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The effect of introducing Mustela nivalis to control the reservoirs of Zoonotic Cutaneous Leishmaniasis at Ain Skhouna in Algeria.

ABSTRACT

A recrudescence of the Zoonotic Cutaneous Leishmaniasis has been recorded in Algeria and constituted a serious problem of public health. The disease prevails in Algeria in an endemo-epidemic mode. In this context, the area of Ain Skhouna situated near to the Chott chergui has recorded several human cases. Filed into the middle of the steppe with a semi-arid climate, this area was chosen to conduct a bio-ecological study on rodent reservoirs from July 2010 to August 2013. Biotope analysis and active burrows counting were realized on nine sites in order to cover the pullulated rodent areas. The catching was realized through each site. Rodents were manually caught after flooding by water cisterns and breaking their burrows. This type of trap was preferred over the rest of traps used because it can trap other small animals. This allows the capture of live animals which offers a very good exploitation. The preparation of faunistic material was carried out by inhalation of volatile anesthesia. Identification, biometric measurements, necropsy of rodents and histological sections of lymph nodes which drain ears lesions were done at the laboratory. Results showed an average of 2 to 3 active burrows per [m.sup.2]. They also showed a varied population of rodents, 84% of Psammomys obesus and 16% of Meriones shawi. The medullary macrophages of lymph nodes revealed numerous amastigotes inside their cytoplasm seen as small intracellular rounded bodies. Later, we introduced captured weasels which we have identified as Mustela nivalis inside a closely monitored zones and investigated their predator effect on rodents and the ecosystem of Ain Skhouna. After a daily monitor of four week, we noticed a gradual decrease until total absence of rodents. Visits on site showed inactive burrows until 2013. Therefore this voracious behavior is an efficient measure of controlling these agricultural devastating reservoirs by its simplicity and ecological impact on the environment.

KEYWORDS: Zoonotic Cutaneous Leishmaniasis, rodents, weasel, biological control.

INTRODUCTION

Zonotic Cutaneous Leishmaniasis is widely spread, with one third of the cases occurring in various epidemiological areas in the US, Mediterranean region, and West of Asia from the Middle East to central Asia. The Global reported ZCL is 214,036 cases per year and its estimated annual incidence ranged from 690,900 to 1,213,300. The highest rates of this disease have also been reported in 10 countries, including Afghanistan, Algeria, Columbia, Brazil, Iran, Syria, Ethiopia, North Sudan, Costa Rica and Peru comprising between 70% and 75% of world's rate. In Algeria, from 2004 to 2008, the reported cases were 44 050 of ZCL, the estimated annual incidence was 123,300 to 202,600 [1]. Zonotic Cutaneous Leishmaniasis dominates the epidemiological situation and parasitic diseases in Algeria. This infestation spreads rapidly giving rise to new foci [2]. According to the Ministry of Health (2010), more than 40 wilayas are affected today. At the origin of this explosive situation, pollution and the deterioration of natural ecosystems have contributed greatly to the development of the disease besides to the spread of Leishmaniasis at an alarming rate across the globe [3]. Zoonotic Cutaneous Leishmaniasis (ZCL) is a parasitic disease called also oriental sore caused by Leishmania major which infests the macrophages of several mammalian including the human being. This form of leishmaniasis occurs in arid and semi-arid areas considered as the ideal biotope for rodents. The most common reservoirs of the disease are gerbils which belong to the genus of Meriones and Psammomys. Recently the Algerian hedgehog, Atelerix algirus was found naturally infested with leishmania parasites in Tunisia [4]. Rodents share with men most of the terrestrial habitats [5]. They count nearly 1700 species and thus consist the largest population of the mammalian class which represents 50% of it distributed throughout the world [6]. The rodents are cosmopolitan and occupy the majority of terrestrial ecosystems by adapting themselves to the various biotopes in which they find food and refuge [7]. According to [8] and the observations realized by [9] a female rodent can have a progeny of 2640 individuals per year. Rodents have extremely attracted attention the agricultural sector, in particular the families of Muridae and Gerbillidae which gnawed produce. In addition of being harmful to agriculture, they were also considered as being reservoirs and carriers for infectious agents [10]. [11] described in details the inflammatory process of lesions of cutaneous leishmaniasis. It takes the form of chronic ulcers which develop from inflammatory papules at the site of the Phlebotomus bite. The leishmania are inoculated by the biting insect and are soon ingested by histyocytes. Rapid proliferation of the protozoa disrupts the phagocytes, and the released organisms are ingested by further phagocytes to repeat the process. Lymphocytes and plasma cells surround the cutaneous lesion and the neutrophiles are attracted to the debris. When the inflammation extends to the overlying epithelium, ulceration occurs. Numerous parasites are present within the macrophages and some are free in tissue. The actual measures rodent control are the use of rat poison, poisonous gases, ploughing which unfortunately leads to rodent movements and water flooding prove to be costly and rarely used. Actually, these measures are not sufficiently effective on the ground. In this context, the areas of Ain Skhouna were chosen as an experimentation field. It covers an areas of 404.4 k[m.sup.2] for a population of 7129 habitants. Ain Skhouna is an integral part of the Chott Ech Chergui basin with has an areas of 40.000 k[m.sup.2]. This Chott gives the region a special natural ecosystem with a humid land nestled in the middle of the steppe. This choice was justified on the one hand by the connection between development of rodent reservoirs of ZCL and the epidemics recorded in this zone from 2002 to 2006, and on the other hand, the presence of groundwater which promote the growth of Chenopodiaceae, a large plant known as the favorite diet for rodents [12]. During our research work and according to the observations on rodent behaviour realized by the inhabitants of the areas which the female rodent gives birth to an offspring called locally Sebseb then turns at the mature age against and devours her. Among predators, weasel is the smallest. Weasel belongs to the Mustelidae family. [13] reported that there are variations in size according to region and gender. The largest are around the Mediterranean where they can be found solitaires on the cereal plains if there are enough preys. The male is larger than the female. A family of weasels eats from 31 to 46 kg of meat per year or 1240 to 1840 small rodents per year. However, this beneficial animal is threaten by wild dogs, cats, jackals, owls, eagles and vipers. Rodent intake by weasel is frequent, about 10 per day [14]. This study aims firstly to investigate the reservoir hosts and to analyze biometric, pathological and parasitological data collected in areas of Ain Skhouna. Secondly to clarify the Sebseb behavior which pointed out our curiosity and finally to experiment it as control measure for rodent ZCL reservoirs.

MATERIALS AND METHODS

From July 2010 to August 2013, our work is based on using an ecosystem approach that promotes participatory procedures. In the beginning, a field visit was carried out with the aim of meeting local citizens, exploring the natural ecosystem of ZCL, choosing the study site and the preparation of the logistic. Three research teams were designed to supervise the work on the reservoir the vector and the vegetal. Data from complaints of the inhabitants following the damage caused by the rodents, the availability of biological material such as the presence of burrows of rodents, their belly traces, footprints, droppings, the proposal by the local inhabitants on the method of capture of rodents and the epidemiological situation of human ZCL cases in the local health center were collected.

1. Materials:

1.1 Presentation of Ain Skhouna:

The commune of Ain Skhouna is located 80 km south east of the chief town of the wilaya of Saida. It has an altitude of 1000, a longitude of X1 = 34[degrees]80 - X2 = 34[degrees] 15 and a latitude of Y1 = 1.55[degrees] - y2= 2.30[degrees]. The study area is near the inhabitant residences and limited to the east by the Chott Ech Chergui basin (Fig1). In order to cover the entire area, nine sites of 01 hectare each were selected according to the presence of burrows, multiplication of rodents, abundance of the Chenopodiaceae vegetation and anthropisation (Fig 2). These sites were duly identified by GPS and shown in Tab 1.

1.2 Counting of burrows:

The indirect method described by [14] was realized in order to facilitate their enumeration. From each site of 1 hectare, a surface area of 100 [m.sup.2] was retained. Throughout each surface area, 5 squares of 1 [m.sup.2] of side were randomly selected to count the burrows and to calculate the average by site. The abundant count of active burrows revealed us the dynamic of the rodent population to study

1.3 Faunistic material:

With the help of the local inhabitants, rodents were manually caught after flooding by water cisterns and breaking their burrows (Fig 3). The cages were numbered to the corresponding sites.

2 Methods:

2.1 Processing of catches:

The capture of rodents took place during the month of July 2010, at the beginning of the day and before sunset and kept in identified cages. Rodents and the Sebseb vertebrate were brought to a veterinary laboratory for better safety and protection against infection (Fig 4). Their preparation was carried out by inhalation of volatile anesthesia in order to facilitate the external examination. Concerning the aggressive vertebrate, special preparation using an analgesic followed by an anesthesic for a better care by ensuring its relaxation during measurements. Species, genus, estimated age, sex, color and special characteristics such as small sores on ears, body surface and extremity of forelegs were noted.

2.2 Morphometry and identification:

Once anesthetized, the rodents were placed on the dorsal face, well flatted without stretching and measured. Biometric measurements of the head, body, tail, ear, legs as well as live weight of each rodent were carefully recorded (Fig 5).

The identification was carried out according to the rodent identification key described by [15, 16, 17] and [18]. The critera for identification of the vertebrate were described by [13].

2.3 Sex determination:

Sex of rodent was determined by external observation of the position of the genital orifices in link to the anus. The female has a developed clitoris and a genital cleft above the anus. Whereas the males have their penis much more distant rom the anus [18].

2.4 Dissection and removal of lymph nodes:

Necropsies were performed in laboratory because of better facilities and senior staff to consult. After systematic examination of the thoracic, abdominal cavities and exposed organs, the size of the prescapular and mesenteric lymph nodes of each rodent was noted. As it is known, that macrophages might inter act with parasite antigens, migrate to distant locations such as the intestines [19]. The lymph nodes were cut transversely and immediately placed in Bouin fixative for 5 days, then processed by standart paraffin methods and finally stained with haematoxilin, eosin and Giemsa [20]. Parasitological examination of the lymph nodes slides for amastigotes inside the macrophages were microscopically realized at x 600-1000 magnification.

2.5 Introduction of weasels:

After confirming that the captured vertebrate belongs to Mustelidae family, an experimental introduction was carried out during the month of August 2010. It consisted of selecting randomly and fencing two separate zones. Each zone had an area of 500 [m.sup.2]. The first one (zone A) used as control where no weasels were introduced and the zone (B) in which adult, captive weasels were released. These zones were intentionally located far from each other in order to avoid any passage of weasels and rodents from one area to another. These weasels, three males and seven females were captured with a great help to us by young local inhabitants during the year 2011. During their captivity, their carnivorous diet was confirmed as they fed only on traditional byproducts of poultry and livestock and captured rodents. Before starting the experiment, the weasels were starved with the exception of water and released in the zone B during August 2011. Despite this number of weasels which really exceeded their prey requirements, it assured at the same time the permanent presence of weasels against animal pests effect. Burrow activity and presence of rodent dynamic were verified by the presence of rat droppings in and around the burrows early in the morning and at sunset for a period of one month.

Results:

1 GPS surveys of the sites:

The geographical data of our studied sites are between 988.4 m and 1007 m for altitude and between N (34[degrees] 29950- 34[degrees] 30040) and between E (00050[degrees] 226- 00050[degrees] 963) for GPS coordinates. The maximum altitude between the various sites is negligible and is in the order of a few meters. The GPS gap is also negligible. (Tab 1)

2 Counting of burrows:

This counting showed an average of two to three burrows per square meter within the selected sites and revealed us in general a homogeneous spatial repartition of rodents (Tab 2).

3 Morphometric identification of the captured rodents:

According to the rodent identification key described by [15, 16, 17] and [18], the two species captured belong to the Muridae family which are Psammomys obesus and Meriones shawi (Tab 3). This identification enabled us to notice that P. obesus is dominant and represents 84% of the catches.

Sex determination:

The sex ratio of captured rodents revealed a predominance of females in comparison to males (Fig 6) In the Psammomys obesus species, the female population is almost the twice of the males. In the Meriones shawi species, females also predominate over males.

5 Morphometric identification of the captured weasel:

The manual caught after flooding by water cistern in site 7 has also allowed to capture accidentally a larger and strong animal with ferocious appearance showing its aggressive canines during handling (Fig 7). This mammal predator was recognized by the local inhabitants to be the Sebseb. The criteria for identification of the weasel described by [13] enabled us to confirm its belonging to Mustela nivalis species.

6 External and parasitological examinations:

The macroscopic examination showed in general no lesions, a part from small sores and ulcerations which were observed on the external ears and the surroundings of the eyes of 4 rodents belonging to Psammomys obesus. During necropsy, these rodents revealed hypertrophic lymph nodes with some degree of congestion. The microscopic observation showed medullary macrophages of lymph nodes with numerous amastigotes inside the cytoplasm seen as small intracellular rounded bodies (Fig 8).

6. Monitor of the experimental introduction of weasels:

The weekly observations carried out during August 2011 on both zones revealed gradual disappearance until the absence of rodent only in zone B. This was confirmed by the water flooding trapping realized on the fourth week of August (Tab 5). The burrows remain inactive until 2013.

Discussion:

Climate changes and desertification observed in the wetland of Ain Skhouna could play a role in the extension of the disease. [21] stated that the decadal increase in the number of ZCL occurrence in the region suggests that changes in climate increased minimum temperatures sufficiently and created conditions suitable for endemicity that did not previously exist. [22] added that the recent human outbreaks which occured during the 2012-2013 epidemic of Ksar Ouled Dabbab in Tunisia was related to ZCL. It probably followed recent environmental changes. In fact, the construction of a dam, a lake and a semi-urban residential area from which the majority of cases came from districts located on the edge of the new hill lake and comprising several irrigated plots. The inhabitants reported a recent proliferation of meriones and sandflies.

Morphometric identification is a very important criterion for distinguishing between two species of rodents. Our species identification agrees with the study realized by [23] conducted in a zone of the large Chott Ech Chergui and which was mainly based on the relationship between the rodents and the plant biotope. These authors noted that Psammomys are not restricted by a limited diet. They revealed the more salinity increases due to the Chott Ech Chergui which is most often inundated with salty water, the more the grassulaceous plants gain the wetland and the more these rodents find food, the less they find it difficult to settle down. [7] reported also that Psammomys obesus is a strict herbivore fond of succulent Chenopodiaceae. We think that the low number of Meriones shawi caught compared to Psammomys obesus is mainly due to their strictly granivorous diet and therefore they are obliged to migrate to neighboring farms characterized by extensive cereal farming. [24] supported this observation and added that the Meriones is a migratory species by nature.

[25] reported that the months of July to August are devoted for females to suckling their young rodents in the nest particularly in the Meriones species which coincide with our study period and facilitated their trapping in large numbers compared to males.

[26] realized a study on human ZCL and highlighted the spread of L. major from the arid zones towards the semi arid areas, particularly in the village of El M'hir, located south, about 180 km of Algiers and on the north side of the chain of the Tell Atlas, in the basin of the Soummam. He reported that on the eight captured Psammomys obesus showing lesions on ears, five strains were isolated and identified to belong all to L. major MON-25. In our study, among the captured Psammomys obesus, only four showed skin lesions on the external ears and the surroundings of the eyes. In parallel to our study, the vector research team has trapped sand fly and identified Phlebotomus papatasi in the same study area [27]. The prescapular lymph nodes drain small sores of the ears. They serve as a no specific mechanism by filtering noxious agents such as protozoan with the help of macrophages. The microscopic observation showed medullary macrophages of lymph nodes with numerous amastigotes inside the cytoplasm seen as small intracellular rounded bodies. Their kinotoplast were not clearly seen, probably due to chemical aggressions during the histological process. [28] reported that after the femeale bite, the inoculated promastigotes are phagocytized by macrophages where they change into amastigotes inside these cells then migrate with macrophages to multiply in cells of various tissues. These last phases represent the diagnostic stages of leishmaniasis using the Giemsa and Immunoperoxidase staining. [29]

The presence of weasels in the burrows has been confirmed by [13]. In fact, this author added that by their agility, these carnivores can slip into burrows of 2 cm of diameter and exercise their hunting mode considered as the most effective control on the population of small rodents. The author also reminded that in the antiquity, the weasel played the role of the cat in the house.

Actually, the fight against the reservoir is difficult. The use of poisonous baits is to be avoided because of the lack of a bait presentation technique compatible with the rodent behavior, non-target species and predators. Also the development of a strong physiological resistance to coumatetralyl under antagonistic K vitamin exposure in rodents which may be related to metabolic enzymes [30]. Similarly, the use of herbicides against Chenopodiaceae is prohibited because steppe areas rich in Psammomys are also used as pasturelands for cow, sheep and goat.

Our successful introduction of weasel in the endemic areas by using the predator effect of weasel against the reservoir of ZCL is necessary knowing the fact that the climate changes and desertification observed in the steppe area northern Sahara further the extension of the disease. As far as we know, such biological rodent control through the use of wild carnivores has been rarely used [31]. A common vole named Microtus arvalis and introduced a few years ago in the Tershelling islands has been eradicated and regulated at a low and constant density after the voracious effect of the weasel.

[FIGURE 1 OMITTED]
Psamomm ys obesus F  49%
Merione shawi M      2%
Merione shawi F      13%
Psamomm ys obesus M  36%


[FIGURE 7 OMITTED]

[FIGURE 8 OMITTED]

Conclusion:

Our study realized in the area of Ain Skhouna highlighted the role of the reservoir and the favorable environmental conditions in the expansion of ZCL to northern western territories of the pre-Saharan regions after crossing the mountain of the Tellian Atlas. The influx of vulnerable human populations and ecological and environmental changes of the Chott leading to a multiplication of the reservoir population caused epidemic outbreaks in this endemic zone during the recent years. The establishment of a biological preventive program using weasels which eliminates the rodent reservoir is essential and will control better this pathogenic complex.

ACKNOWLEDGEMENTS

This article is based on research supported by the cooperation project Algero-Canadian CRASC/CRDI (Leila Houti) Code 1057738-011: Exploration of the adaptation scenario: Cutaneous Leishmaniasis and climatic changes in Algeria. Warm thanks are due to Z. Harrat, Parasitology Department, Pasteur Institut Algiers.

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[30] JULIE ANDRU., 2012. Les populations invasives de rongeurs en milieu agricole: These de doctorat: une etude menee dans des cultures de grande echelle, les plantations de palmiers a huile en Indonesie - Approche paysagere, genetique et ecotoxicologique. pp: 123.

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(1) F. Benmahdi-Tabet aoul, (2) K. Bouderoua, (2) T. Benmahdi, (3) A. Ammam

(1) University of Mostaganem Abelhamid Ibn Badis- Faculty of Exact Sciences and Sciences of the Living- Mostaganem Department of Agronomy. Algeria.

(2) Regional Veterinary Laboratory of Mostaganem-Algeria.

(3) Laboratory of bio-toxicology pharmacognosie and biological valorisation of the plant. University of Dr Moulay Tahar Saida. Algeria

Address For Correspondence:

F. Benmahdi-Tabet aoul, University of Mostaganem Abelhamid Ibn Badis- Faculty of Exact Sciences and Sciences of the Living-Mostaganem Department of Agronomy. Algeria.

This work is licensed under the Creative Commons Attribution International License (CC BY). http://creativecommons.org/licenses/by/4.0/

[ILLUSTRATION OMITTED]

[ILLUSTRATION OMITTED]

Received 12 January 2016; Accepted 10 March 2017; Available online 26 March 2017
Table 1: GPS surveys of the sites catches.

Zone    Altitude/m     North/East

Site 1  1007           N: 34[degrees] 30 042 E: 000 50 822
Site 2  1006           N: 34[degrees] 30 038 E: 000 50 825
Site 3  999            N: 34[degrees] 30 018 E: 000 50 829
Site 4  1001           N: 34[degrees] 30 013 E: 000 50 835
Site 5  988.4          N: 34[degrees] 29 964 E: 000 50 835
Site 6  994.5          N: 34[degrees] 29 950 E: 000 50 875
Site 7  993.2          N: 34[degrees] 30 016 E: 000 50 226
Site 8  993.9          N: 34[degrees] 30 031 E: 000 50 943
Site 9  999.2          N: 34[degrees] 30 003 E: 000 50 963

Table 2: Counting of burrows

Selected square of 1  Site 1  Site 2  Site 3  Site 4  Site 5
[m.sup.2]

1                        2       3       4       1       1
2                        3       2       2       1       1
3                        3       2       1       3       3
4                        1       0       3       4       2
5                        1       4       5       1       3
Average/[m.sup.2]      2       2       3       2       2
Selected square of 1  Site 6  Site 7  Site 8  Site 9
[m.sup.2]
1                        3       2       2       4
2                        3       2       2       2
3                        3       2       3       3
4                        1       1       3       2
5                        2       3       0       2
Average/[m.sup.2]      2       2       2       3

Table 3: Morphometric identification of the captured rodents

Psammomys obesus          Characteristics of the species

Weight/g                /
Ear/cm                  Round and short
Tail/cm                 Black to the end of the tail
Head and body/ cm         Long nose
Head, body and tail/cm  /
Forefeets/cm            Claws of 5 mm
Color of the coat         Sandy in color surmounted by a
                          black furrow with white belly
Eye shape                 Fairly large, black and protruded
Corpuscle                 Very obese (strong)
Meriones shawi
Weight/g
Ear/cm                  Slightly wide
Tail/cm                 Black brush at the end of the tail, less
                          long than the body, 30-40mm. The dorsal
                          face of the tail is more pale than the
                          cinnamon colored belly. Tail < Head + Body.
Head and body/ cm         Long nose
Head, body and tail/cm  /
Forefeets/cm            /
Color of the coat         Fawn back and white belly
Eye shape                 Round, large and black almond in
                          color with a pale band around the eyes.
Corpuscle                 Slightly obese
Psammomys obesus          Reference    Interval of measurements
Weight/g                125-208      114-260
Ear/cm                  1-1.9        1.5-1.6
Tail/cm                 9-15.0       9-13.0
Head and body/ cm         13.0-18.5    13.0-18.5
Head, body and tail/cm  22.0-33.5    20.3-31.0
Forefeets/cm            2.9-6        3.0-4.5
Color of the coat                      Confirmed
Eye shape                              Confirmed
Corpuscle                              Confirmed
Meriones shawi
Weight/g                105-250      94-134
Ear/cm                  1-2          1.5
Tail/cm                 12.0-18.0    9.0-11.0
Head and body/ cm         13.0-20.0    13.0-18.0
Head, body and tail/cm  25.0-38.0    22.0-29.0
Forefeets/cm            3,2 - 4,2    3.0-3.7
Color of the coat                      Confirmed
Eye shape                              Confirmed
Corpuscle                              Confirmed

Table 4: Morphometric identification of the captured weasel

Mustella nivalis   Characteristics             Reference  Interval of
                   of the species                         measurements

Weight/g        /                          40-140     340
Head/cm         /                         /         5.5
Ear/cm          /                         /         15
Forefeets /cm     /                         /         4.5
Tail/cm          Black brush at the end of   4-6        8
                   the tail of 1.4cm Tail
                   < Head + Body
Head and body/ cm  Long nose                   16-25      25.5
Color of the coat  Reddish-brown                          Confirmed
Eye shape          Black and protruded                    Confirmed
Corpuscle          Very obese (strong)                    Confirmed

Table 5: Evolution of rodent following the introduction of weasels
Days/weeks  Control zone (A) Rondents

Day 1         19 in the morning and 11 at sun set, burrows: actives
Week 1        14 in the morning and 11 at sun set, burrows: actives
Week 2        14 in the morning and 09 at sun set, burrows: actives
Week 3        14 in the morning and 10 at sun set, burrows: actives
Week 4        Capture of rodents by water flooding of Psammomys obesus
              and Meriones shawi burrows
Days/weeks  Experimented zone (B) Rodents + 10 weasels
Day 1         10 in the morning and 17 at sun set, weasels outside,
              burrows: active
Week 1        04 in the morning and 03 at sun set, weasels outside,
              burrows: actives
Week 2        Absence of weasels
Week 3        Burrows: inactive
Week 4        Absence of rodents after water flooding of burrows
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Author:aoul, F. Benmahdi-Tabet; Bouderoua, K.; Benmahdi, T.; Ammam, A.
Publication:Advances in Environmental Biology
Article Type:Report
Geographic Code:6ALGE
Date:Mar 1, 2017
Words:5220
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