Impact of climate change on foodborne infections and intoxications

2.1 Campylobacter

Bacteria of the genus Campylobacter (C.) cause an intestinal infection typically associated with abdominal pain and watery, occasionally bloody diarrhoea. Rare complications may include joint inflammation and Guillain-Barré syndrome, a nerve disease associated with paralysis. Even a low infectious dose of ≥500 germs can trigger a Campylobacter infection. Approximately 50,000 to 70,000 cases are reported to the Robert Koch Institute (RKI, Germany’s national public health institute) annually. For years, Campylobacter enteritis has been the most common bacterial diarrhoeal disease in Germany that has a mandatory notification requirement as per the German Protection against Infection Act (IfSG). The most important Campylobacter species pathogenic to humans are C. jejuni and C. coli. Transmission to humans occurs primarily via contaminated food of animal origin. In particular, consumption of contaminated chicken meat is a significant risk factor for Campylobacter infection [4–6]. Transmission to humans is also possible via other foods like non-pasteurised milk. Unlike Salmonella, Campylobacter is considered unlikely to multiply in food because of its microbiological characteristics (growth under microaerobic conditions, i. e. reduced oxygen concentration in the atmosphere, and at temperatures of 30°C to 42°C) [7]. Campylobacter infections via contaminated drinking water or bathing water contaminated with animal faeces have also been described [8, 9].

2.2 Salmonella

The bacteria of the genus Salmonella are zoonotic agents that can be transmitted directly or indirectly between humans and animals. They are widely distributed in nature. The main reservoir for Salmonella is warm-blooded animals, including livestock and wildlife. Salmonella also occurs in cold-blooded animals, such as reptiles or insects, which can act as vectors and transmit Salmonella to warm-blooded animals or humans. Although most salmonellae do not usually cause symptoms in animals, they can cause mild to severe health problems in humans. Human salmonellosis is often accompanied by fever, nausea, vomiting, abdominal pain, and headache, but signs of illness may be completely absent.

In Germany, salmonellosis is the second most frequently reported bacterial foodborne infection in humans after campylobacteriosis; Salmonella (S.) enterica is an important cause of foodborne outbreaks. Among these, S. Enteritidis and S. Typhimurium are the most common serovars, together accounting for approximately 75% of all reported salmonellosis cases [26]. Poultry is presumed the most important source of Salmonella infections in humans. In particular, eggs and egg products play a predominant role. Pork and pork products represent another important source [27, 28]. Increasingly, Salmonella infections are also reported to be associated with the consumption of foods of non-animal origin [27, 29]. Among these, raw leafy vegetables, onion and stem vegetables, tomatoes, and melons were the most commonly affected products. Contamination of these products with Salmonella can occur both before harvest (through faecal matter, irrigation water, dust, insects, etc.) and after harvest (through harvesting equipment, transport containers, insects, dust, rinsing water, ice, transport vehicles, processing equipment) [30].

2.3 Vibrio

Vibrio are environmental bacteria that colonise saline and brackish water bodies as well as wetlands worldwide, but can also occur in the microbial flora of aquatic animals. For humans, water contact and ingestion of Vibrio (V.)-containing seafood (fish, marine animals) can be problematic. As bacterial contaminants, V. cholerae, V. vulnificus, and V. parahaemolyticus in particular can cause infections [35, 36]. The significance of each species for humans varies regionally and is linked to area-specific factors, such as the salinity of water bodies, air and water temperatures, and fluctuations to which they are subject [37]. The genus Vibrio includes more than 135 species [38], three of which are largely causative of intestinal (e. g. gastroenteritis) or extraintestinal infections (e. g. middle ear infection) [35]. V. cholerae serotypes O1/O139, which produce the cholera toxin, are significant worldwide, as they can lead to pandemic cholera outbreaks in tropical and subtropical regions with poor water hygiene. In Europe, the only endemic Vibrio types are V. cholerae non-O1/non-O139 serogroups and other Vibrio species, collectively called non-cholera Vibrio (NCV). V. cholerae non-O1/non-O139 can lead to self-limiting infections with moderate diarrhoeal symptoms, but are rarely associated with food consumption. Gastrointestinal illness in Europe is mainly associated with haemolysin (trh/ tdh)-encoding V. parahaemolyticus isolates and consumption of raw or undercooked seafood. V. vulnificus, on the other hand, plays an important role in severe wound infections, which is discussed in another article in this status report that looks more closely at effects of climate change on waterborne infections and intoxications (Dupke et al. [39]). This species is common in coastal waters of moderate salinity worldwide and has been associated with fatal infections from consumption of contaminated oysters, with mortality rates for primary septicaemia (blood poisoning) sometimes exceeding 50% [37]. Accurate information on foodborne Vibrio infections is not yet available, as pathogen detection in diarrhoeal diseases is often not part of risk-based diagnostics, and a mandatory notification requirement for human Vibrio infections does not exist throughout Europe. In Germany, only isolated cases of gastrointestinal NCV infections have been recorded since the introduction of mandatory notification according to the IfSG in 2020, which may indicate either low exposure to Vibrio-containing products or that a large proportion of the illnesses are not detected and thus not reported [40].

The importance of seafood has increased due to its high protein, vitamin and mineral content. For many years, the annual per capita consumption in Germany was covered by wild catch, but now increasingly comes from aquacultures. Usually, seafood is offered in processed form (e. g. heated, marinated, smoked) and should thus contain no or hardly any Vibrio. However, raw and insufficiently heated products pose a risk [40]. Mussels and oysters in particular are predestined to enrich even small amounts of Vibrio due to their way of filtering of nutrients from the water. Thus, they pose a health risk, especially for people with weakened immune systems or pre-existing conditions.

In mussels and oysters, V. alginolyticus (sometimes associated with middle ear infections in humans) and V. parahaemolyticus are frequently detected, and rarely V. cholerae non-O1/non-O139 and V. vulnificus have been reported, with V. alginolyticus occurring year-round and the other species occurring exclusively during the warm summer and fall months [41]. Within Europe, several countries (e. g. Spain, France, United Kingdom) cultivate mussels and oysters, some of which are heavily contaminated with toxigenic Vibrio (up to 25% toxigenic V. parahaemolyticus ) [40].

There are hardly any reliable data available on the probability of occurrence of a health impairment after exposure to Vibrio species pathogenic to humans. In principle, the risk of health impairment correlates with the amount of ingested pathogenic Vibrio and is also dependent on the respective species. In addition, the probability of occurrence of a health impairment is increased in vulnerable groups of people (YOPI: young, old, pregnant, immunocompromised people).

3.1 Cryptosporidia

More than 40 different species of the protozoan genus Cryptosporidium have been described to date, which can infect a large number of different animal species and humans. Here, we focus on the species Cryptosporidium (C.) parvum and C. hominis, as they are responsible for the largest proportion of human infections [44]. C. hominis occurs almost exclusively in humans, while the primary hosts for C. parvum are cattle, horses, goats, and sheep, and, to a lesser extent, dogs, cats, and birds [45]. Infection occurs via the faecal-oral route by ingestion of the infective developmental stages (oocysts); transmissions from animal to animal, human to human, animal to human, and vice versa are possible [46]. However, infection can also occur through ingestion of contaminated water (e. g. swimming pool, river, lake, or spring water). Another source of infection can be plant-based foods that have been contaminated with infested water.

Cryptosporidiosis is one of the most common diarrhoeal diseases associated with the ingestion of contaminated water. In 2013, an outbreak with 167 cases was recorded in Germany in association with flooding after a heavy rain event [47]. Foodborne illnesses have also been described in Europe, which have been attributed to the consumption of lettuce [24].

In Germany, there is a mandatory notification requirement for detection of cryptosporidia in connection with an illness in accordance with the IfSG. Between 900 and 2,000 cases are reported to the RKI annually; in Europe, there are 8,000 to 14,000 cases annually. Data from the European Centre for Disease Prevention and Control (ECDC) show that cryptosporidiosis in Europe has seasonal increases in late spring and late summer to early autumn, respectively [48].

Young children, people with weakened immune systems, travellers to developing countries, and people who drink untreated water are at increased risk of infection.

Infection may be asymptomatic or symptomatic. Symptoms described include prolonged watery diarrhoea with weight loss, severe abdominal pain or cramps, nausea, vomiting, and headaches [49]. After infection, further complications (e. g. inflammation of the pancreas, appendicitis, impairment of the lungs) and even death may occur. After the symptoms have subsided, the oocysts continue to be excreted in the stool for many weeks. The infectious dose of cryptosporidia is low, ranging from 10 to 1,000 oocysts, depending on the species [50]. However, it is suspected that one oocyst may be sufficient for infection in humans [51].

3.2 Giardia

Parasites of the protozoan genus Giardia can also be affected by climate change. Giardia are currently classified into eight species [52]. However, the species Giardia (G.) duodenalis (synonyms: G. lamblia, G. intestinalis) is the only species of this genus that can infect humans as well as numerous mammalian species. G. duodenalis is distributed worldwide; humans are considered the main reservoir. Infection occurs faecal-orally by ingestion of the infectious developmental stages of the parasite (1 to 10 cysts are sufficient) with contaminated tap water or untreated fresh water from lakes or streams. However, Giardia cysts can also be transmitted by eating contaminated food or by close contact with infected persons or animals [53].

Giardiasis caused by G. duodenalis is one of the most common intestinal parasitoses in humans worldwide [54]. Prevalence rates are significantly higher in developing countries than in developed countries. For example, 3,296 travel-associated cases of the disease were reported to the RKI in 2019; the most frequently cited country of infection was India [26]. However, as warming due to climate change continues, increased local infections will also be expected. Infants and young children, older persons, travellers, and immunocompromised persons are among the high-risk groups [55]. In more than 50% of cases, the disease is asymptomatic, but the course can be severe in infants and older persons [56].

In Germany, detection of this pathogen in connection with an illness is notifiable.

Globally, G. duodenalis is estimated to cause 28.2 million cases of diarrhoeal disease per year due to food contamination [52]. The European Food Safety Authority (EFSA) recorded 14 foodborne outbreaks and 3 outbreaks due to water consumption in Europe in 2019 [57]. Data on foodborne outbreaks in Germany are not yet available.

3.3 Climate influence on parasites

Cryptosporidium and Giardia can remain infectious for a long period of time and cause disease, especially after consumption of raw contaminated food.

Their high stability against environmental influences, in particular the long survivability in aqueous environments, suggests that these parasites could appear more frequently as pathogens in the future. Extreme weather such as heavy rainfall and flooding, which are also expected to increase in our latitudes as a result of climate change, increase the risk of infectious oocysts/cysts entering bodies of water, as well as the risk of contamination of plant-based foods. The risk for humans can be minimised by good kitchen hygiene.