{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T01:55:30Z","timestamp":1777600530707,"version":"3.51.4"},"reference-count":49,"publisher":"Springer Science and Business Media LLC","issue":"11","license":[{"start":{"date-parts":[[2013,5,1]],"date-time":"2013-05-01T00:00:00Z","timestamp":1367366400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Bioprocess Biosyst Eng"],"published-print":{"date-parts":[[2013,11]]},"DOI":"10.1007\/s00449-013-0954-y","type":"journal-article","created":{"date-parts":[[2013,5,1]],"date-time":"2013-05-01T12:14:01Z","timestamp":1367410441000},"page":"1787-1796","source":"Crossref","is-referenced-by-count":39,"title":["Influence of flow rate variation on the development of Escherichia coli biofilms"],"prefix":"10.1007","volume":"36","author":[{"given":"J. M. R.","family":"Moreira","sequence":"first","affiliation":[]},{"given":"J. S.","family":"Teod\u00f3sio","sequence":"additional","affiliation":[]},{"given":"F. C.","family":"Silva","sequence":"additional","affiliation":[]},{"given":"M.","family":"Sim\u00f5es","sequence":"additional","affiliation":[]},{"given":"L. F.","family":"Melo","sequence":"additional","affiliation":[]},{"given":"F. J.","family":"Mergulh\u00e3o","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2013,5,1]]},"reference":[{"key":"954_CR1","doi-asserted-by":"crossref","first-page":"2413","DOI":"10.1128\/JB.00003-12","volume":"194","author":"OE Petrova","year":"2012","unstructured":"Petrova OE, Sauer K (2012) Sticky situations\u2014key components that control bacterial surface attachment. J Bacteriol 194:2413\u20132425","journal-title":"J Bacteriol"},{"key":"954_CR2","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1134\/S0026261707020014","volume":"76","author":"Y Nikolaev","year":"2007","unstructured":"Nikolaev Y, Plakunov V (2007) Biofilm\u2014\u201cCity of microbes\u201d or an analogue of multicellular organisms? Microbiology 76:125\u2013138","journal-title":"Microbiology"},{"key":"954_CR3","doi-asserted-by":"crossref","first-page":"2936","DOI":"10.1128\/AEM.72.4.2936-2941.2006","volume":"72","author":"NF Azevedo","year":"2006","unstructured":"Azevedo NF, Pinto AR, Reis NM, Vieira MJ, Keevil CW (2006) Shear stress, temperature, and inoculation concentration influence the adhesion of water-stressed Helicobacter pylori to stainless steel 304 and polypropylene. Appl Environ Microbiol 72:2936\u20132941","journal-title":"Appl Environ Microbiol"},{"key":"954_CR4","doi-asserted-by":"crossref","first-page":"7418","DOI":"10.1128\/AEM.70.12.7418-7425.2004","volume":"70","author":"SM Hunt","year":"2004","unstructured":"Hunt SM, Werner EM, Huang B, Hamilton MA, Stewart PS (2004) Hypothesis for the role of nutrient starvation in biofilm detachment. Appl Environ Microbiol 70:7418\u20137425","journal-title":"Appl Environ Microbiol"},{"key":"954_CR5","doi-asserted-by":"crossref","first-page":"19S","DOI":"10.1111\/j.1365-2672.1998.tb05279.x","volume":"85","author":"P Stoodley","year":"1998","unstructured":"Stoodley P, Dodds I, Boyle JD, Lappin-Scott HM (1998) Influence of hydrodynamics and nutrients on biofilm structure. J Appl Microbiol 85:19S\u201328S","journal-title":"J Appl Microbiol"},{"key":"954_CR6","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.tim.2006.07.001","volume":"14","author":"R Singh","year":"2006","unstructured":"Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389\u2013397","journal-title":"Trends Microbiol"},{"key":"954_CR7","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/1475-2859-4-24","volume":"4","author":"N Qureshi","year":"2005","unstructured":"Qureshi N, Annous B, Ezeji T, Karcher P, Maddox I (2005) Biofilm reactors for industrial bioconversion processes: employing potential of enhanced reaction rates. Microb Cell Fact 4:24","journal-title":"Microb Cell Fact"},{"key":"954_CR8","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/scientificamerican0701-74","volume":"285","author":"JW Costerton","year":"2001","unstructured":"Costerton JW, Stewart PS (2001) Battling biofilms\u2014the war is against bacterial colonies that cause some of the most tenacious infections known. The weapon is knowledge of the enemy\u2019s communication system. Sci Am 285:74\u201381","journal-title":"Sci Am"},{"key":"954_CR9","doi-asserted-by":"crossref","first-page":"1318","DOI":"10.1126\/science.284.5418.1318","volume":"284","author":"JW Costerton","year":"1999","unstructured":"Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318\u20131322","journal-title":"Science"},{"key":"954_CR10","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1016\/j.tifs.2009.01.054","volume":"20","author":"X Shi","year":"2009","unstructured":"Shi X, Zhu X (2009) Biofilm formation and food safety in food industries. Trends Food Sci Technol 20:407\u2013413","journal-title":"Trends Food Sci Technol"},{"key":"954_CR11","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1111\/j.1365-2672.2010.04756.x","volume":"109","author":"R Houdt Van","year":"2010","unstructured":"Van Houdt R, Michiels CW (2010) Biofilm formation and the food industry, a focus on the bacterial outer surface. J Appl Microbiol 109:1117\u20131131","journal-title":"J Appl Microbiol"},{"issue":"Suppl 1","key":"954_CR12","doi-asserted-by":"crossref","first-page":"S331","DOI":"10.1016\/S0098-1354(98)00072-6","volume":"22","author":"MC Georgiadis","year":"1998","unstructured":"Georgiadis MC, Rotstein GE, Macchietto S (1998) Modelling and simulation of complex plate heat exchanger arrangements under milk fouling. Comput Chem Eng 22(Suppl 1):S331\u2013S338","journal-title":"Comput Chem Eng"},{"key":"954_CR13","doi-asserted-by":"crossref","first-page":"7456","DOI":"10.1128\/AEM.00845-07","volume":"73","author":"T Juhna","year":"2007","unstructured":"Juhna T, Birzniece D, Larsson S, Zulenkovs D, Sharipo A, Azevedo NF, Menard-Szczebara F, Castagnet S, Feliers C, Keevil CW (2007) Detection of Escherichia coli in biofilms from pipe samples and coupons in drinking water distribution networks. Appl Environ Microbiol 73:7456\u20137464","journal-title":"Appl Environ Microbiol"},{"key":"954_CR14","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.ijfoodmicro.2011.07.004","volume":"149","author":"D Dourou","year":"2011","unstructured":"Dourou D, Beauchamp CS, Yoon Y, Geornaras I, Belk KE, Smith GC, Nychas G-JE, Sofos JN (2011) Attachment and biofilm formation by Escherichia coli O157:H7 at different temperatures, on various food-contact surfaces encountered in beef processing. Int J Food Microbiol 149:262\u2013268","journal-title":"Int J Food Microbiol"},{"key":"954_CR15","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.resmic.2005.10.003","volume":"157","author":"MH Castonguay","year":"2006","unstructured":"Castonguay MH, van der Schaaf S, Koester W, Krooneman J, van der Meer W, Harmsen H, Landini P (2006) Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res Microbiol 157:471\u2013478","journal-title":"Res Microbiol"},{"key":"954_CR16","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.colsurfb.2005.04.004","volume":"43","author":"MJ Chen","year":"2005","unstructured":"Chen MJ, Zhang Z, Bott TR (2005) Effects of operating conditions on the adhesive strength of Pseudomonas fluorescens biofilms in tubes. Colloid Surface B 43:61\u201371","journal-title":"Colloid Surface B"},{"key":"954_CR17","first-page":"3661","volume":"129","author":"DE Brooks","year":"1983","unstructured":"Brooks DE, Trust TJ (1983) Enhancement of bacterial adhesion by shear forces: characterization of the haemagglutination induced by Aeromonas salmonicida strain 438. J Gen Microbiol 129:3661\u20133669","journal-title":"J Gen Microbiol"},{"key":"954_CR18","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1038\/379266a0","volume":"379","author":"EB Finger","year":"1996","unstructured":"Finger EB, Purl KD, Alon R, Lawrence MB, von Andrian UH, Springer TA (1996) Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature 379:266\u2013269","journal-title":"Nature"},{"key":"954_CR19","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1002\/(SICI)1097-0290(20000620)68:6<628::AID-BIT5>3.0.CO;2-D","volume":"68","author":"N Mohamed","year":"2000","unstructured":"Mohamed N, Rainier TR, Ross JM (2000) Novel experimental study of receptor-mediated bacterial adhesion under the influence of fluid shear. Biotechnol Bioeng 68:628\u2013636","journal-title":"Biotechnol Bioeng"},{"key":"954_CR20","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1205\/fbp.04021","volume":"83","author":"BBB Jensen","year":"2005","unstructured":"Jensen BBB, Friis A, Benezech T, Legentilhomme P, Lelievre C (2005) Local wall shear stress variations predicted by computational fluid dynamics for hygienic design. Food Bioprod Process 83:53\u201360","journal-title":"Food Bioprod Process"},{"key":"954_CR21","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1007\/s004490050605","volume":"20","author":"MJ Vieira","year":"1999","unstructured":"Vieira MJ, Melo LF (1999) Intrinsic kinetics of biofilms formed under turbulent flow and low substrate concentrations. Bioprocess Biosyst Eng 20:369\u2013375","journal-title":"Bioprocess Biosyst Eng"},{"key":"954_CR22","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1021\/bp010129s","volume":"18","author":"H Beyenal","year":"2002","unstructured":"Beyenal H, Lewandowski Z (2002) Internal and external mass transfer in biofilms grown at various flow velocities. Biotechnol Prog 18:55\u201361","journal-title":"Biotechnol Prog"},{"key":"954_CR23","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1002\/1097-0290(20000905)69:5<504::AID-BIT5>3.0.CO;2-S","volume":"69","author":"C Picioreanu","year":"2000","unstructured":"Picioreanu C, VanLoosdrecht MCM, Heijnen JJ (2000) Effect of diffusive and convective substrate transport on biofilm structure formation: a two-dimensional modeling study. Biotechnol Bioeng 69:504\u2013515","journal-title":"Biotechnol Bioeng"},{"key":"954_CR24","volume-title":"Perry\u2019s chemical engineers\u2019 handbook","author":"RH Perry","year":"1997","unstructured":"Perry RH, Green DW (1997) Perry\u2019s chemical engineers\u2019 handbook. McGraw-Hill, New York"},{"key":"954_CR25","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s004490050604","volume":"20","author":"LF Melo","year":"1999","unstructured":"Melo LF, Vieira MJ (1999) Physical stability and biological activity of biofilms under turbulent flow and low substrate concentration. Bioprocess Eng 20:363\u2013368","journal-title":"Bioprocess Eng"},{"key":"954_CR26","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/0021-9991(86)90099-9","volume":"62","author":"RI Issa","year":"1986","unstructured":"Issa RI (1986) Solution of the implicitly discutised fluid flow equations by operating-splitting. J Comput Phys 62:40\u201365","journal-title":"J Comput Phys"},{"key":"954_CR27","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/0045-7825(79)90034-3","volume":"19","author":"BP Leonard","year":"1979","unstructured":"Leonard BP (1979) A stable and accurate convective modelling procedure based on quadratic upstream interpolation. Comput Methods Appl Mech Eng 19:59\u201398","journal-title":"Comput Methods Appl Mech Eng"},{"key":"954_CR28","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.2514\/3.12149","volume":"32","author":"FR Menter","year":"1994","unstructured":"Menter FR (1994) Two-equation eddy-viscosity turbulence models for engineering applications. AIAA J 32:1598\u20131605","journal-title":"AIAA J"},{"key":"954_CR29","volume-title":"Mathematical models of turbulence","author":"BE Launder","year":"1972","unstructured":"Launder BE, Spalding DB (1972) Mathematical models of turbulence. Academic Press Inc, London"},{"key":"954_CR30","volume-title":"Turbulence modeling for CFD","author":"D Wilcox","year":"1998","unstructured":"Wilcox D (1998) Turbulence modeling for CFD. DCW Industries Inc, California"},{"key":"954_CR31","doi-asserted-by":"crossref","unstructured":"Teod\u00f3sio JS, Sim\u00f5es M, Alves MA, Melo LF, Mergulh\u00e3o FJ (2012) Setup and validation of flow cell systems for biofouling simulation in industrial settings. Sci World J ID 361496","DOI":"10.1100\/2012\/361496"},{"key":"954_CR32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/08927014.2010.535206","volume":"27","author":"JS Teod\u00f3sio","year":"2011","unstructured":"Teod\u00f3sio JS, Sim\u00f5es M, Melo LF, Mergulh\u00e3o FJ (2011) Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling 27:1\u201311","journal-title":"Biofouling"},{"key":"954_CR33","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.ijfoodmicro.2008.09.003","volume":"128","author":"M Sim\u00f5es","year":"2008","unstructured":"Sim\u00f5es M, Sim\u00f5es LC, Vieira MJ (2008) Physiology and behavior of Pseudomonas fluorescens single and dual strain biofilms under diverse hydrodynamics stresses. Int J Food Microbiol 128:309\u2013316","journal-title":"Int J Food Microbiol"},{"key":"954_CR34","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1111\/j.1365-2672.2012.05332.x","volume":"113","author":"JS Teod\u00f3sio","year":"2012","unstructured":"Teod\u00f3sio JS, Sim\u00f5es M, Mergulh\u00e3o FJ (2012) The influence of non-conjugative Escherichia coli plasmids on biofilm formation and resistance. J Appl Microbiol 113:373\u2013382","journal-title":"J Appl Microbiol"},{"key":"954_CR35","first-page":"426","volume":"31","author":"GL Miller","year":"1959","unstructured":"Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. J Am Chem Soc 31:426\u2013428","journal-title":"J Am Chem Soc"},{"key":"954_CR36","volume-title":"Use of flow cells and annular reactors to study biofilms","author":"P Stoodley","year":"2003","unstructured":"Stoodley P, Warwood BK (2003) In: Lens P, O\u2019Flaherty V, Moran AP, Stoodley P, Mahony T (eds) Use of flow cells and annular reactors to study biofilms. IWA Publishing Place, London"},{"key":"954_CR37","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1080\/08927010903114603","volume":"25","author":"MM Salek","year":"2009","unstructured":"Salek MM, Jones SM, Martinuzzi RJ (2009) The influence of flow cell geometry related shear stresses on the distribution, structure and susceptibility of Pseudomonas aeruginosa 01 biofilms. Biofouling 25:711\u2013725","journal-title":"Biofouling"},{"key":"954_CR38","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/j.ces.2013.02.045","volume":"94","author":"JMR Moreira","year":"2013","unstructured":"Moreira JMR, Gomes LC, Ara\u00fajo JDP, Miranda JM, Sim\u00f5es M, Melo LF, Mergulh\u00e3o FJ (2013) The effect of glucose concentration and shaking conditions on Escherichia coli biofilm formation in microtiter plates. Chem Eng Sci 94:192\u2013199","journal-title":"Chem Eng Sci"},{"key":"954_CR39","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1111\/j.1471-0307.2005.00213.x","volume":"58","author":"S Jun","year":"2005","unstructured":"Jun S, Puri VM (2005) 3D milk-fouling model of plate heat exchangers using computational fluid dynamics. Int J Dairy Technol 58:214\u2013224","journal-title":"Int J Dairy Technol"},{"key":"954_CR40","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1142\/S1758825111001226","volume":"3","author":"J Lantz","year":"2011","unstructured":"Lantz J, Renner J, Karlsson M (2011) Wall shear stress in a subject specific human aorta\u2014influence of fluid-structure interaction. Int J Appl Mech 3:759\u2013778","journal-title":"Int J Appl Mech"},{"key":"954_CR41","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.desal.2011.03.045","volume":"276","author":"S Ahmed","year":"2011","unstructured":"Ahmed S, Seraji MT, Jahedi J, Hashib MA (2011) CFD simulation of turbulence promoters in a tubular membrane channel. Desalination 276:191\u2013198","journal-title":"Desalination"},{"key":"954_CR42","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1006\/jcis.2002.8321","volume":"250","author":"G Konuklar","year":"2002","unstructured":"Konuklar G, Gunasekaran S (2002) Rennet-induced milk coagulation by continuous steady shear stress. J Colloid Interface Sci 250:149\u2013158","journal-title":"J Colloid Interface Sci"},{"key":"954_CR43","doi-asserted-by":"crossref","first-page":"H1031","DOI":"10.1152\/ajpheart.00989.2006","volume":"293","author":"AD Augst","year":"2007","unstructured":"Augst AD, Ariff B, McG. Thom SAG, Xu XY, Hughes AD (2007) Analysis of complex flow and the relationship between blood pressure, wall shear stress, and intima-media thickness in the human carotid artery. Am J Physiol-Heart 293:H1031\u2013H1037","journal-title":"Am J Physiol-Heart"},{"key":"954_CR44","doi-asserted-by":"crossref","first-page":"2035","DOI":"10.1001\/jama.282.21.2035","volume":"282","author":"AM Malek","year":"1999","unstructured":"Malek AM, Alper SL, Izumo S (1999) Hemodynamic shear stress and its role in atherosclerosis. J Am Med Assoc 282:2035\u20132042","journal-title":"J Am Med Assoc"},{"key":"954_CR45","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1016\/S0043-1354(01)00379-7","volume":"36","author":"Y Liu","year":"2002","unstructured":"Liu Y, Tay J (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36:1653\u20131665","journal-title":"Water Res"},{"key":"954_CR46","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/nrmicro1838","volume":"6","author":"PS Stewart","year":"2008","unstructured":"Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199\u2013210","journal-title":"Nat Rev Microbiol"},{"key":"954_CR47","doi-asserted-by":"crossref","first-page":"2711","DOI":"10.1128\/AEM.60.8.2711-2716.1994","volume":"60","author":"P Stoodley","year":"1994","unstructured":"Stoodley P, deBeer D, Lewandowski Z (1994) Liquid flow in biofilm systems. Appl Environ Microbiol 60:2711\u20132716","journal-title":"Appl Environ Microbiol"},{"key":"954_CR48","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1002\/(SICI)1097-0290(19971220)56:6<681::AID-BIT11>3.0.CO;2-B","volume":"56","author":"P Stoodley","year":"1997","unstructured":"Stoodley P, Yang S, Lappin-Scott H, Lewandowski Z (1997) Relationship between mass transfer coefficient and liquid flow velocity in heterogenous biofilms using microelectrodes and confocal microscopy. Biotechnol Bioeng 56:681\u2013688","journal-title":"Biotechnol Bioeng"},{"key":"954_CR49","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1161\/01.ATV.10.4.607","volume":"10","author":"W Inauen","year":"1990","unstructured":"Inauen W, Baumgartner HR, Bombeli T, Haeberli A, Straub PW (1990) Dose- and shear rate-dependent effects of heparin on thrombogenesis induced by rabbit aorta subendothelium exposed to flowing human blood. Arterioscler Thromb Vasc Biol 10:607\u2013615","journal-title":"Arterioscler Thromb Vasc Biol"}],"container-title":["Bioprocess and Biosystems Engineering"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00449-013-0954-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00449-013-0954-y\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00449-013-0954-y","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,7,26]],"date-time":"2020-07-26T04:09:41Z","timestamp":1595736581000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00449-013-0954-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,5,1]]},"references-count":49,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2013,11]]}},"alternative-id":["954"],"URL":"https:\/\/doi.org\/10.1007\/s00449-013-0954-y","relation":{},"ISSN":["1615-7591","1615-7605"],"issn-type":[{"value":"1615-7591","type":"print"},{"value":"1615-7605","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,5,1]]}}}