Seroprevalence of Toxoplasma Gondii in Commensal Rodents Sampled Across Senegal, West Africa
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Parasite 25, 32 (2018) Ó C. Brouat et al., published by EDP Sciences, 2018 https://doi.org/10.1051/parasite/2018036 Available online at: www.parasite-journal.org RESEARCH ARTICLE OPEN ACCESS Seroprevalence of Toxoplasma gondii in commensal rodents sampled across Senegal, West Africa Carine Brouat1,*, Christophe Amidi Diagne1,2, Khadija Ismaïl3, Abdelkrim Aroussi3, Ambroise Dalecky4, Khalilou Bâ2, Mamadou Kane2, Youssoupha Niang2, Mamoudou Diallo2, Aliou Sow2, Lokman Galal3, Sylvain Piry1, Marie-Laure Dardé3, and Aurélien Mercier3 1 CBGP, IRD, CIRAD, INRA, Montpellier SupAgro, Univ. Montpellier, 755 avenue du campus Agropolis, 34988 Montferrier-sur-Lez cedex, France 2 BIOPASS, CBGP-IRD, ISRA, UCAD, Campus de Bel-Air, BP 1386, Dakar CP 18524, Senegal 3 UMR-S 1094, Neuroépidémiologie Tropicale, INSERM, Univ. Limoges, 2 rue du Dr Marcland, 87025 Limoges, France 4 LPED, IRD, Aix Marseille Univ., Centre St Charles, case 10, 3 place Victor Hugo, CS 80249, 13331 Marseille cedex 03, France Received 6 February 2018, Accepted 20 June 2018, Published online 16 July 2018 Abstract – Risks related to Toxoplasma gondii infection in humans remain poorly known in Senegal. Although rodent surveys could help to assess the circulation of T. gondii, they have seldom been set up in sub-Saharan Africa. The aim of this study was to examine Toxoplasma seroprevalence in rodents from villages and towns across Senegal. Rodents were sampled in 40 localities using a standardised trapping protocol. Detection of T. gondii antibodies was performed on 1205 rodents, using a modified agglutination test (MAT) technique. Seroprevalence data were analysed depending on geography, the local rodent community, and individual characteristics of the rodent hosts. We found 44 seropositive rodents from four different species (Mastomys erythroleucus, Mastomys natalensis, Mus musculus domesticus, Rattus rattus). Toxoplasma seroprevalence was low, averaging 4% in the localities. Higher Toxoplasma seroprevalence (up to 24%) was found in northern Senegal, a region known to be the heart of pastoral herding in the country. Key words: Africa, rodents, Senegal, seroprevalence, Toxoplasma gondii. Résumé – Séroprévalence de Toxoplasma gondii chez les rongeurs commensaux au Sénégal, Afrique de l’Ou- est. Les risques liés à l’infection par Toxoplasma gondii chez l’homme restent mal connus au Sénégal. Bien que les rongeurs soient considérés comme des marqueurs pertinents de la circulation de T. gondii, peu d’études ont ciblé ces hôtes en Afrique sub-saharienne. Le but de cette étude était d’étudier la séroprévalence de Toxoplasma chez les rongeurs des villes et des villages du Sénégal. Les rongeurs ont été échantillonnés dans 40 localités avec un protocole de piégeage standardisé. La détection des anticorps contre T. gondii a été faite sur 1205 rongeurs avec un test d’agglutination modifié. Les données de séroprévalence ont été analysées en fonction de la géographie, de la communauté locale de rongeurs et de caractéristiques individuelles du rongeur. Nous avons trouvé 44 individus séropositifs, de quatre espèces différentes (Mastomys erythroleucus, Mastomys natalensis, Mus musculus domesticus, Rattus rattus). La séroprévalence moyenne est faible, de l’ordre de 4 % au sein des localités. Les plus fortes séroprévalences (jusqu’à 24 %) ont été observées dans le Nord du Sénégal, une région connue pour être le cœur de l’élevage pastoral dans le pays. Introduction immunosuppressed patients. Transmission to humans may occur either congenitally, or by ingestion of undercooked meat Toxoplasma gondii [25] is an intracellular pathogen with a containing tissue cysts, or of food and water contaminated with worldwide distribution [17]. In humans, infections range in oocysts shed into the environment in the faeces of felids. severity from asymptomatic to lethal, and are particularly Although felids are the only known definitive host of T. gondii, dangerous to the unborn child during pregnancy and to all homoeothermic animals may act as intermediate hosts [33]. Rodents constitute important prey for domestic felids, and are *Corresponding author: [email protected] among the few wild mammals to persist in villages and towns. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 C. Brouat et al.: Parasite 2018, 25,32 Fig. 1. Seroprevalence of Toxoplasma gondii in rodent communities in villages and towns in Senegal. See Table 1 for locality codes. Light and dark colours indicated the percentage of negative (À) and positive (+) rodents of each dominant species in the community (Mus musculus, Rattus rattus or Mastomys spp.), respectively. For this reason, they are often considered relevant markers under our laboratory authorisation for experiments on wild ani- to assess the circulation of T. gondii in commensal habitats mals (No. D 34-169-1), and followed the official guidelines of [23, 30]. the American Society of Mammalogists [31]. The detailed In sub-Saharan Africa, human seroprevalence is highly description of the standardised trapping protocol used here variable, with reported values ranging from 4% to 83% [20]. was provided in [7]. Rodents were captured alive and eutha- In Senegal, T. gondii infection in humans has been found to nised using cervical dislocation, weighed to the nearest vary between 4% and 40% [19, 24]. However, most studies 0.5 g, sexed and dissected. Intra-cardiac blood was sampled concerned the city of Dakar and the distribution of risks related immediately after death and spotted onto Whatman No. 3 to the disease across the country remains largely unknown. papers that were air-dried and then stored in a plastic bag at Moreover, the seroprevalence of Toxoplasma in animal popula- room temperature (RT) in the field and then at 4 °Cinthe tions has rarely been characterised in Senegal [8, 12]. laboratory. In this study, we provide serological data for T. gondii Rodents were identified to the species level using morpho- obtained from 1205 rodents sampled in villages and towns in logic tools [14]. The rodent community was characterised at Senegal. Seroprevalence data were analysed regarding the geo- each locality using trap success (e.g., the ratio between the graphical location of the sampling locality, its rodent commu- number of captured rodents and active traps set), as a proxy nity, and the individual characteristics of the rodent hosts. for relative rodent abundance, and Simpson’s diversity index [32]. Dried blood samples were used for the detection of Material and methods T. gondii antibodies using a modified agglutination test Sampling (MAT) technique [9] adapted for dried blood samples, with a cut-off titre at 1:16 [20]. Two 5 mm diameter dried blood spots Fieldwork was conducted in 40 localities in Senegal were punched out of each blotting paper circle and placed into between 2011 and 2014 (Fig. 1, Table 1). Trapping within pri- the well of a flat bottomed microtitre plate. The blood was vate properties was performed with prior agreement from local eluted out in 80 lL of phosphate buffered saline, pH 7.2 authorities. All animal-related procedures were carried out (bioMérieux). Plates were covered and left to elute overnight C. Brouat et al.: Parasite 2018, 25,32 3 Table 1. Rodent sampling in Senegal, number of seropositive individuals for Toxoplasma gondii, and mean seroprevalence per locality and rodent species. a b c d e f Locality Code Long. Lat. N Nsero SP S TS Rodent species (%) A. M. M. P. M. m. R. rattus niloticus erythroleucus natalensis daltoni domesticus Aere Lao AEL À14.32 16.40 73 41 2.4 0.58 0.36 22\20\0 51\21\1 Badi Nieriko BAN À13.38 13.38 89 38 0 0.72 0.41 14\14\0 01\00\– 74\24\0 Boutougoufara BOU À12.49 13.40 67 65 4.6 0.46 0.28 01\01\0 21\21\2 05\05\0 40\38\1 Bransan BRA À12.10 13.26 41 32 0 0.67 0.33 01\01\0 06\04\0 33\26\0 01\01\0 Croisement Boube CRB À15.06 16.51 49 13 7.7 0.85 0.11 01\00\– 03\00\– 45\13\1 Dagathie DAG À16.25 15.63 30 20 0 1.00 0.29 30\20\0 Dendoudi DEN À13.54 15.39 49 39 0 0.47 0.20 03\00\– 28\21\0 18\18\0 Diakene-Wolof DIK À16.64 12.46 39 33 3.0 0.63 0.36 08\07\0 01\01\0 30\25\1 Diattacounda DIT À15.68 12.57 52 45 0 0.55 0.42 16\15\0 01\01\0 35\29\0 Diomandou Walo DIW À14.43 16.51 15 14 0 0.88 0.08 01\00\– 14\14\0 Dodel DOD À14.43 16.49 57 40 12.5 0.51 0.40 33\20\3 24\20\2 Doumnga Lao DOL À14.22 16.34 46 20 10.0 0.96 0.49 01\00\– 45\20\2 Galoya GAL À13.86 16.08 94 31 3.2 0.66 0.32 05\00\– 14\10\1 75\21\0 Gandiaye GND À16.27 14.24 29 28 3.6 0.93 0.26 28\28\1 Kedougou KED À12.18 12.55 65 59 3.4 0.50 0.52 30\29\1 35\30\1 Keur Seyni Dieng KSD À16.17 15.59 23 23 17.4 0.84 0.22 02\02\0 21\21\4 Lambago LAM À13.54 15.46 24 20 0 0.92 0.07 01\00\– 23\20\0 Lougue LOU À13.91 16.06 56 41 12.2 0.47 0.41 02\00\– 26\20\3 28\21\2 Mako MAK À12.35 12.86 52 26 0 0.86 0.46 48\26\0 04\00\– Marsassoum MAR À15.98 12.83 34 30 0 0.74 0.41 03\03\0 02\01\0 29\26\0 Mbakhana MBA À16.37 16.09 30 23 0 1.00 0.28 30\23\0 Mbirkilane BKL À15.75 14.13 32 32 0 1.00 0.42 32\32\0 Mereto MRT À14.44 13.82 68 62 0 0.33 0.37 09\09\0 06\05\0 30\29\0 23\19\0 Ndiareme NDR À15.44 16.56 26 24 0 0.86 0.33 02\00\– 24\24\0 Ndombo NDB À15.70 16.44 24 20 0 0.92 0.16 01\00\– 23\20\0 Nguith NGT À15.15 15.40 22 22 13.6 1.00 0.30 22\22\3 Niahene NHN À15.19 14.02 36 35 0 0.50 0.27 01\01\0 22\21\0 13\13\0 Niandane NIA À14.99 16.59 45 44 4.5 1.00 0.49 45\44\2 Podor POD À14.96 16.65