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      Taenia solium, Taenia saginata, Taenia asiatica, their hybrids and other helminthic infections occurring in a neglected tropical diseases' highly endemic area in Lao PDR

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          Abstract

          Most part of Southeast Asia is considered endemic for human-infecting Taenia tapeworms; Taenia solium, T. saginata, and T. asiatica. However, until now there was no report of the occurrence of human cases of T. asiatica in Lao PDR. This study, conducted in Savannakhet Province, Lao PDR, microscopically examined a total of 470 fecal samples by Kato Katz method and found 86% of people harboring at least one helminth. Hookworms were detected in 56% of the samples besides Opisthorchis like eggs (42%), Trichuris trichiura (27%), Ascaris spp. (14%), and Taenia spp. (4%) eggs. Serology for cysticercosis showed 6.8% positives with results varying from 3% to 14.3% in Ethnic School students and Kalouk Kao village respectively. Species-specific PCR targeting mitochondrial DNA (mtDNA) of 28 tapeworms, recovered from 16 patients, revealed T. solium (n = 2), T. saginata (n = 21), and T. asiatica (n = 5). Two patients were confirmed to be coinfected with T. saginata and T. asiatica, indicating the endemicity of the 3 human Taenia in Lao PDR. However, nucleotide sequencing of a nuclear DNA gene, DNA polymerase delta ( pold) revealed that all the tapeworms identified as T. asiatica using mtDNA had T. saginata type allele at pold locus, demonstrating that they are not “pure T. asiatica” but the hybrid descendants between the two species, confirming the wide distribution of hybrids of T. saginata/ T. asiatica in Southeast Asia. The high prevalence of several helminthic NTDs in east Savannakhet area even with conventional control measures indicates the importance to establish wide and multifaceted health programs to sustainably improve the quality of life of the populations living in these communities.

          Author summary

          Southeast Asian Countries are endemic for several foodborne and soil-transmitted helminths occurring in different levels and areas, depending on environmental and cultural conditions. This study aimed to study the soil-transmitted helminths (STHs) and foodborne parasites in Savannakhet Province of Lao PDR, bordering with Vietnam. We found people infected with hookworms, roundworms, whipworms, intestinal/liver flukes, and tapeworms. We also detected antibodies against cysticercosis, an infection caused by eating the eggs of Taenia solium, the pork tapeworm. Focusing on human tapeworm infection, using molecular techniques based on mitochondrial DNA, we detected the three species of human tapeworms T. solium, T. saginata and T. asiatica. Interestingly, when we checked the same material using nuclear gene markers we noted that T. asiatica found in the region were the hybrid descendants of T. saginata and T. asiatica. The causes of hybridization may include people harboring different tapeworm’s species at the same time, allowing the exchange of genetic material but, the consequences of this hybridization are unknown including the seriousness of disease in people. Despite the deworming programs, there is a high prevalence of STHs and foodborne parasites in east Savannakhet area, therefore wide and sustainable health programs are an urgent task to improve the quality of life of the people living in the area.

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          Most cited references35

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          The tumorigenic liver fluke Opisthorchis viverrini--multiple pathways to cancer.

          Liver fluke infection caused by Opisthorchis viverrini is a major public health problem in Thailand and adjacent countries. In addition to infection-associated morbidity, infection with O. viverrini and the related Clonorchis sinensis are unarguable risk factors for cholangiocarcinoma (CAA, bile-duct cancer). Here we review the pathogenesis of opisthorchiasis and the association between O. viverrini infection and bile-duct cancer, focusing on the molecular parallels between wound healing, chronic inflammation, and cancer development. We review a schema for human disease progression from fluke infection, chronic opisthorchiasis, advanced periductal fibrosis, and cholangiocarcinogenesis, and present a rationale for biomarker discovery to facilitate early intervention. We conclude by addressing post-genomic advances with a view to developing new control strategies to combat this infectious cancer. Copyright © 2012 Elsevier Ltd. All rights reserved.
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            Neurocysticercosis: updated concepts about an old disease.

            Neurocysticercosis, the infection of the human brain by the larvae of Taenia solium, is a major cause of acquired epilepsy in most low-income countries. Cases of neurocysticercosis are becoming more common in high-income countries because of increased migration and travel. Diagnosis by neuroimaging and serological assessment has greatly improved over the past decade, and the natural progression of the disease and response to antiparasitic drugs is now much better understood. Neurocysticercosis is potentially eradicable, and control interventions are underway to eliminate this infection. Meanwhile, updated information on diagnosis and management of neurocysticercosis is required, especially for clinicians who are unfamiliar with its wide array of clinical presentations.
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              DNA differential diagnosis of taeniasis and cysticercosis by multiplex PCR.

              Multiplex PCR was established for differential diagnosis of taeniasis and cysticercosis, including their causative agents. For identification of the parasites, multiplex PCR with cytochrome c oxidase subunit 1 gene yielded evident differential products unique for Taenia saginata and Taenia asiatica and for American/African and Asian genotypes of Taenia solium with molecular sizes of 827, 269, 720, and 984 bp, respectively. In the PCR-based detection of tapeworm carriers using fecal samples, the diagnostic markers were detected from 7 of 14 and 4 of 9 T. solium carriers from Guatemala and Indonesia, respectively. Test sensitivity may have been reduced by the length of time (up to 12 years) that samples were stored and/or small sample volumes (ca. 30 to 50 mg). However, the diagnostic markers were detected by nested PCR in five worm carriers from Guatemalan cases that were found to be negative by multiplex PCR. It was noteworthy that a 720 bp-diagnostic marker was detected from a T. solium carrier who was egg-free, implying that it is possible to detect worm carriers and treat before mature gravid proglottids are discharged. In contrast to T. solium carriers, 827-bp markers were detected by multiplex PCR in all T. saginata carriers. The application of the multiplex PCR would be useful not only for surveillance of taeniasis and cysticercosis control but also for the molecular epidemiological survey of these cestode infections.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                8 February 2018
                February 2018
                : 12
                : 2
                : e0006260
                Affiliations
                [1 ] Department of Tropical Medicine and Parasitology, Dokkyo Medical University, Mibu, Tochigi, Japan
                [2 ] Graduate School of Health Sciences, Niigata University, Niigata, Niigata, Japan
                [3 ] Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan
                [4 ] Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                [5 ] Station of Malariology, Parasitology, and Entomology of Savannakhet Province, Savannakhet, Lao PDR
                [6 ] Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
                [7 ] National Institute of Public Health, Ministry of Health, Vientiane, Lao PDR
                [8 ] Primate Research Institute, Kyoto University, Aichi, Japan
                [9 ] Graduate School of International Health Development, Nagasaki University, Nagasaki, Japan
                Instituto de Investigaciones Biomédicas, UNAM, MEXICO
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-9204-0602
                Article
                PNTD-D-17-01582
                10.1371/journal.pntd.0006260
                5821399
                29420601
                6bc08e19-be3e-487d-8cd8-2ae421150974
                © 2018 Sato et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 October 2017
                : 22 January 2018
                Page count
                Figures: 2, Tables: 2, Pages: 14
                Funding
                Funded by: Research Institute for Humanity and Nature
                Award ID: Environmental Changes and Infectious Diseases in Tropical Asia
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 24406011
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004396, Thailand Research Fund;
                Award ID: BRG 5180005
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004156, Mahidol University;
                Award Recipient :
                This research was supported by the RIHN research project on "Environmental Changes and Infectious Diseases in Tropical Asia" (Kazuhiko Moji), the Japan Society for the Promotion of Science project 24406011 (Munehiro Okamoto), the Thailand Research Fund (BRG 5180005), and Faculty of Tropical Medicine, Mahidol University grant (Jitra Waikagul). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                People and Places
                Population Groupings
                Ethnicities
                Lao People
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Cysticercosis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Cysticercosis
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and life sciences
                Genetics
                DNA
                Forms of DNA
                Mitochondrial DNA
                Biology and life sciences
                Biochemistry
                Nucleic acids
                DNA
                Forms of DNA
                Mitochondrial DNA
                Medicine and Health Sciences
                Parasitic Diseases
                Social Sciences
                Sociology
                Education
                Schools
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Taeniasis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Taeniasis
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Taeniasis
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-02-21
                All relevant data are within the paper.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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