VETERINARY MEDICINE /MÉDECINE VÉTÉRINAIRE
Symptoms of Canine Leishmaniosis in Tunisian Dogs
Symptômes de la leishmaniose canine chez des chiens tunisiens
M. Gharbi · K. Jaouadi · D. Mezghani · M.A. Darghouth
Received: 11 April 2017; Accepted: 12 October 2017
© Société de pathologie exotique et Lavoisier SAS 2017
Abstract Canine leishmaniosis (CanL) is a fatal disease caused byLeishmania infantumwhich is a zoonotic proto- zoan transmitted to humans from dogs through sandflies. In Tunisia, there is a lack of knowledge on CanL risk and pro- tective factors that limits the possibilities to design control strategies. In this study, 269 dogs suffering from CanL that were presented by their owners to the clinic of the National School of Veterinary Medicine of Sidi Thabet (Tunisia), were examined. Male dogs were more infected than female dogs (sex-ratio = 1.53). The age distribution in dogs has a normal distribution; mostly animals less than 4 years old (48.7%) gets affected by this disease. The majority of the animals were German Shepherded (14.4%) followed by Staffordshire (12.6%) and Rottweiler (9.6%). Most of the dogs live outdoor (87%), did not receive any acaricidal treat- ment (88.5%) and were not dewormed (70.3%). Poor body condition (73.2%), depilation (69.1%), lymph node enlarge- ment (67.3%) and lethargy (60.2%) were the most frequent symptoms. Further studies need to be carried out to establish the presence of a relation between the zymodems and the clinical typology of CanL. It is also important to know if these disparities were due to differences in the canine popu- lation under study, to inherent differences in susceptibility to the disease or to a genetic diversity of the parasite.
KeywordsCanine leishmaniosis ·
Phlebotomus perniciosus(L.) · Dogs · German Shepherd · Staffordshire · Rottweiler · Braque français · Pitbull · Boxer ·Leishmania infantum· Symptom · District of Great Tunis · National School of Veterinary Medicine of Sidi Thabet Tunisia · Northern Africa · Maghreb
RésuméLa leishmaniose viscérale canine est une maladie fatale due àLeishmania infantumqui est un protozoaire zoo-
notique transmis aux humains par les chiens par l’intermé- diaire de phlébotomes. En Tunisie, il y a un manque d’infor- mations sur la leishmaniose viscérale canine, les facteurs de risque et de protection, limitant les possibilités de dévelop- pement de stratégies de contrôle. Les auteurs ont examiné 269 chiens présentés par leurs propriétaires en consultation à la clinique de l’École nationale de médecine vétérinaire de Sidi Thabet (Tunisie), présentant une leishmaniose viscérale canine en Tunisie. Les chiens mâles étaient plus infectés que les chiens femelles (sex-ratio = 1,53). La distribution de l’âge des chiens est en cloche, la maladie a concerné princi- palement les animaux âgés de moins de 4 ans (48,7 %). La majorité des animaux étaient de race berger allemand (14,4 %), suivis par les Staffordshire bull-terrier (12,6 %) et les rottweilers (9,6 %). La majorité des chiens vivaient à l’extérieur (87 %), ne recevaient pas de traitements acari- cides (88,5 %) et n’étaient pas vermifugés (70,3 %). Le mau- vais état général (73,2 %), la dépilation (69,1 %), l’hypertro- phie des nœuds lymphatiques (67,3 %) et la léthargie (60,2 %) étaient les symptômes les plus fréquents. Des études ultérieures sont nécessaires pour établir une relation entre les zymodèmes et la typologie clinique de la leishma- niose viscérale du chien. Il serait intéressant également de savoir si ces disparités étaient dues à une différence de la population canine étudiée, à une différence de la sensibilité des chiens ou à une diversité génétique du parasite.
Mots clésLeishmaniose viscérale ·
Phlebotomus perniciosus(L.) · Chiens · Berger allemand · Staffordshire bull terrier · Rottweiler · Braque · Pitbull · Boxer ·Leishmania infantum · Symptômes · District du Grand Tunis · École nationale de médecine vétérinaire de Sidi Thabet Tunisie · Maghreb · Afrique du Nord
Introduction
Canine leishmaniosis (CanL) [Leishmania infantum infec- tion] is a devastating vector-borne zoonotic disease prevalent
M. Gharbi (*) · K. Jaouadi · D. Mezghani · M.A. Darghouth Laboratoire de parasitologie,
École nationale de médecine vétérinaire Sidi Thabet, université Manouba, 2020 Sidi Thabet, Tunisia e-mail : [email protected]
DOI 10.3166/bspe-2018-0017
in several regions of the world including the Mediterra- nean countries. The incidence of Human Visceral Leishma- niosis (L. infantuminfection) [HVL] in the Mediterranean region was estimated to 875 new cases/year [4]. In Tunisia, the mean annual incidence of HVL was estimated to 150 cases and it is spreading from the northern to the central and southern regions of the country [15].
A good knowledge of the epidemioclinical features of this disease in dogs would lead to an early detection of the infec- tion allowing a better prognosis and a decrease of the reser- voir role of the dogs. Due to its very long incubation period and its polysymptomatic evolution, clinical diagnosis of CanL is somehow difficult [9,17]. In Tunisia, CanL is due to L. infantum;it is mainly transmitted by the bite of infected females ofPhlebotomus perniciosus(Larroussius). Although dogs are the reservoir ofL. infantum, few studies have inves- tigated the epidemioclinical typology of CanL in Tunisia [6,10,13]. Dogs are mainly infected by MON-1 zymodem [5,7,9], several minor other strains have been isolated from dogs in the Mediterranean region [19].
Few clinical studies have been reported to describe the clinical symptoms of CanL in Tunisia and in other countries of North Africa. This article therefore presents a clinical description of CanL in a Tunisian population of dogs pre- senting clinical symptoms of canine leishmaniosis.
Materials and methods
This study concerned 269 dogs suspected of canine leishma- niosis (CanL) which were presented to the hospital of the National School of Veterinary Medicine of Sidi Thabet, Tunisia. All dogs originate from the district of Great Tunis (North Tunisia), a semi-arid region where 79.5% of sandflies
belong to the subgenusLarroussius(L.) [18]. In HVL foci located in semi-arid and arid bioclimatic Tunisian stages, Phlebotomus perniciosus(L.) was the most frequent sandfly species [18].
Each dog was clinically examined for the presence of any symptom. Temperature higher than 39.5 °C was considered as fever. For each dog presenting a lymph node enlargement, a Giemsa stained lymph node biopsy was examined under microscope at ×1.000 magnification with immersion oil.
Comparisons of percentages were carried out using a Chi- square test at 5% threshold [28].
Results and discussion
In Tunisia, no studies were performed on the canine popula- tion demography; all the results reported in the present study seem difficult to compare since no previous references related to Tunisian canine population were available. A total number of 269 dogs consisting of 163 males and 106 females (sex- ratio M:F = 1.53) [p = 0.01] were confirmed by Giemsa stained lymph node biopsies to be infected by Leishmania sp. The dogs were presented by their owners to the clinic of the National School of Veterinary Medicine of Sidi Thabet (Tunisia). These dogs are not totally representative of the overall canine population in Tunisia.
The age distribution of infected dogs was bell-shaped and varied between 0,6 and 15 years (mean = 4 years). Roughly, half the animals were aged less than 4 years (48.7%); only 1.5 and 2.2% were aged less than one year and more than 10 years respectively (Fig. 1). The small number of old dogs in the group may be explained by the lifespan shortening effect of the disease but this conclusion would be difficult to assess in the absence of a control group. Several risk
Fig. 1 Relation age–prevalence of dogs presenting canine leishmaniosis / Relation âge–prévalence des chiens présentant une leishma- niose canine
factors have been reported for CanL, including age, breed and genetic background. Age seems to be an important risk factor. It was reported that the distribution of the disease is bimodal with two peaks, one for dogs aged less than 3 years and the other for those more than 8 years old [1,8].
A total proportion of 86.2% were purebred animals, Ger- man Shepherd was the most frequent breed (14.4%), fol- lowed by several others, namely, Staffordshire (12.6%), Rottweiler (9.6%), Braque (8.5%), Pit bull (7.4%) and Boxer (6.3%). Breeds of dogs such as the Boxer and Cocker Span- iel, seem to be more susceptible to L. infantum infection [16,29]. In cats, certain MHC II (Major Histocompatibility Complex class II) alleles and the Solute carrier family 11 member a1 (formerly known as N-RAMP1 (Natural Resistance-Associated Macrophage Protein), have been associated with high susceptibility toL. infantuminfection [25,27]. The majority of the dogs were held as watchdogs (58%) (Fig. 2).
Most of the dogs lived outdoor (87%) [p< 0.01] and a high similar percentage did not receive any acaricidal treat- ment (88.5%) [p< 0.01].
In Corfu (Greece), the proximity of sandflies to human habitations, especially in rural areas, ensures transmission of L. infantumfrom infected dogs to humans through sandflies;
the majority of infected dogs lived outdoor (78.7%) [23].
A total percentage of 70.3% were not dewormed (p <
0.01). Among the treated animal, only 3.34% had a deltame- thrin collar. These collars are used to prevent dogs’sandflies bites; however, and as reviewed by Otranto and Dantas- Torres [24], the efficacy of these collars varies between 50 and 100%.
Globally, the majority of diseased dogs were not receiving preventive treatments against both endoparasites and ectopar- asites, indicating a low level of veterinary care. This explains the high frequency of polysymptomatic CanL clinical cases.
Indeed, all the animals were polysymptomatic (Fig. 3), the most frequent symptom was bad condition (73.2%), followed by depilation (69.1%), lymph node enlargement (67.3%) and lethargy (60.2%) (Fig. 3).
CanL is a very common disease in the Mediterranean region. The incubation period of the disease may range from 30 days [20] to 4 years [21], so that the appearance of clinical signs can lead to misdiagnosis as a result of the complexity of the immunopathogenic interactions, the diver- sity of the affected tissues and organs, and the strain of the protozoan [12]. In the Mediterranean region, dogs are the main host of L. infantum and the main reservoir for human infection [3]. The impact of HVL is high and the dis- ease is spreading to regions previously considered as non- endemic [11]. This could be explained by climate change, human activity impact and both animals’and humans’move- ments [14].
In Tunisia, CanL is spatially associated with HVL affect- ing mostly children younger than 5 years [30]. Zoghlami et al. reported that the seroprevalence of CanL was assessed in highly endemic regions of the district of Kairouan (Central Tunisia) where more than 50 % of Tunisian HVL cases were reported. This study showed a spatial correlation between the incidence of HVL and a high CanL seroprevalence. In Algeria, there is an extension of the geographic area of CanL from west to east. There is a correlation between CanL sero- prevalence and HVL incidence; a maximum of CanL sero- prevalence was recorded in Bejaia region (47%) [2].
Fig. 2 Prevalence of canine leishmaniosis in each dog category / Prévalence de la leishmaniose canine dans chaque catégorie de chiens
In some localities of Morocco (Issouikene, Boudouait, Ouled Taleb and Brarcha), high CanL seroprevalence was associated with HVL cases [22]. The North-Eastern slope of the Rif mountains is one of the most active Mediterranean visceral leishmaniasis foci and confirms that dogs are the mainL. infantumreservoirs [26].
In this study, the presence ofL. infantumwas confirmed by Giemsa stained lymph node biopsies in the 269 dogs.
This may be explained by the clinical condition of the animal at the time of study where all dogs were classified as poly- symptomatic. Further studies are needed to find a relation- ship between the genotypes of the parasites and the clinical expression of leishmaniosis, as well as with a Tunisian ran- dom dog sample.
Acknowledgments we are indebted to Pr. Mourad Rekik (International Centre for Agricultural Research in the Dry Areas (ICARDA), Amman, Jordan) for revising the manuscript.
Conflict of interest: authors do not have any conflic of inter- est to declare.
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