Environ. Sci. Technol. 2006, 40, 6799-6804
Removal of Two Waterborne Pathogenic Bacterial Strains by Activated Carbon Particles Prior to and after Charge Modification H E N K J . B U S S C H E R , †,‡ RENE J. B. DIJKSTRA,† EEFJE ENGELS,† DON E. LANGWORTHY,§ D I M I T R I S I . C O L L I A S , || DAVID W. BJORKQUIST,§ M I C H A E L D . M I T C H E L L , || A N D H E N N Y C . V A N D E R M E I * ,† Department of Biomedical Engineering, University Medical Center Groningen and University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands, SASA BV, G.N. Schutterlaan 4, 9797 PC Thesinge, The Netherlands, Health Care Research Center, The Procter & Gamble Company, 8700 Mason-Montgomery Road, Cincinnati, Ohio, and Corporate R&D, The Procter & Gamble Company, 8611 Beckett Road, West Chester, Ohio
Waterborne diseases constitute a threat to public health despite costly treatment measures aimed at removing pathogenic microorganisms from potable water supplies. This paper compared the removal of Raoultella terrigena ATCC 33257 and Escherichia coli ATCC 25922 by negatively and positively charged types of activated carbon particles. Both strains display bimodal negative ζ-potential distributions in stabilized water. Carbon particles were suspended to an equivalent external geometric surface area of 700 cm2 in 250 mL of a bacterial suspension, with shaking. Samples were taken after different durations for plate counting. Initial removal rates were less elevated for the positively charged carbon particle than expected, yielding the conclusion that bacterial adhesion under shaking is mass-transport limited. After 360 min, however, the log-reduction of the more negatively charged R. terrigena in suspension was largest for the positively charged carbon particles as compared with the negatively charged ones, although conditioning in ultrapure or tap water of positively charged carbon particles for 21 days eliminated the favorable effect of the positive charge due to counterion adsorption from the water. Removal of the less negatively charged E. coli was less affected by aging of the (positively charged) carbon particles, confirming the role of electrostatic interactions in bacterial removal by activated carbon particles. The microporous, negatively charged coconut carbon performed less than the mesoporous, positively charged carbon particle prior to conditioning but did not suffer from loss of effect after conditioning in ultrapure or tap water. * Corresponding author phone: +31 503633140; fax: +31 50363159; e-mail:
[email protected]. † University Medical Center Groningen and University of Groningen. ‡ SASA BV. § Health Care Research Center, The Procter & Gamble Co. || Corporate R&D, The Procter & Gamble Co. 10.1021/es061282r CCC: $33.50 Published on Web 09/22/2006
2006 American Chemical Society
Introduction Waterborne diseases constitute a threat to public health in many if not all parts of the world, despite a large number of regulations and preventive measures aimed at removing pathogenic microorganisms from potable water supplies (1). There are many rural areas where people rely on untreated and unmonitored private groundwater supplies (2). In spite of improvements in water treatment methods, outbreaks continue to occur. There is much concern in the drinking water industry with emerging pathogens such as Cryptosporidium, Giardia, norovirus, rotavirus, non-tuberculous mycobacteria, Yersinia, Campylobacter, Legionella and Escherichia coli O157:H7 (3-5). Disinfectants that are most often used for microbial decontamination of potable water supplies frequently disappoint consumer’s expectations due to the low aesthetic (taste) quality of these treated waters. Additionally, chlorine and associated disinfection byproducts such as trihalomethanes have been associated with toxicity and carcinogenicity (1, 6). One major potential source of post-treatment microbial recontamination in potable water systems are biofilms that grow on the surfaces within the water distribution system and episodically detach. This detachment or shedding is an irregular process that can be absent for prolonged periods of time and then occur suddenly after monitoring of the water quality. Additional health impacts in certain settings can even make the microbial contamination problem worse. For instance, microbial accumulation through adhesion and growth in dental water unit lines constitute, according to some, a public health risk (7, 8). Particularly troublesome in this respect is that microorganisms in these biofilms are far less susceptible to disinfectants than organisms in a planktonic state, and reports of disinfection failure with chlorine continue to emerge (9, 10). Other water purification methods involve the use of activated carbons in filtration devices to remove waterborne pathogens (11, 12). Microorganisms attach to activated carbon particles through strong Lifshitz-van der Waals forces by overcoming electrostatic repulsion between negatively charged cells and carbon surfaces (13). Especially in low ionic strength systems such as potable water systems, electrostatic repulsion can be sizable. The low ionic strength environment of potable water systems at the same time offers possibilities to enhance the efficacy of activated carbons to remove microorganisms from water by charge modification of the carbon surfaces. Once made positively charged, the electrostatic attraction between negatively charged microbial cell surfaces and positively modified carbon particles will be strong (14). The stability of positively charged surfaces is generally low, however, and in many natural environments, macromolecular adsorption and adsorption of negatively charged counterions rapidly neutralizes the positive charge created on a surface (15). It is not known whether this conditioning film formation (16) also occurs in potable water systems and, if it does, whether it influences microbial removal by positively charged, activated carbons. Therefore, this paper compares microbial removal by different activated carbon particles, including a positively VOL. 40, NO. 21, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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charged carbon type, prior to and after conditioning in ultrapure and tap water.
Materials and Methods Strains and Culture Conditions. Two strains were chosen as surrogates for microbial contamination in water distribution systems, Raoultella terrigena ATCC 33257 and E. coli ATCC 25922. R. terrigena ATCC 33257 was cultured in nutrient broth (OXOID, Basingstoke, Great Britain) and E. coli ATCC 25922 in tryptone soya broth (OXOID, Basingstoke, Great Britain) at 37 °C in ambient air. R. terrigena was isolated from a drinking water distribution system and the E. coli strain was a clinical isolate. For each experiment, a preculture was inoculated from agar in broth and cultured for 24 h. A second culture was inoculated and grown for 16 h. Bacteria were harvested by centrifugation (5 min at 10 000g) during the stationary phase, washed twice with ultrapure water (i.e., tap water filtrated through an ultrapure cartridge kit, Millipore Corp., Bedford, MA; specific conductivity better than 0.05 µS) and resuspended in stabilized water. For stabilization, the water was very weakly buffered with 0.00025 M KH2PO4/K2HPO4, yielding an ionic strength of 0.001 M and pH 6.8. We have chosen pH 6.8, because the pH of most tap waters is around 7, in order to avoid corrosion of the water pipelines. Bacterial Cell Surface Characterization. For ζ-potential measurements, each bacterial strain was resuspended in 50 mL of stabilized water (see above) to a density of approximately 1 × 107 cells per mL. The electrophoretic mobility of each sample was measured at 150 V using a Lazer Zee Meter 501 (PenKem, Bedford Hills, NY), equipped with image analysis options for ζ-sizing. The mobility of the bacteria under the applied voltage was converted to an apparent ζ-potential using the Helmholtz-Smoluchowski equation. The ζ-potentials were measured in triplicate with separately cultured bacteria. Contact angles were determined with water, formamide, methyleneiodine, and R-bromonaphthalene using the sessile drop technique (17). Briefly, bacteria were resuspended in demineralized water and deposited onto a 0.45 µm pore size filter (Millipore) using negative pressure. A lawn of approximately 50 stacked layers of bacteria (determined by using a fixed amount of bacterial suspension) was produced on the filter. The filters were left to air-dry (approximately 30 min) at room temperature and humidity until so-called “plateau water contact angles” could be measured. Droplets of 0.5-1.0 µL were put by a syringe on the partly dried bacterial lawns and droplet contours were determined using a CCD camera and homemade image analyzer, from which contact angles were calculated. For each strain, contact angles were measured in triplicate with separately cultured bacteria. Carbon Particles. A basic wood-based activated carbon, RGC (MeadWestvaco Corp., Carbon Department, Covington, VA); an acidic wood-based activated carbon, CA-10 (Carbochem, Inc., Ardmore, PA); and coconut carbon (Calgon Carbon Corp., Pittsburgh, PA) were used as received, while Celite Hyflo diatomaceous earth (DE) (World Minerals, Inc., Santa Barbara, CA) was used as a negative control (no adhesion expected). RGC was furthermore coated with polyvinyl amine (PVAM) to a level of about 4-5% (w/w) as measured by thermogravimetric analysis. CA-10 and RGC are carbon particles with a total pore volume of around 1.26 mL/g and a volume of pores with diameter larger than 2 nm of about 0.64 mL/g. Coconut carbon (total pore volume 0.77 mL/g) had a volume of pores with diameter larger than 2 nm of about 0.15 mL/g. On the basis of the pore volumes, coconut carbon can be classified as microporous, and all other carbons used are mesoporous. Coating the RGC carbon with PVAM did not affect the mesoporous character of the carbon 6800
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particles. Scanning electron micrographs of the particles are given in Figure 1. Carbon particles were sieved upon receipt to obtain a fraction with size between 25 and 50 µm. The actual particle size distributions were obtained using the Mastersizer by Malvern Instruments Ltd (Malvern, U.K.), yielding the external geometric surface areas: Celite Hyflo DE, 1.7 cm2/ mg; CA-10, 4.8 cm2/mg; RGC, 5.0 cm2/mg; RGC + PVAM, 3.9 cm2/mg; and coconut, 2.3 cm2/mg. Experiments were done with carbon particles prior to and after conditioning film formation for an arbitrarily chosen 21 days in ultrapure or tap water (composition of tap water in Groningen, The Netherlands: DOC, 3.8 mg/L; Ca, 55 mg/L; K, 2.9 mg/L; Mg, 5.6 mg/L; Na, 22.2 mg/L; Cl, < 0.1 mg/L; and trace elements; pH 7.7). In order to condition the particles, an amount of particles with a total external geometric surface area equivalent to 700 cm2 was suspended in 250 mL of the appropriate water and left under slight agitation at room temperature. X-ray Photoelectron Spectroscopy on Activated Carbon Particles. Chemical surface compositions of the carbon particles were measured using X-ray photoelectron spectroscopy (XPS). Carbon particles prior to and after conditioning, were deposited on double-sided sticky tape fixed on a XPS sample holder and transferred into the XPS chamber (Surface Science Instruments, S-Probe, Mountain View, CA). X-ray production (10 kV, 22 mA) at a spot size of 250 µm × 1000 µm occurred using an aluminum anode. Scans were made of the overall spectrum in the binding energy range of 1-1100 eV at low resolution (pass energy 150 eV). The area under each peak was used to calculate peak intensities, yielding elemental surface concentrations, after correction with sensitivity factors provided by the manufacturer. Adhesion Experiments. Carbon particles were suspended in 250 mL of the bacterial suspension (5 × 105 bacteria per mL) in stabilized water to a concentration equivalent to an external geometric surface area of 700 cm2 for each carbon type. The resulting suspension was left to incubate at room temperature, while being shaken just sufficiently to prevent sedimentation of the carbon particles. Ten-milliliter aliquots were taken after 0, 30, 60, 120, 240, and 360 min. Carbon particles in the aliquots were allowed to settle for 10 min before plating to prevent carbon particle contamination on the agar during culturing. Serial dilutions were made and plated on agar plates that were incubated at 37 °C for 16 h. The colony forming units (cfu) were counted, yielding the number of bacteria left in suspension, and the number of cfu removed by the carbon particles was calculated. An initial removal rate (cfu cm-2 s-1) was determined by linear regression analysis of the number of free bacteria in suspension versus time (s) for each activated carbon particle over the first 120 min. In addition, the number of bacteria present in the suspension after 360 min was determined and compared with the initial concentration to yield a logreduction per liter at 360 min. Experiments were done with carbon particles prior to and after conditioning film formation. All experiments were done in triplicate with separately cultured strains and differences analyzed for statistical significance by a paired Student t-test.
Results On the basis of the contact angle measurements, the cell surfaces of both strains involved in this study are hydrophilic, as shown by their low water and formamide contact angles, while their apolar surface properties are nearly equal, as judged from the methyleneiodine and R-bromonaphthalene contact angles (see Table 1) (18). R. terrigena ATCC 33257 and E. coli ATCC 25922 are both negatively charged, concluded from the ζ-potential measurements, with both strains displaying a bimodal ζ-potential, indicative of culture heterogeneity. For R. terrigena, both subpopulations carry a
FIGURE 1. Scanning electron micrographs of the diatomaceous earth (A, Celite Hyflo DE) and activated carbon particles (B, CA-10; C, RGC; D, RGC + PVAM; E, coconut) used in this study. The bar marker indicates 100 µm.
TABLE 1. Contact Angles (deg) with Various Liquids and ζ-Potentials (mV) in Stabilized Water of the Two Bacterial Strains Involved in This Studya strain
water
formamide
methyleneiodine
r-bromonaphthalene
R. terrigena ATCC 33257 E. coli ATCC 25922
32
33
46
43
25
37
46
40
ζ -32 (42%) -49 (58%) -5 (24%) -32 (76%)
a The size of the bacterial subpopulations in one culture as revealed by ζ-sizing is indicated in percentages within parentheses. All measurements were done in triplicate with separately cultured bacteria, yielding an average standard deviation of 2° in contact angles and 3 mV in ζ-potentials.
sizable net negative charge, but 24% of the E. coli organisms in a population are almost uncharged with a ζ-potential of only -5 mV. On average, however, R. terrigena is more negatively charged than the E. coli strain. Table 2 summarizes the elemental surface compositions of the particles employed. Celite Hyflo DE is rich in oxygen and silicon, as expected for diatomaceous earth. All carbon particles have an extremely high amount of carbon exposed at their surfaces, with a small amount of oxygen and some trace elements like sodium or chlorine. RGC + PVAM has around 10% adsorbed nitrogen at its surface, originating from the ammonium groups in PVAM and yielding the positive charge. XPS analyses indicated in general a minor increase in the oxygen surface concentration of the carbon particles after conditioning in water. Celite Hyflo DE also shows a
minor increase in oxygen and a decrease in sodium, carbon, and silicon, depending on the water type employed. Figure 2 gives an example of the removal kinetics of R. terrigena ATCC 33257 by the different particles. Note that in the absence of any particles (i.e., the control), no significant removal is observed. Also for Celite Hyflo DE, the negative control, little or no removal is observed as compared to the activated carbon particles. A quantitative summary of the removal experiment is presented in Table 3. The initial removal rates for R. terrigena ATCC 33257 to activated carbon particles are smaller than for E. coli ATCC 25922 (Student t-test: p < 0.05). However, within each strain, the differences in initial removal rates to the various carbon particles including the positively charged RGC + PVAM particles are small and not statistically significant (p > 0.1). The logVOL. 40, NO. 21, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Elemental Surface Compositions (in Atomic Percent) Determined by XPS of Activated Carbon and Diatomaceous Earth (DE) Particles, Prior to and after Conditioning in Ultrapure Water and Tap Water carbon or DE type Celite Hyflo DE
no ultrapure water tap water no ultrapure water tap water no ultrapure water tap water no ultrapure water tap water no ultrapure water tap water
CA-10 RGC RCG + PVAM b
coconut
a
Below detection.
conditioning
b
Contains 2.2% P
c
%C 9.9 8.7 12.8 92.2 84.5 89.3 94.8 93.0 90.3 74.9 77.4 74.7 93.6 89.9 nmc
reductions achieved by the various carbon particles show major differences for R. terrigena, which is more negatively charged than E. coli, and are clearly largest (p < 0.05) for the positively charged RGC + PVAM particle. Less negatively charged E. coli shows less preference to adhere to RGC + PVAM than does R. terrigena. After conditioning in water, the particle is no longer able to achieve such high levels of R. terrigena removal and the log-reduction returns to the values observed for the other carbon types.
Discussion In this paper, the removal of waterborne pathogens by activated carbons is compared for various carbon types, including a positively charged variant. The value of applying a positively charged coating to the carbon surface becomes evident from increased log-reductions of bacteria in suspensions exposed for 360 min to amounts of carbon particles having 700 cm2 of external surface area, although the effect of the positive charge on removal of the most negatively charged strain, R. terrigena ATCC 33257, seems to disappear after conditioning of the carbon particles for 21 days in ultrapure or tap water. The microporous, negatively charged coconut carbon performed less well than the mesoporous, positively charged carbon RGC + PVAM prior to conditioning, but it did not suffer a loss of effect after conditioning in water as did the positively charged carbon. Initial removal rates of the more negatively charged R. terrigena strain were somewhat higher than of the less negatively charged E. coli strain. 9
%N
%Na
%Si
%Cl
57.0 58.8 58.3 7.8 9.8 10.7 5.2 7.0 9.7 10.5 11.4 12.9 6.4 10.1 nm
-a
5.9 2.6 1.7 1.0 2.6 nm
27.1 30.0 27.2 nm
0.9 2.2 0.8 nm
3.7 9.9 10.4 10.1 nm
Not measurable due to excessive charging.
FIGURE 2. The number of R. terrigena ATCC 33257 in stabilized water during removal by various activated carbon particles prior to conditioning in representative single experiments: ], control, cell suspension in the absence of particles; O, CA-10; 9, RGC; [, coconut; 2, RGC + PVAM; b, Celite Hyflo DE.
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Both strains employed showed culture heterogeneity with differences in ζ-potentials between subpopulations of 17 and 27 mV for R. terrigena and E. coli, respectively. These differences are substantial and have been suggested to assist the survival of these organisms in natural environments through adhesion to surfaces of different charge (19, 20). The initial removal rates by RGC and the positively charged variant after PVAM coating were surprisingly similar. Usually, positively charged surfaces attract significantly more bacteria than negatively charged surfaces (15, 21). This suggests that the conditions in this adhesion assay are mass-transportcontrolled rather than interaction-controlled (22). Indeed, it can be rationalized that shaking, done in the first instance to prevent sedimentation of the suspended bacteria and particles, does not contribute in bringing bacteria and particles together, as both are equally carried by the suspension fluid and in the same direction. Diffusion is thus the sole means of mass transport to establish contact between bacteria and carbon particles. This is opposite of what happens in parallel plate or stagnation point flow chambers, for example, where a combination of convection and diffusion are responsible for mass transport (22). In flow displacement systems, the influence of electrostatic attraction becomes evident from increased initial deposition rates, but not quite so in the batch assay applied here (see also Figure 2). In the present experimental setup, the influence of electrostatic interactions becomes evident from the log-reductions after 360 min, as seen in the later stages of the experiment. For R. terrigena, the log-reductions are larger for the positively charged RGC + PVAM particle than for negatively charged RGC. Usually the later stages of an adhesion experiment reflect not only the interaction between an adhering organism and a substratum surface but also the interaction between already adhered bacteria and new arriving ones. This indicates that arriving bacteria must overcome the electrostatic repulsion between bacteria already adhered to a carbon particle in order to attach (see Figure 3) through increased attractive forces. This is easier when the carbon particle is positively charged than when it is negatively charged (see Table 3). In this respect, it is important to realize that, owing to the extremely large substratum surface available (700 cm2), the bacterial coverage of the carbon particles remains low even after 360 min of exposure (less than 0.2%). The stabilized water used in this study for conditioning has more or less a similar ionic strength than tap water and its composition can be reproduced all over the world. Tap water on the other hand, is much more unique from place to place, especially with regard to DOC and divalent cation concentrations and the presence of trace elements, which
TABLE 3. Initial Removal Rates (cfu cm-2 s-1) and Log-Reductions Per Liter after 360 min of R. terrigena ATCC 33257 and E. coli ATCC 25922, Suspended in Stabilized Water by Activated Carbon Particles Prior to and after 21 Days of Conditioning in Ultrapure Water or Tap Watera prior to conditioning
carbon type
initial removal rate
logreduction
none Celite Hyflo DE CA-10 RGC RCG + PVAM coconut
-b -14.7 -29.1 -37.4 -39.3 -33.4
0.0 0.1 1.8 3.3 8.6 3.2
none Celite Hyflo DE CA-10 RGC RCG + PVAM coconut
nd -42.0 -43.0 -53.9 -50.1
0.1 nd 5.5 3.7 2.5 3.9
after conditioning in ultrapure water initial removal rate
after conditioning in tap water
logreduction
initial removal rate
logreduction
R. terrigena ATCC 33257 -7.4 -20.1 -24.4 -32.8 -35.4
0.0 0.0 2.9 3.0 1.6 3.3
ndc -21.9 -19.7 -21.5 -23.8
0.0 nd 4.1 3.4 1.4 3.4
E. coli ATCC 25922 nd -56.3 -39.2 -41.3 -59.0
0.1 nd 6.6 3.9 2.6 2.8
nd -51.1 -58.4 -37.0 -30.6
0.1 nd 4.3 5.7 1.4 2.8
a All experiments were conducted in triplicate with separately cultured bacteria, yielding an average SD of 5.9 cfu cm-2 s-1 and 0.4 in initial removal rates and log-reductions, respectively. b Below detection. c Not done.
FIGURE 3. Interactions between depositing microorganisms and a substratum surface initially only involve the interaction between the substratum and the organism (left), but in the later stages of the adhesion process interaction forces between depositing and already adhering bacteria come into play as well (right). For two similarly charged cell surfaces, which is usually the case (13), this is a repulsive electrostatic force that has to be overcome. have a huge influence on the adhesion of microorganisms to carbon particles and the life time of a filter system. Conditioning in water only increases the oxygen surface concentration of the carbon particles but did not yield an indication of the presence of macromolecular film. Likely, the increase in oxygen surface concentration is due to adsorption of counterions such as CO32-, which is in line with the neutralization of the positive charge of and reduced bacterial removal by positively charged activated carbon particles. Note that the positively charged PVAM coating is not removed during exposure to water, since the nitrogen surface concentration is not decreased after exposure to water (see Table 2). In summary, we can draw the following conclusions: (1) The initial removal rates of the four carbon types are about the same for both R. terrigena ATCC 33257 and E. coli ATCC 25922, which is likely due to the mass transport limited conditions of the adhesion assay used. (2) Carbon porosity, i.e., mesoporosity or microporosity, did not affect the initial removal rate and log reduction in R. terrigena ATCC 33257 and E. coli ATCC 25922 prior to or after conditioning in water, as RGC and coconut had the same performance within the experimental error. (3) The highest log reduction was achieved by the positively charged carbon (RGC + PVAM) in the most negatively charged R. terrigena ATCC 33257. However, after conditioning that carbon in water for 21 days, the reduction was strongly reduced and it was lower than by any other carbon. In contrast, conditioning did not significantly affect the reduction by RGC and coconut and increased the
reduction by CA-10. This indicates that the useful lifetime of positively charged carbon filters should be carefully monitored.
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Received for review May 29, 2006. Revised manuscript received August 23, 2006. Accepted August 28, 2006. ES061282R
