The persistence of flood-borne pathogens on building surfaces under drying conditions

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International Journal of Hygiene and Environmental Health 216 (2013) 91–99 Contents lists available at SciVerse ScienceDirect International Journal of Hygiene and Environmental Health journa l h o me page: www.elsevier.com/locate/ijheh The persistence of flood-borne pathogens on building surfaces under drying conditions Jonathon Taylor a,b , Mike Davies b , Melisa Canales a , Ka man Lai a,a Department of Civil, Environmental, and Geomatic Engineering, UCL, London, United Kingdom b The Bartlett School of Graduate Studies, UCL, London, United Kingdom a r t i c l e i n f o Article history: Received 25 August 2011 Received in revised form 13 February 2012 Accepted 26 March 2012 Keywords: Flood Bacteria Persistence Hygrothermal Buildings Surfaces a b s t r a c t Previous research into microbial persistence on material surfaces following flooding has produced a wide range of results due to differing experimental conditions, including the temperature and humidity conditions of the experimental material and/or surrounding air. However, investigations to identify and quantify these factors and their links to the hygrothermal properties of building materials and the tran- sient environmental conditions are rarely reported. This paper examines the viability of bacterial species on drying material surfaces that have been saturated with water or synthetic sewage. Escherichia coli and Enterococcus faecalis were inoculated on brick, wood, or plaster and allowed to dry at the conditions intended to mimic the remediation environments commonly found in domestic dwellings following a flood event. The inactivation rates were compared between environmental conditions, water type and the material properties of the surfaces. Significant differences were found in the declines in E. coli accord- ing to water type, the surface relative humidity and air relative humidity and between drying rates for sewage floods. Simulations using hygrothermal software were performed to illustrate the wide variation in material drying rates under different scenarios, taking into account material size, wall composition, and ventilation. The significantly differing rates of microbial death on flooded building materials under different drying regimes suggest that building simulation models can be useful tools for predicting the level and duration of microbial contamination in buildings following a flood event. A better understand- ing of microbial survival on drying surfaces can be used to assess the health risks to occupants in flood affected properties. © 2012 Elsevier GmbH. All rights reserved. Introduction Climate change is predicted to produce highly variable condi- tions and extreme events, including more frequent extreme rainfall. In the United Kingdom an increase in extreme rainfall events combined with rising sea levels and tidal surges caused by more frequent heavy winds and storms means the risk of flooding is expected to grow (Intergovernmental Panel on Climate Change (IPCC), 2007). An increase in flood frequency and severity will test the resilience of the building stock and local communities to water damage and contamination. Flood water and the sediment carried by flood water can con- tain a number of potentially pathogenic bacteria (Fewtrell et al., 2010) including those resistant to antibiotics (Wolf-Rainer and Dirk, 2005). Persistence of bacteria on surfaces is generally con- sidered to be dependent on factors such as solar irradiation, the Corresponding author at: Department of Civil, Environmental, and Geomatic Engineering, UCL, London WC1E 6BT, United Kingdom. E-mail address: [email protected] (K.m. Lai). presence of organic matter such as dust or sediment and most importantly, temperature and relative humidity (RH) (Maier et al., 2009). Therefore, the ability of a material or envelope design to dry quickly is an important consideration in understanding the con- tamination persistence following a flood. Additionally, the drying regime the property is subjected to will also impact the ability of a contaminant to survive on building surfaces and the risk to occupants through direct contact. Microbial contaminants in buildings can also impact occu- pant health through respiratory pathways. Dampness in buildings is consistently associated with respiratory illnesses, such as asthma, wheeze, cough, respiratory infections and upper respira- tory tract infections (Mendell et al., 2009). While most literature has focused on mould growth in damp or flooded properties, bacte- ria (Andersson et al., 1997; Hyvarinen et al., 2002; Torvinen et al., 2006), protozoa (Yli-Pirilä et al., 2004, 2009) and viruses (Bornehag, 2001; Hersoug, 2005) have also been found on damp surfaces or in elevated levels in the indoor air of damp houses. Microbes such as mould and bacteria can release spores or fragments and toxins into the indoor air, which may impact the health of occu- pants. 1438-4639/$ see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ijheh.2012.03.010

Transcript of The persistence of flood-borne pathogens on building surfaces under drying conditions

Page 1: The persistence of flood-borne pathogens on building surfaces under drying conditions

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International Journal of Hygiene and Environmental Health 216 (2013) 91– 99

Contents lists available at SciVerse ScienceDirect

International Journal of Hygiene andEnvironmental Health

journa l h o me page: www.elsev ier .com/ locate / i jheh

he persistence of flood-borne pathogens on building surfacesnder drying conditions

onathon Taylora,b, Mike Daviesb, Melisa Canalesa, Ka man Laia,∗

Department of Civil, Environmental, and Geomatic Engineering, UCL, London, United KingdomThe Bartlett School of Graduate Studies, UCL, London, United Kingdom

r t i c l e i n f o

rticle history:eceived 25 August 2011eceived in revised form 13 February 2012ccepted 26 March 2012

eywords:loodacteriaersistenceygrothermaluildingsurfaces

a b s t r a c t

Previous research into microbial persistence on material surfaces following flooding has produced awide range of results due to differing experimental conditions, including the temperature and humidityconditions of the experimental material and/or surrounding air. However, investigations to identify andquantify these factors and their links to the hygrothermal properties of building materials and the tran-sient environmental conditions are rarely reported. This paper examines the viability of bacterial specieson drying material surfaces that have been saturated with water or synthetic sewage. Escherichia coliand Enterococcus faecalis were inoculated on brick, wood, or plaster and allowed to dry at the conditionsintended to mimic the remediation environments commonly found in domestic dwellings following aflood event. The inactivation rates were compared between environmental conditions, water type andthe material properties of the surfaces. Significant differences were found in the declines in E. coli accord-ing to water type, the surface relative humidity and air relative humidity and between drying rates forsewage floods. Simulations using hygrothermal software were performed to illustrate the wide variation

in material drying rates under different scenarios, taking into account material size, wall composition,and ventilation. The significantly differing rates of microbial death on flooded building materials underdifferent drying regimes suggest that building simulation models can be useful tools for predicting thelevel and duration of microbial contamination in buildings following a flood event. A better understand-ing of microbial survival on drying surfaces can be used to assess the health risks to occupants in floodaffected properties.

ntroduction

Climate change is predicted to produce highly variable condi-ions and extreme events, including more frequent extreme rainfall.n the United Kingdom an increase in extreme rainfall eventsombined with rising sea levels and tidal surges caused by morerequent heavy winds and storms means the risk of flooding isxpected to grow (Intergovernmental Panel on Climate ChangeIPCC), 2007). An increase in flood frequency and severity will testhe resilience of the building stock and local communities to wateramage and contamination.

Flood water and the sediment carried by flood water can con-ain a number of potentially pathogenic bacteria (Fewtrell et al.,

010) including those resistant to antibiotics (Wolf-Rainer andirk, 2005). Persistence of bacteria on surfaces is generally con-

idered to be dependent on factors such as solar irradiation, the

∗ Corresponding author at: Department of Civil, Environmental, and Geomaticngineering, UCL, London WC1E 6BT, United Kingdom.

E-mail address: [email protected] (K.m. Lai).

438-4639/$ – see front matter © 2012 Elsevier GmbH. All rights reserved.ttp://dx.doi.org/10.1016/j.ijheh.2012.03.010

© 2012 Elsevier GmbH. All rights reserved.

presence of organic matter such as dust or sediment and mostimportantly, temperature and relative humidity (RH) (Maier et al.,2009). Therefore, the ability of a material or envelope design to dryquickly is an important consideration in understanding the con-tamination persistence following a flood. Additionally, the dryingregime the property is subjected to will also impact the abilityof a contaminant to survive on building surfaces and the risk tooccupants through direct contact.

Microbial contaminants in buildings can also impact occu-pant health through respiratory pathways. Dampness in buildingsis consistently associated with respiratory illnesses, such asasthma, wheeze, cough, respiratory infections and upper respira-tory tract infections (Mendell et al., 2009). While most literaturehas focused on mould growth in damp or flooded properties, bacte-ria (Andersson et al., 1997; Hyvarinen et al., 2002; Torvinen et al.,2006), protozoa (Yli-Pirilä et al., 2004, 2009) and viruses (Bornehag,2001; Hersoug, 2005) have also been found on damp surfaces

or in elevated levels in the indoor air of damp houses. Microbessuch as mould and bacteria can release spores or fragments andtoxins into the indoor air, which may impact the health of occu-pants.
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Table 1Potential flood-borne pathogens (Fewtrell et al., 2010) show a wide range of survivaltimes on different material types (Kramer et al., 2006).

Potential flood-borne pathogens Total survival time

Bacteria Campylobacter jejuni Up to 6 daysSalmonella spp. 1 dayShigella 2 days–5 monthsLeptospira –Enterococci spp. 5 days–4 monthsE. coli 1.5 h–16 monthsLegionella –

Viruses Norovirus 8 h–7 daysHepatitis A 2 h–60 daysRotavirus 6–60 daysAdenovirus 7 days–3 monthsEnterovirus 1 day–8 weeksParvovirus >1 year

Fungus Candida albicans 1–120 daysCandida parapsilosis 14 daysTorulopsis glabrata 102–150 days

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bers, allowing the materials to dry at different rates. Both saltsare hygroscopic, with Mg(NO3)2 capable of maintaining RH of

Microbial survival studies on surfaces show a range of persis-ence levels for the same microbial agent (Table 1). The UK-based

ater Research Centre studied the biological decay of flood-bornescherichia coli on a variety of building materials (WRc, 2000). Thisesearch found that survival was related to humidity, temperature,nd sunlight, as well as the building material, but that contami-ated houses should only need to be quarantined for 24 h after aood for E. coli to fall to undetectable levels. Other studies of E. coli157 on faeces-contaminated surfaces have found countable levelsf E. coli for up to 28 days following contamination, depending onhe drying conditions (Williams et al., 2005).

It is widely recognised that the range of results from differenttudies into the survival of microbial contaminants on building sur-aces is due to the differing experimental conditions, including theemperature and humidity conditions of the experimental mate-ial and/or surrounding air. However, investigations to identify anduantify the factors involved and their links to the hygrothermalroperties of building materials and the transient environmen-al conditions during remediation are rarely reported. In porous

aterials, the heat and moisture behaviour of building materials isictated by the material’s hygrothermal parameters. The amount ofontaminated water the material can absorb and the rates of mate-ial drying will affect the amount of water available to flood borneathogens as the materials dry. Therefore, differences in death raten material types in previous studies into persistence may dependn the ability of materials to dry as well as the environmental con-itions.

The objective of this work was to examine the survival ofacteria on the wet surfaces of different building materials underifferent drying conditions. Escherichia coli and Enterococcus faecalisere inoculated on the surface of wood, plaster, and brick coupons

ollowing immersion in synthetic sewage and then allowed to dry atifferent rates and at different temperatures. To compare the effectsf nutrients within the floodwater, the experiment was repeatedsing E. coli and deionised water. The hypothesis of the experiment

s that the behaviour of bacteria deposited on surfaces over timeill depend on the water quality, drying rate, temperature, mate-

ial, and species. An emphasis on the impact of the hygrothermalehaviour of the materials was included by examining the surfaceH of material samples as they dried, thus accounting for the rel-tive drying abilities of materials under the same conditions. Theerm water activity, generally used by microbiologists, is equivalento the equilibrium relative humidity of the material divided by 100

Brown, 1976). By relating bacterial population size to the changing

oisture levels of the materials, it will be possible to understand the

d Environmental Health 216 (2013) 91– 99

persistence of pathogens within flooded buildings under differentdrying scenarios.

Methodology

Building materials

Coupons were cut from wood (kiln-dried spruce soft-wood) and brick (Mayfield yellow multibrick) to approximately15 mm × 15 mm × 15 mm. Plaster samples were obtained by pour-ing mixed gypsum plaster (Thistle MulitFinish) into a similar sizedmould and allowing it to dry for 14 days. In order to simulate differ-ent types of flooding, coupons were immersed in deionised water orsynthetic sewage for 48 h. Synthetic sewage was prepared accord-ing to the guidelines used in British Standards (British Standards,2007), mixing 16 g peptone, 11 g meat extract, 3 g urea, 0.7 g NaCl,0.4 g CaCl22H2O, 0.2 g MgSO47H2O, and 2.8 g K2HPO4 into 1 L water.Following soaking, the coupons were placed inside the individualdrying chambers and sterilised at 121 ◦C for 15 min in an autoclave.Three coupons were prepared for each drying temperature, dryingtreatment, material, and water type in order to have experimentalrepetition.

Microbial indicators

E. coli and E. faecalis were chosen as representative species offlood-borne bacteria. E. coli and E. faecalis are considered to beappropriate model organisms for Shigella, enterotoxigenic E. coli,Campylobacter, and Vibrio cholerae (Petterson and Ashbolt, 2003).The US Environmental Protection Agency (EPA) recommends theuse of E. coli as an indicator species in freshwater and Enterococ-cus spp. for both fresh water and saltwater (U.S. EnvironmentalProtection Agency, 2000).

E. faecalis (American Type Culture Collection 29212) and E. coliK12 were stored in 10% glycerol at −80 ◦C. Bacterial cultures used inthis experiment were prepared by inoculating a loopful of cell solu-tion on Tryptic Soy Agar (TSA) agar (Difco Laboratories, Detroit, MI)and incubated at 37 ◦C for 18 h in order to obtain the cultures duringgrowth phase. Bacterial colonies were then suspended in phos-phate buffered saline (PBS) (NaCl 0.8%, KH2PO4 0.02%, Na2HPO40.115%, KCl 0.02%, pH 7.4). To ensure that the bacterial concentra-tion in the inoculant for separate experiments were similar, theabsorbance of the prepared bacterial suspension was measured at620 nm (OD620). Serial dilutions of the inoculants from 10−1 to10−10 were performed in 0.1% Tween and plated onto MacConkey(Oxoid Ltd., Hampshire, UK) (E. coli K12 only) and Bile esculine agar(Sigma–Aldrich, Fluka BioChemika, UK) (E. faecalis only) in order todetermine cell concentration. Colonies exhibiting typical E. coli K12(characteristic pink colour) and E. faecalis (characteristic blackeningcolonies) morphology were counted following incubation at 37 ◦Cfor 24 h. This revealed a final inoculant concentration of approxi-mately 5 × 1011 CFU mL−1 E. faecalis and 3 × 1012 CFU mL−1 E. coliK12. The sterile, sewage-soaked coupons were inoculated with10 �L of bacterial suspension, with E. coli and E. faecalis inoculatedon opposite sides of individual coupons, while the water-soakedmaterials were inoculated with 10 �L of E. coli suspension only.Wood was inoculated on the with-grain face.

Drying

Magnesium nitrate (Mg(NO3)2) and sodium hydroxide (NaOH)were used to remove moisture from the air inside the cham-

54.38(±0.23)% at 20 ◦C and NaOH 8.91(±2.4)% RH at 20 ◦C at equi-librium (Greenspan, 1976). A petri dish containing granulated salts

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A B

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plaster coupon the same size as the ones used in the experimentand one of the most common wall types in the UK (a solid 9′′ brick

ig. 1. Air and surface RH of (A) water soaked materials, and; (B) sewage soaked mrying Ambient Temp. (HDAT), and High Drying Low Temp (HDLT).

f Mg(NO3)2 (70 g) was used to provide a low drying rate, while aish with NaOH (90 g) was used to provide a high drying rate.

The following experiments were carried out:

Low drying rate at ambient temperature (21–23 ◦C) in chamber(LDAT).High drying rate at ambient temperature (21–23 ◦C) in chamber(HDAT).Low drying rate at a low temperature (8 ◦C) in chamber (LDLT).High drying rate at a low temperature (8 ◦C) in chamber (HDLT).Optimal conditions for E. coli growth (37 ◦C and >97% air RH) in asealed incubated chamber (wood and brick only) (OPT).

The petri dishes containing the granulated salts were placednside a sterile chamber containing the 16 coupons of each mate-ial type for the desiccating experiments, while no salts were usedor the heat treatment. The airtight chamber was then sealed andxposed to the appropriate temperature conditions. A data loggerHOBO U10) recorded the temperature (±0.54 ◦C) and RH (±5%)nside the boxes for the duration of the experiment.

icrobial sampling and counting

Sampling was performed immediately after inoculation andhen at 24, 48 72 and 144 h. Individual coupon samples wereemoved from each chamber and placed into a sterile 250 mLolypropylene vials containing 40 mL of 0.1% Tween. Three couponsere taken for each material type, temperature and drying rate to

nsure repetition. The vials were vortexed for 20 s and then dilu-ions in 0.1% Tween solution performed. Dilutions were plated on

cConkey and Bile Esculin agar. Plates were incubated at 37 ◦C for4–48 h before counting.

At sampling times a designated reference coupon was removednd the surface RH measured using a humidity and water activitynalyser (Rotronic Hygrolab 3) until the measurement value sta-

ilised, or for 45 min. The surface RH of the material was recordednd the material returned to the desiccating box.

for Low Drying Ambient Temperature (LDAT) Low Drying Low Temp. (LDLT), High

Material parameters and statistical analysis

Statistical tests were performed to examine the differences insurface drying rates between water and material types and the dif-ferences in bacterial behaviour depending on the water, material,drying type, temperature, time, and the transient RH conditions onthe surface and in the air. To test the effects of the drying conditionson the surface water activity, a univariate ANOVA was performed inSPSS with the surface RH as the dependant variable, the drying type,water, and material type as fixed independent factors and time andthe RH of the air as covariates.

To understand the changes in microbial population, the val-ues of Log10 CFU material−1 and the standard error of the mean(SEM) were calculated for each series of samples using MicrosoftExcel. A univariate ANOVA analysis was performed in SPSS for thedependant Log10 CFU material−1 data with temperature, the typeof water, and the type of material as fixed factors, and time andair and surface RH as covariates. The level of significance was 95%(p < 0.05). Results were examined for both between-subjects effectsand interactions between factors.

Simulation

Hygrothermal building simulation software can predict themoisture content and temperature on drying surfaces based onmaterial data and the surrounding environmental conditions,allowing for the drying behaviour of surfaces to be predicted. Inorder to illustrate how the surface of a material (plaster) will dryunder different environmental conditions and geometries, simula-tions were carried out in the 2D hygrothermal building simulationsoftware Delphin 4 (IBK, 2008) drying at a nominal 20 ◦C at 50% RH.

To demonstrate how the drying behaviour of plaster will varybetween a simple coupon experiment and a full wall assembly, a

wall with 10 mm plaster coating) were simulated drying withoutconsideration for the air change rate of the surrounding air (i.e.

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ig. 2. Air and surface RH of water and sewage soaked materials under optimalonditions (OPT).

nlimited ventilation of damp air). To demonstrate the impact ofall types and ventilation, the surface of the solid 9′′ brick wall and

n a wall that has been observed to take longer to dry (a brick cav-ty wall with glass fibre insulation) were simulated drying in a 8 m3

oom, where all the walls were flooded to a nominal height of 2 m.n air change rate of 4 air changes per hour (ach), approximatelyqual to that of a single storey building with the windows opennd cross ventilation (BRE, 2005), was provided. Materials proper-ies for brick, gypsum plaster, and glass fibre were taken from thenternational Energy Agency (IEA) Annex 24 (Kumaran, 1996). TheH of the plaster 0.5 mm inside the interior surfaces was outputourly.

Flooded dwellings are often treated by using industrial heatersnside the property. Simulations were performed to examine how auilding treated through heating the inside with high temperaturend low RH air can impact the conditions inside the cavity of theall. The glass fibre insulated wall was simulated being treatedith 50 ◦C air and 15% RH internally – values which one could

xpect indirect fired heating equipment used in the remediationndustry to easily achieve – and a weather file containing typicalondon conditions externally. Simulations started January 1st, andemperature and RH values for the plaster surface and internal cav-ty output hourly. The results of all simulations were comparedsing Microsoft Excel.

esults

icrobial recovery and drying rates

Fig. 1 shows the change in the RH of the air and the materialurfaces of the drying experiments, while Fig. 2 shows the sameata for the optimal experiment. As expected, the air and materialoupons in the chambers containing the more hygroscopic saltsried much more rapidly that those with less hygroscopic salts.he RH on the surface of the coupons dried at the same rate as their inside the boxes, with a slight lag. The RH of the materials variedepending on the drying rate. A significant difference between therying rates of brick versus the other materials could be observedp = 0.007), with brick tending to dry slower than the other mate-ials. Water type did not appear to make a significant difference tohe drying rate (p = 0.207).

urvival of E. coli and E. faecalis on material surfaces

Physical recovery of bacteria from building materials immedi-tely after inoculation showed recovery of viable bacteria varied

d Environmental Health 216 (2013) 91– 99

from 0.04% to 86.7%. A decline could be observed in all bacterialpopulations over time, with the exception of the experiment underoptimal conditions for microbial growth (OPT), which showed anaverage of 0.9Log10 CFU (E. faecalis) and 0.7 Log10 CFU (E. coli)increase in bacteria counts per coupon over the initial four daysbefore a subsequent population decline (Figs. 3E and 4E).

Effect of water types

Different survival curves could be observed depending on thetreatment of the inoculated coupons (Figs. 3 and 4). The deionisedwater treated materials tended to show a rapid initial decline inthe population, followed by a tail, while sewage-treated materi-als tended to show slower, more linear death rates after an initialstationary phase. There was a significant difference (p = 0.000)between the population decline of E. coli on drying samples depend-ing on whether the material had been immersed in sewage or water,with the bacteria on sewage-contaminated materials exhibiting aslower decline. The impact of water type did not make a significantdifference to the amount of growth observed during the optimaltreatment (p = 0.078).

Effect of drying rate

There was a significant difference between the populationdeclines of E. coli subjected to different drying treatments when theobject had been immersed in sewage (p = 0.043), while no signifi-cant difference could be observed in any of the treatments followingsoaking in water (p = 0.145). Average inactivation rates for the treat-ments based on the fitted curves varied from −0.10 Log10 CFU perday (Low Drying Ambient Temperature) to −1.07 Log10 CFU per day(High Drying Low Temperature) for sewage and −1.26 Log10 CFUper day (Low Drying Low Temperature) to −1.56 Log10 CFU perday (High Drying High Temperature) for water per coupon. Theimpact of temperature in the drying experiments was not signif-icant by itself (p = 0.174). For E. faecalis, there was no significantdifference between the death rates based on the drying methodused (p = 0.327).

A significant correlation between the air RH and the E. coli bac-terial population die-off was observed (p = 0.000). The relationshipbetween the surface RH of the materials and the bacterial declinewas significant (p = 0.004), although not as strong as the relation-ship with the air RH, which may be due to inaccuracies in thesurface water measurements – for materials with high surface RH,the measurement did not always stabilise. No significant differencebetween the surface and air RH and the death of E. faecalis was found(p = 0.127).

Effect of materials

There was no significant difference between the building mate-rials when looking at the decline of the E. coli population in watersoaked materials (p = 0.902). A significant difference (p = 0.04)between brick and the other materials was observed for the sewagetreatment for E. coli, with brick having a slower population decline.This is most likely related to the observable difference between thedrying of the surface RH of the brick when compared to the othermaterials, with the brick material drying rate slower. No significantdifference between the materials and material properties and thedeath of E. faecalis in sewage was observed (p = 0.453).

Difference between bacteria

No significant differences were observed between the deathrates or the growth rates of the bacteria species on sewage in eitherthe drying or the optimal treatment experiments (0.699).

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J. Taylor et al. / International Journal of Hygiene and Environmental Health 216 (2013) 91– 99 95

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ig. 3. E. coli population counts at (A) Low Drying Ambient Temp.; (B) Low Drying Loars represent standard error of the mean (SEM).

uilding simulation

The simulation of the drying coupons and walls showed a wideange of different results for the RH of the plaster surfaces, depend-ng on the construction of the wall and the inclusion of internalentilation rates in the simulation (Fig. 5). This indicates the impor-

ance of understanding the building as a whole when determininghe drying rate of material surfaces following flooding.

The simulation of the heat treatment indicates that heat canove from the internal environment through to the cavity space, in

p.; (C) High Drying Ambient Temp.; (D) High Drying Low Temp.; (E) optimal. Error

which restrictions in the ventilation and moisture-retaining mate-rials such as glass fibre may mean the existence of both a hightemperature and high RH (Fig. 6).

Discussion

Different bacterial death rates were observed for experimentswith differing water types and drying treatments (Fig. 3). Manyof the population curves in this study indicate an initial orfinal stationary phase, suggesting that a linear assumption about

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96 J. Taylor et al. / International Journal of Hygiene and Environmental Health 216 (2013) 91– 99

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ig. 4. E. faecalis population changes at (A) Low Drying Ambient Temp.; (B) Low Dryrror bars represent standard error of the mean (SEM).

nactivation rates may not be appropriate and that low-level con-amination may linger regardless of the drying treatment. Therowth over the first few days that could be observed during theptimal conditions treatment suggests that under certain remedia-

ion techniques, or in warmer climates, growth may be a possibility.he death after the first few days suggests that the growth of theopulation is limited by a limiting factor such as available nutrientsr toxin production.

w Temp.; (C) High Drying Ambient Temp.; (D) High Drying Low Temp.; (E) optimal.

Water quality

A range of different results could be observed from the exper-iment. The difference between the bacterial population change

observed for materials soaked in water and in sewage indicatesthat the content of the water can impact the survival time of themicrobial contaminants. While mould, another post-flood contam-inant, is capable of utilising the nutrient content of organic and
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Ft

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ig. 5. Building simulation results show how plaster drying rate can differ accordingo construction and ventilation (drying at 20 ◦C and 50% RH).

any man-made materials, bacteria will be more dependent onhe nutrient levels of the contaminating floodwater. There waso significant difference between the drying rates of the wateroaked and sewage soaked materials, however previous studiesKoniorczyk and Gawin, 2008) have indicated that materials soakedith salt-containing water dry slower and it has been suggested

hat sediment in the water can also delay drying (Nicholas et al.,001). Therefore, the presence of sediment and salts inside theontaminating water can influence microbial survival by providingutrients while potentially slowing the reduction in the surface RH.

rying regimes

Different rates of decline in the E. coli populations for the sewageoaked materials with different drying treatments suggest that thenvironmental conditions have a significant impact on the persis-ence of contaminants. The drying treatment directly impacts theurface RH of the material coupons. Surfaces with a reduced dryingapacity, for instance areas with reduced ventilation such as spacesehind furniture, may be prone to longer periods of contaminationhan others.

While understanding microbial persistence can help informhose entering flooded properties, it can also help advise theest remediation technique. Flooded properties can be remediatedsing a number of techniques, such as natural ventilation, dehu-

idification, or indirect heating. High temperatures are commonly

sed when treating flooded properties, often by installing an indi-ect heater capable of injecting large volumes of very warm veryry air into the building. This heat can be transferred into cavities

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d Environmental Health 216 (2013) 91– 99 97

and unventilated spaces, where trapped moisture may remain forextended periods. Growth was observed in the bacterial popula-tion over the first three days when the material was treated at ahigh temperature and with no ventilation or drying. This suggeststhat in certain situations, heat treatment of a building may result ingrowth of human pathogenic bacteria. For example, in houses withglass fibre insulated exterior walls, heat can move into the cavitywhile moisture can be retained by the insulation (Fig. 6). The bacte-rial population declined after the initial growth period, suggestinga growth-limiting factor is present.

Materials

The population change on different materials was examined inorder to identify whether there was any link between the mate-rials themselves, the potential water retention, and the ability ofbacteria to survive. It was expected that the materials would dryat significantly different rates; however a large difference was notobserved (Fig. 1). This may be due to the small size of the materialcoupons used, which resulted in a large surface area to volume ratioand an increased ability for the materials to dry. Space restrictionsand the need to keep the materials sterile meant it was unrealisticto use larger coupons.

The drying ability of materials varies, with the moisture trans-port behaviour and the vapour diffusion resistance factor of thematerials being the most influential hygrothermal parameters fordrying (Holm, 2001), while the porosity and water content of thematerials at effective saturation dictates the ability of the mate-rial to absorb floodwater. A reduced decline in the bacterial deathrate was observed on brick; however this could not be significantlycorrelated to any individual hygrothermal parameter. Hygrother-mal material parameters have a major influence on the ability of amaterial to dry and so will influence the surface RH. Further workshould examine the impact of strongly hygroscopic materials suchas a wider range of wood products, or materials which are not con-sidered to be hygroscopic but can potentially soak and retain watersuch as vermiculite and mineral fibre insulation. Those enteringflooded properties should be wary of porous materials that areprone to retaining contaminated water.

As the hygrothermal simulations demonstrated, the drying abil-ity of flooded materials will also depend on the nature of thebuilding envelope, and built form and estimating the persistenceof flood-borne microorganisms on surfaces should take this intoaccount. Using a 2D simulation to model the drying of a 3D couponwould overestimate the drying time in this scenario, as there arefewer faces for the material to dry from. Despite this, the couponsurface was found to dry within hours of flooding, much faster thanthe days and weeks it took to dry full-wall simulations. The widedifference between the results in Fig. 5 indicates that results takendirectly from material coupons within the laboratory may not becomparable to conditions inside a flooded building due to the sizeand exposed surface areas. In particular, materials that can retainmoisture can take a long time to dry and can impact the watercontent of the surrounding materials.

Bacteria

While no difference was observed between the two types ofbacteria tested, this may be due to E. faecalis having only beeninoculated on sewage-treated materials, reducing the amount ofcomparable data. Different bacteria may persist for longer periodson surfaces for a variety of reasons, such as a resistance to desicca-

tion and ability to form spores. While some pathogens are thoughtto die out quickly, for example Campylobacter, others may persistfor months (e.g. C. difficile) (IFH, 2007). Bacteria can also produceendotoxins which can become aerosolised into the indoor air as the
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opulation grows and dies off. Further work into the persistencef different pathogens following a flood can help inform the riskselative to the changing conditions inside a flooded property. Inter-ctions with other flood-borne bacteria may enhance or restrictacterial survival.

uilding simulation

The drying behaviour of a flooded material will depend on theygrothermal characteristics of the surface and component mate-ials, the surface area exposed to the surrounding air relative tohe volume of the material, and the boundary environmental con-itions including temperature, RH, radiation, and the rate of airhange and air movement around the material. Plaster and brickre porous, hygroscopic inorganic materials, while wood is organic,orous, and highly hygroscopic. These materials can absorb waterrom the surrounding environment, which in turn can changeheir thermal and moisture behaviour. At high moisture contentsood can undergo structural changes due to swelling, causingore sizes to increase and reducing the hygroscopic effects (Clarkend Yaneske, 2009), and can exhibit strong non-linear changes tots water vapour permeability with water content. These effectsre difficult to model due to a lack of available material infor-ation, and may lead to an overestimate of drying time when

sing hygrothermal models. Uncertainties, structural changes, and lack of data in material databases can make modelling the dry-ng of flooded buildings problematic, particularly with the uniquerying behaviour of wood and other organic porous materials.aterial and environmental factors can alter significantly between

wellings, and should be considered when evaluating a floodedroperty.

mplications for building safety

In the many guidelines and recommendations for drying floodeduildings (Taylor et al., 2011), there is no agreed consensus onhat constitutes a safe ‘dry’ building. It has been suggested that

n indoor RH target of 40% or less should be attained as quicklys possible following a flood in order to minimize microbial healthhreats (Cole, 1989). Often this is not possible; occupants and reme-iators may have to enter properties that have been flooded and

eft standing, sealed and without ventilation. While professionalood remediators often use ATP (Adenosine Triphosphate) Bio-

uminescence test kits to search for contamination (Taylor et al.,011), this identifies only the presence of bacteria within the areaested and not bacterial pathogenicity nor the presence of any viralontaminants. Therefore, a better understanding of building dampollowing flooding developed through building simulation can besed to identify the risk of microbial contamination in areas proneo lingering damp under different post-flood scenarios and indicatereas susceptible to microbial persistence.

The experimental results indicate the importance of the waterype, drying regime, and material type on the bacterial death rate.hose entering flooded properties should be aware of the type ofoodwater present, the ability of different material types to dry, andhe potential for microbiological niches to develop in areas whererying is restricted due to construction materials, poor ventilation,nd/or built form. This study has shown that, under certain con-itions, growth of pathogenic bacteria in a flooded property maye possible. In cases where a flood contains highly contaminated

black’ water, an understanding of the origin of the contamina-ion, the potential pathogens present in the floodwater, and their

bilities to survive on surfaces can help prevent further risks.

Previous research of bacterial contaminants on material sur-aces shows a range of different survival times under differentonditions. This research confirms the impact of the different

d Environmental Health 216 (2013) 91– 99

drying rates and water types on bacterial survival. However, defin-ing a fixed duration for microbial risk on a flooded surface thatapplies to all scenarios is impossible, since the amount of viablebacteria remaining at any one time will depend on the initial con-tamination levels, the drying ability of the material in question, andthe surrounding environmental conditions. The levels and speciesof bacteria found in floods will vary depending on the type of floodevent. As an example, concentrations of E. coli and E. faecalis levelsin floodwater following an urban sewer flood in the Hague werefound to range from 8.7 × 101 to 1 × 103 CFU mL−1 in flood waterand 1.1 × 105 CFU mL−1 in sediment (ten Veldhuis et al., 2010). Theinoculated levels of bacteria in our experiment were intentionallyhigh in order to ensure countable levels throughout the experiment.The risk to occupants will depend on the amount of a pathogendeposited on the wall during the flood, as well as it is infectiousdose.

Our experiment assessed the survival of bacteria deposited onbuilding surfaces. The method of recovery was intended to extractthe highest number of viable cells possible. While much researchhas been done on the fomite to human transfer rates of bacteriathrough direct contact (e.g. fingers), further research is required tounderstand how flood borne pathogens may impact human healththrough direct or airborne pathways.

Building simulation is a powerful tool in assessing the indoorcomfort and health of building occupants. Mould models havebeen previously developed which can be used to estimate the riskof mould growth on building surfaces under certain conditions(Rowan et al., 1999; Sedbauer, 2001; Viitanen, 2007). Modellingbacterial growth on drying surfaces has been performed (Lebertet al., 2007), but not related to the built environment. Modellingsurvival on building surfaces relative to the environmental andmaterial conditions will allow for the application of microbiolog-ical models alongside building simulation models. By combiningthese models, it will be possible to identify areas within a propertyat risk of prolonged microbial contamination and the movementof aerosolised contaminants from these point sources within thebuildings. This can inform remediation workers and residents aboutthe risks present in different building types from different con-taminants as the buildings dry. The potential health risks insidethese buildings due to inadequate drying practices can also beassessed. Further work, incorporating the research presented inthis paper into building simulation models, will be performed inthe future.

Conclusion

This study was intended to aid the understanding of the impli-cations of the drying conditions commonly found in domesticdwellings following a flood event. Previous studies have exam-ined the survival on surfaces relative to different material typesand surrounding environmental conditions, but have not related itto the transient drying abilities of the individual building mate-rials. By monitoring the surface RH and temperature, a betterunderstanding of the persistence of pathogens on a flooded sur-face was developed. These results will be used alongside buildingsimulation software, which can predict the drying out of surfacesand materials within the building envelope, to better inform therisks inside flooded properties based on building construction andinternal and external drying conditions. By combining an under-standing of the persistence of flood-borne pathogens on buildingsurfaces relative to the materials temperature and moisture levels

with the ability to simulate the drying out of a flooded propertyunder different remediation regimes using building simulation,we can develop a holistic model of the microbial risk to occupanthealth.
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cknowledgements

This experiment study was partly funded by the Engineeringnd Physical Sciences Research Council (EPSRC), UK. Grant Refer-nce EP/G029881/1. PhD studentship awarded to JT was funded byPSRC.

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