direct and indirect effects of climate change on the risk of infection by water-transmitted...

Direct and Indirect Effects of Climate Change on the Riskof Infection by Water-Transmitted PathogensAnkie Sterk,†,* Jack Schijven,†,‡,∥ Ton de Nijs,†,∥ and Ana Maria de Roda Husman†,§

†National Institute for Public Health and the Environment, Bilthoven, The Netherlands‡Utrecht University, Faculty of Geosciences, Department of Earth Sciences, Utrecht, The Netherlands§Utrecht University, Faculty of Veterinary Medicine, Institute for Risk Assessment Sciences, Utrecht, The Netherlands

*S Supporting Information

ABSTRACT: Climate change is likely to affect the infectious diseaseburden from exposure to pathogens in water used for drinking andrecreation. Effective intervention measures require quantification ofimpacts of climate change on the distribution of pathogens in theenvironment and their potential effects on human health. Objectives ofthis systematic review were to summarize current knowledge availableto estimate how climate change may directly and indirectly affectinfection risks due to Campylobacter, Cryptosporidium, norovirus, andVibrio. Secondary objectives were to prioritize natural processes andinteractions that are susceptible to climate change and to identifyknowledge gaps. Search strategies were determined based on aconceptual model and scenarios with the main emphasis on TheNetherlands. The literature search resulted in a large quantity ofpublications on climate variables affecting pathogen input and behavior in aquatic environments. However, not all processes andpathogens are evenly covered by the literature, and in many cases, the direction of change is still unclear. To make usefulpredictions of climate change, it is necessary to combine both negative and positive effects. This review provides an overview ofthe most important effects of climate change on human health and shows the importance of QMRA to quantify the net effects.

■ INTRODUCTION

Waterborne pathogens have caused large disease outbreaks,especially when associated with extreme weather events.1 Mostof these outbreaks have been caused by Vibrio, Campylobacter,noroviruses, and Cryptosporidium. All are important causativeagents of gastroenteritis worldwide. Their sources differ, withCryptosporidium and Campylobacter being zoonotic pathogens,whereas noroviruses are restricted to humans, and Vibrio cangrow in the environment. In some cases, survival of thesepathogens in the environment can be extended when associatedwith protozoan hosts.2 Besides differences in source, thesepathogens differ in persistence, range of size, and infectivity,3

but all are responsive to climate.Climate scenarios and models predict major changes in

temperatures on earth.4 Worldwide changes in precipitation,extreme weather events, and rising sea level can be expected. Alsoin The Netherlands, such changes are expected to occur.5 Accordingto several reviews, they will directly impact infectious disease burdenfrom exposure to pathogens in water used for drinking andrecreation.6−10 This will affect terrestrial and aquatic ecosystems,leading to indirect effects on water-transmitted human pathogens.Both direct and indirect effects determine the extent and directionof changes in the water-transmitted infectious disease burden.A method to quantify the potential effects of climate change

on human health is quantitative microbial risk assessment(QMRA). QMRA may provide a better understanding of

uncertainties and insights in risk management, prioritization ofpublic health hazards, and development of successful adaptationstrategies.11 Recently a QMRA tool was developed by Schijvenet al.12 to estimate direct effects of changes in temperature andprecipitations on risks of infection by water-transmittedpathogens. However, it does not take into account indirecteffects of climate change that may influence pathogen behavior,such as changes in nutrient cycles and turbidity.The objective of this review was to summarize current

knowledge which is usable to estimate how climate change mayaffect infection risks posed by water-transmitted pathogens. Tostructure the systematic literature search, a conceptual model and anarray of scenarios focusing on The Netherlands was developed. Theresults can be used to prioritize which processes and interactionsshould be included in the QMRA framework. Knowledge gapsidentified can be used to prioritize future research.

■ MATERIALS AND METHODSThe literature review was structured using a conceptual modelwhich described the emission, distribution, and behavior ofpathogens in the environment in relation to environmental

Received: August 10, 2013Revised: October 9, 2013Accepted: October 14, 2013Published: October 14, 2013

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parameters. In addition, scenarios provided information on theenvironmental parameters that are expected to change in TheNetherlands under influence of climate change. A trial search,with keywords including, instead of the selected pathogens (seeScenarios for The Netherlands), “pathogens in general” as wellas “surrogates” or “fecal indicators”, resulted in 41 337 hits andshowed the necessity of more focused search strategies.Conceptual Model. The conceptual model was developed

following the traditional steps of QMRA.11 To quantitativelyassess the risk of infection, hazard identification was combinedwith “exposure” (e.g., the concentrations and distribution of thepathogens in the water to which humans are exposed, as well asthe duration and extent of the exposure) and the “doseresponse” assessment (see Figure 1). The model was developedsuch that it could be used as a base for a mathematical model.Hazard identification includes the identification of all potential

hazards, sources, and events that can lead to the presence ofmicrobial pathogens.11 Four pathogens were selected based onextent of disease burden and data availability and representing arange of behavior and sources. They included three fecallyderived pathogens Campylobacter, norovirus, and Cryptospori-dium to represent each of the main microbial groups (bacteria,viruses, and parasites) plus the naturally occurring Vibrio,representing bacterial pathogens that may be reproducing inaquatic environments. In The Netherlands, Vibrio cholera is rareand therefore the main concern is with Vibrio species like Vibrioparahemolyticus or Vibrio alginolyticus.13 Therefore the main

focus of this review is on Vibrio noncholerae species. And eventhough human feces is an important source for Vibrio cholerae indeveloping regions,14 human-to-human transmission is notconsidered in this review. Hazard identification looked at pathogenpresence in four environmental compartments of land surface,surface water, sediments, and aquifer.The land surface compartment was defined as the upper soil

layer and processes taking place there. A subcompartmentrepresenting animal feces was included because these depositsare part of the topsoil layer. Animal deposits were defined asmain input source of pathogens for land surface, largelydetermining the loads of zoonotic pathogens such asCampylobacter and Cryptosporidium. Transmission betweenland surface compartment and surface waters was representedthrough runoff, including overland flow and throughflow (flowtemporally submerged below the surface), and flooding.The surface water compartment represented both fresh and

saline waters. Each of the four selected pathogens was seen asrelevant here, as this compartment receives input from bothhumans and animals and also supports the growth of Vibrio.Interaction between the sediment and surface water

compartment was described through sedimentation andresuspension.Pathogens in the aquifer compartment (water bearing layer of

soil/rock) are introduced through leakage from sewage, septictanks, or landfills; from infiltration from soil surface, or throughinteraction with surface waters.

Figure 1. Schematic overview of the conceptual model.

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The exposure pathways of drinking water and recreationalwater were considered in this conceptual model. Althoughexposure may also occur through direct contact with soil orfood that are contaminated by irrigation or growth incontaminated waters, these transmission routes were beyondthe scope of this review.Scenarios for The Netherlands. Climate scenarios

developed by the Royal Netherlands Meteorological Institute(KNMI)5 were assumed to capture the possible range of futureclimate changes. The scenarios included changes in airtemperature, precipitation, and sea level up to 2050 andsecondary changes in ecosystems and human behavior (seeTable 1 for an overview of scenarios considered).The rise in air temperature is expected to result in a gradual

rise of surface water temperatures.9,15,16 Large-scale climatechange also affects aquifers, but with a delay that increases withdepth from the land surface; short-term climate variability haslittle or no impact.17,18

Higher air temperatures could also cause changes in bio-geochemical reactions in the surface water or soil. For example,organic matter concentration is dependent on temperature andhumidity.19 Biota could respond to the warming trend and to theexpected prolongation of the growing season, with shifts ingeographical ranges and timing of lifecycle events in both plantsand animals.20

Climate change will also affect water quantity. Increasedwinter precipitation will increase river flow rates and lead to higherrisk of flooding. During summer, increased periods of lowdischarge, such as expected for the river Meuse,21 will increaseresidence times of water and reduce stream capacity for dilution.22

Changing precipitation patterns could affect surface runoff,increasing erosion and adding input from terrestrial systems intosurface waters. Increased precipitation may increase overland flowevents. Drier summers may extend periods of low moisture in soil,leading to increased hydrophobicity of soil surfaces and increasedrunoff events.23 On the other hand, droughts may increase crackscaused by soil shrinkage raising infiltration capacity.23

Increasing temperature and changing precipitation will mostlikely alter groundwater recharge.18 Depending on manage-ment, groundwater tables in sandy aquifers may drop locallyseveral meters in summer and rise 10−50 cm during winterperiods, affecting hydraulic conductivity and flow velocity.9

The rising sea-level could lead to increased salinization inriver deltas, aggravated by lower discharge during summers.24

Also, salinization of coastal groundwaters might change due tosea-level rise and changing recharge patterns.25

Adaptation of human behavior in reaction to climate changeis still very uncertain. Surface water recreation may increase, aspeople may seek refreshment under rising temperatures ordecrease if temperatures drive people to shelter from UVexposure and heat.26 The demand for drinking water is likewiseuncertain and could vary in The Netherlands from an increaseto a decrease.27 To fully assess the impacts of climate change oninfection risks, such changes cannot be ignored.

Search Strategy and Selection Criteria. Two systematicsearches were conducted on October third, 2012, using thescientific database Scopus, for papers published between 1January 1991 and 1 October 2012. Publications in languagesother than English, Dutch, or German were excluded.For both searches, key terms consisted of the selected

pathogen and terms describing “aquatic environments”. For thefirst search these terms were combined with key terms on“climate change”, to find literature reporting on possible effectsof climate change on pathogen behavior in the aquaticenvironment. The second search was more specifically aimedat relations between pathogen behavior and environmentalvariables that are examined outside the context of climatechange but could be, based on the scenarios, directly orindirectly affected (see Figure 2).Three main criteria were used to select publications. Studies

were included if they provided information on (1) at least oneof the selected pathogens; (2) pathogen behavior within anycompartment of the conceptual model, and (3) The Netherlandsor a similar region (based on climate type: Koppen-Geiger climateclassification28 including classification Cfa, Cfb, and Cfc andeconomic development).Publications identified by the online search engine were first

screened by one reviewer as to the inclusion criteria based ontitle and abstract. Relevant documents were retrieved andscreened based on full-text review by one reviewer. Any doubtas to inclusion was resolved by two other reviewers.Publications were categorized per compartment and main

subject. Individual papers could be included within more thanone category.

Table 1. Climate Scenarios and Secondary Changes in The Netherlands

Climate Scenarios Secondary Changes in Aquatic Ecosystems

air temperature will continue to rise surface water temperatures will increaseon average, winters will become wetter, and extreme precipitation amounts will increase changes in biogeochemical cycles will lead to changes in nutrient

concentrations in water or soilduring summers, the amount of rainy days will decrease while the intensity of extremerain showers will increase

biota will be affected by climate change because of their temperature-dependent life cycles

the sea level will continue to rise changes in water quantities will affect:discharge/water levelsfloodingsoil humidity

changes in runoff regimes will affect:terrestrial input, affecting nutrient and sediment concentrations andturbiditychanges in salinity will occur

secondary changes through human adaptation

changes in water demand for irrigation or drinkingchanges in recreational patternschanges in agriculture practice, including fertilization, tillage, and use and type of pesticides



■ RESULTSThe online database search yielded 2732 publications reportinginformation on climate change, ecosystems, and water-trans-mitted pathogens. Of these, 524 were retrieved for full textreview, of which 146 met the inclusion criteria. Table 2 dis-plays the number of publications providing information onthe four compartments and pathogens under study. Fulldetails on the papers (n = 146) are available in the SupportingInformation.Most publications were from North-America, followed by

Europe and Australia. Seventeen, reported on outbreaks ofwater-transmitted infectious disease related to climate con-ditions. showing seasonal fluctuations.29−31 Such fluctuationsare often explained by seasonal variations in human behaviorand in the prevalence of pathogens in reservoirs and sources.Analysis of the relationship between precipitation and

waterborne disease outbreaks in the United States32 foundthat heavy precipitation and subsequent runoff are importantfactors. A similar study in England and Wales33 showed thatoutbreaks caused by Campylobacter and Cryptosporidium wereoften preceded by both low rainfall or heavy rainfall periods.Furthermore, disease outbreaks are positively correlated withhigh air temperature34,35 and flooding events.36

The remaining 129 publications provided information onpathogen behavior linked to climate parameters in one or moreof the compartments of the conceptual model. These results are

combined with the information from the scenarios and aresummarized in the next sections.QMRA requires not only hazard identification but also the

exposure and dose response assessment. No studies reportedon climate variables affecting dose response. Only one37

provided information on factors affecting the exposure.However, their collection of exposure data for swimmers (i.e.,volume of water swallowed and frequency and duration ofswimming events) did not confirm the hypothesis thatfrequency and duration of swimming may be influenced bylocal factors such as summer weather fluctuations.

Input Sources. Human Input Sources. This section willfocus on input through human wastewater, as the literature searchyielded nothing on climate variables affecting direct human inputnor on leakage from sewage, septic tanks, or landfills.Contamination of surface water through discharge of sewage

is relevant only for Campylobacter, Cryptosporidium, andnorovirus. Six studies focused on wastewater input under dryweather conditions. Most of these studies reported a seasonalpattern in the pathogen concentration from effluent of waste-water treatment plants. Reasons were related to agriculturalpractices and increased tourism that overloaded the treatmentsystems38 and to correlation with the clinical prevalence inhumans.39,40 These are not directly linked to climate changebut could well be indirect effects.Scenarios have predicted the increase of intense rainfall

events. During these periods, combined sewage overflow (CSO)could cause direct discharge of untreated wastewater thatcontaminate surface waters. The literature indicates the importanceof sewage overflow on the input of pathogens to the surface waters.For example, Campylobacter concentrations clearly increasedduring periods of heavy rainfall in rivers downstream of CSOs.41

Animal Input Sources. Six studies indicated a seasonalrelation to the numbers of Campylobacter or Cryptosporidiumexcreted in the feces of animals. Reasons for this seasonal patterninclude coincidence with the birth season of calves, which are moresusceptible to infections than mature animals42,43 or correlation withpasture quality, possibly reflecting a dietary effect.44

A statistical analyses revealed significant evidence forseasonal periodicity in the carriage rate and population size ofCampylobacter over time in dairy herds.45 Environmentalparameters, such as maximum and minimum temperature,rainfall, or number of hours of sunshine could not explain thepattern, but peaks roughly coincided with the transition fromsummer grazing to winter housing of the animals.In general, seasonal patterns of these pathogens in feces of

animals discussed in the literature were not explained throughparameters that could be directly affected by climate change,like temperature or rainfall. However, changes in lifecycles ofbiota and changes influencing animal diet, like vegetation andagricultural practices, are indicated as drivers of seasonalfluctuations.Besides the direct deposition of fecal material by grazing

animals and indigenous fauna, catchment sources of fecalpollution also include manure applied as fertilizer to agriculturalland. Three studies showed correlations between on-farmpractices and the prevalence or levels of zoonotic pathogens inmanure stored on farms. Decline or die-off of pathogens storedin manure on farms is not dependent on season.46 Becausemost farms do not manage their waste stores as batchoperations, most stores are subject to constant additions ofwaste and its associated pathogens. The concentration of

Figure 2. Keywords literature search, searched for in title, abstract andkeywords (*: truncation; W/n: words are within n words of another,regardless the order; -: words are next to each other either separatelyor combined as one word).



pathogens in stored manure depends largely on the rate ofdecline under management and storage conditions.47

Combining this information with the climate scenarios indicatesthat direct climate effects are not expected to have a large influenceon pathogen prevalence in manure. The influential factors relatemainly to storage, controlled by humans; hence, only secondarychanges could perhaps cause any change.Compartments. Land Surface. In total, 29 publications

addressed the land surface compartment, with two seeking linksbetween pathogen presence and environmental conditions.One found that Cryptosporidium prevalence on pasture land washighest in summer and lowest in winter.48 It suggested thathigher air temperatures might change surface properties of theCryptosporidium oocysts and/or the vegetation to which theyattach, enhancing their attachment ability. A study of thefrequency and spatial distribution of Campylobacter in fecesdeposits49 found that prevalence seemed to diminish with ageof the feces, possibly due to bacterial inactivation over time.The age of feces depends on time between deposition and aprecipitation event that may transfer material from land surfaceinto another compartment. Thus prevalence may be affected byclimate change through changes in precipitation.Eleven publications reported on die-off of Campylobacter or

Cryptosporidium in feces deposited on land surface. Laboratory

experiments showed water temperature, soil type50 andammonia51 to be factors affecting die-off. Desiccation of feces isalso a factor, but one group52 suggests that increased temperatures,rather than desiccation, most strongly influenced Campylobactersurvival. Also studies on die-off rates of Campylobacter in sheep53

and goose54 feces showed that temperature appeared to be themost significant parameter.In general, the reduction of pathogens in the land surface

compartment is clearly related to temperature, solar radiation,and desiccation. Other determinants of die-off, like soil type,could indirectly be affected by climate change as well.Increasing temperatures or changes in soil tillage could affectgeochemical cycles in soil and hence the amounts of organicmaterial and nutrient concentrations.In case of manure, its application method affects bacterial

die-off rate. When injected as a slurry into soil rather thanspread as solid material on soil surface, manure dries moreslowly and is exposed to less UV radiation, which both favorpathogen survival.55 When slurry and solids were alike spreadon soil surface, no significant differences were found betweenthe rates of pathogen decline in liquid versus farm manure.56

Application methods are not directly affected by climate changebut could be affected by climate-driven changes in agriculturalpolicy and regulations.

Table 2. Number of Publications Providing Information on Compartments and Pathogens under Studya

Process Campylobacter Cryptosporidium norovirus Vibrio

General studies: (n = 19)Waterborne disease outbreaks: 17QMRA: 2

Input sources: (n = 18) Wastewater input 2 3 1 n/aHumans (n = 9) Sewage overflow 2 3 0 n/a

Direct input 0 0 0 n/aLeakage 0 0 0 n/a

Animals (n = 9) Fecal shedding 3 4 n/a n/aManure 3 2 n/a n/a

Compartments: (n = 111)Land surface (n = 29) Presence and seasonality 1 1 n/a n/a

Survival 9 2 n/a n/aAttachment/release 0 1 n/a n/aLeaching 3 5 n/a n/aRunoff 4 10 n/a n/a

Surface waters (n = 75) Presence and seasonality 10 20 2 19Survival 8 10 1 2Growth n/a n/a n/a 1Interaction susp. sediments 0 3 0 0Sedimentation 0 3 0 0

Sediments (n = 7) Presence and seasonality 1 1 0 5Survival 0 0 0 0Resuspension 0 0 0 0

Aquifer (n = 8) Presence and seasonality 1 0 0 n/aSurvival 0 1 0 n/aAttachment/detachment 0 3 0 n/aTransport 0 4 0 n/aSeepage 0 0 0 n/aWithdrawal 0 0 0 n/a

an/a = not applicable.



Precipitation causes release of pathogens from feces indeposits and manure. However, only one publication providedinformation on factors affecting release of pathogens from feceson land. It correlated the release of pathogens with salinity,based on solution electrical conductivity.57

Pathogen transmission from land surface occurs throughleaching to the aquifer and runoff to surface waters (describedin, respectively, 8 studies and 10 studies). A factor in leaching issoil water saturation which can substantially promote themanure-borne oocyst transport through soil cores.58 Otherfactors promoting pathogen transport include decrease in the timeperiod between manure application and rainfall and increase inrainfall intensity.59 The application method of manure on the landsurface also influences the transmission of pathogens to the othercompartments. Injection of slurry was found to increase the riskfor contamination of the groundwater, because infiltration of thepathogens became more likely.60,61

For a case-study in Australia, QMRA principles were adapted toestimate the impact on health risks arising from rainfall-inducedrunoff entering a surface water reservoir.62 It concluded that highrunoff periods contributed to a large proportion of annualinfections with Cryptosporidium and Campylobacter.Factors affecting pathogen transport in runoff have been

studied during several plot scale experiments. Important factorsaffecting runoff include slope,63 vegetation, flow-rate, soil type,relative timing of pathogen application to soil and rain event,soil infiltration rate, rainfall intensity, and size of transportedmicroorganism.63−69

Tyrrel and Quinton70 emphasized the importance of the state inwhich pathogens are transported; as single cells, aggregated cells,or attached to soil or feces. However, experiments showed that itwas more likely that Cryptosporidium oocysts in runoff weretransported as single entities than attached to particles.71,72

Combining literature results with scenarios shows thattransmission of pathogens, from land surface to othercompartments, is very likely to be affected by climate change.Both infiltration and runoff are mainly driven by precipitationcharacteristics, which are expected to change in the future. Inaddition, factors like soil composition, vegetation, and manureapplication method are indirectly susceptible to climate change.Surface Waters. In total, 75 publications reported on

pathogen behavior in the surface water compartment, halfdescribing programs to monitor pathogen variability todetermine seasonal trends or relations with environmentalfactors. However, findings were not always consistent amongthe various pathogens and studies.One group detected summer peaks in Campylobacter concen-

tration in surface water,73 but others reported the lowestprevalence in summer.74−76 Explanations for the low prevalenceincluded bacterial inactivation due to higher temperatures andincreased UV radiation, as compared with winter conditions. Peakconcentrations in summer were explained by increased precip-itation, which likewise peaked in summer along with clinical casesin humans. It was hypothesized that in the watershed under study,environmental loading in summer months was mediated by rainfalland runoff, and input was sufficiently high to offset decreasedsurvival caused by high seasonal temperatures. Absence of aseasonal pattern was also reported in some cases.77,78 However,Jokinen et al. did find Campylobacter prevalence and rainfall to benegatively correlated, possibly associated with dilution ofpathogens already present in the river under study.78

For Cryptosporidium, most studies refer to fall/winter as theperiod with highest prevalence of oocysts.79−83 Explanations

include a higher persistence at low temperature,81 seasonalchanges in pathogen prevalence in the animal reservoir,83

agricultural practices82 and rainfall.80 However, other studiesdetected peaks in other seasons,84,85 or detected no seasonalpattern.86

Several studies did not focus on seasonal patterns but onenvironmental factors directly affecting the Cryptosporidiumconcentrations in surface waters. In several studies rainfall isindicated as a significant factor.67,84,87

Increased norovirus concentrations were registered duringthe winter periods in surface waters in two studies in TheNetherlands.88,89 The first-cited study explained the increase bythe seasonality of noroviruses, which are more prevalent in thehuman population in winter. Causes proposed by the otherstudy included heavy rainfall events causing combined seweroverflows or, variability in sewage treatment.The seasonality of Vibrio was described in 19 studies. In

general, high levels occurred during summer.90−92 Its prevalencewas mainly determined by temperature and salinity93 but alsoseemed related to nutrients and chlorophyll-a levels,92,94,95whichaffect its growing conditions. The literature suggested thatenvironmental factors could indirectly affect the growingconditions for Vibrio. To illustrate, Vibrio concentrations in theChesapeake Bay were related positively to river flow, affected byregional precipitation through its effect on salinity.96

Only one study focused on factors affecting growth of Vibriounder controlled laboratory conditions.97 These factorsincluded temperature, salinity and organic carbon concen-trations. The results suggested moderate salinity and a“threshold” apparent assimilable organic carbon (AOCapp =60 mg/L) concentration promote growth of Vibrio.Whether or not climate change is likely to influence seasonal

patterns depends on the mechanisms behind them. Whenvariation is caused by factors mentioned in the scenarios,changes are likely to occur. This is clearly the case for factorslike temperature, precipitation, and salinity. As mentionedearlier, factors like nutrient concentrations, dilution, or changesin agricultural practices could be indirect effects of climatechange as well.As for seasonality, die-off and inactivation of pathogens in

surface water compartment has been described intensively.From the 19 studies included on this topic, the majorityfocused on reduction in concentration for Campylobacter andCryptosporidium. Information on reduction rates was mainlygathered through laboratory experiments. Many factorsaffecting reduction for each pathogen, as listed in Table 3,are likely to be affected by climate change.Besides the laboratory studies, two groups created models of

pathogen transport in location-specific study catchments todetermine the relative importance of environmental factors forthe reduction of pathogens. One model, for a case study inAustralia, showed that reduction of Cryptosporidium by UV lightwas low compared to reduction by temperature.112 Sensitivityanalysis of the other model likewise indicated that temperaturewas the most important parameter regulating Cryptosporidiumoocyst concentrations.68

Three studies described the interaction of selected pathogenswith suspended sediment particles and the sedimentationprocess for both freely floating pathogens and pathogensattached to sediment particles. The size of these particles wasfound to influence transport. Given equal flow velocity, largesediment particles settle more rapidly than smaller particles orfree-floating pathogens.113 A study of sedimentation behavior of



Cryptosporidium oocysts and Giardia cysts likewise showed thatsettling velocity increased with particle size.114 Also, settlingcolumn and batch experiments demonstrated that Cryptospori-dium oocysts are removed from suspension at much higher ratewhen attached to sediments.115,116

One group showed that Giardia cysts and Cryptosporidiumoocysts rarely attach to soil particles and mainly travel freely.117

However, sedimentation rates found by Medema et al.,114 couldonly be explained by (oo)cyst attachment to larger particles. Daiand Boll117 argue that differences in results were likely due todifferent media characteristics: soil with some organic matter versuseffluent particles. However, Searcy et al.115 cited the lowconcentration of their suspended sediments, implying that aminimum concentration is necessary before attachment can occur.They also found that attachment of Cryptosporidium is influencedby sediment types and that changes in background water conditionshave little impact on the extent of oocyst-particle attachment.Through processes like runoff and turbulence, climate change

could indirectly affect sediment concentration and character-istics in the aquatic environment. These changes could affectinteraction of suspended sediments with pathogens in aquaticecosystems. Furthermore, as input of pathogens from surfacewater to sediments is dependent on flow velocity, predictions ofincreased periods of low discharge during summer could haveconsequence for input of pathogens to the sediments.Sediments. Of the 146 selected publications, 6 reported on

processes within the sediment compartment, of which fiveconcerned Vibrio.91,118−121 One of these isolated Vibrio frommarine sediments and concluded that these sedimentsrepresent an important microbial reservoir.120 They emphasizedthe importance of this finding because, even though the storage ofmicroorganisms in sediments can decrease their concentration inthe surrounding water, it also permits the microbial agents to bereleased again into the environment through natural or human-made resuspension events. Such events, depending on the cause,could be affected by climate change.

Seasonal patterns for the presence of Vibrio in the sedimentshave been described.91,119 Using a marine environment in Italy,the first group found that concentration of Vibrio in sedimentspeaked during intermediate seasons corresponding to springand autumn although previously a positive correlation withtemperature was found. Comparing the numbers of Vibrio insediments versus the overlying water column revealed higherconcentrations in the sediments119 and over a longer period oftime.121 Evaluating the influence of environmental variablesshowed that salinity had a greater influence on the presence ofVibrio in sediments than temperature.119,121 Salinity might playa role in bacterial adsorption to and elution from sediment,implying that climate change may affect Vibrio concentrationsin sediments.Only one study concerned the sedimentary presence of

Campylobacter, showing higher concentrations in the sedimentscompared to the water column, but no seasonal relation wasdetermined.75

None of the selected studies assessed factors affectingsurvival of pathogens in the sediment or during resuspensionprocesses.

Aquifer. Eight studies reported on pathogen transport and/or reduction of concentration in the aquifer, but none concernednorovirus. Measurement of Campylobacter in a shallow aquifershowed little seasonal difference in detection rate, with 12% ofsamples being positive during the irrigation season as comparedwith 9% during the winter122 However, the authors noted thatwinter findings were based on limited samples.A laboratory study of inactivation rates of Cryptosporidium

under diverse conditions showed the positive effect ofincreasing temperatures and a significant effect of groundwatertype, possibly due to differences in water composition.102 Thescenarios show that, as groundwater temperatures are quitestable throughout the year, they are not expected to be muchaffected by climate change.An important factor determining transport of Cryptosporidium

in aquifer is the flow velocity: more oocysts can be attached atlower pore-velocities, when they are likely to have more contactwith solid surfaces than at higher velocities.123−125 Another im-portant transport factor is preferential flow,126 which promotesfast microorganisms migration through unsaturated soil.Attachment of pathogens to soil during transport is

dependent on water quality and the geochemical characteristicsof the soil. For example, pH124 but also dissolved organic carbonin the groundwater127 can influence the adsorbance of oocysts.These parameters may be indirectly affected by climate change.

■ DISCUSSIONAs evidenced by the amount of literature reviewed here, muchinformation is already available on climate variables affectingpathogen input and behavior in the environment. However, notall processes, compartments and selected pathogens are evenlycovered by literature (see Table 2). For example, norovirus isdescribed less frequently than other three pathogens. Table 4summarizes in which parts of the conceptual model, based onliterature, climate change is likely to have an effect. It shows thedirection of change, when known, as not all changes will have anegative effect for human health.Combining what is known on pathogen behavior with informa-

tion from disease outbreaks could help to define the direction of acertain change. For example, heavy rainfall and subsequent runoffcan affect the risk of waterborne disease outbreaks32,33 and it istherefore plausible to assume that increased precipitation will favor

Table 3. Literature Results Indicating Factors AffectingPathogen Inactivation/Die-off in the Surface Waters

pathogenvariables affecting

reduction correlationa references

Campylobacter temperature + 76,98−100competition withautochthonous watermicroflora

+ 98,99

solar radiation + 76,101

Cryptosporidium temperature + 51,102−105solar radiation + 106salinity + 107,108dissolved organic carbon - 106high concentration ofammonia

+ 51

mineral content + 105

norovirus temperature + 109

Vibrio salinity ± 110nutrients ± 110iron concentration - 111pH - 111

aCorrelation between environmental factor and pathogen inactivation/die-off, which can be positive (+), negative (-) or unclear (±).



pathogen transport through runoff. However, other changes inducedby climate change may cancel out such effects. For example, changesin the timing of manure application to soil and subsequent rainevent could decrease pathogen input by increasing the period ofdie-off on land surfaces.A clear example of counteracting effects of climate change

effects: Summer droughts are lowering river discharges and couldincrease infection risks due to decreased dilution, but they couldalso decrease infection risks due increased inactivation of pathogensby increased temperatures and residence time. The QMRA tool ofSchijven et al.,12 shows that the net effect depends on pathogencharacteristics. Infection risks for exposure to waterborne pathogensthat are very temperature-sensitive (like Campylobacter) willdecrease due to increased inactivation, whereas infection risks willincrease for slowly inactivating pathogens like norovirus, that ismainly affected by the decrease in dilution.Such examples indicate the need for quantitative modeling

approaches. QMRA can help to find out how negative andpositive effects of climate change will combine and interact toaffect human health outcomes. QMRA can also help toprioritize the impacts of changes. It is already clear that certainchanges will occur, but when the impact is minor, there willbe less need for adaptation measures. Adaptive ingenuity andspending can be prioritized to focus on changes in order oftheir importance and urgency.As can be seen in Table 4, the direction of change is unclear

for many processes. However, the literature review indicates

which processes are likely to be susceptible to climate change,and should therefore be included in the QMRA framework.To summarize, changes in input sources of pathogens are

most likely to occur through changes in frequency of sewageoverflow or changing seasonal patterns of input from waste-water treatment plants and animal fecal shedding. Processesthat could be affected within the compartments, because oftemperature and precipitation changes, include pathogengrowth and die-off/inactivation. Transmission between the com-partments, including runoff and infiltration, are mainly driven byprecipitation and therefore very likely to be affected by climatechange.For some parts of the conceptual model, no information is

available. Maybe no studies are available in these areas, as theyare considered unlikely to be affected by climate change.Possibly other studies were not found by the search because oflimitations as time and resources limited the number ofpublications that could be screened for inclusion.Some keywords, such as “water”, elicited more papers in

general, but not many that were relevant. This indicated thatselected keywords could not be too general. Consequently, theresults were biased by search terms, and a number of knownpapers were not identified by this approach. For example, thesearch indicated only one study57 on release of pathogens fromfeces, showing a relation with salinity. However, intensity andduration of precipitation are also known to influence the releaseof pathogens128,129 and may be relevant for the elution ofpathogens from feces. Hence, “elution of pathogens from feces”

Table 4. Effecta of Changing Climate Parameters for Human Health

Pathogen processTemperatureincrease

Changes inprecipitation

Sealevelrise

Secondary changesecosystems

Secondary changeshuman adaptation

Input sources:b

Humans Wastewater input ±Sewage overflow - n/aDirect input n/aLeakage n/a

Animals Fecal shedding x x n/a ± ±Manure x x n/a ±

Compartments:Land surfaceb Survival + ± x ± ±

Attachment/release xTransport by leaching ± x ± ±Transport by runoff ± x ± ±

Surface waters Survival + ± ±Growthc - ± ±Interaction suspended sediments ±Sedimentation ± ± ±

Sediments SurvivalResuspension

Aquiferb Survival +Attachment/detachment ±Transport ±Seepage/RBFWithdrawal

aEffect can be positive (+), negative(-), uncertain (±) or nonexistent (x). The blanks indicate that no information was provided by the literaturereview. bNot considered relevant for Vibrio. cRelevance limited to Vibrio.



should not be excluded when researching the effects of climatechange.In addition, selection criteria may have excluded some

potentially useful publications. For example, the Koppen-Geiger climate classification was applied very strictly.Publications focused on nontemperate climates were excludedeven though they might contain information applicable to aclimate like The Netherlands. Other limitations might be theexclusion of so-called gray (i.e., nonpeer-reviewed) literatureand the use of a single search engine, namely Scopus. Thissearch engine was selected because it includes publicationsfrom multiple research domains whereas PubMed, for example,includes mainly medical literature.The data gaps in Table 4 also indicate that information may

not yet be available concerning parts of the conceptual model.Data are indispensable in performing a QMRA to yield aspecific infection risk for one of the selected pathogens. Datagaps concerning certain pathogens can sometimes be filled bydata available on their surrogates and indicator organisms. Thesearch for the selected pathogens found 2732 publications, butthe inclusion of indicator organisms resulted in more than40 000 hits. The utility of pathogen surrogates is illustrated by therelatively little information found on norovirus in this review. Thelack of a norovirus infectivity assay130 has necessitated the use ofviral surrogates such as murine noroviruses, feline caliciviruses, orbacteriophages.Data is likewise scarce concerning aquifers, perhaps reflecting

a lack of field studies on pathogens in this compartment.Natural concentrations of pathogens in aquifers are often underthe detection limit, impeding studies on pathogen transport in anatural environment. Field experiments are mainly performedusing indicators, as one cannot add pathogens to aquifers.Such experiments suggest that factors such as salinity131 anddissolved organic matter132,133 influence pathogen attachmentand therefore may influence pathogen transport in aquifers.Indicating that other climate parameters than those addressedin this review could affect pathogen transport and behavior inaquifers, and indicator data are useful to signal these factors.No publications were found describing survival and

resuspension of the selected pathogens in river sediments.Mainly for Vibrio but also for Campylobacter, the “presence andseasonality studies” suggests persistence in sediments in higherconcentrations than in the overlying water column. Studies ofother bacteria and fecal indicators show that bacteria survivelonger in sediments than suspended in the water.134,135 Maybethis also holds for the selected pathogens. Because low flowconditions due to climate change may affect concentrations ofpathogen in the river sediments this could promote the survivalof pathogens. Resuspension of pathogens in sediments occursduring high flow and could give rise to high concentrationpeaks in the water.136,137

This literature study mainly focused on possible climate-related changes in hazard identification. However, to quantifythe impact of pathogens on human health, one must determinealso the possible changes in exposure and dose response. Usefulinformation on these two modeling steps is limited. Secondaryeffects of climate change could influence the exposure ofhumans to recreation water. However, Schets et al.37 could notconfirm a link between climate variables and human recreationbehavior.Drinking water needs are weather-dependent, rising during

hot weather.138 But evidence for changes in exposure throughdrinking water was not found during the literature search.

Furthermore, based on the link between seasonality and thehuman immune system,139 there is a possibility that climatechange may affect dose response, but the literature offers noevidence. The dose response relation may also be affected byclimate change, if changes in environmental conditions alter theevolution of infectivity of pathogens. However, this is notconfirmed by the literature either.To summarize, it is clear that climate change will induce

changes in pathogen fate and transport. It is still unclear whatwill be direction and extent of the effects of climate change. Theconceptual model needs to be developed with mathematicalformulations that quantitatively describe all the processes topermit investigation of their interplay under a range of climatechange scenarios.

■ ASSOCIATED CONTENT*S Supporting InformationTable S1−S3: Full details of all papers (n = 146) which met theinclusion criteria. This material is available free of charge via theInternet at http://pubs.acs.org.

■ AUTHOR INFORMATIONCorresponding Author*E-mail: [email protected] Contributions∥The manuscript was written through contributions of allauthors. All authors have given approval to the final version ofthe manuscript. These authors contributed equally.NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTSThanks to J.P. Ridder-Kools for her assistance with thesystematic search. The work was funded through the RIVMStrategic Research Project Climate Cascades (S/607021).

■ ABBREVIATIONSAOC assimilable organic carbonCSO combined sewage overflowsQMRA quantitative microbial risk assessment

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