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Prevalence of Intestinal Parasites in Dogs and Cats from the Kvarner Region in Croatia

Prevalence of Intestinal Parasites in Dogs and Cats from the Kvarner Region in Croatia Acta Veterinaria-Beograd 2023, 73 (1), 41-54 UDK: 636.7/.8.09:616.99-084(497.5) DOI: 10.2478/acve-2023-0004 Research article PREVALENCE OF INTESTINAL PARASITES IN DOGS AND CATS FROM THE KVARNER REGION IN CROATIA 1 2* 3 Siniša FARAGUNA , Ivan VLAHEK , Kristina Tea MIOČIĆ , 4 5 Tibor ANDREANSZKY , Marko PEĆIN Research assistant, University of Zagreb, Faculty of Veterinary Medicine, Department of Pathophysiology, Zagreb, Croatia; University of Zagreb, Faculty of Veterinary Medicine, Department of Animal Breeding and Livestock Production, Zagreb, Croatia; Croatian Health Insurance Fund, 4 5 Rijeka, Croatia; Croatian Veterinary Institute, Department Rijeka, Rijeka, Croatia; University of Zagreb, Faculty of Veterinary Medicine, Clinic for Surgery, Orthopaedics and Ophthalmology, Zagreb, Croatia (Received 14 September 2022, Accepted 23 February 2023) Intestinal parasites of dogs and cats may affect their health with a signifi cant zoonotic risk to public health. Therefore, establishing an effi cient control program should pass through the determination of the diversity, prevalence, and pathogenicity of those parasites. This study aimed to determine the prevalence of intestinal parasites in dogs and cats and proceed to infection comparisons between young and adult animals. The detection of parasites in fecal samples was determined using fl otation and immunofl uorescent methods across 320 dogs and 64 cats from the Kvarner region in Croatia. The prevalence was calculated for each detected parasite in its host. Differences in prevalence between young animals and adults were analyzed. Parasites were detected in 32 dogs and 34.4% of cats. In total, 12 different genera were detected; Giardia spp. was the most prevalent parasite in both species, infecting 24.7% and 18.8% of investigated dogs and cats, respectively. Cryptosporidium spp. and Toxocara cati had a prevalence of (18.4%) and (6.3%), respectively. Prevalences of Giardia spp., Cryptosporidium spp., and Cystoisospora spp. were signifi cantly (P < 0.05) higher in puppies compared to adult dogs. Pentatrichomonas hominis (P. hominis) was detected in one puppy. In addition to the fi rst report of P. hominis, a relatively high prevalence of intestinal parasites in dogs and cats in the Kvarner region of Croatia was recorded, posing a potential zoonotic risk. Keywords: cats, Croatia, dogs, intestinal parasitic infection, prevalence INTRODUCTION Dogs and cats can harbour various intestinal parasites, which can cause gastrointestinal disturbances [1]. Many of these parasites have a zoonotic potential, posing a risk to the human population. Thus, epizootiological studies aimed to determine the presence and the prevalence of parasites within pet populations represent a relatively simple, *Corresponding author: e-mail: ivlahek@vef.unizg.hr 41 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 effi cient, and useful source of information for practitioners in veterinary and human medicine. Common intestinal parasites in dogs and cats from the Middle-European region include protozoans like Giardia spp., Cryptosporidium spp., Sarcocystis spp., and Cystoisospora spp., roundworms Toxocara spp. and Toxascaris spp., hookworms Ancylostoma spp. and Uncinaria spp., whipworm Trichuris vulpis, bladder worm Capillaria plica and fl atworms Dipylidium spp. and Taenia spp. [2,3]. These parasites are considered signifi cant as they might cause diarrhoea and malabsorption in their hosts. In young dogs and cats, some parasites are responsible for weight loss and the normal development of an animal. In clinical cases, severe dehydration and even death can occur [4]. Commonly, the most prevalent intestinal parasites in dogs and cats are protozoans, especially Giardia, which explains the importance of the research on its zoonotic and epizootiological potential [5]. A study showed that the prevalence of giardiasis in humans is generally low in developed countries compared to developing countries [6]. Poor hygiene, low standards, and overcrowding may play an important role as possible zoonotic factors in transmission by cohabiting pet dogs [7]. Undisposed dog faeces positive for zoonotic and non-zoonotic intestinal parasites and environmental contamination have been reported in city parks, which make them potential sources of protozoan and worm infections for dogs and humans [8]. In another study, authors found a signifi cant association between dogs who attended parks and Giardia spp./Cryptosporidium spp. infection [9]. Also, public shelters present a signifi cant source of infection due to close cohabitation and poor hygienic conditions [2]. The constant presence of zoonotic intestinal parasites in dogs and cats indicates the need for planned, systematic, and adequate parasite control programs, which would ultimately positively affect human health. One of the fi rst steps towards this goal should be a precise and detailed determination of the parasites’ diversity, prevalence, and pathogenicity. The aim of this study was to determine the presence and prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia through coprological analyses. Furthermore, the prevalence of multiple infections and the differences in the number of infections between young and adult dogs and cats were assessed. MATERIALS AND METHODS Ethical statement This research is not related to the use of animals. No ethical approval was obtained because this study did not involve animals but only non-invasive procedures (collecting faecal samples from the environment). 42 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Animals and sampling A total of 384 fecal samples were collected between January 2019 and January 2021 from privately owned dogs (n=293; 138 females and 155 males) and 27 dogs from one shelter (19 females and eight males), and privately owned cats (n=64; 38 females and 26 males) from different parts of Kvarner region for a coprological examination. Basic information on examined dogs and cats is summarised in Table 1 and Table 2, respectively. Collected samples represented a mixture of clinically healthy animals and animals demonstrating clinical symptoms indicative of intestinal parasitism (e.g. diarrhoea, failure to gain weight) [10]. Table 1. Basic demographics of the dogs (N = 320) whose feces were examined Breed 187 mix breed; 35 unknown; 98 pure breeds (4 Cane Corso, 7 Maltese, 1 English bulldog, 5 German shepherd, 13 Labrador retriever, 1 Pitbull, 3 Bichon Frise, 5 Poodle, 4 Bernese Mountain, 3 Afghan hound, 8 Golden retriver, 3 German spitz, 5 Beagle, 2 Dalmatian, 1 German boxer, 1 Shar-pei, 2 Welsh Corgi, 2 West Highland White Terrier, 1 Greater Swiss Mountain, 2 Vizsla, 2 German short-haired pointer, 4 Cocker spaniel, 3 Irish setter, 1 Great Dane, 2 Miniature Schnauzer, 1 Siberian Husky, 1 Cavalier King Charles Spaniel, 1 Dogo Argentino, 1 Posavac Hound, 1 Dachshund, 4 Pugs, 1 Istrian short-haired hound, 2 Basset Hound, 1 English Cocker Spaniel and 1 Chihuahua) Age 78 ≤ 6 months, considered as puppy; 207 > 6 months, considered as adult dogs; 35 unknown Gender 163 male and 157 female Use of anthelmintics YES: 249 dogs ; NO: 36 dogs; UNKNOWN: 35 dogs (if any) 162 dogs ≤ 6 months; 87 dogs > 6 months Dogs from animal 27 dogs from animal shelter; 293 household dogs shelters/household dogs N – total number of samples Table 2. Basic demographics of the cats (N = 64) whose feces were examined Breed 54 mix breed; 10 pure breeds ( 3 Maine coon, 2 Persian cat, 3 British Shorthair, 1 Sphynx, 1 Russian Blue) Age 11 ≤ 6 months, considered as kittens; 49 > 6 months, considered as adult cats; 4 unknown Gender 26 male and 38 female Use of anthelmintics (if any) YES: 49 cats; NO: 15 cats 23 cats ≤ 6 months; 26 cats > 6 months Household cats 64 household cats N – total number of samples For parasitological examination, dogs and cats were divided into two groups to test the possible relationship between age and the presence or absence of parasitism. Dogs 43 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 and cats were classifi ed as puppies/kittens (≤ six months of age) and adults ( > six months of age). The apparent prevalence of infections was calculated by dividing the number of animals diagnosed with a parasite on fecal examination by the total number of fecal examinations performed for each age group. Questionnaire survey Owners who participated in this study were asked to provide additional information in a questionnaire that contained questions on data of age, sex, breed, previous dehelmintisation, recent clinical symptoms consistent with intestinal parasitism, history of diagnosed intestinal parasites in the past, and stool consistency [11]. For 35 dogs and four cats, the age was unknown. Collection and storage All fecal samples (10 – 20 g approximately) were collected from the ground immediately after defecation by the instructed owners in a provided labelled, clean plastic cup and stored in a refrigerator at +4 °C. Microscopic examination was performed up to 48 hours after sample collection. Methods Parasitological examination. Firstly, a macroscopic examination of all samples for detecting proglottids of cestodes was performed. All admitted samples were divided into two parts of approximately 5-7 g each (if available). Each part was analysed in the diagnostic laboratory of the Croatian Veterinary Institute, Department Rijeka, with two different diagnostic methods: (1) standardised fl otation method with saturated sodium chloride solution (specifi c gravity 1.2) [12] and (2) commercially available MERIFLUOR® Cryptosporidium/Giardia kit (Meridian Bioscience, Inc., SAD) by direct immunofl uorescent detection procedure according to the manufacturer’s instructions for simultaneous detection of Cryptosporidium spp. oocysts and Giardia spp. cysts by immunofl uorescence assay. Morphological determination. The sample was considered positive if at least one test showed a positive result based on morphological keys [13]. The species of parasites found were microphotographed and then classifi ed according to genus, including Giardia, Cryptosporidium, Cystoisospora, Pentatrichomonas, Toxocara, Toxascaris, Trichuris, Capillaria, Ancylostoma, Uncinaria, Dipylidium, and Taenia. Molecular diagnosis. For the exact diagnosis of trichomoniasis, parasite DNA was extracted using the QIAamp® Mini Kit (Qiagen, Hilden, Germany), according to the manufacturer’s instructions. Further molecular diagnosis, including PCR, gel electrophoresis, DNA purifi cation, and sequencing were done according to Felleisen, 1997. protocol [14]. 44 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Statistical analysis Data were analysed using the statistical program TIBCO Statistica® [15]. Fisher exact test was used to determine the statistical signifi cance of the differences in the prevalences of intestinal parasitic infections between young and adult dogs and cats. The confi dence level was set at 95%, and the results were considered signifi cant if P < 0.05. RESULTS Dogs Parasitic forms were detected in 103 of 320 (32.2%) dogs with a 95% confi dence interval (95% CI) of 27.1 - 37.6. Overall, 11 intestinal parasite species/genera were identifi ed with fl otation and direct immunofl uorescent methods (Table 3). Table 3. Proportions of single and multiple parasitic infection in dogs n. positive Endoparasite infections 95% CI (prevalence) Single endoparasite infections Ancylostoma spp. 2 (0.6%) 0.08-2.2 Capillaria spp. 3 (0.9%) 0.2-2.7 Toxascaris leonina 4 (1.3%) 0.3-3.2 Toxocara canis 11 (3.4%) 1.7-6.1 Trichuris vulpis 3 (0.9%) 0.2-2.7 Uncinaria stenocephala 1 (0.3%) 0.01-1.7 Dipylidium caninum 1 (0.3%) 0.01-1.7 Giardia spp. 79 (24.7%) 20.1-29.8 Isospora spp. 8 (2.5%) 1.1-4.9 Cryptosporidium spp. 59 (18.4%) 14.3-23.1 Pentatrichomonas hominis 1 (0.3%) 0.01-1.7 Mixed endoparasitic infections Isospora spp.+ Giardia spp. 5 (1.6%) 0.5-3.6 Toxocara canis + Capillaria spp. 2 (0.6%) 0.08-2.2 Giardia spp. + Cryptosporidium spp. 18 (5.6%) 3.4-8.7 Isospora spp. + Pentatrichomonas hominis 1 (0.3%) 0.01-1.7 Toxocara canis + Giardia spp. 1 (0.3%) 0.01-1.7 Trichuris vulpis + Toxocara canis 1 (0.3%) 0.01-1.7 Giardia spp.+ Uncinaria stenocephala 1 (0.3%) 0.01-1.7 Trichuris vulpis + Toxocara canis + Toxascaris leonina 1 (0.3%) 0.01-1.7 n – number of positive samples, CI – confi dence interval 45 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 The most common parasites were Giardia spp. and Cryptosporidium spp. Mixed infections were detected in 30 dogs, of which 18 had coinfection with Giardia spp. and Cryptosporidium spp. parasites. Overall prevalence in puppies and adults was 89.7% (95% CI = 80.8-95.5) and 47.3% (95% CI = 40.4-54.4), respectively. Ancylostoma spp., Trichuris vulpis, and Dipylidium caninum were detected only in adult dogs, while Uncinaria stenocephala and Pentatrichomonas hominis were detected only in puppies (Table 4). Puppies had a signifi cantly (P < 0.05) higher prevalence of Giardia spp., Cystoisospora spp., and Cryptosporidium spp. parasites compared to adult dogs (Table 4). There was no signifi cant difference (P > 0.05) between the prevalence in male (35.8%; 95% CI = 28.4-43.7) and female (28.5%; 95% CI = 21.6-36.2) dogs. The pooled prevalence of Giardia spp. and Cryptosporidium spp. was 43.1% (CI = 37.6-48.8). Table 4. Prevalence of endoparasites in dogs according to age Age category Puppy (≤6 mo) Adult (>6 mo) Parasite P-value N = 78 N = 207 n Prev. 95% CI n Prev. 95% CI Ancylostoma spp. / / / 2 1.0% 0.1-3.5 / Capillaria spp. 1 1.3% 0.03-6.9 2 1.0% 0.1-3.5 0.618 Toxascaris leonina 1 1.3% 0.03-6.9 3 1.5% 0.3-4.2 0.698 Toxocara canis 2 2.6% 0.3-9.0 9 4.4% 2.0-8.1 0.381 Trichuris vulpis / / / 3 1.5% 0.3-4.2 / Uncinaria stenocephala 1 1.3% 0.03-6.9 / / / / Dipylidium caninum / / / 1 0.5% 0.01-2.7 / Giardia spp. 33 42.0% 31.1-54.0 44 21.3% 15.9-27.5 0.001 Isospora spp. 5 6.4% 2.1-14.3 3 1.5% 0.3-4.2 0.038 Cryptosporidium spp. 26 33.3% 23.1-44.9 31 15.0% 10.4-20.6 0.004 Pentatrichomonas hominis 1 1.3% 0.03-6.9 / / / / p<0.05, N – total number of samples, n – number of positive samples, CI – confi dence interval, Prev – prevalence Cats Twenty-two of 64 (34.4%; 95% CI = 23.0-47.3) investigated cats were infected with intestinal parasites. Seven different intestinal parasite species/genera were identifi ed with fl otation and direct immunofl uorescent methods, of which Giardia spp. and Toxocara cati were the most prevalent (Table 5). Infection with two parasites was detected in fi ve cats (Table 5). Overall prevalence in kittens and adult was 27.3% (95% CI = 6.0-61.0) and 38.8 (95% CI = 25.2-53.8), respectively. In kittens, only Giardia spp. was found, which also had the highest prevalence in adult cats (Table 6). There was no signifi cant difference (P > 0.05) between the prevalence of intestinal parasites in male (24.0%; 95% CI = 9.4-45.1) and female (27.5%; 95% CI = 14.6-43.9) cats. 46 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Table 5. Proportions of single and multiple parasitic infection in cats n. positive Endoparasite infections 95% CI (prevalence) Single endoparasite infections Capillaria spp. 1 (1.6%) 0.04-8.4 Toxocara cati 4 (6.3%) 1.7-15.2 Dipylidium caninum 1 (1.6%) 0.04-8.4 Taenia spp. 2 (3.1%) 0.4-10.8 Giardia spp. 12 (18.8%) 10.1-30.5 Isospora spp. 1 (1.6%) 0.04-8.4 Cryptosporidium spp. 1 (1.6%) 0.04-8.4 Mixed endoparasitic infections Toxocara cati + Giardia spp. 2 (3.1%) 0.4-10.8 Toxocara cati + Capillaria spp. 1 (1.6%) 0.04-8.4 Isospora spp. + Dipylidium caninum 1 (1.6%) 0.04-8.4 Giardia spp.+ Cryptosporidium spp. 1 (1.6%) 0.04-8.4 n – number of positive samples, CI – confi dence interval Table 6. Prevalence of endoparasites in cats acording to age Age category Kitten (≤6 mo) Adult (>6 mo) Parasite P-value N = 11 N = 49 n Prev. 95% CI n Prev. 95% CI Capillaria spp. / / / 1 2.0% 0.05-10.9 / Toxocara cati / / / 4 8.2% 2.3-19.6 / Dipylidium caninum / / / 1 2.0% 0.05-10.9 / Taenia spp. / / / 2 4.1% 0.5-14.0 / Giardia spp. 3 27.3% 6.0-61.0 9 18.4% 8.8-32.0 0.382 Isospora spp. / / / 1 2.0% 0.05-10.9 / Cryptosporidium spp. / / / 1 2.0% 0.05-10.9 / p<0.05, N – total number of samples, n – number of positive samples, CI – confi dence interval, Prev – prevalence DISCUSSION Data on the prevalence of intestinal parasites in dogs and cats from Croatia are scarce. Thus, the primary aim of this study was to determine the prevalence of intestinal parasitic infection in a Croatian population of dogs and cats using the fl otation and direct immunofl uorescent method. Twelve different genera of intestinal parasites were found, and 32.2% of the examined dogs and 28.1% of the cats were infected. These fi ndings correspond with the large-scale analysis in Germany, which found 47 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 that 32.2% of the dogs and 24.3% of the cats had intestinal parasites [16]. A larger overall prevalence of intestinal parasites in dogs from the Zagreb area, Croatia (48.1% - 64.9%) was reported in 2017 [17]. In our study, protozoan parasites were the most prevalent, and 5.6% of dogs had both Giardia spp. and Cryptosporidium spp. infections. In this research, Giardia spp. was the most common parasite in dogs and cats. These results are in agreement with the report, which found Giardia spp. to be the most prevalent parasite in dogs (20.2%) and cats (36.0%) in Slovakia [3]. In a previous study in Zagreb, the prevalence of this parasite in dogs ranged between 23.8 and 26.7% [17]. Similarly, the prevalence of Giardia spp. was 28.47%, 23.75%, 25.1%, 27.53%, 25.89%, and 24.62% in dogs from Belgium, Germany, Spain, France, Italy, and the Netherlands, respectively [18]. However, our research used the direct immunofl uorescence test for Giardia spp. detection, a more sensitive method than the SNAP Giardia test. A lower prevalence (7.0%) of Giardia spp. was detected in household and sheltered dogs from Central Italy [19]. In this research, puppies were more likely ( P < 0.05) to have Giardia spp. than adults, which is consistent with the results of a similar previous study conducted in Colombia [1]. Also, Giardia spp. was the only parasite found in kittens. Regardless of clinical signs, Giardia spp. is ubiquitous in dogs and cats [20,21]. Considering that it has a zoonotic potential [22] and that prevalence of giardiasis in dogs can reach up to 43.9% [23], its zoonotic risk should not be overlooked. Cryptosporidium spp. has been found in dogs and cats with different prevalences, and its presence can be associated with diarrhoea [24,25,20]. In this study, it was the second most prevalent parasite (18.4%) in dogs. The results in the Zagreb area between 2012 and 2015 stated that the prevalence of Cryptosporidium spp. in dogs ranged between 8.0% and 18.7% [17]. One meta-analysis showed that the pooled prevalence of Cryptosporidium spp. in the world is 8% and 3% in Europe, which indicates that the prevalence of this parasite in Croatia is relatively high [26]. Puppies seem twice as likely (P < 0.05) to have it than adults. High-level infection in puppies could be explained by the fact that the immune system of young animals is not fully developed [27,28]. A contributing factor to the high prevalence of Cryptosporidium spp., as well as of Giardia spp., might be the frequent contact with other animals from different epizootiological areas during tourist season. Kvarner region is a well-known tourist destination where tourists will likely arrive with their pets from different regions of Europe and the world. Data about coccidian prevalence in Europe is scarce. In this study, Cystoisospora spp. was detected in adult cats and in both age categories of dogs. Moreover, signifi cant (P < 0.05) differences were observed between the prevalence in puppies and adult dogs, with puppies being the more exposed group. This is in agreement with the research that found that the prevalence of Cystoisospora spp. in dogs signifi cantly declined after four months of age [4]. [29] reported a higher prevalence of Isospora felis in cats younger than six months (9%) compared to older cats (2%). However, all investigated cats in their research showed symptoms of gastrointestinal disease. 48 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Pentatrichomonas hominis (P. hominis) was found in one puppy, along with the Cystoisospora spp. The puppy had soft, malodorous diarrhoea. Several studies reported similar clinical signs in young dogs infected with this parasite [30,31,32]. Even though one study reported the prevalence of P. hominis in puppies from French kennels to be 15.8%, it is relatively rarely diagnosed in dogs and cats [33]. One reason for this might be that for its detection, highly specifi c and sensitive PCR assays need to be used [32]. However, due to its zoonotic potential, P. hominis may represent a serious health problem, and it is important to control its prevalence in domestic animal populations. To the best of our knowledge, this is the fi rst report that P. hominis is involved in clinical diseases of dogs in Croatia. Toxocariasis is one of the most common zoonotic parasitic infections worldwide [34,35]. As reported in a study, its prevalence can reach up to 33.5% in young sheltered dogs [2]. One of the most important sources of ground contamination with T. canis is free-roaming dogs [36], and human infection is possible by lying on the contaminated grass or soil [37]. Although most human infections with T. canis are subclinical, they may also cause severe clinical symptoms due to larval migration [38]. In this study, the prevalence of T. canis and T. cati was 3.4% and 6.3%, respectively. These results were lower than expected since the worldwide pooled prevalence of T. canis, and T. cati reported in large meta-analyses was 11.1% and 17.0%, respectively [34,39]. The relatively low prevalence of T. canis and T. cati in this study may be the result of concerned pet owners being under continuous veterinary control, with a higher degree of care and preventative measures. Indeed, 87% of dog owners (who answered that question) and 77% of cat owners stated that their pets were treated with anthelmintics. Similar prevalences to those obtained in this study were reported [11,17,1]. Even though young age is recognized as a risk factor for toxocariasis in dogs [40], results from this study showed non-signifi cant (P > 0.05) differences in prevalences regarding age. In this study, hookworms (Ancylostoma spp. and Uncinaria stenocephala) and Trichuris vulpis (T. vulpis) were found in 0.6%, 0.3%, and 0.9% of dogs, respectively. Eggs of Ancylostoma spp. and T. vulpis were found in adult dogs, while Uncinaria stenocephala was found in one puppy. Similar prevalence was reported in a study from Germany [11], although reports from South America stated that T. vulpis [41] and Ancylostoma spp. [1] were the second most common parasites in dogs, with a prevalence of 16.2% and 12.6%, respectively. However, one study reported a prevalence of hookworms of 0.7 – 0.9% in rural dogs and 0.4% in urban dogs in the Czech Republic [42]. The low prevalence of Ancylostoma spp., Uncinaria stenocephala, and T. vulpis might be due to regular dehelminthisation, or the samples might be taken in the prepatent period of the infection. The prevalence of the Taeniidae and Dipylidiidae parasites was: 0.3% for D. caninum in dogs and 1.6% in cats, while 3.1% of cats had Taenia spp. All parasites were determined in adults. Relatively low prevalences of D. caninum and Taenia spp. determined by fecal 49 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 examination in this study probably do not represent the true prevalence, mainly because of the excretion behavior of the cestodes. Indeed, one study reported that cestodes were found in 1% of dogs after coprological examination, while post-mortem analysis revealed 46% of tapeworm-infected dogs [43]. Thus, in this study, the real prevalence of cestode infections in dogs and cats is probably much higher than recorded. This study had a few limitations. Firstly, Giardia spp. is probably underestimated due to the intermittent excretion of Giardia cysts. Examination of just one fecal sample, as was done in this study, may produce false-negative results and underestimates the true prevalence value. This may also apply to the results for tapeworm prevalence. In this study, a fl otation method with a saturated sodium chloride solution was used to detect Taenia spp. In contrast, the most common method is fl otation with a saturated solution of zinc sulphate. The second limitation was poor anamnesis provided by the owners in the questionnaire, particularly in describing the presence and the character of diarrhoea. If the information were provided, it could aid in interpreting the laboratory fi ndings, as the causes of diarrhoea are not always infectious. Some authors stated that most cases of chronic diarrhoea in dogs are not infectious but rather infl ammatory enteropathies that are food, antibiotic, or steroid responsive [44]. CONCLUSION This study showed a considerably high prevalence of intestinal parasites in dogs and cats in the Kvarner region, Croatia. Findings may indicate a potential zoonotic risk, especially in the case of Giardia spp., Cryptosporidium spp., and Toxocara spp., which in this study were the most prevalent parasites. The investigated population of dogs and cats is well-cared, but the higher occurrence of detected Giardia spp. advocates the need for more effective deworming schemes, regular faecal examinations, and cleaning up faeces from the soil. P. hominis was detected for the fi rst time in dogs in Croatia, and it might be a causative agent of the clinical disease in puppies. Acknowledgments We thank the pet owners for the time spent fi lling out the questionnaire. Funding This research did not receive any specifi c grant from funding agencies, commercial or non-profi t organizations. Authors’ contributions SF conceived and designed the study, and wrote the manuscript together with IV. KTM, TA, and MP participated in collecting and analyzing the samples. They also revised the manuscript and made a substantial contribution to the interpretation of collected data. 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Kim YA, Kim HY, Cho SH, Cheun HI, Yu JR, Le SE: PCR detection and molecular characterisation of Pentatrichomonas hominis from feces of dogs with diarrhea in the Republic of Korea. Korean J Parasitol 2010, 48:9-13 31. Li WC, Gong PT, Ying M, Li JH, Yang J, Li H, Yang ZT, Zhang GC, Zhang XC: Pentatrichomonas hominis: fi rst isolation from the feces of a dog with diarrhea in China. Parasitol Res 2014, 113:1795-1801. 32. Brložnik M, Faraguna S, Slavec B, Kostanjšek R, Vergles Rataj A, Gr untar I: Pentatrichomonas hominis coinfection in a puppy from a Slovenian animal shelter. Slo Vet Zb 2016, 53: 229- 52 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia 33. Grellet A, Polack B, Feugier A, Boucraut-Baralon C, Grandjean D, Vandewynckel L, Cian A, Meloni D, Viscogliosi E: Prevalence, risk factors of infection and molecular characterisation of trichomonads in puppies from French breeding kennels. Vet Parasitol 2013, 197:418- 34. Rostami A, Sepidarkish M, Ma G, Wang T, Ebrahimi M, Fakhri Y, Mirjalali H, Hofmann A, Macpherson CNL, Hotez PJ, Gasser RB: Global prevalence of Toxocara infection in cats. Adv Parasitol 2020, 109:615-639. 35. Schwartz R, Bidaisee S, Fields PJ, Macpherson MLA, Macpherson CNL: The epidemiology and control of Toxocara canis in puppies. Parasite Epidemiol Control 2022, 16:e00232. 36. Traversa D: Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors 2012, 5:91-110. 37. Lee AC, Schantz PM, Kazacos KR, Montgomery SP, Bowman DD: Epidemiologic and zoonotic aspects of ascarid infections in dogs and cats. Trends Parasitol 2010, 26:155-161. 38. Despommier D: Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 2003, 16:265-272. 39. Rostami A, Riahi SM, Hofmann A, Ma G, Wang T, Behniafar H, Taghipour A, Fakhri Y, Spotin A, Chang BCH, Macpherson CNL, Hotez PJ, Gasser RB: Global prevalence of Toxocara infection in dogs. Adv Parasitol 2020, 109:561-583. 40. Nijsse R, Ploeger HW, Wagenaar JA, Mughini-Gras L: Toxocara canis in household dogs: prevalence, risk factors, and owners’ attitude towards deworming. Parasitol Res 2015, 114:561-569. 41. Sierra-Cifuentes V, Jiménez-Aguilar JD, Alzate-Echeverii A, Cardona-Arias JA, Ríos-Osorio LA: Prevalencia de parásitos intestinales en perros de dos centros de bienestar animal de Medellín y el oriente antioqueño (Colombia). Rev Med Vet 2015, 30:55-66. 42. Dubná S, Langrová I, Nápravník J, Vadlejch J, Pekár S, Fechtner J: The prevalence of intestinal parasites in dogs from Prague, rural areas, and shelters of the Czech Republic. Vet Parasitol 2007, 145:120-128. 43. Martínez-Carrasco C, Berriatua E, Garijo M, Martínez J, Alonso FD, Ruiz de Ybáñez R: Epidemiological study of non-systemic parasitism in dogs in Southeast Mediterranean Spain assessed by coprological and post-mortem examination. Zoonoses Public Health 2007, 54:195-203. 44. Volkman M, Steiner JM, Fosgate GT, Zentek J, Hartman S, Kohn B: Chronic diarrhea in dogs – retrospective study in 136 cases. J Vet Intern Med 2017, 31:1043-1055. PREVALENCIJA CREVNIH PARAZITA KOD PASA I MAČAKA IZ REGIONA KVARNERA Siniša FARAGUNA, Ivan VLAHEK, Kristina Tea MIOČIĆ, Tibor ANDREANSZKY, Marko PEĆIN Paraziti intestinalnog trakta pasa i mačaka mogu da utiču na njihovo zdravstveno stanje uz značajan rizik po javno zdravlje. Iz tog razloga, uspostavljanje efi kasnog programa treba da se zasniva na određivanju diverziteta, prevalencije kao i patognosti ovih para- 53 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 zita. Cilj ove studije je bio da se odredi prevalencija crevnih parazita kod pasa i mačaka kao i da se nastavi sa upoređivanjm infekcije kod mladih i odraslih životinja. Nalaz parazita u uzorcima fecesa obavljeno je korišćenjem metoda fl otacije i imunofl uores- cencije i to iz 320 uzoraka poreklom od pasa i 64 uzoraka poreklom od mačaka, iz Kvarnerskog regiona Hrvatske. Utvrđena je prevalencija svakog dokazanog parazita u uzorcima fecesa njihovih domaćina. Isto tako, obavljena je i analiza razlika u prevalen- ciji parazita između mladih i odraslih životinja. Utvrđeno je prisustvo parazita u uzor- cima poreklom od 32 psa i kod 34,4% mačaka. Ukupno je dijagnostikovano prisustvo 12 različitih vrsta parazita; kod obe vrste životinja ustanovljena je najveća prevalencija Giardia spp. koja je izazivala oboljenje kod 24,7% pasa i 18,8% mačaka. Prevalencija Cryptosporidium spp. je bila 18,4%, a prevalencija Toxocara cati 6,3%. Prevalencija Giardia spp., Cryptosporidium spp. i Cystoisospora spp. bila je značajno (P < 0,05) veća kod štenadi u poređenju sa odraslim psima. Pentatrichomonas hominis (P. hominis) je dokazan kod jednog šteneta. Pored toga što se radi o prvoj prijavi invazije sa P. hominis, može da se zaklju- či postojanje relativno velike prevalencije intestinalnih parazita kod pasa i mačaka u Kvarnerskom regionu Hrvatske što svakako predstavlja potencijalni zoonotski rizik. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Acta veterinaria de Gruyter

Prevalence of Intestinal Parasites in Dogs and Cats from the Kvarner Region in Croatia

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Acta Veterinaria-Beograd 2023, 73 (1), 41-54 UDK: 636.7/.8.09:616.99-084(497.5) DOI: 10.2478/acve-2023-0004 Research article PREVALENCE OF INTESTINAL PARASITES IN DOGS AND CATS FROM THE KVARNER REGION IN CROATIA 1 2* 3 Siniša FARAGUNA , Ivan VLAHEK , Kristina Tea MIOČIĆ , 4 5 Tibor ANDREANSZKY , Marko PEĆIN Research assistant, University of Zagreb, Faculty of Veterinary Medicine, Department of Pathophysiology, Zagreb, Croatia; University of Zagreb, Faculty of Veterinary Medicine, Department of Animal Breeding and Livestock Production, Zagreb, Croatia; Croatian Health Insurance Fund, 4 5 Rijeka, Croatia; Croatian Veterinary Institute, Department Rijeka, Rijeka, Croatia; University of Zagreb, Faculty of Veterinary Medicine, Clinic for Surgery, Orthopaedics and Ophthalmology, Zagreb, Croatia (Received 14 September 2022, Accepted 23 February 2023) Intestinal parasites of dogs and cats may affect their health with a signifi cant zoonotic risk to public health. Therefore, establishing an effi cient control program should pass through the determination of the diversity, prevalence, and pathogenicity of those parasites. This study aimed to determine the prevalence of intestinal parasites in dogs and cats and proceed to infection comparisons between young and adult animals. The detection of parasites in fecal samples was determined using fl otation and immunofl uorescent methods across 320 dogs and 64 cats from the Kvarner region in Croatia. The prevalence was calculated for each detected parasite in its host. Differences in prevalence between young animals and adults were analyzed. Parasites were detected in 32 dogs and 34.4% of cats. In total, 12 different genera were detected; Giardia spp. was the most prevalent parasite in both species, infecting 24.7% and 18.8% of investigated dogs and cats, respectively. Cryptosporidium spp. and Toxocara cati had a prevalence of (18.4%) and (6.3%), respectively. Prevalences of Giardia spp., Cryptosporidium spp., and Cystoisospora spp. were signifi cantly (P < 0.05) higher in puppies compared to adult dogs. Pentatrichomonas hominis (P. hominis) was detected in one puppy. In addition to the fi rst report of P. hominis, a relatively high prevalence of intestinal parasites in dogs and cats in the Kvarner region of Croatia was recorded, posing a potential zoonotic risk. Keywords: cats, Croatia, dogs, intestinal parasitic infection, prevalence INTRODUCTION Dogs and cats can harbour various intestinal parasites, which can cause gastrointestinal disturbances [1]. Many of these parasites have a zoonotic potential, posing a risk to the human population. Thus, epizootiological studies aimed to determine the presence and the prevalence of parasites within pet populations represent a relatively simple, *Corresponding author: e-mail: ivlahek@vef.unizg.hr 41 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 effi cient, and useful source of information for practitioners in veterinary and human medicine. Common intestinal parasites in dogs and cats from the Middle-European region include protozoans like Giardia spp., Cryptosporidium spp., Sarcocystis spp., and Cystoisospora spp., roundworms Toxocara spp. and Toxascaris spp., hookworms Ancylostoma spp. and Uncinaria spp., whipworm Trichuris vulpis, bladder worm Capillaria plica and fl atworms Dipylidium spp. and Taenia spp. [2,3]. These parasites are considered signifi cant as they might cause diarrhoea and malabsorption in their hosts. In young dogs and cats, some parasites are responsible for weight loss and the normal development of an animal. In clinical cases, severe dehydration and even death can occur [4]. Commonly, the most prevalent intestinal parasites in dogs and cats are protozoans, especially Giardia, which explains the importance of the research on its zoonotic and epizootiological potential [5]. A study showed that the prevalence of giardiasis in humans is generally low in developed countries compared to developing countries [6]. Poor hygiene, low standards, and overcrowding may play an important role as possible zoonotic factors in transmission by cohabiting pet dogs [7]. Undisposed dog faeces positive for zoonotic and non-zoonotic intestinal parasites and environmental contamination have been reported in city parks, which make them potential sources of protozoan and worm infections for dogs and humans [8]. In another study, authors found a signifi cant association between dogs who attended parks and Giardia spp./Cryptosporidium spp. infection [9]. Also, public shelters present a signifi cant source of infection due to close cohabitation and poor hygienic conditions [2]. The constant presence of zoonotic intestinal parasites in dogs and cats indicates the need for planned, systematic, and adequate parasite control programs, which would ultimately positively affect human health. One of the fi rst steps towards this goal should be a precise and detailed determination of the parasites’ diversity, prevalence, and pathogenicity. The aim of this study was to determine the presence and prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia through coprological analyses. Furthermore, the prevalence of multiple infections and the differences in the number of infections between young and adult dogs and cats were assessed. MATERIALS AND METHODS Ethical statement This research is not related to the use of animals. No ethical approval was obtained because this study did not involve animals but only non-invasive procedures (collecting faecal samples from the environment). 42 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Animals and sampling A total of 384 fecal samples were collected between January 2019 and January 2021 from privately owned dogs (n=293; 138 females and 155 males) and 27 dogs from one shelter (19 females and eight males), and privately owned cats (n=64; 38 females and 26 males) from different parts of Kvarner region for a coprological examination. Basic information on examined dogs and cats is summarised in Table 1 and Table 2, respectively. Collected samples represented a mixture of clinically healthy animals and animals demonstrating clinical symptoms indicative of intestinal parasitism (e.g. diarrhoea, failure to gain weight) [10]. Table 1. Basic demographics of the dogs (N = 320) whose feces were examined Breed 187 mix breed; 35 unknown; 98 pure breeds (4 Cane Corso, 7 Maltese, 1 English bulldog, 5 German shepherd, 13 Labrador retriever, 1 Pitbull, 3 Bichon Frise, 5 Poodle, 4 Bernese Mountain, 3 Afghan hound, 8 Golden retriver, 3 German spitz, 5 Beagle, 2 Dalmatian, 1 German boxer, 1 Shar-pei, 2 Welsh Corgi, 2 West Highland White Terrier, 1 Greater Swiss Mountain, 2 Vizsla, 2 German short-haired pointer, 4 Cocker spaniel, 3 Irish setter, 1 Great Dane, 2 Miniature Schnauzer, 1 Siberian Husky, 1 Cavalier King Charles Spaniel, 1 Dogo Argentino, 1 Posavac Hound, 1 Dachshund, 4 Pugs, 1 Istrian short-haired hound, 2 Basset Hound, 1 English Cocker Spaniel and 1 Chihuahua) Age 78 ≤ 6 months, considered as puppy; 207 > 6 months, considered as adult dogs; 35 unknown Gender 163 male and 157 female Use of anthelmintics YES: 249 dogs ; NO: 36 dogs; UNKNOWN: 35 dogs (if any) 162 dogs ≤ 6 months; 87 dogs > 6 months Dogs from animal 27 dogs from animal shelter; 293 household dogs shelters/household dogs N – total number of samples Table 2. Basic demographics of the cats (N = 64) whose feces were examined Breed 54 mix breed; 10 pure breeds ( 3 Maine coon, 2 Persian cat, 3 British Shorthair, 1 Sphynx, 1 Russian Blue) Age 11 ≤ 6 months, considered as kittens; 49 > 6 months, considered as adult cats; 4 unknown Gender 26 male and 38 female Use of anthelmintics (if any) YES: 49 cats; NO: 15 cats 23 cats ≤ 6 months; 26 cats > 6 months Household cats 64 household cats N – total number of samples For parasitological examination, dogs and cats were divided into two groups to test the possible relationship between age and the presence or absence of parasitism. Dogs 43 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 and cats were classifi ed as puppies/kittens (≤ six months of age) and adults ( > six months of age). The apparent prevalence of infections was calculated by dividing the number of animals diagnosed with a parasite on fecal examination by the total number of fecal examinations performed for each age group. Questionnaire survey Owners who participated in this study were asked to provide additional information in a questionnaire that contained questions on data of age, sex, breed, previous dehelmintisation, recent clinical symptoms consistent with intestinal parasitism, history of diagnosed intestinal parasites in the past, and stool consistency [11]. For 35 dogs and four cats, the age was unknown. Collection and storage All fecal samples (10 – 20 g approximately) were collected from the ground immediately after defecation by the instructed owners in a provided labelled, clean plastic cup and stored in a refrigerator at +4 °C. Microscopic examination was performed up to 48 hours after sample collection. Methods Parasitological examination. Firstly, a macroscopic examination of all samples for detecting proglottids of cestodes was performed. All admitted samples were divided into two parts of approximately 5-7 g each (if available). Each part was analysed in the diagnostic laboratory of the Croatian Veterinary Institute, Department Rijeka, with two different diagnostic methods: (1) standardised fl otation method with saturated sodium chloride solution (specifi c gravity 1.2) [12] and (2) commercially available MERIFLUOR® Cryptosporidium/Giardia kit (Meridian Bioscience, Inc., SAD) by direct immunofl uorescent detection procedure according to the manufacturer’s instructions for simultaneous detection of Cryptosporidium spp. oocysts and Giardia spp. cysts by immunofl uorescence assay. Morphological determination. The sample was considered positive if at least one test showed a positive result based on morphological keys [13]. The species of parasites found were microphotographed and then classifi ed according to genus, including Giardia, Cryptosporidium, Cystoisospora, Pentatrichomonas, Toxocara, Toxascaris, Trichuris, Capillaria, Ancylostoma, Uncinaria, Dipylidium, and Taenia. Molecular diagnosis. For the exact diagnosis of trichomoniasis, parasite DNA was extracted using the QIAamp® Mini Kit (Qiagen, Hilden, Germany), according to the manufacturer’s instructions. Further molecular diagnosis, including PCR, gel electrophoresis, DNA purifi cation, and sequencing were done according to Felleisen, 1997. protocol [14]. 44 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Statistical analysis Data were analysed using the statistical program TIBCO Statistica® [15]. Fisher exact test was used to determine the statistical signifi cance of the differences in the prevalences of intestinal parasitic infections between young and adult dogs and cats. The confi dence level was set at 95%, and the results were considered signifi cant if P < 0.05. RESULTS Dogs Parasitic forms were detected in 103 of 320 (32.2%) dogs with a 95% confi dence interval (95% CI) of 27.1 - 37.6. Overall, 11 intestinal parasite species/genera were identifi ed with fl otation and direct immunofl uorescent methods (Table 3). Table 3. Proportions of single and multiple parasitic infection in dogs n. positive Endoparasite infections 95% CI (prevalence) Single endoparasite infections Ancylostoma spp. 2 (0.6%) 0.08-2.2 Capillaria spp. 3 (0.9%) 0.2-2.7 Toxascaris leonina 4 (1.3%) 0.3-3.2 Toxocara canis 11 (3.4%) 1.7-6.1 Trichuris vulpis 3 (0.9%) 0.2-2.7 Uncinaria stenocephala 1 (0.3%) 0.01-1.7 Dipylidium caninum 1 (0.3%) 0.01-1.7 Giardia spp. 79 (24.7%) 20.1-29.8 Isospora spp. 8 (2.5%) 1.1-4.9 Cryptosporidium spp. 59 (18.4%) 14.3-23.1 Pentatrichomonas hominis 1 (0.3%) 0.01-1.7 Mixed endoparasitic infections Isospora spp.+ Giardia spp. 5 (1.6%) 0.5-3.6 Toxocara canis + Capillaria spp. 2 (0.6%) 0.08-2.2 Giardia spp. + Cryptosporidium spp. 18 (5.6%) 3.4-8.7 Isospora spp. + Pentatrichomonas hominis 1 (0.3%) 0.01-1.7 Toxocara canis + Giardia spp. 1 (0.3%) 0.01-1.7 Trichuris vulpis + Toxocara canis 1 (0.3%) 0.01-1.7 Giardia spp.+ Uncinaria stenocephala 1 (0.3%) 0.01-1.7 Trichuris vulpis + Toxocara canis + Toxascaris leonina 1 (0.3%) 0.01-1.7 n – number of positive samples, CI – confi dence interval 45 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 The most common parasites were Giardia spp. and Cryptosporidium spp. Mixed infections were detected in 30 dogs, of which 18 had coinfection with Giardia spp. and Cryptosporidium spp. parasites. Overall prevalence in puppies and adults was 89.7% (95% CI = 80.8-95.5) and 47.3% (95% CI = 40.4-54.4), respectively. Ancylostoma spp., Trichuris vulpis, and Dipylidium caninum were detected only in adult dogs, while Uncinaria stenocephala and Pentatrichomonas hominis were detected only in puppies (Table 4). Puppies had a signifi cantly (P < 0.05) higher prevalence of Giardia spp., Cystoisospora spp., and Cryptosporidium spp. parasites compared to adult dogs (Table 4). There was no signifi cant difference (P > 0.05) between the prevalence in male (35.8%; 95% CI = 28.4-43.7) and female (28.5%; 95% CI = 21.6-36.2) dogs. The pooled prevalence of Giardia spp. and Cryptosporidium spp. was 43.1% (CI = 37.6-48.8). Table 4. Prevalence of endoparasites in dogs according to age Age category Puppy (≤6 mo) Adult (>6 mo) Parasite P-value N = 78 N = 207 n Prev. 95% CI n Prev. 95% CI Ancylostoma spp. / / / 2 1.0% 0.1-3.5 / Capillaria spp. 1 1.3% 0.03-6.9 2 1.0% 0.1-3.5 0.618 Toxascaris leonina 1 1.3% 0.03-6.9 3 1.5% 0.3-4.2 0.698 Toxocara canis 2 2.6% 0.3-9.0 9 4.4% 2.0-8.1 0.381 Trichuris vulpis / / / 3 1.5% 0.3-4.2 / Uncinaria stenocephala 1 1.3% 0.03-6.9 / / / / Dipylidium caninum / / / 1 0.5% 0.01-2.7 / Giardia spp. 33 42.0% 31.1-54.0 44 21.3% 15.9-27.5 0.001 Isospora spp. 5 6.4% 2.1-14.3 3 1.5% 0.3-4.2 0.038 Cryptosporidium spp. 26 33.3% 23.1-44.9 31 15.0% 10.4-20.6 0.004 Pentatrichomonas hominis 1 1.3% 0.03-6.9 / / / / p<0.05, N – total number of samples, n – number of positive samples, CI – confi dence interval, Prev – prevalence Cats Twenty-two of 64 (34.4%; 95% CI = 23.0-47.3) investigated cats were infected with intestinal parasites. Seven different intestinal parasite species/genera were identifi ed with fl otation and direct immunofl uorescent methods, of which Giardia spp. and Toxocara cati were the most prevalent (Table 5). Infection with two parasites was detected in fi ve cats (Table 5). Overall prevalence in kittens and adult was 27.3% (95% CI = 6.0-61.0) and 38.8 (95% CI = 25.2-53.8), respectively. In kittens, only Giardia spp. was found, which also had the highest prevalence in adult cats (Table 6). There was no signifi cant difference (P > 0.05) between the prevalence of intestinal parasites in male (24.0%; 95% CI = 9.4-45.1) and female (27.5%; 95% CI = 14.6-43.9) cats. 46 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Table 5. Proportions of single and multiple parasitic infection in cats n. positive Endoparasite infections 95% CI (prevalence) Single endoparasite infections Capillaria spp. 1 (1.6%) 0.04-8.4 Toxocara cati 4 (6.3%) 1.7-15.2 Dipylidium caninum 1 (1.6%) 0.04-8.4 Taenia spp. 2 (3.1%) 0.4-10.8 Giardia spp. 12 (18.8%) 10.1-30.5 Isospora spp. 1 (1.6%) 0.04-8.4 Cryptosporidium spp. 1 (1.6%) 0.04-8.4 Mixed endoparasitic infections Toxocara cati + Giardia spp. 2 (3.1%) 0.4-10.8 Toxocara cati + Capillaria spp. 1 (1.6%) 0.04-8.4 Isospora spp. + Dipylidium caninum 1 (1.6%) 0.04-8.4 Giardia spp.+ Cryptosporidium spp. 1 (1.6%) 0.04-8.4 n – number of positive samples, CI – confi dence interval Table 6. Prevalence of endoparasites in cats acording to age Age category Kitten (≤6 mo) Adult (>6 mo) Parasite P-value N = 11 N = 49 n Prev. 95% CI n Prev. 95% CI Capillaria spp. / / / 1 2.0% 0.05-10.9 / Toxocara cati / / / 4 8.2% 2.3-19.6 / Dipylidium caninum / / / 1 2.0% 0.05-10.9 / Taenia spp. / / / 2 4.1% 0.5-14.0 / Giardia spp. 3 27.3% 6.0-61.0 9 18.4% 8.8-32.0 0.382 Isospora spp. / / / 1 2.0% 0.05-10.9 / Cryptosporidium spp. / / / 1 2.0% 0.05-10.9 / p<0.05, N – total number of samples, n – number of positive samples, CI – confi dence interval, Prev – prevalence DISCUSSION Data on the prevalence of intestinal parasites in dogs and cats from Croatia are scarce. Thus, the primary aim of this study was to determine the prevalence of intestinal parasitic infection in a Croatian population of dogs and cats using the fl otation and direct immunofl uorescent method. Twelve different genera of intestinal parasites were found, and 32.2% of the examined dogs and 28.1% of the cats were infected. These fi ndings correspond with the large-scale analysis in Germany, which found 47 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 that 32.2% of the dogs and 24.3% of the cats had intestinal parasites [16]. A larger overall prevalence of intestinal parasites in dogs from the Zagreb area, Croatia (48.1% - 64.9%) was reported in 2017 [17]. In our study, protozoan parasites were the most prevalent, and 5.6% of dogs had both Giardia spp. and Cryptosporidium spp. infections. In this research, Giardia spp. was the most common parasite in dogs and cats. These results are in agreement with the report, which found Giardia spp. to be the most prevalent parasite in dogs (20.2%) and cats (36.0%) in Slovakia [3]. In a previous study in Zagreb, the prevalence of this parasite in dogs ranged between 23.8 and 26.7% [17]. Similarly, the prevalence of Giardia spp. was 28.47%, 23.75%, 25.1%, 27.53%, 25.89%, and 24.62% in dogs from Belgium, Germany, Spain, France, Italy, and the Netherlands, respectively [18]. However, our research used the direct immunofl uorescence test for Giardia spp. detection, a more sensitive method than the SNAP Giardia test. A lower prevalence (7.0%) of Giardia spp. was detected in household and sheltered dogs from Central Italy [19]. In this research, puppies were more likely ( P < 0.05) to have Giardia spp. than adults, which is consistent with the results of a similar previous study conducted in Colombia [1]. Also, Giardia spp. was the only parasite found in kittens. Regardless of clinical signs, Giardia spp. is ubiquitous in dogs and cats [20,21]. Considering that it has a zoonotic potential [22] and that prevalence of giardiasis in dogs can reach up to 43.9% [23], its zoonotic risk should not be overlooked. Cryptosporidium spp. has been found in dogs and cats with different prevalences, and its presence can be associated with diarrhoea [24,25,20]. In this study, it was the second most prevalent parasite (18.4%) in dogs. The results in the Zagreb area between 2012 and 2015 stated that the prevalence of Cryptosporidium spp. in dogs ranged between 8.0% and 18.7% [17]. One meta-analysis showed that the pooled prevalence of Cryptosporidium spp. in the world is 8% and 3% in Europe, which indicates that the prevalence of this parasite in Croatia is relatively high [26]. Puppies seem twice as likely (P < 0.05) to have it than adults. High-level infection in puppies could be explained by the fact that the immune system of young animals is not fully developed [27,28]. A contributing factor to the high prevalence of Cryptosporidium spp., as well as of Giardia spp., might be the frequent contact with other animals from different epizootiological areas during tourist season. Kvarner region is a well-known tourist destination where tourists will likely arrive with their pets from different regions of Europe and the world. Data about coccidian prevalence in Europe is scarce. In this study, Cystoisospora spp. was detected in adult cats and in both age categories of dogs. Moreover, signifi cant (P < 0.05) differences were observed between the prevalence in puppies and adult dogs, with puppies being the more exposed group. This is in agreement with the research that found that the prevalence of Cystoisospora spp. in dogs signifi cantly declined after four months of age [4]. [29] reported a higher prevalence of Isospora felis in cats younger than six months (9%) compared to older cats (2%). However, all investigated cats in their research showed symptoms of gastrointestinal disease. 48 Faraguna et al.: Prevalence of intestinal parasites in dogs and cats from the Kvarner region in Croatia Pentatrichomonas hominis (P. hominis) was found in one puppy, along with the Cystoisospora spp. The puppy had soft, malodorous diarrhoea. Several studies reported similar clinical signs in young dogs infected with this parasite [30,31,32]. Even though one study reported the prevalence of P. hominis in puppies from French kennels to be 15.8%, it is relatively rarely diagnosed in dogs and cats [33]. One reason for this might be that for its detection, highly specifi c and sensitive PCR assays need to be used [32]. However, due to its zoonotic potential, P. hominis may represent a serious health problem, and it is important to control its prevalence in domestic animal populations. To the best of our knowledge, this is the fi rst report that P. hominis is involved in clinical diseases of dogs in Croatia. Toxocariasis is one of the most common zoonotic parasitic infections worldwide [34,35]. As reported in a study, its prevalence can reach up to 33.5% in young sheltered dogs [2]. One of the most important sources of ground contamination with T. canis is free-roaming dogs [36], and human infection is possible by lying on the contaminated grass or soil [37]. Although most human infections with T. canis are subclinical, they may also cause severe clinical symptoms due to larval migration [38]. In this study, the prevalence of T. canis and T. cati was 3.4% and 6.3%, respectively. These results were lower than expected since the worldwide pooled prevalence of T. canis, and T. cati reported in large meta-analyses was 11.1% and 17.0%, respectively [34,39]. The relatively low prevalence of T. canis and T. cati in this study may be the result of concerned pet owners being under continuous veterinary control, with a higher degree of care and preventative measures. Indeed, 87% of dog owners (who answered that question) and 77% of cat owners stated that their pets were treated with anthelmintics. Similar prevalences to those obtained in this study were reported [11,17,1]. Even though young age is recognized as a risk factor for toxocariasis in dogs [40], results from this study showed non-signifi cant (P > 0.05) differences in prevalences regarding age. In this study, hookworms (Ancylostoma spp. and Uncinaria stenocephala) and Trichuris vulpis (T. vulpis) were found in 0.6%, 0.3%, and 0.9% of dogs, respectively. Eggs of Ancylostoma spp. and T. vulpis were found in adult dogs, while Uncinaria stenocephala was found in one puppy. Similar prevalence was reported in a study from Germany [11], although reports from South America stated that T. vulpis [41] and Ancylostoma spp. [1] were the second most common parasites in dogs, with a prevalence of 16.2% and 12.6%, respectively. However, one study reported a prevalence of hookworms of 0.7 – 0.9% in rural dogs and 0.4% in urban dogs in the Czech Republic [42]. The low prevalence of Ancylostoma spp., Uncinaria stenocephala, and T. vulpis might be due to regular dehelminthisation, or the samples might be taken in the prepatent period of the infection. The prevalence of the Taeniidae and Dipylidiidae parasites was: 0.3% for D. caninum in dogs and 1.6% in cats, while 3.1% of cats had Taenia spp. All parasites were determined in adults. Relatively low prevalences of D. caninum and Taenia spp. determined by fecal 49 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 examination in this study probably do not represent the true prevalence, mainly because of the excretion behavior of the cestodes. Indeed, one study reported that cestodes were found in 1% of dogs after coprological examination, while post-mortem analysis revealed 46% of tapeworm-infected dogs [43]. Thus, in this study, the real prevalence of cestode infections in dogs and cats is probably much higher than recorded. This study had a few limitations. Firstly, Giardia spp. is probably underestimated due to the intermittent excretion of Giardia cysts. Examination of just one fecal sample, as was done in this study, may produce false-negative results and underestimates the true prevalence value. This may also apply to the results for tapeworm prevalence. In this study, a fl otation method with a saturated sodium chloride solution was used to detect Taenia spp. In contrast, the most common method is fl otation with a saturated solution of zinc sulphate. The second limitation was poor anamnesis provided by the owners in the questionnaire, particularly in describing the presence and the character of diarrhoea. If the information were provided, it could aid in interpreting the laboratory fi ndings, as the causes of diarrhoea are not always infectious. Some authors stated that most cases of chronic diarrhoea in dogs are not infectious but rather infl ammatory enteropathies that are food, antibiotic, or steroid responsive [44]. CONCLUSION This study showed a considerably high prevalence of intestinal parasites in dogs and cats in the Kvarner region, Croatia. Findings may indicate a potential zoonotic risk, especially in the case of Giardia spp., Cryptosporidium spp., and Toxocara spp., which in this study were the most prevalent parasites. The investigated population of dogs and cats is well-cared, but the higher occurrence of detected Giardia spp. advocates the need for more effective deworming schemes, regular faecal examinations, and cleaning up faeces from the soil. P. hominis was detected for the fi rst time in dogs in Croatia, and it might be a causative agent of the clinical disease in puppies. Acknowledgments We thank the pet owners for the time spent fi lling out the questionnaire. Funding This research did not receive any specifi c grant from funding agencies, commercial or non-profi t organizations. Authors’ contributions SF conceived and designed the study, and wrote the manuscript together with IV. KTM, TA, and MP participated in collecting and analyzing the samples. They also revised the manuscript and made a substantial contribution to the interpretation of collected data. 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Martínez-Carrasco C, Berriatua E, Garijo M, Martínez J, Alonso FD, Ruiz de Ybáñez R: Epidemiological study of non-systemic parasitism in dogs in Southeast Mediterranean Spain assessed by coprological and post-mortem examination. Zoonoses Public Health 2007, 54:195-203. 44. Volkman M, Steiner JM, Fosgate GT, Zentek J, Hartman S, Kohn B: Chronic diarrhea in dogs – retrospective study in 136 cases. J Vet Intern Med 2017, 31:1043-1055. PREVALENCIJA CREVNIH PARAZITA KOD PASA I MAČAKA IZ REGIONA KVARNERA Siniša FARAGUNA, Ivan VLAHEK, Kristina Tea MIOČIĆ, Tibor ANDREANSZKY, Marko PEĆIN Paraziti intestinalnog trakta pasa i mačaka mogu da utiču na njihovo zdravstveno stanje uz značajan rizik po javno zdravlje. Iz tog razloga, uspostavljanje efi kasnog programa treba da se zasniva na određivanju diverziteta, prevalencije kao i patognosti ovih para- 53 Acta Veterinaria-Beograd 2023, 73 (1), 41-54 zita. Cilj ove studije je bio da se odredi prevalencija crevnih parazita kod pasa i mačaka kao i da se nastavi sa upoređivanjm infekcije kod mladih i odraslih životinja. Nalaz parazita u uzorcima fecesa obavljeno je korišćenjem metoda fl otacije i imunofl uores- cencije i to iz 320 uzoraka poreklom od pasa i 64 uzoraka poreklom od mačaka, iz Kvarnerskog regiona Hrvatske. Utvrđena je prevalencija svakog dokazanog parazita u uzorcima fecesa njihovih domaćina. Isto tako, obavljena je i analiza razlika u prevalen- ciji parazita između mladih i odraslih životinja. Utvrđeno je prisustvo parazita u uzor- cima poreklom od 32 psa i kod 34,4% mačaka. Ukupno je dijagnostikovano prisustvo 12 različitih vrsta parazita; kod obe vrste životinja ustanovljena je najveća prevalencija Giardia spp. koja je izazivala oboljenje kod 24,7% pasa i 18,8% mačaka. Prevalencija Cryptosporidium spp. je bila 18,4%, a prevalencija Toxocara cati 6,3%. Prevalencija Giardia spp., Cryptosporidium spp. i Cystoisospora spp. bila je značajno (P < 0,05) veća kod štenadi u poređenju sa odraslim psima. Pentatrichomonas hominis (P. hominis) je dokazan kod jednog šteneta. Pored toga što se radi o prvoj prijavi invazije sa P. hominis, može da se zaklju- či postojanje relativno velike prevalencije intestinalnih parazita kod pasa i mačaka u Kvarnerskom regionu Hrvatske što svakako predstavlja potencijalni zoonotski rizik.

Journal

Acta veterinaria – de Gruyter

Published: Mar 1, 2023

Keywords: cats; Croatia; dogs; intestinal parasitic infection; prevalence

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