Trichuris trichiura (Linnaeus, 1771) From Human and Non-human Primates: Morphology, Biometry, Host Specificity, Molecular Characterization, and Phylogeny

Abstract

Human trichuriasis is a Neglected Tropical Disease, which affects hundreds of millions of persons worldwide. Several studies have reported that non-human primates (NHP) represent important reservoirs for several known zoonotic infectious diseases. In this context, Trichuris infections have been found in a range of NHP species living in natural habitats, including colobus monkeys, macaques, baboons, and chimpanzees. To date, the systematics of the genus Trichuris parasitizing humans and NHP is unclear. During many years, Trichuris trichiura was considered as the whipworm present in humans and primates. Subsequently, molecular studies suggested that Trichuris spp. in humans and NHP represent several species that differ in host specificity. This work examines the current knowledge of T. trichiura and its relationship to whipworm parasites in other primate host species. A phylogenetic hypothesis, based on three mitochondrial genes (cytochrome c oxidase subunit 1, cytochrome b, and large subunit rRNA-encoding gene) and two fragments of ribosomal DNA (Internal Transcribed Spacer 1 and 2), allowed us to define a complex of populations of T. trichiura hosting in a large variety of NHP species, in addition to humans. These populations were divided into four phylogenetic groups with a different degree of host specificity. From these data, we carry out a new morphological and biometrical description of the populations of Trichuris based on data cited by other authors as well as those provided in this study. The presence of T. trichiura is analyzed in several NHP species in captivity from different garden zoos as possible reservoir of trichuriasis for humans. This study contributes to clarify questions that lead to identification of new taxa and will determine parasite transmission routes between these primates, allowing the implementation of appropriate control and prevention measures.

Intestinal parasites infecting captive non-human primates in Italy

“…The cuticle presented transversal striation and the anterior portion of the body showed bacillary bands. Males ( Figure 2 ) and females ( Figure 3 ) showed similar morphological features described for Trichuris trichiura from Papio papio and M. sylvanus ( 31 ), Trichuris sp. from M. sylvanus ( 34 , 35 ) and T. ursinus from Papio ursinus ( 36 ).…”

“…Regarding the molecular characterization, ten high quality rrn L sequences (nine from M. fascicularis and one from M. fuscata ) and four cox 1 sequences (all from M. fascicularis ) were obtained from the collected nematodes and used for phylogenetic inferences in comparison to GenBank retrieved data, with final datasets of 43 input and 460 bp and of 32 input and 341 bp, respectively. Both phylogenetic trees identified the presence of two main clades, namely “Clade 1” and “Clade 2” ( 31 ). The rrn L ML consensus tree in Figure 4 described Clade 1 named as the T. suis clade, including Trichuris colobae as a sister clade of T. suis + Trichuris sp.…”

“…Nematodes were repeatedly washed with saline solution, and then used for morphological observation after clarification in lactophenol. A body portion was used for molecular characterization based on sequence analyses of the two partial mitochondrial regions cox 1 and rrn L, informative for phylogenetic assignment ( 31 , 32 ). The obtained sequences were compared to homologous GenBank retrieved data, and used for phylogenetic inferences with the maximum likelihood (ML) method by MEGA7 ( 33 ), after testing for the best evolutionary models explaining the data ( 33 ).…”

The Use of MALDI-TOF MS as a Diagnostic Tool for Adult Trichuris Species

“…Adult worms were defrosted and dried at room temperature. The morphological identification of different Trichuris species was carried out according to previous studies ( 15 , 18 , 20 , 50 – 52 ). Nonetheless, morphologically the different species of Trichuris are difficult to differentiate.…”

“…But due to the phenotypic plasticity of these parasites (host-induced variation, lack of morphological characteristics, and overlap of morphological characteristics and biometrical data between species), it is highly difficult to distinguish between closely related Trichuris species ( 11 – 14 ). Hence, molecular studies, such as polymerase chain reaction (PCR) and sequencing, are used as a tool to differentiate species ( 5 – 7 , 9 , 10 , 15 – 20 ). While the morphological identification is a rapid and less costly procedure, the related Trichuris species are hardly morphologically distinguishable.…”