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      Scanning electron microscopy of Onchocerca fasciata (Filarioidea: Onchocercidae) adults, microfilariae and eggs with notes on histopathological findings in camels

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          Abstract

          Background

          Onchocerca fasciata is a prevalent filarial species in camelids of Asia and Africa forming nodules in the skin of dromedary and Bactrian camels. In spite of recent advances in the biology and epidemiology of this nematode species, a relatively scant number of studies have focussed on the morphology of this parasite. The main objective of this study was to describe morphological characteristics of adults, microfilariae and eggs of O. fasciata by scanning electron microscopy (SEM), staining and histology.

          Methods

          From April 2016 to March 2017 dromedary camels ( n = 456) were inspected for infection with O. fasciata in a slaughterhouse in Kerman (south of Iran). Adult worms in nodules were isolated by digestion of nodules in collagenase and used for SEM. Skin nodules were also fixed, sectioned and stained with hematoxylin and eosin for histopathology. Skin microfilariae that were isolated from tissues surrounding the nodules were confirmed as O. fasciata by sequencing of the cytochrome c oxidase subunit 1 ( cox1) and 12S rRNA genes and used for SEM and Giemsa staining.

          Results

          Single or multiple O. fasciata nodules (1.2–2.2 cm in diameter and 507–845 mg in weight) were found in 30.3% of the examined camels. SEM analysis helped identify 18 papillae in the caudal region of the male. Discontinuous longitudinal cuticular crests were observed in the posterior region of the male. In female nematodes, the ridges had a rounded shape with a height/width ratio of 7/16 in longitudinal sections. Unsheathed skin microfilariae with a rounded anterior extremity measured 210.7 × 2.5 μm on average. Developed eggs containing microfilariae measured 35.9 × 31.0 μm and their smooth shell surface had characteristic tongue-like appendages. In addition to inflammatory reactions surrounding the parasites, accumulation of intracellular ceroid pigment, golden-yellow to brown in colour, was observed within macrophages upon histopathological examination.

          Conclusions

          We found longitudinal crests on the surface of the posterior region of the male nematode. Measurements of the main morphological features of microfilariae and eggs, and the shape index of ridges (height/width) in female nematodes are described for the first time.

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          Most cited references41

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          A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts

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            Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution.

            Wolbachia pipientis is a bacterial endosymbiont associated with arthropods and filarial nematodes. In filarial nematodes, W. pipientis has been shown to play an important role in the biology of the host and in the immuno-pathology of filariasis. Several species of filariae, including the most important parasites of humans and animals (e.g. Onchocerca volvulus, Wuchereria bancrofti and Dirofilaria immitis) have been shown to harbour these bacteria. Other filarial species, including an important rodent species (Acanthocheilonema viteae), which has been used as a model for the study of filariasis, do not appear to harbour these symbionts. There are still several open questions about the distribution of W. pipientis in filarial nematodes. Firstly the number of species examined is still limited. Secondly, it is not clear whether the absence of W. pipientis in negative species could represent an ancestral characteristic or the result of a secondary loss. Thirdly, several aspects of the phylogeny of filarial nematodes are still unclear and it is thus difficult to overlay the presence/absence of W. pipientis on a tree representing filarial evolution. Here we present the results of a PCR screening for W. pipientis in 16 species of filariae and related nematodes, representing different families/subfamilies. Evidence for the presence of W. pipientis is reported for five species examined for the first time (representing the genera Litomosoides, Litomosa and Dipetalonema); original results on the absence of this bacterium are reported for nine species; for the remaining two species, we have confirmed the absence of W. pipientis recently reported by other authors. In the positive species, the infecting W. pipientis bacteria have been identified through 16S rDNA gene sequence analysis. In addition to the screening for W. pipientis in 16 species, we have generated phylogenetic reconstructions based on mitochondrial gene sequences (12S rDNA; COI), including a total of 28 filarial species and related spirurid nematodes. The mapping of the presence/absence of W. pipientis on the trees generated indicates that these bacteria have possibly been lost during evolution along some lineages of filarial nematodes.
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              Parasitic diseases of camels in Iran (1931–2017) – a literature review

              Parasitic diseases of camels are major causes of impaired milk and meat production, decreases in performance or even death. Some camel parasites also represent a threat to human health. About 171,500 one-humped camels (Camelus dromedarius) and 100–300 two-humped camels (Camelus bactrianus) live in Iran. Knowledge of the biodiversity of their parasites is still limited. The present review covers all information about camel parasitic diseases in Iran published as dissertations and in both Iranian and international journals from 1931 to February 2017. Ten genera of Protozoa (Trypanosoma, Eimeria, Cryptosporidium, Toxoplasma, Neospora, Sarcocystis, Besnoitia, Theileria, Babesia and Balantidium), 48 helminth species detected in the digestive system, including three species of Trematoda, four species of Cestoda, and 41 species of Nematoda, as well as helminths from other organs – Echinococcus spp., Dictyocaulus filaria, Thelazia leesei, Dipetalonema evansi and Onchocerca fasciata – have so far been described in Iranian camels. Furthermore, 13 species of hard ticks, mange mites, the myiasis flies Cephalopina titillator and Wohlfahrtia magnifica, and immature stages of the Pentastomida Linguatula serrata have also been reported from camels of Iran. Camel parasitic diseases are a major issue in Iran in terms of economics and public health. The present review offers information for an integrated control programme against economically relevant parasites of camels.
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                Author and article information

                Contributors
                dr.younes2015@gmail.com
                dr_mirzaie_mo@uk.ac.ir
                shadihashemnia@uk.ac.ir
                golchin@uk.ac.ir
                kheirandish@uk.ac.ir
                unishigehiko@um.edu.my
                jairo.mendozaroldan@uniba.it
                domenico.otranto@uniba.it
                alireza.sazmand@basu.ac.ir
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                13 May 2020
                13 May 2020
                2020
                : 13
                : 249
                Affiliations
                [1 ]GRID grid.412503.1, ISNI 0000 0000 9826 9569, Department of Pathobiology, Faculty of Veterinary Medicine, , Shahid Bahonar University of Kerman, ; 7616914111 Kerman, Iran
                [2 ]GRID grid.412503.1, ISNI 0000 0000 9826 9569, Department of Basic Sciences, Faculty of Veterinary Medicine, , Shahid Bahonar University of Kerman, ; 7616914111 Kerman, Iran
                [3 ]GRID grid.411103.6, ISNI 0000 0001 0707 9143, Department of Public Health, Faculty of Nursing, , Kobe Women’s University, ; Kobe, 650-0046 Japan
                [4 ]GRID grid.7644.1, ISNI 0000 0001 0120 3326, Department of Veterinary Medicine, , University of Bari Aldo Moro, ; Str. prov. per Casamassima km 3, Valenzano, 70010 Bari, Italy
                [5 ]GRID grid.411807.b, ISNI 0000 0000 9828 9578, Department of Pathobiology, Faculty of Veterinary Science, , Bu-Ali Sina University, ; 6517658978 Hamedan, Iran
                Author information
                https://orcid.org/0000-0002-0969-4921
                https://orcid.org/0000-0001-9787-932X
                https://orcid.org/0000-0002-7518-476X
                https://orcid.org/0000-0002-8450-2993
                Article
                4123
                10.1186/s13071-020-04123-0
                7218593
                32404208
                1b01611c-0aaf-40ef-b4e8-b57608bc7f05
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 7 February 2020
                : 6 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007726, Shahid Bahonar University of Kerman;
                Award ID: Younes Ghahvei PhD Thesis Project
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Parasitology
                onchocerca fasciata,camelus dromedarius,camelus bactrianus,vector-borne disease,scanning electron microscopy,histopathology

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