SYSTEMATIC REVIEW Extreme water-related weather events and waterborne disease

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Epidemiol. Infect. (2013), 141, 671–686. f Cambridge University Press 2012
          doi:10.1017/S0950268812001653

          SYSTEMATIC REVIEW
          Extreme water-related weather events and waterborne disease

          K. F. C A NN 1*, D. RH. T HO M A S 1, R. L. SA L MO N 1, A. P. W Y N - J O N E S 2 A N D D. KA Y 2
          1
            Communicable Disease Surveillance Centre, Public Health Wales, Temple of Peace and Health, Cathays Park,
          Cardiff, UK
          2
            IGES, Aberystwyth University, Aberystwyth, UK

          Received 12 October 2011; Final revision 26 June 2012; Accepted 11 July 2012;
          first published online 9 August 2012

          SUMMARY
          Global climate change is expected to affect the frequency, intensity and duration of extreme
          water-related weather events such as excessive precipitation, floods, and drought. We conducted a
          systematic review to examine waterborne outbreaks following such events and explored their
          distribution between the different types of extreme water-related weather events. Four medical
          and meteorological databases (Medline, Embase, GeoRef, PubMed) and a global electronic
          reporting system (ProMED) were searched, from 1910 to 2010. Eighty-seven waterborne
          outbreaks involving extreme water-related weather events were identified and included, alongside
          235 ProMED reports. Heavy rainfall and flooding were the most common events preceding
          outbreaks associated with extreme weather and were reported in 55.2 % and 52.9% of accounts,
          respectively. The most common pathogens reported in these outbreaks were Vibrio spp. (21.6 %)
          and Leptospira spp. (12.7 %). Outbreaks following extreme water-related weather events were
          often the result of contamination of the drinking-water supply (53.7 %). Differences in reporting
          of outbreaks were seen between the scientific literature and ProMED. Extreme water-related
          weather events represent a risk to public health in both developed and developing countries, but
          impact will be disproportionate and likely to compound existing health disparities.

          Key words: Climate – impact of, water-borne infections.

          INTRODUCTION                                                                        to acceleration of the water cycle caused by atmos-
                                                                                              pheric heating. Altered pressure and temperature
          Global climate change is expected to affect the fre-
                                                                                              patterns, caused by global warming, may also shift the
          quency, intensity and duration of extreme water-
                                                                                              distribution of when and where extreme water-related
          related weather events such as excessive rainfall,
                                                                                              events usually occur [4]. .The frequency of heavy pre-
          storm surges, floods, and drought [1–3]. Recent ex-
                                                                                              cipitation events is thought to have increased over
          treme water-related weather events have included
                                                                                              many mid-latitude regions since 1950, even where
          drought in Russia and flooding in Sri Lanka, the
                                                                                              there has been a reduction in the total precipitation.
          Philippines, Pakistan, Australia and Brazil. Weather
                                                                                              The area affected by drought is thought to have in-
          is expected to become more extreme and variable due
                                                                                              creased since the 1970s in many areas of the world [4].
                                                                                              There is also evidence to suggest that other ex-
          * Author for correspondence: Miss K. F. Cann, CDSC, Temple of
          Peace and Health, Cathays Park, Cardiff CF10 3NW, UK.
                                                                                              treme water-related weather events such as El Niño
          (Email: Kimberley.cann@wales.nhs.uk)                                                Southern Oscillation (ENSO), hurricanes, and
          The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons
          Attribution-NonCommercial-ShareAlike licence . The written permission of
          Cambridge University Press must be obtained for commercial re-use.

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672         K. F. Cann and others

                   cyclones are becoming more frequent, intense and of                                 Search strategy
                   greater duration [4, 5].
                                                                                                       Four major medical and meteorological databases
                      Excessive or heavy rainfall events can mobilize
                                                                                                       (Medline, EMBASE, GeoRef, PubMed) were
                   pathogens in the environment and increase run-off of
                                                                                                       searched on 6 May 2010 to identify documented out-
                   water from fields, transporting them into rivers,
                                                                                                       breaks of waterborne infectious disease in humans,
                   coastal waters and wells [1, 6]. Such events can there-
                                                                                                       occurring since 1910, where an extreme water-related
                   fore increase raw water turbidity, which has been
                                                                                                       weather event was believed to have been involved. An
                   found to be associated with gastrointestinal illness [7].
                                                                                                       extreme water-related weather event was defined as a
                   Heavy rainfall can also lead to changes in the direc-
                                                                                                       meteorological change in the conditions of a region,
                   tion of flow of water through channels that would not
                                                                                                       involving a quantity of water more or less than is
                   normally occur [8]. During periods of heavy rainfall,
                                                                                                       usually seen in the region. Key terms used for identi-
                   water treatment plants may be overwhelmed, there
                                                                                                       fication of extreme water-related weather events were
                   may be cross-contamination between sewage and
                                                                                                       identified from the National Climate Data Centre [13]
                   drinking-water pipes (particularly where water infra-
                                                                                                       and included : flooding, drought, heavy rainfall, El
                   structure is old), sewage overflow, or bypass into local
                                                                                                       Niño Southern Oscillation (ENSO), hurricane, cyc-
                   waterways [9]. Extreme precipitation events may
                                                                                                       lone, other extreme storm, seawater inundation, ex-
                   also increase the risk of flooding in many areas, in-
                                                                                                       treme water run-off, and extreme changes in water
                   creasing human exposure to waterborne pathogens
                                                                                                       level or temperature (see Table 1). A list of known
                   [10]. Droughts or extended dry periods are known to
                                                                                                       waterborne pathogens was compiled and used to
                   reduce the volume of river flow and potentially in-
                                                                                                       generate key search terms for the identification of
                   crease the concentration of effluent-derived patho-
                                                                                                       waterborne infectious disease. Search strategies which
                   gens, due to reduced dilution by stream-receiving
                                                                                                       combined the key search terms and subject headings
                   waters [11].
                                                                                                       for both waterborne infectious disease and extreme
                      Outbreaks caused by the contamination of com-
                                                                                                       water-related weather events were used to interrogate
                   munity water systems have the potential to cause ex-
                                                                                                       the online databases. The titles, key words and ab-
                   tensive disease [12], particularly where the public
                                                                                                       stracts of articles included in the online databases
                   health infrastructure is less resilient. Waterborne dis-
                                                                                                       were searched for these search terms. It was not
                   eases are expected to rise with increases in extreme
                                                                                                       possible to search the full texts as not all citations had
                   rainfall and deterioration in water quality following
                                                                                                       been indexed and scanned into the online databases
                   wider drought events [2]. It is important to establish
                                                                                                       and relevant published articles without abstract or
                   the current impact of such events on public health to
                                                                                                       key words may not have been picked up based on
                   allow future predictions, aid policy formulation, and
                                                                                                       their titles alone. An example of the search strategies
                   improve adaptive capacity. The impact of recent
                                                                                                       used can be found in the Supplementary online
                   events demonstrates that even high-income countries
                                                                                                       material (Appendix 1). The grey literature was also
                   are not well prepared to cope with extreme weather
                                                                                                       searched on 12 May 2010 using the Program for Moni-
                   events [2]. There is also limited information available
                                                                                                       toring Emerging Diseases (ProMed-mail) [14] and an
                   on how different extreme water-related weather events
                                                                                                       online search engine [15]. Both sources were searched
                   will impact different geographical areas and patho-
                                                                                                       using combinations of the key search terms; a list of
                   gens. This is the first global systematic review of
                                                                                                       these combinations can be found in Appendix 2 (online).
                   the impact of weather on waterborne disease. The
                   aim was to assess how the different categories of ex-
                   treme water-related weather events impact water-                                    Selection criteria
                   borne disease, by geographical area, pathogen and
                                                                                                       All waterborne pathogens resulting in infectious dis-
                   outcome.
                                                                                                       ease were included, with the exception of those that
                                                                                                       require an obligate intermediary host. All study de-
                                                                                                       sign types were included. Non-English language stu-
                   METHODS
                                                                                                       dies were included and translated. To check whether
                   A full protocol was written a priori specifying the                                 key papers had been identified and to validate
                   search strategy, selection criteria, and data extraction                            the sensitivity of the search strategy, the following
                   and analysis strategies (available upon request).                                   journals were manually searched : Journal of Water

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Extreme weather and waterborne disease                            673

                           Table 1. Key search terms used to identify waterborne disease outbreaks involving an
                           extreme water-related weather event

                           Waterborne disease outbreak                                        Extreme water-related weather event

                           Water ; waterborne                                                 Ocean ; sea ; seawater ; lake; river ;
                                                                                              rain ; rainfall ; water supply; water movement ;
                           WITH
                                                                                              weather ; storm ; climate ; precipitation
                           Infection ; infectious ;                                           WITH
                           communicable ; disease ; illness;                                  Extreme ; spate ; excessive ; surge; disaster
                           enteric ; pathogen ; organism;
                                                                                              OR
                           agent; WBDO ; gastroenteritis ;
                           AG; Giardia ; Cryptosporidium;                                     Floodwater ; drought ; water scarcity;
                           E. coli ; Shigella ; Legionella;                                   heavy rainfall ; flood; heavy precipitation ;
                           Salmonella; Naegleria fowleri ;                                    el Niño; la Niña
                           Plesiomonas shigelloides ; Campylobacter;
                           Amoebiasis ; Dracunculus ; Hymenolepis ;
                           Ascaris; Enterobius ; Mycobacterium marinum ;
                           dysentery; Leptospira ; Vibrio ; Enterovirus ;
                           Norovirus; Norwalk ; Hepatitis A ; HAV ;
                           Hepatitis E; Adenovirus ; Astrovirus ; Calicivirus ;
                           Coronavirus; Poliomyelitis ; Poliovirus ;
                           Picornaviridae ; Coxsackievirus ; Echovirus ;
                           Rotavirus ; Reovirus
                           WITH
                           Outbreak; epidemic ; occurrence
                           WITH
                           Human

          and Climate Change ; Journal of Water and Health ;                                      Population : human.
          Water ; Water Policy ; and Water Research. The                                          Event : extreme water-related weather event.
          reference lists of included publications were also                                      Outcome measure : waterborne disease outbreak
          checked for further eligible articles. Duplicate articles,                              (described as waterborne by the author or attribu-
          identified from their titles, were included only once.                                   ted to a pathogen which is transmitted solely
             Citations identified from the literature were                                         through water).
          screened for inclusion criteria by two independent
                                                                                              Exclusion criteria were as follows :
          reviewers (R.S., D.T.), first using the titles and ab-
          stracts, then using the full papers (where available).                                  Literature type : news articles.
          Publications identified from the online search engine                                    Population : non-human ; displaced populations.
          were first screened for inclusion criteria by one re-                                    Event : extreme climatic weather events not in-
          viewer (K.C.) using either the abstract or first page.                                   volving water.
          Relevant documents were downloaded in full and                                          Outcome measure : non-waterborne disease out-
          screened by two independent reviewers (R.S., D.T.)                                      breaks; outbreaks due to pathogens with obliga-
          alongside the articles published in peer-reviewed                                       tory, intermediary hosts.
          journals. The ProMED reports were screened by one
                                                                                              Algorithms and notes for citation review were devel-
          reviewer (K.C.) and inclusion criteria applied.
                                                                                              oped to reduce variation between reviewers and
          Relevant ProMED reports were analysed separately
                                                                                              to clarify which pathogens and events should be
          to allow comparison with the published literature.
                                                                                              included (see Fig. 1). Reviewer agreement on the in-
                                                                                              clusion/exclusion of abstracts and full papers was
          Inclusion criteria were as follows :
                                                                                              80.4% and 75.4 %, respectively. Any disagreement
               Literature type : published articles ; official pub-                             over inclusion of a publication was resolved by a third
               lications.                                                                     reviewer (K.C.).

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674         K. F. Cann and others

                                                                                                       environmental events rarely provide sufficient detail.
                              Citation inspection                                                      Articles were rated according to their applicability as
                                                                                                       either ‘ direct ’ to signify strong causality and direct
                                                                                                       applicability of its content ; ‘moderate ’, if they pro-
                                                                NO                                     vided strong circumstantial evidence but data taken
                          Is an extreme water* event                            Exclude:
                                  mentioned?                                No extreme event           from these articles required careful interpretation be-
                                                                                                       fore it could be used ; or ‘indirect ’, if they did not
                   YES / UNCLEAR                                                                       support causal inference and if the content could only
                      Is an outbreak/epidemic/increase
                                                                NO                                     be used as background information.
                                                                               Exclude:
                        in cases of infectious disease
                                                                              No outbreak
                                                                                                          Large differences in study designs and in the popu-
                                 mentioned?                                                            lations involved precluded the pooling of data from
                   YES / UNCLEAR
                                                                                                       different outbreaks and a traditional meta-analysis.
                                                                                                       Frequency distributions of the type of publication,
                      Is the outbreak/epidemic/increase        NO
                                                                               Exclude:                type of extreme water-related weather event, country
                           in cases due to waterbore
                                 pathogens†?
                                                                            Not waterborne             affected, and pathogens involved were listed. Those
                                                                                                       publications which provided information on the
                   YES / UNCLEAR                                                                       numbers of cases, deaths or attack rates were included
                                                                                                       in the quantitative synthesis which calculated geo-
                                    Include                                                            metric means (due to the highly skewed nature of the
                                                                                                       data) by causal pathogen and by type of weather
                   Fig. 1. Algorithm used by reviewers when screening ab-                              event. Numbers of cases were stratified by case defi-
                   stracts and grey literature to determine if inclusion criteria                      nition type : laboratory-confirmed, clinical diagnosis,
                   were met. * A list of examples of extreme water-related
                                                                                                       or self-reported.
                   events to be included was provided. # A list of examples of
                   waterborne pathogens to be included was provided

                   Data extraction                                                                     RESULTS
                   Data from included publications were extracted into a                               Evidence from the scientific literature
                   database using a custom-made form (K.C.). The pri-
                                                                                                       A total of 83 identified papers were included in the
                   mary outcome was the number of cases of waterborne
                                                                                                       analysis, four of which were not in English (Spanish,
                   disease as defined by the author. Where the number of
                                                                                                       Portuguese, French, Czech) (see Fig. 2). Full details
                   cases was stated in the publication, these data were
                                                                                                       of included publications are available in Appendix 4
                   extracted regardless of whether these were laboratory
                                                                                                       (online). Four relevant papers were identified by hand
                   confirmed, self-reported, or diagnosed on clinical
                                                                                                       searching of relevant journals; all of which had
                   grounds. Where the number of cases was stated to be
                                                                                                       been identified by the search strategy and already in-
                   an estimate this was recorded. Secondary outcome
                                                                                                       cluded.
                   measures were the attack rate and the number of
                                                                                                          Of the 83 papers identified, 35 (42.2 %) were out-
                   deaths. Other data extracted included : citation de-
                                                                                                       break investigations, 28 (33.7 %) were other quanti-
                   tails, type of study, applicability, details of the ex-
                                                                                                       tative studies, 13 (15.7%) were reviews, three (3.6%)
                   treme water-related weather events, water quality,
                                                                                                       were qualitative studies, two (2.4%) were mixed
                   details of the outbreak, and details of how the weather
                                                                                                       methods studies, one (1.2%) was a case study, and
                   event was thought to have led to the outbreak. Full
                                                                                                       one (1.2%) was an official report. Eight (9.6%)
                   details of extraction fields used are available in
                                                                                                       of these publications were classed as having direct
                   Appendix 3 (online). Where more than one pub-
                                                                                                       applicability, 48 (57.8 %) had moderate applicability,
                   lication referred to the same study, any further rel-
                                                                                                       and 27 (32.5%) had indirect applicability.
                   evant data available on the event found in subsequent
                                                                                                          The papers included 93 accounts of 87 different
                   accounts were added to the initial data identified.
                                                                                                       waterborne outbreaks involving extreme water-
                                                                                                       related weather events from 29 different countries
                   Data analysis
                                                                                                       (eight reviews documented two or three outbreaks).
                   No pre-defined tool for the assessment of the qua-                                   The majority of the reported outbreaks, where ex-
                   lity of evidence was used as publications about                                     treme water-related weather events were involved,

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Extreme weather and waterborne disease                            675

                                                      Records identified through                     Additional records identified
                                                        database searching                             through online search
                                                             (n = 281)                                        (n = 18)

                                                                         Records after duplicates removed
                                                                                     (n = 196)

                                                                                  Records screened                            Records excluded
                                                                                     (n = 196)                                   (n = 133)

                                    Additional records                        Full-text articles assessed                      Full-text articles
                                     identified from                                  for eligibility                              excluded
                                      reference lists                                   (n = 88)                                     (n = 5)
                                         (n = 25)

                                                                                   Studies included
                                                                                in qualitative synthesis
                                                                                        (n = 83)

                                                                                 Studies included in
                                                                                quantitative synthesis
                                                                                       (n = 65)

                   Fig. 2. Flow chart detailing the passage of scientific and grey literature through the systematic review process.

          were in North America, followed by Asia and Europe.                                 events reported more than one event to have been in-
          The pathogens involved were specified in 74 (85.1 %)                                 volved. Heavy rainfall and flooding were the most
          of the outbreaks following extreme weather events                                   common combination of events preceding outbreaks
          and are listed in Table 2. The most commonly re-                                    (27.6 % of all accounts). Heavy rainfall was also
          ported were Vibrio spp. (28.4 %) and Leptospira spp.                                linked with heavy water run-off and hurricane, and
          (17.6 %). Most reported outbreaks of Vibrio spp. fol-                               flooding was also linked with hurricane. Fifty-four
          lowing extreme water-related weather events occurred                                (58.0 %) reports of outbreaks following extreme
          in Asia, followed by Africa and South America, while                                water-related weather events gave details of how the
          most reported outbreaks due to Leptospira spp. were                                 event was thought to have led to the outbreak. In just
          in North America or Asia. More than one pathogen                                    over half (53.7%) of reports providing this infor-
          was identified on 16/74 (21.6 %) occasions, mostly in                                mation, the extreme water-related weather event
          North America or Asia (37.5 % and 31.3 %, respect-                                  caused the outbreak through contamination of the
          ively), followed by Europe (18.8%). Of the 74 out-                                  water supply, usually through increased run-off of
          breaks in which the causal pathogen was identified, 31                               water from the surrounding area (22.2%) or by in-
          (41.9 %) reported testing the water supply. Of these,                               undation (20.4 %). Exposure to contaminated water
          the causal pathogen was stated to have been identified                               by physical activity occurred in 16.7% of the out-
          in just over half (54.8 %), confirming the water supply                              break reports associated with extreme water-related
          as the source.                                                                      weather events, but this was recreational activity in
             Out of all outbreaks associated with extreme water-                              only 3.7 %. More commonly contact with floodwater
          related weather events, heavy rainfall and flooding                                  occurred while wading or during the cleaning up
          were by far the most commonly reported antecedents                                  process (9.3 %). A change in the survival rates of
          (in 55.2% and 52.9 % of published accounts, re-                                     pathogens due to changing environmental conditions
          spectively) (see Fig. 3). Forty-five (51.7 %) of the                                 (such as water temperature or stagnation) was
          outbreaks following extreme water-related weather                                   thought to be the cause in 9.3 % of outbreak reports

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676         K. F. Cann and others

                   Table 2. Waterborne pathogens implicated in outbreaks following extreme water-related weather events identified
                   from the scientific literature (6 May 2010) and ProMED reports (12 May 2010)

                                                                                             No. (%)* of times reported

                   Waterborne pathogen                                                       Scientific literature                                ProMED reports

                   All viruses                                                               19 (25.7)                                             5 (2.4)
                     Hepatitis virus                                                          7 (9.5)                                              3 (1.4)
                        Hepatitis A virus                                                     4 (5.4)                                              2 (0.9)
                        Hepatitis E virus                                                     2 (2.7)                                              1 (0.5)
                        Hepatitis virus : type unknown                                        1 (1.4)                                             —
                     Norovirus                                                                6 (8.1)                                              1 (0.5)
                     Rotavirus                                                                3 (4.1)                                              1 (0.5)
                     Adenovirus                                                               2 (2.7)                                             —
                     Enterovirus                                                              1 (1.4)                                             —
                   All bacteria                                                              66 (89.1)                                           198 (93.8)
                     Vibrio spp.                                                             21 (28.4)                                           145 (68.7)
                        Vibrio cholerae                                                      20 (27.0)                                           137 (64.9)
                        Other Vibrio spp.                                                     2 (2.7)                                              8 (3.8)
                     Leptospira spp.                                                         13 (17.6)                                            36 (17.1)
                        Leptospira interrogans                                                4 (5.4)                                             —
                        Leptospira sp. not known                                              9 (12.2)                                            36 (17.1)
                     Campylobacter spp.                                                      10 (13.5)                                             3 (1.4)
                        Campylobacter jejuni                                                  6 (8.1)                                             —
                        Campylobacter sp. not known                                           4 (5.4)                                              3 (1.4)
                     Escherichia coli                                                         9 (12.2)                                             9 (4.3)
                     Shigella spp.                                                            4 (5.4)                                             —
                        Shigella flexneri                                                      2 (2.7)                                             —
                        Shigella boydii                                                       2 (2.7)                                             —
                     Salmonella spp.                                                          3 (4.1)                                              5 (2.4)
                        Salmonella typhi                                                      1 (1.4)                                              4 (1.9)
                        Salmonella sp. unknown                                                2 (2.7)                                              1 (0.5)
                     Burkholderia pseudomallei                                                3 (4.1)                                              9 (4.3)
                     Yersinia enterocolitica                                                  2 (2.7)                                             —
                     Aeromonas spp.                                                           1 (1.4)                                             —
                   All protozoa                                                              16 (21.6)                                            12 (5.7)
                     Cryptosporidium spp.                                                     9 (12.2)                                             3 (1.4)
                        Cryptosporidium parvum                                                2 (2.7)                                             —
                        Cryptosporidium sp. not known                                         7 (9.5)                                             3 (1.4)
                     Giardia lambia                                                           5 (6.8)                                             —
                     Acanthamoeba spp.                                                        1 (1.4)                                             —
                     Cyclospora spp.                                                          1 (1.4)                                             —

                   * Percentage of either 74 outbreak accounts or 211 ProMED reports reporting the pathogens involved.

                   in which an extreme water-related weather event was                                 infection was through the mains water supply for
                   implicated. Failure to cope by the water treatment                                  66.9 %, through other treated water for 37.0 %, and
                   plant were blamed in 7.4 % of papers providing in-                                  through a well supply for 29.6 %. By comparison,
                   formation on the role of the extreme water-                                         22.2 % were infected through environmental exposure
                   related event in the outbreak. Failure or inability                                 and 11.1 % of the outbreaks involved both environ-
                   to cope by sewage systems, resulting in contamination                               mental exposure and the water supply. Campylobacter
                   of the water supply were also blamed in 7.4 % of                                    spp. and Cryptosporidium spp. were common causal
                   reports.                                                                            pathogens in outbreaks associated with extreme
                      Of 27 accounts of waterborne outbreaks following                                 water-related weather events originating from treated
                   extreme water-related weather events from developed                                 mains water. Waterborne pathogens originating from
                   countries which reported the information, the route of                              environmental exposure following extreme weather

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          Table 3. Attack rates reported during outbreaks of infectious disease due to waterborne pathogens, where extreme
          water-related weather events are involved identified from the scientific literature (6 May 2010), by pathogen

                                                              No. reporting                        Mean attack                Median attack                    Lowest attack                  Highest attack
          Pathogen                                            attack rate*                         rate (%)#                  rate (%)                         rate reported (%)              rate reported (%)

          Viruses                                             10                                    7.8                       27.6                             0.2                            79.0
          Rotavirus                                            1                                   79.0                       79.0                            79.0                            79.0
          Norovirus                                            3                                   44.0                       36.2                            30.6                            77.0
          Hepatitis A                                          3                                    3.1                        5.5                             0.2                            24.5
          Hepatitis E                                          2                                    3.4                       29.2                             0.2                            58.2
          Enterovirus                                          1                                    0.4                        0.4                             0.4                             0.4
          Bacteria                                            16                                    0.8                        0.5
678                                           K. F. Cann and others

                    (a)                                                                                                                                   (b)
                                                          120                       (4)                                                                                       70000
                                                                                                                                                                                                     (2)

                                                                                                                                                      Mean number of cases
                                                                                                                                                                              60000
                                   Mean number of cases
                                                          100
                                                                                                                                                                              50000
                                                           80
                                                                                                                                                                              40000
                                                           60
                                                                  (1)                                                                                                         30000
                                                           40                                                     (1)
                                                                                                                                                                              20000
                                                           20                                               (2)         (8)
                                                                        (3)                     (1)                                                                           10000
                                                                              (1)                                             (0) (0) (0) (0)                                          (0) (0) (0)         (0) (0) (0) (0) (0) (0) (2) (0) (7) (2)
                                                                                          (0)         (0)
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                                                          2500                                                                                                                18000                                                        (8)
                                                                                                                                    (2)                                       16000

                                                                                                                                                      Mean number of cases
                    Mean number of cases

                                                          2000                                                                                                                14000
                                                                                                                                                                              12000
                                                          1500                                                                                                                10000
                                                                                                                                                                               8000
                                                          1000                                                                            (4)                                  6000
                                                                                                                                                                               4000                                (1)
                                                           500                                                    (1) (3)                                                                                                                        (3)
                                                                                                                              (1)               (1)                            2000    (0) (0) (1) (0) (0) (0)           (0) (0) (1) (1)               (1)
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                   Fig. 4. Mean numbers of cases reported in accounts of waterborne disease outbreaks where extreme weather events have
                   been implicated, by pathogen and case definition type (scientific literature) : (a) using a laboratory-confirmed diagnosis,
                   (b) using a self-reported diagnosis, (c) using a clinical diagnosis, (d) where type of diagnosis is not reported. Figures in
                   parentheses indicate number of accounts reporting this information.

                   reported laboratory-confirmed cases, 13 (20.6%) re-                                                                                             following a severe storm, as shown in Figure 5. Of
                   lied on self-reporting of cases, 13 (20.6%) relied on a                                                                                        those using a clinical diagnosis or where the type
                   clinical diagnosis, and 16 (25.4 %) did not report this                                                                                        of case definition was not given, the highest number
                   information.                                                                                                                                   of cases was seen following a cyclone and seawater
                      Where a laboratory-confirmed or self-reported case                                                                                           inundation.
                   definition was used, the highest mean number of cases
                   resulted from Cryptosporidium outbreaks, as shown
                                                                                                                                                                  Evidence from ProMED reports
                   in Figure 4. However, most outbreaks using a self-
                   reported case definition identified multiple pathogens                                                                                           There were 235 eligible ProMED reports of water-
                   (7/11). Where a clinical diagnosis was used or the type                                                                                        borne outbreaks following extreme water-related
                   of case definition was not given, V. cholerae outbreaks                                                                                         weather events, involving 304 events from 66 different
                   following extreme water-related weather events re-                                                                                             countries. The majority of these reports were in
                   sulted in the highest reported mean number of cases.                                                                                           Africa, followed by Asia and North America. Far
                   Outbreaks in which the type of case definition was not                                                                                          more of the outbreaks following extreme water-re-
                   given reported the highest mean number of cases for                                                                                            lated weather events were based in Africa than in the
                   any pathogen (n=2726), followed by self-reported                                                                                               scientific literature (42.6 % vs. 6.9 %, respectively) and
                   cases (n=994), clinical diagnoses (n=309), and lab-                                                                                            less were based in either Europe or North America
                   oratory-confirmed (n=19). Of those accounts re-                                                                                                 (4.4% vs. 18.4% and 12.0 % vs. 33.3 %, respectively).
                   porting laboratory-confirmed cases or self-reported                                                                                             The pathogen was given in 211 (89.8 %) reports, of
                   cases, the highest mean number of cases was seen                                                                                               which V. cholera was by far the commonest (64.9 %),

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. https://doi.org/10.1017/S0950268812001653
Extreme weather and waterborne disease                                           679

                          (a)                                                                                                      (b)
                                                180                                                                                                        450000
                                                                                                     (2)                     (2)                                                                                       (1)
                                                160
                        Mean number of cases

                                                                                                                                    Mean number of cases
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                                                140                                                                                                        350000
                                                120                                                                                                        300000
                                                100                                                                                                        250000
                                                 80                                                                                                        200000
                                                 60                                                                                                        150 000
                                                 40                                                                                                        100 000
                                                    (12) (13)     (2)                    (3)                                                                50000                                                                        (1) (0)
                                                 20           (0)                  (0)         (0)         (0)   (0)   (0)                                                (7) (7) (0)          (0)   (4)   (0) (0)           (0)   (0)
                                                  0                                                                                                              0

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                                                                                         (1)                     (1)                                       120000
           Mean number of cases

                                                                                                                                    Mean number of cases
                                       12000                                                                                                                                                               (1)                     (1)
                                                                                                                                                           100000                                                (2)
                                       10000
                                                                                                                                                            80000
                                               8000
                                                                                                                                                            60000
                                               6000
                                                                                                                                                            40000                              (1)
                                               4000                                                  (1)                                                                                                                     (3)
                                               2000                                                                                                         20000
                                                         (8)     (8) (0)       (3) (1)                     (0)         (1)   (0)                                         (8) (8)         (3)         (0)               (0)               (0)   (0)
                                                                                               (0)
                                                  0                                                                                                              0

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          Fig. 5. Mean numbers of cases reported in accounts of waterborne disease outbreaks where extreme weather events have
          been implicated, by event and case definition type (scientific literature) : (a) using a laboratory-confirmed diagnosis, (b) using
          a self-reported diagnosis, (c) using a clinical diagnosis, (d) where type of diagnosis is not reported. Figures in parentheses
          indicate number of accounts reporting this information.

          of which 65.4 % occurred in Africa and 20.6 % oc-                                                                                   The number of cases involved was reported in 174
          curred in Asia. Out of all ProMED waterborne out-                                                                                 (74.0 %) and the number of deaths in 145 (61.7 %)
          break reports which were associated with an extreme                                                                               of the ProMED accounts of waterborne outbreaks
          water-related weather event, the most common events                                                                               following extreme water-related weather events. We
          were again flooding and heavy rainfall (see Fig. 3),                                                                               were unable to stratify ProMED reports by type of
          with 15.7 % of reports involving both. Sixty-four                                                                                 case definition due to the limited detail available in the
          (27.2 %) of the reports implicated more than one type                                                                             brief reports.
          of extreme water-related weather event. These also
          linked heavy rainfall with El Niño, drought and cyc-
                                                                                                                                            DISCUSSION
          lone, while flooding was also linked with extreme
          storm, cyclone, hurricane, drought and tidal surge.                                                                               This review has a number of limitations which can be
          Ninety-eight (41.7 %) of the reports of waterborne                                                                                considered in two groups ; systematic review limita-
          outbreaks following extreme water-related weather                                                                                 tions and primary literature reporting limitations. The
          events gave details of the likely cause; the most com-                                                                            identification of so many suitable new references
          mon were contamination of water (32.9%), shortage                                                                                 through the reference lists of publications identified
          of clean drinking water (18.9%), and poor sanitation                                                                              by the search engines, i.e. 23.1% of all references in-
          and hygiene following the event (14.7 %).                                                                                         cluded, suggests that the search strategies may have

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. https://doi.org/10.1017/S0950268812001653
. https://doi.org/10.1017/S0950268812001653
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                                                                                                                                                                                                                                                                                                                                                                                 680
                                                                                                                                                                                                                                                                                                                                                                                 K. F. Cann and others
                                                                                                                                                                                                     Table 4. Number of known deaths during outbreaks of infectious disease due to waterborne pathogens, where extreme water-related weather events are involved
                                                                                                                                                                                                     identified from the scientific literature (6 May 2010) and ProMED (12 May 2010), by event

                                                                                                                                                                                                                                     Scientific literature                                                  ProMED reports

                                                                                                                                                                                                                                     No. reporting    Mean          Median       Lowest       Highest      No. reporting   Mean          Median       Lowest        Highest
                                                                                                                                                                                                     Extreme event*                  no. deaths       no. deaths#   no. deaths   no. deaths   no. deaths   no. deaths      no. deaths#   no. deaths   no. deaths    no. deaths

                                                                                                                                                                                                     Heavy rainfall                   8               10            11            1           253           54              19            19           0             1156
                                                                                                                                                                                                     Flooding                        14               29            42            1           500           80              19            18           0            70 000
                                                                                                                                                                                                     Heavy rainfall and flooding       6               11            15            0            53           23              13            12           1               352
                                                                                                                                                                                                     Cyclone                          2               64            66           51            81            8              37            18           1            70 000
                                                                                                                                                                                                     Drought                          1                2             2            2             2           19              15            12           1               274
                                                                                                                                                                                                     Extreme water run-off            —                —             —            —             —
                                                                                                                                                                                                     Severe storm                     1               15            15           15            15           5               49            89          5               167
                                                                                                                                                                                                     Extreme water temperature       —                —             —            —             —            —               —             —           —                —
                                                                                                                                                                                                      change
                                                                                                                                                                                                     Hurricane                       —                —             —            —             —             8               3             4           0                 5
                                                                                                                                                                                                     ENSO                            —                —             —            —             —            15              13             5           1             2231
                                                                                                                                                                                                     Seawater inundation              2               64            66           51            81            1              28            28          28                28
                                                                                                                                                                                                     Extreme change in water level   —                —             —            —             —            —               —             —           —                 —
                                                                                                                                                                                                     Other                           —                —             —            —             —            —               —             —           —                 —
                                                                                                                                                                                                     All                             16               20            28            1           500          190             221           263          42           144 018

                                                                                                                                                                                                     * Where more than one extreme event was involved, the figures were imputed into each type of event.
                                                                                                                                                                                                     # Geometric mean (accounts reporting 0 not included).
. https://doi.org/10.1017/S0950268812001653
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                                                                                                                                                                                                     Table 5. Number of known deaths during outbreaks of infectious disease due to waterborne pathogens, where extreme water-related weather events are involved
                                                                                                                                                                                                     identified from the scientific literature (6 May 2010) and ProMED reports (12 May 2010), by pathogen

                                                                                                                                                                                                                           Scientific literature                                                   ProMED reports

                                                                                                                                                                                                                           No. reporting     Mean no.     Median no.   Lowest no.   Highest no.   No. reporting    Mean no.   Median no.   Lowest       Highest
                                                                                                                                                                                                     Pathogen              no. deaths#       deaths*      deaths       deaths       deaths        no. deaths#      deaths*    deaths       no. deaths   no. deaths

                                                                                                                                                                                                     Viruses                1                 1            1            1             1             1              127        127          127             127
                                                                                                                                                                                                     Enterovirus            1                 1            1            1             1             0               —          —            —               —
                                                                                                                                                                                                     Hepatitis E virus      0                —            —            —             —              1              127        127          127             127
                                                                                                                                                                                                     Bacteria              11                24           41            1           276           130               18         14            0          70 000
                                                                                                                                                                                                     Vibrio cholera         6                70           52           41           276            90               24         19            1          70 000
                                                                                                                                                                                                     Non-choleragic         0                —            —            —             —              7                3          4            0               5
                                                                                                                                                                                                      Vibrio spp.
                                                                                                                                                                                                     Leptospira             4                 4            4            1            15            23               17         17            0             182
                                                                                                                                                                                                     Salmonella typhi       0                —            —            —             —              1                2          2            2               2

                                                                                                                                                                                                                                                                                                                                                                     Extreme weather and waterborne disease
                                                                                                                                                                                                     Shigella spp.          1                51           51           51            51             0               —          —            —               —
                                                                                                                                                                                                     E. coli                0                —            —            —             —              4                3          4            1               6
                                                                                                                                                                                                     B. pseudomallei        0                —            —            —             —              5                6          7            1              15
                                                                                                                                                                                                     Protozoa               0                —            —            —             —              0               —          —            —               —
                                                                                                                                                                                                     Multiple pathogens     4                26           44            2           500             0               —          —            —               —
                                                                                                                                                                                                     Not stated             1                42           42           42            42            14               35         54            2           1350
                                                                                                                                                                                                     All                   16                20           28            1           500           145              186        234          134          71 687

                                                                                                                                                                                                     * Geometric mean.
                                                                                                                                                                                                     # Includes only those accounts which report this information.

                                                                                                                                                                                                                                                                                                                                                                     681
682         K. F. Cann and others

                   been too specific. It is difficult to achieve the optimal                              evidence but in need of careful interpretation ’ and few
                   balance between sensitivity and specificity, as time                                 of the publications described a comparison group.
                   and resource constraints limited the number of ab-                                  The limited reporting of many of the included studies
                   stracts which could be screened for inclusion and a                                 also prevented many in-depth conclusions being
                   number of known papers were not identified by this                                   drawn.
                   approach. This was due to relying on authors men-                                      These study reporting limitations highlight key
                   tioning the extreme water-related weather event in                                  areas which future outbreak reports should seek to
                   either the title, abstract or key words to enable them                              address. Future research in this area should aim to
                   to be identified by the search strategy. Papers without                              measure and report clearly population, weather
                   abstracts or key words may not have been identified                                  and water parameter details when investigating
                   on the basis of their title alone, for example, the article                         waterborne disease outbreaks where an extreme
                   by Walzer et al. on the balantidiasis outbreak in Truk                              water-related weather event is thought to be involved.
                   following a typhoon [16]. Papers where the event was                                Where an outbreak is reported, some effort should
                   only mentioned as a detail in the full text and not in                              also be made to classify the probable route (or routes)
                   the title, key words or abstract may also have been                                 of transmission. This would allow a greater pro-
                   missed. We therefore suggest that future reviews take                               portion of waterborne outbreaks to be identified and
                   a more comprehensive approach. It was also very                                     included in analyses such as these. Where the number
                   difficult to make comparisons between outbreaks fol-                                  of cases involved in an outbreak is reported, the case
                   lowing different types of extreme events as there were                               definition used should be clearly stated. If an extreme
                   vast differences in key characteristics of the popula-                               water-related climatic event is thought to be im-
                   tions affected. Where reported, there was also sub-                                  plicated in an outbreak, details of how it may have led
                   stantial variation in case definitions between                                       to contamination of the water should be reported. It is
                   outbreaks identified ; accounts based on self-reported                               also important to raise awareness of the potential role
                   cases had a substantially higher mean number of cases                               of such events in waterborne outbreaks, to encourage
                   than those requiring a clinical diagnosis or laboratory                             authors to question explicitly whether such an event
                   confirmation and those that did not report the type of                               occurred prior to the outbreak and if so, to detail it in
                   case definition used at all had, on average, the largest                             a structured way.
                   number of cases. Calculation of attack rate is also                                    The global distribution of waterborne outbreaks
                   likely to have varied by study.                                                     following extreme water-related weather events as re-
                      The review also suffered from a lack of reporting of                              ported in the scientific literature is also likely to be
                   detail. For example, it was difficult to assess the evi-                              prone to considerable publication bias. A greater
                   dence supporting the classification of the outbreaks as                              proportion of those identified through ProMED were
                   waterborne or the degree of association between                                     in Africa and South America compared to those re-
                   water and disease given the limited amount of infor-                                ported in peer-reviewed journals, with less from
                   mation often provided, particularly in the ProMED                                   North America or Europe. Outbreaks following
                   reports. For example, where testing of the water sup-                               drought or an ENSO event, both more common in
                   ply was reported, the causal pathogen was identified                                 developing countries, were more often reported via
                   in just over half of the outbreaks. A quarter of                                    ProMED than in the scientific literature but out-
                   those which provided the number of cases seen                                       breaks following hurricanes were more often reported
                   did not report the type of case definition used, i.e.                                in the latter, with 40.8 % from the USA alone. Risk of
                   whether they were laboratory-confirmed, clinically                                   diarrhoeal disease outbreaks following natural dis-
                   diagnosed, or self-reported cases. Details of the                                   asters has previously been found to be higher in de-
                   extreme water-related weather events thought to be                                  veloping countries than in industrialized countries
                   involved in the outbreaks, such as the amount of                                    [17]. Flooding events, for example, in high-income
                   precipitation seen or parameters such as water tem-                                 countries are rarely thought to result in epidemics of
                   perature, pH and level of turbidity, were rarely given.                             infectious disease or, where they do occur, they are
                   This severely limits the suitability of the results for                             thought to often be easily controlled and not wide-
                   extrapolation to different circumstances and geo-                                    spread due to the rapid implementation of prevent-
                   graphical locations. Such were the quality of the                                   ative measures [18, 19]. The scientific literature is also
                   literature identified, the majority of the data were                                 likely to be dominated by accounts of waterborne
                   classed only as providing ‘strong circumstantial                                    disease from higher-income countries, with greater

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Extreme weather and waterborne disease                            683

          academic and surveillance capacity. The amount and                                  the water source through run-off or inundation.
          type of literature published on an extreme weather                                  While in developing countries this was usually un-
          event, therefore, may not be proportionate to the size                              treated water, in developed countries, in the majority
          and impact of the event. Risk of publication bias was                               of cases, this was contamination of a treated water
          addressed, to some extent, by searching grey literature                             source. This suggests that even in developed countries
          and by comparisons with the ProMED reports.                                         the water supply system is not immune to the effects of
          However, ProMED is a passive reporting tool and                                     such events. Although well-managed public water
          there may also be discrepancies in reporting practices.                             supply systems are expected to be able to cope with
          Griffith et al. [20] found, for example, that outbreaks                               weather extremes, such extremes can cause both
          of cholera in Africa were more likely to be reported in                             physical and managerial stresses which may impact
          areas of international interest and where there were                                water quality [21]. For example, rainstorm events and
          fewer commercial consequences.                                                      following increases in natural organic matter have
             Nevertheless, this review suggests that outbreaks of                             been shown to significantly impair turbidity removal
          waterborne infectious disease do occur following ex-                                at water treatment works in England [22]. Similarly,
          treme water-related weather events in both developed                                the dry summer of 2003 and resulting low river flows
          and developing countries. This already constitutes a                                were shown to cause deterioration in water quality
          significant burden on public health and as the fre-                                  in The Netherlands [23]. Public health practitioners
          quency of such events increases, so too will associated                             and water companies should be aware of the risks
          outbreaks of disease. The outbreaks identified in this                               of waterborne disease outbreaks following these
          review are also likely to be underestimates of the true                             events. Addressing the infectious waterborne disease
          prevalence of outbreaks resulting from extreme water-                               consequences of climate change is likely to require
          related weather events due to under-reporting of                                    specific engineering solutions to protect potable
          waterborne outbreaks and the difficulties in identify-                                water.
          ing papers which implicate such events (see above).                                    The reported outbreaks associated with extreme
          Future research into what proportion of all water-                                  water-related weather events were primarily due to
          borne outbreaks involve an extreme weather event                                    heavy rainfall with or without flooding. Flooding may
          and what proportion of all extreme weather events                                   have resulted from heavy rainfall in many cases and
          result in waterborne outbreaks would help to estimate                               many of the other extreme water-related weather
          the true burden to public health.                                                   events may have involved heavy rainfall even if it was
             The impacts of extreme water-related weather                                     not specified in the paper or report. Authors may have
          events on waterborne disease will disproportionately                                focused only on the causal event and not its climatic
          affect certain populations and will likely compound                                  effects. Whereas much has been published on the
          existing health disparities. Less developed countries                               health impacts of flooding [24–26], there is less on the
          may be at greater risk due to both higher sensitivity                               impact of heavy rainfall which did not result in
          and lower adaptive capacity [21]. Non-climate stres-                                flooding, even though the latter may still result in
          sors such as poverty or conflict can increase vulner-                                pressure on the water supply. Studies have linked
          ability by reducing resilience and adaptive capacity                                waterborne disease with heavy rainfall in several
          due to competing resource needs [17]. Less developed                                countries [27–29]. Curriero et al. [27] reviewed 548
          countries are therefore thought to be more vulnerable                               disease outbreaks between 1948 and 1994 in the USA
          and less able to recover rapidly or effectively.                                     and found a significant association between rainfall
          Climate change is predicted to increase the burden of                               and illness ; 68% of the events were found to be pre-
          diarrhoeal disease in low-income regions by about                                   ceded by precipitation events above the 80th percen-
          2–5 % by 2020, while countries with an annual GDP                                   tile. While Thomas et al. [30] found that from 1975 to
          per capita of oUS$6000 are thought to be at no                                      2000 in Canada rainfall events over the 93rd percen-
          additional risk [21]. However, responses to recent ex-                              tile increased the risk of a waterborne disease out-
          treme weather events suggest higher levels of vulner-                               break by a factor of 2.3. In light of the expected
          ability in both developing and developed countries                                  increases in frequency of heavy rainfall events in
          than thought previously [2]. This review found that in                              many regions, it is important to assess the individual
          both developing and developed countries the most                                    impact of such events in local and regional areas
          common cause of outbreaks following extreme                                         and incorporate these into health and infrastructure
          water-related weather events was contamination of                                   policy.

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684         K. F. Cann and others

                      The scientific literature suggests that, of those                                 and the elderly, who are more likely to be based in and
                   extreme water-related weather events linked to                                      around the home, are more likely to be affected by
                   waterborne outbreaks, cyclones, other severe storms,                                flooding events with a rapid onset [35]. Indigenous
                   ENSO events, or seawater inundation result in the                                   populations are also likely to be greatly impacted due
                   highest numbers of cases of waterborne illness. Risk                                to their occupation of economically and politically
                   of seawater inundation is expected to increase over                                 marginal areas and fragile ecosystems [36]. Such
                   the next few decades, due to predicted sea level rise                               variability needs to be incorporated into the develop-
                   and increasing frequency of extreme weather events,                                 ment of any policies or interventions to improve
                   with the risk zone predicted to spread further inland                               adaptive capacity. There is evidence to suggest that
                   and higher [31]. ENSO is known to be linked with                                    individual weather-related extreme events can facili-
                   extreme water temperature change. Two of the four                                   tate adaptations such as policy and regulatory
                   accounts of outbreaks (both of which were cholera)                                  change, as immediately afterwards the policy climate
                   following an ENSO event in the scientific literature                                 may be more conducive to change [37]. Yet pressure
                   were also linked to an extreme water temperature                                    for a quick recovery and short-term risk reduction can
                   change. Studies have repeatedly linked ENSO events                                  actually result in greater vulnerability to future events
                   and extreme water temperature change to large-scale                                 [38, 39]. There is also a lack of information on avail-
                   V. cholerae outbreaks [32, 33] and V. cholerae is                                   able and successful extreme water-related weather-
                   known to show an increased growth rate at increased                                 event adaptation strategies for waterborne disease
                   temperatures, with increasing global temperatures                                   outbreaks. Research into the impact of waterborne
                   also expected to increase prevalence both geographi-                                outbreaks following extreme weather events on dif-
                   cally and temporally [34]. V. cholerae was by far the                               ferent sub-populations which may be particularly
                   most common pathogen implicated in outbreaks fol-                                   vulnerable and the effectiveness of different adap-
                   lowing extreme water-related weather events, from                                   tation strategies should be undertaken.
                   both the scientific literature and ProMED, which
                   may in part reflect the predominance of outbreaks
                                                                                                       CONCLUSIONS
                   following heavy rainfall and flooding. In a review of
                   ProMED cholera outbreak reports from 1995 to                                        Waterborne diseases are one of the major con-
                   2005, Griffith et al. [20] found that rainfall and                                    tributors to global disease burden and mortality [40].
                   flooding were the most common risk factors globally                                  Improving the understanding of the impact that the
                   (constituting 25% of all risk factors), alongside water                             different extreme water-related weather events have
                   source contamination (29 %) and refugee settings                                    on waterborne disease is an important step towards
                   (13 %). The number of cholera outbreaks reported                                    finding ways to mitigate the risks. At a time when cli-
                   following extreme water-related weather events may                                  mate change is predicted to increase both the frequency
                   also be attributable to a number of other factors such                              and intensity of extreme water-related weather events
                   as the severity of the disease or reporting bias. When                              in many regions, understanding and reducing the im-
                   assessing the risk to public health of such outbreaks it                            pact of these events is vital to the health of many.
                   is important to incorporate information not only
                   from the most likely extreme water-related weather
                                                                                                       S U P P LE M E N T A R Y M A T E R I A L
                   events (such as heavy rainfall and flooding), but also
                   those from lower-probability but higher consequence                                 For supplementary material accompanying this paper
                   events (such as ENSO or seawater inundation) [21].                                  visit http://dx.doi.org/10.1017/S0950268812001653.
                      The ability of a population to adapt and limit
                   the effects of such events is likely to depend on
                                                                                                       ACKNOWLEDGEMENTS
                   socioeconomic and environmental circumstances and
                   the availability of information and technology [21].                                The authors thank the Library and Knowledge
                   There is also evidence to show that human and social                                Management Team at Public Health Wales for their
                   capital are key determinants of adaptive capacity at                                help with the collation of supporting materials. We
                   all scales [21]. Adaptive capacity is uneven both be-                               also thank Dr Meirion Evans and the Reviewers at
                   tween and within societies. For example, following                                  Epidemiology and Infection for their helpful re-
                   weather-related disasters there is a differential impact                             commendations on the layout and content of this
                   on deaths and well-being by gender, while children                                  paper.

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Extreme weather and waterborne disease                            685

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