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      Responses of the putative trachoma vector, Musca sorbens, to volatile semiochemicals from human faeces

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          Abstract

          The putative vector of trachoma, Musca sorbens, prefers to lay its eggs on human faeces on the ground. This study sought to determine whether M. sorbens females were attracted to volatile odours from human faeces in preference to odours from the faeces of other animals, and to determine whether specific volatile semiochemicals mediate selection of the faeces. Traps baited with the faeces of humans and local domestic animals were used to catch flies at two trachoma-endemic locations in The Gambia and one in Ethiopia. At all locations, traps baited with faeces caught more female M. sorbens than control traps baited with soil, and human faeces was the most successful bait compared with soil (mean rate ratios 44.40, 61.40, 10.50 [ P<0.001]; 8.17 for child faeces [ P = 0.004]). Odours from human faeces were sampled by air entrainment, then extracts of the volatiles were tested by coupled gas chromatography-electroantennography with laboratory-reared female M. sorbens. Twelve compounds were electrophysiologically active and tentatively identified by coupled mass spectrometry-gas chromatography, these included cresol, indole, 2-methylpropanoic acid, butanoic acid, pentanoic acid and hexanoic acid. It is possible that some of these volatiles govern the strong attraction of M. sorbens flies to human faeces. If so, a synthetic blend of these chemicals, at the correct ratios, may prove to be a highly attractive lure. This could be used in odour-baited traps for monitoring or control of this species in trachoma-endemic regions.

          Author summary

          Musca sorbens, also known as the Bazaar Fly, visits people’s faces to feed on ocular and nasal discharge. While feeding, M. sorbens can transmit Chlamydia trachomatis, the bacterium that causes the infectious eye disease trachoma. Around 1.9 million people worldwide are visually impaired or blind from this disease. Although it is believed that M. sorbens transmits trachoma, very few studies have looked at ways to control this fly. A large-scale trial has shown that control of fly populations with insecticide reduces active trachoma disease prevalence. Odour-baited traps for the suppression of disease vector populations are an attractive option as there is no widespread spraying of insecticide; however, highly attractive baits are critical to their success. Here, we demonstrate that the preference of these flies for breeding in human faeces is probably mediated by odour cues, and we isolate chemicals in the odour of human faeces that cause a response in the antennae of M. sorbens. These compounds may play a role in the specific attractiveness of human faeces to these flies, perhaps by being present in greater amounts or at favourable ratios. These may be developed into a chemical lure for odour-baited trapping to suppress M. sorbens populations.

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          Most cited references35

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          A review of the volatiles from the healthy human body.

          A compendium of all the volatile organic compounds (VOCs) emanating from the human body (the volatolome) is for the first time reported. 1840 VOCs have been assigned from breath (872), saliva (359), blood (154), milk (256), skin secretions (532) urine (279), and faeces (381) in apparently healthy individuals. Compounds were assigned CAS registry numbers and named according to a common convention where possible. The compounds have been grouped into tables according to their chemical class or functionality to permit easy comparison. Some clear differences are observed, for instance, a lack of esters in urine with a high number in faeces. Careful use of the database is needed. The numbers may not be a true reflection of the actual VOCs present from each bodily excretion. The lack of a compound could be due to the techniques used or reflect the intensity of effort e.g. there are few publications on VOCs from blood compared to a large number on VOCs in breath. The large number of volatiles reported from skin is partly due to the methodologies used, e.g. collecting excretions on glass beads and then heating to desorb VOCs. All compounds have been included as reported (unless there was a clear discrepancy between name and chemical structure), but there may be some mistaken assignations arising from the original publications, particularly for isomers. It is the authors' intention that this database will not only be a useful database of VOCs listed in the literature, but will stimulate further study of VOCs from healthy individuals. Establishing a list of volatiles emanating from healthy individuals and increased understanding of VOC metabolic pathways is an important step for differentiating between diseases using VOCs.
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            Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism.

            Concentrations of phenolic compounds in human gut contents were more than fourfold higher in the distal colon (6.2 mmol kg-1) compared to the proximal bowel (1.4 mmol kg-1). Tryptophan metabolites were never found in more than trace amounts in large intestinal contents and phenol substituted fatty acids were the major products of aromatic amino acid fermentation that accumulated in the proximal colon, whereas phenol and p-cresol were more important in the distal gut, accounting for 70% of all products of dissimilatory aromatic amino acid metabolism. In vitro incubations of colonic material showed that phenol was produced most rapidly (1.0 mumol g-1 h-1), whereas indole was formed comparatively slowly (0.06 mumol g-1 h-1). Most probable number (MPN) estimations demonstrated that large populations of phenol and indole producing bacteria occur in the large intestine (range log10 9.8-11.5 (g dry wt faeces)-1, mean 10.6, N = 7). With respect to phenolic compounds, phenylacetate and phenylpropionate producers predominated, while indoleacetate-forming bacteria were the major tryptophan-utilizing organisms. Quantitation of products of dissimilatory aromatic amino acid metabolism in MPN tubes showed that phenol and phenylpropionate mainly accumulated at low sample dilutions, whereas phenylacetate, p-cresol, indoleacetate and indolepropionate were formed in greatest amounts at high sample dilutions. The significance of pH and carbohydrate availability with respect to aromatic amino acid metabolism was shown in batch culture fermentation studies, where net production of phenolic compounds by mixed populations of intestinal bacteria was reduced by approximately 33% during growth at pH 5.5 compared to pH 6.8, and by 60% in the presence of a fermentable carbohydrate. Experiments with 16 species of intestinal bacteria belonging to six different genera showed that environmental factors such as low pH and high carbohydrate availability markedly reduced dissimilatory aromatic amino acid metabolism in some organisms, but stimulated this process in others. A three-stage continuous culture model of the colon was used to investigate the effect of system retention time (27.1 or 66.7 h) on aromatic amino acid fermentation. Qualitative and quantitative increases in phenol production occurred from vessel 1 to vessel 3 in this model. Concentrations of phenolic compounds in vessel 3 were three times greater at R = 66.7 h compared to R = 27.1 h. Phenol and p-cresol were not detected in vessel 1, though formation of these metabolites increased from vessel 2 to vessel 3, in a pattern similar to that observed in the distal colon.
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              Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant.

              West Nile virus, which is transmitted by Culex mosquitoes while feeding on birds and humans, has emerged as the dominant vector borne disease in North America. We have identified natural compounds from humans and birds, which are detected with extreme sensitivity by olfactory receptor neurons (ORNs) on the antennae of Culex pipiens quinquefasciatus (Cx. quinquefasciatus). One of these semiochemicals, nonanal, dominates the odorant spectrum of pigeons, chickens, and humans from various ethnic backgrounds. We determined the specificity and sensitivity of all ORN types housed in different sensilla types on Cx. quinquefasciatus antennae. Here, we present a comprehensive map of all antennal ORNs coding natural ligands and their dose-response functions. Nonanal is detected by a large array of sensilla and is by far the most potent stimulus; thus, supporting the assumption that Cx. quinquefasciatus can smell humans and birds. Nonanal and CO(2) synergize, thus, leading to significantly higher catches of Culex mosquitoes in traps baited with binary than in those with individual lures.
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                Author and article information

                Contributors
                Role: Formal analysisRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: Formal analysisRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Supervision
                Role: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: 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
                3 March 2020
                March 2020
                : 14
                : 3
                : e0007719
                Affiliations
                [1 ] Department of Disease Control, London School of Hygiene and Tropical Medicine, Keppel Street, London, United Kingdom
                [2 ] Biological Chemistry and Crop Protection, Rothamsted Research, Harpenden, Hertfordshire, United Kingdom
                [3 ] Medical Research Council Unit, The Gambia, The Gambia
                [4 ] The Fred Hollows Foundation, Addis Ababa, Ethiopia
                [5 ] Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, United Kingdom
                [6 ] Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, United Kingdom
                [7 ] Global Partnerships Executive, The Fred Hollows Foundation, Crawford Mews, London, United Kingdom
                [8 ] ARCTEC, Chariot Innovations Ltd, London School of Hygiene and Tropical Medicine, London, United Kingdom
                [9 ] Department of Biosciences, Durham University, Durham, County Durham, United Kingdom
                RTI International, UNITED REPUBLIC OF TANZANIA
                Author notes

                The authors have declared that no competing interests exist.

                [¤a]

                Current address: The University of Sussex, Falmer, Brighton, United Kingdom

                [¤b]

                Current address: Entocycle Ltd., United Kingdom

                [¤c]

                Current address: Disease Control and Elimination, Medical Research Council Unit, The Gambia at the London School of Hygiene and Tropical Medicine, Fajara, The Gambia

                [¤d]

                Current address: Biointeractions and Crop Protection, Rothamsted Research, Harpenden, Hertfordshire, United Kingdom

                [¤e]

                Current address: School of Chemistry, Cardiff University, Cardiff, United Kingdom

                Author information
                http://orcid.org/0000-0002-4291-6696
                http://orcid.org/0000-0003-1972-6787
                http://orcid.org/0000-0002-8770-1680
                http://orcid.org/0000-0002-2371-5709
                http://orcid.org/0000-0002-3302-2025
                http://orcid.org/0000-0003-1799-370X
                http://orcid.org/0000-0003-2080-3890
                http://orcid.org/0000-0002-2370-5578
                http://orcid.org/0000-0001-6041-3796
                http://orcid.org/0000-0001-6341-5009
                http://orcid.org/0000-0003-1872-9169
                Article
                PNTD-D-19-01361
                10.1371/journal.pntd.0007719
                7069642
                32126087
                1ec2d3bd-e158-47ef-9a5a-763674f0f4e6
                © 2020 Robinson 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
                : 9 August 2019
                : 13 January 2020
                Page count
                Figures: 2, Tables: 2, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 206275/Z/17/Z
                Award Recipient :
                This work was supported by (1) a studentship to JB jointly funded by the Biotechnology and Biological Sciences Research Council and the Medical Research Council; (2) The Fred Hollows Foundation; and (3) The Wellcome Trust through the Stronger SAFE Collaborative Award to MJB, VS and JGL (206275/Z/17/Z). The Fred Hollows Foundation applied untied funds to this project and staff participated in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication. The Wellcome Trust had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Trachoma
                Medicine and Health Sciences
                Ophthalmology
                Eye Diseases
                Trachoma
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Trachoma
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Sheep
                Physical Sciences
                Chemistry
                Chemical Compounds
                Acids
                Carboxylic Acids
                Butyric Acids
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Carboxylic Acids
                Butyric Acids
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Carboxylic Acids
                Butyric Acids
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Equines
                Horses
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Equines
                Asses
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Heterocyclic Compounds
                Indoles
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Heterocyclic Compounds
                Indoles
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-03-13
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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