Pipe Scales and Biofilms in Drinking-Water Distribution Systems: Undermining Finished Water Quality

This article was downloaded by: [Moskow State Univ Bibliote]On: 13 January 2014, At: 06:28Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Critical Reviews in Environmental Science andTechnologyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/best20

PIPE SCALES AND BIOFILMS IN DRINKING-WATERDISTRIBUTION SYSTEMS: UNDERMINING FINISHED WATERQUALITYKonstantinos C. Makris a , Syam S. Andra a & George Botsaris ba Water and Health Laboratory, Cyprus International Institute for Environmental andPublic Health in association with Harvard School of Public Health , Cyprus University ofTechnology , Limassol , Cyprusb Department of Agricultural Sciences, Biotechnology and Food Science , Cyprus Universityof Technology , Limassol , CyprusAccepted author version posted online: 06 Sep 2013.Published online: 06 Sep 2013.

To cite this article: Critical Reviews in Environmental Science and Technology (2013): PIPE SCALES AND BIOFILMS IN DRINKING-WATER DISTRIBUTION SYSTEMS: UNDERMINING FINISHED WATER QUALITY, Critical Reviews in Environmental Science andTechnology, DOI: 10.1080/10643389.2013.790746

To link to this article: http://dx.doi.org/10.1080/10643389.2013.790746

Disclaimer: This is a version of an unedited manuscript that has been accepted for publication. As a serviceto authors and researchers we are providing this version of the accepted manuscript (AM). Copyediting,typesetting, and review of the resulting proof will be undertaken on this manuscript before final publication ofthe Version of Record (VoR). During production and pre-press, errors may be discovered which could affect thecontent, and all legal disclaimers that apply to the journal relate to this version also.

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

http://www.tandfonline.com/loi/best20

http://www.tandfonline.com/action/showCitFormats?doi=10.1080/10643389.2013.790746

http://dx.doi.org/10.1080/10643389.2013.790746

http://www.tandfonline.com/page/terms-and-conditions

http://www.tandfonline.com/page/terms-and-conditions

ACCEPTED MANUSCRIPT

ACCEPTED MANUSCRIPT 1

PIPE SCALES AND BIOFILMS IN DRINKING-WATER DISTRIBUTION SYSTEMS:

UNDERMINING FINISHED WATER QUALITY

Konstantinos C. Makris a*

, Syam S. Andra a and George Botsaris

b

a Water and Health Laboratory, Cyprus International Institute for Environmental and Public

Health in association with Harvard School of Public Health, Cyprus University of Technology,

Limassol, Cyprus.

b Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of

Technology, Limassol, Cyprus.

CORRESPONDING AUTHOR EMAIL ADDRESS ( [email protected] )

ACKNOWLEDGEMENT. We would like to acknowledge PIRG05-GA-2009-249271, EU FP7

Marie Curie RG grant to KCM.

SUPPORTING INFORMATION. No supporting information.

COMPETING INTERESTS: None.

* Corresponding author. Assistant Professor of Environmental Health, Cyprus International

Institute for Environmental and Public Health in association with Harvard School of Public

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

mailto:[email protected]

ACCEPTED MANUSCRIPT


Health, Cyprus University of Technology. Irenes 95, Limassol 3041, Cyprus. Telephone: +357-

25002398. Fax: +357-25002676.

ABSTRACT

Safety and security are two important features of urban drinking-water distribution systems

(UDWDS), worldwide, that are often compromised by a suite of physical, hydraulic and

chemical factors adversely impacting quality of potable water reaching consumer taps. Growth of

scales and biofilm conglomerates (SBC) coupled to sorption of water chemicals and planktonic

microorganisms by SBC have been increasingly recognized as underestimated contaminant

sources in aging pipe networks of UDWDS. The main objective of this study was to provide an

updated review of factors and processes associated with the increasing frequency of deteriorated

finished water quality incidences as a result of SBC effects in UDWDS. This critical review

integrated scattered knowledge on the effects of either pipe scales or pipe-anchored biofilm

systems on contaminant destabilization and subsequent release into water. It was emphasized that

little information exists on combined or concomitantly studied effects of SBC on finished water

quality. Important synergistic SBC effects on finished water quality were identified as: i) those

promoting chemical release from pipe scales due to biofilm-induced alterations at the pipe

surface/water interface, ii) the synergistic SBC action on promoting increased release rates of

pathogens or toxic chemicals into water, and iii) the microbially-enhanced corrosive phenomena

on pipe scales and their constituents. Substantial room for improvement is anticipated for the

water and global health research agenda by formulating innovative hypotheses and research

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


designs that water authorities could benefit from as they strive towards further securing access to

safe water in urban settings.

KEYWORDS. Pipe Scales, Biofilms, Drinking water, Exposure, Environmental Health,

Urbanization.

1. Characteristics of Urban Drinking-Water Distribution Systems-UDWDS

Unsafe water, sanitation and hygiene is one of the top#4 leading global risks for the burden of

disease measured in disability-adjusted life years (DALYs) (4% of global DALYs), along with

alcohol use and unsafe sex (5% each), and underweight (6%) (WHO, 2009). Globally, unsafe

water sanitation and hygiene is by far the leading environmental risk for morbidity when

compared with other environmental factors such as, urban outdoor air pollution, indoor smoke

from solid fuels, environmental lead exposure, and global climate change (WHO, 2009). The

impact of global stressors on water supply and demand, such as, increasing number of mega

cities (population > 10 million) around the globe coupled with the booming urbanization rates

observed primarily in developing countries (Zimmerman et al., 2008), puts enormous pressure on

the industry and regulatory agencies to secure safe access to clean water for urban dwellers.

Despite improvements in sanitation and hygiene via access to centralized water treatment

facilities and advances in water treatment technologies, i.e., reverse osmosis, it is widely

accepted that human exposures to water-borne pathogens and episodic events of chemicals

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


release in finished water of urban drinking-water distribution systems (UDWDS) are of

considerable magnitude (NRC, 2006; Edwards et al., 2009). Since 1982, the number of

waterborne outbreaks in community water systems has been steadily declining in the U.S., while

the % contribution of UDWDS to the overall frequency of waterborne outbreaks is steadily

increasing to > 60% (NRC, 2006). The number of annual waterborne outbreaks may be actually

exceeding current estimates, based on the U.S. Government Accountability Office report

highlighting the alarming number of health-related breaches in drinking-water going unreported

(U.S. GAO, 2011). The UDWDS have been charged with increasing incidents of waterborne

illnesses and outbreaks (Liang et al., 2006), revisiting the notion that pathogens and chemicals

behave conservatively between the point of entry (after conventional or reverse osmosis-

desalination water treatment) and the point of use (Jorgensen et al., 2008). The drinking water

directive (98/83/EC) is currently under scrutiny by EU scientific experts and stakeholders on

whether extensive revision is necessary (Jorgensen et al., 2008).

Points of water use (home taps, bottled water, etc.) and points within UDWDS (nearly equally

in magnitude) represent the two most frequently occurring deficiencies associated with

waterborne disease and outbreaks (Liang et al., 2006; Yoder et al., 2008). Growth of pipe scales

and biofilm conglomerates (SBC) coupled to sorption of water chemicals and planktonic

microorganisms by SBC have been increasingly recognized as underestimated contaminant

sources in UDWDS (Lytle et al., 2004). The predominant etiologic agents of waterborne disease

and outbreaks in the USA have been consistently linked to human exposures of chemicals/toxins

(27%) and pathogens (27%), followed by other bacteria (17%), and unidentified agents (17%)

(Liang et al., 2006). In all countries with urban areas, UDWDS are typically characterized by

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


extensive pipe networks of old age, extending from the water service main that brings drinking-

water from the treatment plant to the urban area and right outside a property (building, school,

household). The portion of the UDWDS extending from the water meter to the home tap, i.e., the

premise plumbing system will not be extensively addressed here, because of its unique

properties, peculiarities and legal constraints, even though the health risks associated with

premise plumbing are too important to ignore. The drinking-water distribution pipes, including

brass/bronze fittings, soldered joints and faucets are made out of various materials, such as, cast

iron, galvanized iron, asbestos/cement, lead, copper, and more recently high or low density

polyethylene (HDPE, LDPE) and polyvinyl chloride (PVC).

The prohibiting cost of replacing the majority of existing aged UDWDS network calls for

intervention measures that encompass pipe durability, longevity and functionality. It is warranted

that aging of UDWDS in combination with enhanced vulnerability at the physical, hydraulic and

water quality level imposes severe economic and health adverse consequences. Economic burden

of aged UDWDS in the USA has been primarily calculated on the basis of corrosive effects at a

rate of US$36 billion year-1

, out of which a total of 22 billions is direct costs for UDWDS and the

rest for sewage distribution systems (Brongers et al., 2002). Build-up of corrosion products and

SBC could result in pipe fouling that diminishes pipe effective diameter, exacerbating energy

requirements for maintaining adequate water flow (Uhlig and Revie, 1985). Epidemiologic data

on the burden of disease associated with the presence of pathogens/chemicals in UDWDS raised

the additional total social cost to tenths of US$ billions year-1

(Hudson et al., 1976; Edwards,

2004). Similarly, 3-4% of GDP goes into corrosion costs in certain countries, such as, Australia,

UK, and Japan (Uhlig and Revie, 1985). Anticipated upgrade in the existing corroded public

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


UDWDS in the USA was valued at 77-325 US$ billions (WIN, 2000). At the smaller community

level (<2000 people), corrosion-related cost in small drinking-water distribution systems was

about 10-20 times greater than that documented for urban UDWDS (Ryder, 1980; Edwards,

2004).

The main objective of this study was to provide an updated review of environmental factors

and processes intrinsically linked to the increasing frequency of deteriorated finished water

quality incidences in UDWDS (Figure 1). The various types of historically formed pipe scales

and biofilms in UDWDS; the environmental conditions that enable pipe and scale conglomerates

to act either as sinks or sources for water contaminants; the elucidation of factors and processes

that induce the episodic release of chemicals and/or microorganisms into finished water (pipe to

tap); the nature and type of released chemical and biological products in finished water; the

stability and transport of released products into finished water; the magnitude and variability of

human exposures to free and particulate water contaminants present in finished water reaching

households; the bioaccessibility of such particulate contaminants in the human gastrointestinal

phase; and the combined acute or chronic health effects on disease process are all topics that are

currently poorly understood. Factors affecting the physical and hydraulic integrity of UDWDS

(NRC, 2006) were not the focus of this review. This critical review integrates scattered

knowledge on deterioration of UDWDS finished water quality due to effects of either pipe scales

or pipe-anchored biofilm communities; little, if any, information exists on combined effects of

SBC on finished water quality (Figure 1). To the best of our knowledge, this is the first critical

review that attempts to improve our understanding of chemical/microorganism release from SBC

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


into finished water by synthesizing knowledge on both chemical-, and microbiologic-based

parameters.

2. Scales and Biofilms Characteristics in Pipes within UDWDS

2.1. Pipe Scales:

The presence of scales, corrosion products, and associated contaminants in pipes of UDWDS

and their release into finished water has gained a heightened scientific and societal interest in

recent years (Renner, 2008). Scales formed in pipes mostly consists of tubercles formed via

precipitation and re-precipitation mechanisms of pipe-originating nucleating elements, such as,

aluminum (Al), copper (Cu), iron (Fe), and lead (Pb) (Table 1). The main sources of dissolved

and particulate forms of contaminants in finished water being available to nucleate scale

formation or enrich existing pipe scales in UDWDS are the following: i) incomplete (µm-

sized)particle removal by conventional drinking-water treatments, and ii) dissolved Fe2+

and

Mn2+

ions entering UDWDS (intermittent water supply, negative pressure - intrusion, pipe

leakage, etc.), which are subject to co-precipitation, oxidation and other processes that lead to

nucleation and gradual crystallization of metal oxyhydroxide particles, i.e., the pipe scale

precursors. Such natural particles may either remain suspended in finished water or adhere to

pipe scales.

Alkaline or calcareous scales are the most commonly observed types of pipe scales composed

of minerals, such as, calcium carbonate, goethite, magnetite, green rust and amorphous Fe phases

(Edwards, 2004; Hodgkiess, 2004). Iron scales are typically composed of oxides - magnetite

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


[Fe3O4] (Fleet, 1981), hematite [Fe2O3]; hydroxides - ferrous [Fe(OH)2] and ferric [Fe(OH)3];

oxyhydroxides - goethite [α-FeOOH] (Verdonck et al., 1982), akaganeite [β- FeOOH] (Stahl et

al., 2003), lepidocrocite [γ-FeOOH] (Ewing, 1935), carbonates - siderite [FeCO3] (Graf, 1961),

chukanovite [Fe2(CO3)(OH)2] (Pekov et al., 2007), and green rust containing either carbonate

[(Fe6(OH)12(CO3)(H2O)3] (Aissa et al., 2006) or chloride [(Fe6(OH)10Cl(H2O)3] (Allmann et al.,

1969) or sulfate [(Fe6(OH)12(SO4)(H2O)8] (Simon et al., 2003). Aluminum scales, such as,

aluminum-silicate, and aluminum-phosphate scales (Kvech and Edwards, 2001, 2002) are similar

to Fe scales, except that they are less frequently encountered due to their lower nucleation rates

(Snoeyink et al., 2003). Corrosion-induced asbestos scales formed in asbestos-cement pipes

could concomitantly release both calcium and asbestos fibers in finished water (Axten et al.,

2008). Lead scales are typically composed of Pb(II)-, and Pb(IV)-containing oxides, litharge

[PbO], dioxide [PbO2]; hydroxides, hydrocerussite [Pb3(CO3)2(OH)2]; carbonates, cerrusite

[PbCO3] (Schock, 1980, 1999; Schock and Gardels, 1983; Davidson et al., 2004), and chloride -

vanadinite [Pb5(VO4)3Cl] (Gerke et al., 2009).

2.2. Biofilms in Pipes:

Internal pipe surfaces (associated or not with pipe scales) support growth and establishment of

microbial colonies (Lehtola et al., 2004; Simoes et al., 2007). The structures formed by

microorganisms via adhesion, nucleation, and growth on surfaces are called biofilms. Biofilms

are defined as matrix-enclosed bacterial populations adhering to each other and/or to surfaces or

interfaces (Costerton et al., 1995). This definition includes microbial aggregates and floccules

and also adherent populations within the pore spaces of porous media (Costerton et al., 1995). A

biofilm colony may be a highly heterogeneous in nature community where cell aggregates are

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


formed with the aid of the exopolymeric substances (EPS) matrix. Exopolymeric substances

represent the major constituent of the dry matter in biofilms, serving as the precursor of bacteria

attachment to pipe surfaces (Sutherland, 2001). An extensive pore network within biofilms

allows for ample circulation of nutrients, and the establishment of pH and redox potential

microsites (Davey and O’Toole, 2000; Donlan and Costerton, 2002; Beveridge et al., 1997).

A biofilm community often consists of a mixture of bacterial species, as well as, fungi and

protozoa (Costerton, 1999) (Table 1). Biofilms in potable water systems are patchy and

heterogeneous with a diverse microbial flora (Costerton, 1999; Percival et al., 2000). Not only do

pathogenic and nonpathogenic bacterial families grow as a biofilm, but they also host other

microbes such as protozoa and viruses (Percival et al., 2000; Flemming et al., 2002). Viruses and

parasitic protozoa are obligate parasites that depend upon multiplication in animal or human

hosts. Such organisms can only be expected to attach and persist in biofilms without being able

to proliferate. Typical examples of microorganisms in biofilms found in UDWDS are (in

alphabetic order): Acinetobacter calcoaceticus; Aeromonas hydrophila; Citrobacter spp.;

Enterobacter spp.; Flavobacterium spp.; Klebsiella pneumonia; Legionella pneumophila;

Moraxella spp.; Mycobacterium avium complex; Burkholderia cenocepecia; Pseudomonas

aeruginosa; Serratia marcescens (Geldreich, 1996; LeChevallier et al., 1987; Norton and

LeChevallier, 2000).

Biofilm growth and establishment on pipe internal surfaces of UDWDS may reach a plateau

within months or more. The total number of cells may range from 104 to 10

8 cells cm

-2, while the

numbers of culturable heterotrophic plate count (HPC) bacteria in established biofilms can vary

between 101 to 10

6 colony-forming units cm

-2 (Wingender and Flemming, 2004). Previous

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


studies on microbial communities in UDWDS have also showed that a major group of

heterotrophic isolates from biofilms consisted of a-, b- and g-Proteobacteria (Tokajian et al.,

2005), and also reported the presence of pathogens in UDWDS, such as Legionella,

Cryptosporidium, Helicobacter, Aeromonas and Mycobacterium spp. (Berry et al., 2006). It is

widely accepted that most of the microbial biomass in UDWDS is located within biofilms

(Laurent et al., 1993; Zacheus et al., 2001). In fact, ~95% of bacterial counts in UDWDS were

located in pipe surfaces, while only 5% were found in the water phase and detected by routine

sampling schemes (Flemming et al., 2002).

Biofilms could also provide shelter for pathogenic bacteria, protecting them from disinfectants.

The type and dose of disinfectant could largely influence the structure of a biofilm community;

bacterial cells tend to be clumped, smaller in size, showing a patchy morphology for chlorinated

systems when compared with non-chlorinated pipe biofilm community; as an example, a shift

from longer rod-shaped cells to rounded ones may appear along with a change in the dominant

bacteria types present in the biofilm community in contact with chlorinated water (Percival et al.,

2000). The improved understanding of the nature and types of microorganisms comprising

biofilm colonies on different pipe surfaces are deemed necessary to evaluate the magnitude and

uncertainty associated with human exposures to pathogens via the oral ingestion of contaminated

tap water.

3. Factors Influencing Pipe Scale Formation

Electrochemical surface corrosive phenomena coupled to dissolution and/or precipitation

reactions of metal salts have been primarily charged with induction of pipe scales, pits, tubercles,

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


and nodules formation, often leading to water discoloration (McNeill and Edwards, 2001). In the

past, water utilities had relied upon the Langelier Index (LI) to predict onset of corrosive events

in UDWDS associated with leaching of lead, zinc, and copper from brass, bronze, soldered joints

and their respective pipe materials, but this approach was shown to be largely misused, and it

was eventually abandoned (AWWA, 1996; Schock and Lytle, 2010).

Depending on the pipe material, various pipe scales have been observed to form in UDWDS.

In non-chlorinated water flowing through cast iron pipes, α-FeOOH and calcium carbonate were

the primary minerals that comprised pipe scales, while α-FeOOH and magnetite were observed as

pipe scale constituents in chlorinated water (Wang et al., 2012a). Pipe scales from cast iron pipes

in contact with chloraminated water were shown to be composed of calcium phosphate and α-

FeOOH (Wang et al., 2012a). The source of treated water flowing through old unlined cast iron

pipes exerted a major influence on the composition of formed pipe scales, since thick tubercles

with >1 magnetite:goethite ratio were formed that contained siderite and green rust when treated

surface water was flowing through the pipes, whereas in the case of ground water, thin hollow

tubercle shells with <1 magnetite:goethite ratio were formed (β-FeOOH, γ-FeOOH) (Yang et al.,

2012). In addition to goethite, lepidocrocite and magnetite, three different type of green rust were

found in pipe scales formed on cast iron pipes, including the least stable chloride form of green

rust despite the notion that green rusts were not be present in drinking water pipe scales (Swietlik

et al., 2012). Porous deposits of iron oxide or oxyhydroxide phases, including magnetite, goethite

and lepidocrocite formed a shell like dense layer at the scale-water interface, while a highly

porous phase was observed near the pipe surface of galvanized steel or cast iron (Sarin et al.,

2001; Lytle et al., 2005). In lead pipes, mixed charge lead scales have been observed, such as

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


hydrocerrussite and cerrussite or hydroxypyromorphite in phosphate-rich waters (Xie and

Giammar, 2011). Aluminosilicate scales formed on lead pipes at water pH <6 or pH>9 did not

protect lead scales from not releasing lead into finished water (Kvech and Edwards, 2001).

Manganese scales were observed to form within iron tubercles of iron pipes, while a brittle thin

manganese oxide that was relatively easy to detach was found in PVC pipes (Cerrato et al.,

2006).

Water pH may exert a major influence on pH-dependent speciation of carbonic acid, thus,

affecting CaCO3 deposition and scale formation (Hodgkiess, 2004); a pH increase from 8.8 to

10.0 could increase CaCO3 deposition from 2 mg cm-2

to 12 mg cm-2

in 2 hours (Andritsos and

Karabelas, 1999). A combination of temperature and pH effects increased CaCO3 deposition by 5

times when pH increased from 7.0 to 8.0 at 70°C temperature (Dawson, 1990). Oxidation of pipe

metallic constituents could be facilitated by the presence of disinfectant agents, such as chlorine;

lead corrosion products consumed chlorine facilitating formation of a more stable PbO2 scale, but

its rate of oxidation by chlorine was diminished in the presence of high concentrations of

carbonate ions (Liu et al., 2009), or addition of orthophosphate to chlorinated water (Lytle et al.,

2009), or natural organic matter that was shown to inhibit formation of cerrussite in lead pipes,

forming amorphous films (Korshin et al., 2005). Phosphate addition as corrosion inhibitor has

been widely used in UDWDS, particularly for lead pipe network systems (McNeill and Edwards,

2002; Edwards and McNeill, 2002). Natural organic matter indirectly influences pipe scale

formation, because of its affinity to form soluble complexes with primary pipe scale constituents,

such as Fe and Al (Campbell and Turner, 1983). Lower molecular weight organic acids (fulvic

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


acids) could form soluble complexes with metals, like copper in finished water, minimizing the

formation of pipe scale precipitates.

4. Factors Influencing Biofilm Formation

Biofilm formation may be influenced by factors, such as, magnitude of residual concentration

of disinfectant agent, establishment of conditioning film, bioavailability of inorganic nutrients in

finished water, hydraulic conditions, pipe material type and surface properties, water flow

velocity, water pH, and water temperature (Norton and LeChevallier, 2000; Van der Kooij and

Veenendaal, 2001). Microbial growth rates are generally slower in a biofilm colony when

compared with those of planktonic cells. The biofilm environment though, can offer a protective

environment for anchored microbes against the action of disinfectants used (Van der Wende et

al., 1989). The biofilm environment is believed to protect cells against the activity of chlorine via

diffusional resistance and neutralization of chlorine when in contact with EPS constituents (e.g.,

alginate) and pipe material (Van der Wende et al., 1989).

A prerequisite of biofilm formation is the establishment of a conditioning film used by

planktonic bacteria to sorb onto pipe surfaces (Bakker et al., 2004). Conditioning films are

formed through the adsorption of proteins, lipids, nucleic acids and other natural surface active

agents onto pipe surfaces. Exopolymeric substances production is instrumental towards biofilm

stability and integrity (Vandevivere and Kirchman, 1993; Danese et al., 2000). In Pseudomonas

aeruginosa biofilms, production of EPS such as the capsule-like polysaccharide called alginate

could downregulate flagellum synthesis and therefore motility (Garrett et al., 1999), turning the

bacteria from a motile to a mucoid phenotype (Hentzer et al., 2001). This mucoid conversion is

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


indicative of the overproduction of alginate, which could either facilitate bacterial adherence to

pipe surfaces, or it could serve as a barrier to phagocytosis, or as a reactant to neutralize oxygen

radicals (Hentzer et al., 2001). A mucoid strain could develop a more structurally heterogeneous

biofilm than that produced by a comparable non-mucoid strain (Hentzer et al., 2001). Increases in

metal divalent cation concentrations (calcium) in biofilm growth medium significantly increased

biofilm production for Pseudomonas spp. (Turakhia and Characklis, 1989). It was speculated that

Ca2+

ions formed complexes with alginate, producing a gelly-type of external surface, offering

enhanced stability to biofilm structure (Chen and Stewart, 2002). Enhanced biofilm formation

could be observed in media with adequate nutrient composition either originating from finished

water’s soluble constituents, or from leaching of biodegradable compounds from synthetic

polymers used in plastic pipes, e.g., plasticizers, antioxidants, etc. (Keevil, 2002; Rogers et al.,

1994b). Iron pipe constituents could also provide essential nutrients in water for microbial

growth, including organic carbon, phosphorus and nitrogen (Morton et al., 2005). The adherence

of surface active biomolecules to pipe surfaces improved access of bacteria to nutrient media, but

also perturbed pipe surface properties, such as, hydrophobicity and roughness (Beveridge et al.,

1997; Bakker et al., 2004). Although certain authors reported that microorganisms attached to a

greater extent onto hydrophobic rather than onto hydrophilic surfaces (Flemming and Wingender,

2001; Donlan, 2002), it was suggested that the affinity to hydrophobic surfaces could be

additionally ascribed to the nature and surface properties of attached bacterial strains (Bakker et

al., 2004).

Microorganisms undergo vast changes during their transformation from planktonic cells to

adhered cells on pipe surfaces. In biofilm colonies, bacteria tend to adapt to environmental

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


changes via gene expression mechanisms (Costerton, 1999; Donlan and Costerton, 2002). In

Pseudomonas aeruginosa biofilms, patterns of genetic differentiation showed that 40 % of

proteins in cellular walls were different from those of planktonic cells (Potera, 1999); such

changes were reflected upon the new phenotypic characteristics developed by bacteria in biofilms

due to various environmental stimulating signals (O’Toole, 1998). Pseudomonas aeruginosa and

Pseudomonas fluorescens will easily form biofilms under nearly all environmental conditions

(O’Toole and Kolter, 1998), whereas, certain strains of Escherichia coli K-12 and Vibrio

cholerae will not form biofilms in minimal medium, unless supplemented with amino acids

(Pratt and Kolter, 1998; Watnick et al., 1999).

Cell hydrophobicity better explained surface adhesion to polystyrene surfaces than less

hydrophobic bacterial cells (Van Loosdrecht et al., 1987). Tendolkar et al (2004) investigated

Esp, a surface protein in Enterococcus faecalis which had been reported to regulate bacterium’s

surface adhesion potential. Esp positive strains were more hydrophobic and attached better to

polystyrene, polypropylene, and polyvinyl chloride surfaces than Esp negative strains, confirming

the positive relationship between cell hydrophobicity and pipe surface attachment potential. It has

been also demonstrated that both the presence of flagella per se and flagellar motility could

positively influence bacterial attachment to surfaces (Donlan, 2002; Klausen et al., 2003; Lemon

et al., 2007). Although fimbriae do not directly participate in biofilm formation, their presence

promotes the process of bacterial adhesion to surfaces (Inoue et al., 2003) probably by

overcoming the initial electrostatic repulsion barrier that exists between the cell and substratum

(Corpe, 1980).

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


The effect of various pipe material types on the growth of biofilms has been widely studied,

suggesting lower biofilm growth rates in plastic pipes. For example, plastic materials supported

the growth of biofilms, but the growth in plastic pipes was the same, if not lower than that in

iron, steel or asbestos/cement (Zacheus et al., 2000; Niquette et al., 2000). Biofilm growth in

UDWDS was significantly lower on polymeric materials (PE, PVC and Teflon) than that of iron

metallic pipes, such as, grey iron, cast iron, galvanized steel, cemented steel, cemented cast iron,

or asbestos/cement (Niquette et al., 2000; Kerr et al., 1999; Momba and Kaleni 2002). The

enhanced biofilm growth in metallic pipes versus those in plastics was partially attributed to the

formation of iron corrosion products that served as physical protective barrier of biofilm

communities against the effects of increased flow rates and residual disinfectant concentration.

Van der Kooij and Veenendaal (2001) and Clark et al. (1994) observed that biofilm formation

was enhanced in PE > PVC, while others concluded no significant difference in colonization

magnitude and rates between PE and PVC materials (Pedersen, 1990; Wingender and Flemming,

2004; Zacheus et al., 2000). Chan (2003) found that biofilm re-growth on pipes made of rough

surface materials such as cast iron, concrete-lined cast iron, and galvanized steel was greater than

that on smooth-surface polyvinyl chloride (PVC) pipe. Lehtola et al. (2004) used PLFA

(phospholipid fatty acid) analysis to show higher numbers of gram negative bacteria in biofilm

established on copper pipe than on PE pipes, but there was no significant difference in biofilm

formation between copper and PE pipes after 200 days of reaction.

Pipe material can also influence composition and biomass density of attached microbes

(Schwartz et al., 1998; Niquette et al., 2000; Zhou et al., 2009; Lehtola et al., 2005; Silhan et al.,

2006). Plastic materials, such as, polyethylene and polyvinylchloride rapidly colonized (within a

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


few days) in significantly higher densities than those observed for steel and copper (Schwartz et

al., 1998). Fewer bacteria have been shown to attach to copper pipes compared with stainless

steel pipe material (Zhou et al., 2009), and this perhaps could be attributed to the toxic effect that

soluble copper ions imparts upon several bacterial species. Lehtola et al (2004) reported that the

formation of biofilm was slower in copper pipes than in polyethylene (PE) pipes, and that copper

ions led to lower microbial numbers in water.

Intermittent water supply in water scarce areas characterized by low flow rates or stagnancy is

anticipated to result in lower microbial adhesion, thus, minimizing the potential of biofilm

cohesion and stabilization (Manuel et al., 2007; Lehtola et al., 2006). Van der Wende et al.

(1989) suggested that at increased flow rates (15 cm h-1

) when compared with lower flow rates

(4.5 cm h-1

), nutrient availability was greater, thereby, enhancing biofilm cell growth rates (0.006

h-1

). The observed increase in counts of planktonic cells in flow systems was not related to a

higher cell growth rate, but to higher cell detachment from adhered bacteria (Van der Wende et

al., 1989; Manuel et al., 2007). Nevertheless, at flow velocities as high as 3 m s-1

cell detachment

increased, thus, adversely impacting biofilm growth rates (Cloete et al., 2003).

The anticipated pH effect on bacterial attachment and biofilm formation seems to be organism

dependent. Certain microorganisms, such as Xylella fastidiosa appeared to be highly sensitive to

small pH changes, being able to produce cell aggregation, attach to surfaces and finally form

biofilm at pH 6.8, but not at < pH 6.2 (Wulff et al., 2008). Other typical UDWDS

microorganisms, Pseudomonas and Klebsiella were able to form biofilms under a wider range of

pH (3-10); however, biofilm thickness at pH3 was reduced to 70% of that at pH 8 (platinum wire

electrodes) (Stoodley et al., 1997).

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Depending on the microorganism, finished water temperature effects on biofilm dynamics are

expressed via the gene activation/deactivation mechanisms, encoding surface adhesion potential

(Lemon et al., 2007; Fitzpatrick et al., 2005). Adhesion of microbes to surfaces is dependent on

both physical and chemical properties, such as, pipe surface hydrophobicity and electrostatic

charge, including the type and nature of microorganisms (Donlan, 2002; Gallardo-Moreno et al.,

2002a; 2002b). The magnitude of surface adhesion force is usually based upon measurements of

Lifshitz-van de Waals and electrostatic acid-base forces (Gallardo-Moreno et al., 2002a; 2002b;

Smets et al., 1999).

5. Destabilization of Pipe Scales- Chemical Release

Environmental conditions inducing destabilization of pipe scales impacting on the stability of

sorbed chemicals/toxins are currently not well understood. Factors mostly studied that influenced

pipe scale destabilization are: chemical composition of the source water (pH, redox potential, ion

composition), nature and extent of water treatment, and pipe material types along with pipe

surface properties (Schock et al., 1996; 2005).

Pipe scale destabilization and subsequent release of scale constituents into finished water can

be visually observed for certain elements, such as, the blue water phenomenon due to high

copper concentrations in water (as much as 500-1000 mg L-1

) (Edwards et al., 2000).

Unpredictable and episodic release of arsenic (As) into finished water (up to 30 μg L-1

) from As-

containing pipe scales occurred in eight different USA-based utilities despite that dissolved As

concentrations in finished water were routinely < 10 μg L-1

(Lytle et al., 2004); arsenic

concentrations of pipe scales collected from half-sided pipe sections and hydrant lines ranged

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


between 10 to 13650 mg As kg-1

(Lytle et al., 2004). In the case of copper pipes, increased

temperature and lower pH enhanced copper release into finished water (Boulay and Edwards,

2001). Similarly, scales formed on Pb pipe surfaces either as the result of classical solution

precipitation or due to pipe surface corrosion phenomena are known to accumulate contaminants,

such as As, Cd, Cr, Hg in the range of 0-99 mg kg-1

; Ba, Bi, Ni, U in the range of 100-999 mg kg-

1; Cu, S, Sn, Zn, V in the range of 1000-9999 mg kg

-1; and Al, Fe, Mn, Pb in the range of >

10,000 mg kg-1

(Schock et al., 2008). Lead service lines (50-75% Pb release) predominantly

contributed to Pb levels in home taps when compared with premise plumbing containing lead

solders and brass (20-35% Pb release) and faucets (1-3% Pb release) (AwwaRF, 2008). Galvanic

corrosion issues could perhaps be elevated in areas with lead service lines, enhancing the

magnitude of Pb release events into finished water (Nguyen et al., 2010).

Release of organic compounds from pipe materials that are either plastic (UPVC, or

plasticized/chlorinated PVC) or have been relined with epoxy resins is widely documented,

despite the fact that little, if any mechanistic work has been conducted on the factors held

responsible for organics’ leaching from plastic pipes. Most famous high production volume

chemical, i.e., bisphenol A (BPA) has been known to leach from epoxy relined pipes into

finished water (ChemSec 2011), but it is anticipated that upon contact with chlorinated water,

BPA degradation to chlorinated BPA congeners would occur (Gallard et al., 2004). Aschengrau

et al. (2003) linked perchloroethylene-contaminated drinking water to the risk of breast cancer,

because of prolonged leaching of perchloroethylene from the vinyl lining of water distribution

pipes in Cape Code, MA, USA. Taste and odor complaints were associated with the leaching of

styrene from plastic pipes (Rigal and Danjou, 1999), while organotins’ leaching was observed

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


from PVC pipes (Impellitteri et al., 2007; Sadiki, 1998). Indeed, sensory organoleptic properties

of water flowing through plastic pipes are often impacted by leaching of organics like, 1,3,

butadiene and cyclohexadiene (gasoline-like odor), phenol (sweet-tarry odor) and cyclohexanone

(solvent-acetone) (Heim and Dietrich, 2007). Steel pipes with epoxy coating have shown scales

leaching benzene, toluene, ethylbenzene and xylene up to 300 mg L-1

in Calgary, Canada

(Satchwill, 1998). PVC-based pipe scales allowed for vinyl chloride migration into drinking

water up to 9 mg L-1

in Kansas, USA (Flournoy et al., 1999). Asbestos release was demonstrated

via measurements of asbestos fibers in Italian drinking waters being around 1.1 million per liter

for >10 microns fiber length category and around 2.8 million per liter for 5-10 microns fiber

length category (ISS, 1993). In a Canadian survey, about 25% population were exposed to greater

than 1 million fibers per liter for 0.5-0.8 microns fiber length category and a small population

exposed to greater than 100 million fibers per liter in the same category (Chatfield and Dillon,

1979).

Groundbreaking research has illustrated several cases of intermittent pulses of inorganic

chemicals (both dissolved and particulates) detected in finished water of UDWDS (Table 3)

(Lytle et al., 2004; Triantafyllidou et al., 2007), but because of their episodic and non-periodic

nature, such contaminant release events often go undetected. In the most eminent case of

childhood poisoning due to Pb leaching from Pb scales grown on Pb pipes in the Washington,

D.C. area, particulate Pb concentrations accounted for even 50% of total soluble Pb

concentrations (Edwards et al., 2004). However, particulate Pb is often missed by existing

sampling protocols, because they were primarily designed to capture the dissolved Pb fraction,

but not suspended Pb particulates, underestimating the total mass of Pb present in water

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


(Triantafyllidou et al., 2007). It is likely that mobilization of chemicals from pipe scales may take

the form of suspended colloidal or nano-sized Pb or As particles that elude from detection due to

analytical limitations or sampling artifacts caused by existing protocols (Triantafyllidou et al.,

2007). Chromium sorbed to particulate Fe oxyhydroxide particles was missed in potable water

sampling collection schemes for metals that underwent acidification, underestimating the total

mass of Cr initially present (Parks et al., 2004).

Chemical desorption may be dependent upon the bonding strength between sorbed ion and

scale surface, since loosely bound to scales chemicals could be reversibly dislodged back into

finished water via physical hydraulic forces. However, if sorbed chemicals were incorporated

into solid phase crystal lattice of the pipe scale through incorporation and/or co-precipitation,

then desorption may follow the patterns of an irreversible process (Schock et al., 2008).

Chlorination of a previously non-disinfected groundwater released large amounts of particulates

in the finished water containing Fe (> 300 mg Fe L-1

) and As (> 1 mg L-1

) (Reiber and Dostal,

2000). Release of Pb from pipe scales was influenced by natural organic matter (Lin and

Valentine, 2008), aqueous Mn2+

or Fe2+

concentrations (Lin and Valentine, 2008). Changes in

water disinfecting agent (chlorine to chloramine) affected lead and copper release into water from

corroded pipes (Edwards and Abhijeet, 2004; Boyd et al., 2008). Changes in redox potential due

to switch from chlorine to monochloramine (NH2Cl) coupled with lower oxidizing capacity of

dissolved Pb to stable mineral lead(IV) oxide was the main reason behind the documented

release of Pb, up to 4800 µg L-1

, exposing humans to unprecedented levels of Pb via oral

ingestion of contaminated water (Edwards et al., 2009; Edwards and Abhijeet, 2004). Lin and

Valentine (2008) discovered that monochloramine was actually responsible for the chemical

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


reduction of the stable mineral lead oxide to dissolved lead, while natural organic matter acted in

a similar chemical reducing fashion. Higher initial monochloramine levels, lower water pH,

higher total carbonate concentration enhanced the formation of dissolved lead via the NH2Cl

decomposition-induced Pb oxide chemical reduction under laboratory conditions (Lin and

Valentine, 2008). Stable Pb(IV) oxide formation was inhibited when orthophosphate was added

to chlorinated water, forming hydroxypyromorphite (Lytle et al., 2009). Changes in coagulant use

in drinking-water treatment protocols adversely influenced the quality of finished water in

Ontario, Canada, since use of alum as the coagulant resulted in lower pH values (from 8 to 7) and

subsequent release of Pb, As, Al, and other metals from Pb pipe scales (Huggins, 2008; Kim et

al., 2011); interestingly, particulate Pb was the predominant Pb fraction released from Pb pipe

scales (Kim et al., 2011).

Galvanic corrosion is a Pb release mechanism from corroded surfaces composed of lead solder

and copper joints, or Pb pipe at copper joints (Nguyen et al., 2010). Increases in the chloride to

sulfate concentration ratio in the finished water induced Pb release via the persistent galvanic

currents flowing between the two neighboring metals (Pb and Cu) (Edwards and Triantafyllidou,

2007; Nguyen et al., 2011). In cases, where Pb pipes were replaced by HDPE, or PVC, brass

fittings and connectors, other than galvanic corrosion factors were responsible for elevated Pb

release in finished water (Kimbrough, 2007).

6. Destabilization of Biofilms-Microbial Release

Much of our understanding of microbial behavior is based on knowledge related to planktonic

cells, but cell metabolism and physiology in a biofilm colony fundamentally differs from that of

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


planktonic types (Table 3). Patches of biofilms could detach under certain environmental

conditions, leading to locally high cell densities in the water phase (“clouds”). The organisms

may attach to surfaces as primary colonizers and actively establish biofilms alone or in

combination with other microorganisms. However, they can also become integrated in

preexisting biofilms as secondary colonizers. Biofilms in UDWDS may host pathogenic

microorganisms that either circumvent treatment, or enter deficient UDWDS; illustrating cases

are Campylobacter jejuni (Lehtola et al., 2006; Buswell et al., 1998), Helicobacter pylori (Giao

et al., 2008; Percival et al., 2009), Legionella pneumophila (Rogers et al., 1994b; WHO 2007),

Pseudomonas aeruginosa (Szewzyk et al., 2000), Mycobacterium avium (Lehtola et al., 2007),

Aeromonas hydrophila (Chauret et al., 2001; Bomo et al., 2004), and Salmonella typhimurium

(Armon et al., 1997; Burke, 2006). Upon sloughing, biofilm pathogens can be released into

water, posing health risks to consumers (Beuken et al., 2008).

Several factors are involved in biofilm destabilization and possible release of microorganisms

into finished water, such as, capacity of the bacteria to produce EPS, the structure of biofilm

colony, the strength of cell attachments, surface roughness, nature of pipe material/substratum,

density of the microbial population on the pipe surface, cavity formation and quorum sensing.

The maturity point of a biofilm community that relates to the onset of biomass detachment rate is

associated with the biomass production rate consistent with fundamental mass balance equations

(Peyton and Characklis, 1992). A substrate facing difficulties in providing primary energy for

biomass production will result in lower detachment rates for the same substrate conversion rate.

Busscher and van der Mei (1995) highlighted the importance of initial microbial adhesion to

biofilm detachment rate, suggesting that the design of new non-adhesive materials and coatings

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


should not be based on initial microbial adhesion, but rather on the ease with which the initially

adhering microorganisms are detached. Smoot and Pearson (1998) explained significant

differences in detachment rates between rubber and stainless steel on the basis of stronger

attachment to rubber, while the same study showed that cell detachment from rubber was

significantly affected by growth temperature, but not by growth pH.

Cell detachment may be also affected by surface roughness with rougher surfaces showing less

cell detachment. Pedersen (1990) in a study investigating different types of steel water pipes,

reports greater microbial density for the matt steel surface over that of electro-polished steel.

Under turbulent conditions (Reynolds number of 5000), larger clusters of biofilm were detached

from substrata into finished water, showing >90% of sessile legionellae mobilized (Storey et al.,

2004). The exopolymeric substances composition may be controlled by different processes, such

as active secretion, shedding of cell surface material, cell lyses, and nutrient sorption processes

from the surrounding water environment (Wingender et al., 1999). Dense biofilms demonstrated

lower detachment rate due to smaller probability of developing detachment forces; under low

detachment forces, biofilm became highly heterogeneous with numerous pores and

protuberances, whereas under relatively high forces a patchy biofilm developed (Kwok et al.,

1997).

Cavity formation, which occurs beyond the point of biofilm maturation can be largely

responsible for weakening microbial adhesion strength (Ohashi and Harada, 1996). Small

clusters tend to detach more frequently than larger aggregates under steady conditions in

turbulent flow (Stoodley et al., 2001). Cell physiology within biofilms may be affected by

adherence and subsequent metabolism and growth on a surface due either to concentrated levels

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


of organics at the substratum, or due to the adhesion mechanism and forces exerted on the cell, or

to the ability of cells to form colonies on a surface allowing communication between cells

(Bryers, 1987).

Cells may also communicate via quorum sensing (QS), which may in turn affect various

biofilm processes (Donlan, 2002), including induction of virulence effects. Quorum sensing is a

mechanism of gene regulation in which bacteria use chemical signals to monitor their own

population density and to control expression of specific genes in response to population density

(Fuqua et al., 1997). Davies et al., (1998) studied the effect of two systems involved in QS on

Pseudomonas aeruginosa, lasR-lasI (related to extracellular signal N-(3-oxododecanoyl)-L-

homoserine lactone) and rhlR-rhlI (related with synthesis of N-butyryl-L-homoserine lactone).

Mutants and wild types were able to produce biofilms; however, only wild type cells were able to

form a mature biofilm in the presence of microcolonies and water channels. Mutants were only

able to form monolayers, suggesting that QS in Pseudomonas aeruginosa was responsible for

biofilm differentiation, even though it was not involved in the attachment process. An established

biofilm provides an optimal environment for the exchange of genetic material between cells;

however, the degree of genetic exchange tends to be lower within a biofilm, adversely impacting

microbial sensitivity to antibiotics, surfactants and sanitizers (Bower and Daeschel, 1999).

7. Biofilm Effects on Finished Water Quality

Some of the most notable effects of biofilms in UDWDS relate to: i) microbially-induced

corrosion; ii) loss of indicator organism utility; iii) taste, color and odor problems; iv)

disinfectant consumption.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


7.1. Microbially-induced corrosion: Corrosion of pipe surfaces represents a major risk

factor deteriorating physical and hydraulic integrity of UDWDS, while adversely impacting

finished water quality. The main factors influencing pipe surface corrosion are: pipe material

type, water corrosivity, the soil/water quality external to pipe, and microbial activity in the pipe

biofilm (Geldreich, 1996). Over time, corrosion may become serious enough to restrict water

passage, causing pipe breaks, and accelerating biofilm formation (Geldreich, 1996). Frequently

encountered bacteria on corrosive pipe surfaces are those of iron and sulfur species. Iron-

oxidising bacteria, such as Gallionella oxidize soluble reduced iron (Fe2+

) at the corroded

pipe/water interface causing Fe3+

precipitation (AWWA, 1995). Microbes involved in the

oxidation of iron on steel surfaces can deposit oxides of iron and manganese in the form of

tubercles (Walch, 1992). Sulfur-oxidizing microbial activity, such as, Thiobacillus could

generate sulfate and hydrogen ions, lowering water pH in the surrounding environment that could

promote pipe pitting. Sulfur-reducing microbes under anaerobic conditions in UDWDS could

generate hydrogen sulfide gas that accelerates corrosion rates, giving off undesirable smell at the

point of use (AWWA, 1995). Other bacteria associated with corrosive reactions are those of

Acidovorax spp., and Sphingomonas sp. resulting in production of blue water, i.e., dissolved and

particulate copper release. Biofilms associated with copper corrosion scale products were

detected after production of blue water (Chauret et al., 2001; Critchley et al., 2004).

7.2. Loss of indicator organism utility: An extensive pipe biofilm structure may

compromise the effectiveness of total coliform tests as an indicator of drinking water quality in

two major ways. Firstly, a high level of heterotrophic bacteria in pipe biofilm and suspended

sediment particles may interfere with the analysis of total coliforms. This may occur when

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


biofilm-released heterotrophic bacteria prevent the growth, and thereby detection of coliforms

with certain analytical media via competitive inhibition for nutrients and production of various

toxins (U.S. EPA, 2002). Instances of coliform proliferation in pipe biofilms are well

documented in the literature as reviewed in Geldreich (1996) and LeChevallier (1990). Secondly,

biofilm coliforms could detach into finished water, resulting in coliform-positive samples; a

coliform-positive test under the aforementioned conditions could suggest growth of other

microbes as well, including opportunistic pathogens.

7.3. Taste, color and odor problems: Aesthetic concerns, such as water discoloration, taste

and odor issues may result from a number of reactions, some of which are microbially-mediated.

The types of microbes often associated with aesthetic issues in drinking-water are actinomycetes

(Zaitlina and Watson, 2006), iron and sulfur bacteria, and algae (blue-green) (AWWA, 1995;

Cohn et al., 1999; Burlingame and Alselme, 1995). Certain algal species and actinomycetes

produce compounds bearing unpleasant odor such as, geosmin and 2-methylisoborneol. Sulfate-

reducing bacteria were found within the structure of iron and copper corrosion scales in UDWDS

and they were associated with taste complaints to elevated sulfides and the visual coloration of

finished water (black water) (Jacobs et al., 1998; Jacobs and Edwards, 2000). Bacteria of the

genus Hyphomicrobium, when sloughed off a biofilm, could cause episodic release of black

water, although this may also be induced via suspension of pipe scale-based Fe/Mn particles

(Van der Wende et al., 1990). Microbially-produced metabolites that may be or not harmful to

public health tend to proliferate in static portions of UDWDS or in stratified regions of water

storage tanks. Pathogenic algal metabolites that may compromise public health are three

neurotoxins with somewhat different modes of blocking neuronal signal transmission (anatoxin-

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


a, anatoxin-a(s), and aphantoxin or saxitoxin), one general cytotoxin which inhibits protein

synthesis (cylindrospermopsin), and a group of toxins termed microcystins that inhibit protein

phosphatases (Chorus et al., 1997).

7.4. Disinfectant Consumption: Biofilms react with chemical disinfectants thereby

decreasing residual disinfectant concentration in water available for planktonic pathogen

inactivation (Berger et al., 2000). An extensive biofilm may decrease disinfectant levels to

minimum, rendering it inadequate to protect the public from waterborne outbreaks. LeChevallier

et al. (1990) showed greater inactivation of heterotrophic plate counts induced by chloramine in

galvanized pipes, whereas chlorine worked better with PVC and copper pipes. Use of

chloramines as a disinfectant often results in faster disinfectant decay due to nitrification in lead

pipes (Zhang and Edwards, 2009). Nitrification-induced pH drop could increase Pb leaching

from lead pipes depending on the magnitude of initial alkalinity and activity of nitrifying bacteria

(Zhang et al., 2009). Disinfectant decay was noted with water age, particularly in chloraminated

simulated water distribution systems, resulting in increased microbial detection frequencies and

densities with water age (Wang et al., 2012b). Pipe corrosion could offset the disinfecting action

of chlorine/chloramine via enhanced pipe surface porosity and surface roughness allowing for

improved anchorage of bacteria while at the same time iron rust could serve bacteria with

essential nutrients for growth (Morton et al., 2005). Chlorine contact with bacterial exopolymeric

biomass of biofilm colonies (Pseudomonas strains) could result in the production of

carbonaceous and nitrogenous disinfection by products (Wang eta l., 2012c).

Maintenance of residual chlorine and/or chloramines in distant areas of UDWDS is often

problematic. Oxidizible compounds, like ferrous ions that can be released from old iron pipes

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


subject to enhanced corrosive phenomena could readily consume residual monochloramine

(Vikesland and Valentine, 2002). Cupric hydroxide solids often deposited in copper pipes rapidly

consume chlorine (Nguyen et al., 2011), or chloramines in new copper pipes (Nguyen et al.,

2012), especially in waters of low pH and high temperatures. In addition, pipe material exerted

large influence on chlorine decay kinetics, where stainless steel exhibited the fastest chlorine

decay kinetics followed by ductile iron and polyethylene pipes (Li et al., 2012). Lehtola et al.

(2005) showed that UV disinfection in the pilot waterworks and outlet water of pipes decreased

viable bacterial numbers by 79%, but UV disinfecting effect in biofilms was minor; on the other,

chlorine effectively decreased microbial numbers in water and biofilms of PE pipes but in copper

pipes the effect of chlorination was weaker; microbial numbers increased back to the level before

chlorination within a few days (Lehtola et al., 2005). In biofilms present in copper pipes, chlorine

decreased microbial numbers only in front of the pipeline, suggesting that copper pipes may

require a higher chlorine dosage than plastic pipes to achieve effective disinfection of the pipes.

The reason the authors give for the weaker oxidizing efficiency of chlorine in copper pipes was

that its concentration declined more rapidly in the copper rather than in the PE pipes (Lehtola et

al., 2005).

8. Biofilms in UDWDS and Health Risks

Public health threats associated with biologic agents in UDWDS typically refer to bacteria,

viruses, protozoa, invertebrates, algae and algal toxins, fungi and microbial toxins (Servais et al.,

1995; Wingender and Flemming, 2004; Kilb et al., 2003). All known exposure pathways, such as

ingestion of contaminated water, inhalation of contaminated aerosols (showering), and dermal

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


absorption during washing, showering and bathing are under consideration in a comprehensive

human exposure assessment for chemicals/toxins and pathogens found in home taps of urban

consumers (pipe to tap) (Table 4, Figure 1). Diarrhea is the main end point of disease used to

calculate the % contribution of lack of access to safe water sanitation and hygiene to the overall

morbidity and mortality figures, but in recent years, other outcomes related to the presence of

chemicals/toxins (neurodevelopment effects, reproductive, hormonal disruption, etc.) emerge,

hinting towards additional contributors/risk factors that could be accounted for in the pertinent

burden of disease calculations. The aforementioned human exposure pathways become of

extreme importance for vulnerable subpopulations, such as those of schools, hospitals and other

health care facilities as biofilm-borne pathogens could considerably contribute to water-

associated nosocomial infections (Exner et al., 2005).

The WHO (2003) identified two major categories of hygienically-relevant microorganisms: (i)

microorganisms with pathogenic properties that are associated with water-related illness and

outbreaks, and (ii) bacteria used as index and indicator organisms in water analysis, indicating

the presence of pathogenic organisms of fecal origin (index organisms) or indicating the

effectiveness of water treatment processes (indicator organisms). Obligate water-related

pathogens, i.e., those causing disease to humans irrespective of their health status are usually

fecally-derived. Others are opportunistic pathogens causing disease to sensitive subpopulations,

such as the elderly, children, immune-compromised individuals, and patients with preexisting

disease or other predisposing conditions, facilitating infection by these organisms. Important

waterborne bacterial pathogens found in UDWDS which can infect the human respiratory system

and the gastrointestinal tract are: Salmonella enterica (e.g., serovar Typhi, Paratyphi and

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Typhimurium), Shigella spp., Vibrio cholerae, pathogenic E. coli variants (e.g., enterotoxigenic

E. coli, enterohaemorrhagic E. coli O157:H7), Yersinia enterocolitica, Campylobacter spp.,

Helicobacter pylori. Legionella pneumophila, and the Mycobacterium avium complex. (Stood et

al., 1985, Park et al., 2001, Declerck et al., 2009, Wingender and Flemming, 2011)

Pathogenic strains have been repeatedly measured in UDWDS, showing remarkable

persistence within pipe biofilms that serve as temporary or long-term reservoirs for pathogens.

More research is needed to evaluate the pathogenic potential of viable, but not culturable

(VBNC) organisms and to identify the factors relevant in UDWDS triggering the VBNC state

and inducing resuscitation to the culturable and infectious state (Wingender and Flemming,

2011).

9. Synthesis - Scale and Biofilm Conglomerate (SBC) Effects on Finished Water

Quality

This critical review attempts to synthesize knowledge from related fields, such as

environmental chemistry, environmental microbiology, and environmental health on the alarming

issue of SBC-induced deterioration of finished water quality within aging UDWDS. Pipe scales

and biofilms co-exist in UDWDS (Table 2), serving as contaminant sources

(chemical/pathogens) to finished water via poorly understood mechanisms, posing an

unaccounted so far synergistic or antagonistic risk to consumer health. Scattered data exists about

main effects of either pipe scales or biofilms on finished water quality in UDWDS, but, little is

known about their combined effects. Intermittent release of inorganic chemicals (As, Pb, Cu,

etc.) in finished water are not explained on the basis of thermodynamic or kinetic models

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


tackling dissolution mechanisms of low solubility mineral phases, since microenvironments

within well-organized microbial communities (biofilms) create unique extracellular and

intracellular niches (Hunter et al., 2008). An illustrating example of SBC in UDWDS is the

presence of Pseudomonas spp. biofilm in close proximity to manganese-based nodules found in

both PVC and HDPE pipe surfaces (Murdoch and Smith, 1999; 2000).

The conservative notion that finished water quality between point of entry and point of use

remains unchanged could hold true in aging UDWDS, if raw water treatment practices, pipe

characteristics along with physicochemical and hydraulic characteristics of finished water

remained unaltered over time. In reality, this is seldom the case, while relevant studies

concomitantly studying SBC within UDWDS are unavailable. One of the major SBC effects

relates to the so-called microbially-induced corrosion (MIC), i.e., the facilitating effect of

biofilms on contaminant release from pipe scales or corroded pipe surfaces. MIC could be

promoted by the presence of complexing agents, such as, EPS and/or metabolites of

microorganisms (Murdoch and Smith, 1999; 2000; Geesey et al., 1986; 1989; Bremer and

Geesey, 1991), or via changes in redox chemistry at the scale/water interface (Lewandowski et

al., 1997; Allen et al., 1980; LeChevallier et al., 1993; Lee et al., 1980). Microbial conglomerates

in close contact with pipe scales, i.e., the SBC could catalyze corrosion rates as it has been

documented for metallic pipes, such as, titanium (Souza et al., 2010) and copper (Keevil, 2004).

Interactions between copper scales and sulfate-reducing bacteria or fungi, such as Alcaligenes,

Achromobacter, Flavobacterium, Methylobacetrium, Pseudomonas and Sphingomonas spp. were

held responsible for progressively grown copper pits (Keevil et al., 1989; Chamberlain and

Angell, 1990; Jacobs and Edwards, 2000). Steel corrosion tubercles were located in close

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


proximity to gram-negative bacteria within biofilms, such as Pseudomonas spp., Afipia spp.,

Rubritepida flocculans, Bacillus pumilus, Blastobacter and Bradyrhizobium japonicum, resulting

in corrosion and pit formation (Bolton et al., 2010). Copper leaching into finished water occurred

as a combined effect of both copper corrosive scales and Acidovorax delafieldii (Critchley et al.,

2001). SBC conglomerates (iron tubercles and bacterial biofilms) were held responsible for

increased counts of coliform bacteria in finished water flowing through bituminous-coated,

cement-lined cast iron pipes (LeChevallier et al., 1987). The establishment of SBC may provide a

protective environment for pathogenic bacteria as they better attach to rough SBC surfaces that

serve as anchorage points for bacterial stability and protection from surface redox reactions

(LeChevallier et al., 1993). Other synergistic SBC effects on finished water quality are those

inducing release of chemicals from pipe scales due to alterations in water chemistry surrounding

SBC. As an example, ammonia supplied by chloramine in UDWDS could be subject to

nitrification by biofilms on pipe surfaces, lowering water pH (pH 6.5), and thus, inducing Pb-

bearing scale destabilization and Pb release (Zhang et al., 2009). The magnitude of Pb release

also depended upon the initial alkalinity and extent of nitrification; a decrease in initial water

alkalinity from 100 to 15 mg L-1

resulted in a 65x fold increase of Pb concentration due to a

major reduction in water pH (from 8 to 6.5) (Zhang et al., 2009). The effect of pipe materials on

nitrification varies, since zerovalent iron and lead pipes could recycle nitrate back to ammonia

substrate, while copper pipes induce microbial toxicity effects due to dissolved copper release,

and concrete pipes tend to enhance nitrification via release of essential nutrients (Zhang et al.,

2010).

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


From a public health perspective, the complex interplay of SBC with different pipe material

types, finished water chemistries and disinfectant types and concentrations is too important to

ignore. Nevertheless, no studies exist that concomitantly evaluate interactive effects of both

scales and biofilm conglomerates on the episodic release of contaminants under various

environmental conditions in aging UDWDS. Future research is warranted to improve our

understanding of processes that dictate chemical and microbial release from SBC, posing acute

and chronic health risks to consumers served by UDWDS around the globe. This critical review

will backup efforts by WHO/UNICEF that struggle to increase provision of safe access to water

of improved quality, despite their success in substantially increasing drinking water coverage of

populations, worldwide (WHO/UNICEF, 2012). It is essential to highlight the importance of

research focusing on the identification of factors that dictate the onset and duration of episodic

contaminant release events, i.e., both microbial outbreaks and chemical release. Attention should

be paid on studies being able to differentiate between factors influencing induction of acute,

meso-term and long-term contaminant release events from SBC in UDWDS. This could better

serve epidemiological studies towards evaluation of the burden of disease via careful design of

exposure assessment protocols associated with such episodic contaminant release events. Such

efforts could be instrumental in guiding future monitoring and surveillance programs of finished

water quality towards capturing possible episodic release events.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


REFERENCES

1) Aissa, R., Francois, M., Ruby, C., Fauth, F., Medjahdi, G., Abdelmoula, M., Genin, J.M.,

2006. Formation and crystallographical structure of hydroxysulphate and

hydroxycarbonate green rusts synthetised by coprecipitation. Journal of Physics and

Chemistry of Solids 67 (5-6), 1016-1019.

2) Allen, MJ., Taylor, R.H., Geldreich, E.E., 1980. The occurrence of microorganisms in

water main encrustations. Journal of the American Water Works Association72 (11),

614–625.

3) Allmann, R., Donnay, J.D.H., 1969. About structure iowaite. Amer Mineral 54 (1-2),

296-299.

4) American Water Works Association (AWWA), 1995. Problem organisms in water:

identification and treatment. Manual of Water Supply Practices, M7. Third edition.

AWWA M7. Denver, CO.

5) American Water Works Association Research Foundation & DVGW-

Technologiezentrum Wasser. Internal corrosion of water distribution systems, 2nd

edition. Denver, CO, USA, 1996.

6) Andritsos, N., Karabelas, AJ. 1999. The influence of particulates on CaCO3 scale

formation. Journal of Heat Transfer 121, 225–227.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


7) Armon, R., Starosvetzky, J., Arbel, T., Green, M., 1997. Survival of Legionella

pneumophila and Salmonella typhimurium in biofilm systems. Water Science and

Technology 35(11-12), 293–300.

8) Aschengrau, A., Rogers, S., D. Ozonoff, 2003. Perchloroethylene-contaminated drinking

water and the risk of breast cancer: Additional results from Cape Cod, Massachusetts,

USA. Environ. Health Perspect., 111: 167-173.

9) Awwa Research Foundation (AwwaRF), 2008. Dsitribution system corrosion and the lead

and copper rule: An overview of AwwaRF Research. 1-24. Available at

http://www.awwa.org/files/GovtPublicAffairs/PDF/LCRResearch.pdf. (Accessed on June

21st 2012).

10) Axten, C.W., Foster, D., 2008. Analysis of airborne and waterborne particles around a

taconite ore processing facility. Regulatory Toxicology and Pharmacology 52 (1), S66-

S72.

11) Bakker, D.P., Postmus, B.R., Busscher, H.J., van der Mei, H.C., 2004. Bacterial strains

isolated from different niches can exhibit different patterns of adhesion to substrata.

Applied and Environmental Microbiology70 (6), 3758–3760.

12) Berger, P.S., Clark, R.M., Reasoner, D.J., 2000. Water, Drinking. In: Encyclopedia of

Microbiology. 2nd Edition. J. Lederberg., Ed.; Academic Press: San Diego. Vol.4, pp

898-913.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://www.awwa.org/files/GovtPublicAffairs/PDF/LCRResearch.pdf

ACCEPTED MANUSCRIPT


13) Beuken, R., Reinoso, M., Sturm, S., Kiefer, J., Bondelind, M., Åström , J., Lindhe, A.,

Losén, L., Pettersson, T., Machenbach, I., Melin, E., Thorsen, T., Eikebrokk, B., Hokstad,

P., Røstum, J., Niewersch, C., Kirchner, D., Kozisek, F., Gari, D., Swartz, C., Menaia, J.,

2008. Identification and description of hazards for water supply systems. A catalogue of

today’s hazards and possible future hazards. WA4 TECHNEAU report D4.1.4. 2008,

August, pp 1-79.

14) Berry, D., C. Xi, and L. Raskin. 2006. Microbial Ecology of drinking water distribution

systems. Curr Op. Biotechnol. 17:1-6.

15) Beveridge, T.J., Makin, S.A., Kadurugamuwa, J.L., Li, Z., 1997. Interactions between

biofilms and the environment. FEMS Microbiology Reviews 20, 291-303.

16) Bolton, N., Critchley, M., Fabien, R., Cromar, N., Fallowfield, H., 2010. Microbially

influenced corrosion of galvanized steel pipes in aerobic water systems. Journal of

Applied Microbiology 109 (1), 239-247.

17) Bomo, A.M., Storey, M.V., Ashbolt, N.J., 2004. Detection, integration and persistence of

Aeromonas in water distribution system biofilms. Journal of Water and Health 2, 83-96.

18) Borch, T., A.K. Camper, J.A. Biederman, P.W. Butterfield, R. Gerlach, J.E. Amonette,

2008. Evaluation of Characterization Techniques for Iron Pipe Corrosion Products and

Iron Oxide Thin Films. J. Environmental Engineering, 134: 835-844.

19) Boulay, N., M. Edwards, 2001. Role of temperature, chlorine, and organic matter in

copper corrosion by-product release in soft water. Water Research, 35, 683-690.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


20) Bower, C., Daeschel, M., 1999. Resistance responses of microorganisms in food

environments. International Journal of Food Microbiology 50 (1-2), 33-44.

21) Boyd, G.R., Dewis, K.M., Korshin, G.V., Reiber, S.H., Schock, M.R., Sandvig, A.M.,

Giani, R., 2008. Effects of changing disinfectants on lead and copper release: Part 1-

Literature Review. Journal of the American Water Works Association 100 (11), 1-44.

22) Bremer, P.J., Geesey, G.G., 1991. Laboratory-based model of microbiologically induced

corrosion of copper. Applied and Environmental Microbiology 57 (7), 1956–1962.

23) Brongers, M.P.H., 2002. Appendix K. Drinking Water and Sewer Systems in Corrosion

Costs and Preventative Strategies in the United States. Report FHWA-RD-01-156. US

Department of Transportation Federal Highway Administration.

24) Bryers, J.D., 1987. Biologically active surfaces: processes governing the formation and

persistence of biofilms. Biotechnology Progress 3 (2), 57-68.

25) Burke, L.M., 2006. Fate of Salmonella Typhimurium in biofilms of drinking water

distribution systems. MSc. Thesis Univ. Pretoria. 2006, pp 123. Available at

http://upetd.up.ac.za/thesis/available/etd-02232007-

192747/unrestricted/00Dissertation.pdf (accessed on June 21st, 2012).

26) Burlingame, G.A., Alselme, C., 1995. Distribution system tastes and odors. In: Advances

in Taste-and-Odor Treatment and Control; Suffet, I. H.; Mallevialle, J.; Kawczynski, E.;

Eds.; eds). AWWARF/Lyonnaise des Eaux publication. American Water Works

Association, Research Foundation, Denver, CO. pp 281-320.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://upetd.up.ac.za/thesis/available/etd-02232007-192747/unrestricted/00Dissertation.pdf

http://upetd.up.ac.za/thesis/available/etd-02232007-192747/unrestricted/00Dissertation.pdf

ACCEPTED MANUSCRIPT


27) Busscher, H.J., Van der Mei, H.C., 1995. Use of flow chamber devices and image

analysis methods to study microbial adhesion. Methods in Enzymology 253, 455–476.

28) Buswell, C. M., Herlihy, Y. M., Lawrence, L. M., McGuiggan, J. T., Marsh, P. D.,

Keevil, C. W., Leach, S. A., 1998. Extended survival and persistence of Campylobacter

spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and

-rRNA staining. Applied and Environmental Microbiology 64 (2), 733–741.

29) Campbell, H.S., Turner, M.E.D., 1983. The Influence of Trace Organics on Scale

Formation and Corrosion. J Inst Wat Eng Sci., 4, 55.

30) Cerrato, J.M., L.P. Reyes, C.N. Alvarado, A.M. Dietrich, 2006. Effect of PVC and iron

materials on Mn(II) deposition in drinking water distribution systems. Water Research,

40, 2720-2726.

31) Chamberlain, A.H.L., Angell, P., 1990. Influences of microorganisms on pitting of copper

tube. In Microbially Influenced Corrosion and Biodegradation. Dowling, N.J.; Mittelman,

M.W.; Danko, J.C. Eds.; University of Tennessee Press, Knoxville.1990, pp 3-65.

32) Chan, M.W.M., 2003. A critical study on corrosion and corrosion control methods for

piping systems in Hong Kong. Ph.D. Thesis. The Hong Kong Polytechnic University,

Department of Building Service Engineering, Hong Kong. Available at

http://repository.lib.polyu.edu.hk/jspui/handle/10397/3009 (Accessed on June 21st,

2012).

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://repository.lib.polyu.edu.hk/jspui/handle/10397/3009

ACCEPTED MANUSCRIPT


33) Chatfield, E.J., Dillon, M.J., 1979. A national study for asbestos fibres in Canadian

drinking water supplies. Ottawa, Canada, Department of National Health and Welfare,

Environmental Health Directorate Report 79-EHD-34.

34) Chauret, C., Volk, C., Creason, R., Jarosh, J., Robinson, J., Warnes, C., 2001. Detection

of Aeromonas hydrophila in a drinking water distribution system: a field and pilot study.

Canadian Journal of Microbiology 47 (8), 782-786.

35) ChemSec., 2011. BPA banned in baby bottles but used in drinking water pipes. Press

Release, 14 December 2011.

http://www.chemsec.org/images/stories/2011/chemsec/111214_ChemSec_press_release_

BPA_and_relining.pdf (December 14th, 2011).

36) Chen, X., Stewart, P.S., 2002. Role of electrostatic interactions in cohesion of bacterial

biofilms. Applied Microbiology and Biotechnology 59 (6), 718–720.

37) Chorus, I., Salas, H.J., 1997. Health impacts of freshwater algae: Draft for guidelines for

recreational water and bathing beach quality. p. 5, Paper presented to the III Regional

AIDIS congress for North America and the Caribbean, San Juan, Puerto Rico, 7-12 June.

1997.

38) Chu, CW; Lu, CY; Lee, CM; et al., 2003. Effects of chlorine level on the growth of

biofilm in water pipes. JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH

PART A. 38: 1377-1388.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://www.chemsec.org/images/stories/2011/chemsec/111214_ChemSec_press_release_BPA_and_relining.pdf

http://www.chemsec.org/images/stories/2011/chemsec/111214_ChemSec_press_release_BPA_and_relining.pdf

ACCEPTED MANUSCRIPT


39) Cloete, E., Westaard, D., van Vuuren, S.J., 2003. Dynamic response of biofilm to pipe

surface and fluid velocity. Water Science and Technology47 (5), 57–59.

40) Cohn, P.D., Cox, M., Berger, P.S., 1999. Health and aesthetic aspects of water quality,

Chapter 2. In: Water Quality and Treatment (5th ed.). Letterman, R.D.; Ed.; McGraw-

Hill, Inc. New York, NY. pp 2.10-2.86.

41) Corpe, W.A., 1980 Microbial surface components involved in adsorption of

microorganisms onto surfaces. In: Bitton G, Marshall KC, editors. Adsorption of

microorganisms to surfaces. New York: John Wiley & Sons;. p. 105–44.

42) Costerton, J. W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., Lappin-Scott, H.M.,

1995. Microbial biofilms, p. 711-745. In L. N. Ornston, A. Balows, and E. P. Greenberg

(ed.), Annu. Rev. Microbiol., vol. 49. Annual Reviews, Inc., Palo Alto, CA

43) Costerton, J.W., 1999. Introduction to biofilm. International Journal of Antimicrobial

Agents. 11, 217-221.

44) Critchley, M.M., Cromar, N.J., McClure, N., Fallowfield, H.J., 2001. Biofilms and

microbially influenced cuprosolvency in domestic copper plumbing systems. Journal of

Applied Microbiology 91 (4), 646-651.

45) Critchley, M.M., Pasetto, R., O’Halloran, R.J., 2004. Microbiological influences in blue

water copper corrosion. Journal of Applied Microbiology 97 (3), 590-597.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


46) Danese, P.N., Pratt, L.A., Kolter, R., 2000. Exopolysaccharide production is required for

development of Escherichia coli K-12 biofilm architecture. Journal of Bacteriology182

(12), 3593–3596.

47) Davey, M.E., O'toole, G.A., 2000. Microbial Biofilms: from Ecology to Molecular

Genetics Microbiology and Molecular Biology Reviews 64 (4), 847 – 867.

48) Davidson, C.M., Peters, N.J., Britton, A., Brady, L., Gardiner, P.H.E., Lewis, B.D., 2004.

Surface analysis and depth profiling of corrosion products formed in lead pipes used to

supply low alkalinity drinking water. Water Science and Technology 49 (2), 49-54.

49) Davies, D.G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W., Greenberg,

E.P., 1998. The involvement of cell-to-cell signals in the development of a bacterial

biofilm. Science 280 (5361), 295–298.

50) Dawson, D.M., 1990. Colloid-A- Tron: A non-chemical water treatment system.

Corrosion Prevention and Control 37 (3), 61–64.

51) Declerck, P., Behets, J., Margineanu, A., van Hoef, V., De Keersmaecker, B., Ollevier,

F., 2009. Replication of Legionella pneumophila in biofilms of water distribution pipes.

Microbiological Research. 164(6), 593-603

52) Donlan, R.M., 2002. Biofilms: Microbial life on surfaces. Emerging Infectious Diseases 8

(9), 881-890.

53) Donlan, R.M., Costerton, J.W., 2002. Biofilms: survival mechanisms of clinically

relevant microorganisms. Clinical Microbiology Reviews 15 (2), 167-193.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


54) Edwards, M., 2004. Controlling corrosion in drinking water distribution systems: a grand

challenge for the 21st century. Water Science and Technology49 (2), 1-8.

55) Edwards, M., Abhijeet, D., 2004. Role of chlorine and chloramine in corrosion of lead

bearing plumbing materials. Journal American Water Works Association. 96: 69-81.

56) Edwards, M., and L.S. McNeill, 2002. Effect of Phosphate Inhibitors on Lead Release

from Pipes. Journal American Water Works Association. 94: 79-90.Ewing, F.J., 1935.

The crystal structure of lepidocrocite. Journal of Chemical Physics 3 (7), 420-424.

57) Edwards, M., and S. Triantafyllidou, S., 2007. Chloride to Sulfate Mass Ratio and Lead

Leaching to Water. JAWWA 99(7): 96-109.

58) Edwards, M., Jacobs, S., Taylor, R.J., 2000. The blue water phenomenon. Journal of the

American Water Works Association 92 (7): 72–82.

59) Edwards, M., Triantafyllidou, S., Best, D., 2009. Elevated blood lead in young children

due to lead-contaminated drinking water: Washington, DC, 2001−2004. Environmental

Science and Technology 43 (5), 1618–1623.

60) Fitzpatrick, F., Humphreys, H., O’Gara, J.P., 2005. The genetics of staphylococcal

biofilm formation—will a greater understanding of pathogenesis lead to better

management of device-related infection? Clinical Microbiology and Infection 11 (12),

967–973.

61) Fleet, M.E., 1981. The structure of magnetite. Acta Crystallographica B37, 917–920.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


62) Flemming, H.C., Percival, S.L., Walker, J.T., 2002. Contamination potential of biofilms

in water distribution systems. Water Supply 2 (1), 271–280.

63) Flemming, H.C., Wingender, J., 2001. Relevance of microbial extracellular polymeric

substances (EPSs) - Part I: Structural and ecological aspects. Water Science and

Technology 43, 1-8.

64) Flournoy, R.L., Monroe, D., Chestnut, N.M., Kumar, V., 1999. Health Effects from Vinyl

Chloride Monomer Leaching from pre-1977 PVC pipe, AWWA Annual Conference

Proceedings.

65) Fuqua, C., Winans, S.C., Greenberg, E.P., 1997. Quorum sensing in bacteria: the LuxR-

LuxI family of cell densityresponsive transcriptional regulators. Journal of

Bacteriology176 (2), 269-275.

66) Gagnon, G.A., J.L. Rand, K.C. O’Leary, A.C. Rygel, C. Chauret, R.C. Andrews, 2005.

Disinfectant efficacy of chlorite and chlorine dioxide in drinking water biofilms. Water

Research, 39, 1809-1817.

67) Gallard, H.; Leclercq, A.; Croue, J. P., Chlorination of bisphenol a: Kinetics and by-

products formation. Chemosphere 2004, 56, (5), 465-473.

68) Gallardo-Moreno, A.M., Gonzalez-Martin, M.L., Perez-Giraldo, C., Bruque, J.M.,

Gomez-Garcia, A.C. 2002a. Serum as a factor influencing adhesion of Enterococcus

faecalis to glass and silicone. Applied and Environmental Microbiology 68 (11), 5784-

5787.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


69) Gallardo-Moreno, A.M., Gonzalez-Martin, M.L., Perez-Giraldo, C., Garduno, E., Bruque,

J.M., Gomez-Garcia, A.C., 2002b. Thermodynamic analysis of growth temperature

dependence in the adhesion of Candida parapsilosis to polystyrene. Applied and

Environmental Microbiology 68 (5), 2610-2613.

70) Garrett, E.S., Perlegas, D., Wozniak, D.J., 1999. Negative control of flagellum synthesis

in Pseudomonas aeruginosa is modulated by the alternative sigma factor AlgT (AlgU).

Journal of Bacteriology181 (23), 7401–7404.

71) Geesey, G.G., Jang, L., Jolley, J.G., Hankins, M.R., Iwaoka, T., Griffiths, P.R., 1989.

Binding of metal ions by extracellular polymers of biofilm bacteria. Water Science and

Techology 20(11/12), 161–165.

72) Geesey, G.G., Mittelman, M.W., Iwaoka, T., Griffiths, P.R., 1986. Role of bacterial

exopolymersin the deterioration of metallic copper surfaces. Materials Performance 25

(2), 37–40.

73) Geldreich, E.E., 1996. Creating microbial quality in drinking water. In: Microbial quality

of water supply in distribution systems. Lewis Publishers, Boca Raton, FL, 39-101.

74) Gerke, T.L., Scheckel, K.G., Schock, M.R., 2009. Identification and Distribution of

Vanadinite (Pb-5(V5+

O4)(3)Cl in Lead Pipe Corrosion By-Products. Environmental

Science and Technology 43 (12), 4412-4418.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


75) Giao, M.S., Azevedo, N.F., Wilks, S.A., Vieira, M.J., Keevil, C.W., 2008. Persistence of

Helicobacter pylori in heterotrophic drinking water biofilms. Applied and Environmental

Microbiology 74 (19), 5898–5904.

76) Graf, D.L., 1961. Crystallographic tables for the rhombohedral carbonates. American

Mineralogist 46, 1283-1316.

77) Heim, T.H., A.M. Dietrich, 2007. Sensory aspects and water quality impacts of

chlorinated and chloraminated drinking water in contact with HDPE and cPVC pipe.

Water Research, 41, 757-764.

78) Hentzer, M., Teitzel, G.M., Balzer, G.J., Heydorn, A., Molin, S., Givskov, M., Parsek,

M.R., 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure

and function. J. Bacteriol. 183 (18), 5395–5401.

79) Hodgkiess, T., 2004. Inter-relationships between corrosion and mineral-scale deposition

in aqueous systems. Water Science and Technology, 49 (2), 121-128.

80) Hudson, H.E., Gilcrea, F.W., 1976. Health and Economic Aspects of Water Hardness and

Corrosiveness. Journal of the American Water Works Association 68(4), 201–204.

81) Huggins, D., 2008. Remediation of Lead Levels in Drinking Water: The City of London’s

Experience. Ontario Water Works Association, Proceedings of the OWWA/OMWA Joint

Annual Conference and Trade Show, London, ON, April 27-30, 2008.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


82) Hunter, R.C., Hitchcock, A.P., Dynes, J.J., Obst, M., Beveridge, T.J., 2008. Mapping the

speciation of iron in pseudomonas aeruginosa biofilms using scanning transmission x-ray

microscopy. Environmental Science and Technology42(23), 8766-8772.

83) Impellitteri, C.A., O. Evans, B. Ravel, 2007. Speciation of organotins in polyvinyl

chloride pipe via X-ray absorption spectroscopy and in leachates using GC-PFPD after

derivatisation. J. Environ. Monit., 9: 358-365.

84) Inoue, T., Shingaki, R., Sogawa, N., Sogawa, C.A., Asaumi, J., Kokeguchi, S., Fukui, K.,

2003. Biofilm formation by a fimbriae-deficient mutant of Actinobacillus

actinomycetemcomitans, Microbiology and Immunology 47 (11), 877-881.

85) Istituto Superiore di Sanita (ISS)., 1993. Environment: Research Projects of the Istituto

Superiore di Sanita. Environment, ISS, Rome. 1-73.

86) Jacobs, S. and M. Edwards, 2000. Sulfide scale catalysis of copper corrosion. Wat. Res.,

34: 2798-2808.

87) Jacobs, S., S. Reiber and M. Edwards, 1998. Sulfide-Induced Copper Corrosion. Journal

American Water Works Association. 90: No. 7, 62-73.

88) Jørgensen, C., Boyd, H.B., Fawell, J., Hydes, O., 2008. Establishment of a list of

chemical parameters for the revision of the Drinking Water Directive. Preliminary draft

final report to DG ENV for the revision of the Drinking Water Directive

ENV.D.2/ETU/2007/0077r, April 2008 ; available at

http://circa.europa.eu/Public/irc/env/drinking_water_rev/library?l=/stakeholder_consultati

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://circa.europa.eu/Public/irc/env/drinking_water_rev/library?l=/stakeholder_consultation/stakeholder_2008_1/parameters_2008-04-25pdf/_EN_1.0_&a=d

ACCEPTED MANUSCRIPT


on/stakeholder_2008_1/parameters_2008-04-25pdf/_EN_1.0_&a=d (Accessed on June

21st, 2012).

89) Keevil, C.W., 2002. Pathogens in environmental biofilms. In: Bitton, G. (Ed.),

Encyclopedia of Environmental Microbiology, Vol. 4. John Wiley and Sons, Inc., New

York, pp. 2339–2356

90) Keevil, C.W., 2004. The physico-chemistry of biofilm-mediated pitting corrosion of

copper pipe supplying potable water. Water Science and Technology49 (2), 91-98.

91) Keevil, C.W., Walker, J.T., McEvoy, J., Colbourne, J.S., 1989. Detection of biofilms

associated with pitting corrosion of copper pipework in Scottish hospitals. In:

Biodeterioration Society Proceedings: Biocorrosion, Volume 5, Preston Biodeterioration

Society. pp 99–117.

92) Kerr, C.J., Osborn, K.S., Robson, G.D., Handley, P.S., 1999. The relationship between

pipe material and biofilm formation in a laboratory model system. Journal of Applied

Microbiology Symp Suppl 85, 29S–38S.

93) Kilb, B., Lange, B., Schaule, G., Flemming, H.C., Wingender, J., 2003. Contamination of

drinking water by coliforms from biofilms grown on rubber-coated valves. International

Journal of Hygiene and Environmental Health 206 (6), 563-573.

94) Kim, E.J., Herrera, J.E., Huggins, D., Braam, J., Koshowski, S., 2011. Effect of pH on the

concentrations of lead and trace contaminants in drinking water: A combined batch, pipe

loop and sentinel home study. Water Research45 (9), 2763-2774.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://circa.europa.eu/Public/irc/env/drinking_water_rev/library?l=/stakeholder_consultation/stakeholder_2008_1/parameters_2008-04-25pdf/_EN_1.0_&a=d

ACCEPTED MANUSCRIPT


95) Kimbrough, D.E., 2007. Brass corrosion as a source of lead and copper in traditional and

all-plastic distribution systems. Journal of the American Water Works Association 99 (8),

70-76.

96) Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jørgensen, A., Molin, S.,

Tolker-Nielsen, T., 2003. Biofilm formation by Pseudomonas aeruginosa wild type,

flagella and type IV pili mutants. Molecular Microbiology 48(6),1511-24.

97) Korshin, G.V., J.F. Ferguson, A.N. Lancaster, 2005. Influence of natural organic matter

on the morphology of corroding lead surfaces and behavior of lead-containing particles.

Water Research, 39, 811-818.

98) Kvech, S., and M Edwards. Solubility controls on aluminum in drinking water at

relatively low and high pH. Water Research, V. 36, 4356-4368 (2002).

99) Kvech, S., and M. Edwards. Role of Aluminosilicate Deposits in Lead and Copper

Corrosion. Journal American Water Works Association. V. 93, N. 11 104-112 (2001).

100) Kwok, W.K., Picioreanu, C., Ong, S.L., van Loosdrecht, M.C.M., Ng, W.J.,

Heijnen, J.J., 1997. Influence of biomass production and detachment forces on biofilm

structures in a biofilm airlift suspension reactor. Biotechnology and Bioengineering 58

(4), 400–407.

101) Laurent, P., Servais, P., Randon, G., 1993. Bacterial development in distribution

networks. Study and modelling. Water Supply 11 (3/4), 387–398.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


102) LeChevallie, M.W., Babcock, T.M., Lee, R.G., 1987. Examination and

characterization of distribution system biofilms. Applied and Environmental

Microbiology53 (12), 2714-2724.

103) LeChevallier, M.W., 1990. Coliform re-growth in drinking water: a review. ournal

of the American Water Works Association 82, 74-86.

104) LeChevallier, M.W., Lowry, C.D., Lee, R.G., Gibbon, D.L., 1993. Examining the

relationship between iron corrosion and the disinfection of biofilm bacteria. Journal of the

American Water Works Association 85 (7), 111-123.

105) LeChevallier, Mark W.; Lowry, Cheryl D.; Lee, Ramon G., 1990. Disinfecting

biofilms in a model distribution system. Journal - American Water Works Association, 82

(7), 87-99.

106) Lee, S.H., O’Connor, J.T., Banerji, S.K., 1980. Biologically mediated corrosion

and its effects onwater quality in distribution systems. Journal of the American Water

Works Association 72 (11), 636–645.

107) Lehtola, M. J., Torvinen, E., Kusnetsov, J., Pitkanen, T., Maunula, L., von

Bonsdorff, C. H., Martikainen, P. J., Wilks, S. A., Keevil, C. W., Miettinen, I. T., 2007.

Survival of Mycobacterium avium, Legionella pneumophila, Escherichia coli, and

Caliciviruses in drinking water-associated biofilms grown under highshear turbulent flow.

Applied and Environmental Microbiology 73 (9), 2854-2859.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


108) Lehtola, M.J., I.T. Miettinen, M.M. Keinänen, T.K. Kekki, O. Laine, A. Hirvonen,

T. Vartiainen, P.J. Martikainen, 2004. Microbiology, chemistry and biofilm development

in a pilot drinking water distribution system with copper and plastic pipes. Water

Research, 38, 3769-3779.

109) Lehtola, M.J., I.T. Miettinen, T. Lampola, A. Hirvonen, T. Vartiainen, P.J.

Martikainen, 2005. Pipeline materials modify the effectiveness of disinfectants in

drinking water distribution systems. Water Research, 39, 1962-1971.

110) Lehtola, M.J., Laxander, M., Miettinen, I.T., Hirvonen, A., Vartiainen, T.,

Martikainen P.J., 2006. The effects of changing water flow velocity on the formation of

biofilms and water quality in pilot distribution system consisting of copper or

polyethylene pipes. Water Research 40 (11), 2151-2160.

111) Lehtola, M.J., Miettinen, I.T., Lampola, T., Hirvonen, A., Vartiainen, T.,

Martikainen, P.J., 2005. Pipeline materials modify the effectiveness of disinfectants in

drinking water distribution systems. Water Research 39 (10), 1962-1971.

112) Lehtola, M.J., Miettinen, K.T., Keinanen, M.M., Kekki, T.K., Laine, O.,

Hirvonen, A., Vartiainen, T., Martikainen, P.J., 2004. Microbiology, chemistry and

biofilm development in a pilot drinking water distribution system with copper and plastic

pipes. Water Research 38 (17), 3769-3779.

113) Lemon, K.P., Higgins, D.E., Kolter, R., 2007. Flagella-mediated motility is

critical for Listeria monocytogenes biofilm formation. Journal of Bacteriology 189 (12),

4418–4424.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


114) Lewandowski, Z., Dickinson, W., Less, W., 1997. Electrochemical interactions of

biofilms with metal surfaces. Water Science and Technology 36 (1), 295–302.

115) Li, C., Yang YJ, Yu J, Zhang TQ, Mao X, Shao W., 2012. Second-order chlorine

decay and trihalomethanes formation in a pilot-scale water distribution systems. Water

Environ Res., 84(8): 656-661.

116) Liang, J.L., Dziuban, E.J., Craun, G.F., Hill, V., Moore, M.R., Gelting, R.J.,

Calderon, R.L., Beach, M.J., Roy, S.L., 2006. Surveillance of water borne disease and

outbreaks associated with drinking water and water not intended for drinking-United

States, 2003-2004. Center for diseases control, Atlanta GA, USA. Morbidity and

mortality weekly report-Surveillance summaries. 55 (SS12), 31-65.

117) Lin, Y. P.; Valentine, R. L. The release of lead from the reduction of lead oxide

(PbO2) by natural organic matter. Environ. Sci. Technol. 2008, 42, 760–765.

118) Lin, Y.P., Valentine, R.L., 2008. Release of Pb(II) from monochloramine-

mediated reduction of lead oxide (PbO2). Environmental Science and Technology 42

(24), 9137–9143.

119) Liu, H.Z., Korshin, G.V., Ferguson, J.F., 2009. Interactions of Pb(II)/Pb(IV) Solid

Phases with Chlorine and Their Effects on Lead Release. Environmental Science and

Technology 43 (9), 3278-3284.

120) Lytle, D.A., Gerke, T.L., Maynard, J.B., 2005. Effect of bacterial sulfate reduction

on iron corrosion scales. J Am Wat Works Assoc 97 (10), 109-120.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


121) Lytle, D.A., M.R. Schock, and K. Scheckel, 2009. The inhibition of Pb(IV) oxide

formation in chlorinated water by orthophosphate. Environ. Sci. Technol., 43 (17), 6624–

6631.

122) Lytle, D.A., Sorg, T.J., Frietch C., 2004. Accumulation of arsenic in drinking

water distribution systems. Environ. Sci. Technol., 38 (20), 5365-5372.

123) Lytle, D.A; Gerke, T.L; Maynard, J.B., 2005. Effect of bacterial sulfate reduction

on iron-corrosion scales. American Water Works Association Journal, 97: 109-120,12.

124) Manuel, C.M., Nunes, O.C., Melo, L.F., 2007. Dynamics of drinking water

biofilm in flow/non-flow conditions. Water Research 41 (3), 551-562.

125) McNeill, L.S., and M. Edwards, 2001. Iron Pipe Corrosion in Distribution

Systems. Journal American Water Works Association. 93: 88-100.

126) McNeill, L.S., and M. Edwards, 2002. Phosphate Inhibitor Use at US Utilities.

Journal American Water Works Association, 94: 57-63.

127) Melidis, P., Sanozidou, M., Mandusa, A., Ouzounis, K., 2007. Corrosion control

by using indirect methods. Desalination 213 (1-3), 152-158.

128) Momba, M.N.B., Kaleni, P., 2002. Re-growth and survival of indicator micro-

organisms on the surfaces of household containers used for the storage of drinking water

in rural communities of South Africa. Water Research 36 (12), 3023-3028.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


129) Morton, S. C., Zhang, Y., and M. Edwards, 2005. Implications of nutrient release

from iron metal for microbial regrowth in water distribution systems. Water Research, 39:

2883-2892.

130) Murdoch, F., Smith, P.G., 1999. Formation of manganese micro-nodules on water

pipeline materials. Water Research 33 (12), 2893-2895.

131) Murdoch, F., Smith, P.G., 2000. The interaction of a manganese-oxidising

bacterium as part of a biofilm growing on distribution pipe materials. Water Science and

Technology 41 (4-5), 295-300.

132) National Research Council (NRC), 2006. Drinking water distribution systems:

assessing and reducing risks. Committee on Public Water Supply Distribution Systems:

Assessing and Reducing Risks, National Research Council. The National Academies

Press, Washington DC, 1-405.

133) Nguyen, C.K., K.R. Stone and M. Edwards, 2011. Chloride to Sulfate Mass Ratio:

Practical Studies in Galvanic Corrosion of Lead Solder. J. AWWA 1:103 81-92.

134) Nguyen, C.K., Stone, K.R., Dudi, A., Edwards, M.A., 2010. Corrosive

microenvironments at lead solder surfaces arising from galvanic corrosion with copper

pipe. Environ. Sci. Technol., 44 (18), 7076-7081.

135) Niquette, P., Servais, P., Savoir, R., 2000. Impacts of pipe materials on densities

of fixed bacterial biomass in a drinking water distribution system. Water Research 34 (6),

1952-1956.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


136) Norton, C.D., LeChevallier, M.W., 2000. A pilot study of bacteriological

population changes through potable treatment and distribution. Applied and

Environmental Microbiology 66 (1), 268–276.

137) O’Toole, G.A., Kolter, R., 1998. Flagellar and twitching motility are necessary for

Pseudomonas aeruginosa biofilm development. Molecular Microbiology 30 (2), 295–

304.

138) Ohashi, A., Harada, H., 1996. A novel concept for evaluation of biofilm adhesion

strength by applying tensile force and shear force. Water Science and Technology 34 (5),

201–211.

139) O'Toole, G., Kaplan, H.B., Kolter, R., 2000. Biofilm formation as microbial

development. Annual Reviews of Microbiology 54, 49-79.

140) Parham, D.N., Tod, C.W., 1953. Condensed Phosphates in the Treatment of

Corrosive Waters. Chemistry and Industry 27, 628.

141) Park, S.R., Mackay, W.G., Reid, D.C., 2001. Helicobacter sp. recovered from

drinking water biofilm sampled from a water distribution system. Water Research 35(6),

1624-6.

142) Parks, J.L., McNeill, L., Frey, M., Eaton, A.D., Haghani, A., Ramirez, L.,

Edwards, M., 2004. Determination of total chromium in environmental water samples.

Water Research 38(12), 2827-2838.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


143) Pedersen, K., 1990. Biofilm development on stainless steel and PVC surfaces in

drinking water. Water Research 24 (2), 239–243.

144) Pekov, I.V., Perchiazzi, N., Merlino, S., Vyacheslav, N., Merlini, M., Zadov,

A.E., 2007. Chukanovite, Fe-2(CO3)(OH)(2), a new mineral from the weathered iron

meteorite Dronino. European Journal of Mineralogy 19 (6), 891-898.

145) Percival, S.L., Thomas, J.G., 2009. Transmission of Helicobacter pylori and the

role of water and biofilms. Journal of Water and Health 7 (3), 469–477.

146) Percival, S.L., Walker, J.T., Hunter, P.R., 2000. Microbiological Aspects of

Biofilms and Drinking Water. CRC Press, Florida. pp 240.

147) Peyton, B.M., Characklis, W.G., 1992. Kinetics of Biofilm Detachment. Water

Science and Technology26 (9-11), 1995-1998.

148) Potera, C., 1999. Forging a link between biofilms and disease. Science 283

(5409): 1837-1839.

149) Pratt, L.A., Kolter, R., 1998. Genetic analysis of Escherichia coli biofilm

formation: defining the roles of flagella, motility, chemotaxis and type I pili. Molecular

Microbiology 30 (2), 285-294.

150) Reiber, S., Dostal, G., 2000. Arsenic and old pipes-a mysterious liason: Well

water disinfection sparks surprises. Opflow 26, 1.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


151) Renner, R., 2008. Pipe scales release hazardous metals into drinking water.

Environmental Science and Technology 42 (12), 4241-4241.

152) Ridgway, H.F., Olson, B.H., 1981. Scanning electron microscope evidence for

bacterial colonization of a drinking-water distribution system. Applied and

Environmental Microbiology 41 (1), 274–287.

153) Rigal, S., and J. Danjou, 1999. Tastes and Odors in Drinking Water Distribution

Systems Related to the Use of Synthetic Materials. Water Science and Technology, 40:

203–208.

154) Rogers, J., Dowsett, A.B., Dennis, P.J., Lee, J.V., Keevil, C.W. 1994b. Influence

of plumbing materials on biofilm formation and growth of Legionella pneumophila in

potable water systems. Applied and Environmental Microbiology 60 (6), 1842-1851.

155) Rogers, J., Dowsett, A.B., Dennis, P.J., Lee, J.V., Keevil, C.W., 1994a. Influence

of temperature and plumbing material selection on biofilm formation and growth of

Legionella pneumophila in a model potable water system containing complex microbial

flora. Applied and Environmental Microbiology 60 (5), 1585-1592.

156) Ryder, R.A., 1980. The Costs of Internal Corrosion in Water Systems. Journal of

the American Water Works Association 72(5), 267-279.

157) Sadiki, A.I., 1998. A Study of Organotin Level in Canadian Drinking Water

Distributed through PVC Pipes. Chemosphere 38 (7), 1541–1548.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


158) Sarin, P., V.L Snoeyink, J. Bebee, W.M. Kriven, J.A. Clement, 2001. Physico-

chemical characteristics of corrosion scales in old iron pipes. Water Research, 35, 2961-

2969.

159) Satchwill, T.S., 1998. The impact of pipe coatings on drinking water quality.

Paper #3. 1998.

160) Schock, M. R. & Lytle, D. A. "Internal Corrosion and Deposition Control." Ch.20

in: Water Quality and Treatment: A Handbook of Community Water Supplies. J. K.

Edzwald, ed., McGraw-Hill, Inc., New York, (Sixth Ed., 2010).

161) Schock, M.R., 1980. Response of lead solubility to dissolved carbonate in

drinking-water. Journal of the American Water Works Association 72 (12), 695-704.

162) Schock, M.R., 1999. Internal corrosion and deposition control, Chapter 17. In:

Water Quality and Treatment (5th Ed.). Letterman, R.D., Ed.; McGraw-Hill, Inc. New

York, NY, 1999.

163) Schock, M.R., 2005. Distribution systems as reservoirs and reactors for inorganic

contaminants. Ch.6 In: Distribution System Water Quality, Challenges in the 21st

Century. MacPhee, M.J. ; Ed ; American Water Works Association, Denver, CO, 105-

140.

164) Schock, M.R., Gardels, M.C., 1983. Plumbosolvency reduction by high pH and

low carbonate – Solubility relationships. Journal of the American Water Works

Association 75 (2), 87-91.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


165) Schock, M.R., Hyland, R.N., Welch, M.M., 2008. Occurrence of contaminant

accumulation in lead pipe scales from domestic drinking-water distribution systems.

Environmental Science and Technology 42 (12), 4285-4291.

166) Schock, M.R., Wagner, I., Oliphant, R., 1996. The Corrosion and Solubility of

Lead in Drinking Water. In Internal Corrosion of Water Distribution Systems, 2nd ed.;

AWWA Research Foundation/ TZW: Denver, CO, 131–230.

167) Schwartz, T., Hoffmann, S., Obst, U., 1998. Formation and bacterial composition

of young, natural biofilms obtained from public bank-filtered drinking water systems.

Water Research 32 (9), 2787–2797.

168) Servais, P., Laurent, P., Randon, G., 1995. Comparison of the bacterial dynamics

in various French distribution systems. Journal of Water Supply Research and

Technology-Aqua 44, 10–17.

169) Silhan, J., Corfitzen, C.B., Albrechtsen, H.J., 2006. Effect of temperature and pipe

material on biofilm formation and survival of Escherichia coli in used drinking water

pipes: a laboratory-based study. Water Science and Technology 54 (3), 49-56.

170) Simoes, L.C., Simoes, M., Oliveira, R., Vieira, M.J., 2007. Potential of the

adhesion of bacteria isolated from drinking water to materials. Journal of Basic

Microbiology 47 (2), 174-183.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


171) Simon, L., Francois, M., Refait, P., Renaudin, G., Lelaurain, M., Genin, J.M.R.,

2003. Structure of the Fe(II-III) layered double hydroxysulphate green rust two from

Rietveld analysis. Solid State Science 5 (2), 327-334.

172) Smets, B.F., Grasso, D., Engwall, M.A., Machinist, B.J., 1999. Surface

physicochemical properties of Pseudomonas fluorescens and impact on adhesion and

transport through porous media. Colloids and Surfaces B: Biointerfaces 14 (1-4), 121-

139.

173) Smoot, L.M., Pierson, M.D., 1998. Influence of environmental stress on the

kinetics and strength of attachment of Listeria monocytogenes Scott A to Buna-N rubber

and stainless steel. Journal of Food Protection 61 (10), 1286-1292.

174) Snoeyink, V.L., Schock, M.R., Sarin, P., Wang, L., Chen, A.S.C., Harmon, S.M.,

2003. Aluminium-containing scales in water distribution systems: prevalence and

composition. Journal of Water Supply 52, 455-474.

175) Souza, J.C.M., Henriques, M., Oliveira, R., Teughels, W., Celis, J.P, Rocha, L.A.,

2010. Do oral biofilms influence the wear and corrosion behavior of titanium? Biofouling

26 (4), 471-478.

176) Stahl, K., Nielsen, K., Jiang, J.Z., Lebech, B., Hanson, J.C., Norby, P., van

Lanschot, J., 2003. On the akaganeite crystal structure, phase transformations and

possible role in post-excavational corrosion of iron artifacts. Corrosion Science 45 (11),

2563-2575.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


177) Stoodley, P., de Beer, D., Lappin-Scott, H.M., 1997. Influence of electric fields

and pH on biofilm structure as related to the bioelectric effect. Antimicrobial Agents and

Chemotherapy 41 (9), 1876-1879.

178) Stoodley, P., Wilson, S., Hall-Stoodley, L., Boyle, J.D., Lappin-Scott, H.M.,

Costerton, J.W., 2001. Growth and detachment of cell clusters from mature mixed-

species biofilms. Applied and Environmental Microbiology 67 (12), 5608–5613.

179) Storey, M.V., Långmark, J., Ashbolt, N.J., Stenström, T.A., 2004. The fate of

legionellae within distribution pipe biofilms: measurement of their persistence,

inactivation and detachment. Water Science and Technology 49(11-12), 269-275.

180) Stout, J.E., Yu, V.L., Best, M.G., 1985. Ecology of Legionella pneumophila

within water distribution systems. Applied Environmental Microbiology 49 (1), 221-8.

181) Stumm, W., 1956. Calcium Carbonate Deposition at Iron Surfaces. Journal of the

American Water Works Association 48 (3), 300.

182) Stumm, W., 1960. Investigation of the Corrosive Behavior of Waters. J ASCE

Sanitary Engineering Division 86 (SA6), 27.

183) Sutherland, I.W., 2001. The biofilm matrix – an immobilized but dynamic

microbial environment. Trends in Microbiology 9 (5), 222–227.

184) Świetlik, J., U. Raczyk-Stanisławiak, P. Piszora, J. Nawrocki, 2012. Corrosion in

drinking water pipes: The importance of green rusts. Water Research, 46, 1-10.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


185) Szewzyk, U., Szewzyk, R., Manz, W., Schleifer, K.H., 2000. Microbiological

safety of drinking water. Annual Reviews of Microbiology 54, 81–127.

186) Tendolkar, P.M., Baghdayan, A.S., Gilmore, M.S., Shankar, N., 2004.

Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis.

Infection and Immunity 72 (10), 6032–6039.

187) Triantafyllidou, S., Parks, J., Edwards, M., 2007. Lead particles in potable water.

Journal of the American Water Works Association 99 (6), 107-117.

188) Turakhia, M.H., Characklis, W.G., 1989. Activity of Pseudomonas aeruginosa in

biofilms: effect of calcium. Biotechnology and Bioengineering 33 (4), 406–414.

189) Uhlig, H.H., Revie, R.W., 1985. Corrosion and Corrosion Control. An

Introduction to Corrosion Science and Engineering. John Wiley and Sons, New York. pp

464.

190) United States Environmental Protection Agency (U.S. EPA), 1998.

Announcement of the Drinking Water Contaminant Candidate List: Notice. Federal

Register, Vol. 63 No. 40. US Government Printing Office, Washington DC: 10274–

10287. Available at http://water.epa.gov/scitech/drinkingwater/dws/ccl/ccl1.cfm

(Accessed on June 21st 2012).

191) United States Environmental Protection Agency (U.S. EPA), 2002. Analysis of

National Occurrence of the 1998 Contaminant Candidate List (CCL) Regulatory

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://water.epa.gov/scitech/drinkingwater/dws/ccl/ccl1.cfm

ACCEPTED MANUSCRIPT


Determination Priority Contaminants in Public Water systems. Office of Water. EPA

815-D-01-002. Washington, DC. 2002.

192) United States Government Accountability Office-GAO (U.S. GAO), 2011. Report

to congressional requesters. Drinking water - Unreliable state data limit EPA’s ability to

target enforcement priorities and communicate water systems’ performance. GAO-11-

381, June 2011, Washington, D.C., USA. Available at

http://www.gao.gov/new.items/d11381.pdf (Accessed on June 21st, 2012).

193) Van der Kooij, D., Veenendaal, H.R., 2001. Biomass production potential of

materials in contact with drinking water: method and practical importance. Water Science

and Technology 1 (3), 39–45.

194) van der Wende, E., Characklis, W.G., 1990. Biofilms in potable water distribution

systems. In: Drinking Water Microbiology: Progress and Recent Developments.

McFeters, G.A. ; Ed. ; Springer, New York. pp 249-268.

195) Van der Wende, E., Characklis, W.G., Smith, D.B., 1989. Biofilms and bacterial

drinking water quality. Water Research 23 (10), 1313–1322.

196) Van Loosdrecht, M.C.M., Lyklema, J., Norde, W., Schraa, G., Zehnder, A.J.B.,

1987. Electrophoretic mobility and hydrophobicity as a measure to predict the initial steps

of bacterial adhesion. Applied and Environmental Microbiology 53 (8), 1898–1901.

197) Vandevivere, P., Kirchman, D.L., 1993. Attachment stimulates exopolysaccharide

synthesis by a bacterium. Applied and Environmental Microbiology 59 (10), 3280-3286.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://www.gao.gov/new.items/d11381.pdf

ACCEPTED MANUSCRIPT


198) Verdonck, L., Hoste, S., Roelandt, F.F., Vanderkelen, G.P., 1982. Normal

coordinate analysis of alpha FeOOH- A molecular approach. Journal of Molecular

Structure 79 (1-4), 273-279.

199) Vikesland, P.J., R.L. Valentine, 2002. Iron oxide surface-catalyzed oxidation of

ferrous iron by monochloramine: implications of oxide type and carbonate on reactivity.

Enviorn. Sci. Technol., 36: 512-519.

200) Volk, C., Dundore, E., Schiermann J., LeChevallier, M., 2000. Practical

Evaluation of Iron Corrosion Control in a Drinking Water Distribution System. Water

Research 34 (6), 1967-1974.

201) Walch, M., 1992. Corrosion, microbial. In: Encyclopedia of Microbiology. (Vol.

1). Lederberg, J.; Ed.; Academic Press. New York, NY. pp. 585-591.

202) Wang, H., C. Hu, X. Hu, M. Yang, J. Qu, 2012a. Effects of disinfectant and

biofilm on the corrosion of cast iron pipes in a reclaimed water distribution system. Water

Research, 46, 1070-1078.

203) Wang, H., S. Masters, Y. Hong, J. Stallings, J.O. Falkinham, M.A. Edwards, and

A. Pruden, 2012b. Effect of Disinfectant, Water Age, and Pipe Material on Occurrence

and Persistence of Legionella, mycobacteria, Pseudomonas aeruginosa, and Two

Amoebas. Environ. Sci. Technol., 46: 11566–11574.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


204) Wang, Z., J. Kim, and Y. Seo, 2012. Influence of Bacterial Extracellular

Polymeric Substances on the Formation of Carbonaceous and Nitrogenous Disinfection

Byproducts. Environ. Sci. Technol., 46 : 11361–11369.

205) Water Infrastructure Network (WIN), 2000. Clean and Safe Drinking Water for

the 21st Century. A Renewed National Commitment to Water and Wastewater

Infrastructure. (Accessed at http://www.amsa-cleanwater.org/advocacy/

winreport/winreport2000.pdf (June 21st, 2012).

206) Watnick, P.I., Fullner, K.J., Kolter, R., 1999. A role for the mannose-sensitive

hemagglutinin in biofilm formation by Vibrio cholerae El Tor. Journal of Bacteriology

181(11), 3606–3609.

207) World Health Organization (WHO)/ National Science Foundation (NSF), 2003.

Heterotrophic plate counts and drinking-water safety: the significance of HPCs for water

quality and human health. Bartram, J., Cotruvo, J., Exner, M., Fricker, C., Glasmacher,

A., 2003. Available at: http://www.nsf.org/conference/hpc/hpc_proceedings.html

(Accessed on June 21st, 2012).

208) WHO/UNICEF, 2012. World Health Organization and UNICEF Joint Monitoring

Programme for Water Supply and Sanitation. Progress on drinking water and sanitation

report, 2012. Washington, D.C, USA.

209) Wingender, J., Flemming, H.C., 2004. Contamination potential of drinking water

distribution network biofilms. Water Science and Technology 49 (11-12), 277-286.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


210) Wingender, J., Flemming, H.C., 2011. Biofilms in drinking water and their role as

reservoir for pathogens. International Journal of Hygiene and Environmental Health

214(6), 417-23.

211) Wingender, J., Neu, T.R., Flemming, H.C., 1999. What are bacterial extracellular

polymeric substances? In: Wingender, J.; Neu, T.R.; Flemming, H.C.; Eds.; Microbial

extracellular polymeric substances: characterization, structure and function. Berlin:

Springer. pp 1-19.

212) World Health Organization (WHO), 2007. Legionella and the prevention of

legionellosis. Bartram, J., Chartier, Y., Lee, J. V., Pond, K., Surman-Lee, S. (eds).

Geneva, Switzerland. 2007.

213) World Health Organization (WHO), 2009. Global health risks, Mortality and

burden of disease attributable to selected major risks. Geneva, Switzerland.

214) World Health Organization (WHO)/ National Science Foundation (NSF), 2003.

Heterotrophic plate counts and drinking-water safety: the significance of HPCs for water

quality and human health. Bartram, J., Cotruvo, J., Exner, M., Fricker, C., Glasmacher,

A., 2003. Available at: http://www.nsf.org/conference/hpc/hpc_proceedings.html

(Accessed on June 21, 2012).

215) Wulff, N.A., Mariano, A.G., Gaurivaud, P., de Almeida Souza, L.C., Virg´ılio,

A.C., Monteiro, P.B., 2008. Influence of culture medium pH on growth, aggregation, and

biofilm formation of Xylella fastidiosa. Current Microbiology 57, 127–132.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

http://www.nsf.org/conference/hpc/hpc_proceedings.html

ACCEPTED MANUSCRIPT


216) Xie, Y., D. E. Giammar, 2011. Effects of flow and water chemistry on lead release

rates from pipe scales. Water Research, 45, 6525-6534.

217) Yang, F., B. Shi, J. Gu, D. Wang, M. Yang, 2012. Morphological and

physicochemical characteristics of iron corrosion scales formed under different water

source histories in a drinking water distribution system. Water Research, 46, 5423-5433.

218) Yoder, J., Roberts, V., Craun, G.F., Hill, V., Hicks, L., Alexander, N.T., Radke,

V., Calderon, R.L., Hlavsa, M.C., Beach, M.J., Roy, S.L., 2008. Surveillance of water

borne disease and outbreaks associated with drinking water and water not intended for

drinking-United States, 2003-2004. Center for diseases control, Atlanta, GA, USA.

Morbidity and mortality weekly report-Surveillance summaries. 57 (SS09), 39-62.

219) Zacheus, O.M., Iivanainen, E.K., Nissinen, T.K., Lehtola, M.J., Martikainen, P.J.

2000. Bacterial biofilm formation on polyvinyl chloride, polyethylene and stainless steel

exposed to ozonated water. Water Research 34 (1): 63-70.

220) Zacheus, O.M., Lehtola, M.J., Korhonen, L.K., Martikainen, P.J., 2001. Soft

deposits the key site for microbial growth in drinking water distribution networks. Water

Research, 35 (7), 1757–1765.

221) Zaitlina, B., S.B. Watson, 2006. Actinomycetes in relation to taste and odour in

drinking water: Myths, tenets and truths. Water Research, vol.40, 6, 1741–1753.

222) Zhang, Y., A. Griffin, and M. Edwards, 2010. Effect of Nitrification on Corrosion

of Galvanized Iron, Copper and Concrete. Journal AWWA 102(4) 83-93.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


223) Zhang, Y., and M. Edwards, 2009. Accelerated chloramine decay and microbial

growth by nitrification in premise plumbing. Journal AWWA, 101(11) 51-62.

224) Zhang, Y., Griffin, A., Rahman, M., Camper, A., Baribeau, H., Edwards, M.,

2009. Lead contamination of potable water due to nitrification. Environ. Sci. Technol., 43

(6), 1890-1895.

225) Zhou LL, Zhang YJ, Li GB. 2009. Effect of pipe material and low level

disinfectants on biofilm development in a simulated drinking water distribution system. J

Zhejiang Univ Science A 10 (5): 725-731.

226) Zimmerman JB, Mihelcic JR, Smith JA. 2008. Global stressors on water quality

and quantity. Environ. Sci. Technol., 42 (12): 4247-4254.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


“PIPE TO TAP”

Figure 1: Schematic depicting the various types of historically formed pipe scales and biofilms

in urban drinking-water distribution systems. Pipe and scale conglomerates may act either as

sinks or sources for water contaminants. Factors and processes that induce the episodic release of

chemicals and/or microorganisms into finished water (pipe to tap) are poorly understood.

Free contaminants (C)

Scales (S)

Urban Drinking Water Distribution Pipe Inner Surface

Released Products

Sorbed contaminants

with scales and biofilm

(SBC)

Chemical and / or Pathogen Destabilization and Release to Tap Water

Biofilm (B)

B C S SC

SBC

BC

“PIPE TO TAP”

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Research questions about the nature and type of released chemical and biological products in

water; the stability and transport of released products into finished water; the magnitude and

variability of human exposures to free and particulate water contaminants present in finished

water reaching households; the bioaccessibility of such particulate contaminants in the human

gastrointestinal phase; and the combined acute or chronic health effects on disease process are all

topics that warrant attention by the scientific community.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Table 1. Selected examples of different pipe scales and biofilm types found in UDWDS and their structural characterization

techniques.

Nature Identification

technique/technology

Pipe material Characterization Reference(s)

Scales 1. TEM (transmission electron

microscopy)

Iron α-FeOOH and Fe(OH)3 (n

H2O) in corrosion products

Borch et al, 2008

2. GID-XRD (grazing incident

diffractometry and X-ray

powder diffractometry)

Iron α-FeOOH and Fe3O4; minor

phase- γ-FeOOH; and

probable phases –green rust

and CaCO3

Borch et al, 2008

3. TMS (transmission

Mössbauer spectroscopy),

micro-Raman spectroscopy (μ-

RS), SEM-EDS and XRD

Galvanized low carbon steel Outer and inner side chemical

composition of corrosion

tubercles show Zn and Fe

compounds

Carbucicchio et al., 2008

4. XRF (X-ray fluorescence

spectrometer)

Steel Chemical composition of the

corrosion material

Lin et al., 2001

5. SM (stereomicrography),

SEM (scanning electron

microscopy), and XRD

Copper Copper pit membranes and pit

contents

Lytle and Nadagouda, 2010

6.SEM-EDS (scanning

electron microscopy- Energy

Iron Goethite, magnetite,

maghemite, siderite and

Sarin et al., 2004

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


dispersive X-ray spectroscopy)

and XRD

unidentified iron components

7. XPS-EIS (X-ray

photoelectron spectroscopy

after electrochemical

impedance spectroscopy)

Copper Cuprous oxides, cupric oxides,

and cupric hydroxide species

Shim and Kim, 2004

8. XRD (X-ray powder

diffractometry)

Cast iron Goethite, maghemite,

hematite, aragonite and calcite

Teng et al., 2008

Elemental 1. SEM-EDS Iron Iron and sulfur presence in

corrosion products

Borch et al, 2008; Sarin et al.,

2004

2. XPS Copper Elemental composition of

copper pits

Edwards et al., 2004

3. AAS (atomic absorption

spectrometry)

Steel Presence of iron in the

corrosion material

Lin et al., 2001

4. SEM-EDS

PVC and HDPE Manganese and oxygen

presence in the micro-nodules

on the pipe surface

Murdoch and Smith, 1999 and

2000

5. ICP-OES (inductively

coupled plasma atomic

emission spectroscopy)

Lead Forty elements in corroded

lead pipes

Schock et al., 2008

6.ICP-MS (inductively

coupled plasma mass

spectrometry)

Lead Rare earth elements and

silicon in corroded lead pipes

Schock et al., 2008

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


7. CV-AAS (continuous flow-

cold vapor atomic

absorption spectrometry)

Lead Mercury in corroded lead

pipes

Schock et al., 2008

8. Combustion furnace Lead Total sulfur and total carbon in

corroded lead pipes

Schock et al., 2008

Biofilms 1. SEM (scanning electron

microscopy)

Stainless steel (a), Rubber (b) Bacterial morphology and

characterization

(a) Gamby et al., 2008; (b)

Kilb et al., 2003

2. Epifluorescent microscopy

and fluorescence in-situ

hybridization

polyethylene (PE) Study changes in pidemio

community structure over time

Deines et al., 2010

3. TM-AFM (tapping mode –

atomic force microscopy)

Stainless steel Imaging bacterial colonies Gamby et al., 2008

4. PM-IRRAS (polarization

modulation infrared reflection

absorption spectroscopy)

Stainless steel Bacterial species diversity

based on infrared spectra

Gamby et al., 2008

5. RDE (rotating disk

electrode – electrochemical

method)

Stainless steel Determine variation in

pidemio thickness

Gamby et al., 2008

6. PEPA (potential

exoproteolytic activity)

Polyvinylchloride (PVC),

cemented steel, cemented cast

iron, asbestos-cement,

polyethylene pipe material

Density of the attached

bacterial biomass

Niquette et al., 2000

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


7. PCR-DGGE (Polymerase

chain reaction – Denaturing

gradient gel electrophoresis)

Cast iron pipe DNA based profiling suggests

occurrence of iron reducing

bacteria viz., Leptospirillum

ferriphilum and Leptospirillum

ferrooxidans

Teng et al., 2008

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Table 2. Examples of scales and biofilms coexistence in drinking water distribution pipes

Scale(s) Biofilm(s) Pipe material Highlight

information

Reference(s)

1. Copper pits Sulphate reducing

bacteria and fungi such

as Alcaligenes,

Achromobacter,

Flavobacterium,

Methylobacterium,

Pseudomonas and

Sphingomonas species

(a); and microbial

heterotrophic species

with thermotolerance

and copper tolerance at

high temperatures such

as Sphingomonas

paucimobilis and

Pseudomonas

solanacearum (b)

Copper pipe Copper pitting

induced by microbial

biofilms observed in

Scotland (a) and

Germany (b) pipes

(a) Keevil et al., 1989

(b) Chamberlain and

Angell, 1990

2. Zinc-galvanized steel

corrosion tubercles

Gram-negative aerobic

bacteria such as

Pseudomonas spp.,

Afipia spp., Rubritepida

flocculans, Bacillus

pumilus, Blastobacter

Denitrifican, and

Bradyrhizobium

Galvanized steel Observed corrosion

and pitting of a

galvanized steel pipe

in an aerobic water

distribution system in

Melbourne, Australia

due to the bacterial

biofilms

Bolton et al., 2010

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


japonicum.

3. Copper corroded

surface

Acidovorax delafieldii Copper pipe Increased copper

concentrations in

water due to microbial

induced copper

corrosion in Adelaide,

Australia

Critchley et al., 2001

4. Iron tubercles Coliform bacteria such

as Escherichia coli,

Corynebacterium

freundii, and

Enterobacter

agglomerans

Bituminous-coated,

cement-lined cast iron

Drinking water

quality deterioration

with coliform bacteria

that was otherwise not

present in water

leaving the treatment

facilities in New

Jersey, USA.

LeChevallier et al.,

1987

5. Manganese micro-

nodules

Manganese pidemiol

Pseudomonas spp

Polyvinylchloride

(PVC) and high-

density polyethylene

(HDPE) pipe

Bacterial association

with the Mn nodule

formation on the pipe

surfaces

Murdoch and Smith,

1999 and 2000

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Table 3. Non-exhaustive list of contaminants from scales and biofilms in drinking water distribution systems.

# Pipe material Contaminant Concentration(s)

range

Treatment/Clean

-up procedure

Concentration

after clean-up

Comments Reference(s)

Inorganic contaminants from scales or corroded pipe parts

1. Copper Copper 500- 1,000 mg/L NA NA Blue water

phenomenon

Edwards et al.,

2000

2. Not specified Copper 0.26 mg/L 10 min flush 0.068 mg/L Flush removes

accumulated

contaminants

Murphy 1993

3. Copper Copper 1 mg/L Orthophospha

te

stabilization

(1 mg/L)

Cu concentrations

reduced by 43 -90

% depending on

pipe age, Ph, and

alkalinity

Orthophosphate

reduced dissolved

Cu levels by

forming cupric

phosphate scale

Edwards et al.,

2002

4. Lead Several

elements

present in the

All concentrations are

given in mg/kg lead pipe

NA NA Pipe scales

accumulate and

concentrate

Schock et al.,

2008

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


lead pipe scales scale:

As (87 ± 88),

Cd (28 ± 55),

Cr (83 ± 156),

Hg (0.33 ± 0.44), Ba (199

± 368), Bi (422 ± 417),

Ni (129 ± 242), Cu (3404

± 6335), S (1202 ±

1054), Sn (1129 ± 1741),

Zn (2616 ± 5705),

V (1729 ± 3208),

Al (11366 ± 11258)

Fe (44722 ± 79393)

Mn (17451 ± 33148)

Pb (530615 ± 192414)

contaminants to

get released into

the drinking water

5. Not specified Lead 0.01 mg/L 10 min flush 0.005 mg/L Flush removes

accumulated

contaminants

Murphy 1993

6. Lead Lead 0.024 mg/L Flush 0.006 mg/L Flush appears to

remove Pb

Fertmann et al.,

2004

7. Cast-iron Iron 1.8 mg/L Orthophospha

te addition at

3 mg/L

Fe levels

decreased

Orthophosphate

sorbs iron and

reduces iron

Lytle et al., 2005

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


dissolution

Microbial contaminants

1. Cast iron Broad range of

microbes in

biofilms formed

on the inner pipe

surfaces and

coliform bacteria

Total cell count

(TCC): 6.7 x 106

to 5.8 x 107

cells/cm2,

heterotrophic

plate count

(HPC): 2.5 x 102

to 3.8 x 105

cfu/cm2, and

coliforms: ND

NA NA Age of the pipes

samples: 2-99 yrs;

Number of

drinking water

distribution pipes

sampled: 9;

Country of

sampling:

Germany

Wingender and

Flemming, 2004

2. Cement-lined Broad range of

microbes in

biofilms formed

on the inner pipe

surfaces and

coliform bacteria

TCC: 3.0 x 105 to

8.0 x 105

cells/cm2,

HPC: 1.5 x 102 to

1.2 x 101 cfu/cm

2,

and coliforms:

0.04-ND cfu/cm2


samples: 8-20 yrs;

Number of

drinking water

distribution pipes

sampled: 2;

Country of

sampling:

Germany

Wingender and

Flemming, 2004

3. Galvanized steel Broad range of

microbes in

biofilms formed

on the inner pipe

surfaces and

coliform bacteria

TCC: 2.0 x 108

cells/cm2,

HPC: 1.2 x 105

cfu/cm2, and

coliforms: ND


samples: 10 yrs;

Number of

drinking water

distribution pipes

sampled: 1;

Wingender and

Flemming, 2004

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Country of

sampling:

Germany

4. PVC Broad range of

microbes in

biofilms formed

on the inner pipe

surfaces and

coliform bacteria

TCC: 1.3 x 106 to

1.6 x 107

cells/cm2,

HPC: 3.0 x 101 to

7.8 x 103 cfu/cm

2,

and coliforms:

ND


samples: 12-34

yrs; Number of

drinking water

distribution pipes

sampled: 5;

Country of

sampling:

Germany

Wingender and

Flemming, 2004

5. Cast iron and

cement-lined

Broad range of

microbes in

biofilms formed

on the inner pipe

surfaces and

coliform bacteria

TCC: 6.1 x 106

cells/cm2,

HPC: 2.0 x 105

cfu/cm2, and

coliforms: ND


samples: 37 yrs;

Number of

drinking water

distribution pipes

sampled: 1;

Country of

sampling:

Germany

Wingender and

Flemming, 2004

6. Rubber-coated

pipe values

Emphasis on

coliform bacteria

in biofilms

TCC: 2.7 x 106 to

1.8 x 109

cells/cm2,

HPC: 3.0 x 105 to

5.4 x 109 cfu/cm

2,

and coliforms: 1.0

– 4.7 x 103

(MPN/cm2)


samples: 3 weeks

to 4 yrs; Number

of drinking water

distribution

systems sampled:

6; Country of

sampling:

Germany

Kilb et al., 2003

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


7. Copper (a) and

plastic

(polyethylene-

aluminum-

polyethylene) (b)

Total bacteria Copper pipe (a):

Total bacteria –

1.6 x 106

bacteria/cm2 and

HPC – 1.0 x 105

cfu/cm2; and

plastic pipe (b):

Total bacteria –

4.5 x 106

bacteria/cm2 and

HPC – 5.0 x 105

cfu/cm2

NA NA Pipe material (a

and b) influences

bacteria

population in

biofilms

Lehtola et al.,

2004

8. Galvanized steel Escherichia coli

in the biofilm

E. coli HPC: 0.5 x

106

cfu/cm2

Heating to 35°C E coli HPC: 0.5 x

105

cfu/cm2

Higher

temperature

reduced E. Coli

survival

Silhan et al., 2006

9. Plastic Legionella spp Legionella count

in the influent:

1.34 x 105

cfu/ml

Copper-carbon

filter (a) and

Copper and silver-

carbon filter (b)

Legionella count

in the effluent:

Copper-carbon

filter (a) -1.26 x

104

cfu/ml, and

Copper and silver-

carbon filter (b) –

4.48 x 103

cfu/ml

Copper and silver-

carbon filter is

more effective in

reducing

Legionella

contamination

Molloy et al.,

2008

Table 4. Exposure sources of chemicals and pathogens including public health concerns with their occurrence in urban

drinking-water distribution systems.

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Contaminant Pipe material Country Exposure Source Public health

concern(s)

Drinking water

regulation(s)

Reference(s)

Pipe scales

1. Copper Copper USA Elevated drinking

water copper

levels in newly

constructed and

remodeled homes

in Wisconsin,

USA.

Copper in

drinking water

above 3 mg/L

induced nausea,

vomiting, diarrhea

and stomach

cramps (a), and

off-flavored water

affecting the

aesthetics (b)

USEPA standard:

1.3 mg/L (c)

Knobeloch et al.,

1998 (a); AWWA,

2006 (b); USEPA,

1991 (c)

2. Copper Copper Germany (a),

Holland (b), and

Canada (b)

Tap water

consumption(c)

Gastrointestinal

problems at acute

levels as high as

>30 mg/L (e), and

possible death

above >1 g/L (f)

WHO standard: 2

mg/L (g),

European Union:

2 mg/L (h)

Zietz et al., 2003

(a); WHO 2003

(b); Dietrich et al.,

2004 (c); Pandit

and Bhave, 1996

(e); NRC, 2000

(f);

3. Lead PVC,

polypropylene,

Egypt (a) Tap water show

Pb levels great

Range of

symptoms form

WHO standard for

Pb in drinking

Lasheen et al., 208

(a); Godwin 2001

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


and galvanized

iron

than WHO

recommendation

anemia to nervous

system

degeneration (b)

water is

10µg/L(c);

Maximum

allowable lead

extraction level

from PVC pipes is

5µg/L (d)

(b); WHO 2004

(c); Mitchener

2004 (d)

4. Lead Lead Germany (a,b) Tap water 6.5% of the study

drinking water

samples have > 10

µg/L (WHO limit)

and 2.8% had >25

µg/L (Germany’s

current limit)

(25 µg/L) (a,b).

WHO standard:

10µg/L (c),

Germany

standard: 25µg/L

(d)

Zietz et al. 2007

(a), Zietz et al.

2010 (b), WHO

2003 (c), TrinkwV

2001 (d)

5. Lead Lead USA (a) Tap water Water lead levels

are proportional to

children blood

lead levels in the

Washington DC

area, USA (a)

WHO standard:

10µg/L (b)

Edwards et al.,

2009 (a); WHO

2004 (b)

6. Aluminum Cement pipes USA Drinking water Al levels were as

high as 700 mg/L.

Resulted in death

of 9 dialysis

patients in Curaco

(a)

MCL: 0.05-0.2

mg/L (b)

Berend and

Trouwborst, 1999

(a); USEPA 2003

(b)

7. Vinyl chloride PVC USA Drinking water 8.9 mg/L when

tested. The

MCL: 0.002 mg/L

(b)

Fluorney et al.,

1999 (a);

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


leaching went up

to 280-410 mg/L

at temperatures

above 50°F (a).

http://www.epa.go

v/safewater/conta

minants/basicinfor

mation/vinyl-

chloride.html (b)

8. Organotin PVC Canada Drinking water Organotin levels

increased with

time and distance

traveled in the

distribution pipe

systems (a). Also

organotin was

reported to

accumulate in

blood and liver (b)

USEPA placed

organotin on the

drinking water

contaminant

candidate list

(CCL)

Sadiki, 1998 (a);

Takahashi, 1999

(b)

Pipe biofilms

1. Acanthamoeba

keratitis (amoeba)

Drinking water

distribution pipe

UK Tap water 90% of the water

samples contained

this pathogen.

Severe eye

infection in those

who wear contact

lens, and

sometimes may

lead to blindness.

Not regulated yet Kilvington et al.,

2004

2. Acanthamoeba Drinking water Chicago, USA Tap water Forty-four cases in Not regulated yet Joslin et al., 2006

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


keratitis (amoeba) distribution pipe 2.5 years

3. Legionella Copper

distribution pipe

New York, USA Tap water Infections of the

central nervous

system and eye in

humans.

USEPA has

not set a limit

for Legionella

yet, but is

monitored as a

drinking water

contaminant

Marciano-Cabral,

2010;

USEPA

(http://www.epa.g

ov/safewater/cont

aminants/index.ht

ml#3)

4. Cryptosporidium Drinking water

distribution pipe

Milwaukee, USA Tap water 403,000 cases

showing

gastrointestinal

illness symptoms

such as diarrhea,

vomiting, cramps

Maximum

Contaminant

Level Goal

(MCLG): zero

MacKenzie et al.,

1994; USEPA

(http://www.epa.g

ov/safewater/cont

aminants/index.ht

ml#3)

Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

ACCEPTED MANUSCRIPT


Dow

nloa

ded

by [

Mos

kow

Sta

te U

niv

Bib

liote

] at

06:

28 1

3 Ja

nuar

y 20

14

Documents

Pipe Scales and Biofilms in Drinking-Water Distribution Systems: Undermining Finished Water Quality