Avian Pathogenic Escherichia coli in Broiler Breeders: History
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Contributor:
Jiddu Joseph
,
Li Zhang
,
Pratima Adhikari
,
Jeffrey D. Evans
,
Reshma Ramachandran

Poultry meat is one of the major animal protein sources necessary to meet the global protein demand. Sustainability in broiler production is the key to achieving its continuous supply, and broiler breeders play a critical role in maintaining this sustainability by providing good quality chicks. Colibacillosis, the disease caused by avian pathogenic Escherichia coli (APEC), causes severe economic losses to the poultry industry globally. Moreover, APEC causes an additional burden among broiler breeders, such as a decrease in egg production and mortality among these birds. There is vertical transmission of APEC to the broiler chicks through eggs, resulting in increased first-week mortality and subsequent horizontal transmission at the hatchery. 

  • avian pathogenic E. coli
  • broiler breeders
  • colibacillosis

1. Introduction

The United States is a major contributor to the world’s broiler supply. It has the highest broiler production with around 20 million metric tons of chicken meat production annually [1]. The value of broiler production from the U.S. in 2022 was $50.4 billion, 60% higher than in 2021 [2]. As the demand for broiler meat increases, there is a need to improve production [1]. However, with the wide acceptance of the No Antibiotic Ever (NAE) system across the U.S., disease control among the poultry population has become a major challenge. Meat- and poultry-related illnesses are causing an economic loss of around $20.3 billion annually. Therefore, it is critical to develop effective control measures against bacterial diseases, such as colibacillosis, salmonellosis, and campylobacteriosis, which are causing a major loss to the industry [3]. Additionally, maintaining a continuous supply of broilers in the market requires an excellent strategy for managing broilers and broiler breeders [4].
Broiler breeders are the parents of broilers and play a critical role in developing a healthy broiler flock [5]. Decreased fertility, hatchability, and egg production are some of the major challenges faced by the broiler breeder industry globally [6]. These challenges could be due to a combination of factors, such as improper management, stress, inadequate nutrition, immunosuppression, and exposure to disease agents. Identifying these factors and finding timely solutions are the key strategies for producing healthy broilers for the market [7].
Escherichia coli (E. coli) is a bacterium commonly found in the normal intestinal flora of humans, other mammals, animals, and birds. However, some of the strains can act as major pathogens causing severe disease and high death tolls [8]. Extraintestinal pathogenic E. coli (ExPEC) causes the disease called colibacillosis in animals and birds. ExPEC has divisions, such as uropathogenic E. coli, newborn meningitic E. coli, septicemia-associated E. coli, and avian pathogenic E. coli (APEC). The APEC causes disease specifically in birds, including chickens, ducks, and turkeys [9]. Avian colibacillosis is manifested in diverse ways, such as peritonitis, salpingitis, yolk sac infection, and cellulitis, which are localized infections while colisepticemia, pericarditis, airsacculitis, coligranuloma, and arthritis are systemic infections leading to high morbidity and mortality [10][11]. This is one of the most commonly occurring and economically devastating bacterial diseases among poultry worldwide [11].
The primary routes of APEC entry include fecal–oral, respiratory, and vaginal origin (ascending route) through the cloaca [9]. The fecal–oral and respiratory-type colibacillosis has been studied the most [12]. However, the ascending route through the cloaca is also very important as it results in outbreaks characterized by salpingitis–peritonitis syndrome in broiler breeders and causes huge economic losses due to decreased egg production and quality, increased mortality, and the cost associated with treatment, culling of birds, and disposal of carcasses. This is further exacerbated by the vertical transmission of APEC from breeders to progenies leading to yolk sac infection, omphalitis, and increased first-week mortality among broiler chicks [13][14]. Moreover, infected chicks, dead embryos, and contaminated eggshells act as potential sources of infection in the hatchery leading to horizontal transmission among uninfected chicks and contamination of equipment [15][16]. Additionally, vertical transmission facilitates the transfer of antibiotic-resistant APEC strains down the production cycle, making their control extremely difficult [17][18].

2. APEC in Broiler Breeders

2.1. Broiler Breeder Hens

Among several manifestations of colibacillosis in chickens, salpingitis–peritonitis syndrome has received relatively little attention [19]. The hens get the infection mainly through three routes: (1) ascending infection through the cloaca or translocation of bacteria from the (2) respiratory tract or (3) intestinal lumen. Among these, the most important routes of infection are the respiratory and fecal–oral routes; however, the ascending infection through the cloaca is also critical for this infection [19][20]. Furthermore, among multiple factors causing mortality in broiler breeder hens, the highest mortality was due to salpingitis–peritonitis syndrome, and E. coli was one of the major pathogens causing this systemic infection in broiler breeders [15]. Initially, the infection in the reproductive tract will be asymptomatic and later proceed to severe septicemia and death. Peritonitis is usually found in acute cases mostly as a complication of oviduct infection [21]. Giovanardi et al. [22] reported vertical transmission of APEC from broiler breeders to their progeny in an integrated poultry production chain and suggested chronic salpingitis in hens as a potential risk factor for transmitting APEC through eggs to progenies. Studies show that APEC infection and first-week mortality among chicks from aged broiler breeders (>50 weeks) are higher than from young (<30 weeks) birds, and the plausible reasons are a decrease in the eggshell quality with age and immunosuppression in birds after the peak production period [16][23]. However, there is only limited information on the salpingitis–peritonitis syndrome in broiler breeders; hence, further studies focused on the pathogenesis of APEC isolates causing salpingitis, as well as factors promoting salpingitis in broiler breeders.

2.2. Broiler Breeder Males

Male fertility in broiler breeders is another important aspect of production. Previous reports show that intestinal bacterial populations can invade the male reproductive system as the cloaca is the common opening for reproductive and digestive systems, thus, affecting sperm motility and fertility [24]. Bacterial orchitis may occur due to E. coli infection of the broiler breeder’s male reproductive system. E. coli mainly invade through the hematogenous route due to septicemia and affect the tubular architecture [25]. The presence of pathogenic bacteria in the semen has been previously reported [26]. Furthermore, the motility of broiler breeder semen samples in the presence of pathogenic bacteria such as E. coli, Salmonella, Campylobacter, Clostridium, Bifidobacterium, and Lactobacillus has been analyzed, and the presence of E. coli in semen affected its motility as well as decreased the pH of the semen sample [27]. Additionally, other reports also validate that the presence of E. coli in the semen could affect sperm motility [28]. This implies that fertility could be affected by APEC infection in males due to low sperm motility and thus, lead to decreased chick production. In the broiler breeder industry, even though a large number of females are fertilized by a single male (1 male:10 females), there is no monitoring of the semen quality of roosters. Furthermore, when the male reproductive tract gets infected, there is a high chance of transmitting E. coli to hens through copulation [28][29][30].

2.3. Virulence Characteristics

Regular characterization of bacterial populations based on their virulence properties is necessary to get updated knowledge about the virulence patterns and to develop effective control measures. Multiple virulence-associated genes (VAGs) that enable E. coli to attach, invade, colonize, replicate, and damage the host cells, as well as evade the host immune response, have been studied. However, there are only limited studies on the properties of APEC isolates specifically collected from broiler breeders. The study on the virulence-associated genes of 28 clinical isolates from broiler breeders in the U.S. using conventional PCR reported iroN (iron acquisition), iss and ompT (protectins), and hlyF (toxin production) as the most prevalent genes (78.6%) among the isolates [31]. Studies from Thailand and Australia with 200 clinical samples from broilers and broiler breeders using pentaplex PCR showed a high prevalence (100%) for ompT and hlyF [32]. About 256 broiler breeder APEC non-clinical isolates from Korea were examined using conventional PCR and showed ompT as the highly prevalent virulence gene (26%) [33]. Moreover, clinical isolates from broiler breeders in Canada also showed another pattern of prevalent genes among the isolates using conventional PCR (cvaC-etsB-fyuA-ireA-iroN-iss-iutA-ompT-sitA) with sitA (iron acquisition) as the most prevalent gene (92.75%) [34].
Phylogenetic classification of broiler breeder isolates shows the prevalence of B2 phylogroup (49%), and the identified prevalence agrees with the general pattern in poultry which followed the old Clermont classification which included phylogroups A, B1, B2, and D [35]. However, according to the new Clermont classification which includes phylogroups A, B1, B, C, D, E, F, and clade 1, B2 is still a major phylogroup but other phylogroups have shown some shifts in some categories such as A to C and D to E or F as mentioned before, which should be considered in future studies while classifying broiler breeder APEC isolates [36][37][38].
Phenotypic virulence characterization of isolates is equally important as genotypic virulence characterization. Understanding the phenotypic variation relative to genetic differences is critical to understanding bacterial characteristics and helps to identify specific factors responsible for bacterial virulence and pathogenesis [39]. Day-old chick challenge and embryo lethality assays are some convenient methods to phenotypically characterize the isolates based on their virulence potential [40][41]. 
In vitro cell culture studies are also helpful to characterize the isolates based on their adherence and invasive properties to eukaryotic cells. As these in vitro studies can mimic the host–pathogen interaction, the adhesion and invasion potential can be used to estimate its relationship with genotypic and phenotypic virulence factors of the bacterial isolates. Moreover, the above-mentioned data can be used to estimate the specific factors responsible for virulence based on a whole genome aspect and to develop effective control methods [42]. Even though the genotypic and phenotypic data provide information about the characteristics of broiler breeder APEC isolates, the vast genetic diversity is a challenge for its control. 

2.4. Antibiotic Resistance Characteristics

One of the major concerns regarding APEC colonization in broiler breeders is the vertical transmission of antibiotic-resistant genes down the poultry production pyramid [43]. Additionally, the possibility of the zoonotic potential of APEC, including the transfer of antibiotic-resistant genes to humans, has been suggested by Johnson et al. [44]. Therefore, it has been recommended that antibiotics utilized in animal production solely be used for the therapeutic treatment of disease and should utilize antibiotics less commonly applied to human medicine. As the antimicrobial resistance pattern among poultry is continuously evolving, it is important to closely monitor the resistance pattern of isolates from breeders [45].

2.5. Metal Resistance Characteristics

Another important challenge besides antibiotic resistance among APEC isolates is the resistance towards heavy metals, which were used as growth promoters in the past, and quaternary ammonium compounds, which are part of disinfectants used for cleaning poultry facilities [46]. Broiler and broiler breeder APEC isolates were reported to show a high prevalence of the arsC gene which codes for arsenic resistance. The use of arsenic-containing feed additive, Roxarsone, in poultry might be a possible reason for this increased prevalence [31][47]. Furthermore, the presence of more than 90% silver resistance among broiler breeder APEC isolates from the U.S. was alarming because silver compounds were used as feed additives [31].

3. APEC Transmission from Broiler Breeders

3.1. Vertical Transmission

Transmission of bacteria from broiler breeders to their progeny, possibly due to colonization in the reproductive tract or due to penetration of eggshell, is described as vertical transmission. It is a major concern for APEC transmission and spread [13]. However, only recently the high degree of vertical transfer of APEC from breeders to broiler chicks has been identified. Giovanardi et al. [48] identified that the strains of E. coli isolated from broiler chicks were similar to those found from their parents. They identified the presence of O78 (36.3%) and O136 (26%) serogroups among both parent flocks and chicks along with some virulence-associated genes such as fim/tsh/iuc that helped to define pathotypes.
The vertical transmission is further confirmed by various other studies that reported the transmission of antibiotic resistance genes of APEC from broiler parents to chicks. The strain obtained from the chicks that died in the first week was also recovered from the broiler parents by following fluoroquinolone-resistant E. coli that was vertically transmitted down the integrated broiler production chain [49]. Furthermore, the extended-spectrum beta-lactamase (ESBL) and plasmid ampicillinase C (pAmpC) resistance were also found to be vertically transmitted from broiler breeders to broilers [18][43][50]. Another relevant finding supporting the vertical transmission potential is the recovery of tetracycline-resistant E. coli from the ovary and egg contents of broiler breeders [51]. 
One of the critical factors affecting vertical transmission is the age of the breeder flock. Monroy et al. [23] reported that the age of broiler breeders affects the colonizing ability of APEC in the host tissue by studying the in vitro adherence ability of E. coli in the ciliated oviduct epithelium. Interestingly, the adherence was more towards the oviduct from aged breeders (50 weeks old) than from young (12 weeks old) breeders. This difference in the adherence pattern might be due to differences in the oviduct epithelium cell types in young and aged hens, which in turn might be the effect of hormones and egg production status. Thus, ciliated epithelium found in egg-laying hens oviducts promotes the colonization of E. coli [40]. 

3.2. Horizontal Transmission

In horizontal transmission, the bacteria from the infected birds in a flock get transmitted to the non-infected ones through contaminated body fluids, aerosols, feathers, and feces. Broiler breeders can transmit E. coli among themselves and vertically to their progenies, and the vertically transmitted APEC can increase the first-week mortality among the chicks because of the horizontal transmission happening at the hatchery and farm [45][49]. In the hatchery, the eggs infected from the hens’ oviduct could potentially transmit APEC to other embryos during incubation, as well as in the hatching basket, non-infected chicks can come in contact with infected ones via feathers and feces. All these sources can act as potent sources of APEC infection [52][53]. APEC is a highly transmissible pathogen that can easily spread between chicks and affect the chick’s quality [54].
Another important aspect that facilitates the spread of E. coli at farms is vectors. Studies showed that APEC isolates were able to colonize vectors such as houseflies, wild birds, and even pigeons [54][55][56]. Of interest, beetles (Alphitobius diaperinus) were also found to be important in transmitting E. coli. Another parasite shown to be involved in the transmission is Tetratrichomonas gallinarum (Trichomonad spp.) [57][58]. Thus, focusing on controlling the vectors is essential to ensure biosecurity and prevent horizontal transmission [57]. 

3.3. First-Week Mortality among Chicks

The first week of growth is crucial for a chick because it determines flock production ability, uniformity of the flock, and the age at processing [14]. APEC infections in chicks are characterized by acute and subacute septicemia. Death may occur due to acute septicemia resulting from infections in the yolk sac and respiratory system, while pericarditis, perihepatitis, and airsacculitis may develop as a result of sub-acute septicemia [14]. Chick quality can be assessed by looking into the first-week mortality pattern, which should be around 0 to 1% [59], and as per Aviagen standards, the first-week mortality should not exceed 0.7% [60]. Moreover, the European Union standards suggest that the first-week mortality is indicative of the welfare of the birds [61]. If mortality is more than 1%, it would affect the entire production system, necessitating its prevention. Even though several factors affect first-week mortality, such as breeder age, egg weight, genetics, hatchery conditions, feed quality, and house environment [62], the primary factor (50%) is infections due to various pathogens, and E. coli is a major pathogen in this group [63].
The bacteria entering through the yolk sac infect the chicks that retain the yolk sac for a long period of time and cause the infection to peak 24–48 h after hatching, and at the end of about 2 weeks, the mortality may increase up to 10%–20%. Data show that, among the surviving population of chicks, about 5% may have stunted growth, while the development of the other birds will be normal [7][64]. Another important source of infection is the feed. Reports suggest that E. coli contaminates animal feed because of the poor-quality ingredients or the poor storage facilities [65]. Water is another important source of infection as E. coli is the indicator organism for fecal contamination [66]. Alarmingly, scientists have identified about 13% prevalence of E. coli in the water tanks of farms. It can act as a potential source of infection and can be avoided by strict biosecurity, proper disinfection, and management [65].

4. Prevention and Control of APEC in Breeders

4.1. Biosecurity and Management

Biosecurity is the primary factor pertaining to the prevention and control of APEC in broiler breeders. There should be more focus on the parent stock by periodic sampling and monitoring because from the breeders the isolates that cause the disease and anti-microbial resistance are transferred vertically. In addition, there are many primary bacterial and viral infections that compromise the immune barrier of birds and promote APEC infection as a secondary pathogen. These primary disease agents should be controlled by periodic monitoring and surveillance [67]. Furthermore, the spike males introduced to the flock must be from the same source and tested for important disease conditions, including APEC infections [68]. When the flock ages, the bird’s immune system gets compromised, eggshell thickness decreases, and the chick’s quality gets affected. Proper management of the flock, including culling and disinfecting the eggs, is critical in breeder flocks that are aged [15].
Care should be taken while transporting the chicks from one farm to another to prevent the transmission of bacteria by implementing good sanitation and biosecurity programs [16]. Importantly, controlling bacterial contamination in areas such as feed mills and packaging areas and prioritizing the biosecurity measures are critical in APEC control. Above that, culling weak chicks during the first week will reduce the loss due to treatment, and mortality is affected. It also helps to control the horizontal transmission [16]. 

4.2. Genetics

Genetics is another factor that could affect APEC infection in breeders. For instance, the fast-growing lineages are found to be more susceptible to APEC infections than the slow-growing lineages [69]. Furthermore, intense genetic selection for rapid growth and growth-related traits have increased the incidence of ascites in broilers and broiler breeders and birds with ascites are highly vulnerable to infectious agents [70]. As a result, Denmark is slowly trying to remove the fast-growing lineages from their production system and grow more slow-growing lines, and this could help to make the birds healthier [71].

4.3. Antibiotics

Various antibiotics are used to treat APEC infections in birds. Antibiotics such as tetracyclines, aminoglycosides, macrolides, sulphonamides, penicillins, cephalosporins, trimethoprim, quinolones, polymyxins, chloramphenicol, and lincosamides are routinely used for the treatment of colibacillosis [72]. However, recent studies have reported resistance of APEC towards most of these antibiotics. The improper and unrestricted use of antibiotics in animal agriculture might be a possible reason for this increase.

4.4. Vaccination

Vaccination is one of the important strategies to limit APEC infections. Birds are vaccinated at day 1 and then around 12–14 weeks of age against E. coli. Developing efficient vaccines to prevent APEC infections is an important solution for limiting the use of antibiotics for treatment [73][74]. Moreover, preventing first-week mortality can be achieved through proper vaccination of the parent flocks [75][76]. Initially, only bacterins or inactivated vaccines were used against APEC, but after years of research, scientists developed live and subunit vaccines that became more popular [77]. Inactivated vaccines were used to study the possibility of vaccinating the broiler parents to provide protection and reduce the cost of vaccination for broilers [78]. The study also showed that antibodies derived from broiler parents could protect broiler chicks for up to 2 weeks before antibody protection was reduced [79]. Nobilis E. coli is a commercially available inactivated vaccine by Merck Sahrp & Dohme (MSD) Animal Health for active immunization of broiler breeders to provide passive immunization to broiler chickens. However, a study has shown a reduction in overall broiler breeder mortality but no effect on first-week chick mortality after Nobilis E. coli vaccination [80].
Due to poor cross-protection of commercially available vaccines, efforts to develop autogenous vaccines against APEC in broiler breeders have been found to be more effective [81]. A study on autogenous vaccines reported that it influenced the selection of phylogroups after vaccination. They repressed most of the phylogroups but resulted in some strain shifts. 

4.5. Probiotics and Prebiotics

Following restrictions on antibiotics, the use of alternatives to control APEC has been investigated for a long time. Probiotics are live non-pathogenic microbial feed supplements that provide health benefits such as protection from infectious agents, while prebiotics are non-digestible supplements that promote the growth of beneficial bacteria in the gut and thereby provide immunity [82][83]. Many scientists investigated the effect of Lactobacillus plantarum B1 probiotic in the feed of broilers and observed improvement in growth parameters along with a reduction in cecal E. coli output [82][83][84][85]. Additionally, the use of fructose oligosaccharide (FOS) along with Lactobacillus plantarum B1 was also tested, and improved performance was noted [84].

4.6. Bacteriophages

Bacteriophages are another possible source of treatment that could effectively prevent colibacillosis in chickens. They are viruses that target infectious bacteria without affecting the normal microflora [86][87][88][89]. A phage mixture using the bacteriophages SPR02 and DAF6 was administered through the air sac route against experimental infection of APEC O2 and showed a significant reduction in mortality in broilers [89]. Studies using phage cocktails supplemented through intra-tracheal and intra-venous routes also significantly reduced mortality and APEC load in the liver, lungs, and heart in broilers [86][87]. Phage-loaded chitosan particles administered orally have also shown a significant reduction in mortalities following experimental APEC infection in chickens. However, there are challenges in the practical application of these phage therapies because of the constraints in large-scale production and use in the poultry industry [89].

4.7. Miscellaneous

Advanced techniques to control APEC infections are also promising. Innate immune stimulants are one among them which can stimulate the immune responses against pathogens. Cytosine–phosphodiester–guanine motifs are one of the important innate immune stimulants which activate pathogen-associated molecular patterns (PAMPs) [90][91]. Additionally, antimicrobial peptides are short positively charged peptides that act against most bacteria including those resistant to antibiotics. D-analog of chicken cathelicidin-2 is an important antimicrobial peptide tested against APEC in an in vivo challenge study in broilers [92][93].

5. Conclusions

Broiler meat is one of the major sources of animal protein that is preferred globally, and broiler breeders play an inevitable role in sustainable broiler production; thus, the challenges in broiler breeder rearing should be minimized. APEC in broiler breeders is critical because it causes disease in breeders as well as is vertically transmitted from the hens’ reproductive tract through eggs to chicks and further horizontally transmitted between chicks. Moreover, evidence showing the transfer of antibiotic resistance genes vertically points out the importance of preventing and controlling APEC in broiler breeders. Using alternatives to antibiotics such as efficient vaccines, probiotics, prebiotics, and bacteriophages along with strict biosecurity and management practices could help limit the infection. Constant research focusing on the phenotypic and genotypic characterization of APEC isolates from broiler breeders is necessary because of the vast genetic diversity of this bacteria and its evolution as time passes.

This entry is adapted from the peer-reviewed paper 10.3390/pathogens12111280

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