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. Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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.). Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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, Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
Extreme weather and waterborne disease 677 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) 0 0 um ni do p. te p . or je i pa p. M rae d us pa A pt E No pira dia li ch us ep e sp C. alle ch rus te p . do p. or je i um ni d pa p. us pa A pt E a ep le No Mu ae dia li ar co sp C. alle te t r tipl idi ju eu a s En sp He sp te No spir ar co He titis Le titis vir En sp idi ju V. vir eu a s t r ltip He sp He titis Le titis ole vir or r V. ovi os m or Gi E. ole No ul ps eb m ro ro Gi E. ps eb ro o r B. mo B. mo a a th th an an to to Ac yp Ac yp Cr Cr (c) (d) 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) (0) (0) (0) (0) (1) (0) (0) (0) 0 0 um ni do p. te p. or je i pa p. M rae d um ni us do p. te p. pa A pt E No pira dia li ch us ep e or je i pa p. No ul e d us pa A pt E No pira dia li ch us ep e sp C. alle sp C. alle ar co te ar co t r tipl M ra idi ju te t r tipl eu a s En sp idi ju He sp eu a s En sp He sp He titis Le titis He titis Le titis vir V. ovir vir V. vir ole or ole or os m os Gi E. m No ul Gi E. ps eb ro ps eb ro ro r B. mo B. mo a a th th an an to to Ac Ac yp yp Cr Cr 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 %), Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . 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 400 000 140 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 r r t re O rr t e Hu ding Dr e ll aw p. c orm el Cy f te n Dr inun e he te g h f fa r r t re O rri g rr t e Dr e ll aw p. c orm el Cy f te n on n Dr inun e -o wa tio ng te g h te eve ENS ev f he fa d in lo n n -o wa tio ca ng te eve ENS ev in Ot wa ou un ca op da l ha in Se em st rl wa ou c oo Ot un ra op da rri ha Se em st rl oo c ra Fl y Fl Hu y av av He er He wa S er wa S at y at y av av He He e e m m tre tre Ex Ex (c) (d) 14000 (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 r r t re O rr t e g D e ll aw p. c orm el Cy f te n Dr inun e r r t re O rr t e g D e ll aw p. c orm el te gh Cy f te n f he Dr inun e fa te gh lon din n f he -o wa tio ng fa te eve ENS ev lon din n -o wa tio ng te eve ENS ev ca in ca wa rou Ot un in wa rou op da Ot un ha Se em st rl c oo op da ha Se em st ra rl c oo rri ra rri Fl Hu y Fl Hu y av av He er He er wa S wa S at y at y av av He He e e m m tre tre Ex Ex 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 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
. https://doi.org/10.1017/S0950268812001653 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms 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 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms 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 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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. Downloaded from https://www.cambridge.org/core. 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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. Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
Extreme weather and waterborne disease 685 D E C L A R A T I O N O F IN T E R E S T mail (http://www.promedmail.org/). Accessed 2 June 2011. This work was supported by the European 15. Google. (http://google.com/#). Accessed 24 November Commission 7th Research Framework Programme 2010. ‘VIROCLIME ’ (Contract 243923). 16. Walzer PD, et al. Balantidiasis outbreak in Truk. American Journal of Tropical Medicine and Hygiene 1973; 22 : 33–41. 17. Watson J, Gayer M, Connolly MA. Epidemic risk REFERENCES after disasters. Emerging Infectious Diseases 2006; 12 : 1468. 1. Semenza JC, Menne B. Climate change and infectious 18. Aavitsland P, et al. Infections during the 1995 diseases in Europe. Lancet Infectious Diseases 2009; 9 : flood in Ostlandet. Prevention and incidence. Tids- 365–375. skrift for Den Norske Laegeforening 1996; 116: 2. Pachauri RK, Reisinger A (eds). Contribution of 2038–2043. Working Groups I, II and III to the fourth assessment 19. Wilder-Smith A. Tsunami in South Asia : what is the report of the Intergovernmental Panel on Climate risk of post-disaster infectious disease outbreaks ? Change. IPCC, Geneva, Switzerland (http://www.ipcc. Annals, Academy of Medicine, Singapore 2005; 34 : ch/publications_and_data/ar4/syr/en/contents.html). 625–631. Accessed 25 June 2012. 20. Griffith DC, Kelly-Hope LA, Miller MA. Review of re- 3. Füssel HM. An updated assessment of the risks from ported cholera outbreaks worldwide, 1995–2005. climate change based on research published since the American Journal of Tropical Medicine and Hygiene IPCC Fourth Assessment Report. Climatic Change 2006; 75 : 973–977. 2000; 97 : 469–482. 21. Parry ML, et al. (eds). Contribution of Working Group 4. Solomon SD, et al. Contribution of Working Group I to II to the fourth assessment report of the Inter- the Fourth Assessment Report of the Intergovernmental governmental Panel on Climate Change, 2007. Panel on Climate Change. Cambridge : Cambridge IPCC. Cambridge University Press: Cambridge, UK University Press, 2007. (http://www.ipcc.ch/publications_and_data/ar4/wg2/ 5. Kristie L, et al. Climate variability and change and their en/contents.html). Accessed 25 June 2012. health effects in small island states: information for 22. Hurst AM, et al. The impact of rainstorm events on adaptation planning in the health sector. Environmental coagulation and clarifier performance in potable water Health Perspectives 2006; 114: 1957–1963. treatment. Science of the Total Environment 2004; 321: 6. CCDR. Waterborne outbreak of gastroenteritis asso- 219–230. ciated with a contaminated municipal water supply, 23. Senhorst HA, Zwolsman JJ. Climate change and effects Walkerton, Ontario, May–June 2000. Canada Com- on water quality : a first impression. Water Science municable Disease Report 2000 ; 26 : 170–173. Technology 2005; 51 : 53–59. 7. Tinker SC, et al. Drinking water turbidity and emerg- 24. Malilay J. Floods. In: Noji EK, ed. The Public Health ency department visits for gastrointestinal illness in Consequences of Disasters. Oxford : Oxford University Atlanta, 1993–2004. Journal of Exposure Science and Press, 1997. Environmental Epidemiology 2008; 20 : 19–28. 25. Reacher M, et al. Health impacts of flooding in Lewes : a 8. Hunter PR. Climate change and waterborne and comparison of reported gastrointestinal and other ill- vectorborne disease. Journal of Applied Microbiology ness and mental health in flooded and non-flooded 2003; 94 : 37–46. households. Communicable Disease and Public Health 9. Semenza J, Nichols G. Cryptosporidiosis surveillance 2004; 7 : 39–46. and water-borne outbreaks in Europe. Eurosurveillance 26. Montana E, et al. Environmental risk factors associated 2007; 12 : E13–E14. with paediatric idiopathic pulmonary hemorrhage and 10. Fewtrell L, et al. The microbiology of urban UK flood- hemosiderosis in a Cleveland community. Pediatrics waters and a quantitative microbial risk assessment 1997; 99 : 8. of flooding and gastrointestinal illness. Journal of Flood 27. Curriero FC, et al. The association between extreme Risk Management 2011; 4: 77–87. precipitation and waterborne disease outbreaks in the 11. Senhorst HAJ, Zwolsman JJG. Climate change and ef- United States, 1948–1994. American Journal of Public fects on water quality : a first impression. Water Science Health 2001; 91 : 1194–1199. and Technology 2005; 51 : 53–59. 28. Miossec L, et al. Magnitude of rainfall on viral con- 12. Karanis P, Kourenti C, Smith H. Waterborne trans- tamination of the marine environment during gastro- mission of protozoan parasites : a worldwide review of enteritis epidemics in human coastal population outbreaks and lessons learnt. Journal of Water and [in French]. Revue Epidemiologie Sante´ Publique 2000; Health 2007; 5 : 1–38. 48 : 2S62–S71. 13. National Climatic Data Center. Extreme weather and 29. Hunter PR, et al. Quantitative microbial risk assessment climate events (http://lwf.ncdc.noaa.gov/oa/climate/se of the risks from very small rural water supplies. Risk vereweather/extremes.html). Accessed 17 January 2011. Analysis 2010; 31 : 228–236. 14. International Society for Infectious Diseases. ProMED- 30. Thomas MK, et al. A role of high-impact weather events Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
686 K. F. Cann and others in waterborne disease outbreaks in Canada, 1975–2001. change. Oxford : Tyndall Centre for Climate Change International Journal of Environmental Health Research Research, 2007 (http://www.ecdgroup.com/docs/lib_ 2006 ; 16 : 167–180. 004630823.pdf). Accessed 25 June 2012. 31. Nicholls RJ. Analysis of global impacts of sea-level rise: 37. Kingdon JW. Agendas, Alternatives and Public Policies. a case study of flooding. Physics and Chemistry of the New York. Harper-Collins, 1995. Earth 2002; 27 : 1455–1466. 38. Penning-Roswell EC, Johnson C, Tunstall SM. Signals 32. Pascual M, et al. Cholera dynamics and El-Nino- from pre-crisis discourse: Lessons from UK flooding Southern Oscillation. Science 2000; 289: 1766–1769. for global environmental policy change? Global Environ 33. Speelmon EC, et al. Cholera incidence and El-Nino- Chang 2006; 16 : 323–339. related higher ambient temperature. Journal of the 39. Pulwarty R, Broad K, Finan T. ENSO forecasts and American Medical Association 2000; 283: 3072–3074. decision making in Brazil and Peru. In: Bankoff G, 34. Lipp E, Huq A, Colwell R. Effects of global climate on Frerkes G, Hilhorst T, eds. Mapping Vulnerability : infectious disease : the Cholera model. Clinical Micro- Disasters, Development and People. London : Earthscan, biology Reviews 2002; 15: 757–770. 2003. 35. Fordham M. Gender, disaster and development : the 40. Prüss A, Havelaar A. The global burden of disease study necessity of integration. In: Pelling M, ed. Natural and applications in water, sanitation and hygiene. In: Disasters and Development in a Globalising World. Fewtrell L, Bartram J, eds. Water Quality : Guidelines, London : Routledge, 2003. Standards and Health. London : IWA Publishing, 2001, 36. Salick J, Byg A. Indigenous peoples and climate pp. 43–59. Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 26 Sep 2021 at 01:31:55, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0950268812001653
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