Abstract
In spite of significant improvement in technology and hygienic practices in developed countries at all stages of poultry production
foodborne diseases remain a persistent threat to human and animal health. Beside the current legislations, the main strategy to control
microbial food borne hazards should include Good Animal Husbandry Practices (GAHPs) at the farm level through sound hygienic measures, applied in poultry houses, environment and feed manufacture, as well as reducing colonization with feed additives, competitive
exclusion, treatment or vaccines. Furthermore, hygienic measure should also be considered during transport and slaughtering. In all
cases, surveillance and monitoring programmes must be adapted and followed strictly in aim to allow early intervention. In addition,
the development of antibiotic resistant bacteria will also be a continuous public health hazard.The present paper describes the main
strategy to control food borne infections in poultry, with special attention to European legislations toward safe poultry meat.
Keywords
Poultry, foodborne diseases, salmonella, campylobacter, antibiotic resistance, regulationsCo-author
Hosny El-Adawy, Friedrich-Loeffler-Institute, Institute of Bacterial Infections and Zoonoses, Jena, GermanyIntroduction
In spite of significant improvements in technology and hygienic practices at all stages of poultry production in developed countries, accompanied by advanced improvement in public sanitation, foodborne diseases remain a persistent threat to human and animal health. Food borne diseases are still big issues of major concern in those countries. In developing countries, the need to produce sufficient food to meet the requirements of population increases, accompanied by bad economic situations often overshadow the need to ensure safe food products. Regardless of this fact, safe food is a fundamental requirement for all consumers, rich or poor. Food safety is not a discovery of recent times; it is a natural basic instinct of human survival. During human evolution, several approaches were adopted to achieve safety of food. One of the most famous approaches was practiced by several kings, which would employed official and well trusted „tasters“ that served as food safety sentinels for the kings and royal family members. Food safety and quality of food are currently big issues of major concern. Many reports during recent years have shown that Salmonella and Campylobacter spp. are the most common causes of human foodborne bacterial diseases linked to poultry (Figure 1). In some areas also verotoxin producing Escherichia coli 0157:H7 (VTEC), Listeria and Yersinia have surfaced as additional foodborne pathogens causing human illness. Several other toxicogenic bacterial pathogens, such as Staphylococcus aureus, Clostridium perfringens, Clostridium botulinum and Bacillus cereus can also enter the human food chain via contaminated poultry carcasses. In addition, the development of antibiotic resistance in bacteria, which are common in both animals and humans, such as Methicillin Resistant Staphylococcus aureus (MRSA) and Extended-spectrum beta-lactamase (ESBL) bacteria, are also an emerging public health hazard.
Salmonella infection
Salmonella infections in poultry are distributed worldwide and result in severe economic losses when no effort is made to control them. In poultry, the genus Salmonella of the family Enterobacteriaceae, which include more than 2500 serovars, can roughly be classified into three categories or groups as follow: Salmonella can also be divided into three groups based on their host specificity and invasiveness (Hafez, 2013). Invasive salmonellas have the capability to “invade” the body from the intestinal lumen and thus infect organs, causing more serious disease. Group 1 contains serovars, which are highly host adapted and invasive. Examples are S. Gallinarum and S. Pullorum in poultry or S. Typhi in humans. Group 2 contains non-host adapted and invasive serovars. Salmonella in this group are of most concern regarding public health, since some of them are capable to infect humans and food producing animals and especially poultry can serve as reservoirs. There are approximately 10 – 20 serovars in this group. Currently, the most relevant serovars of them are S. Typhimurium, S. Enteritidis, S. Heidelberg, S. Hadar as well as S. Arizonae. Figure 2 shows the distribution of S. Enteritidis among food and animal sources, which are closely related.

Campylobacters
Thermophilic campylobacters are the most common bacterial cause of diarrhoea in humans worldwide. Enteric diseases caused by the thermophilic species C. jejuni, C. coli, C. lari, and C. upsaliensis range from asymptomatic infections to severe inflammatory bloody diarrhoea. The natural habitat of thermophilic Campylobacter is the intestinal tract of healthy birds and raw meat that can be contaminated during the slaughtering process (EFSA, 2015). It is estimated that as many as 90% of broilers and turkeys may harbour Campylobacter while showing little or no clinical signs of illness (Sahin et al., 2002). Hafez et al. (2001) investigate 10 turkey flocks for the presence of Campylobacter. Faecal samples were collected weekly from 1st week of age until slaughter. All monitored turkey flocks were positive for Campylobacter. Three flocks (30.0%) appeared to be infected with only one biotype. In the other 7 flocks (70.0%) two or more different biotypes were isolated during the rearing period and in slaughtered house too. In addition, Düpre et al. (2010) examined bacteriologically 1167 boot swabs taken from 161 fattening turkeys for Campylo bacter spp. Campylobacter spp. were isolated from 56 % of the investigated farms. 65.1 % of isolates were C. jejuni and 30.2% were C. coli. From 4.8% of positive samples C. jejuni as well as C. coli were isolated (Fig 3). Furthermore, Ahmed et al. (2016) examined the prevalence, genotyping and risk factors of thermophilic Campylobacter spreading in organic turkey farms in Germany. Campylobacter spp. were detected in cloacal swabs in all 5 turkey flocks with prevalence ranging from 90.0 to 100 %. 13 cloacal swabs from birds in two farms harboured mixed population of thermophilic campylobacters. In total, from 158 Campylobacter isolated from turkeys 89 (56.33 %) were identified as C. coli and 69 (43.76 %) as C. jejuni. Three Campylobacte (2 C. jejuni and 1 C. coli) were detected in drinkers of two farms and 3 C. coli were isolated from darkling beetles of one farm. No Campylobacter were isolated from main water tanks. The genotype of campylobacters isolated from wate samples or beetles were identical with those isolated from turkeys. (Table 2)

Antibiotic resistant
The development of antibiotic resistance in bacteria, which are common in both animals and humans, is an emerging public health hazard. Controlling of the above mentioned foodborne micro-organisms requires a broader understanding of how microbial pathogens enter and move through the food chain, as well as the conditions that promote or inhibit growth for each type of organism.
Multi-resistant bacteria are increasingly posing a hazard to human and animal health worldwide, impeding successful antibacterial treatment (Arias et al., 2010; EFSA, 2017). In addition, the development of novel antibiotics does not keep step with the emergence of antimicrobial resistance in bacteria (García-Rey, 2010). El- Adway et al. (2012) investigated 76 Camyplobacter jejuni isolates recovered from 67 epidemiologically unrelated meat turkey flocks in different regions of Germany in 2010 and 2011. Only one isolate was sensitive to all tested antibiotics. The numbers of isolates that were sensitive to streptomycin, erythromycin, neomycin, and amoxicillin were 69 (90.8%), 61 (80.2%), 58 (76.4%), and 44 (57.9%), respectively. The emergence of a high resistance rate and multidrug resistance to three or more classes of antimicrobial agents were observed. The resistance against sulphamethoxazole/trimethoprim, metronidazole, ciprofloxacin, naladixic acid, and tetracycline was 58 (76.3%), 58 (76.3%), 53 (69.7%), 51 (67.1%), and 42 (55.3%), respectively. Multidrug resistance to three or more classes of antimicrobial agents was found and ranged from 3.9% to 40.8%. Similar results were also found by examination of isolates collected from different free-range turkey flocks in Germany (El-Adway et al., 2015). ESBL-producing Enterobacteriaceae have emerged as pathogens in both poultry and humans (Bradford, 2001, Rawat and Nair, 2010, Moawad et al., 2018). Among multi-resistant bacteria, vancomycin-resistant enterococci (VRE) have been estimated as one of the most common bacteria causing a rise in cases of nosocomial infections in humans in the last few years (Arias et al., 2010). The prevalence of VRE in 20 turkey flocks reared in the southwest of Germany was investigated. Enterococci were tested on the presence of the vancomycin resistance genes vanA, vanB (B1/B2/B3), and vanC (C1/C2/C3). Vancomycin-resistant enterococci were detected in 15 (75%) of the 20 turkey flocks investigated. In a total of 68 isolates from birds and dust samples, enterococci bearing van-genes were detected. Of these, 12 isolates carried the vanA gene (17.6%) and 56 isolates carried the vanC1 gene (82.6%). Neither vanB (B1, B2, B3) genes nor the vanC2 or vanC3 genes could be detected (Sting et al., 2013)
Maasjost et al. (2015) investigated the antimicrobial susceptibility patterns of Enterococcus faecalis and Enterococcus faecium isolated from poultry flocks in Germany and they found that high resistance rates were identified in both Enterococcus species for lincomycin (72%–99%) and tetracycline (67%–82%). Half or more than half of Enterococcus isolates were resistant to gentamicin (54%–72%) and the macrolide antibiotics erythromycin (44%–61%) and tylosin-tartate (44%–56%). Enterococcus faecalis isolated from fattening turkeys showed the highest prevalence of antimicrobial resistance compared to other poultry production systems.
In addition, Livestock-associated methicillin-resistant Staphylococcus aureus (LAMRSA) have been isolated from a number of livestock species and persons involved in animal production. Turkey meat was also showed to be contaminated with MRSA (De Boer et al., 2009). Richter et al. (2012) investigated the prevalence of LAMRSA in fattening turkeys and people living on farms that house fattening turkeys. MRSA was detected in 18 (90%) of the 20 turkey flocks investigated. Out of examined 59 nasal swabs from persons working on the farms 22 samples were MRSpositive (37.3%). None of these persons showed clinical symptoms indicative of an MRSA infection. People with frequent access to the stables were more likely to be positive for MRSA. Similar results were about MRSA in turkeys were published by El-Adway et al. (2016).
General approaches to control food borne infections
To control the food borne organisms, information is required to understand more fully, how microbial pathogens enter and move through the food chain, and the conditions, which promote or inhibit growth for each type of organism. In general, the main strategy to control food borne infections in poultry should include monitoring, cleaning the production chain from the top, especially for vertically transmitted microorganism such as Salmonella by culling infected breeder flocks, hatching egg sanitation and limiting introduction and spread of infections at the farm level through effective hygiene measures (Hafez, 1999, 2005, Mueller-Doblies et al., 2010). An intensive and sustained rodent ontrol is essential and needs to be well planned and routinely performed and its effectiveness should be monitored. In addition, reducing bacterial colonization by using feed additives such as short chain organic acids (formic acid, propionic acid), carbohydrates (lactose, mannose, galactose, saccharose), probiotics, competitive exclusion (Schneitz, 2005, Vicente et al., 2007) or use of vaccines are further possibilities. Live and inactivated vaccines are used to control Salmonella in poultry (Gast, 2013). Generally, vaccination alone is of little value, unless it is accompanied by improvements in all aspects of management and biosecurity. In addition, further attention must be paid to the development of efficient vaccines against campylobacter infections. Since the success of any disease control programme depends on the farm and personal sanitation, it is essential to incorporate education programmes about microorganisms, modes of transmission as well as awareness of the reasons behind such control programmes by people involved in poultry production. In addition, effective education programmes must be implemented to increase public awareness of the necessary measures to be taken for protection against bacteria in food products from poultry. In spite of significant improvements in technology and hygienic practices at all stages of food production, accompanied by improvement in public sanitation, food borne infections remain a persistent threat to human and animal health. Since many humans fail to apply hygienically acceptable food handling and cooking practices, and since processing plants are not able to reduce the level of pathogenic bacteria in poultry products, every effort must be made to reduce the Salmonella contamination of live birds before despatch to processing plants. New approaches to the problem of contamination must be adopted and the discussion on the decontamination of the end product must be reevaluated carefully and without emotion. In addition, research must continue to find additional control and preventive means. As a long term contribution, poultry lines genetically resistant to some pathogens should be developed.Conclusions
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Toward food safety in the EU several legislations are into force and their aims can be summarized according to Mulder (2011) as follows:
- Safety (consumer health): by new methods to reduce the use of antibiotics /medicines; improve disease resistance; zoonosis control; traceability of animals and products
- Safety (product safety): stimulate and control hygienic processing, traceability of products and materials intended to come into contact with food
- Animal welfare: animals kept according to rules/systems
- Product quality: improved quality and composition; quality and chain control systems; traceability of animals and products.
- Environment: reducing environmental contamination, Nitrogen and Phosphorous. There is a critical look at the use of by-products of human food production. The re-use of byproducts for non-food applications (feathers) should be encouraged.
- Rural impact, economic effects and bio-diversity
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