Introduction

Salmonella is of significant public health concern, causing a large amount of morbidity and mortality globally (1). Salmonella is a common foodborne disease caused by bacteria, of which there are many different serotypes. The global burden of Salmonella has been estimated at 93.8 million infections of gastroenteritis each year leading to 155,000 deaths (2). It is estimated that most of these cases are caused by contaminated food. This highlights the importance of prevention and control efforts for foodborne Salmonella (3). The symptoms of Salmonella infection usually begin 12 to 72 hours after infection and include diarrhoea, fever and cramps. It is generally a self-limiting illness lasting from 4 to 7 days. More serious complications can arise including severe dehydration (2). Young children, people aged >65 years and those with weakened immune systems are at higher risk of infection (2).

In 2000, the World Health Organisation (WHO), the US Centres for Disease Control (CDC) and the Danish Veterinary founded WHO Global Salm-Surv, which is now the Global Foodborne Infections Network (GFIN), in order to promote global laboratory-based surveillance of Salmonella outbreaks among member countries (4, 5). Every year, GFIN pooled surveillance data from its 142 country members, notably a list of 15 most common serotypes from each country. An analysis of data from WHO Global Salm-Surv country databank from 2000-2002 found that Salmonella Enteritidis and Typhimurium were the most common human serotypes globally, whereas the top 3 serotypes for non-human serotypes are Salmonella Typhimurium, Heidelberg and Enteritidis respectively. The trends become more heterogeneous at regional level, with serotypes Newport, Heidelberg and Javiana in high ranking among isolates from North America. Many serotypes, such as Salmonella Marina, Tilene or Weltevreden were restricted to certain regions of the world (6).

Historically Salmonella outbreaks have been commonly associated with chicken and eggs (7-11). From 1995 to 2000, meat (30%) was identified as the most common foodborne vehicle causing Salmonella outbreaks in Australia, with chicken the most commonly implicated meat (12). Trends remained similar in Australia from 2010 to 2011 with eggs and chicken identified as the sources responsible for the highest proportion of Salmonella outbreaks (9,10). In the USA, chicken and egg products have been identified as two of the primary sources responsible for outbreaks in the time period from 1998 to 2008 (13). Whilst chicken and eggs continue to contribute to the spread of Salmonella infections globally, in recent years the number and proportion of outbreaks linked to fresh vegetables, including recent outbreaks associated with cucumbers, have been increasing (14). In this review we aimed to summarise the trends in Salmonella infection caused by fruit and vegetables globally, comparing the USA and Australia, and particularly outbreaks caused by the novel vehicle, cucumbers.

Methods

A review of the literature was conducted using search engines MEDLINE and EMBASE, to identify relevant articles from 1 Jan 1990 to 30 April 2017. The search terms used were as follows: “Salmonella” AND “cucumber” OR “fruit and vegetables” OR “vegetables”. A grey literature search, using a Google and Google Scholar, was also conducted to identify other relevant sources of information such as health department websites and reports. The same search terms were used for this search.

All references from the articles included in the final report were then reviewed and experts in the field were consulted, to identify any further relevant publications. There were no age or geographical restrictions.

Studies were included if they described outbreaks of Salmonella caused by cucumbers in any population from January 1990 to April 2017. Additional literature regarding Salmonella outbreaks involving other types of fruit and vegetables were also included to allow for comparisons only, this was not a complete review of the literature to document all fruit and vegetables-related outbreaks. Foodborne disease outbreaks in Australia were identified from OzFoodNet Quarterly Reports (15). Foodborne disease outbreaks in the US were identified from the Centres for Disease Control and Prevention, National Outbreak Reporting System (NORS) (16). Other portals that were consulted include WHO (17) and the European Centre for Disease Prevention and Control (ECDC) (18,19). We adapted the classification scheme proposed by Painter et al. to categorize reported foods associated with Salmonella outbreaks (19). Vehicles where only one food was identified, or all foods fell into the same category, were classified into specific groups. Where more than one item, or a mixed ingredient (e.g. chicken/salad sandwich, mixed salad), was identified, the vehicles were classified as “Others”.

In addition, surveillance data from an open source epidemic observatory, Epi-Watch (20), was scanned for media articles relating to outbreaks. Only Salmonella outbreaks that occurred from 2017 to 2019 were included in this review.

Data retrieved from searches were analysed using descriptive epidemiology, and multistate outbreaks were further analysed. Foodborne outbreak data in the US and Australia were summarised and compared to identify any changing trends in the epidemiology of salmonellosis.

Results

Salmonella in cucumbers

There have been a growing number of foodborne outbreaks associated with fruit and vegetables in recent years. Specifically, there have been several recent Salmonella outbreaks associated with a novel food vehicle, cucumbers.

The first multi-state outbreaks of Salmonella caused by cucumbers was identified in the USA in 2013. An outbreak of Salmonella Saintpaul occurred from 12 January 2013 to 28 April 2013 with 84 cases identified. Of 60 people for whom information was available, 17 required hospitalisation. This outbreak was found to be linked to imported cucumbers from Mexico. Importing restrictions were placed on two implicated suppliers, who were then required to prove imported cucumbers were Salmonella free before they could be imported in to the USA (21).

The second outbreak of Salmonella, in which the Newport serotype was implicated, occurred from 20 May to 30 September 2014 across 29 states in the USA. There were 275 cases reported linked to the outbreak with 48 of those requiring hospitalisation, and one case resulting in death. The outbreak was traced back to production in Maryland. The investigation involved environmental sampling from the supplier, including areas in which the cucumbers were grown and processed, as well as samples of sediment and manure. No samples were positive for Salmonella, although the testing was conducted several months after harvest. A definitive contamination source was not identified. Laboratory typing showed that Salmonella with a similar pulsed-field gel electrophoresis (PFGE) pattern had been previously associated with contaminated tomatoes from eastern Virginia (22).

The third and the largest outbreak, occurred from 3 July 2015 to 29 February 2016 in the USA. The outbreak was cause by Salmonella Poona. A total of 907 cases across 40 states were identified. Six people died and 204 people were hospitalised as a result of the outbreak (23). Epidemiological and environmental investigation identified cucumbers from one particular company, who imported the produce from Mexico, as the source. The company responsible voluntarily recalled the product (24). The peak of cases occurred in August and September 2015, after the number of cases declined. However, it took several months to return to the baseline level of Salmonella infections, with cases continuing until February 2016. The cause of the ongoing cases is unclear, as cucumbers have a short shelf life and the infected produce was no longer available for purchase during this time. Trace-back and laboratory investigations isolated the outbreak serotype from cucumbers in stores, as well as from the distributing facility (23).

The fourth outbreak, caused by Salmonella Oslo, was discovered in April 2016 in the United States of America (USA). A total of 14 people from 8 states, three of who were hospitalised, became ill between March 21 and April 9, 2016. The outbreak spread across three states and Persian cucumbers were identified as the source. A traceback investigation identified two common suppliers from Canada, linked to three different growers in Mexico, Canada and the Dominican Republic. No one grower was identified as the source. Laboratory testing of samples conducted one month after the outbreak found no traces of Salmonella. As this was the fourth outbreak since 2013 in the USA, the Food and Drug Administration has initiated enhanced surveillance of cucumbers (25).

The most recent outbreak occurred in five provinces in Canada, with the onset date from mid-June to late-October 2018. A total of 56 laboratory-confirmed cases of Salmonella Infantis were reported, the majority centred on British Columbia. 11 individuals were hospitalised. Although English cucumbers were the primary suspected vehicle, laboratory testing of samples found no positive trace of Salmonella (26). This outbreak was possibly related to another outbreak in the Washington state of the USA, which shares a border with British Columbia, in which six Salmonella infections were also linked to English cucumbers (27).

Outside the North American continent, a multi-country outbreak of Salmonella Agona was described in a joint report by the ECDC and the European Food Safety Authority. 147 cases were reported from five EU countries (the United Kingdoms (UK), Finland, Denmark, Ireland and Germany), with 122 cases since 2017 and 25 historical cases between 2014 and 2016. The UK had the most cases (129), followed by Finland (15). Human samples were analysed using the core genome multilocus sequence typing scheme and were found to be genetically close (with a maximum difference of 2 alleles), suggesting a common source. Although Salmonella food isolates from cucumbers (17 isolates) were found to be genetically linked to the human serotype, pointing to cucumbers as a possible vehicle of contamination, there was inefficient epidemiological information to definitively prove this hypothesis. These isolates were found in both cucumbers during processing (before and after washing) and ready-to-eat products, but all contaminated samples were from separate production chains, and thus there was no concrete evidence of where contamination might have taken place. This report highlights the challenges of traceback investigations, especially in navigating complex production chains where multiple processing stages take place in different countries (28).

The association found between Salmonella outbreaks and cucumbers is new. To the best of our knowledge, there are no outbreaks of Salmonella associated with cucumbers in the literature prior to the first USA multistate outbreak in 2013.

Salmonella in other fruit and vegetables

Whilst cucumbers are a novel vehicle, outbreaks of Salmonella are also associated with other types of fruit and vegetables have previously been identified as the cause of Salmonella outbreaks globally, including leafy vegetables, papayas, tomatoes, melons, sprouts, shredded coconut, peas and hazelnuts (29-61). Major identified outbreaks are summarised in Table 1 below.

Changing trends in Salmonella outbreaks

Whilst there have been no Salmonella outbreaks associated with cucumbers reported in Australia to date, outbreaks of Salmonella associated with fruit and vegetables appear to be increasing in recent years. In Australia from 2001 to 2005, 4% (n=16) of foodborne outbreaks where a vehicle was identified were linked to fruit and vegetables (62). In annual reports from OzFoodNet, Australia’s foodborne disease surveillance network, it was reported that in 2007, 7/56 (8%) of outbreaks were a vehicle was identified were caused by fruit and vegetables (63). In 2008, 6/75 (8%), of food borne outbreaks where a vehicle were caused by salad and/or sandwiches (64). Data from 2009 is similar, with a total of 69 foodborne outbreaks had a vehicle identified, of which eight (12%) were caused by fruit and vegetables or sandwiches (65). Data from 2010 and 2011 was reported for outbreaks in which a single food source was identified as the cause of an outbreak. In 2010, 3/43 (7%) were caused by fruits or nuts (9) and in 2011, 3/49 (6%) were caused by fruits, nuts, grains or beans (10). More recent annual national data in relation to foodborne outbreaks does not appear to be published.

The increase in fruit and vegetable-related Salmonella outbreaks has also been shown in the USA. Outbreaks which were caused by fruit and vegetables rose from less than 1% in the 1970’s to approximately 6% in the 1990s (66). A review of data from the USA showed that from 1973 to 1997 showed the proportion of foodborne outbreaks occurring linked to fruit and vegetables had increased in this time from 0.7% to 6%. The most commonly identified bacteria associated with these outbreaks was Salmonella. A number of different food vehicles were identified, but of these the most common identified were lettuce, sprouts, melon, and berries (67). More recent US data, from 1990-2005 showed that fruit and vegetables is responsible for 13% of foodborne outbreaks (68). An additional review from 1973 to 2012, 5% (n=606) of foodborne outbreaks in the USA were caused by leafy greens. Of those with a cause identified, 11% were identified as Salmonella (69). It has been shown that some serotypes of Salmonella are more common to plant-derived foods, with data from 1998–2008 showing that serotypes Javiana, Litchfield, Mbandaka, Muenchen, Poona, and Senftenberg were responsible for greater than 50% of outbreaks caused by foods that come from plants (13). A review of melon associated outbreaks in the USA showed that from 1973 to 2011 showed that the rate of melon associated outbreaks was found to increase over this time period from 0.5 to 1.3 outbreaks per year. For outbreaks in which the source had been identified, the majority were imported from Mexico (9/13). The majority of contamination was also identified to occur during the production process at different stages including during the growing, harvesting, processing and packaging stages (70).

Incidence of Salmonella in cucumbers

Salmonella contamination has been identified in cucumbers globally. In April 2011, the U.S. Food & Drug Administration (FDA) found cucumbers positive for Salmonella during routine testing. The company was informed and a recall was put in place. There was no associated illness reported with these contaminated cucumbers (71). Salmonella has also been found in cucumbers in Japan as a result of its National Food Surveillance System, which was initiated in 1998 following three major outbreaks in 1996-1997 linked to radish sprouts from school lunches. Data from 1998 to 2009 shows that Salmonella was detected in approximately 0.1-0.2% of cucumber samples tested for food safety surveillance (72).

Emergence of new serotypes

Traditionally, global epidemiology of salmonellosis tends to be dominated by a few Salmonella serotypes. For example, in 1995, more than 76% of global isolates were caused by Salmonella Enteritidis, Typhimurium and Typhi (4). These serotypes, especially Enteritidis, were associated with eggs and poultry, thus making these food groups the target of food surveillance programmes and control measures by public health authorities (73).

Among outbreaks caused by fruits and vegetables in 2017-2019, some were caused by typical serotypes, such as Salmonella Newport (22,38,45,58), Infantis (26,38) and Typhimurium (31,43,59,60). However, many other outbreaks were associated with less common serotypes. For example, Salmonella Anatum, which was implicated in 2016 multistate outbreak in Australia (29) and 2017 multi-state outbreaks in the US (39), had been previously popular in Asia, Africa and South America, but had not been reported in North America from 2001-2007 (74). Similarly, serotypes St Paul, Poona, Oslo and Agona were behind major outbreaks associated with cucumbers in the USA and Europe (21,23,25,28), although they have not been featured in the top 5 common serotypes in these regions from 2001-2007 (74). Most significantly, serotype Enteritidis – the world’s leading Salmonella serotype (6) – was notably absent in these outbreaks

Modes of contamination

There is growing evidence which shows the ways in which Salmonella can contaminate produce during growing, process, transport and storage. The rising number of Salmonella infections caused by fruit and vegetables has led to investigations into the mechanisms by which produce can become contaminated with Salmonella. These include produce grown close to water sources which have been contaminated by excretion from cattle and wildlife, exposure in fields to wild animals and their waste materials, sewage, and the use of contaminated fertiliser (69). In addition, a review of the literature investigated associations between contaminated fruit and vegetables, predominantly leafy greens and tomatoes, and growing practices. The study identified risks that increase the likelihood of contamination include growing produce in clay-type soil, the use of contaminated water and untreated manure, and the use of contaminated irrigation water (72). Contamination can also occur during storage and distribution if storage facilities and transport vehicles are not using appropriate hygiene and disinfectant procedures (75-76).

Reina, et al., found that several factors contribute to Salmonella surviving specifically on the surface of cucumbers. The most important of these are higher temperatures, higher concentration and longer length of exposure to contaminated water. The study also highlighted the importance of using appropriately treated water (77). One popular theory of contamination of fruit and vegetables currently being explored in the internalisation theory. This suggests that Salmonella may be able to enter and replicate within produce. To date experiments regarding internalisation have focused on leafy vegetables/greens and herbs (78). A recent study found that Salmonella can internalise in cucumbers when introduced in the early stages of growth via the flowers of the plant. When Salmonella was introduced via the flower, 83% (n=58) of cucumbers were contaminated with Salmonella and 67% (n=39) had internalised Salmonella. This was much lower for cucumbers which had Salmonella introduced into the soil (8%). The most common Salmonella identified in the contamination experiment was Salmonella Poona (70%) (79).

Other studies have investigated the length of time Salmonella can survive on the outside of fruit and vegetables. Evidence shows that once introduced on the surface of tomatoes, Salmonella can grow and live for up to 18 days depending on temperature. Higher concentration of the Salmonella was shown in the first seven days (80). Tomatoes have also been shown to internalise Salmonella. This can occur when tomatoes are washed in water that is contaminated and a lower temperature than the tomatoes, which causes the produce to draw in water, along with the contaminants (67).

Data from 21 farms growing produce in New York State show that Salmonella can be found in irrigation and non-irrigation water, 6.1% of fields and 11% of water samples. Although only 4% of water positive samples were from water used for irrigation purposes, the study found that the use of manure to fertilise a field within the last year and cultivation of the field within the previous 7 days were associated with a higher risk of Salmonella contamination. A buffer zone of 5 metres or more from potential risks such as animals or contaminated water was associated with a decreased risk of Salmonella contamination (81).

Changes in cucumber production and consumption

The increase in outbreaks associated with fruit and vegetables may be due to several factors including changes in the diet of populations. The US population have increased their per capita consumption of fruits and vegetables from 95kg per capita in 1970 to 114kg per capita in 2013, according to statistics from the Food and Agriculture Organisation (82). Australia’s per capita intake of fruits and vegetables has increased over time. The Australian Bureau of Statistics report that Australians ate 162kg per capita of vegetables in 1998-1999, which increased from 117kg per capita in the late 1950’s. A similar trend is seen with fruit; reported consumption was 135 kg per capita in 1998-1999, increasing from approximately 85kg per capita in the late 1960’s (83).

There are also different issues which need to be considered with fruit and vegetables such as cucumbers. These include the facts that the typical shelf life of cucumbers is 16-25 days (84), and fruit and vegetables are often eaten raw, with no heating method to eliminate possible contamination. In addition, cucumbers specifically, may often be eaten with the skin on. Other factors which may contribute to the increase in produce-related outbreaks are changes in methods of food production, and an increase in the distance in which produce is transported (85).

Prevention

With the number of outbreaks associated with fruit and vegetables, and cucumbers specifically, prevention is key to limiting the spread. Methods of sanitising fruit and vegetables for consumers is limited. This is because a lot of fruit and vegetables, such as cucumbers, are eaten raw so bacteria can’t be killed with heat as with chicken. Additionally, washing vegetables with water alone under commercial conditions is not particularly effective to reduce Salmonella risk to consumers (86), and in some cases can even introduce risks of cross-contamination (87).

There are several methods used to sterilize food prior to consumption, including chlorine, high pressure processing, the use of UV light and high temperature treatments. Research has shown that chlorine can be effective at reducing Salmonella contamination in tomatoes but only when used at appropriate concentrations (80). This may be less effective due to the strength of the attachment of the bacteria to fruit and vegetables, as well as the difficulty in accessing inner parts of fruit and vegetables. Both UV light and the use of high temperatures to eliminate Salmonella in fruit and vegetables have been shown to be effective. However, high levels of both types of interventions are needed to successfully kill or eliminate Salmonella from fruit and vegetables, and they have been shown to damage the produce being treated in some instances (70).

As shown, each of these methods have limitations in terms of reducing the contamination on the surface of fruit and vegetables, and do not address the issue of internalisation. Visible blue light is a new prevention measures being investigated. Cucumbers were used to test the effectiveness of this prevention method in killing bacteria. The results showed that the use of visible blue light at appropriate levels killed between 80 and 100% of Salmonella (88). The investigation of new methods of sanitisation of fruit and vegetables should continue. A combination of regulation, legislation and auditing of suppliers to ensure good agricultural practices is critical, which remains a challenge for internationally marketed products.

Discussion

The recent outbreaks of Salmonella reported in the USA have identified cucumbers as a novel vehicle for Salmonella outbreaks. With the number and severity of cases associated with the most recent outbreaks of Salmonella associated with produce, it is unlikely that the increase in outbreaks caused by fruit and vegetables is artefactual and represents a real change in the epidemiology of Salmonella. The sizeable geographic spread also suggests that the outbreaks are caused by a source early in the supply chain, prior to distribution, which is supported by trace-back investigations. Whilst cucumbers are a novel vehicle for Salmonella outbreaks, outbreaks associated with other types of fruit and vegetables have increased in recent decades such as papayas, tomatoes and melons (67, 32, 40-51). This is due to contamination on the surface of produce as well as the possibility of bacteria internalization (67, 78-81). There are a number of ways in which produce can become contaminated during the growing, storage and delivery stages, including insufficiently sanitized irrigation water and processing equipment (69, 75-77).

Increases in the consumption of fruit and vegetables and the increased distance between distribution and sale may account for some of these infections. However, the recent outbreaks raise several issues that require exploration, including possible changes to farming practices, changes in the number, frequency and location of imports of cucumbers, and the need for tighter regulations for farming and exportation of fruit and vegetables. Of the trace-back investigations that have been conducted and reported, it appears that many cucumber outbreaks in the USA have been caused by produce imported from Mexico (21).

Given the limited availability of prevention methods for consumers to reduce their own risk, food safety at the pre-harvest and production phase is important. There are currently several methods available to sterilize fruit and vegetables including the use of chlorine, UV light and high temperature treatments (69, 80). However, each of these methods have limitations in relation to fruit and vegetables. There are new technologies such as visible blue light being explored to protect fruit and vegetables from contamination (84).

The emergence of less common serotypes among Salmonella isolates raises the question of whether these serotypes should be incorporated in foodborne surveillance programmes for this food group (vegetables and fruits). There are several possible reasons behind this emergence. The first theory is that these serotypes are traditionally found in nonhuman sources (e.g. food and live animals), for which routine surveillance was limited due to international trade concerns (6). With the rise in incidence of outbreaks related to vegetables and fruits, testing of nonhuman sources as part of traceback investigations brings to light these serotypes. Another possibility is that of a real change in epidemiologic features of salmonellae, which warrants further epidemiologic studies.

The list of outbreaks in this review is non-exhaustive and does not reflect the true incidence of Salmonella worldwide. It is highly possible that publication bias is present as outbreaks outside Northern America, Australia and Europe may be under-represented for various reasons: use of languages other than English for reporting, absence of an active surveillance and reporting system, or lack of mandatory laboratory culture protocols for foodborne outbreaks.

Conclusion

It is clear the numbers of Salmonella outbreaks caused by fruit and vegetables are increasing, with new, less common serotypes emerging among nonhuman isolates. Further investigation into this issue is required to better understand the role of fruit and vegetables in Salmonella outbreaks and new effective methods for sanitization at the production stage are needed.

Supplemental Information

Additional figures can be found here.

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