. DOI: 10.1128/IAI.00101-17BurgessL.GilchristC.A.LynnT.C.PetriW.Jr2017Parasitic Protozoa and Interactions with the Host Intestinal MicrobiotaInfect Immun858e001011710.1128/IAI.00101-17Abierto DOISearch in Google Scholar
Companion Animal Parasite Council (CAPC) (2019): Giardia. Retrieved from https://capcvet.org/guidelines/giardia/Companion Animal Parasite Council (CAPC)2019GiardiaRetrieved from https://capcvet.org/guidelines/giardia/Search in Google Scholar
Cervone, M., Giannelli, A., Otranto, D., Perrucci, S. (2016): Strongyloides stercoralis hyperinfection in an immunosuppressed dog from France. Rev. Vet. Clin., 51(2): 55 – 59. DOI: 10.1016/j.anicom.2016.05.001CervoneM.GiannelliA.OtrantoD.PerrucciS.2016Strongyloides stercoralis hyperinfection in an immunosuppressed dog from FranceRev. Vet. Clin.512555910.1016/j.anicom.2016.05.001Abierto DOISearch in Google Scholar
Eydal, M., Skirnisson, K. (2016): Strongyloides stercoralis found in imported dogs, household dogs and kennel dogs in Iceland. Icel Agric Sci, 29(1): 39 – 51. DOI: 10.16886/IAS.2016.04EydalM.SkirnissonK.2016Strongyloides stercoralis found in imported dogs, household dogs and kennel dogs in IcelandIcel Agric Sci291395110.16886/IAS.2016.04Abierto DOISearch in Google Scholar
Feng, Y., Xiao L. (2011): Zoonotic Potential and Molecular Epidemiology of Giardia Species and Giardiasis. Clin Microbiol Rev, 24 (1): 110 – 140. DOI: 10.1128/CMR.00033-10FengY.XiaoL.2011Zoonotic Potential and Molecular Epidemiology of Giardia Species and GiardiasisClin Microbiol Rev24111014010.1128/CMR.00033-10Abierto DOISearch in Google Scholar
Feng, Y., Ryan, U., Xiao, L. (2018): Genetic diversity and population structure of Cryptosporidium. Trends Parasitol, (34):997 – 1011. DOI: 10.1016/j.pt.2018.07.009FengY.RyanU.XiaoL.2018Genetic diversity and population structure of CryptosporidiumTrends Parasitol34997101110.1016/j.pt.2018.07.009Abierto DOISearch in Google Scholar
Genchi, M., Vismarra, A., Zanet, S., Morelli, S., Galuppi, R., Cringoli, G., Otranto, D. Multicentre Study of Endo-Ectoparasite Infection in Italian Cats. Parasit Vectors (preprint under review). DOI: 10.21203/rs.3.rs-558064/v1GenchiM.VismarraA.ZanetS.MorelliS.GaluppiR.CringoliG.OtrantoD.Multicentre Study of Endo-Ectoparasite Infection in Italian CatsParasit Vectors(preprint under review).10.21203/rs.3.rs-558064/v1Abierto DOISearch in Google Scholar
Geurden, T., Berkvens, D., Casaert, S., Vercruysse, J., Claerebout, E. (2008): A Bayesian evaluation of three diagnostic assays for the detection of Giardia duodenalis in symptomatic and asymptomatic dogs. Vet. Parasitol, 157(1–2): 14 – 20. DOI: 10.1016/j.vetpar.2008.07.002GeurdenT.BerkvensD.CasaertS.VercruysseJ.ClaereboutE.2008A Bayesian evaluation of three diagnostic assays for the detection of Giardia duodenalis in symptomatic and asymptomatic dogsVet. Parasitol1571–2142010.1016/j.vetpar.2008.07.002Abierto DOISearch in Google Scholar
Gharekhani, J. (2014): Study on gastrointestinal zoonotic parasites in pet dogs in Western Iran. Turkiye Parazitol Derg, 38(3): 172 – 176. DOI: 10.5152/tpd.2014.3546GharekhaniJ.2014Study on gastrointestinal zoonotic parasites in pet dogs in Western IranTurkiye Parazitol Derg38317217610.5152/tpd.2014.3546Abierto DOISearch in Google Scholar
Gillespie, S., Bradbury, R.S. (2017): A Survey of Intestinal Parasites of Domestic Dogs in Central Queensland. Trop Med Infect Dis, 21(4): 60. DOI: 10.3390/tropicalmed2040060GillespieS.BradburyR.S.2017A Survey of Intestinal Parasites of Domestic Dogs in Central QueenslandTrop Med Infect Dis2146010.3390/tropicalmed2040060Abierto DOISearch in Google Scholar
Hussein, E.M., Ismail, O.A., Mokhtar, A.B., Mohamed, S.E., Saad, R.M. (2017): Nested PCR targeting intergenic spacer (IGS) in genotyping of Giardia duodenalis isolated from symptomatic infected Egyptian school children. Parasitol Res, 116(2): 763 – 771. DOI: 10.1007/s00436-016-5347-0HusseinE.M.IsmailO.A.MokhtarA.B.MohamedS.E.SaadR.M.2017Nested PCR targeting intergenic spacer (IGS) in genotyping of Giardia duodenalis isolated from symptomatic infected Egyptian school childrenParasitol Res116276377110.1007/s00436-016-5347-0Abierto DOISearch in Google Scholar
Ilic, T., Kulisic, Z., Antic, N., Radisavljevic, K., Dimitrijevic, S. (2017): Prevalence of zoonotic intestinal helminths in pet dogs and cats in the Belgrade area. J Appl Anim Res, 45(1): 204 – 208, DOI: 10.1080/09712119.2016.1141779IlicT.KulisicZ.AnticN.RadisavljevicK.DimitrijevicS.2017Prevalence of zoonotic intestinal helminths in pet dogs and cats in the Belgrade areaJ Appl Anim Res45120420810.1080/09712119.2016.1141779Abierto DOISearch in Google Scholar
Jaleta, T., Zhou, S., Bemm, F., Schär, F., Khieu, V., Muth, S., Odermatt, P., Lok, J., Streit, A. (2017): Different but overlapping populations of Strongyloides stercoralis in dogs and humans-Dogs as a possible source for zoonotic strongyloidiasis. PLoS Negl Trop Dis, 11(8): e0005752. DOI: 10.1371/journal.pntd.0005752JaletaT.ZhouS.BemmF.SchärF.KhieuV.MuthS.OdermattP.LokJ.StreitA.2017Different but overlapping populations of Strongyloides stercoralis in dogs and humans-Dogs as a possible source for zoonotic strongyloidiasisPLoS Negl Trop Dis118e000575210.1371/journal.pntd.0005752Abierto DOISearch in Google Scholar
Jothikumar, N., Murphy, J., Hill, V. (2021): Detection and identification of Giardia species using real-time PCR and sequencing. J Microbiol Methods, 189: 106279. DOI: 10.1016/j.mimet.2021.106279JothikumarN.MurphyJ.HillV.2021Detection and identification of Giardia species using real-time PCR and sequencingJ Microbiol Methods18910627910.1016/j.mimet.2021.106279Abierto DOISearch in Google Scholar
Kostopoulou, D., Claerebout, E., Arvanitis, D., Ligda, P., Voutzourakis, N., Casaert, S., Sotiraki, S. (2017): Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations: The scenario of Crete, Greece. Parasit Vectors, 10: 43. DOI: 10.1186/s13071-017-1989-8KostopoulouD.ClaereboutE.ArvanitisD.LigdaP.VoutzourakisN.CasaertS.SotirakiS.2017Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations: The scenario of Crete, GreeceParasit Vectors104310.1186/s13071-017-1989-8Abierto DOISearch in Google Scholar
Li, J., Dan, X., Zhu, K., Li, N., Guo, Y., Zheng, Z., Feng, Y., Xiao, L. (2019): Genetic characterization of Cryptosporidium spp. and Giardia duodenalis in dogs and cats in Guangdong, China. Parasit Vectors, 12(1): 571. DOI: 10.1186/s13071-019-3822-zLiJ.DanX.ZhuK.LiN.GuoY.ZhengZ.FengY.XiaoL.2019Genetic characterization of Cryptosporidium spp. and Giardia duodenalis in dogs and cats in Guangdong, ChinaParasit Vectors12157110.1186/s13071-019-3822-zAbierto DOISearch in Google Scholar
Liberato, C., Iatta, R., Scarito, M., Grifoni, G., Dante, G., Otranto, D. (2022): Strongyloides stercoralis in a dog litter: Evidence suggesting a transmammary transmission. Acta Trop, 231: 106465. DOI: 10.1016/j.actatropica.2022.106465LiberatoC.IattaR.ScaritoM.GrifoniG.DanteG.OtrantoD.2022Strongyloides stercoralis in a dog litter: Evidence suggesting a transmammary transmissionActa Trop23110646510.1016/j.actatropica.2022.106465Abierto DOISearch in Google Scholar
Luis Enrique, J.P., Moreno, L.R., Núñez Fernández, F.A., Millán, I.A., Rivero, L.R., González, F.R., Pérez Rodríguez, J.C. (2018): Prevalence of intestinal parasitic infections in dogs from Havana, Cuba: risk of zoonotic infections to humans. Anim Husb Dairy Vet Sci, 2(3): 1 – 5. DOI: 10.15761/AHDVS.1000133Luis EnriqueJ.P.MorenoL.R.Núñez FernándezF.A.MillánI.A.RiveroL.R.GonzálezF.R.Pérez RodríguezJ.C.2018Prevalence of intestinal parasitic infections in dogs from Havana, Cuba: risk of zoonotic infections to humansAnim Husb Dairy Vet Sci231510.15761/AHDVS.1000133Abierto DOISearch in Google Scholar
Liu, H., Shen, Y.J., Yuan, Z.Y., Jiang, Y.Y., Xu, Y.Z., Pan, W., Hu, Y., Cao, J.P. (2014): Prevalence and genetic characterization of Cryptosporidium, Enterocytozoon, Giardia and Cyclospora in diarrheal outpatients in China. BMC Infect. Dis, 14: 25. DOI: 10.1186/1471-2334-14-25LiuH.ShenY.J.YuanZ.Y.JiangY.Y.XuY.Z.PanW.HuY.CaoJ.P.2014Prevalence and genetic characterization of Cryptosporidium, Enterocytozoon, Giardia and Cyclospora in diarrheal outpatients in ChinaBMC Infect. Dis142510.1186/1471-2334-14-25Abierto DOISearch in Google Scholar
Mircea, V., Györke, A., Cozma, V. (2012): Prevalence and risk factors of Giardia duodenalis in dogs from Romania. Vet Parasitol, 184(2–4): 325 – 329. DOI: 10.1016/j.vetpar.2011.08.022MirceaV.GyörkeA.CozmaV.2012Prevalence and risk factors of Giardia duodenalis in dogs from RomaniaVet Parasitol1842–432532910.1016/j.vetpar.2011.08.022Abierto DOISearch in Google Scholar
Moreira, A., Baptista, C., Brasil, L., Valente, J., Bruhn, F., Pereira, D. (2018): Risk factors and infection due to Cryptosporidium spp. in dogs and cats in southern Rio Grande do Sul. Rev Bras Parasitol Vet, 27(1): 113 – 118. DOI: 10.1590/S1984-296120180012MoreiraA.BaptistaC.BrasilL.ValenteJ.BruhnF.PereiraD.2018Risk factors and infection due to Cryptosporidium spp. in dogs and cats in southern Rio Grande do SulRev Bras Parasitol Vet27111311810.1590/S1984-296120180012Abierto DOISearch in Google Scholar
Mravcova, K., Strkolcova, G., Goldova, M. (2019): The Prevalence And Assemblages of Giardia Duodenalis in Dogs: A Systematic Review in Europe. Folia Vet, 63(4): 38 – 45. DOI: 10.2478/fv-2019-0036MravcovaK.StrkolcovaG.GoldovaM.2019The Prevalence And Assemblages of Giardia Duodenalis in Dogs: A Systematic Review in EuropeFolia Vet634384510.2478/fv-2019-0036Abierto DOISearch in Google Scholar
Nguyen, T., Dorny, P., Dinh, T., Nguyen, V., Nguyen, H., Nguyen, T., Dao, H., Dermauw, V. (2022): Helminth infections in dogs in Phu Tho Province, northern Vietnam. Curr Res Parasitol Vector Borne Dis, 2: 100091. DOI: 10.1016/j.crpvbd.2022.100091NguyenT.DornyP.DinhT.NguyenV.NguyenH.NguyenT.DaoH.DermauwV.2022Helminth infections in dogs in Phu Tho Province, northern VietnamCurr Res Parasitol Vector Borne Dis210009110.1016/j.crpvbd.2022.100091Abierto DOISearch in Google Scholar
De Oliveira, A., Sudre, A., Bomfim, T., Santos, H. (2021) Molecular characterization of Cryptosporidium spp. in dogs and cats in the city of Rio de Janeiro, Brazil, reveals potentially zoonotic species and genotype. PLoS One, 16(8): e0255087. DOI: 10.1371/journal.pone.0255087De OliveiraA.SudreA.BomfimT.SantosH.2021Molecular characterization of Cryptosporidium spp. in dogs and cats in the city of Rio de Janeiro, Brazil, reveals potentially zoonotic species and genotypePLoS One168e025508710.1371/journal.pone.0255087Abierto DOISearch in Google Scholar
Palmer, C., Thompson, R., Traub, R., Rees, R., Robertson, I. (2008): National study of the gastrointestinal parasites of dogs and cats in Australia. J Vet Parasitol, 151: 181 – 190. DOI: 10.1016/j.vetpar.2007.10.015PalmerC.ThompsonR.TraubR.ReesR.RobertsonI.2008National study of the gastrointestinal parasites of dogs and cats in AustraliaJ Vet Parasitol15118119010.1016/j.vetpar.2007.10.015Abierto DOISearch in Google Scholar
Paradies P., Iarussi, F., Paradies, P., Iarussi, F., Sasanelli, M., Capogna, A., Lia, R., Zucca, D., Greco, B., Cantacessi, C., Otranto D. (2017): Otranto occurrence of strongyloidiasis in privately owned and sheltered dogs: clinical presentation and treatment outcome. Parasit Vectors, 10: 345. DOI: 10.1186/s13071-017-2275-5ParadiesP.IarussiF.ParadiesP.IarussiF.SasanelliM.CapognaA.LiaR.ZuccaD.GrecoB.CantacessiC.OtrantoD.2017Otranto occurrence of strongyloidiasis in privately owned and sheltered dogs: clinical presentation and treatment outcomeParasit Vectors1034510.1186/s13071-017-2275-5Abierto DOISearch in Google Scholar
Piekara-Stępinska, A., Piekarska, J., Gorczykowski, M. (2021): Cryptosporidium spp. in dogs and cats in Poland. Ann Agric Environ Med, 28(2): 345 – 347. DOI: 10.26444/aaem/120467Piekara-StępinskaA.PiekarskaJ.GorczykowskiM.2021Cryptosporidium spp. in dogs and cats in PolandAnn Agric Environ Med28234534710.26444/aaem/120467Abierto DOISearch in Google Scholar
Raicevic, J., Pavlovic, I., Coghill, T. (2021): Canine intestinal parasites as a potential source of soil contamination in the public areas of Krusevac, Serbia. J Infect Dev Ctries, 15(1): 147 – 154. DOI: 10.3855/jidc.12694RaicevicJ.PavlovicI.CoghillT.2021Canine intestinal parasites as a potential source of soil contamination in the public areas of Krusevac, SerbiaJ Infect Dev Ctries15114715410.3855/jidc.12694Abierto DOISearch in Google Scholar
Rojekittikhun, W., Chaisiri, K., Mahittikorn, A., Pubampen, S., Sa-Nguankiat, S., Kusolsuk, T., Maipanich, W., Udonsom, R., Mori, H. (2014): Gastrointestinal parasites of dogs and cats in a refuge in Nakhon Nayok, Thailand. Southeast Asian J Trop Med Public Health, 45(1): 31 – 39RojekittikhunW.ChaisiriK.MahittikornA.PubampenS.Sa-NguankiatS.KusolsukT.MaipanichW.UdonsomR.MoriH.2014Gastrointestinal parasites of dogs and cats in a refuge in Nakhon Nayok, ThailandSoutheast Asian J Trop Med Public Health4513139Search in Google Scholar
Silva, V., Silva, J., Goncalves, M., Brandao, C., Brito, V. N. (2020): Epidemiological survey on intestinal helminths of stray dogs in Guimarães, Portugal. J Parasit Dis, 44(4): 869 – 876. DOI: 10.1007/s12639-020-01252-2SilvaV.SilvaJ.GoncalvesM.BrandaoC.BritoV. N.2020Epidemiological survey on intestinal helminths of stray dogs in Guimarães, PortugalJ Parasit Dis44486987610.1007/s12639-020-01252-2Abierto DOISearch in Google Scholar
Stafford, K., Kollasch, T., Duncan, K., Horr, S., Goddu, T., Heinz-Loomer, C., Rumschlag, A., Ryan, W., Sweet, S., Little, S. (2020): Detection of gastrointestinal parasitism at recreational canine sites in the USA: the DOGPARCS study. Parasit Vectors, 13(1): 275. DOI: 10.1186/s13071-020-04147-6.StaffordK.KollaschT.DuncanK.HorrS.GodduT.Heinz-LoomerC.RumschlagA.RyanW.SweetS.LittleS.2020Detection of gastrointestinal parasitism at recreational canine sites in the USA: the DOGPARCS study.Parasit Vectors13127510.1186/s13071-020-04147-6.Abierto DOISearch in Google Scholar
Sweet, S., Szlosek, D., McCrann, D., Coyne, M., Kincaid, D., Hegarty, E. (2020): Retrospective analysis of feline intestinal parasites: trends in testing positivity by age, USA geographical region and reason for veterinary visit. Parasit Vectors, 13(1): 473. DOI: 10.1186/s13071-020-04319-4SweetS.SzlosekD.McCrannD.CoyneM.KincaidD.HegartyE.2020Retrospective analysis of feline intestinal parasites: trends in testing positivity by age, USA geographical region and reason for veterinary visitParasit Vectors13147310.1186/s13071-020-04319-4Abierto DOISearch in Google Scholar
Sweet, S., Hegarty, E., McCrann, D., Coyne, M., Kincaid, D., Szlosek, D. (2021): A 3-year retrospective analysis of canine intestinal parasites: fecal testing positivity by age, U.S. geographical region and reason for veterinary visit. Parasit Vectors, 14: 173. DOI: 10.1186/s13071-021-04678-6SweetS.HegartyE.McCrannD.CoyneM.KincaidD.SzlosekD.2021A 3-year retrospective analysis of canine intestinal parasites: fecal testing positivity by age, U.S. geographical region and reason for veterinary visitParasit Vectors1417310.1186/s13071-021-04678-6Abierto DOISearch in Google Scholar
Tangtrongsup, S., Scorza, A., Reif, J., Ballweber, L., Lappin, M., Salman, M. (2020): Seasonal distributions and other risk factors for Giardia duodenalis and Cryptosporidium spp. infections in dogs and cats in Chiang Mai, Thailand. Prev Vet Med, 174: 104820. DOI: 10.1016/j.prevetmed.2019.104820TangtrongsupS.ScorzaA.ReifJ.BallweberL.LappinM.SalmanM.2020Seasonal distributions and other risk factors for Giardia duodenalis and Cryptosporidium spp. infections in dogs and cats in Chiang Mai, ThailandPrev Vet Med17410482010.1016/j.prevetmed.2019.104820Abierto DOISearch in Google Scholar
Thompson, R.C., Monis, P.T. (2004): Variation in Giardia: implications for taxonomy and epidemiology. Adv Parasitol, (58): 137 – 141. DOI: 10.1016/S0065-308X(04)58002ThompsonR.C.MonisP.T.2004Variation in Giardia: implications for taxonomy and epidemiologyAdv Parasitol5813714110.1016/S0065-308X(04)58002Abierto DOISearch in Google Scholar
Thompson, R.C., Palmer, C.S., O’Handley, R. (2008): The public health and clinical significance of Giardia and Cryptosporidium in domestic animals. Vet J, 177(1): 18 – 25. DOI: 10.1016/j.tvjl.2007.09.022ThompsonR.C.PalmerC.S.O’HandleyR.2008The public health and clinical significance of Giardia and Cryptosporidium in domestic animalsVet J1771182510.1016/j.tvjl.2007.09.022Abierto DOISearch in Google Scholar
Uiterwijk, M., Nijsse, R., Kooyman, F., Wagenaar, J., Mughini-Gras, L., Ploeger, H. (2019): Host factors associated with Giardia duodenalis infection in dogs across multiple diagnostic tests. Parasit Vectors, 12(1): 556. DOI: 10.1186/s13071-019-3810-3UiterwijkM.NijsseR.KooymanF.WagenaarJ.Mughini-GrasL.PloegerH.2019Host factors associated with Giardia duodenalis infection in dogs across multiple diagnostic testsParasit Vectors12155610.1186/s13071-019-3810-3Abierto DOISearch in Google Scholar
Uiterwijk, M., Mughini-Gras, L., Nijsse, R., Wagenaar, J., Ploeger, H., Kooyman, F. (2020): Giardia duodenalis multi-locus genotypes in dogs with different levels of synanthropism and clinical signs. Parasit Vectors, 13(1): 605. DOI: 10.1186/s13071-020-04496-2UiterwijkM.Mughini-GrasL.NijsseR.WagenaarJ.PloegerH.KooymanF.2020Giardia duodenalis multi-locus genotypes in dogs with different levels of synanthropism and clinical signsParasit Vectors13160510.1186/s13071-020-04496-2Abierto DOISearch in Google Scholar
Umur, S., Meral, Y., Bolukbas, S., Gurler, A., Acici, M. (2017): First clinical Strongyloides stercoralis case in a dog in Turkey. Turk J Vet Anim Sci, 41: 312 – 315. DOI: 10.3906/vet-1606-2UmurS.MeralY.BolukbasS.GurlerA.AciciM.2017First clinical Strongyloides stercoralis case in a dog in TurkeyTurk J Vet Anim Sci4131231510.3906/vet-1606-2Abierto DOISearch in Google Scholar
Ursache, A., Gyorke, A., Mircean, V., Dumitrache, M., Codea, A., Cozma, V. (2021): Toxocara cati and Other Parasitic Enteropathogens: More Commonly Found in Owned Cats with Gastrointestinal Signs Than in Clinically Healthy Ones. Pathogens, 10(2): 198. DOI: 10.3390/pathogens10020198UrsacheA.GyorkeA.MirceanV.DumitracheM.CodeaA.CozmaV.2021Toxocara cati and Other Parasitic Enteropathogens: More Commonly Found in Owned Cats with Gastrointestinal Signs Than in Clinically Healthy OnesPathogens10219810.3390/pathogens10020198Abierto DOISearch in Google Scholar
Unterköfler, M. S., Eipeldauer, I., Merz, S., Pantchev, N., Hermann, J., Brunthaler, R., Basso, W., Hinney, B. (2022): Strongyloides stercoralis infection in dogs in Austria: two case reports. Parasit Vectors, 15(1): 168. DOI: 10.1186/s13071-022-05270-2UnterköflerM. S.EipeldauerI.MerzS.PantchevN.HermannJ.BrunthalerR.BassoW.HinneyB.2022Strongyloides stercoralis infection in dogs in Austria: two case reportsParasit Vectors15116810.1186/s13071-022-05270-2Abierto DOISearch in Google Scholar
Zajac, A.M., Conboy, G.A. (2012): Veterinary Clinical Parasitology, 8th Edition. Wiley-Blackwell Chichester, 368ZajacA.M.ConboyG.A.2012Veterinary Clinical Parasitology8th EditionWiley-BlackwellChichester368Search in Google Scholar
Zanzani, S.A., Gazzonis, A.L., Scarpa, P., Berrilli, F., Manfredi, M.T. (2014): Intestinal parasites of owned dogs and cats from metropolitan and micropolitan areas: prevalence, zoonotic risks, and pet owner awareness in northern Italy. Biomed Res Int, 2014: 696508. DOI: 10.1155/2014/696508ZanzaniS.A.GazzonisA.L.ScarpaP.BerrilliF.ManfrediM.T.2014Intestinal parasites of owned dogs and cats from metropolitan and micropolitan areas: prevalence, zoonotic risks, and pet owner awareness in northern ItalyBiomed Res Int201469650810.1155/2014/696508Abierto DOISearch in Google Scholar
