Livestock Research for Rural Development 30 (8) 2018 Guide for preparation of papers LRRD Newsletter

Citation of this paper

Endo- and ectoparasites (Ixodidae) of camels (Camelus dromedarius) from Southern Algeria

Amel Djerbouh1,2, Ismail Lafri1,3, Nadia Kechemir-Issad2 and Idir Bitam2,3,4

1 Institut des Sciences Vétérinaires. Université Saad DAHLAB Blida 1. Blida, 09000. Algerie.
djerbouhveto@yahoo.fr
2 Faculté des Sciences Biologiques, Université des sciences et de la technologie Houari Boumediene (USTHB. BP 32 EL ALIA, BAB EZZOUAR ALGER, Algerie, 16111
3 UMR VITROME, Aix-Marseille Université, IRD, Service de Santé des Armées, Assistance Publique-Hôpitaux de Marseille, IHU Méditerranée-Infection, 19-21 Boulevard Jean Moulin, Marseille, 13005. France.
4 Ecole Supérieure en Sciences de l'Aliment et des Industries Agroalimentaires (ESSAIA). Algiers, 16000. Algerie

Abstract

The socioeconomic importance of camels (Camelus dromedarius) cannot be neglected in Algeria. Camel milk and meat are largely consumed in the South part of the country because of their high nutritional value. This study describes the first survey of both endoparasites and ectoparasites in the camel’s population in Algeria using different techniques and methods. During March 2011 to June 2012, a number of 785 camels (healthy and asymptomatic) were examined for the presence of ectoparasites and endoparasites in five localities in the South of Algeria. For endoparasites, gastrointestinal parasites (Helminths and Protozoans) were found in 36 faeces samples (36/ 83) with prevalence of 34 %. Haemo- parasite namely Trypanosomes were found in 18 blood samples (18/122) with prevalence of 14%. A total of 3526 ticks were collected from 580 infested camels. Entomological identification revealed the presence of six species of one genera: Hyalomma impressum, Hyalomma marginatum rufipes, Hyalomma impeltatum,Hyalomma dromedarii, Hyalomma anatolicum, Hyalomma detritum.

Key words: disease, Ixodidae, prevalence, protozoans, trypanosomes


Introduction

The camel was, and in some areas still is, vital for survival in an inhospitable environment. They serve the needs of peoples, help for thousands of years, and have provided them with food, hide and fuel. Parasitic diseases of camels are major causes of impaired milk and meat production, decreased performance or even death. Some camel parasites also present as a threat to human health. Parasitic diseases of the gastrointestinal tract are known to be the major camel health problem worldwide (Wernery and Ruger Kaddenb 2002; Radfar et al 2013).

However, the clinical manifestations of helminthosis may be subclinical or asymptomatic, in which case the animal appears normal but performs below its full potential (Borji et al 2010). Camels have important role in maintaining and transmitting zoonotic helminthes infections. Balantidium coli is a ciliate protozoan and is frequently found in the intestinal tract of over 50 species of vertebrates, such as swine, human, non-human primates, and ruminants (Vosdingh and Vanniasingham 1969) (Cho et al 2006).

Additionally, there is little report about the presence of B. coli in camel fecal samples (Cox 2005). Camel specific nematodes include; Haemonchus longistipes, Nematodirus mauritanicus, N. dromedarii but most camel nematodes are also common to sheep and goats, as an instance: Trichostrongylus prololurus,T. vitrinus, Ostertagia mongolica, Marshallagia mentulata, N. spathiger, Oesophagostomum venulosum (Banaja and Ghadour 1994;  Wernery and Ruger Kadden 2002; Parsani et al 2008). Haemonchus spp. is the main causative agent in gastrointestinal disorder in camels (Parsani et al 2008).

Coccidiosis of camels is an intestinal protozoan infection caused by apicomplexan parasites of the genus Eimeria. Disease caused by these parasites is of great economic importance because of losses due to enteritis, diarrhea and poor weight gain (Wernery and Kaaden 2002). Moreover, cestodes such as Moniezia expansa were relatively rare. Same results were found in works by Mirzayans and Halim (1980) and Borji et al (2010).

The dromedary is also frequently and severely infected by ectoparasites that weaken it and make it susceptible to secondary infections (Faye 1997). They also suffer from skin infections caused by mites and ticks and the maggots of flies which feed on open wounds or live in the nose. Most of these nuisance pests are related to their ability to transmit pathogens and economic losses due to fall in production (Jongejan and Uilenberg 2004).

The tick infestations are sometimes important (Higgins 1984). The pathogenic role of these parasites in the dromedary seems mainly due to the traumatic action (Faye 1997; Higgins 1984; Kauffman 1996). Ticks can serve as starting point of cutaneous myiasis or bacterial infections (Faye 1997; Higgins 1984). The confiscatory action is sometimes the cause of anemia and asthenia (Richard 1989).

Rickettsioses are among the oldest known vector-borne diseases. In Algeria, several species of Spotted Fiver Group Rickettsiae have been detected in ticks, including Ri. aeschlimannii inHyalomma marginatum marginatum and H. aegyptium, Ri. massiliae in Rh. sanguineus and Rh. Turanicus (Bitam et al 2006; Bitam et al 2009). Ri. aeschlimannii in H. dromedarii and H .m. rufipes were collected from camels in southern Algeria (Djerbouh et al 2012 ).

Ticks are pathogens belonging to the Spotted Fever Group Rickettsiae. In the past few years, an increasing number of studies have been performed providing new understanding on the zoonotic role and diversity of these agents. Such researches also contributed to clarify their geographical distribution; indeed, some rickettsiae which were previously considered to be restricted to a specific geographical area have then been detected in different continents (Parola et al 2013).

Trypanosoma evansi is the most pathogenic and economically important protozoan parasite of camels that causes severe disease (surra) throughout camel rearing areas of the world (Boid et al 1985) T. evansi is now considered as an emerging zoonotic parasite (Fong 2017).

In Algeria, the prevalence of camel trypanosomosis and its vectors have not yet been fully documented. A study conducted in southern Algeria indicates a prevalence of 14% (Bennoune et al 2013). Data about the frequency of tick infestation in dromedaries are limited (Djerbouh et al 2012).

This is due to the difficulty of following the herd continuously moving and the need for mobile veterinary teams in southern region. So far, little information is available about camel diseases in Algeria. In these regions, a huge number of camels (Camelus dromedarius) are concentrated in the dry desert south areas of the country and constitute the major source of animal protein for nomads. Our study was conducted to determine the prevalence rate and provide a little insight on parasitic camel diseases in the South of Algeria.


Materials and methods

Trypanosoma spp., Gastrointestinal-parasites and tick sampling

This study was carried out between May 2011 and June 2012 in five in one bioclimatic zone in Algeria (Sahara). The study was performed during a non-epidemic year on camels that were neither symptomatic nor vaccinated against diseases.

Samples were collected in: Biskra (34°51′01″ N/5°43′40″E), El Oued (33° 22' 16.823" N/ 6° 50' 52.686" E), Ghardaia (32°29′27″ N/3°40′24″ E), Bechar (31°37′00″ N/2°13′00″ O) and Adrar (27°52′27″ N/0°17′37″ O).

Trypanosoma spp. detection

Out of 785 camels submitted to different analyses, a total of 122 camels have been randomly selected for research of Trypanosoma spp. These animals were originated from (Biskra, El Oued). Camels belonged to different ages and both sexes (79 males and 43 females). Ten ml of blood were collected from each animal into a tube containing EDTA by jugular venipuncture.

Samples were transferred to the laboratory on ice with minimal delay. By using the blood smears technique, thin blood drops were prepared from each sample immediately after collection, fixed with methanol, stained with Giemsa and examined microscopically within 100 × oil immersion objective

Gastrointestinal parasites detection

Fecal samples collected from 83 Camels (38 males and 45 females) were examined to observe the prevalence of gastrointestinal parasites. Camels were originated from (Biskra, El Oued, Ghardaia). Samples were individually collected per rectum to avoid contamination by soil nematodes and conserved in the universal sample bottles identified by adhesive labels which mention the general information of the animal (age, sex, race, weight and date of sampling).

The samples were stored on ice and forwarded to laboratory for examination by flotation technique. All eggs parasites were identified based on morphological characteristics. The floatation technique is used easily for the identification of eggs of nematodes and cestodes. Briefly, faeces were comminuted in saturated salt solution, faecal debris were discarded. The fluid was poured into a straight-sided tube until a convex meniscus appeared at the top of the tube and a cover slip was applied immediately.

The preparation was allowed to stand on level surface for fifteen minutes, the cover slip was removed and applied to the glass slide and examined.

Tick collection

Ticks were collected from 580 out of 758 camels, originated from Bechar, Ghardaia, El Oued and Adrar. Ticks were manually removed from body of infested camels, taking care to avoid damage to the mouth parts. After collection, all biological materials were immediately stored in ethanol (one tube per animal) and then forwarded to laboratory.

Tick identification

Ticks collected from each animal were counted and identified by morphological criteria using standard taxonomic keys (Walker et al 2003).


Results

Trypanosoma spp. detection

In total, 122 blood samples were collected and examined. The parasites were very well visible with a spindle shaped stretched out body with one nucleus situated in its half-length and one flagellum.

Overall, 18 of the 122 samples tested positive for Trypanosoma evansi with the prevalence of 14%. No other Trypanosoma species ws detected. Out of the total examined camels, 4/122 (3 %) positive cases were males and 14/122 (11%) females (Table 1).

Table 1. Prevalence of camel Trypanosomosis in southern of Algeria (n=122)

Sex

N° of animals
examined

Origin of
animals

N° of positive
animals

Prevalence
(%)

Male

779

Biskra 56
EL OUED 23

4

3

Female

43

Biskra 33

14

11

Total

122

EL OUED 10

18

114

Gastrointestinal parasites

Out of 83 faeces samples examined, 36 camels revealed tested positive for gastrointestinal parasites (Helminthes and Protozoans) with the overall prevalence of 43% (36 /83 ) distributed as; 15/83 (18%) positive cases were males and 21/83 (25%) females (Table 2, 3). Other gastrointestinal parasites genera have been detected including: Coccidia, Eimeria, Moniezia, Balantidium (Tables 2, 3).

Most of the Camels examined presented co-infection status with two or three species of Helminth parasites. Different classes of gastro-intestinal parasites were recorded in the present study. A range of Helminths represented by Nematode Strongyle spp. (Nématodirus, Marshallagia, Hemanchus, Trichstrongylus)) presented a high prevalence.

Table 2. Prevalence of Gastrointestinal parasites (n= 36)

Parasites

No. positive

Prevalence (%)

Helminths

Nématodirus spp.

5

6

Marshallagia spp.

3

3,6

Hemanchus spp.

3

3,6

Trichstrongylus spp.

4

4,8

Moniezia spp.

3

3,6

Protozoans

Eimeria dromedarii

4

4,8

Eimeria camelii

8

9,6

Balantidium spp.

6

7,2

Total

36

43, 3



Table 3. Prevalence of gastrointestinal parasites based on sex (36/83)

Sex

N° of animals
examined

Origin of animals

N° of positive
animals

Prevalence
(%)

Male

38

(El oued 25, Biskra 5, Ghardai 8

15

18

Female

45

(El oued 29, Biskra 9,Ghardai 7)

21

25

Total

83

36

43

Ticks

A total of 3526 ticks were collected in all 580 camels delaminated at five sites located in the South of Algeria. The morphological identification of ticks using entomological keys revealed the presence of six distinct species belonging to one genera including: Hyalomma dromedarii,Hyalomma impressum, Hyalomma marginatum rufipes,Hyalomma impeltatum, Hyalomma anatolicum, Hyalomma detritum.

Table 4. The proportion of tick species collected from 580 randomly selected camels in southern Algeria

Tick species and origin

No. of ticks
collected

Proportion
(%)

Hyalomma dromedarii (El Oued 1981,Ghardaia 392, Adrar 286, Bechar 176)

2835

57

Hyalomma impeltatum (Bechar 10, Ghardaia 25, Adrar 37, El Oued 504)

5 67

16

Hyalomma marginatum rufipes (Adrar 26 , El Oued 45)

71

2

Hyalomma impressum (Gharda , El Oued 35)

38

1

Hyalomma detritum (El )

10

0.2

Hyalomma anatolicum (El Oued 5)

5

0.14

Total

3526


Discussion

Gastrointestinal parasites of camels has received the attention of many scientists in recent years. The present study illustrated the prevalence of intestinal parasites among camels in Algeria by examination of 83 samples of feces, with a prevalence of 43.4% infected with intestinal parasites. The results reported in our study are lower compared to those obtained in some countries: Jordan with a total prevalence of 98% (Moustafa et al 2003), in Nigeria with an overall prevalence of 87.3% (Ukashatu et al 2012) , in Iran with 81.3% (Anvari-Tafti et al 2013 )and Saudi Arabia with a prevalence of 59.6% (Wafa and Al Megrin 2015).

Our results were near to those obtained in Saudi Arabia with a prevalence of 38% (Al hendi 2000). The prevalence of Moniezia expansa detected in dromedary was similar to that reported in Iran 3% (Borji et al 2010) and lower in comparing with results obtained in Jordan with a prevalence of (33%) (Al-Ani et al 1998). Our results, reporting the infection of camels with Nematodirus spp. which was the most represented nematode. This finding is lower in comparing with results obtained in Iran with a prevalence of 32% (Tajik et al 2011). The infection with Eimeria spp. in camels in the present study was 8,4% represented by two species: The prevalence of Eimeria dromedarii estimated with 4,8 % is lower in comparing by results reported In India with a prevalence of 24% (Grill 1976) and in United Arab Emirates with a prevalence of 25% (Kinne and Wernery 1997). In addition to E. dromedarii and Eimeria cameli, one of the pathogenic species in camels was found in 9,6 % of samples in our study. Thus results remain lower than that obtained by Sazmand who reported a prevalence of 45% (Sazmand et al 2012)

There are a few reports about the presence of B. coli in camel fecal samples. Tekle and Abebe (2001) reported presence of B. coli in 11.9% of camel faecal samples in Ethiopia, and Abubakr et al (2000) found this parasite in camels suffering from diarrhea in Bahrain. However, in this study, we detect for the first time camel balantidiasis in Algeria (6 cases / 7,2%). Previous studies in different contries revealed that camels affected by different parasites and parasitosis are a major problem in this animal.

The camel has important role in maintaining and transmitting zoonotic helminthic infections. In this current study this is the first report of camel balantidiasis in Algeria which supports the proposed role of camel as a reservoir host for B. coli in Algeria.

One of the most important diseases among camels that cause serious economic losses in America, Africa and Asia, including Algeria. is Trypanosoma evansi ,now considered as an emerging zoonotic parasite (Fong 2017). T. evansi is the most pathogenic and economically important protozoan parasite of camels that causes severe disease (Boid et al 1985). This study is the first report of trypanosomosis in camels in Biskra and El Oued. The overall prevalence of T. evansi infection in camels was found to be 14 %. This might be associated with the season of the study period and sensitivity of the diagnostic techniques used. This result is higher compared to those found by several authors (Bennoune et al 2013. Tekle and Abebe 2001, Shah et al 2004 and Dia et al 1997) who reported a prevalence of T. evansi of 13.2%, 10.9%, 10%, 1.3% respectively in camels in Saudi Arabia, Ethiopia, Pakistan and Mauritania. In Morocco, an epidemiological study revealed that seroprevalence of Trypanosomiasis is 14 % using card agglutination test for trypanosomiasis (CATT) and 18.2 % using ELISA (Atarhouch et al 2003).

In this study higher infection rate was recorded in females than males;  this could be due to stress during pregnancy and lactation which decrease resistance in female camels and render them more susceptible to T. evansi infection. Thus, our results agreed with those reported in Pakistan (Shah et al 2004).

Ticks are blood-sucking ectoparasites which transmit serious diseases to animals and humans. They are considered as main vectors for transmission of many viral, bacterial, rickettsial and parasitical pathogens (Garcia 2007) . Six species of ixodid ticks were collected from camels in this study including: Hyalomma dromedarii, Hyalommaimpressum, Hyalomma marginatum rufipes,Hyalomma impeltatum, Hyalomma anatolicum, Hyalomma detritum. In Algeria, 9 tick species were reported to parasitize camels: H. dromedarii, H. impeltatum,Hyalomma impressum, H. scupense, H. anatolicum,Hyalomma rufipes, Hyalomma truncatum,R. sanguineus, and Rhipicephalus evertsi (Bouhous et al 2008). In Tunisia five species of ixodid ticks were collected from camels: H. impeltatum, H. dromedarii, H. excavatum, H. marginatum and R. turanicus (Gharbi et al 2013). In the present study, H. dromedarii was the predominant tick species found on infested camels, Dromedary camels are the preferred hosts of this species; however, it can infest cattle, sheep, goats and horses (Walker et al 2003). H. dromedarii was the most abundant tick specie. It represents nearly 90% of ticks infesting camels. In the present study, H. dromedarii represented the main tick species infesting camels (73.5 %) followed by H. impeltatum (23.5%) and H. marginatum rufipes (3.5%). Other tick species found in this study in small numbers were H. truncatum, H. impressum, H. anatolicum, H. detritum. In Egypt, the main tick species infesting camels is H. dromedarii representing up to 95 % of ticks (Van Straten and Jongejan 1993). Further studies are needed to improve our knowledge on camel tick phenology and their interaction with the tick fauna of other animal species.


Conclusion


Acknowledgments

We would like to acknowledge the veterinary specialists in the study localities for their appreciated help


Conflict of Interest

None declared.


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Received 4 June 2018; Accepted 8 July 2018; Published 1 August 2018

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