Examining the relationship between infectious diseases and flooding in Europe

Figures & data

Table 1. Search strategy

EXPOSURE (COMBINED WITH OR) dam, embankment*, flood*, hurricane*, inundation, monsoon*, overflow*, seawater intrusion, storm surge*, storm water*, tropical storm*, typhoon*, waterlogging

(AND)

OUTCOME (COMBINED WITH OR) amoebiasis, bacillary dysentery, burul*, campylo*, chikungunya, cholera, communicable disease*, contamination, crypto*, dengue, dengue virus, dermatitis, diarrhea*, diarrhea*, disease*, disease vector*, disease outbreak*, epidemic*, enteric fever, Escherichia coli, gastrointestinal, giardia*, hanta virus infections, health, health effect*, health impact*, hemorrhagic fever, hepatitis A, hepatitis E, illness, infectio*, infectious disease*, Japanese encephalitis, legionellosis, leptospirosis, lyme disease, lymphatic filariasis, malaria, morbidity, mosquito*, norovirus, naeg*, outbreak*, onchocerciasis, physical health, plague, pollut*, public health, q fever, risk factor*, rodent*, rodentborne, rodent-borne, rodent related, rodent-related, salmonellosis, sars virus, severe acute respiratory syndrome, shigellosis, schistosomiasis, tick*, tick-borne encephalitis, tularaemia, tularemia, typhoid, water, waterborne, water-borne, water related, water-related, west nile fever, vector*, vectorborne, vector-borne, vector related, vector-related, yellow fever, yersini*

Table 2. Summary of studies assessing infectious disease transmission following flood events

COUNTRY	YEAR(S) STUDIED	INFECTIOUS DISEASE(S)	REF.
Australia	1998–2001, 2011	Leptospirosis, Ross River virus	(46,57)
Austria	2010	Leptospirosis	(43)
Bangladesh	1983–2007	Cholera, rotavirus, acute respiratory infection	(23–24,72–73,75–76)
Canada	1975–2001	Diarrhea	(22,26)
China	1979–2000	Schistosomiasis	(58)
Czech Republic	1997,2002	Leptospirosis, Tahyna virus	(41,54)
England	2000	Diarrhea	(28)
France	2009	Leptospirosis	(38)
Germany	2005,2007	Norovirus, leptospirosis	(29,34)
Guyana	2005	Leptospirosis	(44)
Italy	1993–2010	Hepatitis A, salmonellosis, diarrhea, leptospirosis, leishmaniasis, legionellosis	(18,36)
India	2001–2006	Leptospirosis	(33,45)
Indonesia	2001–2003	Paratyphoid fever	(27)
Mexico	2007,2010	Leptospirosis, dengue fever	(37,55)
Pakistan	2010	Diarrhea, skin and soft tissue infection, conjunctivitis, respiratory tract infection, suspected malaria	(69)
The Philippines	2009	Leptospirosis	(47)
Sudan	2007	Rift Valley fever	(56)
Taiwan	1994–2009	Leptospirosis, melioidosis, enteroviruses, dengue fever, bacillary dysentery, Japanese encephalitis	(21,40,48,74)
Thailand	2012	Melioidosis	(70)
United States	2001,2004	Diarrhea, leptospirosis	(25,32,35)
Vietnam	2008	Conjunctivitis, dermatitis	(71)

Figure 1. The occurrence of infectious disease outbreaks following flooding in relation to time.

Appendix A. Studies assessing the relationship between infectious diseases and flooding - Multiple diseases

Authors	Location and Year of Flood	Design	Main Results
Ahmed et al.^69	Pakistan, 2010	Cross-sectional study- 7,814 flood affected individuals interviewed to determine frequency of infectious diseases.	Gastrointestinal (30%), skin and soft tissue infection (33%), conjunctivitis (7%), ear, nose and throat infection (5%), respiratory tract infection (21%), suspected malaria (4%). No comparative data before flooding.
Bich et al.^71	Vietnam, 2008	Cross-sectional study- rural and urban districts interviewed within 1 mo after flood about social, economic, and health impacts. In each district, a flooded commune and a less affected commune (control commune) were selected.	No statistically significant differences in proportion of dengue cases in flood affected and less affected communes. Higher proportions of pink eye and dermatitis in severely flood affected communes. In flood affected communes, 10/10 urban cases (p < 0.05) and 64/69 rural cases (p < 0.05) contracted pink eye after flood. In flood affected communes, 30/34 urban cases and 221/229 (p < 0.05) rural cases contracted dermatitis after flood.
Chen et al.^21	Taiwan, 1994–2008	Routine data- analysis of a database integrating daily precipitation and temperature and an infectious disease case registry.	Heavy precipitation (130–200mm) a significant risk factor for enteroviruses (RR = 2.45; 95% CI 1.59–3.78) and dengue fever (RR = 1.96; 95% CI 1.53–2.52). Extreme torrential rain (> 350mm) a significant risk factor for enteroviruses (RR = 5.981; 95% CI 1.474–23.760) and bacillary dysentery (RR = 7.703; 95% CI 5.008–11.849). Associations between precipitation levels and enterovirus infections, Japanese encephalitis (p < 0.001), and stronger linear relationships between precipitation and bacillary dysentery, dengue fever, leptospirosis (p < 0.001).
Marcheggiani et al.^18	Italy, 1993–2010	Routine data- national statistics collected by Italian Ministry of Health.	Association between hepatitis A, salmonellosis, infectious diarrhea, leptospirosis, cutaneous and visceral leishmaniasis, legionellosis and flood events from 1993–2010 seemed to exist.
Milojevic et al.^75	Bangladesh, 2001–2007	Controlled interrupted time series- diarrheal incidence of a cohort of 211,000 residents classified as flooded or non-flooded in 2004.	After fully controlling pre-flood rate differences and seasonality, no clear evidence of excesses mortality or diarrhea risk during/after flooding. No evidence of excess risk from acute respiratory illnesses during flood but moderate increase in risk 6 mo after flood (RR = 1.25; 95% CI 1.06–1.47).
Su et al.^40	Taiwan, 2009	Routine data- to clarify association between leptospirosis and melioidosis epidemics and flooding.	Positive correlation for leptospirosis (r = 0.54; p < 0.05) and for melioidosis (r = 0.52; p < 0.05) with cumulative rainfall. Increase in melioidosis cases significantly associated with > 500mm/day (p < 0.05). Number of leptospirosis cases positively correlated with 24-h cumulative rainfall (r = 0.71; p = 0.14).

Appendix B. Studies assessing the relationship between infectious diseases and flooding - Water-borne

Authors, Year	Location and Year of Flood	Study Design	Main Results
Apisarnthanarak et al.^70	Thailand, 2012	Case report- 5 melioidosis patients located through active case surveillance.	5 cases reported excess flooding of homes and 0 had traditional risk factors for melioidosis. All cases survived.
Auld et al.^22	Canada, 2000	Outbreak investigation- E. coli O157:H7 and Campylobacter outbreak.	Outbreak occurred several days after heavy rainfall (5-d accumulation 130–140mm). Heavy rainfall hypothesized as a causative factor of the outbreak.
Carrel et al.^72	Bangladesh, 1983–2003	Longitudinal study- 21-y data cluster analysis of health surveillance and Geographic Information System to investigate temporal and spatial distribution of cholera following flood protection interventions.	8,500 confirmed cholera cases. Two clusters of lower than expected cases, 3 clusters of higher than expected cases found (p < 0.001). Following flood protection interventions, overall decrease in cholera incidence, differences in the geography of high vs. low spatial clusters of cholera, and shifts in location of unusually high spatio-temporal cholera clusters.
Harris et al.^73	Bangladesh, 1998, 2004, 2007	Routine data- comparison of pathogens in flood-associated diarrheal epidemics in 1998, 2004, and 2007.	In 2007, V. cholerae O1 (33%), rotavirus (12%), and enterotoxigenic E. coli (ETEC) (12%) were most prevalent. Significantly higher percentage of labile toxin-producing ETEC isolated in 2007 flood than in previous floods (p < 0.001). More severe dehydration seen in 2007 compared with 2004 and 1998 (p < 0.001). Findings showed alterations in clinical features and phenotypic changes of major bacterial pathogens.
Hashizume et al.^23	Bangladesh, 1998	Routine data- number of observed cases of cholera and non-cholera diarrhea per week during flood and post-flood periods compared with expected numbers.	During flooding, cholera cases 5.9 times higher (95% CI 5–7) and non-cholera cases 1.8 times higher (95% CI 1.6–1.9) than expected. Post-flood period, cholera cases 2.1 times higher (95% CI 1.9–2.4) and non-cholera cases 1.2 times higher (95% CI 1.1–1.3).
Ko et al.^74	Taiwan, 2009	Routine data- melioidosis outbreak.	40 melioidosis cases identified following flooding. Onset within 4 d.
Qadri et al.^76	Bangladesh, 2004	Routine data- diarrheal stools collected from patients during flooding.	Of 350 stool specimens tested, 78 positive for V. cholerae O1 (22.2%), 11 for shigella spp (3.4%), 5 for salmonella spp (1.7%).
Reacher et al.^28	England, 2000	Historical cohort study- post-flooding survey interview.	Flooding associated with significant increase in risk of gastroenteritis with depth of flooding (RR = 1.7; 95% CI 0.9–3.0 p = 0.09, p for trend by flood depth = 0.04).
Schwartz et al.^24	Bangladesh, 1988, 1998, 2004	Routine data- diarrheal patients during the 1988, 1998, and 2004 floods compared with non-flood periods.	During flood-related epidemics, V. cholerae most common cause of diarrhea, followed by rotavirus. Patients with V. cholerae (OR = 1.63; 95% CI 1.23–2.14; p = 0.001) and those without microbiologically identifiable V. cholerae (OR = 2.75; 95% CI 2.11–3.59; p < 0.001) more likely to have severe dehydration during floods than during non-flood periods. Median of 8.5 d (range 3–13 d) from time rivers reached flood stage until beginning of epidemics, and median of 17.5 d (range 8–36 d) for epidemics to end after rivers fell below flood stage.
Setzer et al.^25	United States, 2004	Routine data- investigation of 6 target pathogens (Cryptosporisium, Giardia lamblia, Toxoplasma gondii, Helicobacter pylori, Mycobacterium avium, adenoviruses) in outpatient visits.	Statistically significant increase in outpatient visits for T. gondii (p < 0.05) and adenoviruses (p < 0.01) in severely flooded areas. Small magnitude of both effects, indicating on average < 1 extra outpatient visit each month in each severely affected county for these pathogens. Significant increase in outpatients visits for ill identified intestinal infections in both severely and moderately flooded counties (p < 0.01).
Schmid et al.^29	Germany, 2005	Outbreak investigation- norovirus.	Gastrointestinal outbreak in 26 American tourists linked to direct exposure to floodwater contaminated with raw sewage. 6/10 firefighters with floodwater contact also fell ill with vomiting/diarrhea.
Thomas et al.^26	Canada, 1975–2001	Longitudinal study- association between extreme rainfall and spring snowmelt and waterborne disease outbreaks.	For rainfall events greater than 93rd percentile, the relative odds of water-borne outbreak increased by 2.283 (95% CI 1.216, 4.285).
Vollaard et al.^27	Indonesia, 2001–2003	Case-control study- 93 (69 typhoid and 24 paratyphoid) enteric fever cases compared with 289 non-enteric fever patient controls and 378 randomly selected community controls.	House flooding a signi□cant risk factor for paratyphoid fever; when paratyphoid group was compared with community control (OR = 4.52; 95% CI 1.90–10.73); when compared with fever controls (OR = 3.25; 95% CI 1.31–8.02).
Wade et al.^32	United States, 2001	Cross-sectional study- 1,110 individuals provided flood survey health data.	House/yard flooding signi□cantly associated with gastrointestinal illness (Incidence rate ratio = 2.36; 95% CI 1.37–4.07).

Appendix C. Studies assessing the relationship between infectious diseases and flooding - Rodent-borne

Authors, Year	Location and Year of Flood	Study Design	Main Results
Amilasan et al.^47	The Philippines, 2009	Hospital-based investigation- investigating risk factors for leptospirosis mortality following flooding. Prospective surveillance and retrospective data collection.	Outbreak of 471 leptospirosis cases, 51 cases died. Patients predominately young and male. Delayed initiation of treatment, older age, jaundice, anuria, hemoptysis increased risk for death.
Bhardwaj et al.^33	India, 2006	Case-control study- identifying risk factors for leptospirosis during flooding. 62 confirmed cases and 253 age and sex matched fever and healthy controls given a questionnaire.	4 factors identified by multivariate analysis: contact of injured part with floodwater (OR 6.69; 95% CI 3.05–14.64), walking barefoot (OR 4.95; 95% CI 2.22–11.06), constant presence of rats (OR 4.95; 95% CI 1.53–16.05), spending > 4 d cleaning (OR 2.64; 85% CI 1.18–5.89).
Chiu et al.^48	Taiwan, 2004–2008	Routine data- analyze characteristics of patients with laboratory-diagnosed leptospirosis and correlate onset of symptoms with exposure to floodwater.	6 patients identified with history of contact with contaminated soil/water. 5/6 patients (83%) suffered from leptospirosis after typhoon.
Dechet et al.^44	Guyana, 2005	Routine data- laboratory testing on suspected leptospirosis hospitalizations and deaths. Confirmed outbreak of leptospirosis after severe flooding.	Of 236 suspected cases admitted, 105 (44%) tested with Dip-S-Tick IgM ELISA; 52 (50%) positive, 41 (39%) negative, and 12 (11%) indeterminate. 34 deaths attributed (11 confirmed, 10 probable, 13 suspected) to leptospirosis. Of 201 patients interviewed, 89% reported floodwater contact.
Desai et al.^34	Germany, 2007	Retrospective cohort study- leptospirosis in strawberry harvesters. Local rodents examined for leptospirosis.	13 confirmed patients. Risk of disease increased with each day an individual worked in the rain with hand wounds (OR = 1.1; 95% CI, 1.04–1.14) and accidental rodent contact (OR = 4.8; 95% CI 1.5–15.9).
Gaynor et al.^35	United States, 2004	Outbreak investigation- leptospirosis.	271 persons responded to Internet survey, 90 (33%) reported febrile illness within 30 d of floodwater contact. One additional acute leptospirosis case identified. Patient 2 epidemiologically linked to Patient 1.
Maskey et al.^45	India, 2001–2005	Longitudinal study- prevalence of leptospirosis.	8 fold rise in leptospirosis in 2005 observed after heavy rainfall and water logging. 432 laboratory confirmed cases.
Pellizzer et al.^36	Italy, 2002	Sero-epidemiogical study- evaluated leptospirosis risk in flood-exposed population.	7/44 patients exposed to floodwaters exhibited anti-Leptospira specific IgM antibodies and 5 confirmed positive. Re-testing months later found significant antibody titers > 100 against serovar Copenhangeni in 3 cases (6.8% seroconversion rate). Flooding appeared to be sole risk factor, verification not possible due to lack of control group.
Radl et al.^43	Austria, 2010	Outbreak investigation- leptospirosis.	1st documented outbreak of leptospirosis in Austria. Four serologically confirmed cases, all triathlon athletes. Triathlon preceded by heavy rainfall (22mm). Cases contracted leptospirosis while swimming in recreational body of water.
Renato et al.^37	Mexico, 2007	Outbreak investigation- leptospirosis.	165 hospital cases showed febrile illness: 30 (18.2%) leptospirosis. 12/30 cases of leptospirosis confirmed serologically, all with moderate to severe floodwater contact. 4/12 positive cases died.
Smith et al.^46	Australia, 2011	Routine data- leptospirosis surveillance.	9 cases confirmed, all with floodwater exposure. 1st reported outbreak in central Queensland.
Socolovschi et al.^38	France, 2009	Longitudinal-study- leptospirosis cases compared with weather conditions and garbage management strikes.	3 autochthonous cases identified in Marseilles (October 2009) preceded by heavy rainfall. 1st autochthonous case identified after period of flooding preceded by heavy rainfall over several days (34.6 mm/day; 79.2 mm/day; 137 mm/day with an episode of 63 mm/3hr). Two autochthonous cases occurred during period of high rainfall (13.6–23.8 mm).
Zitek and Benes^41	Czech Republic, 1997,2002	Routine data- leptospirosis surveillance.	Rates of reported and serologically confirmed cases of leptospirosis 3 times higher with specific morbidity (0.9 cases/100,000 inhabitants). 94 confirmed cases in 1997 and 92 confirmed cases in 2002. Two-thirds from inundation areas, half directly associated with floodwater.

Appendix D. Studies assessing the relationship between infectious diseases and flooding - Vector-borne

Authors, Year	Location and Year of Flood	Study Design	Main Results
Hassan et al.^56	Sudan, 2007	Outbreak investigation- Rift Valley fever.	747 confirmed human cases including 230 deaths. Outbreak followed heavy rainfall with severe flooding.
Hubalek et al.^54	Czech Republic, 2002	Routine data- specimens from residents in flooded area examined serologically for mosquito-borne viruses.	Antibodies detected after flood for Tahyna, Sindbis, and Batai viruses, with only activity found for Tahyna virus among 150 residents.
Jiménez-Sastré et al.^55	Mexico, 2010	Cross-sectional study- convenience sampling of dengue fever in flooded colonies.	3 cases with positive serology of IgG (0.6%) and 5 cases of positive IgM (0.9%). Geographical distribution associated with proximity to 2 permanent water bodies.
Tong et al.^57	Australia, 1998–2001	Routine data- assessment of variability in environmental and vector factors on Ross River virus transmission.	Increases in high tide (RR = 1.65; 95%CI 1.2–2.26), rainfall (RR = 1.45; 95%CI 1.21–1.73), and mosquito density (RR = 1.17; 95%CI 1.09–1.27) significantly associated with rise of monthly Ross River virus.
Wu et al.^58	China, 1979–2000	Longitudinal study- review of retrospective data to determine intermediate host snail dispersal patterns and acute and chronic infections of schistosomiasis after floods.	Average number of acute schistosomiasis cases recorded in flood years 2.8 times higher than in years with little to no flooding. Re-emerging and new snail infested areas in flood years on average 2.6 and 2.7 times larger than in years with normal water levels. Flooding of marshlands identified as main driver for vector dispersal.

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