{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,15]],"date-time":"2026-03-15T02:35:40Z","timestamp":1773542140575,"version":"3.50.1"},"reference-count":32,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2018,9,11]],"date-time":"2018-09-11T00:00:00Z","timestamp":1536624000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Sensors"],"abstract":"<jats:p>Fecal volatile organic compound (VOC) analysis has shown great potential as a noninvasive diagnostic biomarker for a variety of diseases. Before clinical implementation, the factors influencing the outcome of VOC analysis need to be assessed. Recent studies found that the sampling conditions can influence the outcome of VOC analysis. However, the dietary influences remains unknown, especially in (preterm) infants. Therefore, we assessed the effects of feeding composition on fecal VOC patterns of preterm infants (born at &lt;30 weeks gestation). Two subgroups were defined: (1) daily intake &gt;75% breastmilk (BM) feeding and (2) daily intake &gt;75% formula milk (FM) feeding. Fecal samples, which were collected at 7, 14 and 21 days postnatally, were analyzed by an electronic nose device (Cyranose 320\u00ae). In total, 30 preterm infants were included (15 FM, 15 BM). No differences in the fecal VOC patterns were observed at the three predefined time-points. Combining the fecal VOC profiles of these time-points resulted in a statistically significant difference between the two subgroups although this discriminative accuracy was only modest (AUC [95% CI]; p-value; sensitivity; and specificity of 0.64 [0.51\u20130.77]; 0.04; 68%; and 51%, respectively). Our results suggest that the influence of enteral feeding on the outcome of fecal VOC analysis cannot be ignored in this population. Furthermore, in both subgroups, the fecal VOC patterns showed a stable longitudinal course within the first month of life.<\/jats:p>","DOI":"10.3390\/s18093037","type":"journal-article","created":{"date-parts":[[2018,9,11]],"date-time":"2018-09-11T11:40:02Z","timestamp":1536666002000},"page":"3037","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Fecal Volatile Organic Compounds in Preterm Infants Are Influenced by Enteral Feeding Composition"],"prefix":"10.3390","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2806-444X","authenticated-orcid":false,"given":"Sofia","family":"El Manouni el Hassani","sequence":"first","affiliation":[{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Academic Medical Center, 1081 HV Amsterdam, The Netherlands"},{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, 1105 AZ Amsterdam, The Netherlands"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0844-7208","authenticated-orcid":false,"given":"Hendrik J.","family":"Niemarkt","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, M\u00e1xima Medical Center, 5504 DB Veldhoven, The Netherlands"}]},{"given":"Hager","family":"Said","sequence":"additional","affiliation":[{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, 1105 AZ Amsterdam, The Netherlands"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0043-1324","authenticated-orcid":false,"given":"Daniel J. C.","family":"Berkhout","sequence":"additional","affiliation":[{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Academic Medical Center, 1081 HV Amsterdam, The Netherlands"},{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, 1105 AZ Amsterdam, The Netherlands"}]},{"given":"Anton H.","family":"Van Kaam","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Emma Children\u2019s Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, The Netherlands"},{"name":"Neonatal Intensive Care Unit, Emma Children\u2019s Hospital, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6321-3853","authenticated-orcid":false,"given":"Richard A.","family":"Van Lingen","sequence":"additional","affiliation":[{"name":"Neonatal Intensive Care Unit, Amalia Children\u2019s Center\/Isala, 8025 AB Zwolle, The Netherlands"}]},{"given":"Marc A.","family":"Benninga","sequence":"additional","affiliation":[{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Academic Medical Center, 1081 HV Amsterdam, The Netherlands"}]},{"given":"Nanne K. H.","family":"De Boer","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, Amsterdam UMC, VU University Medical Center, 1081 HV Amsterdam, The Netherlands"}]},{"given":"Tim G. J.","family":"De Meij","sequence":"additional","affiliation":[{"name":"Department of Pediatric Gastroenterology, Emma Children\u2019s Hospital, Amsterdam UMC, Vrije Universiteit Amsterdam, 1105 AZ Amsterdam, The Netherlands"}]}],"member":"1968","published-online":{"date-parts":[[2018,9,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1093\/jb\/mvr090","article-title":"The scent of disease: Volatile organic compounds of the human body related to disease and disorder","volume":"150","author":"Shirasu","year":"2011","journal-title":"J. Biochem."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.trac.2016.12.004","article-title":"Detection of exogenous VOCs as a novel in vitro diagnostic technique for the detection of pathogenic bacteria","volume":"87","author":"Lough","year":"2017","journal-title":"TrAC Trends Anal. Chem."},{"key":"ref_3","first-page":"337","article-title":"Volatile organic compounds as diagnostic biomarkers in gastrointestinal and liver diseases","volume":"18","author":"Probert","year":"2009","journal-title":"J. Gastrointest. Liver Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2069","DOI":"10.1097\/MIB.0b013e31829a91f6","article-title":"Analysis of volatile organic compounds of bacterial origin in chronic gastrointestinal diseases","volume":"19","author":"Walton","year":"2013","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1097\/MPG.0000000000001250","article-title":"Sniffing out Paediatric Gastrointestinal Diseases: The Potential of Volatile Organic Compounds as Biomarkers for Disease","volume":"63","author":"Buijck","year":"2016","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.jpeds.2015.05.044","article-title":"Early Detection of Necrotizing Enterocolitis by Fecal Volatile Organic Compounds Analysis","volume":"167","author":"Berkhout","year":"2015","journal-title":"J. Pediatr."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"De Meij, T.G., De Boer, N.K., Benninga, M.A., Lentferink, Y.E., de Groot, E.F., van de Velde, M.E., van Bodegraven, A.A., and van der Schee, M.P. (2014). Faecal gas analysis by electronic nose as novel, non-invasive method for assessment of active and quiescent paediatric inflammatory bowel disease: Proof of principle study. J. Crohns Colitis.","DOI":"10.1016\/j.crohns.2014.09.004"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.1002\/ijc.28446","article-title":"Electronic nose can discriminate colorectal carcinoma and advanced adenomas by fecal volatile biomarker analysis: Proof of principle study","volume":"134","author":"Larbi","year":"2014","journal-title":"Int. J. Cancer"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1097\/MPG.0b013e3181a3bfbc","article-title":"Analysis of faecal volatile organic compounds in preterm infants who develop necrotising enterocolitis: A pilot study","volume":"49","author":"Garner","year":"2009","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e47","DOI":"10.1097\/MPG.0000000000001471","article-title":"Detection of Sepsis in Preterm Infants by Fecal Volatile Organic Compounds Analysis: A Proof of Principle Study","volume":"65","author":"Berkhout","year":"2017","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1038\/pr.2017.268","article-title":"Development of severe bronchopulmonary dysplasia is associated with alterations in fecal volatile organic compounds","volume":"83","author":"Berkhout","year":"2018","journal-title":"Pediatr. Res."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Berkhout, D.J.C., van Keulen, B.J., Niemarkt, H.J., Bessem, J.R., de Boode, W.P., Cossey, V., Hoogenes, N., Hulzebos, C.V., Klaver, E., and Andriessen, P. (2018). Late-onset sepsis in preterm infants can be detected preclinically by fecal volatile organic compound analysis: A prospective, multicenter cohort study. Clin. Infect. Dis., in press.","DOI":"10.1093\/cid\/ciy383"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1111\/apt.12657","article-title":"Review article: Next generation diagnostic modalities in gastroenterology\u2014Gas phase volatile compound biomarker detection","volume":"39","author":"Arasaradnam","year":"2014","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Wilson, A.D. (2018). Application of Electronic-Nose Technologies and VOC-Biomarkers for the Noninvasive Early Diagnosis of Gastrointestinal Diseases (dagger). Sensors, 18.","DOI":"10.3390\/s18082613"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1128\/CMR.00020-13","article-title":"Clinical application of volatile organic compound analysis for detecting infectious diseases","volume":"26","author":"Sethi","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"13002","DOI":"10.3390\/s121013002","article-title":"The detection of patients at risk of gastrointestinal toxicity during pelvic radiotherapy by electronic nose and FAIMS: A pilot study","volume":"12","author":"Covington","year":"2012","journal-title":"Sensors"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1016\/j.bios.2014.10.044","article-title":"Development and application of a new electronic nose instrument for the detection of colorectal cancer","volume":"67","author":"Westenbrink","year":"2015","journal-title":"Biosens. Bioelectron."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"333","DOI":"10.3109\/03091902.2012.690015","article-title":"Evaluation of gut bacterial populations using an electronic e-nose and field asymmetric ion mobility spectrometry: Further insights into \u2018fermentonomics\u2019","volume":"36","author":"Arasaradnam","year":"2012","journal-title":"J. Med. Eng. Technol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Berkhout, D.J., Benninga, M.A., van Stein, R.M., Brinkman, P., Niemarkt, H.J., de Boer, N.K., and de Meij, T.G. (2016). Effects of Sampling Conditions and Environmental Factors on Fecal Volatile Organic Compound Analysis by an Electronic Nose Device. Sensors, 16.","DOI":"10.3390\/s16111967"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"7972","DOI":"10.1021\/acs.analchem.8b00688","article-title":"Optimized Sampling Conditions for Fecal Volatile Organic Compound Analysis by Means of Field Asymmetric Ion Mobility Spectrometry","volume":"90","author":"Bosch","year":"2018","journal-title":"Anal. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Wu, I.H., Tsai, M.H., Lai, M.Y., Hsu, L.F., Chiang, M.C., Lien, R., Fu, R.H., Huang, H.R., Chu, S.M., and Hsu, J.F. (2017). Incidence, clinical features, and implications on outcomes of neonatal late-onset sepsis with concurrent infectious focus. BMC Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2574-7"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1159\/000489677","article-title":"Risk Factors for Necrotizing Enterocolitis: A Prospective Multicenter Case-Control Study","volume":"114","author":"Berkhout","year":"2018","journal-title":"Neonatology"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Corvaglia, L., Fantini, M.P., Aceti, A., Gibertoni, D., Rucci, P., Baronciani, D., and Faldella, G. (2014). Predictors of full enteral feeding achievement in very low birth weight infants. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0092235"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1097\/NNR.0000000000000208","article-title":"Influence of Feeding Type on Gut Microbiome Development in Hospitalized Preterm Infants","volume":"66","author":"Cong","year":"2017","journal-title":"Nurs. Res."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Cong, X., Xu, W., Janton, S., Henderson, W.A., Matson, A., McGrath, J.M., Maas, K., and Graf, J. (2016). Gut Microbiome Developmental Patterns in Early Life of Preterm Infants: Impacts of Feeding and Gender. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0152751"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1186\/s40168-016-0214-x","article-title":"Influence of maternal breast milk ingestion on acquisition of the intestinal microbiome in preterm infants","volume":"4","author":"Gregory","year":"2016","journal-title":"Microbiome"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1007\/s12078-009-9044-6","article-title":"Characterization of the Volatile Composition and Variations between Infant Formulas and Mother\u2019s Milk","volume":"2","author":"Hausner","year":"2009","journal-title":"Chemosens. Percept."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Palmer, C., Bik, E.M., DiGiulio, D.B., Relman, D.A., and Brown, P.O. (2007). Development of the human infant intestinal microbiota. PLoS Biol., 5.","DOI":"10.1371\/journal.pbio.0050177"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.jpeds.2009.06.063","article-title":"Intestinal microbial ecology in premature infants assessed with non-culture-based techniques","volume":"156","author":"Mshvildadze","year":"2010","journal-title":"J. Pediatr."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Bos, L.D., Sterk, P.J., and Schultz, M.J. (2013). Volatile metabolites of pathogens: A systematic review. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003311"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"12522","DOI":"10.1073\/pnas.1409497111","article-title":"Patterned progression of bacterial populations in the premature infant gut","volume":"111","author":"Warner","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Dahl, C., Stigum, H., Valeur, J., Iszatt, N., Lenters, V., Peddada, S., Bj\u00f8rnholt, J.V., Midtvedt, T., Mandal, S., and Eggesb\u00f8, M. (2018). Preterm infants have distinct microbiomes not explained by mode of delivery, breastfeeding duration or antibiotic exposure. Int. J. Epidemiol., dyy064.","DOI":"10.1093\/ije\/dyy064"}],"container-title":["Sensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8220\/18\/9\/3037\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:19:57Z","timestamp":1760195997000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8220\/18\/9\/3037"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,9,11]]},"references-count":32,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2018,9]]}},"alternative-id":["s18093037"],"URL":"https:\/\/doi.org\/10.3390\/s18093037","relation":{},"ISSN":["1424-8220"],"issn-type":[{"value":"1424-8220","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,9,11]]}}}