Gastrointestinal parasites in rural dogs and cats in Selangor and Pahang states in Peninsular Malaysia

Similar documents
Prevalence of intestinal protozoan parasites of dogs in Ibadan, south western Nigeria

The Prevalence of Some Intestinal Parasites in Stray Dogs From Tetova, Fyr Macedonia

Parasites and their vectors

The role of domestic dogs in the transmission of zoonotic helminthes in a rural area of Mekong river basin

Determining the Most Prevalent Parasitic Worms Found in Canines Surrounding the Bryan/College Station Area

FECAL EGG AND OOCYST COUNTS IN DOGS AND CATS FROM ANIMAL SHELTERS FROM SOUTH DAKOTA

Cardiac blood samples were collected in EDTA tubes as described in Chapter 2, and

OCCURRENCE OF ENDOPARASITES IN INDIGENOUS ZAMBIAN DOGS. Bruce-Miller, M., Goldová, M.

Canine giardiosis in an urban are Title source on infection of man. NikoliĆ, Aleksandra, DimitrijeviĆ Author(s) BobiĆ, Branko

Prevalence of zoonotic intestinal parasites in household and stray dogs in rural areas of Hamadan, Western Iran

Division of Health Sciences School of Veterinary and Biomedical Sciences Murdoch University Western Australia

Proceedings of the World Small Animal Veterinary Association Sydney, Australia 2007

Intestinal Parasites in Shelter Dogs and Risk Factors Associated with the Facility and its Management

The epidemiology of Giardia spp. infection among pet dogs in the United States indicates space-time clusters in Colorado

Prevalence of zoonotic and other gastrointestinal parasites in police and house dogs in Alexandria, Egypt

April is National Heartworm Awareness month, a

Introduction to Helminthology

Copyright is owned by the Author of the thesis. Permission is given for a copy to be downloaded by an individual for the purpose of research and

Prevalence of Gastrointestinal Helminthes among Dogs in Bahir Dar Town, Ethiopia

Age-Dependant Prevalence of Endoparasites in Young Dogs and Cats up to One Year of Age

Gastrointestinal helminthes of dogs and owners perception of dogs parasitic zoonoses in Hawassa, Southern Ethiopia

This is the publisher s copyrighted version of this article. The original can be found at:

VICH Topic GL20 EFFICACY OF ANTHELMINTICS: SPECIFIC RECOMMENDATIONS FOR FELINE

Epidemiological Comparative Study of Giardia lamblia Between Human and Cow in Basrah, Iraq

Diagnosing intestinal parasites. Clinical reference guide for Fecal Dx antigen testing

Prevalence of Gastro-Intestinal Parasites of Dairy Cows in Thailand

The impact on the routine laboratory of the introduction of an automated ELISA for the detection of Cryptosporidium and Giardia in stool samples

Diagnosing intestinal parasites. Clinical reference guide for Fecal Dx antigen testing

Prevalence and zoonotic potential of canine hookworms in Malaysia

Data were analysed by SPSS, version 10 and the chi-squared test was used to assess statistical differences. P < 0.05 was considered significant.

Guard against intestinal worms with Palatable All-wormer

Proceeding of the LAVC Latin American Veterinary Conference Oct , 2010 Lima, Peru

Department of Tropical Hygiene, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchawithi Road, Bangkok 10400, Thailand.

Research Article Prevalence and Risk Factors of Intestinal Parasites in Cats from China

This information is intended to give guidance for vets and CP staff and volunteers in the treatment of a CP cat with diarrhoea.

FOR ANIMAL TREATMENT ONLY

EFFICACY OF ANTHELMINTICS: SPECIFIC RECOMMENDATIONS FOR CANINES

PCR detection of Leptospira in. stray cat and

PARASITOLOGICAL EXAMINATIONS CATALOGUE OF SERVICES AND PRICE LIST

Prevalence of gastrointestinal helminthes among dogs and owners perception about zoonotic dog parasites in Hawassa Town, Ethiopia

IDEXX PetChek IP A new approach to intestinal parasites in veterinary medicine

International Journal of Science, Environment and Technology, Vol. 7, No 1, 2018,

School-based Deworming Interventions: An Overview

Asian Pacific Journal of Tropical Disease

Stray dogs and cats as potential sources of soil contamination with zoonotic parasites

Prevalence and awareness of zoonotic parasites of dogs on Curaçao

VICH Topic GL19 EFFICACY OF ANTHELMINTICS: SPECIFIC RECOMMENDATIONS FOR CANINES

JOURNAL OF INTERNATIONAL ACADEMIC RESEARCH FOR MULTIDISCIPLINARY Impact Factor 2.417, ISSN: , Volume 4, Issue 2, March 2016

Title: ontamination of the hair of owned dogs with the eggs of Toxocara spp.

Quantifying the risk of zoonotic geohelminth infections for rural household inhabitants in Central Poland

Estimation of canine intestinal parasites in Córdoba (Spain) and their risk to public health

CAZITEL FLAVORED ALLWORMER FOR DOGS

Helminthic food-borne infection in Japan

Parasitology Division, National Veterinary Research Institute, PMB 01 Vom Plateau State, Nigeria * Association

Academia Arena 2017;9(3) Prevalence of parasites in soil samples in Tehran public places.

Coccidia and Giardia Diagnosis, Prevention and Treatment

Label (2 tab) - front panel Issue Date: Page: 1 of 14 The information above this line is not included in the label FOR ANIMAL TREATMENT ONLY

Prevalence of intestinal protozoan parasites in stray and domicile dogs in Ilorin, North Central, Nigeria

04/02/2013. Parasites and breeding dogs: These parasites we don t hear so much about. Main internal parasites found in breeding kennels

Correspondence should be addressed to Maria Teresa Manfredi;

Protozoan Parasites of Veterinary importance 2017

STUDIES ON THE PREVALENCE OF HOOKWORM INFECTION AMONGST RURAL FARMERS IN EMOHUA L.G.A, RIVERS STATE

Stray animal and human defecation as sources of soil-transmitted helminth eggs in playgrounds of Peninsular Malaysia

Parasitology PAR 311

Lecture 4: Dr. Jabar Etaby

Zoonoses in food and feed

Medical Parasitology PAR 311

AARJMD VOLUME 1 ISSUE 19 (MARCH 2014) ISSN : A Peer Reviewed International Journal of Asian Academic Research Associates AARJMD

Guidelines for Veterinarians: Prevention of Zoonotic Transmission of Ascarids and Hookworms of Dogs and Cats

ROLE OF DOMESTIC CATS FELIS CATUS AS RESERVOIR HOSTS OF INTERNAL PARASITES AND PROTOZOA IN BAGHDAD

EMERGING AND RE-EMERGING ZOONOTIC PARASITES: PREVENTIVE AND CONTROL STRATEGIES

Detection of Gastrointestinal Helminthic and Protozoan Infections in Diarrhoeic Goats

Efficacy of Moxidectin 6-Month Injectable and Milbemycin Oxime/Lufenuron Tablets Against Naturally Acquired Toxocara canis Infections in Dogs*

SEMESTER ONE 2007 INFECTION and IMMUNITY GRADUATE ENTRY PROGRAMME PARASITOLOGY PRACTICAL 9 Dr TW Jones NEMATODES

Ectoparasites of Stray Cats in Bangkok Metropolitan Areas, Thailand

KNOWLEDGE, ATTITUDE AND PRACTICE OF DENGUE FEVER AND HEATH EDUCATION PROGRAMME AMONG STUDENTS OF ALAM SHAH SCIENCE SCHOOL, CHERAS, MALAYSIA

A revolution in the parasite control for cats. Dr Anne Bollart Merial Technical & Marketing Manager - Pets Business

FACULTY OF VETERINARY MEDICINE

THE VETERINARIAN'S CHOICE. Compendium clinical Trials. Introducing new MILPRO. from Virbac. Go pro. Go MILPRO..

STUDIES ON THE PREVALENCE OF HOOKWORM INFECTION AMONGST RURAL FARMERS IN EMOHUA L.G.A, RIVERS STATE.

Iranian J Parasitol: Vol. 4, No.1, 2009, pp Intestinal Helminthoses in Dogs in Kaduna Metropolis, Kaduna State, Nigeria

PARASITIC INFECTIONS FOUND IN PET AND STRAY DOGS IN IPOH, MALAYSIA

Ebonyi State University. Abakaliki Ebonyi State

Most clients are well aware that puppies

PREVALENCE OF OPISTHORCHIS VIVERRINI INFECTION IN THE CANINE AND FELINE HOSTS IN THREE VILLAGES, KHON KAEN PROVINCE, NORTHEASTERN THAILAND

Intestinal parasites in various animals at a zoo in Malaysia

In a tasty bone shape.

Prevalence of gastro-intestinal strongyles in native beef cattle under small holder management condition in Udon Thani, Thailand

Surveillance of animal brucellosis

Vet Integ Sci. Veterinary Integrative Sciences

The epidemiology of infections with Giardia species and genotypes in well cared for dogs and cats in Germany

Cryptosporidium and Giardia shedding among humans and animals in coastal Orissa, India

Coproantigen prevalence of Echinococcus spp. in rural dogs from Northwestern Romania

General introduction

Study on prevalence of ancylostomosis in dogs at Anand district, Gujarat, India

Hydatid Disease. Overview

ZOONOSES ACQUIRED THROUGH DRINKING WATER. R. M. Chalmers UK Cryptosporidium Reference Unit, NPHS Microbiology Swansea, Singleton Hospital, Swansea, UK

Protozoan Parasites: Flagellates, Amoebae, Ciliates & Apicomplexans

Prevalence of Giardia in Household Dogs and Cats in the State of Rio de Janeiro using the IDEXX SNAP Giardia Test

Copyright is owned by the Author of the thesis. Permission is given for a copy to be downloaded by an individual for the purpose of research and

Transcription:

DOI: 10.2478/s11686-014-0306-3 W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2014, 59(4), 737 744; ISSN 1230-2821 Gastrointestinal parasites in rural dogs and cats in Selangor and Pahang states in Peninsular Malaysia Romano Ngui 1 *, Soo Ching Lee 1, Nan Jiun Yap 1, Tiong Kai Tan 1, Roslan Muhammad Aidil 1, Kek Heng Chua 2, Shafie Aziz 3, Wan Yusoff Wan Sulaiman 1, Arine Fadzlun Ahmad 1, Rohela Mahmud 1 and Yvonne Lim Ai Lian 1 1 Department of Parasitology, Faculty of Medicine, University of Malaya, 50603, Kuala Lumpur, Malaysia; 2 Department of Biomedical Science, Faculty of Medicine, University of Malaya, 50603, Kuala Lumpur, Malaysia; 3 Department of Geography, Faculty of Arts and Social Sciences, University of Malaya, 50603, Kuala Lumpur, Malaysia Abstract To estimate the current prevalence of gastrointestinal (GI) parasites in dogs and cats, a total of 105 fresh faecal samples were collected from rural areas in Peninsular Malaysia. Each faecal sample was examined for the presence of GI parasites by microscopic examination after formalin-ether concentration technique and for protozoa, trichrome and Ziehl-Neelsen staining were employed. The overall prevalence of GI parasitic infection was 88.6% (95% CI = 82.5 94.7) in which 88.3% of dogs and 89.3% of cats were infected with at least one parasites species, respectively. There were 14 different GI parasites species (nematodes, cestodes and protozoa) detected, including Ancylostoma spp. (62.9%), Toxocara spp. (32.4%), Trichuris vulpis (21.0%), Spirometra spp. (9.5%), Toxascaris leonina (5.7%), Dipylidium caninum (4.8%), Ascaris spp. (2.9%), Hymenolepis diminuta (1.0%) and others. General prevalence of GI parasites showed a significant difference between helminth (84.4%) and protozoa (34.3%) infections. Monoparasitism (38.1%) was less frequent than polyparasitism (46.7%). As several of these GI parasites are recognized as zoonotic agents, the results of this investigation revealed that local populations may be exposed to a broad spectrum of zoonotic agents by means of environmental contamination with dogs and cats faeces and this information should be used to mitigate public health risks. Prevention and control measures have to be taken in order to reduce the prevalence rates especially in socioeconomically disadvantaged communities where animals live in close proximity to people, poor levels of hygiene and overcrowding together with a lack in veterinary attention and zoonotic awareness. Keywords Dogs, Cats, Gastrointestinal helminths and protozoa, rural area, zoonosis Introduction Pet dogs and cats are often considered to be the faithful friends and intimate companions of humans. This human-animal bond can provide substantial positive benefits with regards to emotional development, socialization and physiological well-being of humans (McGlade et al. 2003). With the increasing number of companion animals, there is more contact between domestic animals and people, exposing humans to zoonotic agents (Robertson et al. 2000, Lorenzini et al. 2007). Although dogs and cats are often considered family members by their owners, it is important to emphasize that they may play important role as host for zoonotic diseases to humans (Schantz 1994, Robertson et al. 2000). Likewise, the potential role of companion animals as reservoirs for zoonotic diseases has been recognized as a significant public health threat of pet ownership worldwide (Schantz 1994). While many potentially zoonotic organisms are associated with dogs and cats, enteric pathogens are of particular concern (Robertson et al. 2000, McGlade et al. 2003). Intestinal helminths are one of the most common pathogenic agents in dogs and cats (Papazahariadou et al. 2007, Bridger and Whitney 2009). Among intestinal helminths, Toxocara and hookworm species of dogs and cats are most important to public health. The infections caused by these parasites receive great attention especially in developing countries and communities that may be socioeconomically challenged (Robertson et al. 2000) and they are responsible for some important zoonotic diseases (Despommier 2003, Prociv and Croese 1996). These dogs and cats tend to discharge helminth eggs or larvae into *Corresponding author: skyromano@gmail.com

738 Romano Ngui et al. the environment that are transmittable to human population (Bridger and Whitney 2009, Overgaauw et al. 2009). The transmission of these zoonotic agents could be through indirect contact with animal faeces, contaminated water and food or through direct contact with infected animals since most of these parasites have an oral-fecal transmission cycle (Martinez-Moreno et al. 2007, Overgaauw et al. 2009).Unlike in the rural communities, the potential role of companion animals as reservoirs for diseases has been recognized as a significant public health problem in urban setting. The subject has received attention, priority and coverage in medical literature of urban communities primarily because of the availability of resources (Traub et al. 2005). The attitudes and economic status of pet owners in these urban areas also ensure that the available veterinary resources are well used (Robertson et al. 2000). However, in rural settings, uncontrolled populations of dogs and cats exist in close proximity with their owners and humans often share a close relationship with them. In these socioeconomically disadvantaged communities, the poor levels of hygiene and overcrowding together with a lack of veterinary attention and zoonotic awareness, exacerbates the risks of disease transmission (Traub et al. 2005, Conlan et al. 2011). In Malaysia, little information on the prevalence of intestinal helminthic infections in rural dogs and cats is available. Most surveys of intestinal helminths conducted in the past have been limited to urban dogs and cats (Shanta et al. 1980, Lee et al. 1993). Until recently, study on diversity and distribution of intestinal helminths is focused on stray cats in major urban cities in Malaysia (Mohd Zain 2010). While previous studies on the prevalence of intestinal helminths in urban setting yielded important results, it cannot be assumed these results are indicative of the situation among rural dogs and cats. Moreover, close contact between humans, dogs and cats is part of natural living conditions particularly where livestock raising is of economic importance (Soriano et al. 2010), thus at risk of acquiring zoonotic diseases transmitted by dogs. As the potential for zoonotic transmission of intestinal helminths and the human health risks associated with dog and cat ownership are now increasing (Robertson et al. 2000, Overgaauw et al. 2009), there is an urgent need to obtain more-recent parasite data especially in rural setting. Materials and Methods Study area The study protocol (MEC Ref. No. 824.11) was approved by the Ethics Committee of the University Malaya Medical Centre, Malaysia. The study was conducted in 2011 among rural villages in the states of Selangor and Pahang, Peninsular Malaysia (Figure 1). Cats and dogs are the most common companion animals among the villagers. They play a diversity of roles to their owners. They are involved in companionship, hunting and guarding. It has been estimated that about 50 to 100 dogs and cats live in each of the surveyed areas. Free-roaming dogs and cats are common and were observed to defecate indiscriminately in the areas surrounding the property of their owners. The practice of removing animal faeces from public areas is not a common habit among the villagers. Due to the lack of awareness and resources, the attitude as well Fig. 1. Location of the study areas

Intestinal Parasitic Infection in Dogs and Cats In Malaysia 739 as economic constrain of the owners, these animals are usually given minimal care and the administration of anthelminthics is uncommon. The villagers have very close contact with these animals, even sharing food from the same plate with them. Occasionally, these animals also slept and defecated indoors. Faecal sample collection Faecal samples were collected with the permission and assistance of the owners. A total of 105 fresh faecal samples (i.e., 77 dogs and 28 cats) were collected during the study period. The ages of the animals ranged from 6 weeks to 36 years old, however the history of these animals was not known. The collected faecal samples were put in clean, wide-mouthed container with tight fitting lids and sealed in plastic bags for transportation. Extra care was taken to avoid contamination with soil which might harm existing or introducing free-living organism from the environment. Samples were then labeled according to the type of animal and date of collection. Faecal samples were brought back to the laboratory at ambient temperature on the same day of collection, preserved in 2.5% potassium dichromate and kept at 4 C until used. Parasitological procedure The collected faecal samples were processed and examined for the presence of GI parasites by using standard direct smear and formalin ethyl acetate concentration technique (Cheesbrough 1998). Briefly, faecal samples were stained with both normal saline and 0.85% iodine and examined using 10 magnification followed by examination under 400 magnification with light microscope (Olympus CX40, USA). In addition, permanent staining technique was also applied for the identification of intestinal protozoa. Two types of staining methods were used in the present study, the trichrome staining for intestinal protozoa and modified Ziehl-Neelsen staining for Cryptosporidium. The slides were examined under oil immersion at 1000x magnification using light microscopy for both staining techniques. Data analysis Detection of GI parasites was determined on the basis of morphological characteristics of specific species under microscopic examination. Each sample was examined and the result was considered as positive when at least one parasite egg or cyst/oocyst was observed in one of each employed technique. The data entry and analysis was carried out using the SPSS software (Statistical Package for the Social Sciences) program for Windows version 17 (SPSS, Chicago, IL, USA). The prevalence and 95% confidence intervals (CIs) were calculated for each parasite. Pearson s Chisquare (X 2 ) test was carried out to test for significance between prevalence of parasite in the host, species and type of infections. The level of statistical significance was set at p<0.05 for each test. Results The total number of samples examined were 105, with 77 (73.3%) from dogs and 28 (26.7%) from cats. Of the 105 samples examined, 93 (88.6%; 95% CI = 82.5 94.7) were parasitized with, at least one GI parasite species. The overall prevalence of GI parasites in dogs and cats were 88.3% (95% CI = 80.7 95.9%) and 89.3% (95% CI = 77.9 100.8), respectively. With regards to the parasite species, helminth (84.8%; 95% CI = 77.9 91.7) were significantly more common compared to protozoa (34.3%; 95% CI = 25.2 43.4) in both animals (p<0.05) (Table I). A total of 14 different GI parasites species were detected in both dogs and cats, including Ancylostoma spp. (62.9%), Toxocara spp. (32.4%), Trichuris vulpis (21.0%), Spirometra spp. (9.5%), Toxascaris leonina (5.7%), Dipylidium caninum (4.8%), Ascaris spp. (2.9%), Hymenolepis diminuta (1.0%), Entamoeba spp. (12.4%), Giardia duodenalis (12.4%), Cryptosporidium spp. (6.7%), Balantidium coli (3.8%), Eimeria spp. (1.9%) and Isospora spp. (1.9%). Twelve and 11 different GI parasites species were detected in dogs and cats, respectively (Table II). Taking into consideration the helminth infections in dogs, Ancylostoma spp. (71.4%) was the most prevalent followed by Toxocara spp. (28.6%) and T. vulpis (24.7%). The remaining helminths identified were Spirometra spp. (10.4%), T. leonina (5.2%), D. caninum (3.9%), Ascaris spp. and H. diminuta (1.6%). The most frequently observed protozoa were Entamoeba spp. and G. duodenalis (13.0%), followed by Cryptosporidium spp. (6.5%), Balantidium coli (5.2%), Eimeria spp. (2.6%) while Table I. Overall prevalence of gastrointestinal parasites in dogs and cats Animals Helminth* Protozoa* N n % 95% CI n % 95% CI Dogs 77 64 83.1 74.73 91.5 28 36.4 25.7 47.2 Cats 28 25 89.3 77.8 100.8 8 28.6 11.9 45.3 Total 105 89 84.8 77.9 91.7 36 34.3 25.2 43.4 N = Number of animals examined; n= Number of infected animals *Significant association (p<0.05)

740 Romano Ngui et al. Table II. Prevalence of gastrointestinal parasites by species in dogs and cats Gastrointestinal Parasites Dogs Cats n % a % b n % a % b Helminth Ancylostoma spp 54 86.0 71.4 11 44.0 39.3 Toxocara spp 22 34.4 28.6 12 48.0 42.9 Trichuris vulpis 19 29.7 24.7 3 12.0 10.7 Spirometra spp 8 12.5 10.4 2 8.0 7.1 Toxascaris leonina 4 6.3 5.2 2 8.0 7.1 Dipylidium caninum 3 4.7 3.9 2 8.0 7.1 Ascaris spp 1 1.6 1.3 2 8.0 7.1 Hymenolepis diminuta 1 1.6 1.3 0 0 0 Protozoa Entamoeba spp 10 15.6 13.0 3 12.0 10.7 Giardia duodenalis 10 15.6 13.0 3 12.0 10.7 Cryptosporidium spp 5 7.8 6.5 2 8.0 7.1 Balantidium coli 4 6.3 5.2 0 0 0 Eimeria spp 2 3.2 2.6 0 0 0 Isospora spp 1 1.6 1.3 1 4.0 3.4 a Frequency was calculated based on total number of infected animals for each species (n) divided by total number of infected animals (64 dogs and 25 cats) b Frequency was calculated based on total number of infected animals for each species (n) divided by total number of animals sampled (77 dogs and 28 cats) 1.3% were infected with Isospora spp. As for cats, very high prevalence of Toxocara infection (42.9%) was recorded, followed by Ancylostoma spp. (39.3%), T. vulpis (10.7%), Spirometra spp., T. leonina, D. caninum and Ascaris spp. (7.1% for each species). The most common protozoa parasites detected in cats were both Entamoeba spp. and G. duodenalis (10.7%) each. The remaining protozoa infections were Cryptosporidium spp. (7.1%) and Isospora spp. (3.4%). Monoparasitism (38.1%) was less frequent than polyparasitism (46.7%) in both animals. There was a high number of cats being infected with at least one of the GI parasite species compared to dogs but this did not differ significantly (Table III). Considering the prevalence of GI parasites in dogs, 33.8% (26/77) was infected by a single parasite species and 49.4% (38/77) harbored more than one parasite species. Combination of helminth and protozoa (31.2%) was most common followed by a mixed infection of more than one helminth species. In cats, 50.0% (14/28) harbored only one parasite species while 39.3% (11/28) was found to be infected with more than one species. No mixed infection of protozoa species was seen in both dogs and cats. With regards to the types of polyparasitism detected in dogs and cats, double infections of Ancylostoma spp. and Toxocara spp. were most prevalent in both animals while only dogs were found to be infected with more than two helminth species (Table IV). Considering the mixed infection with helminth and protozoa, double infections with two species were more common compared to a combination of three or four parasite species in both dogs and cats, but this did not differ significantly between each category. Table III. Prevalence of monoparasitism and polyparasitism in dogs and cats N % Number of Monoparasitism Cases Number of Polyparasitism Cases Helminth + Helminth Type of Polyparasitism Helminth + Protozoa Protozoa + Protozoa n % n % n % n % n % Dogs 64 83.1 26 33.8 38 49.4 14 18.2 24 31.2 0 0 Cats 25 89.3 14 50.0 11 39.3 11 39.3 0 0 0 0 Total number of animals examined (77 dogs and 28 cats) N = Number of infected animals

Intestinal Parasitic Infection in Dogs and Cats In Malaysia 741 Table IV. Types of gastrointestinal parasites and polyparasitism in dogs and cats Helminth + Helminth Double Infections Type of Polyparasitism Dogs* Cats* n % n % Ancylostoma spp + Toxocara spp 11 17.2 4 16.0 Ancylostoma spp + T. vulpis 8 12.5 2 8.0 Ancylostoma spp + Spirometra spp 4 6.3 1 4.0 T. vulpis + Toxocara spp 2 3.2 0 0 Ancylostoma spp + D. caninum 1 1.6 0 0 Ancylostoma spp + Ascaris spp. 0 0 1 4.0 T. leonina + Toxocara spp 0 0 1 4.0 Toxocara spp + D. caninum 0 0 1 4.0 Triple Infections Ancylostoma spp + T. vulpis +Toxocara spp 5 7.8 0 0 Ancylostoma spp + T. vulpis + T. leonina 2 3.2 0 0 Ancylostoma spp + Toxocara spp + Spirometra spp 2 3.2 0 0 Ancylostoma spp + Ascaris spp. + Toxocara spp 1 1.6 0 0 Ancylostoma spp + T. vulpis + Spirometra spp 1 1.6 0 0 Ancylostoma spp + T. leonina + D. caninum 1 1.6 0 0 Helminth + Protozoa Double Infections Ancylostoma spp + G. duodenalis 4 6.3 0 0 Ancylostoma spp + Entamoeba spp 4 6.3 1 4.0 Ancylostoma spp + Cryptosporidium spp 2 3.2 0 0 H. diminuta + Entamoeba spp 1 1.6 0 0 Spirometra spp + Entamoeba spp 1 1.6 0 0 Spirometra spp + Balantidium coli 1 1.6 0 0 Toxocara spp + Entamoeba spp 0 0 1 4.0 D. caninum + Entamoeba spp 0 0 1 4.0 Ascaris spp. + G. duodenalis 0 0 1 4.0 Triple Infections Ancylostoma spp + Toxocara spp + Entamoeba spp 2 3.2 0 0 Ancylostoma spp + Toxocara spp + G. duodenalis 1 1.6 0 0 Ancylostoma spp + T. vulpis + G. duodenalis 1 1.6 0 0 Ancylostoma spp + D. caninum + G. duodenalis 1 1.6 0 0 Ancylostoma spp + T. vulpis + Cryptosporidium spp 1 1.6 0 0 Ancylostoma spp + Toxocara spp + Eimeria spp 1 1.6 0 0 Ancylostoma spp + Balantidium coli + G. duodenalis 1 1.6 0 0 Ancylostoma spp + Toxocara spp + Isospora spp 0 0 1 4.0 Others Ancylostoma spp + T. vulpis + Toxocara spp + G. duodenalis 1 1.6 0 0 Ancylostoma spp + T. vulpis + Toxocara spp + Eimeria spp 1 1.6 0 0 Ancylostoma spp + T. vulpis + Toxocara spp + Balantidium coli 1 1.6 0 0 Ancylostoma spp + T. vulpis + Cryptosporidium spp + Isospora spp 1 1.6 0 0 Ancylostoma spp + T. vulpis + Cryptosporidium spp + Entamoeba spp 1 1.6 0 0 Ancylostoma spp + T. vulpis + Spirometra spp + Cryptosporidium spp 0 0 1 4.0 *Frequency was calculated based on total number of infected animals for each species (n) divided by total number of infected animals (64 dogs and 25 cats)

742 Romano Ngui et al. Discussion The results of this study showed that the prevalence of GI parasitic infections among dogs and cats of rural areas in Malaysia is very high. Despite strong evidence indicating the endemicity of several zoonotic species as reported in the present study, knowledge of the prevalence of zoonotic parasites in dogs and cats in Malaysia is largely lacking. Therefore, it is difficult to compare the prevalence of GI parasites in this study with studies within the country as most surveys of dogs and cats conducted in the past have been limited only to urban settings. Worldwide, there is significant variation in the prevalence of GI parasites reported in dogs and cats with percentage ranging between 26% and 96% (Schantz 1994, Traub et al. 2005, Overgaauw et al. 2009). As many of the identified GI parasite species can have significant health implications, it is important to have an understanding of regional parasite burden so that public health effects can be minimized. The high prevalence of GI helminths reported in this study was in accordance with several studies conducted among dogs and cats in Spain (Calvete et al. 1998), Costa Rica (Paquet- Durand et al. 2007), Brazil (Lorenzini et al. 2007) and Belgium (Claerebout et al. 2009), with prevalence rates ranging between 88% and 90%. In contrast, studies conducted among dogs and cats in Australia and Argentina have reported low prevalence rates from 1% to 10% (McGlade et al. 2003, Sommerfelt et al. 2006). Likewise, study of the GI helminths in rural dogs in Argentina found prevalence rates ranging from 37.9% to 52.4% (Soriano et al. 2010). Similarly, studies conducted among shepherd and hunting dogs in Greece (Papazahariadou et al. 2007) noted prevalence rates of 35.5% and 26%, respectively. In all cases, hookworm was found to be the most common GI parasite detected in both dogs and cats. Similar observations have been reported in several surveys undertaken among dogs and cats worldwide (Inpankaew et al. 2007, Lorenzini et al. 2007, Papazahariadou et al. 2007, Traub et al. 2008, Scorza et al. 2011). The high prevalence of hookworm infections among dogs and cats in these rural communities could play a significant role in contributing to the occurrence of zoonotic ancylostomiasis such as creeping eruption and eosinophilic enteritis (EE) or less frequently symptoms of localized myositis, erythema multiforme and ophthalmological manifestations in human (Bowman et al. 2010). It is difficult to compare the species-specific of hookworm infections in dogs and cats in Malaysia since there is limited prior documented data. Previous local studies reported that more than 95% of the dogs were infected with A. ceylanicum based on autopsies examination of the adult worm (Yoshida et al. 1973). More recent studies based on polymerase chain reaction (PCR) in dogs and cats demonstrated that only A. ceylanicum, A. caninum and A. braziliense were detected in the surveyed dogs and cats populations in Malaysia (Mahdy et al. 2012, Ngui et al. 2012). Toxocara spp., was the second most common GI helminth species detected in both hosts, a finding that is in accordance with parasitic survey of dogs and cats conducted in St. Pierre Island (Bridger and Whitney 2009), Argentina (Sommerfelt et al. 2006) and Spain (Calvete et al. 1998). However, prevalence rate reported in the present study was higher than that reported in Thailand (7.5%) (Inpankaew et al. 2007) and Spain (17.7%) (Martinez-Moreno et al. 2007). Although Toxocara cati and Toxocara canis are common species infecting dogs and cats respectively, it would appear that the Toxocara eggs recovered in this study may also be Toxocara malaysiensis. This is because earlier local studies assumed T. malaysiensis to be T. cati or T. canis. However, molecular analysis revealed that these three nematode were distinct species. T. malaysiensis has a prevalence rate ranging between 20% and 50% (Zhu et al. 2000). However, species differentiation at molecular level was not carried out in the present study, a subject for future study. On the other hand, T. vulpis was the third most frequent GI helminth. Similar observation has been recorded in Costa Rica with prevalence rates of 15% to 26% among the surveyed dogs and cats (Paquet-Durand et al. 2007, Scorza et al. 2011). The worldwide distribution and prevalence of T. vulpis in dogs and cats varies regionally with rates varying from 3.7% to 49.5% (Katagiri and Oliveira-Sequeira 2008). Although the egg detected in this study was morphologically identical to human-specific species, i.e., Trichuris trichiura, measurements of the eggs are within the range for T. vulpis (approximately 82 39 µm) which is larger and broader than T. trichiura (approximately 55 22 µm). It was observed that T. trichiura was the highest helminth species detected in human samples in the same study locations (Ngui et al. 2011). Thus, the role of the dog as mechanical host of T. trichiura infection may also seem likely in these rural communities. Necropsy examination to differentiate adult worm morphology on Trichuris-positive dogs and cats or molecular tools for species identification of Trichuris eggs in fecal sample would be useful to further investigate this hypothesis. The finding of Ascaris eggs in dogs and cats feces suggests that these animals might act as significant mechanical transmitter of ascariasis in human population especially in communities where promiscuous and indiscriminate defecation habit exist. The role of dogs and cats in the transmission of Ascaris lumbricoides to humans has been widely recognized (Traub et al. 2003). Recent study carried out in Egypt suggested that dogs are acting as biological transmitter and reservoir hosts of A. lumbricoides as well as environmental contaminators in communities where indiscriminate defecation is common (Shalaby et al. 2010). Likewise, Traub and co-workers (2003) demonstrated that Ascaris from positive dogs were 100% homology with the A. lumbricoides derived from human fecal sample using molecular based tools in India. In addition, Traub and coworkers (2003) also indicated that dog positive with Ascaris belonged to the household where at least one family member was infected with A. lumbricoides. These Ascaris-positive dogs might ingest the feces of their infected owner, therefore acting as disseminators and environmental contaminators by increasing the net exposure of infective stages when in contact with human. However, this finding still needs further investigation

Intestinal Parasitic Infection in Dogs and Cats In Malaysia 743 particularly through the use of molecular based tool for specific species identification and discrimination. Spirometra spp. was also recorded in both dogs and cats. Although not many studies had documented Spirometra spp., similar observation has been reported in a survey undertaken among dogs population in India (Traub et al. 2003). The presence of Spirometra spp. is a reflection of the fact that most dogs and cats were allowed to roam freely and had access to paratenic hosts as their food sources. The possible source of infection to dogs and cats is via ingestion of raw fish offal fed to them by their owners and therefore acting as important indirect reservoirs of this parasite to human. Entamoeba spp. was the most common protozoa parasite reported in the present study. To date, information on the prevalence of Entamoeba spp. in dogs and cats has been rather sporadic and limited (Wittnich 1976,Shimada et al. 1992). A recent study conducted to determine the prevalence of GI parasites in Barcelona, Spain reported prevalence rates of Entamoeba spp. of 0.4% in the surveyed dogs and cats (Gracenea et al. 2009). However, the risk to public health from zoonotic transmission of Entamoeba spp. particularly the pathogenic, E. histolytica would appear to be minimal. Although, dogs and cats can serve as a potential source of infections to human following coprophagy of human faeces, this reverse zoonosis is unlikely to result in significant environmental contamination since E. histolytica rarely encysts in dogs and cats (Eyles et al. 1954). The infected dogs and cats excrete only the motile and fragile trophozoite which is non-infective. Infected human however, excretes cysts which are extremely resistant and highly infective (Wittnich 1976). Coprological examination of faecal samples revealed that 13.0% and 10.7% of dogs and cats were infected with Giardia spp., respectively. The finding was in line with previous reports conducted in Brazil (Oliveira-Sequeira et al. 2002), Argentina (Fontanarrosa et al. 2006) and Netherland (Overgaauw et al. 2009). It is estimated that the worldwide prevalence of Giardia in dogs is about 8% (Kirkpatrick 1990). However, the prevalence in cats tends to be much lower, at about 4% (Kirkpatrick 1990). Although epidemiological data would suggest that the main reservoir of human giardiasis is more likely to be man himself and direct person to person transmission is more important than zoonotic transmission (Robertson et al. 2000). Animals still harbor Giardia strains which are potentially zoonotic to humans given that molecular studies have demonstrated that some Giardia genotype particularly assemblage A can be infective for both human and animal hosts (Robertson et al. 2000, Oliveira-Sequeira et al. 2002, Traub et al. 2003, Inpankaew et al. 2007, Scorza et al. 2011). Cryptosporidium spp., was among the most common GI parasites reported in the present study. Studies conducted among dogs from many other countries via various techniques such as fecal-, molecular- and serological-based surveys revealed that up to 44.8% of dogs have been infected with Cryptosporidium spp. On the other hand, it has been indicated that up to 38.5% of cats examined have been exposed to or are excreting Cryptosporidium oocysts (Lindsay and Zajac 2004). The zoonotic potential of Cryptosporidium spp. is well known and domestic animals are the important reservoir of infection for humans (Robertson et al. 2000, Xiao et al. 2004, Fontanarrosa et al. 2006).To date, there are 16 different species of Cryptosporidium spp. and over 40 genotypes that have been recognized, with new genotypes regularly being identified (Ng et al. 2008). The high prevalence of several potentially zoonotic GI parasites species found in dogs and cats as reported in the present study indicates a need to prevent public health risks. This is particularly important in socioeconomically disadvantaged communities where they often share a close relationship with their companion animals together with lack of veterinary awareness. Monitoring presence of parasites in domestic pets should be a continuous task due to the risk of zoonotic infections and the potential impact on public health. The actual prevalence of zoonoses species transmitted to humans from dogs and cats is difficult to estimate. It depends on several factors such as mode of transmission, numbers of infected animals, behavior or knowledge and understanding of the owners on the prevention measures. The implementation of a chemotherapeutic program to control intestinal parasitic infections in dogs and cats in rural communities would not be feasible due to economic constraints. Alternatively, population control of dogs and cats together with public health education should be implemented. Non-chemotherapeutic measures such as improvement in education, economy, sanitation and hygiene would also help reduce the prevalence of intestinal parasites in both animal and human hosts. Acknowledgements. The authors are grateful to the Ministry of Rural development for giving entry approval to enter the villages. We also thank the pet owners for their support during the sample collection. Special thanks also go to Mr. Saidon Ishak for his technical assistance during the fieldtrips. This research work was funded by the University of Malaya Research Grant (PV024/2011B and BKP007-2014). References Bridger K.E., Whitney H. 2009. Gastrointestinal parasites in dogs from the Island of St. Pierre off the south coast of New foundland. Veterinary Parasitology, 162,167-170. Bowman D.D., Montgomery S.P., Zajac A.M., Eberhard M.L., Kazacos K.R. 2010. Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends Parasitology, 26, 162 167. Calvete C., Lucientes J., Castillo J.A., Estrada R., Gracia M.J., Peribanez M.A., Ferrer M. 1998. Gastrointestinal helminth parasites in stray cats from the mid-ebro Valley, Spain. Veterinary Parasitology, 75, 235 240. Claerebout E.S., Casaert A.C., Dalemans N., De Wilde N., Levecke B., Vercruysse J., Geurden T. 2009. Giardia and other intestinal parasites in different dog populations in Northern Belgium. Veterinary Parasitology, 161, 41 46. Conlan J.V., Sripa B., Attwood S., Newton P.N. 2011. A review of parasitic zoonoses in a changing Southeast Asia. Veterinary Parasitology, 182, 22 40. Despommier D. 2003. Toxocariasis: Clinical aspects, epidemiology, medical ecology, and molecular aspects. Clinical Microbiology Reviews, 16, 265 272.

744 Romano Ngui et al. Eyles D.E., Jones F.E., Jumper J.R., Drinnon V.P. 1954. Amebic infection in dogs. Journal of Parasitology 40, 163 166. Gracenea M., Mar Gómez M.S., Torres J. 2009. Prevalence of intestinal parasites in shelter dogs and cats in the metropolitan area of Barcelona (Spain). Acta Parasitologica, 54, 73 77. Inpankaew T., Traub R., Thompson R.C., Sukthana Y. 2007. Canine parasitic zoonoses in Bangkok temples. Southeast Asian Journal of Tropical Medicine and Public Health, 38, 247 255. Katagiri S., Oliveira-Sequeira T.C.G. 2008. Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in Sao Paulo State, Brazil. Zoonoses and Pubic Health, 55, 406 413. Kirkpatrick C.E. 1990. Enteric protozoal infections, in greene ce (ed): Infectious diseases of the dog and cat. Philadelphia WB Saunders, 804 814. Lee C.C., Cheng N.A.B.Y., Bohari Y. 1993. Toxocara canis from domestic cats in Kuala Lumpur. Tropical Biomedicine, 10, 79 80. Lindsay D.S., Zajac A.M. 2004. Cryptosporidium infections in cats and dogs. Compendium on Continuing Education for the Practising Veterinarian, 26, 864 874. Lorenzini G., Tasca T., De Carli G.A. 2007. Prevalence of intestinal parasites in dogs and cats under veterinary care in Porto Alegre, Rio Grande do Sul, Brazil. Brazilian Journal of Veterinary Research and Animal Science, 44, 137 145. McGlade T.R., Robertson I.D., Elliot A.D., Read C., Thompson R.C. 2003. Gastrointestinal parasites of domestic cats in Perth, Western Australia. Veterinary Parasitology, 117, 251 262. Mahdy M.A., Lim Y.A.L., Ngui R., Siti Fatimah M.R., Choy S.H., Yap N.J., Al-Mekhlafi H.M., Jamaiah I., Johari S. 2012. Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasites and Vectors, 5, 88. Martinez-Moreno F.J., Hernandez S., Lopez-Cobos E., Becerra C., Acosta I., Martinez-Moreno A. 2007. Estimation of canine intestinal parasites in Cordoba (Spain) and their risk to public health. Veterinary Parasitology, 143, 7 13. Mohd Zain S.N. 2010. Comparative study of the macroparasite communities of stray cats from four urban cities in Peninsular Malaysia. Proceedings of the Fourth ASEAN Congress of Tropical Medicine and Parasitology 2010. Ng J., Eastwood K., Durrheim D., Massey P., Walker B., Armson A., Ryan U. 2008. Evidence supporting zoonotic transmission of Cryptosporidium in rural New South Wales. Experimental Parasitology, 119, 192 195. Ngui R., Saidon I., Chow S.C., Rohela M., Lim YAL. 2011. Prevalence and risk factors of intestinal parasitism in rural and remote West Malaysia. PLoS Neglected Tropical Diseases, 5, e974. Ngui R., Lim Y.A.L., Traub R., Mahmud R., Mistam M.S. 2012. Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Neglected Tropical Diseases, 6, e1522. Oliveira-Sequeira T.C., Amarante A.F., Ferrari T.B., Nunes L.C. 2002. Prevalence of intestinal parasites in dogs from Sao Paulo State, Brazil. Veterinary Parasitology, 103, 19 27. Overgaauw P.A.M., van Zutphen L., Hoek D., Yaya F.O., Roelfsema J., Pinelli E., van Knapen F., Kortbeek L.M. 2009. Zoonotic parasites in fecal samples and fur from dogs and cats in the Netherlands. Veterinary Parasitology, 163, 115 122. Papazahariadou M., Founta A., Papadopoulos E., Chilounakis S., Antoniadou-Sotiriadou K., Theodorides Y. 2007. Gastrointestinal parasites of shepherd and hunting dogs in the Serres Prefecture, Northern Greece. Veterinary Parasitology, 148, 170 173. Paquet-Durand I., Hernandez J., Dolz G., Zuniqa J.J., Schneider T., Epe C. 2007. Prevalence of Toxocara spp., Toxascaris leonina and ancylostomidae in public parks and beaches in different climate zones of Costa Rica. Acta Tropica, 104, 30 37. Prociv P., Croese J. 1990. Human eosinophilic enteritis caused by dog hookworm Ancylostoma-caninum. Lancet, 335, 1299 1302. Robertson I.D., Irwin P.J., Lymbery A.J., Thompson R.C. 2000. The role of companion animals in the emergence of parasitic zoonoses. International Journal for Parasitology, 30, 1369 1377. Schantz P.M. 1994. Of worms, dogs, and human hosts: Continuing challenges for veterinarians in prevention of human disease. Journal of the American Veterinary Medical Association, 204, 1023 1028. Scorza A.V., Duncan C., Miles L., Lappin M.R. 2011. Prevalence of selected zoonotic and vector-borne agents in dogs and cats in Costa Rica. Veterinary Parasitology, 183, 178 183. Shanta C.S., Wan S.P., Kwong K.H. 1980. A survey of the endo and ectoparasites of cats in and around Ipoh, West Malaysia. Malay. Veterinary Journal, 7, 17 27. Shimada A., Muraki Y., Awakura T., Umemura T., Sanekata T., Kuroki T., Ishihara M. 1992. Necrotic colitis associated with Entamoeba histolytica infection in a cat. Journal of Comparative Pathology, 106, 195 199. Sommerfelt I.E., Cardillo N., Lopez C., Ribicich M., Gallo C., Franco A. 2006. Prevalence of Toxocara cati and other parasites in cats faeces collected from the open spaces of public institutions: Buenos Aires, Argentina. Veterinary Parasitology, 140, 296 301. Soriano S.V., Pierangeli N.B., Roccia I., Bergagna H.F., Lazzarini L.E., Celescinco A., Saiz M.S., Kossman A., Contreras P.A., Arias C., Basualdo J.A. 2010. A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquen, Patagonia, Argentina. Veterinary Parasitology, 167, 81 85. Traub R.J., Inpankaew T., Sutthikornchai C., Sukthana Y., Thompson R.C. 2008. PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in bangkok. Veterinary Parasitology, 155, 67 73. Traub R.J., Robertson I.D., Irwin P., Mencke N., Monis P., Thompson R.C.A. 2003. Humans, dogs and parasitic zoonoses Unravelling the relationships in a remote endemic community in Northeast India using molecular tools. Parasitology Research, 90, S156 S157. Traub R.J., Robertson I.D., Irwin P.J., Mencke N., Thompson R.C.A. 2005. Canine gastrointestinal parasitic zoonoses in India. Trends Parasitology, 21, 42 48. Wittnich C. 1976. Entamoeba histolytica infection in a German shepherd dog. Canadian Veterinary Journal, 17, 259 263. Xiao L., Fayer R., Ryan U., Upton S.J. 2004. Cryptosporidium taxonomy: Recent advances and implications for public health. Clinical Microbiologyl Reviews, 17, 72 97. Yoshida Y., Okamoto K., Matsuo K., Kwo E.H., Retnasabapathy A. 1973. The occurrence of Ancylostoma braziliense (de Faria, 1910) and Ancylostoma ceylanicum (Looss, 1911) in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health, 4, 498 503. Zhu X.Q., Gasser R.B., Jacobs D.E., Hung G.C., Chilton N.B. 2000. Relationships among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitology Research, 86, 738 744. Received: February 5, 2014 Revised: July 9, 2014 Accepted for publication: August 6, 2014