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      Evaluation of Volatile Organic Compounds Obtained from Breath and Feces to Detect Mycobacterium tuberculosis Complex in Wild Boar ( Sus scrofa) in Doñana National Park, Spain

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          Abstract

          The presence of Mycobacterium tuberculosis complex (MTBC) in wild swine, such as in wild boar ( Sus scrofa) in Eurasia, is cause for serious concern. Development of accurate, efficient, and noninvasive methods to detect MTBC in wild swine would be highly beneficial to surveillance and disease management efforts in affected populations. Here, we describe the first report of identification of volatile organic compounds (VOC) obtained from the breath and feces of wild boar to distinguish between MTBC-positive and MTBC-negative boar. We analyzed breath and fecal VOC collected from 15 MTBC-positive and 18 MTBC-negative wild boar in Donaña National Park in Southeast Spain. Analyses were divided into three age classes, namely, adults (>2 years), sub-adults (12–24 months), and juveniles (<12 months). We identified significant compounds by applying the two-tailed statistical t-test for two samples assuming unequal variance, with an α value of 0.05. One statistically significant VOC was identified in breath samples from adult wild boar and 14 were identified in breath samples from juvenile wild boar. One statistically significant VOC was identified in fecal samples collected from sub-adult wild boar and three were identified in fecal samples from juvenile wild boar. In addition, discriminant function analysis (DFA) was used to build classification models for MTBC prediction in juvenile animals. Using DFA, we were able to distinguish between MTBC-positive juvenile wild boar and MTBC-negative juvenile wild boar using breath VOC or fecal VOC. Based on our results, further research is warranted and should be performed using larger sample sizes, as well as wild boar from various geographic locations, to verify these compounds as biomarkers for MTBC infection in this species. This new approach to detect MTBC infection in free-ranging wild boar potentially comprises a reliable and efficient screening tool for surveillance in animal populations.

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          Most cited references 25

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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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            The status of tuberculosis in European wild mammals

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              Breath biomarkers of active pulmonary tuberculosis.

              Volatile organic compounds (VOCs) in breath may contain biomarkers of active pulmonary tuberculosis derived from the infectious organism (metabolites of Mycobacterium tuberculosis) and from the infected host (products of oxidative stress). We analyzed breath VOCs in 226 symptomatic high-risk patients in USA, Philippines, and UK, using gas chromatography/mass spectroscopy. Diagnosis of disease was based on sputum culture, smear microscopy, chest radiography and clinical suspicion of tuberculosis (CSTB). Chromatograms were converted to a series of 8s overlapping time slices. Biomarkers of active pulmonary tuberculosis were identified with a Monte Carlo analysis of time-slice alveolar gradients (abundance in breath minus abundance in room air). Breath VOCs contained apparent biomarkers of active pulmonary tuberculosis comprising oxidative stress products (alkanes and alkane derivatives) and volatile metabolites of M. tuberculosis (cyclohexane and benzene derivatives). Breath biomarkers identified active pulmonary tuberculosis with C-statistic (area under curve of receiver operating characteristic)=0.85 (i.e. 85% overall accuracy, sensitivity=84.0%, specificity=64.7%) when sputum culture, microscopy, and chest radiography were either all positive or all negative. Employing a single criterion of disease, C-statistic=0.76 (smear microscopy), 0.68 (sputum culture), 0.66 (chest radiography) and 0.65 (CSTB). A breath test identified apparent biomarkers of active pulmonary tuberculosis with 85% accuracy in symptomatic high-risk subjects.
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                Author and article information

                Journal
                Pathogens
                Pathogens
                pathogens
                Pathogens
                MDPI
                2076-0817
                02 May 2020
                May 2020
                : 9
                : 5
                Affiliations
                [1 ]Centers for Epidemiology and Animal Health, Veterinary Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, CO 80526, USA
                [2 ]Department of Electronics, Electrical and Automatic Engineering, Rovira i Virgili University, 43007 Tarragona, Spain; radu.ionescu@ 123456urv.cat (R.I.); irati.barrenetxea92@ 123456gmail.com (I.B.); florina.ionescu@ 123456urv.cat (F.I.)
                [3 ]The Ångström Laboratory, Division of Solid State Physics, Department of Materials Science and Engineering Sciences, Uppsala University, 75121 Uppsala, Sweden; tesfalem.welearegay@ 123456angstrom.uu.se
                [4 ]VISAVET Health Surveillance Centre, Animal Health Department, Faculty of Veterinary Medicine, Complutense University of Madrid, 28040 Madrid, Spain; joseangel.barasona@ 123456gmail.com
                [5 ]SaBio Instituto de Investigación en Recursos Cinegéticos IREC, ETSIA Ciudad Real, University Castilla La Mancha & CSIC, 13003 Ciudad Real, Spain; joaquin.vicente@ 123456uclm.es
                [6 ]Faculty of Engineering, Universidad Autónoma del Caribe, Barranquilla 080020, Colombia; rikelvin1984@ 123456gmail.com
                [7 ]Department of Chemical Engineering, Complutense University of Madrid, 28040 Madrid, Spain
                [8 ]Biomedical Institute of Sevilla (IBiS), University of Seville, University Hospital Virgen del Rocío/CSIC, 41071 Seville, Spain; mjtorres@ 123456us.es
                [9 ]National Veterinary Services Laboratory, Veterinary Services, Animal and Plant Health Inspection Service, United States Department of Agriculture, Fort Collins, Colorado, Fort Collins, CO 80521 USA; rhyanjack@ 123456yahoo.com
                Author notes
                [* ]Correspondence: pauline.nol@ 123456usda.gov ; Tel.: +1-970-218-1418
                [†]

                Retired.

                Article
                pathogens-09-00346
                10.3390/pathogens9050346
                7281121
                32370281
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

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