* T. E. CloeteDepartment of Microbiology and Plant Pathology,University of PretoriaPretoria 0001 (South Africa)

Biofouling control in industrial water systems:What we know and what we need to know

T. E. Cloete*

Biofouling contributes substantially to economic losses in indus-try. Although much progress has been made in understanding bio-fouling and its implications in industrial water systems, many ques-tions remain unanswered.

The cost of biofouling has not been enumerated. A prerequisitefor this is research to elucidate the contribution that microbiologi-cally influenced corrosion makes, to the overall corrosion process.Surface characteristics play a major role in the initial stages of mi-crobial attachment. Ways of preventing preferential attachment to

certain areas, i.e. grain boundaries and welds need further investi-gation. Biocides are routinely used to control biofouling. Due to theproblem of resistance and potential environmental impact, alterna-tive strategies for biofouling control need to be investigated and putto practice. These should focus on an integrated approach with theminimum impact on the environment. A number of biofouling mon-itoring devices have been developed. The advantages of biofoulingmonitoring needs to be demonstrated and monitors should becomecommercially available.

1 Introduction

During the past 20 years much progress has been made inthe study of biofouling and biocorrosion and the control there-of. Although the exact cost, direct and/or indirect has not beenaccurately determined, it is generally accepted that it is sig-nificant.

During the early days, we saw the focus moving away fromstudying planktonic to sessile microorganisms. Much progresshas since been made in the field of biofilm research. New so-phisticated equipment and tools have brought new insightsinto the ultrastructure and function of biofilms. Biofilm mon-itoring is also one of the key issues in understanding biofilmphenomena. Although numerous methods have been reported,few have been commercialised.

A number of control strategies were developed. These in-cluded novel biocides, of which the mechanism of action hasbeen elucidated. A major problem with the use of non-oxidis-ing biocides is the build up of resistance in microorganismsand the potential detrimental impact these chemicals mighthave on the environment. This has led to the developmentof more environmentally friendly biofouling control strate-gies, including non-persistent biocides, surfactants and an in-tegrated approach to biofouling control.

Recently biological control of biofouling has received at-tention, as well as the development of “smart” materials cap-able of acting biocidal. The objective of this review, is to coversome of the more recent developments in a number of fieldsrelated to biofouling control in industrial water systems and tohighlight some of the questions that still need to be answered.

2 Microheterogeneities affecting surface colonization

There are a number of factors that promote the adhesion ofmicroorganisms to surfaces [1]. Surface roughness and com-position play a major role in the early stages of biofilm for-mation and may influence the rate of cell accumulation andcell distribution. Another key factor in microbial adhesionis hydrodynamic shear stress. These factors will now be dis-cussed in more detail.

2.1 Flow rate

Although it is very difficult to relate initial colonisation toone single determining factor, results from several studies sug-gest that a definite relationship exists between flow rate, at-tachment and extracelullar polymeric substances (EPS) pro-duction. Some controversy still exists regarding the influenceof water velocity and biofilm development. Flemming andSchaule [2] concluded that higher flow velocities and thusstrong shear forces do not prevent biofilm formation butlead to thinner and firmer biofilms. Higher velocities mayhave an influence on the amount of EPS found within the bio-film. Higher EPS production and higher bacterial counts were

520 Cloete Materials and Corrosion 54, 520–526 (2003)

0947-5117/03/0707-0520$17.50þ.50/0 F 2003 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

observed when increasing the flow (turbulent) rate in a drink-ing water system [3]. Biofouling in pipelines is a function ofthe inner roughness of the specific piping material that is usedin distribution systems and the concomitant biofilm forma-tion. To test the effect of velocity on the growth of biofilm,a Roto-Scope was designed and built to imitate different ma-terials and flow conditions in potable water distribution sys-tems. Biofilm formation was monitored using DAPI staining,scanning electron microscopy and total viable number of bac-teria. Increased velocity in the system resulted in a specificdetaching velocity, where the formation of biofilm was lim-ited. Most of the time these detaching velocities were not thehighest velocities tested. The range of detaching velocitieswere between� 3 m � s�1 and 4 m � s�1. A flow velocity with-in this range would thus be ideal for achieving reduced biofilmgrowth in a distribution system [4].

2.2 Production of extracellular polymers

Many bacterial strains are capable of producing extracellu-lar polymeric substances. The major functions of EPS are to:(i) bind cells together in the biofilm, (ii) protect them againsthostile conditions, (iii) retain water, and (iv) accumulate nu-trients.

Bacteria producing EPS seem to be important to initial bio-film formation. The microbial EPS can, contribute to redoxreactions involving metals. Development of EPS-formingbacteria can cause the formation of patchy biofilms on thesteel surface and the so-called concentration cells [5], whichcould initiate the corrosion process [6].

2.3 Bacterial adhesion at welds and heat-affected zones

Welds and unpickled heat-affected zones (HAZ) of stain-less steels are most susceptible to MIC-associated pitting cor-rosion due to the “sensitisation” in these regions [7]. ThisHAZ exhibits distortions in the size and shape of the metalgrains as a result of the uneven postweld cooling process (min-or effect).

There seems to be a correlation between biocorrosion andthe sensitisation state of austenitic stainless steels [8], or moreexactly with the chromium depleted zones and carbide preci-pitations at the grain boundaries or in the austenite-ferrite in-terfaces. The structural and physiological heterogeneities inthe biofilm may locally increase corrosivity [9].

2.4 Bacterial adhesion at inclusions and grain boundaries

Random attachment, proliferation and/or aggregation ofbacteria at any location is determined by proximity to metal-lurgical features such as inclusions [10]. Even the compositionand morphology of these inclusions influences the bio-corrosion [11]. It has been indicated that biofilm-forming bac-teria selectively colonised grain boundaries [12]. This causeslong-term patchiness in surface coverage by the biofilm bac-teria and offers ample opportunity for the initiation of loca-lised corrosion that might evolve from such biological hetero-geneity.

2.5 Bacterial adhesion at crevices

Perhaps the area of largest controversy relates to the invol-vement of microorganisms in crevice corrosion. Some resultsindicated that the presence of a biofilm on cathodic areas pro-duces an increase of the corrosion rate by about two orders ofmagnitude by depolarisation of the oxygen reduction [13].

3 Chemical control of biofouling

MIC is caused by the presence of bacteria in water systems,especially by bacterial biofilms. It is the most obvious conclu-sion, that such bacterial biofilms must be removed. Five ap-proaches are currently followed: (i) bacteria are chemicallykilled by application of bactericidal compounds termed bio-cides at lethal doses; (ii) biofilms are physically removed by aprocess known as “pigging”; (iii) biofilms in heat exchangerscan be removed by a patented process known as ice nuclea-tion, where the heat exchanger is frozen, and ice crystals phy-sically dislodge the biofilms; (iv) biofilms are dispersed bydispersants; and (v) biofilms are degraded by enzymes [14].

A range of bactericidal substances, commonly termed bio-cides or microbicides, are available, all of which are claimedby their agents to kill bacteria in aqueous systems quantita-tively (Table 1) [14]. However, different bacteria react differ-ently to bactericides, either due to differing cell wall proper-ties, or to other mechanisms of resistance, either inherent orinducible [14].

3.1 Environmental considerations

Sooner or later biocides used to treat industrial water will bereleased into the environment. Ideally a biocide should affectonly the target microorganisms against which its use was in-tended. All chemicals, however, have some effect at a greateror lesser concentration on plant and animal life. It is alwaysassumed that dilution and natural degradation will inactivateany biocide and laboratory investigation has indicated that thecommercially available biocides can be biodegraded.

Such findings do not necessarily imply that biodegradationwill take place equally readily in the environment. It must beclear from the foregoing that, if industry is to continue to usebiocides for the control of biofouling, questions of “in situ”biocide effectiveness, resistance, biodegradability and envir-onmental impact will have to be answered. These answers will

Table 1. The most commonly used non-oxidising and oxidisingbiocides used to control biofouling in industrial water systems

Non-oxidising Oxidising Biocides

Biguanides ChlorineIsothiazolones OzonePhosphonium biocides BromineGlutaraldehyde Bromochlorodimenthyl-

hydantionMethylene bisthiocyanate Chlorine dioxideChlorophenols Hydrogen peroxideQuaternary ammonium salts Stabilized bromineOrganic sulphurs (& sulphones) Electrochemically activated

waterThiocarbamates

Materials and Corrosion 54, 520–526 (2003) Biofouling control in industrial water systems 521

only be found by co-operation between biocide manufacturersand producers, operators, chemists, biochemists, microbiolo-gists, marine biologists and legislative authorities [15].

Research has indicated the problem of microbial resistanceto nonoxidising biocides. Very little information is furthermore available on the biodegradability of these compoundsin natural water systems. This makes these compounds hazar-dous from an environmental point of view. Chlorine is themost widely used oxidizing biocide, with its own limitations.An environmentally sensible alternative to chlorine and othercommonly used biocides is needed. Electrochemically acti-vated water (ECA) solutions, may provide such an alternative.Water of varying mineralisation is passed through an electro-chemical cell, the specific design of which, permits the har-nessing of two distinct and electrically opposite streams ofactivated water. Aside from its distinctive attributes, the ne-gatively charged anti-oxidant solution (Catholyte) can also bechanneled back into the anode chamber, thereby modulatingthe quality of the positively charged oxidant solution (Ano-lyte) that is produced.

Without maintenance of the activated state, these diverseproducts degrade to the relaxed state of benign water andthe anomalous attributes of the activated solutions such as al-tered conductivity and surface tension similarly revert to pre-activation status. However, the heightened electrical activityand altered physico-chemical attributes of the solutions differsignificantly from the benign state, but yet remain non-toxic tomammalian tissue and the environment. The anti-microbialactivity of the current ECA technology has been confirmedin this study. Electrochemically activated water (ECA) isless toxic, less volatile, easier to handle, compatible with otherwater treatment chemicals, effective against biofilms and gen-erates no by-products compared to currently used biocides.

During anode electrochemical treatment, water acidity in-creases. ORP increases due to the formation of stable and un-stable acids (sulfuric, hydrochloric, hypochlorous, persulfu-ric), as well as hydrogen peroxide, peroxo-sulfates, peroxo-carbonates, oxygen-containing chlorine compounds and dif-ferent intermediate compounds arising in the process of spon-taneous decomposition and interaction of the indicated sub-stances. Also, as a result of anode electrochemical treatmentsurface tension somewhat decreases, electric conductivityrises, as does the content of dissolved chlorine and oxygen,concentration of hydrogen and nitrogen decreases, and waterstructure changes.

The bacterial cell membrane provides the osmotic barrierfor the cell and catalyses the active transport of substancesinto that cell. Alternations in transmembrane potential causedby the action of electron donor or electron acceptor factors areassociated with powerful electro-osmotic processes accompa-nied by water diffusion against ORP gradients, with resultantrupture of the membranes and outflow of the bacterial cellcontents.

The bacterial membrane itself has an electrical charge. Theanions present in Anolyte act on this membrane. Anolyte canalso disrupt other functions of the cell. Unlike “higher” organ-isms, single celled organisms such as bacteria obtain their en-ergy sources form the environment immediately outside thecell. Small molecules are transported across the cell mem-brane via an electro-chemical gradient.

Thus, any significant change in the ORP of the immediateenvironment has drastic consequences for the cell. Even if in-stantaneous death of the cell does not occur, all enzymaticfunctions in the membrane are affected and this will also resultin loss of cell viability [16].

3.2 Bacterial resistance to biocides

Resistance has been defined as the temporary or permanentability of an organism and its progeny to remain viable and / ormultiply under conditions that would destroy or inhibit othermembers of the strain. Bacteria may be defined as resistantwhen they are not susceptible to a concentration of antibac-terial agent used in practice. Traditionally, resistance refers toinstances where the basis of increased tolerance is a geneticchange, and where the biochemical basis is known. Whereasthe basis of bacterial resistance to antibiotics is well known,that of resistance to antiseptics, disinfectants and food preser-vatives is less well understood.

Antimicrobial substances target a range of cellular loci,from the cytoplasmic membrane to respiratory functions, en-zymes and the genetic material [14]. However, differentbacteria react differently to bactercides, either due to inherentdifferences such as unique cell envelope composition andnon-susceptible proteins, or to the development of resistance,either by adaptation or by genetic exchange. At low con-centrations bactericides often act bacteriostatically, and areonly bacteriocidal at higher concentrations. For bactericidesto be effective, they must attain a sufficiently high concen-tration at the target site in order to exert their antibacterialaction.

Possible explanations for the increased resistance of bio-film bacteria include:

l limited diffusion of antimicrobial agents through the bio-film matrix, [17, 18].

l interaction of the antimicrobial agents with the biofilm ma-trix (cells and polymer) [19–36, 29, 37–38, 26]

l enzyme mediated resistance [39, 40],l level of metabolic activity within the biofilm [28, 41–44]l genetic adaptation [45, 46]l efflux pumps and [47–51],l outer membrane structure [52, 53].

3.3 Monitoring biocide concentrations

The efficacy of bactericide programmes for biofouling con-trol in industrial water systems relies not only on the spectrumof antibacterial activity of the bactericide, but also on theavailable concentration. In many cases the correct availableconcentration is not attained due to a lack of knowledge onthe size of the system or the difficulty to determine the resi-dual concentration of the bactericide. In recirculating watersystems, bactericide concentrations decrease after additiondue to system blow-down and interaction with bacteria. Nor-mal practice would be add bactericide periodically to maintainthe required concentration. In the case of most bactericides, asmall decrease in concentration will result in a large decreasein activity. For bactericide programmes to be effective onewould be to add bactericide periodically to maintain the re-quired concentration [14].

Due to the difficulty in determining available in situ bac-tericide concentration, rates of depletion due to inactivationare unknown and this has led to the mismanagement and fail-ure of many biofouling control programmes. The concentra-tions of non-oxidising bactericides can be determined by con-ventional analytical means.

Most of these involve extraction followed by instrumentalanalysis. These techniques are sophisticated and cumbersome,and too lengthy and expensive for routine use [54]. Rapid con-venient tests are available for some oxidising bactericides, e.g.

522 Cloete Materials and Corrosion 54, 520–526 (2003)

Merckoquant peroxide for hydrogen peroxide and Mercko-quant chlorine for chlorine determinations (Merck,PTY.LTD).

A more serious problem is the lack of suitable techniquesfor the in situ determination of available bactericide concen-trations. In this regard one bioindicator has been developed[54]. Bioindicators are considered to be biological prepara-tions that usually contain spores of a single bacterial strainwith a known susceptibility towards an antimicrobial agent.Sterikon is used as a bioindicator in heat sterilisation. It isa glass vial containing spores of the apathogenic Bacillusstearothermophilus ATCC 7953 suspended in a broth contain-ing glucose and a pH indicator. After heat exposure the vial isincubated at 45 8C and viable spores, produce acid and renderthe indicator yellow. Ayellow vial is indicative of insufficientheat treatment. Sterikon has been evaluated for the determi-nation of bactericide concentrations. A range of concentra-tions of each bactericide was added directly to the ampoules.These were then sealed and incubated at 45 8C for 24 h. Alldeterminations were performed in triplicate. A clear violetcolour after 24 h was taken as sufficient bactericide to inhibitspore germination, or alternatively, to kill the spores. Yellowampoules were an indication of acid production due to germi-nation and growth, indicating insufficient bactericide. The re-sults indicate that the Sterikon bioindicator can be used suc-cessfully for the determination of the concentration of bacter-icides in water samples. Since B. stearothermophilus sporesgerminate only at a temperature above 45 8C, the Sterikon am-poule must be incubated at this temperature. The bacterialflora of the water samples tested will, therefore, not interferewith the determination, as these bacteria are mostly mesophi-lic. They cannot grow at 45 8C, or only at a very slow rate, andwill not cause a colour-change to indicate an incorrect bacter-icide concentration. Water samples can, therefore, be used di-rectly and do not have to be filter-sterilised as would be thecase if the indicator organism itself were a mesophile [54].

3.4 Dispersants for controlling biofouling

More recently surface-active compounds (surfactants) havebeen employed to prevent bacterial adhesion to surfaces. Cur-rently there is no evidence that surfactants will have any mu-tagenic effects on bacteria, or that micro-organisms could be-come resistant to the action of surfactants, as in the case ofbiocides [55, 56]. Unfortunately little published informationis available on the effectivity of different biodispersants (sur-factants) against bacterial attachment [57]. According to Pauland Jeffrey [58], dilute surfactants completely inhibited theattachment of estuarine and marine bacteria. Surfactants resultin uniform wetting of the surface to be treated and have anadditional cleaning effect [57, 59]. Whitekettle [60] found acorrelation between the ability of a surface-active compoundto lower surface tension and its ability to prevent microbialadhesion.White and Russel [61] classified surfactants accord-ing to the ionic nature of the hydrophilic group viz. anionic,cationic, non-ionic and zwitterionic.

Five non-ionic and three anionic surfactants were evaluatedusing 4’6-diamidino-2-phenylidole (DAPI) staining, scanningelectron microscopy (SEM) and spectrophotometry for theirefficacy in preventing adhesion and removing Ps. aeruginosaattached to 3CR12 stainless steel coupons and glass [62]. Allthe surfactants tested gave more than 90% inhibition of adhe-sion to the surfaces tested with no significant difference be-tween the effectivity of the different anionic surfactants

(p > 0.18) nor between the effectivity of the non-ionic surfac-tants (p > 0.16). The non-ionic and anionic surfactants re-sulted in more than 80% and 63% removal of attached Ps.aeruginosa cells, respectively. The non-ionic surfactantswere significantly more effective in removing attached bac-teria, than the anionic surfactants (p < 0.001). The preventionof attachment of Ps. aeruginosa cells to a glass surface, usingthe surfactants, was also monitored spectrophotometrically.There was no significant difference (p ¼ 0.437) when com-paring the DAPI-staining technique with spectrophotometricevaluations [62].

4 Biofouling monitoring

The most effective way to alleviate biofouling related pro-blems in water systems is to control the accumulation and ac-tivity of the microorganisms responsible for the formation ofbiofilms. To monitor this, reliable methods are needed to de-tect and quantify biofouling. Culturing techniques are conven-tionally used to enumerate biofouling related microorganisms.There are several limitations in these techniques, not only withrespect to the methodology but also in the interpretation of theresults and especially in the quantification of sessile bacteria.Hence, a range of monitoring techniques and devices havebeen developed.

Some examples of monitoring devices include [63]:l Fiber optical devices (FOS) consisting of optical fibers, in-

tegrated into the walls of pipes, using the intensity of back-scattered light for assessing the thickness of the deposit [64]

l Differential turbidity measurement devices (DTM), con-sisting of two turbidity measurement devices, one ofthem being continously cleaned. The difference betweenthe cleaned and non-cleaned device is caused by the deposit[65]

l Quartz crystal microbalance devices (QMB), exploiting thedecrease of vibration caused by material deposited on thecrystal surface [66–68]

l Surface acoustic waves (SAW), determining the differenceof the speed of surface waves on surfaces with and withoutdeposits [69]

l Friction resistance measurement, exploiting the pressuredrop which is caused by increasing thickness and roughnessof a given deposit [70]

l Heat transfer exchange resistance devices, based on the de-crease of the heat transfer rate by fouling layers [71]

l Electrochemical measurement devices which are based onthe change in electric conductivity of a surface caused by adeposit or on cathodic depolarization which is indirectlyattributed to microorganisms [66]

l FTIR-spectroscopy specific for amid bands. This approachis suitable for systems which usually do not contain biolo-gical molecules, e.g., cooling or process water systems

l Use of auto-fluorescence of amino acids such as trypto-phane or other biomolecules [64, 66, 72, 73]

l Microscopical observation of biofilm formation in a bypassflow chamber and morphological identification of microor-ganisms [66].The monitoring of biofouling is continuously evolving with

new and better techniques being developed all the time. Themajor drawback of the currently used techniques is that thesemethods are complicated and time-consuming, involving cul-turing and counting of attached organisms. Many techniquesthat have proven useful for elucidating some of the fundamen-tal electrochemical properties of MIC under laboratory con-

Materials and Corrosion 54, 520–526 (2003) Biofouling control in industrial water systems 523

ditions are neither practical nor successful under field condi-tions. Measurements of specific and/or generic microorgan-isms and their unique metabolic products represent indirectevidence for MIC but their presence alone does not necessa-rily substantiate MIC.

4.1 Molecular techniques

To understand biocorrosion, it is important to integrate che-mical and physical phenomena with microbial physiology. In-vestigation of microbial parameters, such as the identity of themicroorganisms and their spatial distribution, e.g. by fluores-cently labelled 16S rRNA probes, is in this context a key fac-tor [74].

However, data on the microbial activity and the chemicalsituation within the biofilm (investigated via micro-electro-des) have more relevance towards the corrosion problemthan knowing which bacteria are present. Together withthis, electrochemical phenomena on the metal surface haveto be quantified and interrelated to have a global view onthe complex situation [9].

4.2 Alternative biofouling control strategies

A number of alternative control strategies have been devel-oped including coatings, enzymes, ice-nucleation and piggingetc. [14]. During the last few years two new and novel tech-niques have been reported. These will now be discussedbriefly.

4.2.1 Corrosion inhibition by microorganisms

It was reported that in some cases, microorganisms and bio-films may decrease the corrosion rate of stainless steel or evenprotect them from corrosion. However, this microbial inhibi-tory action has only been demonstrated on labscale basis withmore or less axenic biofilms. These inhibiting actions arebased on different processes: (i) passive sulphide film forma-tion by SRB, [75], (ii) presence of an uniform layer of livingbacteria (related to decreasing oxygen concentrations) [76] or(iii) formation of a diffusion barrier e.g. of corrosion products,due to presence of exopolymers [6], iv) oxygen depletion atthe surface [76], v) antibiosis [87], vi) coating of surfaces withan immunoglobulin film [88] and vi) predation. There arehowever some reports that mention the protective action ofmicroorganisms and biofilms towards stainless steel corrosion[77, 78]. Because the microbiological component of corrosionis seldom identified as a single organism or a unique mechan-ism, special investigation has to be conducted to elucidate theinfluence of consortia of bacteria on the corrosion processes.However, in order to have a representative situation, naturalwaters with their naturally occurring consortia should be usedinstead of synthetic media with artificially composed groupsof co-operative microorganisms. Moreover, certain nutritionalsupplements present in yeast extract or Trypticase soy (aminesand nitrates), and minerals such as phosphates commonly in-troduced into microbiological media are chemical corrosioninhibitors that can skew results.

4.2.2 Antimicrobial releasing metals

The possible use of bactericide releasing materials, andmore particularly bactericidal stainless steels have been re-ported [79–86]. In fact, there are several possibilities of al-loying elements with possible bactericidal effects: mercury,silver and copper are well-known examples.

There are however several concerns regarding the efficacyof the latter technology. Firstly, bacterial resistance build upagainst silver and the other metals may limit the efficacy ofthese bactericide releasing materials. Results also indicatedthat colonisation could only be delayed, but ultimately notprevented. This may, nevertheless, be of some value makingintermittent biocide dosage more effective. A further limitingfactor may be the cost of such biocide releasing materials, aswell as the rate of leaching of the oligodynamic metals result-ing in protection against MIC for only a limited period of time.

5 Conclusions

l The cost of biofouling has not been enumerated. A prere-quisite for this is research to elucidate the contribution thatmicrobiologically influenced corrosion makes, to the over-all corrosion process.

l Surface characteristics play a major role in the initial stagesof microbial attachment. Ways of preventing preferentialattachment to certain areas, i.e. grain boundaries and weldsneed further investigation.

l Biocides are routinely used to control biofouling. Due to theproblem of resistance and potential environmental impact,alternative strategies for biofouling control need to be in-vestigated and put to practice. These should focus on anintegrated approach with the minimum impact on the envir-onment.

l A number of biofouling monitoring devices have been de-veloped. The advantages of biofouling monitoring needs tobe demonstrated and monitors should become commer-cially available.

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