EPIDEMIOLOGICAL STUDY OF ECTOPARASITES IN STRAY DOGS IN
KALUBYIA GOVERNORATE OF EGYPT
WITH A SPECIAL REFERENCE TO ITS CONTROL IN PUPPIES BY DELTAMETHRIN AND IVERMECTIN

Abstract

Mohamed Yousef Ramadan Abla Desoky Abdel‐Mageid Dept . of Parasitology, Fac. Vet. Med. Moshtohor; Dept. of Entomology Fac. of Science, Benha University
Correspondence: Mohamed Yousef,tel.0123110305‐0123324724.&
e‐mail:ahmeduosif@ yahoo.com

The present work aimed to determine and compare prevalence and intensity of ectoparasites infestation on dogs as well as their control by recent insecticides. For this purpose, a total of 94 stray dogs were examined for the presence of ectoparasites in Kalubyia Governorate during the period extended from March 2008 to Februray2009. A total number of 2964 ectoparasites were found corresponding to 5 species in 54 out of 94 examined dogs (57.45%). The collected ectoparasites were identified as 27.43% Ctenocephalides canis, 1.32% Ctenocephalides felis, 26.79% Trichodectus canis, 44.47% Rhipecephilus sanguineous and Sarcoptes scabiei var canis which infect dogs at 21/94 (22.34%), 5/94 (5.32%), 20/94(21.28%), 23/94(24.47%) and 3/94(3.19%) respectively. The mean parasitic intensity of ectoparasites was 54.89 and that of R. sanguineous was (57.3 tick/animal) followed by Tr. Canis (39.7 lice/anima), C. canis (38.71 flea/animal) ,while the lowest intensity was recorded in C. felis (7.8 flea/animal). The highest ectoparasitic infestation in dogs was recorded in spring (43.06%) followed by summer (33.33%) while the lowest percentages were recorded in autumn(13.89%) and winter (9.72%). Female dogs harbored higher infestation (74.19%) compared to males (49.21%). The ectoparasites infestation rate in puppies was 55.26 % and in young dogs 62.5% while in adult dogs (54.56%). Young dogs were infested by 4 parasitic sp. (C. canis, Tri. Canis, R. sanguineous and S. scabiei var canis) and puppies were infested by 3 sp. (C. canis, C. felis and Tri. canis) while adult dogs were infested by two sp. (R. sanguineous and C. canis). Superinfection by two ectoparasites was detected in 18 (33.33%) infested dogs. Both dipping of puppies in deltamethrin 0.025% or subcutaneous injection of ivermectin resulted in 100% reduction in the mean number of all fleas during the period extended from 48th hrs to 35th day post treatment. Deltamethrin also resulted in100% reduction in the mean number of Tr. canis from 48th hrs to 28th day post dipping.. Subcutaneous injection of ivermectin resulted in 6.67% reduction in the mean number of lice for 48th hrs post injection and 0.00 % after. It was concluded that, stray dogs specially puppies were infected by C. canis, C. felis, Tr. canis , R. sanguineous and S. scabiei var canis with higher infestation during spring. Fleas and lice were successfully treated by using deltamethrin dipping once in low concentration 0.025% which was more effective than ivermectin injection. Key wards: Ctenocephalides canis, C. felis, Trichodectus canis Rhipecephilus sanguineous and S. scabiei var canis Ivermectin, deltamethrin

INTRODUCTION

Arthropod ectoparasites constitute a diverse and highly adapted group of animals that inhibit the external body surface and internal vital systems (Soulaby, 1986). They may live permanently on their hosts or occupy the host‘s nest and visit the host periodically. In the two cases, there is a close dependency on the host for various life–sustaining resources (Kettle, 1985).

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Some species of arthropods play an important role in causing clinical disorders in man and domestic animals as well as acting as vectors of important contiguous diseases. Among them, fleas have been known to infest man and animals and may cause life threating anemia in young and/or debilitated animals (Araujo et al., 1998). Fleas are moderately host specific and the species Ctenocephalides canis, Ctenocephalides felis and, Pulex irritans are usually described in dogs (Alcaino et al., 2002). These parasites usually associated with dermatitis and affect animals to different degrees according to nutrition status of the host, its immunological condition and to parasite intensity, and in extreme cases can lead to death (Doganay, 1990, Guclu, 2002, Gonzalez, 2003). Fleas particularly the species of Ctenocephalides can cause considerable irritation to animals and humans and are responsible for cases of severe cases of allergic dermatitis (Kalkofen and Greenberg, 1974, Amin, 1976, Burgu, 1985, Alcaino 1990). Ectoparasites that affect the domestic dogs (fleas, lice and ticks) can also act as vectors of pathogenic agents, such as borreliasis, rickettsiasis and piroplasmosis and/or intermediate hosts of filarids and cestodes which cause serious diseases not only in dogs but also in humans (Leriche, 1988, Gonzalez, 2003). Various studies have found that Ctenocephalides canis, Ctenocephalides felis, Pulex irritans are the 3 most common flea species on dogs. However, the prevalence of these species varies in different geographic areas, C.felis is the most prevalent in London B(eresford‐Jones, 1981), Egypt (Amin, 1966) and Denmark (Kristensen, 1978), while C .canis is the most dominant species in dogs in the rural parts in of the United Kingdom (Chesney, 1995) and Australia (Coman, 1981). P. irritans was commonly found in dogs in Hawaii (Haas, 1967) Rebublic of Korea (Tippton, 1972). Deltamethrin is a synthetic chemical based on pyrethrin and acts on the insect nervous system to give a rapid knockdown. It is of greater stability and low mammalian toxicity. It is used for the control of ectoparasites of domesticated farm animals (Wall and Shearer, 1997, Curtis, 2004). Ivermectin is a macro cyclic lactone interferes with the gamma amino butyric glutamate of
arthropods and induces a flaccid paralysis leading to its death. Both injectable and pour‐on formulations had been shown to control internal as well as external ectoparasites (Paradis and Villenenve 1988).
The species of dog ectoparasites have been known for long time, but few studies have focused on the prevalence of their infestation in Kalubyia Governorate, Egypt although the stray dog populations is common. Consequently, The present work was conducted in order to determine and compare prevalence and intensity of ectoparasites infestation on dogs as well as their control by deltamethrin and ivermectin.

MATERIAL AND METHODS

I‐ Prevalence of different ectoparasites
Animals : A total of 94 stray dogs were collected in Kalubyia Governorate during the period extended from March 2008 to Februray2009 and examined for the presence of ectoparasites
. Their sex and age were recorded. All investigated dogs in the present study did not receive
control treatment .
Parasitological examination: The collection of ectoparasites was performed according to the protocol previously described by Gonzalez et al. ( 2003) and Aldemir (2007) as follow:
Each dog was thoroughly examined by using a fine comb in all areas of the body including head, pinna, ear canal, thoracic abdominal areas, elbow) for 10 minutes four times a day on each sampling date. The skin of dogs was rubbed with apiece of cotton soaked in ether in order to facilitate the extraction of ectoparasites by making them drowsy. The collected 
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ectoparasites were afterwards kept in 70% ethanol and identified according to the literature data given by Whitlock (1960) in addition to the keys provided by Macy and Berntzen (1971) and Wall and Shearer (1997) Areas of the skin with dermatologic lesions were moistened 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 . The detected mites were identified according to Baker (1956). The presence of 1 mite at any developmental stage of dog examined was considered to be a positive result Aldemir (2007).

II‐ Experimental study on the effect of acricides on ectoparasites in puppies

A‐ Pesticides:

1‐	Deltamethrin: (Butox®) (IR 3R). 3(2.3.dipromoving) 2‐2‐diethyl‐lcyc lopropane carboxtlate of (5) ‐ ά ‐cy‐ano‐3‐phenoxy‐benzyl. Produced by Hoechst Roussel. Vet.
2‐ Ivermectin: Nasromectin® 1% product of El nasr Pharmaceutical Chemicals Co. Abu‐Zaabal.
B‐ Experimental animal groups: Eleven puppies showed mixed infection by C. canis and Tr. cains were captured, transferred t o laboratory , classified into 3 groups and kept in separate boxes in 3 separate rooms under strict hygienic measures and treated as follows :
Group A : consists of 4 puppies and was immersed once in 0.025 % Deltamethrin for 1 min.
according to Ramadan (2004) .
Group B : consists of 4 puppies and was injected subcutaneously by Ivermectin 1% at a dose of 	0.2 mg/kg. body weight. according to Losson and Lonneux (1996 ), Payne and Ridley (1999)
Group C : consists of 3 puppies, not treated and kept as control group.
Each dog group was thoroughly investigated just before, 48 hrs, 7th, 14th 28th and 35th days
post treatment for the presence of ectoparasites.

The efficacy of insecticide was calculated as follow:

Efficacy % = number of parasite before treatment ‐ number of parasite after treatment x 100 number ofparasite before treatment

RESULTS

A total number of 2964 ectoparasites were found corresponding to 5 species in 54 out of 94 examined dogs (57.45%). The collected ectoparasites were identified as 27.43% Ctenocephalides canis, 1.32% Ctenocephalides felis, 26.79% Trichodectus canis, 44.47% Rhipecephilus sanguineous and Sarcoptes scabiei var canis which infect dogs at 21/94 (22.34%), 5/94 (5.32%), 20/94(21.28%), 23/94( 24.47%) and 3/94(3.19%) respectively.
R. sanguineous was the most abundant infesting species in this study followed by C. canis
while Sarcoptes scabiei var canis was the lowest abundant species Table (1). The table showed also that the mean parasitic intensity of ectoparasites was 54.89 and that of R. sanguineous was the highest (57.3 tick/animal) followed by Tr. canis (39.7 lice/anima), C. canis (38.71 flea/ animal), while the lowest intensity was recorded in C. felis (7.8 flea/animal). Table (2) showed that, the ectoparasites infestation rate in puppies was 55.26 % and in young dogs 62.5% while in adult dogs was the lowest (54.56%).

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Young dogs were infested by 4 parasitic sp. (C. canis, Tri. Canis, R. sanguineous and S. scabiei var canis) and puppies were infested by 3 sp. (C. canis, C. felis and Tri. Canis) while adult dogs were infested by two sp. (R. sanguineous and C. canis). Superinfection by two ectoparasites was detected in 18 (33.33%) out of 54 infested dogs. Tr. canis was detected with C. canis in 11 puppies and with C. felis in 2 puppies. In young dogs, it was also detected in with C. canis in 3 animals and with R. sanguineous in 2 animals. Single infection was detected in 36 ( 66.67%) animals mainly in adult and old dogs.
Results in table (3) indicated that the highest ectoparasitic infestation in dogs was recorded in spring (43.06%) and summer (33.33%) while the lowest percentages were recorded in autumn(13.89%) and winter (9.72%). C. felis was detected in spring (80%) and summer(20%) while S. scabiei var canis detected only in summer (100%).
Table (4) showed that female dogs harbored higher infestation by ectoparasites (74.19%) compared to (49.21% ) in males
Control of lice and fleas by using deltamethrin and.ivermectin
Table (5) showed that, both dipping of puppies in deltamethrin 0.025% or subcutaneous injection of ivermectin resulted in 100% reduction in the mean number of all fleas during the period extended from 48th hrs to 35th day post treatment . Deltamethrin also resulted in100% reduction in the mean number of Tr. canis. during the period extended from 48th hrs to 28th day post dipping and some lice were found dead, dry and attached to the skin of the treated puppies. The efficacies of deltamethrin at 35th day post dipping against Tr. Canis was 71.07 % as some lice re‐infect puppies. Subcutaneous injection of ivermectin against lice in puppies resulted in 6.67% reduction in the mean number of lice for 48th hrs post injection and 0.00 % after.

Fig(1) Trichodectus canis female

ca

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Fig (2): Ctenocephalides felis female

Fig (3): Ctenocephalides felis male

C
Fig (4) :Cetenocephalides canis female

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Table (1): Incidence and intensity of ectoparasites infesting dogs in Kalubyia Governorate (n=94)
Parasite	Number of
Infected dogs	Infestation rate	No. of Collected Parasite               %	Parasite intensity/
animal	
C. canis	21	22.34	813 	27.43	38.71	
C. felis	5	5.32	39 	1.32	7.8	
Tr. cains	20	21.28	794 	26.79	39.7	
R. sanguineous	23	24.47	1318 	44.47	57.30	
S. scabiei var canis	3	3.19	‐ 	‐	‐	
Total	54	57.45	2964 	‐	54.89	

Table (2):Incidence of ectoparasites in dogs by age
Age	No . of dogs	No. of
positive dogs	Detection rate	Parasite sp.	Single infection	Superparasitism	
Puppies (less than 6 months)	
38	21	55.26	1‐ C. canis 16l21
2‐ C. felis 5/21
3‐ Tri. Canis 13/21	5
3
‐	13
3&1 ( 11)
3&2 (2)	
Young dogs
(6 m.‐ 1 year )	
24	15	62.5	1‐ C. canis 3/15
2‐ Tri. Canis 5/15
3‐ R. sanguineous
9/15
4‐ S. scabiei var canis 3/15	‐
‐
7
3	5
2&1 ( 3 animals)
2&3 (2 animals)	
Adult dogs (From 1‐
4 years)	
22	12	54.56	R. sanguineous 11
C. canis 1	11
1	‐	
Old dogs (More than 4 y )	
10	6	60	R. sanguineous 3
C. canis 1
Tr. Canis 2	3
1
2	‐
‐
‐	
Total	
94	54	57.45		36	18	

Table (3): Seasonal incidence of ectoparasites in dogs
Parasite	Spring 	Inf.%	Summer Inf.%	Autumn Inf.%	Winter Inf.%	
C. canis	9 	42.86	7 	33.33	3 	14.29	2 	9.52	
C. felis	4 	80.00	1 	20.00	‐ 	‐	‐ 	‐	
Tr. cains	10 	50.00	5 	25.00	3 	15.00	2 	10	
R. sanguineous	8 	34.78	8 	34.78	4 	17.39	3 	13.04	
S. scabiei var canis	‐ 	     ‐	3 	100.0	‐ 	‐	‐ 	‐	
total	31 	43.06	24 	33.33	10 	13.89	7 	9.72	
Inf.% = Infestation rate

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Table (4):Incidence of ectoparasites in dogs by sex
Sex	No . of dogs	No. of positive dogs	Detection rate	
Males	63	31	49.21	
Females	31	23	74.19	
Total	94	54	57.45	

Table (5): Effecacy of Deltamethrin and Ivermectin against ectoparasites in puppies
Group	Parasite	Insecticide	Mean number of alive parasites	Effecacy %	
			Before treat.	48hrs	7th	14th	28th	35th	48 hrs	35th
day	
Group
A	C. canis
Tr. Anis	Deltam 
Ethrin 0.025%	38.25
39.75	0.00
0.00	0.00
0.00	0.00
0.00	0.00
0.00	0.00
11.5	100
100	100
71.07	
Group
B	C. canis
Tr.canis	Iverme 
ctine	39.25.
37.5	0.00
35	0.00
35.75	0.00
35.25	0.00
41.75	0.00
44.25	100
6.67	100
0.00	
Group
C	C. canis
Tr.cani	‐	40.67
39.66	39.33
39.80	34.67
40	29
43	18.67
43.67	17.33
44.67	0.00
0.00	0.00
0.00	

DISCUSSION

In the present study 2964 ectoparasites belonged to 4 species were collected from dogs in rural areas of Kalubyia Governorate and identified as 27.43% Ctenocephalides canis, 1.32% Ctenocephalides felis 26.79% Trichodectus canis, 44.47% Rhipecephilus sanguineous beside S.scabiei var canis. Similar results were recorded Aldemir (2007) in Turkey, Chee et al. (2008) in the republic of Korea and Farkas et al. (2009) in Hungary. Higher number of ectoparasites 5193 were collected from dogs in Argetina by Gonzalez et al. (2003).
The present study revealed that, the overall infestation rate by ectoparasites in different dog was 76,6%. There are no previous studies dealt with most ectoparasites in dogs in Egypt. However, Lower incidences were recorded by Aldemir (2007), and higher incidences were recorded by Liberato (1998), Bostamante (1998) and Chee et al. (2008). Such differences may be attributed to breeds of dogs, environmental condition as well as management system of breeding. 
R. sanguineous was the most abundant infesting species among dog parasites found  in this study and were evidence in 24.47% of infested dogs with high density 57.30. This result was in agreement with data of Gonzalez  et al. (2003) in Argentina,  and disagreed with Aldemir (2007) in Turkey who recorded that C. canis was the most frequent sp. Infecting dogs. Silveira et al. (2009) in Brazil also recorded infestation rate of R. sanguineous in dog 7.8%. Such difference might be due to changes in the nature of stray dogs in rural areas in Kalubyia Governorate and  the examined dogs from the pet care Dept. of small animal veterinary clinic in Brazil.

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Regarding Siphonptera occurrence, C. canis was most predominant flea in dogs than C. felis as the respective infestation rates were 22.34% and 5.32%. These results agreed with results of Gonzalez et al. (2003) in Argentina and Aldemir (2004) in Turkey. In contrast with Amin (1966) in Egypt, Painter and Echeri (1985) in USA Gracia et al. (2008) in Spain who recorded that C. felis is the predominant sp. This discrepancy is not easy to explain, but changes in the environmental and climatic factors as well as social and development of cultural aspects related to urban and rural ways of life might be play a role. it may also attributed to site of collection as Amin (1966) carried out his study on Siphonaptera in Nile valley and delta while our study was carried out in the rural areas in Kalubyia Governorate. Gracia (2008) mentioned that, the mean annual temperature is positively related to C. felis abundance and negatively related to C. canis abundance
Tr. canis was recorded mainly in dogs less than 1 year and its prevalence was 21.28 % and intensity 39.70. Our results was higher than results of Chee et al. (2008) in Republic of Korea who recorded Tr. Canis for the first time in 1% in the examined dogs and suspected a higher infestation rate if more dogs and animal shelters were involved in the investigation. The difference between the two results may be due to epidemiological factors such as weather, seasonal variation, geographical location, innate resistance and particularly the age of the animals examined.
Our results showed that female dogs harbored more ectoparasites than males. This
observation was in agreement with studies of Alcaino et al. (2002), Edward and Kristensen (1969), Gonzalez et al. (2003) Kristensen et al. (1978) and Aldemir (2007) who have also reported a greater susceptibility of females to ectoparasites. This may due to hormonal changes in females during reproductive period that could favored reinfestation by ectoparasites. In contrast Nayak et al. ( 1997), Rodriguez–Vivas et al. (2003) suggested that both sexes are equally susceptible. Chee et al. (2008) found that, the prevalence of ectoparasites was more frequent in males than females. Also, Silveira et al. (2009) reported that the incidence of R. sanguineous were significantly higher in females than in males Such differences may attributed to some environmental factors as well as differences in breeds of dogs.
In the present study, dogs less than 1 year are more susceptible to ectoparasites as the
detection rate in puppies less than 6 months was 55.26% and in young dogs 62.5% compared to 54.56% in adult dogs ranged from 1‐4 years. This result agreed with Nayak et al. (1997), Weisbroth et al. (1974), Kwochka (1987) and Chee et al. (2008). This might be due to their constant exposure to carrier mothers (Scott 1979). It was also recorded that young dogs were infested by most ectoparasites. Such higher infestation resulted from bad management under Egyptian condition and/or lack of immunity under the effect of weaning. The higher infection old dogs compared to dogs ranged from 1‐3 years Might be due to decline of immunity and exhaustion of the immune system as a result of poor feeding and superparasitism.
Concerning seasonal abundance, the overall ectoparasitic infestation rate significantly increased in warm seasons ( spring and summer) and decline in autumn and winter. Similar results were recorded in Egypt by Amin (1966). Also Alcaino et al. (2002) established that ectoparasites were predominant in spring in Chile but their population began to decline at the beginning of summer and completely disappeared in autumn. This might be due to sudden increase in the temperature in spring after winter which accompanied with high relative humidity that is important factors in acceleration of life cycles of ectoparasites.
Concerning control of fleas and lice in puppies, our results showed that, both dipping of puppies in deltamethrin 0.025% or subcutaneous injection of ivermectin resulted in 100% 

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reduction in the mean number of all fleas during the period extended from 48th hrs to 35th day post treatment. Deltamethrin also resulted in100% reduction in the mean number of Tr. canis. during the period extended from 48th hrs to 28th day post dipping and its efficacy at 35th day post dipping against Tr. canis was 71.07 %.. Subcutaneous injection of ivermectin against lice in puppies resulted in 6.67% reduction in the mean number of lice for 48th hrs post injection and 0.00 % after. Our result agreed with the previous results of Ramadan (2004) and Ramadan and Abdel, Mageid (2008) who mentioned that, spraying goats and sheep by low dilution of deltamethrin reduced the number of lice and all sprayed goats were free from lice until 28th day post spraying. The lower effect of subcutaneous injection of ivermectin against Tr. canis may be attributed to the feeding habit of this lice as it is a chewing lice, feed on debris, tissues and skin scales and not suck blood Kettle (1985). The prolonged efficacy of deltamethrin against ovine lice may attributed to its loucidal and ovicidal effect. In this respect Wall and Shearer (1997) noted that the microencapsulation of the pyrethroids prolonged their activity to weeks with greater stability as the microcapsules adhere to the insect ectoskeleton and the pyrethroid is absorbed through the chitin to produce its toxic effect.
It was concluded that, stray dogs specially puppies were infected by C. canis, C. felis, Tr. canis, R. sanguineous and S. scabiei var canis with higher infestation during spring. Fleas and lice were successfully treated by using deltamethrin dipping once in low concentration 0.025% which was more effective than ivermectin injection. The zoonotic nature of the detected fleas, lice and ticks of dogs in this study could be regarded as public health alert. To prevent the possibility of continuous transmission of the ectoparasites from dogs, practicing veterinarians should be advice who contact with stray dogs to pay attention and to be aware of ectoparasites of zoonotic importance and also to choose the more effective and save insecticide in its control.

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