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Tolerance to refrigeration (a), freezing (b), and heat (c) stresses in 70 strains of C. jejuni from retail chicken. The results are representative of three independent experiments. Similar results were observed in all three experiments. Solid black bars show the mean CFU. Statistical significance was determined using two-way ANOVA. **P < 0.01, ***P < 0.005, ****P < 0.0001.
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Campylobacter jejuni is a microaerophilic foodborne pathogen that is sensitive to stress conditions. However, it is not yet understood how this stress-sensitive pathogen may cause a significant number of cases of human gastroenteritis worldwide. In this study, we examined stress tolerance in 70 C. jejuni strains isolated from retail chicken under s...
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... in the chicken supply system. In addition, C. jejuni will be exposed to high temperatures during cooking. The OS strains exhibited a significant CFU reduction at a refrigeration temperature. Storing at 4 °C for seven days reduced bacterial counts by approximately 4.9, 5.1, and 7.4 CFU/ml in the HAT, AT, and OS strains of C. jejuni, respectively (Fig. 4a). Similarly, the OS strains of C. jejuni were more sensitive to freeze-thaw stress that the AT and HAT strains. More than half (ca. 52%) of HAT and AT strains survived at −20 °C for seven days; however, only two OS strains were detected after seven days (Fig. 4b). Unlike the results of the refrigeration and freeze-thaw tolerance tests, ...
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... 4.9, 5.1, and 7.4 CFU/ml in the HAT, AT, and OS strains of C. jejuni, respectively (Fig. 4a). Similarly, the OS strains of C. jejuni were more sensitive to freeze-thaw stress that the AT and HAT strains. More than half (ca. 52%) of HAT and AT strains survived at −20 °C for seven days; however, only two OS strains were detected after seven days (Fig. 4b). Unlike the results of the refrigeration and freeze-thaw tolerance tests, the aerotolerance level was not associated with thermotolerance as only one HAT strain and one AT strain survived after exposure to 70 °C for 30 sec (Fig. 4c). Based on the findings, C. jejuni strains from retail chicken exhibited different levels of tolerance to ...
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... HAT and AT strains survived at −20 °C for seven days; however, only two OS strains were detected after seven days (Fig. 4b). Unlike the results of the refrigeration and freeze-thaw tolerance tests, the aerotolerance level was not associated with thermotolerance as only one HAT strain and one AT strain survived after exposure to 70 °C for 30 sec (Fig. 4c). Based on the findings, C. jejuni strains from retail chicken exhibited different levels of tolerance to cold and heat stresses, and AT and HAT C. jejuni were highly tolerant to refrigeration and freeze-thaw stresses, but not to heat stress. tolerance to hyperosmotic stress. Hyperosmotic stress is a stress condition for Campylobacter ...
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... AT and HAT strains of C. jejuni were more tolerant to refrigeration and freezing temperatures compared to OS strains (Fig. 4a,b). Most bacterial species, such as E. coli, Salmonella, and Bacillus, produce cold shock proteins upon a temperature downshift [30][31][32] . However, C. jejuni does not possess genes encoding cold shock proteins 15 , which suggests that C. jejuni may have other tolerance mechanisms to respond to cold shocks. Studies thus far have shown ...
Citations
... Aerotolerance in Campylobacter also correlates with the ability to survive other stressful conditions. For example, a high percentage of cold-tolerant C. jejuni strains were also aerotolerant and showed higher survival in response to refrigeration and freeze-thaw stress [16,19,78,89,90]. However, there was no correlation between aerotolerance in different Campylobacter strains and their ability to survive in refrigerated milk [91]. ...
... A genetic link between the cold stress response and oxidative stress response has also been suggested [92][93][94], which is discussed further in Section 5.2 of this review. Strains of C. jejuni with increased aerotolerance survived better than aerosensitive strains when exposed to peracetic acid [90]. It is important to mention that evidence is conflicting as to whether aerotolerance correlates with resistance to heat and osmotic stress [19,90]. ...
... Strains of C. jejuni with increased aerotolerance survived better than aerosensitive strains when exposed to peracetic acid [90]. It is important to mention that evidence is conflicting as to whether aerotolerance correlates with resistance to heat and osmotic stress [19,90]. Currently, the number of published studies examining the correlation between aerotolerance and other environmental traits is relatively small, and further research is needed to explore the significance and prevalence of these correlations. ...
Campylobacter spp. constitute a group of microaerophilic bacteria that includes strains that are aerotolerant and capable of surviving in aerobic conditions. Recent studies have shown that aerotolerant strains are highly prevalent in meats, animals, and clinical settings. Changes in growth media and other environmental conditions can affect the aerotolerance of Campylobacter strains and must be considered when studying their aerotolerance in vitro. Polymicrobial interactions and biofilms also play a significant role in the ability of Campylobacter to survive oxygen exposure. Continuous subculturing may foster aerotolerance, and studies have demonstrated a positive correlation between aerotolerance and virulence and between aerotolerance and the ability to survive stressful environmental conditions. Various mechanisms and genetic origins for aerotolerance have been proposed; however, most of the potential genes involved in aerotolerance require further investigation, and many candidate genes remain unidentified. Research is also needed to investigate if there are any clinical implications for Campylobacter aerotolerance. Understanding the aerotolerance of Campylobacter remains an important target for further research, and it will be an important step towards identifying potential targets for intervention against this clinically important food-borne pathogen.
... However, C. jejuni may be collected from any number of environmental sources [2]. Planktonic C. jejuni is particularly sensitive to numerous stressors [4,5], notably oxygen pressure in the environment, which further complicates its ability to induce foodborne diarrheal disease [6,7]. This may be due to aerotolerance characteristics, which contribute significantly to the aerobic transmission of C. jejuni to humans through food [8]. ...
Background and Aim: Campylobacter jejuni is a major contributor to bacterial enteritis, a common health problem. The
resistance of this microaerophilic bacterium to oxidative stress allows it to thrive under aerobic conditions. This study
aimed to investigate whether the capacity of C. jejuni to form biofilms in the presence of oxidative stress contributes to the
pathogen’s ability to thrive in agricultural settings as well as in chicken slaughter lines.
Materials and Methods: Twenty identified strains originating from chicken samples (eight from caeca contents and
12 from frozen chicken carcasses) were previously isolated and identified according to standard bacteriological protocols,
followed by confirmation at the species level using multiplex polymerase chain reaction assay. Crystal violet staining was
used to evaluate biofilm formation by these bacteria. Two exposure periods to gaseous ozone (1 and 2 min) were used to
assess resistance to oxidative damage.
Results: Most of the strong biofilm-forming Campylobacter strains came from imported frozen chicken meat (25%), whereas
only 10% came from caeca content. After exposure to gaseous ozone at 600 mg/h for 2 min, strong biofilm-producing
strains exhibited a higher survival rate with a limited reduction of up to 3 logs, whereas negative biofilm-producing strains
exhibited a limited survival rate with a reduction of 6 logs.
Conclusion: Based on our findings, we hypothesized that the presence of C. jejuni strains capable of forming biofilms in
poultry farms and/or chicken production facilities triggers a public health alarm as this bacterium seems to be able to adapt
more easily to live and thrive in hostile environmental conditions.
Keywords: biofilm, Campylobacter jejuni, hostile environment, oxidative stress, poultry meat.
... For instance, C. jejuni is recognized as an important contributor to gastroenteritis and, in certain instances, may trigger the development of autoimmune conditions such as Guillain-Barré syndrome (GBS) and Miller Fisher syndrome during the transmission process (Al-khreshieh et al., 2023;Kemper and Hensel, 2023;Zhong et al., 2020). These biofilms shield the bacteria from various environmental stresses like UV radiation, desiccation, dehydration, as well as antibacterial and sanitizing agents, therefore, confirming their survival (Oh et al., 2019). Growing as a biofilm allows bacteria to demonstrate up to 1000-fold reduction in susceptibility to antibiotics (Hughes and Webber, 2017). ...
Chitosan is known to exert antimicrobial activity without the need for any chemical modification; however, new derivatives of chitosan can be created to target multi-drug resistant bacteria. In this study, chitosan (CS) was cross-linked with sodium tripolyphosphate to form nanoparticles, which were then coated with polyacrylic acid (PAA). The SEM images revealed that the CS-PAA nanoparticles had spherical shapes with smooth surfaces and the size of the dried nanoparticles was approximately 222 nm. Biofilm formation was significantly inhibited by 0.5 mg/mL of CS-PAA. In-situ optical microscopy showed that CS-PAA nanoparticles inhibited the bacterial biofilm formation in Campylobacter jejuni, Pseudomonas aeruginosa, and Escherichia coli after a single treatment with 40 μg. Additionally, 20 µg of CS-PAA nanoparticles demonstrated antibacterial activity against the growth of C. jejuni, P. aeruginosa, and E. coli with notable inhibitory zones of 9, 12, and 13 mm, respectively (P < 0.01). The development of a novel and ecofriendly method for the preparation of chitosan nanoparticles through an interaction of chitosan with PAA shows promise tool to combat bacterial infections and validates effective antibacterial and antibiofilm properties against antibiotic resistant pathogens.
... In addition, Studies have shown that drug-resistant and epidemic strains of Campylobacter jejuni are more effective in surviving on refrigerated raw chicken in the air than sensitive strains [18], the high prevalence of drug-resistant and epidemic strains of Campylobacter jejuni in retail poultry may affect food safety [19]. ...
... Bacterial tolerance to stress conditions threatens food safety by enabling foodborne pathogens to cope with harsh environmental conditions during foodborne transmission (Begley & Hill, 2015;Oh et al., 2019). C. jejuni is sensitive to environmental stress primarily due to the lack of stress-tolerant proteins commonly present in other well-studied foodborne pathogens (Battesti et al., 2011;Parkhill et al., 2000;Spector & Kenyon, 2012). ...
... Cold shock upshifts the expression of genes related to oxidative stress responses (Stintzi & Whitworth, 2003). Our previous study showed that C. jejuni strains with increased aerotolerance exhibit higher cold tolerance than aerosensitive strains (Oh et al., 2019). However, little is known about the mechanisms and bacterial physiology behind the cold tolerance of C. jejuni. ...
... In addition, our previous study also demonstrated that cfrA, encoding the ferric enterobactin receptor involved in ion transport and metabolism, contributes to cold tolerance in C. jejuni by altering the levels of intracellular iron and oxidative stress (Hur et al., 2022). Previously, we also demonstrated that aerotolerant C. jejuni strains, which possess increased levels of catalase and superoxide dismutase activities, are highly tolerant to refrigeration stress (Oh et al., 2019). These previous studies suggest that cold tolerance may be associated with oxidative stress defense in C. jejuni. ...
... The alteration of membrane fluidity with modified lipid bilayer compositions, the inhibition of membrane enzymes, and enzymatic decomposition or DNA disruption contribute to their survival under food preservation and sanitation conditions [3,4]. Many pathogens and spoilage bacteria are able to adapt effectively to various stresses in their environment [5][6][7][8][9][10]. Biocides and other stress factors during food pro-Bio ® Salmonella Base and Brilliance TM Salmonella Agar Base for Salmonella sp.; and Listeria Identification Agar Base-Palcam and ChromoBio ® Listeria Plus for Listeria monocytogenes [39][40][41]. ...
In this study, we determined and identified the bacterial diversity of different types of artisanal and industrially produced cheese. The antibiotic (erythromycin, chloramphenicol, kanamycin, ampicillin, clindamycin, streptomycin, tetracycline, and gentamicin) and biocide (peracetic acid, sodium hypochlorite, and benzalkonium chloride) resistance of clinically relevant bacteria was determined as follows: Staphylococcus aureus, Macrococcus caseolyticus, Bacillus sp., Kocuria varians, Escherichia coli, Enterococcus faecalis, Citrobacter freundii, Citrobacter pasteurii, Klebsiella oxytoca, Klebsiella michiganensis, Enterobacter sp., Enterobacter cloacae, Enterobacter sichuanensis, Raoultella ornithinolytica, Shigella flexneri, and Salmonella enterica. Also, the effect of the sub-inhibitory concentration of three biocides on antibiotic resistance was determined. The microbiota of evaluated dairy products comprise diverse and heterogeneous groups of bacteria with respect to antibiotic and disinfectant tolerance. The results indicated that resistance was common in the case of ampicillin, chloramphenicol, erythromycin, and streptomycin. Bacillus sp. SCSSZT2/3, Enterococcus faecalis SRGT/1, E. coli SAT/1, Raoultella ornithinolytica MTT/5, and S. aureus SIJ/2 showed resistance to most antibiotics. The tested bacteria showed sensitivity to peracetic acid and a different level of tolerance to benzalkonium chloride and sodium hypochlorite. The inhibition zone diameter of antibiotics against Enterococcus faecalis SZT/2, S. aureus JS11, E. coli CSKO2, and Kocuria varians GRT/10 was affected only by the sub-inhibitory concentration of peracetic acid.
... Survival is accomplished by lower temperatures (4-10°C), darkness and a moist atmosphere. Hence, retail storage conditions for poultry meat ins several countries are frequently ideal for survival of the Campylobacter, as long as meat is not frozen (10, 11). Although the bacteria are considered to be sensitive to stress related to environmental conditions, in the course of evolution, they were able to develop several complex mechanisms of survival and virulence factors, including motility, chemotaxis, adherence, and invasion of the host cell, structures of the cell envelope, iron uptake system, multidrug and bile resistance toxin production, and mechanisms of responses to stress (12,13). ...
... In most countries, the rate of infection is higher than 50% in broiler, layer, and turkey flocks (27, 28). C. jejuni is the predominant species in poultry, while C. coli is less common and C. lari is rare (6,11,25,29). Flocks younger than 3 weeks of age are rarely affected and there is also a seasonal variation, since infection rates are higher in spring and fall compare to winter and summer (30,31). In general, there are no evidence has been found either for vertical and/or for horizontal transmission from one flock to the next via persistent house-contamination. ...
The goal of poultry industry worldwide is the production of safe food products, via
efficient and goal-oriented health care to prevent the development of disease
conditions in poultry. However, a several number of poultry diseases can negatively
affect the breeding values and have the potential to be zoonotic and transmit the
infections to humans such as Campylobacteriosis. C. jejuni is highly prevalent in
commercial poultry farms and act as major reservoirs of the infection. Horizontal
transmission from the environment is considered to be the primary source of
bacterial foodborne worldwide. The high prevalence of Campylobacter spp. in
poultry meat is a result of several contamination and cross-contamination sources in
the entire production chain. Recent investigations demonstrated that various stages
of food processing in slaughterhouse and consumption of raw or undercooked
poultry meat is considered the significant risk factor for human Campylobacteriosis
worldwide. Furthermore, survival factors such as biofilm formation and
antimicrobial resistance, enable its persistence during food processing. On the other
hand, the increase of multiple and multidrug-resistant Campylobacter worldwide is
not only related to the over-consumption of antibiotics in human medicine, but also
in poultry production chain as growth promotors and/or to treat and prevent bacterial
infections. Antibiotic resistant Campylobacter presents an obvious and impending
challenge to One Health. In the future, the consumer expectations for high standards
quality of poultry products will strongly influence the production methods. This
means that farmers, stockholders’, veterinarians, and all other partners involved in
the production chain, will have to share more responsibilities and the cooperation
should be intensified. This review represents an updated overview of the global
epidemiology, the correlation of official control, the disease associated with food
handler and the importance of food safety with respect to Campylobacteriosis.
Keywords: Antimicrobial resistance, C. jejuni, Campylobacteriosis, Food safety, Human,
Poultry
... Hyper aerotolerant strains of C. jejuni are common in human infections that have been linked to poultry meat [12][13][14]. Although numerous studies have reported the aerotolerance level of C. jejuni isolates from various sources (chicken, humans, and dairy products) [12,15], there are limited studies that have reported the level of aerotolerance among isolates from commercial broiler processing plants. ...
... Based on this observation, the survivability of C. jejuni under cold stress may be underestimated since C. jejuni has been shown to tolerate refrigeration stress and survive [12]. Aerotolerant strains have been shown to survive longer in refrigeration compared to aero-sensitive ones [12,15]; however, these studies used a C. jejuni suspension in a 96-well plate that was stored at 4 • C for 7 days. Moreover, limited data are available on the relationship between the aerotolerance of C. jejuni and its cold tolerance in poultry meat. ...
... C. jejuni counts were reduced in all aerotolerance categories, though HAT strains were subject to a greater reduction at both storage conditions. These results differ from a previous study in which IAT and HAT were more tolerant compared to AS when incubated for 7 days at 4 • C and (−20 • C [15]. Similarly, another study showed that HAT is more tolerant to refrigeration and freezing than AS and IAT [12]. ...
Campylobacter jejuni is one of the leading causes of acute diarrhea in the United States. Despite being a microaerophilic pathogen, C. jejuni continues to endure within the domain of food production, especially in poultry processing. Recent research on aerotolerance indicates that close monitoring of this pathogen is necessary. A total of 40 C. jejuni isolates previously obtained from commercial broiler processing plants were analyzed for aerotolerance and genetic diversity. In addition, the effect of aerotolerance and storage time (days) on the survival of C. jejuni on broiler drumsticks at refrigeration (4 °C) and freezing conditions (−20 °C) was also evaluated. Out of 40 isolates, 25 (62.5%) were aero-sensitive (AS), 10 (25%) were intermediately aerotolerant (IAT), and 5 (12.5%) were hyper aerotolerant (HAT). The isolates belonged to four clonal complexes (CCs) and six sequence types, with the majority of isolates assigned to the CC–353 clonal complex. C. jejuni counts were reduced by 0.40 log CFU/g after 7 days at 4 °C and by 1.50 log CFU/g after 14 days at −20 °C, respectively, irrespective of aerotolerance (p < 0.001). At both refrigeration (p < 0.013) and freezing (p < 0.001), HAT showed greater reductions as compared to AS and IAT. These findings suggest that both refrigeration and freezing reduce C. jejuni counts.
... For example, Salmonella strains belonging to the S. Agona and S. Ohio serovars were highly resistant, showing no reduction in counts after 1 day of desiccation, whereas other strains within these same serovars displayed significant reductions of ≥3 logs CFU/mL. Even though other studies have demonstrated the variability in stress resistance amongst Salmonella strains or serovars, including acid, heat, oxidative and osmotic stresses (Guillén et al., 2020a;Guillén et al., 2020b;Lianou and Koutsoumanis, 2013;Oh et al., 2019;Shah et al., 2012;Sherry et al., 2004), this study is unique due to the large set of strains and serovars isolated from similar sources in the soybean processing chain. ...
This study compared the resistance to different desiccation conditions of 190 Salmonella enterica strains previously isolated from the soybean meal production chain and belonging to 23 serovars. Additionally, the post-rehydration growth and heat tolerance of the strains previously exposed to desiccation were determined. Variability in desiccation resistance was observed both within and between serovars. Strains belonging to S. Havana and S. Schwarzengrund serovars were the most resistant, regardless of storage condition. The drying temperature (20 °C and 30 °C) did not influence the desiccation resistance of the Salmonella strains. On the other hand, increasing drying time from 1 to 7 days reduced Salmonella counts. The origin (isolation sources) also influenced the desiccation resistance of the Salmonella strains. The growth of the Salmonella strains after rehydration varied considerably depending on the drying conditions and incubation temperature during cultivation. An increase in the time and temperature of drying led to a reduction in population of most Salmonella strains after rehydration. Salmonella strains previously desiccated also showed differences in the heat tolerance in all temperature-time binomials tested. Some strains were highly resistant to heat tolerance conditions, presenting <1 log CFU/mL reduction from the initial population. The results obtained in this study suggest that the strategies to mitigate Salmonella in low-aw foods must consider the existence of high-stress resistant strains and their multiple-stress adaptability profiles, including effects of processing, food composition, and storage conditions.
... In the current study, from IFC, only 3 out of 75 (4%) were characterized as Campylobacter, and only 2 confirmed cases of C. jejuni were obtained. It has been proven that freezing clearly decreases the viability and capturability of Campylobacter (Georgsson et al., 2006;Oh et al., 2019). Industrial rapid freezing and long-term storage of broiler meat can significantly reduce the detectable Campylobacter percentage, even to zero (Yu et al., 2021). ...
Campylobacter jejuni is one of the major foods borne pathogen that cause diarrhea in human. Consumption of undercooked poultry meats and its by-products is believed to be the main source of human campylobacteriosis. This study aims to determine the prevalence of this bacteria in LBC and IFC using conventional culture methods and conventional PCR assay, with molecular identification by sequencing of 16S rRNA. Two hundred and twenty-five samples from LBC (n=150) and IFC (n=75) were collected. Conventionally, overall, 21.3% (n = 48) were identified as C. jejuni. In LBC 30% (45/150), from this 9% and 72% identifies as C. jejuni when used enrichment and direct isolation method, respectively. Generally, the PCR confirmed 53.3% from LBC and 66.6% from IFC to be C. jejuni. All isolates were strongly resistant to Tetracycline, Ciprofloxacin, Nalidixic acid, and Oxytetracycline, while susceptible to Erythromycin and Gentamycin. Therefore, they were considered as Multi drug resistant strains. Based on the 16S rRNA sequencing, LBC and IFC were similar and genetically related to each other. Comparing with respective databases in NCBI, these isolates had the variation in their closeness with different strains from other countries isolated from different sources. Further study recommended, related to the virulence genes, physio-morphological characteristic, and whole genome sequencing of some isolated strains.