ABSTRACT

Bacillus cereus has been reported as a foodborne pathogen worldwide. Although food processing technologies to inactivate the pathogen have been developed for decades, foodborne outbreaks related to B. cereus have occurred. In the present review, foodborne outbreaks, germination, inactivation, and detection of B. cereus are discussed, along with inactivation mechanisms. B. cereus outbreaks from 2003 to 2016 are reported based on food commodity, number of cases, and consequent illnesses. Germination before sporicidal treatments is highlighted as an effective way to inactivate B. cereus, because the resistance of the pathogen increases significantly following sporulation. Several germinants used for B. cereus are listed, and their efficacies are compared. Finally, recently used interventions with sporicidal mechanisms are identified, and rapid detection methods that have been developed are discussed. Combining two or more interventions, known as the hurdle technology concept, is suggested to maximize the sporicidal effect. Further study is needed to ensure food safety and to understand germination mechanisms and sporicidal resistance of B. cereus.

HIGHLIGHTS
  • Bacillus cereus has been associated with several foodborne outbreaks.

  • Several germinants have been used to induce Bacillus cereus germination.

  • Resistance of Bacillus cereus may depend on the germination method.

  • Sporicidal effect of interventions can be maximized by hurdle technology.

Globalization is one of the most popular keywords of modern society. People can travel throughout the world and enjoy local food and drinks at relatively low expense. Moreover, people can indulge in local food from other countries through trade. Despite the availability of these food products, food safety remains an issue of concern. Globalization increases the risk of foodborne illnesses, because disease can spread rapidly (68). In addition, factors such as antibiotic resistance and climate change contribute to these repeated foodborne outbreaks, despite developments in food science and technology (50). In this regard, foodborne illness has become one of the most important issues related to public health worldwide. The Centers for Disease Control and Prevention reported that one in six people acquires a foodborne illness each year, resulting in 128,000 hospitalizations and 3,000 deaths in the United States (11). Bacterial and viral pathogens were the top two causative agents in the United States, related to 39.5 and 46.9% of foodborne illnesses, respectively, in 2017 (12). Bacterial pathogens were the most prevalent causative agents in South Korea and were related to 62.9% of foodborne illnesses in 2017 (43). It has been reported that some bacterial pathogens, such as Escherichia coli O157:H7, Salmonella, Vibrio parahaemolyticus, Campylobacter, Staphylococcus aureus, Clostridium perfringens, and Bacillus cereus, are major sources of these outbreaks (56, 60). In this regard, several interventions have been adopted to control microbiological hazards such as E. coli O157:H7, Salmonella Typhimurium, Listeria monocytogenes, B. cereus, and norovirus (34, 35, 40). Among these hazardous microorganisms, Bacillus species are found to have high resistance to external physical or chemical treatments via the formation of endospores (52).

Bacillus species, which are ubiquitous in nature, are characterized as gram-positive, rod-shaped, spore-forming bacteria (17). Some Bacillus species are obligate aerobes, while most species are facultative anaerobes (4). Two species of Bacillus are primarily known to be hazardous: B. anthracis and B. cereus (7). Anthrax, a fatal disease to the human body, is caused by skin, lung, or gastrointestinal infection by B. anthracis (8). In contrast, intoxication by B. cereus is usually mediated via food products. Foodborne illness can be caused by food contaminated with more than 100,000 CFU/g (5 log CFU/g) of B. cereus and is further divided into diarrheal and emetic syndromes (58). Enterotoxins related to the diarrheal syndrome are produced in the gut and are known to be heat sensitive, whereas the toxins related to the emetic syndrome (cereulide) are already present in food and are known to be heat stable (22). It has been reported that various foods may be associated with the diarrheal syndrome, while rice is the major source of the emetic syndrome (2). Thus, B. cereus remains a microorganism of concern with respect to food safety, and it is of interest to understand recent attempts to control B. cereus contamination and/or growth in food products.

In the present review, recent outbreaks by B. cereus (2003 to 2016) and studies about the germination and inactivation of B. cereus are discussed to add to the existing body of review literature (1, 9). This article covers several germination agents and sporicidal interventions, as well as a combination of those technologies, also known as hurdle technology. Details regarding recent B. cereus outbreaks and data concerning the germination and inactivation of the pathogen may be helpful in controlling B. cereus in food products and preparing for potential future outbreaks.

RECENT FOODBORNE OUTBREAKS CAUSED BY B. CEREUS (2003 TO 2016)

Foodborne outbreaks caused by B. cereus have been reported (Table 1). Various foods, such as pasta salad, spaghetti, tomato sauce, navy beans, refried beans, and water have been indicated as contamination sources of B. cereus (10, 13, 15, 49, 51), resulting in hospitalizations and two deaths. Severe metabolic acidosis and liver failure were indicated as causes of death. Most cases were attributed to incorrectly preserved food, such as refrigeration temperatures as high as 14°C (15) or long-term storage of the food at room temperature (49). Food stored at a refrigeration temperature (ca. 4°C) may suffer temperature abuse, leading to increased growth of the pathogen; thus, in many cases, refrigeration is not a fundamental solution for B. cereus foodborne outbreak prevention contingent on temperature control of refrigeration systems. In particular, some B. cereus species, known to be psychrotrophs, growing at a refrigeration temperature (6°C), could increase the risk of foodborne outbreaks (24).

TABLE 1

Foodborne outbreaks by B. cereus, 2003 to 2016

Foodborne outbreaks by B. cereus, 2003 to 2016
Foodborne outbreaks by B. cereus, 2003 to 2016

From reported outbreaks of B. cereus, it can be deduced that several factors, including food storage location, contamination source, and dissemination of foods, may affect the number of illnesses. Outbreaks that occur as a result of restaurant meals or by meal services may be involved in significantly higher numbers of foodborne illnesses than household cases. Moreover, contaminated underground water can lead to large outbreaks by contaminating foods directly or indirectly via utensils. Cross-contamination from a contaminated environment, utensils, or food handlers to the food products can occur during food preparation (23). Kusumaningrum et al. (39) reported that foodborne pathogens remain viable on dry stainless steel surfaces and transfer to foods at rates of 20 to 100%. In this regard, cross-contamination of B. cereus can occur because B. cereus cells are can survive in dry conditions for long periods following sporulation. It is impossible to avoid cross-contamination, but the cross-contamination rate can be reduced by implementing management programs such as hazard analysis and critical control point, good agricultural practices, and good manufacturing practices, because these programs deal with water, food processing, utensils, education, etc.

GERMINATION OF B. CEREUS ENDOSPORES

Harsh conditions, often including nutrition limitation, prompt Bacillus species to protect themselves via sporulation (3). The resistance of Bacillus species to external chemical or physical treatments increases following sporulation because of a multilayer structure (31). A vegetative cell has peptidoglycan in its exterior, while spores have additional structures, including the cortex, spore coats, and exosporium (Fig. 1). Even though peptidoglycan and the cortex look similar, a cortex-lytic enzyme can differentiate the two structures (46). Spores can respond to the surrounding environment based on receptors and may revert to the vegetative state when external conditions become favorable through germination (20).

FIGURE 1

Example structure of a B. cereus spore.

FIGURE 1

Example structure of a B. cereus spore.

The general mechanisms of nutrient germinants such as l-alanine on bacterial endospores is described as follows (44). First, the germinant transverses the inner membrane adjacent to the germinant receptor. Some cations and dipicolinic acid are released from the core after the germinant binds to the receptor. At this stage, rehydration is observed in the core, and cortex hydrolysis occurs. Finally, the spore coat collapses, and the cell begins outgrowth. Several germinant agents for B. cereus spores have been reported (Table 2). l-Alanine and inosine have been widely used for the germination of B. cereus spores. Various other agents, such as disodium 5′-inosinate, adenosine, or other amino acids, can also be used for germination (70). It has been reported that the germination efficacy depends on the bacterial strain and treatment conditions. For example, it was reported that B. cereus ATCC 14579 could be germinated not only with the addition of l-alanine and inosine but also by disodium 5′-inosinate, l-cysteine, l-threonine, and l-glutamine (29). A combination of more than two germinants can have a synergistic effect compared with individual treatments; thus, it is supposed that several germinants can bind to multiple receptors simultaneously or sequentially. In this regard, further study is needed to maximize B. cereus germination by investigating novel germinants or by combining already reported germinants.

TABLE 2

Agents used for germination of B. cereus

Agents used for germination of B. cereus
Agents used for germination of B. cereus

SPORICIDAL TREATMENTS FOR THE INACTIVATION OF B. CEREUS

Thermal treatments with or without high pressure have been conventionally used for the inactivation of B. cereus spores (57), while several attempts using superheated steam, UV-C irradiation, pulsed electric field, thermosonication, and gaseous chlorine dioxide treatments have also been recently reported (Table 3). Maximum reduction rates of B. cereus spores varied from 4- to 7-log CFU depending on the sporicidal treatments and treatment conditions. In addition, biocontrol using bacteriophages is a novel approach for the inactivation of B. cereus spores (37).

TABLE 3

Sporicidal treatments used for the inactivation of B. cereus spores

Sporicidal treatments used for the inactivation of B. cereus spores
Sporicidal treatments used for the inactivation of B. cereus spores

Treatment conditions in the literature varied based on sample type, treatment method, and B. cereus strain. For example, the temperatures of superheated steam were 120 to 180°C and 200 to 300°C for garlic and stainless steel coupon treatments, respectively. In the study focusing on stainless steel coupon treatments, the treatment time or the temperature of the superheated steam could be reduced by combining it with UV-C irradiation. In this regard, researchers investigated the combination of treatments maximizing the sporicidal effect, including a pulsed electric field–nisin combination and a thermosonication treatment. Marco et al. (42) also reported that the addition of olive powder had an additive effect on high hydrostatic pressure processing of B. cereus spores. Samples with 2.5% olive powder treated at 400 and 500 MPa showed inhibition of B. cereus growth at 32°C when B. cereus outgrowth rates at 32 and 20°C were examined under 0, 200, 500, and 500 MPa with or without 1.5 and 2.5% olive powder. Sagong et al. (55) demonstrated the combined effect of ultrasound and surfactants to inactivate B. cereus spores on lettuce and carrots. These combination treatments are more effective in inactivating B. cereus or in inhibiting the growth of B. cereus than the treatments applied individually. However, the treatment conditions may be too harsh for some food commodities, resulting in quality deterioration.

Germination before sporicidal treatment has been reported as an effective way to control B. cereus spores, minimizing the deterioration of food quality (21). Various germinants or germination methods have been used, as indicated in the previous section. Spore cells enter the vegetative state during germination, and inactivation of germinated cells is comparably less difficult than inactivation of spores. However, some limitations have been pointed out related to application in the food industry. Germination of spores may be induced in liquid food products, but it is more difficult to apply these methods to semisolid or solid food products. In particular, reported germination methods are difficult apply to powdered food products, such as red pepper powder and pepper powder, in which large numbers of heat-resistant spores have been detected (33). Moreover, it was recently reported that the resistance of germinated cells to water-bath heating was significantly higher than that of the original vegetative cells (30). Reductions of B. cereus vegetative cells ranged from 4 to 4.5 log CFU/g after 30 to 90 s of heating at 80°C, whereas the reductions of wet heating germinated spores were 1 to 1.5 log CFU/g. Furthermore, the thermal or pressure resistance of B. cereus was influenced by the sporulation temperature (54) and the pH of the sporulation medium (53). These results indicate that the resistance of pathogens can change following germination, which is an important factor to be considered before application of an inactivation technology. In this regard, practical germination and sporicidal methods to control the spores in the various types of food products, including powders, should be investigated further.

MECHANISMS FOR THE INACTIVATION OF B. CEREUS

Identifying bactericidal mechanisms for B. cereus has been of interest, and several have been proposed (Table 4). It is well known that key proteins are denatured by heat treatments, while an acid-shock effect may lead to cell death by the accumulation of excessive radicals (14, 45). Similar to the acid-shock effect, reactive oxygen species produced from cold plasma treatment damage the internal macromolecules or molecular systems that are critical to cell metabolism (16). It has been reported that reactive oxygen species also play a role in the inactivation of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes by UV irradiation (32), and a similar mechanism may be suggested for the inactivation of B. cereus by UV-C irradiation, even though related investigations are limited. Ultee et al. (61) reported that changes in membrane potential and permeability led to cell death, and Na et al. (47) indicated that endolysin produced by bacteriophage PBC4 showed enzymatic activity for B. cereus. Likewise, various targets and mechanisms have been suggested for the inactivation of B. cereus.

TABLE 4

Mechanical mode of action for the inactivation of B. cereus

Mechanical mode of action for the inactivation of B. cereus
Mechanical mode of action for the inactivation of B. cereus

Multiple inactivation targets for B. cereus would be one of the factors contributing to the synergistic effect by the hurdle technology, because several targets may be damaged simultaneously with the combined treatments. Targets for B. cereus spores may be more diverse compared with those for vegetative cells, because the structure of the spore is more complicated, as indicated in Figure 1. Ha and Kang (25) indicated that damage to the ribosome and cell wall, but not to DNA and RNA, accumulated by the combination treatments of UV-C irradiation and near-infrared heating for the inactivation of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes. Comprehensive studies concerning the inactivation mechanisms of B. cereus spores by combination treatments are limited, even though an increased dipicolinic acid release ratio was observed by the combination treatments of superheated steam and UV-C irradiation (36). Further research is needed to identify the underlying mechanisms of individual or combined treatments for the inactivation of B. cereus.

METHODS FOR DETECTING B. CEREUS

The U.S. Food and Drug Administration (FDA) reported that B. cereus grows at temperatures between 4 and 48°C, with optimal growth temperatures of 28 to 35°C and a pH range of 4.9 to 9.3. The bacteria's salt tolerance was indicated as 7.5% (63). The FDA recommended against holding B. cereus outbreak–associated foods, such as meat, poultry, starchy foods (rice and potatoes), pudding, soups, and cooked vegetables, in the danger zone of 5 to 57°C (64). Moreover, it is important to monitor populations of B. cereus and temperatures during transportation, processing, and preservation. The Bacteriological Analytical Manual published by the FDA suggests mannitol–egg yolk–polymyxin agar as a standard medium for plating B. cereus (59). This is part of a conventional method to detect B. cereus in food products, but it has a limitation of being time-consuming. Therefore, several rapid detection methods have been developed to detect B. cereus in food products.

Various attempts have been made to detect B. cereus rapidly. PCR has long been adopted for the detection of B. cereus. Hansen and Hendriksen (26) indicated that the enterotoxic B. cereus and Bacillus thuringiensis strains can be detected by PCR using primer sets for the detection of genes encoding the enterotoxin. Lim et al. (41) developed a duplex real-time PCR method to differentiate emetic B. cereus from the nonemetic B. cereus in food products. Wehrle et al. (69) used a multiplex real-time PCR assay based on SYBR green I to differentiate Bacillus groups (B. cereus, B. mycoides, B. thuringiensis, and B. weihenstephanensis), while Forghani et al. (19) developed a rapid multiplex real-time PCR assay for the simultaneous detection of B. cereus, L. monocytogenes, and S. aureus in food products. In this regard, PCR can be used effectively for the detection of B. cereus. However, it is still difficult to differentiate B. cereus from B. thuringiensis in food products by PCR. Methods using double-antibody sandwich enzyme-linked immunosorbent assay (71) or endolysin cell wall binding domain from bacteriophage (38) have also been reported. The major limitation of these methods is that their efficiency decreases significantly when applied to complex food matrixes. Further study is needed to increase rapid B. cereus detection sensitivity and selectivity in various food products.

REGULATIONS TO CONTROL SPORE-FORMING PATHOGENS IN FOODS

Several regulations have been indicated to ensure microbiological safety in food products. The U.S. Department of Agriculture (USDA) cited the bacterial danger zone as 4.4 to 60°C, in which bacteria can grow rapidly in food products (62). The USDA recommends not leaving food products out of refrigeration for 2 h (or 1 h when the ambient temperature is above 32°C) (62). Moreover, it is recommended to roast meat and poultry at temperatures higher than 162°C (324°F) and to reheat food thoroughly to an internal temperature of 60, 63, 71, and 74°C for ham, beef, ground meat, and poultry, respectively, after prolonged storage to inactivate reintroduced microorganisms (62). The Pasteurized Milk Ordinance indicates that the interaction of pH and water activity (aw) affects the control of spores in milk and milk products (66). Time-temperature treatments are not needed when the pH is lower than 4.6, but time-temperature treatments are required when pH values are 4.6 to 5.6 and aw is higher than 0.95 or pH is higher than 5.6 and aw is higher than 0.92. The Food Safety Modernization Act (FSMA) guidance for the industry indicates that the growth conditions of B. cereus are as follows (65): minimum aw, 0.92; minimum pH, 4.3; maximum pH, 9.3; maximum percentage of water-phase salt, 10; minimum temperature, 4°C; and maximum temperature, 55°C. From these growth conditions, FSMA reported the following time-temperature guidance for the growth and toxin formation conditions by B. cereus in food products: 4 to 6°C, 5 days; 7 to 15°C, 1 day; 16 to 21°C, 6 h; and more than 21°C, 3 h.

CONCLUSIONS AND RECOMMENDATIONS

B. cereus is a foodborne pathogen of interest involved in several foodborne outbreaks and deaths, and cases may exceed the number reported based on limitations in reporting systems and data collection. Control of B. cereus in food, in groundwater, and on utensils during processing is essential, including preventing cross-contamination. Foodborne illnesses from B. cereus can occur even when food samples are pasteurized appropriately because of surviving spores; thus, challenge studies for conventional or alternative inactivation treatments are critical, as well as postprocessing cold storage.

Inducing germination before an intervention treatment is one of the most effective ways to control B. cereus spores. Various germinants have been reported, but the resistance of B. cereus to intervention treatments following germination may increase and should be studied further. Germinated B. cereus can be inactivated effectively by combination treatments, which have received attention as alternative technologies. Several hurdle technologies have been indicated for the inactivation of spores or germinated cells in the present review, while more studies are needed for technologies applied singly or in combination. In addition, understanding of the bactericidal mechanisms by individual or combined interventions and development of rapid detection methods are helpful in providing more meticulous control of B. cereus in the food industry.

ACKNOWLEDGMENT

The present research was conducted by the research fund of Dankook University in 2019.

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