STUDIES ON THE PREVALENCE OF ECTOPARASITES IN OWNED DOGS AND MAJOR RISK INFESTATION TO HUMAN HEALTH IN KARACHI, SINDH PAKISTAN

STUDIES ON THE PREVALENCE OF ECTOPARASITES IN OWNED DOGS AND MAJOR RISK INFESTATION TO HUMAN HEALTH IN KARACHI, SINDH PAKISTAN Mujeeb-ur-Rahman Memon 1*, Jahan Ara Baloch 2, Abdullah G. Arijo 3, Allah Bux Kachiwal 4 and Nida Pirzada 5 1 Department of Veterinary Medicine 2 Pathology Section, Central Veterinary Diagnostic Laboratory, Tandojam 3 Department of Veterinary Parasitology, Sindh Agriculture University, Tandojam 4 Department of Veterinary Physiology 5 Baqai Veterinary College, Karachi *Corresponding author: drmujeebsau@gmail.com Abstract: The present study was conducted to investigate the prevalence, intensity and distribution of natural infestation of ectoparasites and their species in owned dogs during the period of June to November 2017 in Karachi, Sindh, Pakistan. One hundred fifty domestic dogs (90 males, 60 females) with age ranging from 60 days to 9 years were examined for ectoparasites infestation including (tick, lice, flea and mite) in Karachi city. A prevalence of ectoparasites 43.33% was identified in dogs. A total number of 164 ectoparasites were collected. The most common ectoparasites were Rhipicephalus sanguineus tick, which infested 59 of the 150 dogs (39.33%) followed by Ctenocephalides canis and Demodex canis was identified on 7/150 dogs (4.67%), Dermacentor reticulates and Trichodectes canis 6/150 dogs (4.0%) respectively and Ctenocephalides felis 2/150 (1.33%), that the highest infestation rate was seen in June (30.86%). No itching and scratching was found in 93.6 percent. Ectoparasites were significantly higher in outdoor dogs as compared with indoor group and the most tick infested location was around head and neck (60.0%). Keywords: Prevalence, ectoparasite, risk infestation, owned dogs, Karachi. INTRODUCTION Arthropod ectoparasites are found on the external body surfaces of vertebrates and constitute a diverse and highly adapted group of animals (Aldemir, 2007). Many of the species of insects belongs to phylum Arthropoda, class: Insecta, and ticks and mites class: Arachnida; order Acarina ectoparasitic of pet animals. Distress and disease are major symptoms of external parasites in dogs (Ettinger and Feldman, 1995). Both Pruritic and non-pruritic skin disorders are a common in dogs caused by ectoparasites and important reason of hypersensitivity disorders (Ettinger and Feldman, 1995). In addition, many species of arthropods are vectors for some diseases and are responsible for the transmission of disease to other animals that are transmitted to humans, causing life threatening anemia in young puppies or debilitated animals (Araujo et al., 1998). Infestation with these arthropods can cause dermatological reactions and considerable discomfort in hosts as they affects directly by feeding blood and cause allergic reactions and dermatitis. Most dogs have no clinical symptoms with ectoparasites. 19

After mosquitoes ticks are most important arthropods transmitting pathogens like protozoa, bacteria, viruses, including rickettsiae and filarial nematodes to other animals and humans. Babesia, Theileria, and Anaplasma spp. to animals is caused by ticks and are also one of the important vectors of pathogens in the world (Razmi et al., 2007). The Rhipicephalus sanguineus (brown dog tick) is the most prevalent tick in the world and a well familiar vector of many pathogens affecting dogs and occasionally humans (Dantas-Torres, 2010). Fleas are one of the most widespread ectoparasites of companion animals that nourish on the blood of their hosts. They are accountable for the invention and communication of several diseases of humans and their young ones. Pulex irritans, Ctenocephalides canis, Ctenocephalides felis are the most frequent flea species on dogs reported in various studies (Chee et al., 2008). The prevalence of these species varies in different geographic zones. Potential source of infection in human is constituted by dogs, by controlling canine parasites is the most important to get rid of clinical symptoms in diseased animals and reduce the zoonotic capacity of ectoparasites infection in human (Borji et al., 2011). The present study was aimed to determine the prevalence of ectoparasites infestation and efficacy of various acaricides in owned dogs of Karachi. MATERIALS AND METHODS Cross sectional investigation was conducted from June to November 2017 in Karachi city (Fig. 1) to record the prevalence of ectoparasites in owned dogs in various towns of Karachi, on the basis of prevalence, the number of one hundred and fifty owned dogs (90 males, 60 females) of different breeds with an age range of 60 days to 9 years were randomly selected and examined for ectoparasites. Detailed questionnaire about management, housing (outdoor, indoor), grooming, bathing interval, and purpose of keeping were obtained from owners. The ectoparasites in symptomatic cases were removed after complete physical skin examination. The hairs of dogs were combed and their skin rubbed with a piece of cotton soaked in alcohol. Deep and superficial skin scraping were prepared from all type of lesions in suspected dogs. All ectoparasites collected from each dog were transferred into labeled specimen bottles containing 70% ethanol. In the laboratory, the ectoparasites from each dog were identified, counted and recorded according to body regions. Areas of the skin with dermatologic lesions were moisture with mineral oil and scraped with a scalpel blade until capillary bleeding was visible. The scrapings were placed on glass slides with a drop of 10% KOH solution and were examined microscopically for the presence of mites. For the presence of mites, deep ear swab specimens were obtained from both ears from all dogs. All ear swab specimens were examined microscopically with mineral oil. Fig. 1. Map of Karachi. 20

Six Districts, eighteen towns and six cantonments of Karachi. (A) DISTRICT SOUTH: 1. Lyari Town, 2. Saddar Town, (B) DISTRICT EAST: 3. Jamshed Town, 4. Gulshan Town, (C) DISTRICT CENTRAL: 5. Liaquatabad Town, 6. North Nazimabad Town, 7. Gulberg Town, 8. New Karachi Town, (D) DISTRICT WEST: 9. Kemari Town, 10. SITE Town, 11. Baldia Town, 12. Orangi Town, (E) DISTRICT MALIR: 13. Malir Town, 14. Bin Qasim Town, 15. Gadap Town. (F) DISTRICT KORANGI: 16. Korangi Town, 17. Landhi Town, 18. Shah Faisal Town, CANTONMENTS: (A) Karachi Cantonment, (B) Clifton Cantonment, (C) Korangi Creek Cantonment, (D) Faisal Cantonment, (E) Malir Cantonment, (F) Manora Cantonment. Statistical analysis Dogs were grouped by age, sex, body weight and sampling time. To determine association of these factors with ectoparasites infestation, Chi square analysis and Fisher s exact test was used. Statistical similarities or dissimilarities were carried out using SPSS 18.0 statistical software. Differences were considered significant at P< 0.05 level. RESULTS The intensity and epidemiology of external parasite infestations examined by body exploration, including whole body comb and examination of skin scrapings from apprehensive skin areas are given in Tables 1,2,3,4 and 5. A total of 164 ectoparasites were found (fleas, ticks, scabies and lice). A total of 63 fleas were found, out of them Ctenocephalides canis (32.93%, n=54) and Ctenocephalides felis (5.49%, n=9), fifty nine dogs had ticks (Rhipicephalus sanguineous, 39.33%) and 6 dogs had ticks (Dermacentor reticulatus, 4.00%) which were seen mostly in June. A total of 76 ticks (46.34 %) were recovered from 65 dogs, out of 76 ticks Rhipicephalus sanguineus 73 (44.51%) and Dermacentor reticulates 3 (1.83%), a total of 19 scabies were found, out of them Demodex canis 9 (5.49%) and Sarcoptes scabiei varcanis. 10 (6.10%) and only 6 (3.66%) louse Trichodectes canis were found. R. sanguineus, C. canis, S. scabiei var. canis and T. canis was the principal species identified on infested dog (Table 1). Out of 150 tested dogs, 65 (43.33%) were positive for ectoparasites, age group (1-3 year 72.22%) was more commonly affected than older dogs (Table 2). Out of 150 examined dogs 59 and 7 were infested with ticks R. sanguineus and D. reticulates, which was mostly observed in June followed by fleas C. canis, which was seen mostly in August, seven dogs had D. canis (4.67%) which was seen mostly in October, six dogs had lice (T. canis, 4.0%) which were seen mostly in August. Mixed infestations (R. sanguineous, Dreticulatus, C. canis, C. felis and D. canis) were detected on 16 dogs (10.67%) (Table 3). Studied samples were routinely checked for clinical symptoms like intense itching and scratching (these were isolated all over the pet s body), loss of hair in various areas of body, various types of skin eruptions, some of which are crusty and may ooze pus or even bleed, head shaking or scratching of ears. Nine positive dogs had itching (13.85%) and 56 dogs (86.15%) had no any clinical symptoms. Ninety out of 150 dogs (60.0%) were males and 60 (40.0%) were females. Small-sized and low body weight dogs 21

were more frequently affected than toy groups (54.54%) (Table 4). Data on distribution of the ectoparasites in the body of the dogs were 15 (60.0%) a round head and neck followed by around the ear, 13 (54.17%), on genital area, 65 (43.33%), on belly, 25 (39.68%) on back side, 7 (38.89%), and on nose 5 (25.0%) (Table 5) respectively. Moreover, there was statistical significant difference observed between sex, age, and weight (P< 0.05). Table 1. Total ectoparasite frequency in owned dogs in Karachi, Sindh. Ectoparasites species Frequency (%) Fleas Ctenocephalides canis 54 (32.93) Ctenocephalides felis 9 (5.49) Ticks Rhipicephalus sanguineus 73 (44.51) Dermacentor reticulates 3 (1.83) Scabies Demodex canis 9 (5.49) Sarcoptes scabiei var. canis. 10 (6.10) Lice Trichodectes canis 6 (3.66) Total 164 (100) Table 2. Occurrence of ectoparasites in owned dogs by age (years) of Karachi, Sindh. Age (Years) examined dogs positive dogs Prevalence (%) < 1 61 23 37.70 1-3 18 13 72.22 4-6 30 18 60 7-9 41 11 26.83 Total 150 65 43.33 22

Table 3. Monthly prevalence of ectoparasites in the owned dog of Karachi, Sindh. Arthropod species Infested dogs Months of examined the year dogs Percentage (%) June 26 21 80.77 July 28 19 67.85 August 30 6 20.00 Rhipicephalus sanguineus September 20 5 25.00 October 28 6 21.43 November 18 2 11.00 Total Ticks 150 59 39.33 June 26 3 11.54 July 28 0 00.00 August 30 1 3.33 Dermacentor reticulatus September 20 1 5.00 October 28 0 00.00 November 18 1 5.55 Total Ticks 150 6 4.00 June 26 0 0.00 July 28 1 3.57 August 30 3 10.00 Ctenocephalides canis September 20 1 5.00 October 28 0 0.00 November 18 2 11.11 Total Fleas 150 7 4.67 June 26 0 0.00 July 28 0 0.00 August 30 1 3.33 Ctenocephalides felis September 20 0 0.00 October 28 0 0.00 November 18 1 5.55 Total Fleas 150 2 1.33 June 26 1 3.85 July 28 0 0.00 August 30 2 6.67 Demodex canis September 20 1 5.00 October 28 3 1.07 November 18 0 0.00 Total Mange 150 7 4.67 June 26 1 3.85 July 28 0 0.00 August 30 3 10.0 Trichodectes canis September 20 0 0.00 October 28 1 3.57 November 18 1 5.55 Total Lice 150 6 4.00 Mixed Infestation August 150 16 10.67 R. sanguineous, D. reticulatus, C. canis, C. felis, T. canis and Demodex canis 23

Table 4. Occurrence of ectoparasites in owned dogs by body weight. Body weight (Kg) examined dogs positive dogs Prevalence (%) < 3 55 30 54.54 3-5 25 5 20.00 5-10 50 23 46.00 >10 20 7 35.00 Total 150 65 43.33 Table 5. Distribution of the ectoparasites in the body of the dogs. Body side examined dogs positive dogs Prevalence (%) Around the ear 24 13 54.17 Backside 18 7 38.89 Around head and neck 25 15 60.00 Nose 20 5 25.00 Belly 63 25 39.68 Genital area 150 65 43.33 DISCUSSION The existence of ectoparasites in dogs is a major risk of infestation and health problem for their owners and for other animals examined in this study. Ticks have the highest prevalence 46.34% in dogs in this study which is represented by two species in dogs, i.e. R. sanguineus (44.51%) and D. reticulatum (1.83%). The presence of a large variety of ectoparasitic species in dogs in various parts of the world have shown different prevalence. This aspect may be due to differences in the geo-climatic and epidemiological factors. In Ethiopia, (Kumsa and Mekonnen, 2011) identified a prevalence of 99.5% in dogs, thus, in Albania, (Xhaxhiu et al., 2009) determined a prevalence of the ectoparasitic infestation of 79% in dogs, in Nigeria, (Adamu et al., 2012) identified ticks as the main species of ectoparasites in dogs, with a prevalence of 47% and R. sanguineus was predominant (24.3%). In Romania, previous studies have reported a prevalence of 45.52% of the infestation with C. canis in dogs, which is the main ectoparasites species identified (Tudor, 2009). In Iran, (Bahrami et al., 2012) determined a prevalence of the ectoparasitic infestation of 44.26% in dogs. In France, (Zenner and Drevon, 2003) reported the identification of three species of ticks in dogs (Ixodes ricinus, D. reticulates and R. sanguineus). Previous studies carried out on dogs in this area showed the prevalence of the species R. sanguineus compared with the species D. reticulates (Mateescu et al., 2011). 24

Ticks are spread across the continent and occur in large numbers, especially in areas with vegetation, such as forest edges but also in the urban environment, i.e. in parks and gardens. They are responsible for transmitting babesiosis to animals, which is why they require paying increased attention to this ectoparasite. Moreover, ticks are responsible for transmitting certain diseases to humans, which have recorded increased values lately. It has been stated that feeding ticks on dogs has the highest activity in May and lowest activity in September in Warsaw, Poland (Zygner and Wedrychowicz, 2006). Morales Soto and Cruz-Vazquez reported a higher prevalence of R. sanguineus in April and a lower prevalence in February and December on dogs in the Morelos area of Mexico (Morales-Soto and Cruz-Vazquez, 1998). In our study the higher prevalence was in June and the lower prevalence was in November. Fleas have the Second highest prevalence ranking 63 (38.41%) in this study in dogs, two species were identified: C. canis 54 (32.93%) and C. felis 9 (5.49%). In Pakistan, (Arijo et al., 2007) identified the presence of the species C. felis in dogs, with a prevalence of 34%, (Beck et al., 2006) determines a prevalence of the infestation with fleas of 5.13% in dogs. Flea infestation of animals and of their environment is frequently seen. The high prevalence of this ectoparasites is a serious problem for practitioners. Firstly, because they cause discomfort the hosts by stinging, causing allergic reactions and itching. Secondly, they are also a vector for numerous parasitic and microbial agents with medical veterinary and human importance. In our study, flea infestations on dogs were observed in August and November. The peak of flea infestation rate was 11.11% observed in November and June and in October months infestation was 0%. Results of this study are not in agreement with other authors who observed that peak flea infestations occurred during the annual warm months (Cruz-Vazquez et al., 2001). The present study showed that ectoparasites were more predominant in females than males; the reason for this discrepancy is unclear but may be in part related to the fact that females have longer life than males. Female abundant infestation has also been reported by other researchers (Edwards, 1969). Greater susceptibility which observed in female dogs than males in this study was in agreement with (Feather et al., 2010). This might be due to the fact that females kept were confined to avoid unwanted breeding and hormonal changes during reproduction period. Scabies were the third ectoparasitic species in terms of frequency in dog with values of 11.58%. While two species were identified in dogs, D. canis (5.49%) and S. scabiei var. canis (6.10%) respectively, significantly lower values of scabies infestations have been reported in several previous studies (Aldemir, 2007; Xhaxhiu et al., 2009; Duarte et al., 2010 and Bahrami et al., 2012). Ali et al., (2011) determined a prevalence of scabies infestation of 62.5% in dogs, noting that the most frequent species was S. scabiei var. canis with 50%, followed by D. canis with 35.4%. (Jamshidi et al., 2010) determined a prevalence of scabies infestation of 25.9%, the species S. scabiei var. canis being the most frequently found, with 21%, followed by O. cynotis (2.8%) and D. canis (2.1%). 25

A louse was the fourth ectoparasitic species in terms of frequency in dog with values of 3.66% in this study. Low levels of lice infestations have been reported in previous other (Gonzales et al., 2004; Jittapalapong et al., 2008 and Chee et al., 2008). On the other hand, (Mosallanejad et al., 2011) reported lice as the main species of ectoparasites in dogs, with a prevalence of 8.73%. These differences can be explained by the geographical differences, the animal population studied, the time dedicated to the study. Lice cause discomfort and dermatitis to the infested animals, but can also be a host for the tapeworm D. caninum (Niculescu and Didã, 1998). The low prevalence of these ectoparasites compared to the other species may be the result of applying preventive treatment against fleas. Results also demonstrated that those dogs who were kept in soil or grass ground were more at risk for ectoparasite infection than those kept at home. The present study is the first study on the prevalence of ectoparasites infestations in owned dogs in Karachi city. The prevalence of ectoparasites infestation was higher among 1-3 years old dogs (72.22%) in present study but in Afghanistan it was stated that dogs less than 1 year old are more susceptible to ectoparasites infestations owing to their constant exposure to carrier mothers (Chee et al., 2008). Dogs less than 3 kg body weight were more affected than heavier groups. This finding may be related to age, because most of the affected animals of this group were less than 1 year old. The results obtained in this study showed that simple infestations were predominant in dogs. This study shows that there is a high prevalence of ectoparasites in dogs in the examined area. This aspect is significant both for veterinarians as well as for human doctors, due to the effects these ectoparasites cause on animals and humans. Informing pet owners about the role of ectoparasites in the transmission of zoonoses and educating them to observe the preventive and control measures against parasites is an important step in reducing the prevalence of parasitic infestation. Due to the well-known the role of vector some species of ectoparasites have in the transmission of infectious diseases, we recommend the application of the preventive treatment against parasites as early as possible to pets. CONCLUSIONS The study concerning ectoparasitoses in dogs in Karachi, recorded a high prevalence 43.33% in dogs. The main species of ectoparasites identified in dogs were tick, fleas, scabies and lice, respectively. The young individual was found to have the highest rate of infestation with ectoparasites, compared to adult animals. To the best of our knowledge this is the first study conducted in Karachi that examined the prevalence of ectoparasites in owned dog populations. However, this survey was limited to the Karachi area and additional studies are required to complete these findings and help veterinarians to prepare a complete program for the control of these parasite and their associated diseases. 26

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