Abstract
Relationship between humans and cats has negative impact associates with zoonotic diseases. It is the reason why studies on the prevalence of gastrointestinal (GI) parasites in cats are important. Some of zoonotic GI parasites in cats are Toxocara spp, Ancylostoma sp, and Toxoplasma gondii. The current study was conducted to investigate the prevalence of GI parasites in owned and stray cats in Lumajang East Java Indonesia. One hundred and twenty fecal samples were collected from owned and stray cats on November 2018 to January 2019. The samples were examined by direct smears, sedimentation and flotation techniques. Identification of parasites was determined based on the morphology of worm eggs and protozoan cysts. The results showed that gastrointestinal parasites were found in 68.33% (82/120) examined samples, respectively, 48.33% (29/60) and 88.33% (53/60) from owned cats and stray cats. We found 7 genera of parasites, 4 genera of worm eggs and 2 genera protozoan oocyst. The egg worm were Toxocara cati (40 %), Toxocara leonina. (10.33%), Ancylostoma sp. (18.33%), Diphylobothrium sp. (3.33%) and Dipylidium caninum (1.67%). The protozoan oocyst were Isospora felis (27.5%), Isospora rivolta (13.33%) and Eimeria spp. (8.33%). Toxocara cati, Ancylostoma sp. (hookworm), Diphylobothrium sp. and Dipylidium caninum were zoonotic parasites. Rate infection in younger and older cat were no significant difference. One cat can be infected one or more parasite. To conclude, the prevalence of zoonotic GI parasites both in owned and stray cats were high. It is necessary to plan a program to control this zoonotic parasites.
Key words: Gastrointestinal parasites, owned cat, stray cat, zoonotic parasite
Introduction
Cats are common pets in all countries. The close relationship between humans and cats has positive and negative impact. Negative impact associates with zoonotic diseases which can be dangerous for human health. Domestic cats and also wild felids are a potential source of a number of infectious disease agents such as several zoonotic parasites,1 while another reseacher reported that stray cats can act as potential sources of soil contamination with zoonotic parasites.2
The gastrointestinal (GI) parasites are cosmopolitan pathogens and some species of parasite are zoonotic. For promoting public health protection, many researchers in the world have been interested in the epidemiology of GI parasites in cats, including in Egypt,3 in Europe,4 in Iran,5 in China6 in Serbia,7 and in Poland.2 They found parasites such as Toxocara sp, Toxascaris leonina, Ancyloastoma sp, Trichuris sp, Dipylidium caninum, Taenia sp, Capillaria spp, Paragonimus sp, Cystoisospora sp, Toxoplasma gondii, Sarcocyst spp, Isospora spp., Blastocystis sp. and Giardia sp.2-7
Considering the role of parasites in human beings and domestic animals helath, therefore this study aimed to estimate the prevalence of GI parasites, including the zoonotic parasites in owned and stray cats in Lumajang, East Java, Indonesia. This knowledge is important to formulate the effectively zoonotic disease control program.
Materials and Methods
Sample Collection
Collecting samples were carried out on November 2018 to January 2019. One hundred and twenty fecal samples were collected from 60 owned and 60 stray cats in Lumajang, East Java, Indonesia. Term of owned cat is a household cat that lives in housing and is maitained by the owner, while stray cat is domestic cat that lives in market and has no owner. Stray cats were caught and caged by reseacher. During the first defecation of the owned cat, excrement was collected by the owner at the house, while stray cat was collected by reseacher. The faeces was placed into a disposable plastic container with 5% formalin for fixation worm egg and 2,5% potassium dichromat for fixation protozoan cysts and all of samples were stored at about 4oC for examination. Data such as the age and gender of cats were recorded.
Parasites Examination
All cat faeces were transported to Department of Veterinary Parasitology, Faculty of Veterinary Medicine Universitas Airlangga for examination. The samples were evaluated by direct wet smears, sedimentation and sugar fluotation method. Direct wet smears were observed by put faeces on slide with a drop of aquades and directly the prepared slides were examined under light microscope at 100x and 400x magnification.
Sedimentation and sugar fluotation method. Faeces samples were diluted with aquades (1:9) and then were filtered. Filtrat was centrifugated 1500 rpm for 5 min and supernatant was discharge. This step was repeated until supernatant was clear. A small of sediment was put on slide with a drop of aquades and was examined under light microscope. Remaining sediment was added with sugar solution and was centrifugated 1500 rpm for 5 min. Centrifuge tube was put on the rack and was added sugar solution until full and the solution sugar covered mouth of tube. Tube was covered by covee slip and was waited for 5 min. Cover slip was took and put on slide and examined under light microscope at 100x and 400x magnification.
Parasites were identified based on morphological and morphometric features of worm eggs and protozoan (oo) cysts. The overall prevalence of gastrointestinal parasites was estimated as the number of cats found to be positive for the presence at least one species of parasite divided by the total number of cats examined. The prevalence of each parasite was calculated as the number of infected individuals over the total number of cats examined.
Statistical Analysis
The comparison between between kind and age of cats were carried out using the Chi-squared test with program SPSS (Statistical Package for Social Sciences). The statistical significance was difined if values of P<0.05.
Results
Of the 120 faecal samples, 68.33% (82/120) were positive constaining at least one species of GI parasite. The prevalence of parasites in stray cats was higher than in owned cats, 88.33% (53/60) for stray cats and 48,33% (29/60) for owned cats (Table 1).
A total of 8 species of GI parasite were identified microscopically both in owned cat and stray cat faeces, 5 species of worm and 3 species of protozoan (Table 2.). That parasites in both owned and stray cats, respectively, were Toxocara cati (18.33% or 11/60 and 61.67% or 37/60), Toxocaris leonina (3.33% or 2/60 and 18,33% or 11/60), Ancylostoma sp. (11.67% or 7/60 and 25% or 15/60), Diphylobothrium sp. (5% or 3/60 and 1.67% or 1/60), Dipylidium caninum (3.33% or 2/60 and 0%), Isospora felis (15% or 9/60 and 40% or 24/60), Isospora rivolta (8.33% or 5/60 and 18.33% or 11/60) and Eimeria spp. (5% or 3/60 and 11.67% or 7/60). And overall, the prevalence of intestinal parasites in the younger (< 1 year) and older (≥ 1 year) cats had no significant difference.
One cat can infect by single or mix parasites and the cats frequently mix infected two parasite species or three, even four parasite species. In this study, mix parasites infections were observed in the owned and stray cat populations (Table 3). Toxocaris leonina and D. caninum eggs and Eimeria sp oocyst always found together with other species. Toxocaris leonina always together with T. cati. D. caninum egg and Eimeria sp oocyst especially together with Ancylostoma sp.
Discussion
The prevalence GI parasite infection in cat in Lumajang was high (68.33%) which in stray cats was higher (88.33%) than in owned cats (48.33%). With these intersting results, the author assumed that owned cats get better care by their owners, while stray cats find own food and often scavenge garbage. The prevalance of GI parasites infections both in stray cats and owned cats in Lumajang Indonesia was very high. The high prevalence of GI infection in cats, aspecially in stray cats, also reported by previous reseachers. Epidemiological studies have confirmed that stray cat populations are a very important reservoir of worm and protozoan parasites and stray cats are as potential sources of soil contamination with zoonotic parasites.2 The prevalence of GI parasite infection in stray cats in Iran 95.6% and 86.4%5,8 and in Egypt 91%3. The prevalence in in owned cat in Europe 50.7%,4 in China 41.39 %6 and in Serbia 40.19%.7
Table 1.
The prevalance of infections with gastrointestinal parasites in faecal examined cats.
| Cat | Parasite | Location | Total | ||
|---|---|---|---|---|---|
| North | Center | South | |||
| Owned Cat | Worm | 3/20 | 4/20 | 8/20 | 29/60 |
| (15%) | (20%) | (20%) | (48.33%) | ||
| Protozoa | 4/20 | 3/20 | 3/20 | ||
| (20%) | (15%) | (15%) | |||
| Worm and Protozoal | 0 | 1/20 | 3/20 | ||
| (20%) | (15%) | ||||
| Stray Cat | Worm | 9/20 | 4/20 | 6/20 | 53/60 |
| (45%) | (20%) | (30%) | (88.33%) | ||
| Protozoa | 0 | 4/20 | 2/20 | ||
| (20%) | (10) | ||||
| Worm and Protozoal | 9/20 | 12/20 | 7/20 | ||
| (45%) | (60) | (35%) | |||
| Total | 25/40 | 28/40 | 29/40 | 82/120 | |
| (62.5%) | (70%) | (72.5%) | (68.33%) |
Table 2.
The prevalence of each species of gastrointestinal parasites in faecal examined cats.
| Parasite | No of cat positive (%) | Total (n=120) | |||||
|---|---|---|---|---|---|---|---|
| Owned Cat (n=60) | Stray Cat (n=60) | ||||||
| ˂ 1 th | ≥ 1th | Total | ˂ 1 th | ≥ 1 th | Total | ||
| Toxocara cati. | 5(8.33) | 6 (10 ) | 11(18.33) | 18(30) | 19(31.67) | 37 (61.67 ) | 48(40) |
| Toxascaris leonina | 1(1.67) | 1(1.67) | 2 (3.33) | 4(6.67) | 7(11.67) | 11(18.33) | 13(10.33) |
| Ancylostoma sp. | 2(3.33) | 5(8.33) | 7(11.67) | 4(6.67) | 11(18.33) | 15(25) | 22(18.33) |
| Diphylobothrium sp. | 2 (3.33) | 1(1.67) | 3 (5 ) | 0 | 1(1.67) | 1(1.67) | 4(3.33) |
| Dipylidium caninum | 0 | 2(3.33) | 2 (3.33) | 0 | 0 | 0 | 2(1.67) |
| Isospora felis. | 6 (10 ) | 3 (5 ) | 9 (15 ) | 11(18.33) | 13(21.67) | 24(40) | 33(27.5) |
| Isospora rivolta | 1(1.67) | 4(6.67) | 5 (8.33 ) | 5(8.33) | 6 (10 ) | 11(18.33) | 16(13.33) |
| Eimeria spp. | 2(3.33) | 1(1.67) | 3 (5 ) | 4(6.67) | 3(5) | 7(11.67) | 10(8.33) |
In this research, four of 5 worm were zoonotic parasites, including, Toxocara cati, Ancylostoma sp., Diphylobothrium sp. and Dipylidium caninum. Toxocara cati was the most common parasite found in both owned and stray cat faeces, 18.33% (11/60) and 61.67% (37/60), respectively. According to,2 Toxocara was an important zoonotic risk that cause larva migrans syndromes and ocular toxocarosis for the human population, especially children. Their research reported that the prevalence of T. cati in stray cats was found to be 27.9 % in Poland. Reseacher from Europe and China also reported that T. cati was dominant parasite infected 19.7% and 17.78% of household cats, respectively.4,6
In this study, Ancylostoma sp. or hookworm was the second zoonotic parasites in cats after T. cati. The prevalence of hookworm in owned cats was 11.67% (7/60), while in srtay cats was 25% (15/60). Several reports of human infections by feline hookworm infections have been reported from soil contaminated cats faeces.1 Hookworm eggs hatch develop to become infective (filariform) larvae that can penetrate the skin of animals or human hosts. Hookworm is one of the four most common soil-transmitted helminths (STH). STH have been documented as causing impairment of growth and nutrition because it causes to damage the intestinal mucosa leading to bleeding, loss of iron and anemia.9
Other species worm that infected cats in these study was Toxocaris leonina. The prevalence was (10.33%) and it was lower than in Korean (31.5%)10. Human infection by T. leonina has not been reported,11 it is non zoonotic worm.
Diphylobothrium sp. and Dipylidium caninum was encountered with low prevalence in comparison with other species. Diphylobothriid typeworm also found very low prevalence (0.2%) in ferral cats in Korea.12 Diphylobothrium sp can infect cat or human by eating raw or undercooked fish. Fish infected with Diphyllobothrium larvae may be consumed in any country in the world. The prevalence of D. caninum infection in stary cats in Egypts was lower (5%),3 while in Iran was lowest (2.9%).5
In recent study, all of protozoan were non zoonotic parasite, they were 27.5%, 13.33% and 8.33% for Isospora felis, I. rivolta and Eimeria sp, respectively. These findings were lower than prevalence in China and Italy.6,13 In China the prevalance I. felis and I. rivolta infection in cat, respectively, were 11.39% and 9.17%,6 while in Italy were 3% and 2.3% and they did not found Eimeria sp. Isospora felis and I. rivolta appear to be non pathogenic for cats.6
The prevalence of intestinal parasites in the younger (<1 year) and older (≥1 year) cats had no significant difference. These finding was similar with result reseach in China,6 but different with report in Italy13 which reported that parasite infections were identified in significantly more cats younger than 18 months of age (P<0.05), and most often associated with the presence of compatible clinical signs (P<0.05).
As well as the results of this study that found one cat can infect by single or mix parasites and the cats frequently mix infected two parasite species or three, even four parasite species, many researcher also reported it.3,6 Indeed, 81.3% domestic cats in Ode – Irele and Oyo communities, Southwest Nigeria were reported that they were infected with two or more parasites.14
Table 3.
The prevalence of single and mixed parasaite infections in cats.
| Infection | The prevalence in cat (%) | Total | ||
|---|---|---|---|---|
| Owned Cat n=60 |
Stray Cat n=60 |
(n=120) | ||
| Single Parasite | Toxocara cati | 7 (11.67) | 8 (13.33) | 15 (12.5) |
| Ancylostoma sp. | 2 (3.33) | 6(10) | 8 (6.67) | |
| Diphylobothrium sp. | 2 (3.33) | 0 | 2 (1.67) | |
| I. felis | 5 (8.33) | 3(5) | 8 (6.67) | |
| I. rivolta | 3(5) | 1(1.67) | 4 (3.33) | |
| Mixed 2Parasite | T. cati; T. leonina | 2 (3.33) | 3(5) | 5 (4.17) |
| T. cati, Ancylostoma sp | 1(1.67) | 0 | 1 (0.83) | |
| T.cati, I. felis | 0 | 9(15) | 9 (7.5) | |
| T. cati, I. rivolta | 0 | 2 (3.33) | 2 (1.67) | |
| T. cati, Eimeria sp | 0 | 2 (3.33) | 2 (1.67) | |
| Ancylostoma sp., D. caninum | 1 (1.67) | 0 | 1 (0.83) | |
| Ancylostoma sp., Eimeria sp | 1 (1.67) | 0 | 1 (0.83) | |
| Ancylostoma sp., I.felis | 0 | 2 (3.33) | 2 (1.67) | |
| Ancylostoma sp., Diphylobothrium sp. | 0 | 1 (1.67) | 1 (0.83) | |
| Diphylobothrium sp., I. felis | 1 (1.67) | 0 | 1 (0.83) | |
| I. felis, I. rivolta | 2 (3.33) | 1 (1.67) | 3 (2.5) | |
| Mixed 3Parasite | T. cati, T. leonina, Ancylostoma sp. | 0 | 1 (1.67) | 1 (0.83) |
| T. cati, T. leonina, Eimeria sp | 0 | 2 (3.33) | 2 (1.67) | |
| T. cati, T. leonina, I. felis | 0 | 1 (1.67) | 1 (0.83) | |
| T. cati, T. leonina, I. rivolta | 0 | 2 (3.33) | 2 (1.67) | |
| T.cati, Ancylostoma sp., Eimeria sp. | 0 | 1 (1.67) | 1 (0.83) | |
| T. cati, Ancylostoma sp., I. felis | 0 | 1 (1.67) | 1 (0.83) | |
| T. cati, I. felis, I. rivolta | 0 | 2 (3.33) | 2 (1.67) | |
| Ancylostoma sp., I, felis, I. rivolta | 0 | 1(1.67) | 1 (0.83) | |
| Ancylostoma sp., Dipylidium caninum, Eimeria sp | 1 (1.67) | 0 | 1 (0.83) | |
| Mixed 4Parasite | T. cati, Ancylostoma sp, I. felis, Eimeria sp. | 1 (1.67) | 1 (1.67) | 2 (1.67) |
| T. cati, T. leonina, I. felis, Eimeria sp. | 0 | 1 (1.67) | 1 (0.83) | |
| T. cati, T. leonina, I. felis, I. rivolta | 0 | 1 (1.67) | 1 (0.83) | |
| T. cati, Ancylostoma sp., I. felis, I. rivolta | 0 | 1 (1.67) | 1 (0.83) | |
| Total | 29 (48.33) | 53(88.33) | 82 (68.33) | |
Conclusions
The prevalence of zoonotic gastrointestinal parasites both in owned and stray cats in Lumajang Indonesia were high. It is necessary to plan a program to control this zoonotic parasites.
Acknowledgements
The authors gratefully acknowledge to Parasitology Department, Faculty of Veterinary Medicine, for supporting with research equipment.
Funding Statement
Funding: Self funding.
References
- 1.Gerhold RW, Jessup DA. Zoonotic Diseases Associated with Free- Roaming Cats. Zoonoses and Public Health 2013;60:189-95. [DOI] [PubMed] [Google Scholar]
- 2.Szwabe K, Błaszkowska J. Stray dogs and cats as potential sources of soil contamination with zoonotic parasites. Ann Agric Environ Med 2017;24:39–43. [DOI] [PubMed] [Google Scholar]
- 3.Khalafalla RE. A Survey Study on Gastrointestinal Parasites of Stray Cats in Northern Region of Nile Delta, Egypt. PLoS ONE 2011;6:e20283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Beugnet F, Bourdeau P, Chalvet-Monfray K, et al. Parasites of Domestic Owned Cat in Europe: Co-infection and Risk Factor. Parasit & Vector 2014;7:291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Khademvatan S, Abdizadeh R, Rahim F, et al. Stray Cats Gastrointestinal Parasites and its Association With Public Health in Ahvaz City, South Western of Iran. Jundishapur J Microbiol 2014;7: e11079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Yang Y, Liang H. Prevalence and Risk Factors of Intestinal Parasites in Cats from China. BioMed Res Internat. 2015; 5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Ilić T, Kulišić Z, Antić N, et al. Prevalence of zoonotic intestinal helminths in pet dogs and cats in the Belgrade area. J App Ani Res 2017;45: 204–208. [Google Scholar]
- 8.Arbabi M, Hooshyar H. Gastrointestinal parasites of stray cats in Kashan, Iran. Trop Biomed 2009;26: 16–22 [PubMed] [Google Scholar]
- 9.Saboyá MI, Catalá L, Ault SK, Nicholls RS. Prevalence and intensity of infection of Soil-transmitted Helminths in Latin America and the Caribbean Countries: Mapping at second administrative level 2000-2010. Pan American Health Organization: Washington D.C., 2011. [Google Scholar]
- 10.Lee S-H, Younsung Ock Y, Choi D, Kwak D. Gastrointestinal Parasite Infection in Cats in Daegu Republic of Korea Efficacy of Treatment Using Topical Emodepside/Praziquantel Formulation. Korean J Parasitol 2019;57: 243-248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Tuzio H, Edwards D, Jarboe L, et al. Feline zoonose guidelines from the American Association of Feline Practitioners. J Fel Med Surg 2005;7:243-e274. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Sohn W-M, Chai J-Y. Infection status with helminthes in feral cats pur-chased from a market in Busan Republic of Korea. Korean J. Parasitol. 2005;43: 93-100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Sauda F, Malandrucco L, De Liberato C, et al. Gastrointestinal parasites in shelter cats of central Italy. Vet Parasitol 2019;18:100321. [DOI] [PubMed] [Google Scholar]
- 14.Sowemimo OA. Prevalence and intensity of gastrointestinal parasites of domestic cats in Ode – Irele and Oyo communities, Southwest Nigeria. 2012; J Par and Vect Biol 2021; 4: 7-13. [Google Scholar]