Current and future interventions for improving poultry health and poultry food safety and security: A comprehensive review

Poultry is thriving across the globe. Chicken meat is the most preferred poultry worldwide, and its popularity is increasing. However, poultry also threatens human hygiene, especially as a fomite of infectious diseases caused by the major foodborne pathogens (Campylobacter, Salmonella, and Listeria). Preventing pathogenic bacterial biofilm is crucial in the chicken industry due to increasing food safety hazards caused by recurring contamination and the rapid degradation of meat, as well as the increased resistance of bacteria to cleaning and disinfection procedures commonly used in chicken processing plants. To address this, various innovative and promising strategies to combat bacterial resistance and biofilm are emerging to improve food safety and quality and extend shelf-life. In particular, natural compounds are attractive because of their potential antimicrobial activities. Natural compounds can also boost the immune system and improve poultry health and performance. In addition to phytochemicals, bacteriophages, nanoparticles, coatings, enzymes, and probiotics represent unique and environmentally friendly strategies in the poultry processing industry to prevent foodborne pathogens from reaching the consumer. Lactoferrin, bacteriocin, antimicrobial peptides, cell-free supernatants, and biosurfactants are also of considerable interest for their prospective application as natural antimicrobials for improving the safety of raw poultry meat. This review aims to describe the feasibility of these proposed strategies and provide an overview of recent published evidences to control microorganisms in the poultry industry, considering the human health, food safety, and economic aspects of poultry production.     

The European Union control strategy for Campylobacter spp. in the broiler meat chain

Campylobacter is the most common cause of bacterial gastroenteritis worldwide and the most frequently reported foodborne pathogen in the European Union (EU). While campylobacteriosis is generally self-limiting, some patients could develop severe sequelae. The predominant source of infection is poultry. This review addresses the most relevant factors influencing the prevalence and contamination level of Campylobacter spp. in the poultry chain continuum. The emphasis was put on the novel control strategy for Campylobacter that is based on evidence-based risk assessment and the introduction of process hygiene criterion intended for monitoring the prevalence and counts of Campylobacter spp. on broiler carcasses at slaughter level. The reduction of Campylobacter spp. in the poultry meat chain in the EU can only be achieved with an integrated meat safety assurance approach. This includes primary interventions at the level of the poultry farm, implementation of effective control measures at slaughterhouses, and fostering awareness campaigns aimed at consumers.     

PREVALENCE OF THERMOPHILIC CAMPYLOBACTER SPP. IN RETAIL CHICKEN MEAT IN ANKARA

From May to August 2004, 127 samples of chicken meat for sale on the retail market in Ankara were analyzed for the prevalence of thermophilic Campylobacter spp. Campylobacter spp. were isolated from 83.4% of the samples analyzed. Campylobacter jejuni was found in 74.8% of all samples. A total of 364 thermophilic Campylobacter strains were isolated and the species distribution among these strains was 70.1% C. jejuni, 21.1% Campylobacter coli and 8.6% Campylobacter lari. The results obtained from the study indicate that hygienic and technical compliance is needed in all stages of poultry processing to reduce contamination and to prevent public health hazard. An integrated HACCP plan must be applied from the farm to the table for the prevention of C. jejuni infections.     

Campylobacter: An overview of cases,occurrence in food,contamination sources,and antimicrobial resistance in Brazil

Campylobacter has been the most prevalent microorganism associated with foodborne gastroenteritis in developed countries in the last years. The consumption of contaminated chicken meat is the main source of campylobacteriosis in humans. However, in developing countries, Campylobacter has not been recognized as a food safety problem. Here, we provide an overview of studies focusing on occurrence of Campylobacter in Brazilian chicken processing chain, epidemiological data, contamination sources, antimicrobial resistance and fields where more studies are needed. Over the past 15 years, only five foodborne outbreaks involving 37 cases of campylobacteriosis were reported in Brazil. However, the occurrence of Campylobacter in samples of carcasses and chicken products was about 32.7%, and the microbial load ranged from <0.30 to 5.15 log10 CFU. This pathogen was also found in feces, caecum, intestine and cloaca of chicken (50.9%), chicken litter (65.4%), and water (13.7%). The most prevalent species identified in the studies were C. jejuni (80%) and C. coli (19.6%). In addition, high antimicrobial resistance rates were noted for cephalosporins (98.5–100%), quinolones (84.5%), and fluoroquinolones (77.6–82.8%). This review demonstrates that Campylobacter seems to be an important pathogen in the chicken processing chain and, consequently, for public health in Brazil.     

Comprehensive Review of Campylobacter and Poultry Processing

Campylobacter has been recognized as a leading bacterial cause of human gastroenteritis in the United States, with 40000 documented cases annually. Epidemiological data suggest that contaminated products of animal origin, especially poultry, contribute significantly to campylobacteriosis. Thus, reduction of contamination of raw poultry would have a large impact in reducing incidence of illness. Contamination occurs both on the farm and in poultry slaughter plants. Routine procedures on the farm such as feed withdrawal, poultry handling, and transportation practices have a documented effect on Campylobacter levels at the processing plant. At the plant, defeathering, evisceration, and carcass chillers have been documented to cross‐contaminate poultry carcasses. Carcass washings and the application of processing aids have been shown to reduce populations of Campylobacter in the carcasses by log₁₀ 0.5 log₁₀ 1.5; however, populations of Campylobacter have been shown to enter a poultry processing plant at levels between log₁₀ 5 colony‐forming units (CFU)/mL and log₁₀ 8 CFU/mL of carcass rinse. The purpose of this article is to review Campylobacter, the infection that it causes, its association with poultry, contamination sources during processing, and intervention methods.     

Nanotechnology in the food sector and potential applications for the poultry industry

BackgroundSalmonellosis and campylobacteriosis are among the most frequently reported foodborne diseases worldwide. Commercial chicken meat has been identified as one of the most important food vehicles for Salmonella and Campylobacter infection. Increased poultry consumption has forced producers to explore methods for increasing their production output, while maintaining the affordability and safety of their products. While the forecast benefits of nanotechnology have yet to be fully realised, it has potential application at many points along the food production chain and offers the opportunity to meet these challenges.Scope and approachThe commercial poultry processing environment plays a significant role in reducing foodborne pathogens and spoilage organisms from poultry products prior to being supplied to consumers. This review discusses the potential opportunities and challenges for adopting nano-enabled technologies in the poultry industry, with respect to applications in microbiological food safety and quality assurance in the processing plant.Key findings and conclusionsSeveral possibilities exist to exploit the benefits of nanotechnologies in the poultry processing plant to enhance the microbiological safety and quality of products. Those applications include the adoption of nano-enabled disinfectants, surface biocides, protective clothing, air and water filters, packaging, biosensors and rapid detection methods for contaminants, and technologies that assure the authenticity and traceability of products. Although the fate and potential toxicity of nanomaterials are not fully understood at this time and scientific risk assessments are required, it is evident that there have been significant advances in the application of novel nanotechnologies in the food industry.     

Effect of processing on the microbiological quality and safety of chicken carcasses at slaughterhouse

Microbiological contamination of chicken meat depends on the conditions under which the animals are reared, slaughtered and processed. The aim of this study was to determine the influence of farm origin and processing stages at slaughterhouse on the microbial safety and quality of chicken. Samples of chicken carcasses from three different farms were taken from a slaughterhouse. Mesophiles, Escherichia coli, coagulase positive Staphylococcci counts, presence of Listeria monocytogenes,Campylobacter and Salmonella were determined at five sampling points: after defeathering, after evisceration, after washing, after chilling and after cutting. Chilling reduced log numbers of mesophiles, coagulase positive Staphylococci and E. coli by 0.85, 1.52 and 2.2 log units, respectively. Salmonella was not detected after chilling. High prevalence of Campylobacter spp was observed at all the stages ranging between 84% and 100%. L. monocytogenes was not detected in chicken carcasses after defeathering. However, it was detected after evisceration and after washing and chilling. The most critical stage for L. monocytogenes contamination was the portioning operation, the prevalence in breast and legs being 88% and 84%, respectively.     

Contamination of meat with Campylobacter jejuni in Saitama, Japan.

To determine the source of food contamination with Campylobacter jejuni, we investigated retail meat, a chicken processing plant and a broiler farm. C. jejuni was found in domestic retailed poultry (45.8%) and imported poultry (3.7%), but not in beef or pork. In the poultry processing plant, there is significant contamination with C. jejuni in chicken carcasses, equipment and workers' hands. This contamination increases during the defeathering and evisceration processes. RAPD analysis shows that contamination with C. jejuni is of intestinal origin. In a broiler farm, C. jejuni was first isolated from a faecal sample of broiler chicken after the 20th day of age. Two weeks later, all birds in this farm became C. jejuni positive. RAPD analysis indicated that C. jejuni spread rapidly from one broiler flock to the other flocks on the farm.     

INCIDENCE OF LISTERIA MONOCYTOGENES IN RETAIL CHICKEN MEAT AND ESTABLISHING RELATIONSHIP WITH SOME BACTERIA BY LOGISTIC REGRESSION

ABSTRACT

The objective of this study was to determine the contamination of retail poultry meat in Erzurum (Turkey) by Listeria monocytogenes and to evaluate its relationship with indicator bacteria using logistic regression. The incidence of L. monocytogenes was 32.76%, found in 38 of 116 samples. The application of logistic regression showed Enterobacteriaceae, Pseudomonas spp. and Brochothrix thermosphacta populations have positive, and yeast and mold population have negative relationship with L. monocytogenes presence. The results of this study demonstrate that there is a serious risk in raw poultry meat for consumer health in Erzurum, because of the high incidence of L. monocytogenes in the samples of the present study. Hygienic conditions described in HACCP program should still be enforced in order to minimize L. monocytogenes in poultry meat during the processing.

PRACTICAL APPLICATIONS

Listeria monocytogenes and other Listeria species have been isolated from many different types of raw and processed food, but the main sources and routes of contamination are still not fully understood. There is a need for more knowledge, and data are needed for risk assessment and for improved preventive measures. In order to prevent and control contamination of the environment and food products with this pathogen, it is important to detect the most important sources of contamination and to understand the mechanisms of growth, including relationships with other bacteria. The main concern with raw poultry meat is the incidence of L. monocytogenes in raw chicken because of cross‐contamination with other foods in the home and the possibility of the microorganism surviving in processed chicken. Application of logistic regression was used to identify the main hazards associated with the presence of microorganisms, as well as for applications in predictive food microbiology, modeling binomially distributed data that involve the use of probability models, where the response variable is a “presence/absence” observation of whether or not growth will occur.     

High occurrence rates of enrofloxacin and ciprofloxacin residues in retail poultry meat revealed by an ultra-sensitive mass-spectrometric method,and antimicrobial resistance to fluoroquinolones in Campylobacter spp

An ultra-sensitive mass spectrometric confirmation and quantification method for the determination of selected fluoroquinolones—enrofloxacin and its main metabolite ciprofloxacin—was developed and validated in poultry meat samples. The achieved limits of quantification were 1 ng kg^?1 for enrofloxacin and 10 ng kg^?1 for ciprofloxacin. The analysis of 40 retail poultry samples originating from Estonia, Latvia, Lithuania, Poland and France revealed that 93% of samples contained residues of enrofloxacin in the range from 3.3 to 1126 ng kg^?1. Previous studies have shown high levels of antimicrobial resistance to fluoroquinolones, particularly in Campylobacter spp. and various faecal indicators isolated from broiler meat. Consequently, the revealed widespread usage of fluoroquinolones in the poultry industry may result in the further emergence of antimicrobial resistance of Campylobacter in the food chain.     

Processing practices contributing to Campylobacter contamination in Belgian chicken meat preparations

The aim of this study was to obtain insight into processing practices in the poultry sector contributing to the variability in Campylobacter contamination in Belgian chicken meat preparations. This was achieved by company profiling of eleven food business operators, in order to evaluate variation of processing management, in addition to statistical modelling of microbiological testing results for Campylobacter spp. contamination in 656 end product samples. Almost half (48%) of chicken meat preparation samples were positive for Campylobacter spp. Results revealed a statistically significant variation in Campylobacter contamination between 11 chicken meat producers across Belgium at both quantitative and qualitative detection levels. All producers provided Campylobacter-positive samples, but prevalence ranged from 9% up to 85% at single producer level. The presence or addition of skin during production of chicken meat preparations resulted in almost 2.2-fold increase in the probability of a sample being positive for Campylobacter, while chicken meat preparations made from frozen meat, or partly containing pre-frozen meat, had a significant (Odds Ratio=0.41; CI 95% 0.18:0.98) lower probability of being positive for Campylobacter. However, the quantitative results indicated that the positive freezing effect on Campylobacter count was compromised by the presence and/or adding of skin.     

Impact of human Campylobacter infections in Southeast Asia: The contribution of the poultry sector

Campylobacter is globally recognized as a major cause of foodborne infection in humans, whilst the development of antimicrobial resistance and the possibility of repelling therapy increase the threat to public health. Poultry is the most frequent source of Campylobacter infection in humans, and southeast Asia is a global leader in poultry production, consumption, and exports. Though three of the world's top 20 most populated countries are located in southeast Asia, the true burden of Campylobacter infection in the region has not been fully elucidated. Based on published data, Campylobacter has been reported in humans, animals, and food commodities in the region. To our knowledge, this study is the first to review the status of human Campylobacter infection in southeast Asia and to discuss future perspectives. Gaining insight into the true burden of the infection and prevalence levels of Campylobacter spp. in the southeast Asian region is essential to ensuring global and regional food safety through facilitating improvements in surveillance systems, food safety regulations, and mitigation strategies.     

Biosecurity Measures to Control Salmonella and Other Infectious Agents in Pig Farms: A Review

Salmonellosis is the 2nd most common cause of human bacterial food poisoning and can be acquired from meat or eggs, either via direct consumption or cross‐contamination in the kitchen. The European Commission has set the criteria to control Salmonella infections within the poultry sector and it is proposed that the swine sector should follow. Pork is considered, after eggs, the major source of infection in humans in the EU, with Salmonella typhimurium, including monophasic strains, being frequently implicated. Good control measures at the farm level are likely to correspond with lower prevalence of Salmonella infection and, subsequently, a reduction of cross‐contamination of carcasses processed at the slaughterhouse and a reduction in human salmonellosis. This review focuses on biosecurity measures in pig farms that can help to control important pig diseases at the same time as reducing the within‐herd prevalence of Salmonella. This information is likely to provide an economic incentive for farmers to apply improved general standards of farm biosecurity and hygiene management that would have a positive impact in food safety.     

Salmonella and Campylobacter biofilm formation: a comparative assessment from farm to fork

It takes several steps to bring food from the farm to the fork (dining table), and contamination with food‐borne pathogens can occur at any point in the process. Campylobacter spp. and Salmonella spp. are the main microorganisms responsible for foodborne disease in the EU. These two pathogens are able to persist throughout the food supply chain thanks to their ability to form biofilms. Owing to the high prevalence of Salmonella and especially of Campylobacter in the food supply chain and the huge efforts of food authorities to reduce these levels, it is of great importance to fully understand their mechanisms of persistence. Diverse studies have evaluated the biofilm‐forming capacity of foodborne pathogens isolated at different steps of food production. Nonetheless, the principal obstacle of these studies is to reproduce the real conditions that microorganisms encounter in the food supply chain. While there are a wide number of Salmonella biofilm studies, information on Campylobacter biofilms is still limited. A comparison between the two microorganisms could help to develop new research in the field of Campylobacter biofilms. Therefore, this review evaluates relevant work in the field of Salmonella and Campylobacter biofilms and the applicability of the data obtained from these studies to real working conditions. © 2018 Society of Chemical Industry     

The risk of transfer of foodborne bacterial hazards in Turkey through the consumption of meat; risk ranking of muscle foods with the potential to transfer Campylobacter spp.

This paper presents a simple approach to semi-quantitatively estimating the risk for human foodborne campylobacteriosis in Turkey, with a focus on typical/traditional meat and meat dishes. The following factors are considered: prevalence/concentration of the pathogen in raw meat according to species, changes in the pathogen’s titre as a result of heat treatment and cross-contamination, serving frequency and size, and demographic data. Regional differences as well as differences between social groups are considered in particular. The biological hazard “Campylobacter” is characterized as associated with conditions prevailing in the meat chain and this information is linked to food consumption and other data thus allowing an estimate of consumers’ exposure to Campylobacter via typical Turkish meat dishes. The latter are ranked on the basis of the presence of meat components and the associated risks.     

Control of Salmonella enterica Typhimurium in chicken breast meat by irradiation combined with modified atmosphere packaging

Salmonella is one of the leading causes of human foodborne illnesses originating from meat and poultry products. Cross-contamination of Salmonella from raw to cooked products continues to be problematic in the food industry. Therefore, new intervention strategies are needed for meat and poultry products. Vacuum or modified atmosphere packaging (MAP) are common packaging techniques used to extend the shelf life of meat products. Irradiation has been well established as an antibacterial treatment to reduce pathogens on meat and poultry. Combining irradiation with high-CO(2)+CO MAP was investigated in this study for improving the control of Salmonella enterica Typhimurium on chicken breast meat. The radiation sensitivities (D10-values) of this pathogen in chicken breast meat were found to be similar in vacuum and in high-CO(2)+CO MAP (0.55 ± 0.03 kGy and 0.54 ± 0.03 kGy, respectively). Irradiation at 1.5 kGy reduced the Salmonella population by an average of 3 log. Some Salmonella cells survived in both vacuum and high-CO(2) + CO MAP through 6 weeks of refrigerated storage following irradiation. This pathogen also grew in both vacuum and MAP when the product was held at 25°C. This study demonstrated that irradiation is an effective means of reducing Salmonella on meat or poultry, but packaging in either vacuum or MAP had little impact during subsequent refrigerated storage.     

Advances in enteropathogen control throughout the meat chicken production chain

Enteropathogens, namely Salmonella and Campylobacter, are a concern in global public health and have been attributed in numerous risk assessments to a poultry source. During the last decade, a large body of research addressing this problem has been published. The literature reviewed contains review articles on certain aspects of poultry production chain; however, in the past decade there has not been a review on the entire chain—farm to fork—of poultry production. For this review, a pool of 514 articles were selected for relevance via a systematic screening process (from >7500 original search articles). These studies identified a diversity of management and intervention strategies for the elimination or reduction of enteropathogens in poultry production. Many studies were laboratory or limited field trials with implementation in true commercial operations being problematic. Entities considering using commercial antienteropathogen products and interventions are advised to perform an internal validation and fit-for-purpose trial as Salmonella and Campylobacter serovars and biovars may have regional diversity. Future research should focus on nonchemical application within the processing plant and how a combination of synergisticinterventions through the production chain may contribute to reducing the overall carcass burden of enteropathogens, coupled with increased consumer education on safe handling and cooking of poultry.     

Listeria monocytogenes in retail establishments: Contamination routes and control strategies

In the past two decades, serious outbreaks of foodborne disease were caused by Listeria monocytogenes, a pathogen frequently found in delicatessens at retail. Although the prevalence of listeriosis is not high, the severity of disease is significant, with high hospitalization and mortality rates. Potential sources of L. monocytogenes and food contamination routes in retail and food service operations include incoming raw materials, food products, food handlers, customers, vendors, and environmental sources. Risk mitigation strategies for L. monocytogenes should be based on integrated control along the food chain continuum, from farm to retail establishment.     

Ciprofloxacin-resistant Campylobacter persists in raw retail chicken after the fluoroquinolone ban

In 2005, the FDA withdrew approval for the use of fluoroquinolones in live poultry production. To assess any changes in countable numbers of ciprofloxacin-resistant Campylobacter before and after the fluoroquinolone withdrawal, retail whole raw chicken carcasses (RTCC) purchased in Northwest Arkansas from 2004 to 2006 were sampled for this purpose. Using a previously published direct-plating method developed in our laboratory, we quantified trends of Campylobacter and ciprofloxacin-resistant Campylobacter loads by direct plating whole chicken carcass rinses on Campylobacter agar (CA) or Campylobacter agar containing 8.6 µg/ml ciprofloxacin (CCA). Countable populations of Campylobacter were recovered from 74, 96, and 63% of carcasses sampled in 2004, 2005, and 2006 respectively. The percentages of carcasses with minimum detectable levels of ciprofloxacin-resistant Campylobacter were 20, 42 and 33%, sampled in 2004, 2005 and 2006, respectively. Our 3 year analysis in one geographical area indicated a persistence of Campylobacter and ciprofloxacin-resistant Campylobacter on retail raw chicken carcasses despite the cessation of fluoroquinolone use in poultry production.     

Application of Ozonated Dry Ice (ALIGAL™ Blue Ice) For Packaging and Transport in the Food Industry

Abstract: Dry ice is used by meat and poultry processors for temperature reduction during processing and for temperature maintenance during transportation. ALIGAL? Blue Ice (ABI), which combines the antimicrobial effect of ozone (O₃) along with the high cooling capacity of dry ice, was investigated for its effect on bacterial reduction in air, in liquid, and on food and glass surfaces. Through proprietary means, O₃ was introduced to produce dry ice pellets to a concentration of 20 parts per million (ppm) by total weight. The ABI sublimation rate was similar to that of dry ice pellets under identical conditions, and ABI was able to hold the O₃ concentration throughout the normal shelf life of the product. Challenge studies were performed using different microorganisms, including E. coli, Campylobacter jejuni, Salmonella, and Listeria, that are critical to food safety. ABI showed significant (P < 0.05) microbial reduction during bioaerosol contamination (up to 5‐log reduction of E. coli and Listeria), on chicken breast (approximately 1.3‐log reduction of C. jejuni), on contact surfaces (approximately 3.9 log reduction of C. jejuni), and in liquid (2‐log reduction of C. jejuni). Considering the stability of O₃, ease of use, and antimicrobial efficacy against foodborne pathogens, our results suggest that ABI is a better alternative, especially for meat and poultry processors, as compared to dry ice. Further, ABI can potentially serve as an additional processing hurdle to guard against pathogens during processing, transportation, distribution, and/or storage. Practical Application: A new product known as ALIGAL? Blue Ice (ABI) incorporates ozone in dry ice pellets, combining the high cooling capacity of dry ice pellets and the antimicrobial efficacy of ozone. This study evaluated the antimicrobial efficacy of ABI compared to dry ice under potential commercial processing conditions, specifically examining the impact on airborne, surface, moisture, and food contamination. Treatment with ABI resulted in higher reductions of bacteria with airborne contamination, on chicken breast, on surfaces, and in liquid compared to dry ice. Thus, ABI can serve as an additional processing hurdle to guard against pathogens during food processing and storage.