Infectious Diseases Associated with Hydrometeorological Hazards in Europe: History
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Maria Mavrouli
,
Spyridon Mavroulis
,
Efthymios Lekkas
,
Athanassios Tsakris

Hydrometeorological hazards comprise a wide range of events, mainly floods, storms, droughts, and temperature extremes. Floods account for the majority of the related disasters in both developed and developing countries. Flooding alters the natural balance of the environment and frequently establishes a favorable habitat for pathogens and vectors to thrive. Diseases caused by pathogens that require vehicle transmission from host to host (waterborne) or a host/vector as part of their life cycle (vector-borne) are those most likely to be affected by flooding. 

  • infectious disease
  • floods
  • waterborne disease
  • rodent-borne disease
  • vector-borne disease
  • outbreak

1. Introduction

Hydrometeorological hazards comprise a wide range of events, mainly floods, storms, droughts, and temperature extremes along with their cascading effects. Despite their atmospheric, hydrological, or oceanographic origin, they can have considerable impact to hazards belonging to other categories, such as biological health hazards (e.g., infectious disease outbreaks and epidemics). Hydrometeorological hazards are characterized by high potential to adversely affect the structural environment including buildings and infrastructures, but also the public health in several ways.
Based on the International Disaster Database EM-DAT compiled by the Center for research on the Epidemiology of Disasters (CRED), one of the foremost international databases of such events, floods, and storms holds the highest number of occurrences during the last 30 years (1990–2020) [1]. As regards 2020, floods accounted for 51.67% of all incidents (ranking first), 40.92% of all fatalities (ranking second after extreme temperatures), 33.71% of the population affected (ranking second after storms), and 29.95% of economic losses in billion USD (ranking second after storms) by all disasters caused by natural hazards worldwide [2]. Taking into consideration the aforementioned numbers and percentages, it is obvious that floods account for the majority of the related disasters in both developed and developing countries.
Various definitions of floods have been provided from several sources [3][4][5][6]. However, their common point is the temporary partial or complete water inundation of normally dry land resulting from various processes and leading to loss of human life, dramatic effects on the natural environment, and considerable damage to the built environment. Regardless of classifications, floods have a wide range of health consequences that can be characterized in terms of time [7]. The immediate health effects of floods include drowning, injury, gastroenteritis outbreaks, and skin and respiratory infections, while the medium-term ones comprise of infected wounds, injury complications, poisoning, starvation and communicable diseases [8]. In the long-term, chronic disease, disability, poor mental health, and poverty-related diseases including malnutrition are usually recorded [8].
Infectious disease spread in populations is a consequence of the interaction and connection between the three components of the Epidemiologic Triangle: an external agent, a susceptible host, and an environment in which the agent and the host are brought together [9]. A vector that transfers the pathogen from one host to another without causing the disease itself could be involved in the infectious disease [10]. However, the effects of each triad component may vary substantially for different settings. Flooding alters the natural balance of the environment and frequently establishes a favorable habitat (breeding ground) for pathogens and vectors to thrive. Diseases caused by pathogens that require vehicle transmission from host to host (waterborne) or a host/vector as part of their life cycle (vector-borne) are those most likely to be affected by flooding [7][11][12].
Since early 2020, amid the evolving COVID-19 pandemic and the ongoing climate crisis, which increase the frequency and magnitude of extreme weather events, floods of various magnitudes have been generated in many countries worldwide (e.g., [1][13][14][15][16][17]) including Europe. Among the most notable recent destructive events are the July 2021 floods that occurred in and affected several Central Europe countries. Excessive rainfall along with saturated soils caused rivers to overflow their banks, resulting in extreme floods and devastation. Several urban and rural residential areas were inundated. Flooding led to significant damage to buildings and business property or equipment as well as destruction of crops and farms. Large parts of the road and railway network were submerged and bridges collapsed resulting in traffic and communication disruption. The water supply network was also compromised, thus negatively affecting the safety of drinking water and causing supply interruption and water shortage in the affected residential areas. The electric power supply network suffered damage to its structural elements, leaving hundreds of thousands households without electricity, telephone, and internet, and making the 112 Emergency Communications Service inaccessible. During intense flooding, the capacity of sewerage was exceeded, thus the sewer systems overflowed and inundated streets and buildings with raw sewage. More than 243 fatalities were reported (196 in Germany, 43 in Belgium, 2 in Romania, 1 in Italy, and 1 in Austria) and attributed to the aforementioned adverse effects of inundation and flooding. About 1000 residents were stranded in inaccessible areas for days, while hundreds of thousands had to evacuate flood-affected areas.

2. Waterborne Diseases

Waterborne diseases are mainly caused by drinking water contaminated with pathogenic microorganisms (bacteria, viruses and parasites) originating from human or animal feces. Flood-related waterborne diseases have been reported in the United Kingdom, the Republic of Ireland, Norway, Sweden, Finland, Denmark, the Netherlands, Austria, Hungary, France, Spain, Germany, Italy, and Greece.
A case-crossover study analyzed rainfall-induced drinking water-related outbreaks reported in England and Wales for the period extending from 1910 to 1999 following both low and excessive rainfall [18]. Various parasites and bacteria such as Giardia, Cryptosporidium, Escherichia coli, Salmonella typhi, Salmonella paratyphi, Campylobacter, and Streptobacillus moniliformis were among the pathogens implicated in 89 outbreaks studied [18]. Street flooding and/or flooding of combined sewerage systems contribute to the mixing of rainwater with sewage, significantly contaminating flood waters with fecal matter. As a result, pathogens such as noroviruses, enteroviruses, and Campylobacter, which are all known causative agents of gastrointestinal and respiratory diseases, may be detected in floodwater [19][20].
Diarrhea and vomiting are the most commonly reported symptoms of waterborne disease; however, other infections of skin, ear, respiratory tract, or eye are also identified [21]. Flooding of households in Lewes, Southern England was strongly associated with earache in patients of all ages, while weaker associations were observed for skin rash, respiratory illness, and all categories of injury [22]. However, an increase in the risk of gastroenteritis occurrence was significantly associated with depth of flooding [22]. Stomach upsets and recurring flu-like symptoms such as sore throat, cough and general sickness were attributed to the floods and were reported by people whose homes had been affected in Cumbria, northwest England [23].
Direct hand contact with floodwater was found to be significantly associated with increased incidence of gastrointestinal, respiratory, and/or dermatological complaints in the Netherlands and Germany [20][24][25][26]. In parallel, participation in post-flooding cleanup tasks was associated with the development of influenza-like symptoms [26] or both acute gastroenteritis (AGE) and acute respiratory infection (ARI) emergence [20]. Having walked or cycled through floodwater was also related to the development of influenza-like symptoms [26] or AGE occurrence [20].
Waterborne diseases can also be spread while bathing, washing, or eating food exposed to contaminated water. Harder-Lauridsen et al. [27] demonstrated that after an extreme rainfall, physical contact with and unintentional intake of sewage-polluted recreational water can increase the risk of severe gastrointestinal illness. A triathlon sports competition took place in Copenhagen, Denmark shortly after an extreme rainfall in August 2010. The athletes who participated in this event swam in water with high post-flooding bacterial contamination and were found to develop gastrointestinal illness five times more often than athletes who had swum the same distance in unpolluted water [27].
Intense precipitation can transfer pathogenic microorganisms of human or animal fecal origin to the aquatic environment through discharge of raw and treated sewage and run-off from the soil, increasing the microbial load on surface water. A gastroenteritis outbreak occurred in Elassona city, central Greece in March 2012 and was characterized as waterborne because the region had suffered heavy rainfall the week before the gastroenteritis episodes began [28]. Heavy rainfall at the beginning of the month could have contributed to water runoff from fields into rivers, contaminating the water supply with human or animal waste from neighboring dwellings and breeding farms and resulting in increased water turbidity [28]. Tornevi et al. [29] analyzed the relationship between daily fluctuations in gastrointestinal symptoms in Gothenburg population and the amount of rainfall upstream of the drinking water utility exposed to upstream run-offs from agricultural areas and occasionally from overflowing combined sewer systems. It was found that heavy rainfall was associated with an increase in nurse advice calls for gastrointestinal illness on the same day and around 5–6 days later [29].
A matched case-control study in four Nordic countries (Denmark, Finland, Norway, and Sweden) over a 21-year period (1992–2012) was conducted to investigate the association between heavy precipitation events and waterborne outbreaks [30]. Heavy precipitation was found to be positively associated with the occurrence of waterborne outbreaks, especially in spring and summer seasons. It was also noted that groundwater sources as well as single household supplies were particularly vulnerable to extreme weather events [30].
Flooding favored the emergence and incidence increase of waterborne diseases in European countries, as shown in Table S1. Increased incidence or outbreaks of waterborne diseases caused by parasites (Cryptosporidium and Giardia), viruses (norovirus and hepatitis A virus), and bacteria (Campylobacter, Escherichia coli, Salmonella, Shigella) were detected (Table S1) and are thoroughly described below.

2.1. Parasites: Cryptosporidium

Heavy rainfall and flooding contributed to an increased risk of Cryptosporidium infection in European countries. Confirmed cryptosporidiosis cases were mainly reported in the United Kingdom (UK) [31][32][33][34][35][36] and the Republic of Ireland [37][38][39][40], while only one large cryptosporidiosis outbreak was detected in Germany [41].
Cryptosporidium infection may be asymptomatic or develop into diarrhea that spontaneously resolves over a couple of weeks in healthy individuals. On the contrary, immunocompromised patients may experience frequent, life-threatening watery diarrhea that is difficult to treat with currently available medications. Oocysts ingestion, direct contact with infected people or animals, and contaminated water and food are all methods of Cryptosporidium fecal-oral transmission. Oocysts of this intestinal parasite can survive in moist soil, water or even harsh environmental conditions for long periods of time. Cryptosporidium can also resist conventional disinfection treatments such as chlorination, which increases the risk of water distribution systems contamination [42].
Cryptosporidiosis outbreaks were usually attributed to consumption of unboiled tap water from a specific source [32][35]. Heavy rainfall in the reservoir catchment area supplying raw water to the treatment works contributed to the introduction of Cryptosporidium oocysts from the environment into the raw water supply [33][43][44]. The origin of the outbreak was confirmed by the detection of Cryptosporidium oocysts in samples from water treatment plants and domestic taps [35].
The spatial distribution of the affected residences in Ayrshire (UK) revealed that most of them shared the same public drinking water supply [31]. A strong statistical correlation has been demonstrated between the reported cryptosporidiosis cases and the residence in an area supplied from two groundwater sources, one of which was found to drain surface water directly from a field carrying cattle feces [34]. In the Republic of Ireland, two cryptosporidiosis outbreaks were reported in April–May 2002 and February–March 2007, and all of the cases were found in regions that used lakes surrounded by farmland as the water source [37][38]. The entry of animal waste into the lake could have been facilitated by heavy rainfall [37][38]. Cryptosporidium oocysts were found in the lake’s raw and treated water, as well as in the surrounding environment [37]. A Cryptosporidium parvum outbreak was recorded among 35 people (27 pupils and 8 teachers), who took part in a school trip to an outdoor adventure farm in South West England, from May 22 to 26 May 2006. The two most plausible routes of transmission were drinking water from a private well or coming into contact with feces-contaminated surface water following heavy rainfall [36].
Boudou et al. [40] found that the increase in cryptosporidiosis cases across the Republic of Ireland from November 2015 to January 2016 was associated with hydrometeorological variables such as cumulative antecedent rainfall, surface water run-off, and groundwater level [40]. Apart from heavy local rainfall, other environmental factors such as river overflow, shutdown of treatment plants due to mechanical problems, increase in water turbidity, and damage to sewage systems could all contribute to an increased risk of cryptosporidiosis [32][41].

2.2. Viruses: Norovirus, Hepatitis A Virus

Human noroviruses (NoVs) represent the leading cause of gastroenteritis outbreaks worldwide, affecting all age groups and being mainly transmitted via an oral-fecal route [45]. NoV is highly contagious due to its low infectious dose and persistence of virus in fecal excretion even weeks after patient recovery [46][47].
NoVs were identified as the main causative agents of the waterborne gastroenteritis epidemics reported in Finland [48][49], France [50][51], Italy [46][50], Greece [52][53], Austria [54], Sweden [55], the Netherlands [56], and Hungary [57].
Acute gastrointestinal disease was detected and related to the microbiological contamination of water supplies following heavy rainfall and flooding events [57]. Floods and surface runoff due to snow melting in spring contributed to groundwater contamination with fecal microbes in Finland and Sweden [48][49][55]. Outbreaks were attributed to drinking non-disinfected ground water [48][49].
According to data from epidemiological and molecular studies, residents living in households connected to the public water network were at a higher risk of developing NoV gastroenteritis [46][55]. In Sicily (Italy), sewage overflowing from septic tanks and latrines as a result of the rainfall caused the contamination with human feces of the wells and springs supplying the public water network [46]. The majority of individuals with symptoms of acute gastroenteritis were drinking water from a single well in Xanthi town, North Eastern Greece [52]. Another large outbreak of non-bacterial gastroenteritis caused by NoVs was reported after heavy rainfall in the same Greek region almost 2 years after the gastroenteritis outbreak described by Papadopoulos et al. [53].
Direct exposure to floodwater contaminated with raw sewage caused the occurrence of a NoV outbreak among American tourists and firefighters who helped pump floodwater out of a hotel inundated due to an extremely heavy rainfall in Salzburg, Austria [54].
Overflow of sewage treatment plants due to heavy rainfall led to the fecal contamination of lakes and rivers in France [50][51]. Consumption of oysters harvested from the Etang de Thau, the second largest lagoon in France, was responsible for NoV gastroenteritis outbreaks not only in France but also in Italy [50]. Oyster consumption following floods near a lagoon with shellfish farming activity was the most important contributing factor in the occurrence of another foodborne viral gastroenteritis outbreak in France [58].
Water contamination by several NoV strains caused an acute gastroenteritis outbreak among swimmers following participation in the Amsterdam City Swim event. Two days before this event, an unusually heavy rainfall caused severe flooding and overflow of the sewage system into the city canals [56].
Hepatitis A virus (HAV) is transmitted through contaminated food and water and thrives in poor sanitary conditions. Increased incidence of HAV infection after flooding was observed in Spain and Italy [59][60]. Apart from extreme rainfall, other climate factors such as weekly day of rainfall and snow were also associated with a rise in the number of Hepatitis A cases in Spain [59].

2.3. Bacteria: Escherichia coli, Campylobacter jejuni, Shigella sonnei

Escherichia coli were the most commonly isolated bacteria followed by Campylobacter jejuni and Shigella sonnei [18][61][62][63][64][65][66][67].
Shiga toxin or verotoxin-producing Escherichia coli (STEC/VTEC) have been related to foodborne and waterborne outbreaks. STEC/VTEC causes a wide range of human gastrointestinal disorders, from watery and bloody diarrhea to hemorrhagic colitis. Infection can also result in the life-threatening hemolytic uremic syndrome (HUS), which is considered to be caused by Shiga toxins (Stx) [68][69]. It is demonstrated that heavy rainfall and high temperature are statistically significantly associated with the occurrence of waterborne VTEC outbreaks [70].
Although cattle are considered to be the primary reservoir of STEC/VTEC strains, sheep are also important carriers of these pathogens [71]. In eastern Scotland, heavy rainfall caused localized flooding on an agricultural showground that was generally used for sheep grazing and hosted a scout camp [61]. E. coli O157 infection was detected in 20 campers, and E. coli O157 was transmitted from the environment to cases via contaminated hands [61]. In August 2004, seven cases of E. coli O157 infection were identified in children on holiday in Cornwall, southwest England [62]. The source of infection was a contaminated freshwater stream flowing across a seaside beach. Because of heavy rainfall in the days preceding the outbreak, feces from cattle found grazing upstream and potentially contaminated by E. coli O157 infiltrated the stream, thereby causing the outbreak [62]. Extremely heavy summer rainfall in the Republic of Ireland resulted in high water table levels, intense run-off, and widespread flooding that significantly increased the potential for microbiological contamination of drinking water [63].
During periods of heavy rainfall, areas of stagnogley soils with mixed animal grazing may be more susceptible to Campylobacter exposure and spread, increasing the likelihood of human cases of the disease [72]. In Finland, two outbreaks of Campylobacter jejuni enteritis were recorded in 2000 and 2001 and were associated to fecal contamination of drinking water sources by surface water runoff after rain [64]. Following an exceptionally heavy rainfall in June 2009, an outbreak of Campylobacter gastroenteritis (163 cases) occurred in the Danish town of Tune [65]. Drinking tap water was the only exposure identified as being related with gastroenteritis, with a clear dose–response association between the amount of tap water drunk and the risk of gastroenteritis. Drinking-water contamination was caused by congestion of the combined rainwater drainage and sewage system [65]. Residents of an economically deprived housing estate built on a steep hill and surrounded by agricultural pastures developed C. jejuni gastroenteritis after severe rainfall on the surrounding hills in the South Wales Valleys (UK) [66].
An outbreak of acute Shigella sonnei gastroenteritis occurred in the town of Santa Maria de Palautordera (Spain), following heavy rainfall that resulted in mud and organic material entering the treatment plants, which were not designed to treat highly turbid water [67].

3. Rodent-Borne Diseases

Flood-related rodent-borne diseases have been reported in Finland, Denmark, France, Belgium, Germany, the Czech Republic, Italy, Austria, Croatia, Bosnia and Herzegovina, Montenegro, Serbia, Republic of North Macedonia, and Bulgaria.

3.1. Leptospira

Rodent-borne diseases may also increase during heavy rainfall and flooding due to altered patterns of contact among humans, pathogens, and rodents [73]. Numerous outbreaks of leptospirosis, a spirochetal zoonosis, have been associated with extreme weather events and flooding in a wide-range of countries around the world [74][75][76][77][78][79].
Humans can acquire infection through direct contact with infected animal hosts such as rodents, domestic pets, and livestock, or through exposure to surface water or soil contaminated by infected animal urine [80][81]. During floods, the increase in leptospirosis transmission is mainly attributed to closer contact between animal hosts and humans, direct contamination of floodwaters, and damage to water and sanitation networks [82]. There have been reports of flood events associated with sporadic and outbreak cases of Leptospirosis from a wide range of countries in Europe such as Bulgaria [83], the Czech Republic [84], Italy [85][86], Germany [87][88], Austria [89], France [90], and Denmark [91][92][93] (Table S2).
Water-based outdoor sports and recreational activities are becoming increasingly popular. Triathletes, canoers and kayakers, rowers, and wild swimmers have all been known to have acquired leptospirosis infection when participating in outdoor sports and activities [94]. Higher recreational activity, ideal temperature, and rainfall favor Leptospira survival in the environment and could plausibly explain the peaks in leptospirosis incidence during the summer months in Bulgaria [83]. Recreational exposure to water, particularly in relation to water sports, is thought to be a key risk factor for leptospirosis occurrence among triathlon athletes in Germany and Austria [88][89]. Heavy rainfall preceding these endurance multisport races is likely to have contributed to the contamination of the man-made lake or the river with Leptospira [88][89].
Leptospirosis has traditionally been thought of as an occupational disease, with humans getting infected predominantly through work exposure. Sewage maintenance, animal husbandry, agriculture, mining, and military exercises are activities that increase the risk of contracting leptospirosis [95]. A leptospirosis outbreak was also detected among seasonal harvesters from Eastern Europe, working in the largest field of a strawberry-producing farm in North Rhine-Westphalia, Germany in July 2007 [87]. The warm winter of 2006–2007 enhanced rodent population growth and expansion. The disease risk increased with each day spent working in the rain and the most likely source of the outbreak was direct contact of hand lesions with contaminated water or soil and infected rodents [87]. Work-related cases accounted for nearly half of all leptospirosis cases reported over a 32-year period (1980–2012) in Denmark [91]. Fish farmers, farmers, and sewage workers were the most frequently notified professions [91].
Improper and poor waste management and garbage accumulation attract rat infestation that is related to leptospirosis infection among urban dwellers [95][96]. The emergence of sporadic laboratory-confirmed human cases of leptospirosis in the city of Marseille, France was associated with heavy rainfall periods accompanied by flooding and garbage collection strikes [90]. Garbage left uncollected contributed to expansion of the urban rat population. Residents of Marseille may have been exposed to Leptospira through contact with contaminated surface water or rat urine near garbage deposits [90]. High prevalence of pathogenic Leptospira spp. in rodents, street flooding, and garbage accumulation could also explain the occurrence of two human leptospirosis cases in the city of Palermo, Italy [86].
Flooding was found to have a significant association with increased incidence of human leptospirosis. When compared to non-flooded areas, widespread flooding may contribute to an increased risk of leptospirosis or create conditions conducive to a leptospirosis outbreak [81]. According to Zitek and Benes [84], the rates of serologically confirmed leptospirosis cases in the Czech Republic were three times higher than usual after the massive floods of 1997 and 2002. Two thirds of these cases came from flooded areas, while half of them were directly exposed to residual water and flood mud in cellars [84]. In August 2002, an excessive rainfall produced a devastating flooding in a suburban area of Vicenza in the northeastern part of Italy. Since only a small percentage of people were wearing personal protective equipment (e.g., gloves and boots) during post-flooding cleanup activities, inundation appeared to be the only demonstrable risk factor for the occurrence of serologically confirmed Leptospira infection [85]. Following the 2011 flash floods that left large areas of Copenhagen inundated, a cluster of five leptospirosis cases was detected in Copenhagen [92][93].

3.2. Hantavirus

Hantaviruses are carried by different types of rodents, and humans get infected by inhaling aerosolized urine, saliva, or droppings of infected rodent hosts [97]. In Asia and Europe, Old World hantaviruses including Puumala virus, Seoul virus, Dobrava Belgrade virus, and hantaan virus infect the highly differentiated endothelial cells of the kidney, causing acute renal failure with tubular and glomerular involvement, also known as hemorrhagic fever with renal syndrome (HFRS) [97][98]. Globally, 150,000–200,000 cases of hantavirus infection are reported annually, whereas more than 10,000 HFRS cases are diagnosed each year in Europe and their number is growing [97][98].
Heavy rainfall brought on by a cyclone contributed to increases in severe flooding events in the Balkans in mid-May 2014 [99]. HFRS incidence was significantly increased in 2014 in five flood-affected Western Balkan (WB) countries including Bosnia and Herzegovina, Croatia, Montenegro, North Macedonia, and Serbia [100]. A significantly strong negative correlation was found between the monthly incidence of HFRS and the number of months after the May floods for the entire WB area [100].
Higher mean annual precipitations are assumed to reflect higher air humidity and should increase the probability of HFRS occurrence. Zeimes et al. [101] showed a positive association between the risk of HFRS and the annual precipitation in France, Belgium, and Finland, which could be attributed to the good survival of the virus not only within the host but also in a wet environment or to the migration of the rodent population into the human environment in search of food supplies, especially when climatic conditions deteriorate [101].

4. Vector-Borne Diseases

Vector-borne diseases are infections transmitted by the bite of infected arthropod species, such as mosquitoes, ticks, triatomine bugs, sandflies, and blackflies. Arthropod vectors are especially susceptible to climatic factors, thus weather influences their survival and reproduction rates. The geographical distribution of vector-borne diseases is determined by the geographical distribution of both vertebrate host and vector [82]. Consequently, the risk of vector-borne diseases could increase if vector-borne pathogens are present along with their competent vectors in the flooded areas.
Precipitation changes are known to affect the reproduction; development; and behavior of arthropod vectors, their pathogens, and non-human vertebrate reservoirs [54]. Floods may indirectly increase the incidence of vector-borne diseases through the expansion in the number and range of vector habitats. Flood waters initially overwhelm breeding habitats and temporarily wash out mosquito populations. However, receding water could provide ideal mosquito breeding grounds and, therefore, enhance the potential for exposure of the flood-affected population and emergency responders to mosquito-borne pathogens causing diseases such as West Nile fever, malaria, and dengue fever [102].
In a 6-year investigation (2011–2016), three zoonotic arboviruses comprising of Usutu, Sindbis, and Batai viruses were found circulating in the German mosquito fauna. According to Scheuch et al., the Elbe flood could explain the relatively high number of pathogen findings in 2013, as flood events favor the mass development of high numbers of mosquitoes, which in turn facilitate enhanced virus circulation [103].
Outbreaks of mosquito-borne diseases associated with heavy rainfall or floods have mainly been observed in tropical areas [102][104]. In Europe, flooding events following extreme rainfall have been mainly linked to the emergence and incidence increase of West Nile virus (WNV), Chikungunya virus (CHIKV), and Tahyna virus (TAHV) infections in Romania, the Czech Republic, Greece, Italy, and France [105][106][107][108][109][110][111].
In the summer of 1996, an unprecedented epidemic of WNV meningoencephalitis (393 hospitalized cases and 17 deaths) occurred in southeastern Romania. Han et al. [105] found WNV infection to be associated with specific residence characteristics, such as presence of mosquitoes indoors and flooded basements of apartment buildings. It is worth mentioning that the basements were inundated with sewage-contaminated water from poorly maintained plumbing, resulting in a high-organic environment conducive to mosquito breeding [105].
After heavy rainfall in Moravia (Czech Republic), the devastating flooding of the Morava River occurred in July 1997. In the flood-affected area, the abrupt increase of mosquitoes infected with arboviruses such as WNV and TAHV contributed to the detection of confirmed and probable cases of WNV infection in that area [106]. Climatic parameters such as high temperature and increased precipitation might have a lagged direct effect on the incidence of WNV infection in Northern Italy [111].
In August 2002, a massive flood struck Prague, the capital of the Czech Republic, as well as extensive rural areas along the Vltava and Labe Rivers. An elevated incidence of “Valtice fever” caused by TAHV was found among inhabitants of the flood-affected areas in Central Bohemia, while WNV, Sindbis virus, and Batai virus infections were not reported. The prevalence of antibodies against TAHV increased with decreasing distance from areas with high mosquito abundance and floodplain forests, the primary mosquito breeding habitats [107][108].
Roiz et al. carried out surveillance of the Asian tiger mosquito Aedes albopictus, a well-known CHIKV vector in Montpellier (France) and found that extreme rainfall that inundated the city in 2014 clearly contributed to an increase of mosquito population growth and abundance, as well as to the prolongation of the autochthonous CHIKV transmission period [110].
An outbreak of WNV infection occurred in the Central Macedonia, (northern Greece) in the summer of 2010. A total of 197 patients with neuroinvasive disease were reported, of whom 33 (17%) died [109]. Danis et al. (2011) noticed that the 2010 WNV outbreak was preceded by unusual precipitation. According to meteorological data for the area, 2010 was warmer than previous years and unusually wet [112].

This entry is adapted from the peer-reviewed paper 10.3390/ijerph191610206

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