Snakes and Souks: Zoonotic pathogens associated to reptiles in the Marrakech markets, Morocco

Abstract

The world-famous markets of Marrakech, also known in Arabic as souks, harbor a vast diversity of reptiles that are sold for medicinal/magic/pet purposes or used for snake charming. This unique epidemiological context has never been studied considering the interactions of humans, reptiles, and zoonotic pathogens. Thus, the aim of this study was to identify the parasites and pathogens present in blood and feces associated with handled reptiles in the markets of Marrakech to assess the risk of zoonotic transmission within the reptile-human interface. Privately owned reptiles (n = 118), coming from vendors or snake charmers, were examined and blood and feces sampled. DNA was extracted and molecular screening (cPCR, nPCR, qPCR, dqPCR) was performed aiming to identify potentially zoonotic pathogens (i.e., Anaplasma/Ehrlichia spp., Rickettsia spp., Borrelia burgdorferi sensu lato, Coxiella burnetii, Babesia/Theileria spp., Cryptosporidium spp., Giardia spp., Leishmania spp., Cestoda). Overall, 28.9% (34/118) of reptiles were positive for at least one pathogen. In blood, Anaplasma spp. were detected in four snakes, with two Montpellier snakes positive for Anaplasma phagocytophilum, while Rickettsia spp. were detected in one Mediterranean chameleon and four puff adders. Leishmania tarentolae was molecularly detected in a Mediterranean chameleon and a Montpellier snake. In feces, the cox1 gene generated a myriad of sequences for nematodes, cestodes, fungi and bacteria. Importantly, Proteus vulgaris was identified from a Mediterranean chameleon. Cryptosporidium spp. nPCR yielded a positive sample (i.e., Cryptosporidium sp. apodemus genotype I) from a Moroccan worm lizard, as well as for bacteria such as Pseudomonas aeruginosa in an Egyptian cobra, and Morganella morganii from a puff adder. Results from this study demonstrated the risk of zoonotic transmission of microorganisms and parasites present in blood and feces from reptiles that are brought to the souks in Marrakech, Morocco, to be sold for medicinal purposes or used for snake charming, being in direct and straight contact with humans.

Parasites and microorganisms associated with the snakes collected for the “festa Dei serpari” in Cocullo, Italy

“…[ 100 , 101 ]. Again, molecular positivity for species of the spotted fever group (i.e., Rickettsia monacensis , Rickettsia helvetica ) was reported in lizards from Italy [ 35 ] and snakes (i.e., Rickettsia asiatica ) from Morocco [ 3 ]. As R .…”

“…Snakes’ (Serpentes: Squamata) perception and interaction with human societies can be contrasting, generating fear and negative feelings (e.g., disgust, repulsion; [ 1 , 2 ]), being merely tolerated or even used for food or economic sources (i.e., snake charming) [ 3 ], or considered as new companion animals [ 4 , 5 ]. One of the major threats on snake conservation is the anthropogenic pressure, directly implicated in the decline of snake populations [ 6 , 7 ].…”

“…The relationships and uses by human communities of reptiles is also known as ethnoherpetology [ 17 ], which studies the importance of reptiles in different ecological, economic, and cultural contexts [ 2 ]. Further investigations were conducted toward integrating One-Health parasitological approaches with ethnoherpetology (i.e., ethnoherpetoparasitology), which allowed to identify the microorganisms and parasites that these animals harbor, as well as the potential risk of zoonotic transmission to snake charmers and vendors in the souks of Marrakech, Morocco [ 3 ]. All of the above was assessed in a place where snakes are feared but highly tolerated, given their cultural and economic importance.…”

Polyphasic Characterization of Brucella spp. in Livestock Slaughtered from Abattoirs in Eastern Cape, South Africa

“…The present study reports the isolation of other pathogenic organisms such as Proteus Vulgaris , Serratia marcescens , and Brevundimonas naejangsanensis. Proteus vulgaris has been reported as a zoonotic infection, which is mainly known for causing wound and urinary infections in humans [ 55 ]. Previous researchers have reported S. marcescens as a common cause of mastitis and early abortions in cows [ 56 , 57 ].…”