Int. J. Environ. Res. Public Health 2010, 7(1), 89-114; doi:10.3390/ijerph7010089

Review
Avian Colibacillosis and Salmonellosis: A Closer Look at Epidemiology, Pathogenesis, Diagnosis, Control and Public Health Concerns
S. M. Lutful Kabir 1,2
1
Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Osaka, Japan
2
Department of Microbiology and Hygiene, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh; E-Mail: lkabir79@yahoo.com
Received: 26 November 2009 / Accepted: 11 January 2010 / Published: 12 January 2010

Abstract

: Avian colibacillosis and salmonellosis are considered to be the major bacterial diseases in the poultry industry world-wide. Colibacillosis and salmonellosis are the most common avian diseases that are communicable to humans. This article provides the vital information on the epidemiology, pathogenesis, diagnosis, control and public health concerns of avian colibacillosis and salmonellosis. A better understanding of the information addressed in this review article will assist the poultry researchers and the poultry industry in continuing to make progress in reducing and eliminating avian colibacillosis and salmonellosis from the poultry flocks, thereby reducing potential hazards to the public health posed by these bacterial diseases.
Keywords:
poultry; colibacillosis; salmonellosis; epidemiology; pathogenesis; public health

1. Introduction

Avian colibacillosis is an infectious disease of birds caused by Escherichia coli, which is considered as one of the principal causes of morbidity and mortality, associated with heavy economic losses to the poultry industry by its association with various disease conditions, either as primary pathogen or as a secondary pathogen. It causes a variety of disease manifestations in poultry including yolk sac infection, omphalitis, respiratory tract infection, swollen head syndrome, septicemia, polyserositis, coligranuloma, enteritis, cellulitis and salpingitis. Colibacillosis of poultry is characterized in its acute form by septicemia resulting in death and in its subacute form by peri-carditis, airsacculitis and peri-hepatitis [1]. On the other hand, Salmonella infection caused by a variety of Salmonella species is one of the most important bacterial diseases in poultry causing heavy economic losses through mortality and reduced production [2]. Avian salmonella infection may occur in poultry either acute or chronic form by one or more member of genus Salmonella, under the family Enterobacteriaceae [3]. Besides, motile Salmonellae (paratyphoid group) infection cause salmonellosis in chickens and have zoonotic significance.

Avian colibacillosis has been noticed to be a major infectious disease in birds of all ages. This disease has an important economic impact on poultry production worldwide. The majority of economic losses results from mortality and decrease in productivity of the affected birds [4]. Infectious bursal disease (IBD), mycoplasmosis, coccidiosis, Newcastle disease or infectious bronchitis, as well as nutritional deficiencies all predispose the birds to this disease [5]. However, faecal contamination of egg may result in the penetration of E. coli through the shell and may spread to the chickens during hatching and is often associated with high mortality rates, or it may give rise to yolk sac infection. On the other hand, with the great expansion of poultry rearing and farming, avian salmonellosis is the most devastating disease worldwide. The epidemiology of fowl typhoid and pullorum disease in poultry, particularly with regard to transmission from one generation to the next is known to be closely associated with infected eggs [6]. The birds that survive from clinical disease when infected at a young stage may show few signs of infection but can become carriers [7].

At slaughter, resistant strains from the gut readily soil poultry carcasses and as a result poultry meats are often contaminated with multiresistant E. coli [ 814]; likewise eggs become contaminated during laying [15]. Hence, resistant faecal E. coli from poultry can infect humans both directly and via food. These resistant bacteria may colonize the human intestinal tract and may also contribute resistance genes to human endogenous flora [16]. Similarly, the emergence of multidrug resistance among Salmonella spp. is an increasing concern. Salmonella serovar Hadar has been reported as one of the most resistant Salmonella serotypes [1719].

Microbial food safety is an increasing public health concern worldwide. Epidemiological reports suggest that poultry meat is still the primary cause of human food poisoning [20]. Poultry meat is more popular in the consumer market because of advantages such as easy digestibility and acceptance by the majority of people [21]. However, the presence of pathogenic and spoilage microorganisms in poultry meat and its by-products remains a significant concern for suppliers, consumers and public health officials worldwide. E. coli and Salmonella has been consistently associated with foodborne illnesses in most countries of the world.

There are many poultry diseases transmissible to human, among them avian colibacillosis and avian salmonellosis are the prime concerns. But the detailed information about avian colibacillosis and avian salmonellosis in connection to the public health concerns are not available yet in one place. So, I intend to write this review article focusing on the various aspects of avian colibacillosis and avain salmonellosis in connection to the public health concerns.

2. Epidemiology of Avian Colibacillosis and Avian Salmonellosis

2.1. Epidemiology of Avian Colibacillosis

E. coli is a gram-negative, non-acid-fast, uniform staining, non-spore-forming bacillus that grows both aerobically and anaerobically and may be variable in size and shape. Many strains are motile and have peritrichous flagella. E. coli is considered as a member of the normal microflora of the poultry intestine, but certain strains, such as those designated as avian pathogenic E. coli (APEC), spread into various internal organs and cause colibacillosis characterized by systemic fatal disease [22,23]. E. coli isolates pathogenic for poultry commonly belong to certain serogroups, particularly the serogroups O78, O1, and O2, and to some extent O15 and O55 [24,25]. In domestic poultry, avian colibacillosis is frequently associated with E. coli strains of serotypes O78:K80, O1:K1 and O2:K1 (2- Filali E). The avian colibacillosis was found widely prevalent in all age group of chickens (9.52 to 36.73%) with specially high prevalence rate in adult layer birds (36.73%) [26].

The most important reservoir of E. coli is the intestinal tract of animals, including poultry. In chickens, there are about 109 colony forming units (CFU) of bacteria per gram of feces and of these, 106 CFU are E. coli. E. coli has also been commonly isolated from the upper respiratory tract. In addition, it is present on the bird’s skin and feathers. These strains always belong to both pathogenic and non-pathogenic types [27]. In the caecal flora of healthy chickens, 10 to 15% of the E. coli strains may belong to an O-serotype that can also be isolated from colibacillosis lesions [28]. As soon as the first hours after hatching, the birds start building up their E. coli flora. The bacteria drastically increase their numbers in the gut. In a single bird a large number of different E. coli types is present, obtained via horizontal contamination from the environment, more specifically from other birds, faeces, water and feed [29]. Moreover, rodents may be carriers of APEC and hence a source of contamination for the birds [22].

The risk for colibacillosis increases with increasing infection pressure in the environment. A good housing hygiene and avoiding overcrowding are very important. Other principal risk factors are the duration of exposure, virulence of the strain, breed, and immune status of the bird [3034]. Every damage to the respiratory system favours infection with APEC. Several pathogens, like NDV, IBV and MG, both wildtype and vaccine strains, may play a part in this process. An unfavourable housing climate, like an excess of ammonia or dust, renders the respiratory system more susceptible to APEC infections through deciliation of the upper respiratory tract [22].

Pulsed field gel electrophoresis (PFGE) is considered to be the most reliable molecular finger-printing technique to differentiate organisms but restriction fragment length polymorphism (RFLP) is the one that is used most frequently. However, both techniques require large quantities of DNA, are time consuming, and require expensive equipment [35]. Other techniques such as ERIC–PCR and REP–PCR [36,37] and random amplification of polymorphic DNA (RAPD)–PCR [38] have been proposed as alternatives and used to characterize Escherichia coli isolates of avian origin [39,40]. Other molecular techniques such as ribotyping and isoenzyme profile have also been used to evaluate the clonality of avian E. coli [41]. Some clones are specific to APEC and a small-scale comparison of commensal and pathogenic isolates revealed that 83% of pathogenic strains belong to only five clones, whereas each of the 10 non-pathogenic strains belong to different clones [42]. On the other hand, clonal relationships were found for O2:K1 isolates from humans and chickens [43] and for O78 isolates from humans, cattle, sheep, pigs and chickens [44], indicating that these species too might act as a source of infection for chickens.

Even though certain O-types are more frequently detected in APEC than in commensal E. coli [45], the isolates are very heterogenous, both in their pheno- and genotype [43,4547]. On the other hand, the prevalence of certain serotypes is linked with the geographical localisation of a flock [48].

Since avian pathogenic E. coli (APEC) and human uropathogenic E. coli (UPEC) may encounter similar challenges when establishing infection in extraintestinal locations, they may share a similar content of virulence genes and capacity to cause disease. In this regard, Rodriguez-Siek et al. [49] compared 200 human uropathogenic E. coli (UPEC) and 524 avian pathogenic E. coli (APEC) isolates for their content of virulence genes (Table 1), including many implicated in extraintestinal pathogenic E. coli (ExPEC) virulence as well as those associated with APEC plasmids for assessing the potential of APEC to cause human extraintestinal diseases and a well-documented ability of avian E. coli to spread to human beings, the potential for APEC to act as human UPEC or as a reservoir of virulence genes for UPEC should be considered.

Avian pathogenic E. coli strains are often resistant to antimicrobials approved for poultry including cephradine [66], tetracyclines [6670], chloramphenicol [66], sulfonamides [67,6971], amino-glycosides [6870,72,73] and β-lactam antibiotics [66,67,69,71]. Resistance to fluoroquinolones was reported within several years of the approval of this class of drugs for use in poultry [45,71,74,75]. There is reason for concern that genes conferring resistance to extended-spectrum beta-lactams will emerge in avian pathogenic E. coli strains [76] and reduce the efficacy of ceftiofur, which is currently used on a limited basis in poultry breeding flocks and hatcheries. In one study, conducted at the University of Georgia, 97 of 100 avian pathogenic E. coli isolates were resistant to streptomycin and sulfonamide and 87% of these multiple antimicrobial resistant strains contained a class 1 integron, intI1, which carried multiple antibiotic resistance genes [70]. Multiple antimicrobial resistance traits of avian pathogenic E. coli have also been associated with transmissible R-plasmids [77].

2.2. Epidemiology of Avian Salmonellosis

Avian Salmonella infections are important as both a cause of clinical disease in poultry and as a source of food-borne transmission of disease to humans. Under the family of Enterobacteriaceae, the genus Salmonella is a facultative intracellular pathogen causing localized or systemic infections; as well as a chronic asymptomatic carrier state [78]. The etiological agent of fowl typhoid and pullorum disease is Salmonella enterica subsp. enterica serovar Gallinarum, which is divided into two distinct biovars under the serogroup D1, Gallinarum and Pullorum, which are denoted as S. gallinarum and S. pullorum, respectively [78,79]. In addition to S. gallinarum-pullorum, other salmonellae such as S. enteritidis, S. panama and S. dublin also belong to the serogroup D1 [79]. The various motile and non-host adapted highly invasive serotypes such as Salmonella enteritidis and Salmonella typhimurium are commonly referred to as paratyphoid salmonellae [80]. Age wise prevalence of avian salmonellosis showed highest infection rate in adult layers (53.25%) in comparison to brooding (14.55%), growing (16.10%) and pullet (16.10%) chickens [26].

Various routes of infection have been described. Oral route of infection represents the normal route of infection [81]. Although infection in newly hatched chicks by nasal and cloacal route are also considered as the important route of transmission. Chicks may be infected early by vertical transmission either from an infected ovary, oviduct or from the infected eggs during the passage through the cloacal faeces from infected or carrier hens. The birds survive from clinical disease when infected in young stage may show few signs of infection but they become carriers [82]. In adult carriers the reproductive organs are the predilection sites that often lead to the infection of ovarian follicles and as a result transovarian transmission of the disease occurs. The bacteria are passed out through the faeces and lateral spread takes place through the fecal contaminated feeds, water and litter [78].

Although more than 2,300 serotypes of Salmonella have been identified, only about 10% of these have been isolated from poultry [80]. Chickens are the natural hosts for the highly host adapted biovar S. gallinarum and S. pullorum, but natural outbreaks have also been reported in turkeys, guinea fowl, quail and pheasants [83]. Fowl typhoid is a peracute, acute or chronic form of disease affecting mostly adult chickens, whereas pullorum disease affects the very young chickens, mostly 2−3 weeks of age. In the adult it tends to be chronic [78,84]. Fowl typhoid is frequently referred to as a disease of adult birds; still, there are also reports of high morbidity and mortality in young chickens [85]. S. gallinarum can produce lesions in chicks, which are indistinguishable from those associated with pullorum disease [78]. A certain percentage of chickens that survive from the initial infection become carriers with or without presence of clinical signs and pathological lesions [83]. Crowding, malnutrition, and other stressful conditions as well as unsanitary surroundings can exacerbate mortality and performance losses due to salmonellosis, especially in young birds [86]. The potential risk factors responsible for Salmonella contamination of broiler-chicken flocks are summarized in Table 2.

In more recent years, the use of DNA-related techniques such as plasmid analysis [95,96], ribotyping [97100], and PFGE [101,102] have proved to be useful in discriminating isolates of Salmonella species. Lapuz et al. [103] investigated the prevalence of Salmonella in four layer farms in eastern Japan between 2004 and 2006 to determine the role of roof rats (Rattus rattus) in the epizootology of Salmonella enterica subsp. enterica serovar Enteritidis (S. enteritidis) and they suggested that roof rats were carriers of S. enteritidis and S. infantis and that persistent S. enteritidis and S. infantis infections in a rat population might play an important role in the spread and maintenance of these pathogens inside the layer premises.

Fowl typhoid and pullorum disease are distributed in many countries of the world, and have economic significance [104]. They are mainly distributed in Latin America, the Middle East, the Indian subcontinent, Africa and perhaps other parts of the world [78,105]. Salmonellosis has also been reported in many countries of South-East Asia including Bangladesh [106,107], India [108,109], Pakistan [110,111] and Nepal [112]. Fowl typhoid is common in both backyard chickens and in commercial poultry [113].

Salmonella and other food borne pathogens acquire antibiotic resistance by random chromosomal mutations, mutation of existing genes, and through specific mechanisms such as transduction, tranformation, and conjugation [114]. These mechanisms involve transfer of drug resistant genes by means of circular DNA plasmids such as R-factor, conjugative plasmid, or chromosomal elements [115122]. The occurrence and proliferation of antibiotic-resistant Salmonella in environmental samples, poultry, and other animals and humans may be due to the use of medicated feeds [123125], the practice of dipping hatching eggs in solutions containing antimicrobial agents [126128], routine inoculation of day-old poults with antibiotics [126128] and treatment of other animals [129] and humans [117] with antibiotics. Salmonella strains of avian origin are also often resistant to variety of antimicrobials approved for poultry including tetracycline [130133], oxytetracycline [134], penicillin [66,130134], aminoglycosides [130,132,133], sulfisoxazole [133] and fluoroquinolones [135]. On the other hand, Manie et al. [136] found several strains of multiple antibiotic-resistant Salmonella strains in chicken.

3. Pathogenesis and Disease Syndromes of Avian Colibacillosis and Avian Salmonellosis

3.1. Pathogenesis and Disease Syndromes of Avian Colibacillosis

The mechanisms by which avian pathogenic E. coli cause infection are largely unknown. The virulence factors contributing to the pathogenesis of avian colibacillosis are summarized in Table 3.

Recently, Hughes et al. [155] described a cross-sectional study of wild birds in northern England to determine the prevalence of E. coli-containing genes that encoded Shiga toxins (stx1 and stx2) and intimin (eae), important virulence determinants of STEC associated with human disease and they stated that while wild birds were unlikely to be direct sources of STEC infections, they did represent a potential reservoir of virulence genes.

APEC are responsible for a considerable number of various diseases at different ages. Neonatal infection of chicks can occur horizontally, from the environment, or vertically, from the hen. A laying hen suffering from E. coli-induced oophoritis or salpingitis may infect the internal egg before shell formation. Faecal contamination of the eggshell is possible during the passage of the egg through the cloaca and after laying. The latter possibility is considered as the main route of infection for the egg [22]. Before hatching, APEC causes yolk sac infections and embryo mortality. The chick can also be infected during or shortly after hatching. In these cases, retained infected yolk, omphalitis, septicemia and mortality of the young chicks up to an age of three weeks is seen [22]. Broilers may be affected by necrotic dermatitis, also known as cellulitis, characterized by a chronic inflammation of the subcutis on abdomen and thighs [22].

Swollen head syndrome (SHS), mainly a problem in broilers, causes oedema of the cranial and periorbital skin. SHS can cause a reduction in egg production of 2 to 3%, and a mortality of 3 to 4% [156]. Data on this disease are contradictory. Picault et al. [157] and Hafez & Löhren [158] considered SHS as a disease caused by avian pneumovirus (APV), usually followed by an opportunistic E. coli infection. Nakamura et al. [159] however reported that APEC were probably playing a significant part in the disease, but that the role of APV was not at all clear. This had been confirmed by Georgiades et al. [160], who did not detect APV in any of the flocks affected by SHS during a field study, but instead detected infectious bronchitis virus (IBV), avian adenovirus, avian reovirus, and Newcastle disease virus (NDV), as well as Mycoplasma synoviae and M. gallisepticum (MG).

APEC probably do not cause intestinal diseases. Nevertheless, enterotoxigenic E. coli (ETEC) are occasionally isolated from poultry suffering from diarrhoea [161163] and diarrhoea was experimentally induced after intramuscular inoculation of APEC [164]. On the other hand, enteropathogenic E. coli (EPEC) were isolated from clinically healthy chickens [165]. In turkeys, experimentally inoculated EPEC can only cause enteritis in combination with coronavirus [166].

Layers as well as broilers may suffer from acute or chronic salpingitis [167,168]. Salpingitis can be the result of an ascending infection from the cloaca [167,168] or an infection of the left abdominal airsac [22], although Bisgaard and Dam [167] considered the latter possibility less likely than an ascending infection. Salpingitis can lead to the loss of egg-laying capacity [163]. In the case of chronic salpingitis, the oviduct has a yellowish-gray, cheese-like content, with a concentric structure [168]. In layers, salpingitis can cause egg peritonitis if yolk material has been deposited in the peritoneal cavity, characterised by a sero-fibrinous inflammation of the surrounding tissues [22].

Airsacculitis is observed at all ages. The bird is infected by inhalation of dust contaminated with faecal material, which may contain 106 CFU of E. coli per gram [169]. This aerogenic route of infection is considered as the main origin of systemic colibacillosis or colisepticemia [33,143,170].

Septicemia also affects chickens of all ages, and is mainly described in broilers. It is the most prevalent form of colibacillosis, characterised by polyserositis [143]. It causes depression, fever and often high mortality. Although its pathogenesis has not been elucidated, several routes of infection are possible: neonatal infections [22], infections through skin lesions [171], infection of the reproductive organs [22,167,168], of the respiratory tract [33] and even infection per os [172]. When E. coli reaches the vascular system, the internal organs and the heart are infected. The infection of the myocard causes heart failure [173]. Septicemia occasionally also leads to synovitis and osteomyelitis [22,174] and on rare occasions to panophthalmia [22]. Coligranuloma or Hjarre’s disease is characterised by granulomas in liver, caeca, duodenum and mesenterium, but not in the spleen. It is a rare form of colibacillosis, but in affected flocks it may cause up to 75% mortality [22].

Further studies are needed to determine the role of newly identified putative virulence genes and genes with unknown functions as virulence markers of APEC to strengthen the current understanding of mechanisms underlying the pathogenesis of avian colibacillosis.

3.2. Pathogenesis and Disease Syndrome of Avian Salmonellosis

The pathogenicity of Salmonella depends on the invasive properties and the ability of the bacteria to survive and multiply within the cells, particularly macrophages [175]. The main site of multiplication of these bacteria is the digestive tract, which may result in widespread contamination of the environment due to bacterial excretion through feces. Following invasion through the intestinal mucosa, cecal tonsils and Peyer’s patches, the organisms are engulfed by macrophages, and through the blood stream and/or lymphatic systems, they spread to organs rich in reticuloendothelial tissues (RES), such as liver and spleen, which are the main sites of multiplication [176]. In case of inadequate body defense mechanism, they may lead to second invasion and be localized in other organs, particularly ovary, oviduct, myocardium, pericardium, gizzard, yolk sac and/or lungs [177]. In the bird challenge, S. typhimurium rapidly caused inflammation of the intestinal mucosa, but S. pullorum preferentially targeted the bursa of Fabricius prior to eliciting intestinal inflammation [178]. Pullorum disease manifests itself predominantly as an enteric disease of chickens, while fowl typhoid shows signs of septicemic disease [78]. Both biovars can cause septicemic infections, which may be acute or chronic, but unlike S. pullorum, S. gallinarum is capable of producing peracute infection and hemolytic anemia in both young and adults [84]. S. gallinarum is extremely pathogenic to young broiler chicks [179].

Fowl typhoid is indistinguishable from pullorum disease unless the etiological agent is isolated and identified [113]. Clinical signs in chicks and poults include anorexia, diarrhea, dehydration, weakness and high mortality [83]. In mature fowls, fowl typhoid and pullorum disease are manifested by anorexia, drop in egg production, increased mortality, reduced fertility and hatchability [83]. S. pullorum infected adult birds may or may not exhibit any clinical signs, or they cannot be detected by their physical appearance [78]. Furthermore, the exact mechanisms of getting these poultry diseases are still remained to be obscured.

4. Diagnosis of Avian Colibacillosis and Avian Salmonellosis

Colibacillos is suspected based on the clinical features and the typical macroscopic lesions. The diagnosis is obtained by E. coli isolation from cardiac blood and affected tissues, like liver, spleen, pericard or bone marrow. Experimentally it was shown that in acute cases, isolation is possible from six hours to three days after infection; in subacute cases, isolation is only possible until seven days after infection [180]. Contamination from the intestines is rarely a problem, if fresh material is used and standard bacteriological procedures are applied [181]. Selective media like McConkey, eosin-methylene blue or drigalki agar are used for isolation. Further identification of the isolated colonies is based on biochemical reactions (indol production, fermentation of glucose with gas production, presence of ß-galactosidase, absence of hydrogen sulphite production and urease, and the inability to use citrate as a carbon source) [29]. O-serotyping is a frequently used typing method. An ELISA, based on sonicated E. coli, has been developed for detection of antibodies against two important pathogenic serotypes of E. coli: O78:K80 and O2:K1 [182]. Another ELISA was based on fimbrial antigen [183]. Both have limited value because they can only detect homologous APEC types. All currently known virulence-associated factors, detected in strains isolated from colibacillosis lesions, can also be detected in faecal isolates from clinically healthy chickens. For this reason, none of these traits can be used for APEC identification.

Diagnosis of avian salmonellosis should be confirmed by isolation, identification, and serotyping of Salmonella strains. Infections in mature birds can be identified by serologic tests, followed by necropsy evaluation complemented by microbiologic culture and typing for confirmation. A serological ELISA test for the diagnosis of avian salmonellosis either with S. typhimurium or S. enteritidis has been established [184]. Szmolka et al. [185] established a diagnostic and a real-time PCR system for rapid and reliable genus- and serovar- (S. enteritidis and S. typhimurium) specific detection of Salmonella for monitoring purposes in the poultry food chain.

5. Preventive Measures for Controlling Avian Colibacillosis and Avian Salmonellosis

5.1. Avian Colibacillosis

A first step is the prevention of egg contamination by fumigating them within two hours after lay, and by removing cracked eggs or eggs soiled with faecal material. It is recommended to vent the incubators and hatchers to the outside and to have as few breeder flocks as possible per breeding unit [22]. In chicks, contamination with APEC from the environment must be controlled by reduction and control of intestinal infection. This can be achieved using competitive exclusion (CE) [186190], i.e., inoculating day-old chicks with normal bacterial flora of healthy adult chickens or a monoculture, for instance of Bacillus subtilis. Birds also need to be protected against pathogens that promote infections with APEC. This is possible by using Mycoplasma-free birds [22] and protecting the birds against mycoplasmas and viral diseases by vaccinations [170]. Disease introduction must also be avoided [170] by a suitable house infrastructure, the correct use of a transition zone (for changing clothes and shoes, and washing hands), and pest control: rodent faeces are a source of pathogenic E. coli [22]. The housing climate must be kept optimal for bird density, humidity, ventilation, dust and ammonia [29,170].

The great diversity among APEC strains limits the possibilities of vaccination, and vaccines are not used on a large scale. Several vaccines based on killed or attenuated strains have been tested experimentally. In general, they give sufficient protection against infection with homologous strains, but protection against heterologous strains is less efficient [29]. However, Melamed et al. [191] reported a certain degree of heterologous protection obtained with an inactivated vaccine. Passive immunisation of young birds via the breeder hens is efficient for two weeks [192], if the birds are challenged with homologous strains. Vaccines based on virulence factors like fimbriae, also give a good homologous protection, i.e., against APEC possessing the same fimbriae [193].

5.2. Avian Salmonellosis

Although fowl typhoid and pullorum disease are widely distributed in most parts of the world, the diseases have been eradicated from commercial poultry in developed countries such as the United States of America, Canada and most countries of Western Europe [78]. Successful control programs can be achieved by developing good hygiene and management together with routine serological tests and slaughter policy [177]. The principal management procedures should include chicks free from infections, and the chicks should be placed in a cleaned, sanitized and S. gallinarum and S. pullorum free environment with strict biosecurity measures [194]. The feed and water should be free from Salmonella contamination. The dead birds need to be well disposed. Adequate precautions are needed to prevent infections from mechanical carriers like footwear, human clothing, hatchery disciplines, equipments, litters, crates, trucks and processing plants [195]. Wray et al. [196] described that the birds need to be tested at the age of 16 weeks due to immunologic maturity, at the point of lay due to stress and two consecutive times one month apart to provide the acceptable evidence that the flock is free from fowl typhoid [177]. Kabir et al. [189] and Kabir [190] demonstrated the potential role of probiotics for the controlling of Salmonella strains of poultry via the mechanisms of competitive exclusion. Vaccines may be used to control the disease, and antibiotics can be used for the treatment of fowl typhoid and pullorum disease.

6. Public Health Concerns of Avian Colibacillosis and Avian Salmonellosis

E. coli of the O2:K1 serotype isolated from human urinary tract infections and from septicemic chickens are phenotypically highly related. A distinction between both groups was only possible by examining their plasmid contents [43]. Cherifi et al. [44] obtained similar results for a group of O78 isolates and concluded that chickens might be a source of septicemic human O78 infections. However, contrasting results were obtained in a study by Caya et al. [197]. In this study, avian E. coli isolates from healthy and diseased birds (airsacculitis and cellulitis) and E. coli strains isolated from sick humans during the same period and in the same geographical area as the avian isolates were compared. The study results suggested that these avian isolates possessed very few of the attributes required to cause disease in humans. Reversely, human isolates can be pathogenic to day-old chicks after subcutaneous inoculation. Strains tested were of the serotypes O1, O2, O18 and O78 [198]. Although O157 verotoxigenic E. coli (VTEC) had been detected in broilers [158], the chicken was not considered as an important reservoir for this zoonotically often reported serotype. Experimental studies showed that chickens might be functioned as a reservoir: O157 strains easily infected the young birds, even at a low dose, and persisted in the caecum for up to three months [199]. The study by Stavric et al. [200] showed that layers were also susceptible to colonisation by O157:H7 and other VTEC after inoculation per os. The intestines were increasingly colonised if increasing inoculation doses were used. The older the bird, the more restricted the colonisation and persistence were. All birds involved in the experiment remained clinically healthy. Histologically, attachment and effacement lesions were detected in the proximal caeca. Chapman et al. [199] reported that at that time no bacteriologically confirmed human cases of O157 infections had been observed, caused by poultry. Nonetheless, chicken meat was sometimes positive for VTEC [201,202]. In addition, Manges et al. [203] conducted a case-control study between April 2003 and June 2004 and they demonstrated that antimicrobial resistant, urinary tract infection (UTI) causing E. coli could have a food reservoir, possibly in poultry or pork. Uncontrolled, avian E. coli represents a serious animal welfare concern and risk to public health as it is a zoonotic organism with avian E. coli species known to adapt to humans.

Salmonellosis is of public health concern because most of the strains of Salmonella are potentially pathogenic to humans and animals. Avian salmonellosis can pose a health risk to people if exposed. Symptoms appear similar to food poisoning, such as diarrhea and acute gastroenteritis. However, it appears that birds mainly acquire the disease from the environment and that infected birds play a relatively small role in the transmission of disease to domestic animals and humans. Public health concerns and the potential for foodborne zoonotic transmission have made Salmonella the subject of numerous international, national, and local surveillance programs [204].

7. Strategies for Reducing Public Health Hazards

The risk of colibacillosis can be reduced through simple precautions.

  • By thorough cleaning of poultry houses.

  • By ensuring proper ventilation of the poultry houses and chlorination of drinking water.

  • By washing hands carefully before and after food preparation and after toileting.

  • By avoiding eating raw or undercooked poultry.

  • By wrapping fresh meats in plastic bags at the market to prevent fluids from dripping on other foods.

  • By ensuring the correct internal cooking temperature especially when using a microwave.

The risk of salmonellosis can be also reduced through simple precautions.

  • By washing hands carefully before and after food preparation and after toileting or changing diapers.

  • By avoiding eating raw or undercooked eggs (or foods made with raw eggs) and poultry.

  • By wrapping fresh meats in plastic bags at the market to prevent fluids from dripping on other foods.

  • By ensuring the correct internal cooking temperature especially when using a microwave.

  • By avoiding chicks and ducklings as pets for small children.

8. Conclusions

Avian colibacillosis and salmonellosis are considered to be the major bacterial disease problems in the poultry industry world-wide and these diseases constitute a major public health burden and represent a significant cost in many countries. The economic and public health burden of these diseases have made this topic time demanding. It is suggested from this review article that more effective application of existing control methods would greatly reduce the hazards to public health.

I would like to thank all the reviewers for their constructive suggestions and comments.

References

  1. Calnek, BW; Barnes, HJ; Beard, CW; McDougald, LR; Saif, YM. Diseases of Poultry, 10th ed ed.; Iowa State University Press: Ames, IA, USA, 1997.
  2. Haider, MG; Hossain, MG; Hossain, MS; Chowdhury, EH; Das, PM; Hossain, MM. Isolation and characterization of enterobacteria associated with health and disease in sonali chickens. Bangl. J. Vet. Med 2004, 2, 15–21.
  3. Hofstad, MS; John, BH; Calnek, BW; Reid, WN; Yoder, HW, Jr. Diseases of Poultry, 8th ed. ed.; Panima Education Book Agency: New Delhi, India, 1992; pp. 65–123.
  4. Otaki, Y. Poultry disease control programme in Japan. Asian Livestock 1995, 20, 65–67.
  5. Wray, C; Davies, RH. Enterobacteriacae. In Poultry Diseases, 5th ed; Jordan, F, Pattison, M, Alexander, D, Faragher, T, Eds.; W. B. Saunders: Philadelphia, PA, USA, 2001; pp. 95–130.
  6. Wigley, P; Berchieri, A, Jr; Page, KL; Smith, AL; Barrow, PA. Salmonella enterica serovar Pullorum persists in splenic macrophages and in the reproductive tract during persistent, disease free carriage in chickens. Infect. Immun 2001, 69, 7873–7879, doi:10.1128/IAI.69.12.7873-7879.2001.
  7. Berchieri, A, Jr; Murphy, CK; Marston, K; Barrow, PA. Observations on the persistence and vertical transmission of Salmonella enterica serovars Pullorum and Gallinarum in chickens: Effect of bacterial and host genetic background. Avian Pathol 2001, 30, 221–231, doi:10.1080/03079450120054631.
  8. Caudry, SD; Stanisich, VA. Incidence of antibiotic resistant Escherichia coli associated with frozen chicken carcasses and characterization of conjugative R-plasmids derived from such strains. Antimicrob. Agents Chemother 1979, 16, 701–709, doi:10.1128/AAC.16.6.701.
  9. Nazer, AH. Transmissible drug resistance in Escherichia coli isolated from poultry and their carcasses in Iran. Cornell. Vet 1980, 70, 365–371.
  10. Bensink, JC; Botham, FP. Antibiotic resistant coliform bacilli, isolated from freshly slaughtered poultry and from chilled poultry at retail outlets. Aust. Vet. J 1983, 60, 80–83, doi:10.1111/j.1751-0813.1983.tb05876.x.
  11. Linton, AH; Howe, K; Hartley, CL; Clements, HM; Richmond, MH; Osborne, AD. Antibiotic resistance among Escherichia coli O-serotypes from the gut and carcasses of commercially slaughtered broiler chickens: a potential public health hazard. J. Appl. Bacteriol 1977, 42, 365–378, doi:10.1111/j.1365-2672.1977.tb00704.x.
  12. Chaslus Dancla, E; Lafont, JP. IncH plasmids in Escherichia coli strains isolated from broiler chicken carcasses. Appl. Environ. Microbiol 1985, 49, 1016–1018.
  13. Jayaratne, A; Collins-Thompson, DL; Trevors, JT. Occurrence of aminoglycoside phosphotransferase subclass I and II structural genes among Enterobacteriaceae spp. isolated from meat samples. Appl. Microbiol. Biotechnol 1990, 33, 547–552.
  14. Turtura, GC; Massa, S; Chazvinizadeh, H. Antibiotic resistance among coliform bacteria isolated from carcasses of commercially slaughtered chickens. Int. J. Food Microbiol 1990, 11, 351–354, doi:10.1016/0168-1605(90)90029-5.
  15. Lakhotia, RL; Stephens, JF. Drug resistance and R factors among enterobacteria isolated from eggs. Poult. Sci 1973, 52, 1955–1962, doi:10.3382/ps.0521955.
  16. van den Bogaard, E; London, N; Driessen, C; Stobberingh, EE. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J. Antimicrob. Chemother 2001, 47, 763–771, doi:10.1093/jac/47.6.763.
  17. Cruchaga, S; Echeita, A; Aladueña, A; García-Peña, J; Frias, N; Usera, MA. Antimicrobial resistance in salmonellae from humans, food and animals in Spain in 1998. J. Antimicrob. Chemother 2001, 47, 315–321, doi:10.1093/jac/47.3.315.
  18. van Looveren, M; Chasseur-Libotte, ML; Godard, C; Lammens, C; Wijdooghe, M; Peeters, L; Goossens, H. Antimicrobial susceptibility of nontyphoidal Salmonella isolated from humans in Belgium. Acta Clin. Belg 2001, 56, 180–186.
  19. Wybot, I; Wildemauwe, C; Godard, C; Bertrand, S; Collard, JM. Antimicrobial drug resistance in nontyphoid human Salmonella in Belgium: Trends for the period 2000–2002. Acta Clin. Belg 2004, 59, 152–160.
  20. Mulder, RW. Hygiene during transport, slaughter and processing. In Poultry Meat Science Poultry Science Symposium Series; Richardson, RI, Mead, GC, Eds.; CABI Publishing: Oxford shire, UK, 1999; pp. 277–285.
  21. Yashoda, KP; Sachindra, NM; Sakhare, PZ; Rao, DN. Microbiological quality of broiler chicken carcasses processed hygienically in a small scale poultry processing unit. J. Food Qual 2001, 24, 249–259, doi:10.1111/j.1745-4557.2001.tb00606.x.
  22. Barnes, HJ; Gross, WB. Colibacillosis. In Diseases of Poultry, 10th ed; Calnek, BW, Barnes, HJ, Beard, CW, McDougald, LR, Saif, YM, Eds.; Iowa State University Press: Ames, IA, USA, 1997; pp. 131–141.
  23. La Ragione, RM; Woodward, MJ. Virulence factors of Escherichia coli serotypes associated with avian colisepticemia. Res. Vet. Sci 2002, 73, 27–35, doi:10.1016/S0034-5288(02)00075-9.
  24. Gross, WB. Diseases due to Escherichia coli in poultry. In Escherichia coli in Domestic Animals and Humans; Gyles, CL, Ed.; CAB International Library: Wallingford, UK, 1994; pp. 237–260.
  25. Chart, H; Smith, HR; La Ragione, RM; Woodward, MJ. An investigation into the pathogenic properties of Escherichia coli strains BLR, BL21, DH5α, and EQ1. J. Appl. Microbiol 2000, 89, 1048–1058, doi:10.1046/j.1365-2672.2000.01211.x.
  26. Rahman, MA; Samad, MA; Rahman, MB; Kabir, SML. Bacterio-pathological studies on salmonellosis, colibacillosis and pasteurellosis in natural and experimental infections in chickens. Bangl. J. Vet. Med 2004, 2, 1–8.
  27. Harry, EG; Hemsley, LA. The relationship between environmental contamination with septicemia strains of Escherichia coli. Vet. Rec 1965, 77, 241–245.
  28. Harry, EG; Hemsley, LA. The association between the presence of septicemia strains of Escherichia coli in the respiratory and intestinal tracts of chickens and the occurrence of coli septicemia. Vet. Rec 1965, 77, 35–40.
  29. Dho-Moulin, M; Fairbrother, JM. Avian pathogenic Escherichia coli (APEC). Vet. Res 1999, 30, 299–316.
  30. Gross, WB; Siegel, PB; Hall, RW; Domermuth, CH; DuBoise, RT. Production and persistence of antibodies in chickens to sheep erythrocytes. 2. Resistance to infectious diseases. Poult. Sci 1980, 59, 205–210, doi:10.3382/ps.0590205.
  31. Rosenberger, JK; Fries, PA; Cloud, SS; Wilson, RA. In vitro and in vivo characterization of avian Escherichia coli. II. Factors associated with pathogenicity. Avian Dis 1985, 29, 1094–1107, doi:10.2307/1590464.
  32. Gross, WB. Effect of short-term exposure of chickens to corticosterone on resistance to challenge exposure with Escherichia coli and antibody response to sheep erythrocytes. Am. J. Vet. Res 1992, 53, 291–293.
  33. Pourbakhsh, SA; Boulianne, M; Martineau-Doizé, B; Dozois, CM; Desautels, C; Fairbrother, JM. Dynamics of Escherichia coli infection in experimentally inoculated chickens. Avian Dis 1997, 41, 221–233, doi:10.2307/1592463.
  34. McGruder, ED; Moore, GM. Use of lipopolysaccharide (LPS) as a positive control for the evaluation of immunopotentiating drug candidates in experimental avian colibacillosis models. Res. Vet. Sci 1998, 66, 33–37.
  35. da Silveiraa, WD; Ferreiraa, A; Lancellottia, M; Barbosaa, AGCD, I; Leitea, DS; de Castrob, AFP; Brocchi, M. Clonal relationships among avian Escherichia coli isolates determined by enterobacterial repetitive intergenic consensus (ERIC)–PCR. Vet. Microbiol 2002, 89, 323–328, doi:10.1016/S0378-1135(02)00256-0.
  36. Gilson, E; Clément, JM; Brutlag, D; Hofnung, M. A family of dispersed repetitive extragenic palindromic DNA sequences in Escherichia coli. EMBO J 1984, 3, 1417–1421.
  37. Hulton, CS; Higgins, CF; Sharp, PM. ERIC sequences: A novel family of repetitive elements in the genomes of Escherichia coli, Salmonella typhimuirum and other enterobacteria. Mol. Microbiol 1991, 5, 825–834, doi:10.1111/j.1365-2958.1991.tb00755.x.
  38. Welsh, J; McClelland, M. Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 1990, 18, 7213–7218, doi:10.1093/nar/18.24.7213.
  39. Chansiripornchai, N; Ramasoota, P; Sasipreyajan, J; Svenson, SB. Differentiation of avian Escherichia coli (APEC) isolates by random amplified polymorphic DNA (RAPD) analysis. Vet. Microbiol 2001, 80, 77–83.
  40. de Moura, AC; Irino, K; Vidotto, MC. Genetic variability of avian Escherichia coli isolates evaluated by enterobacterial reptitive intergenic consensus and repetitive extragenic palindromic polymerase chain reation. Avian Dis 2001, 45, 173–181, doi:10.2307/1593025.
  41. Silveira, WD; Lancellotti, M; Ferreira, A; Solferini, VN; de Castro, AFP; Stehling, EG; Brocchi, M. Determination of the clonal structure of avian Escherichia coli strains by isoenzyme and ribotyping analysis. J. Vet. Med. B Infect. Dis. Vet. Public Hlth 2003, 50, 63–69, doi:10.1046/j.1439-0450.2003.00607.x.
  42. White, DG; Dho-moulin, M; Wilson, RA; Whittam, TS. Clonal relationships and variation in virulence among Escherichia coli strains of avian origin. Microb. Pathog 1993, 14, 399–409, doi:10.1006/mpat.1993.1039.
  43. Achtman, M; Heuzenroeder, M; Kusecek, B; Ochman, H; Caugant, D; Selander, RK; Vaïsanen-Rhen, V; Korhonen, TK; Stuart, S; Orskov, F; Orskov, I. Clonal analysis of Escherichia coli O2: K1 isolated from diseased humans and animals. Infect. Immun 1986, 51, 268–276.
  44. Cherifi, A; Contrepois, M; Picard, B; Goullet, P; Orskov, I; Orskov, F. Clonal relationships among Escherichia coli serogroup O78 isolates from human and animal infections. J. Clin. Microbiol 1994, 32, 1197–1202.
  45. Blanco, JE; Blanco, M; Mora, A; Blanco, J. Production of toxins (enterotoxins, verotoxins, and necrotoxins) and colicins by Escherichia coli strains isolated from septicemic and healthy chickens: relationship with in vivo pathogenicity. J. Clin. Microbiol 1997a, 35, 2953–2957.
  46. de Moura, AC; Irino, K; Vidotto, MC. Genetic variability of avian Escherichia coli strains evaluated by enterobacterial repetitive intergenic consensus and repetitive extragenic palindromic polymerase chain reaction. Avian Dis 2001, 45, 173–181, doi:10.2307/1593025.
  47. Ewers, C; Janßen, T; Kießling, S; Philipp, HC; Wieler, LH. Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry. Vet. Microbiol 2004, 104, 91–101, doi:10.1016/j.vetmic.2004.09.008.
  48. Blanco, JE; Blanco, M; Mora, A; Jansen, WH; Garcia, V; Vazquez, ML; Blanco, J. Serotypes of Escherichia coli isolated from septicemic chickens in Galicia (Northwest Spain). Vet. Microbiol 1998, 61, 229–235, doi:10.1016/S0378-1135(98)00182-5.
  49. Rodriguez-Siek, KE; Giddings, CW; Doetkott, C; Johnson, TJ; Fakhr, MK; Lisa, KN. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 2005, 151, 2097–2110, doi:10.1099/mic.0.27499-0.
  50. Gilson, L; Mahanty, HK; Kolter, R. Four plasmid genes are required for colicin V synthesis, export, and immunity. J. Bacteriol 1987, 169, 2466–2470.
  51. Russo, TA; Carlino, UB; Mong, A; Jodush, ST. Identification of genes in an extraintestinal isolate of Escherichia coli with increased expression after exposure to human urine. Infect. Immun 1999, 67, 5306–5314.
  52. Binns, MM; Davies, DL; Hardy, KG. Cloned fragments of the plasmid ColV, I-K94 specifying virulence and serum resistance. Nature 1979, 279, 778–781, doi:10.1038/279778a0.
  53. Chuba, PJ; Leon, MA; Banerjee, A; Palchaudhuri, S. Cloning and DNA sequence of plasmid determinant iss, coding for increased serum survival and surface exclusion, which has homology with lambda DNA. Mol. Gen. Genet 1989, 216, 287–292, doi:10.1007/BF00334367.
  54. de Lorenzo, V; Neilands, JB. Characterization of iucA and iucC genes of the aerobactin system of plasmid ColV-K30 in Escherichia coli. J. Bacteriol 1986, 167, 350–355.
  55. de Lorenzo, V; Bindereif, A; Paw, BH; Neilands, JB. Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12. J. Bacteriol 1986, 165, 570–578.
  56. Runyen-Janecky, LJ; Reeves, SA; Gonzales, EG; Payne, SM. Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect. Immun 2003, 71, 1919–1928, doi:10.1128/IAI.71.4.1919-1928.2003.
  57. Achtman, M; Kennedy, N; Skurray, R. Cell–cell interactions in conjugating Escherichia coli: Role of TraT protein in surface exclusion. Proc. Natl. Acad. Sci. USA 1977, 74, 5104–5108, doi:10.1073/pnas.74.11.5104.
  58. Moll, A; Manning, PA; Timmis, KN. Plasmid determined resistance to serum bactericidal activity: A major outer membrane protein, the traT gene product, is responsible for plasmid-specified serum resistance in Escherichia coli. Infect. Immun 1980, 28, 359–367.
  59. Provence, DL; Curtiss, R, III. Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect. Immun 1994, 62, 1369–1380.
  60. Russo, TA; Carlino, UB; Johnson, JR. Identification of a new iron-regulated virulence gene, ireA, in an extraintestinal pathogenic isolate of Escherichia coli. Infect. Immun 2001, 69, 6209–6216, doi:10.1128/IAI.69.10.6209-6216.2001.
  61. Schubert, S; Rakin, A; Karch, H; Carniel, E; Heesemann, J. Prevalence of the “high-pathogenicity island” of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect. Immun 1998, 66, 480–485.
  62. Hacker, J; Goebel, W; Hof, H; Konig, W; Konig, B; Scheffer, J; Hughes, C; Marre, R. Adhesins, serum resistance and cytolysins of E coli-genetic structure and role in pathogenicity. In Bacteria, Complement and the Phagocytic Cell; Cabello, FC, Pruzzo, C, Eds.; Springer-Verlag: New York, NY, USA, 1988; pp. 221–229.
  63. Fields, PI; Blom, K; Hughes, HJ; Helsel, LO; Feng, P; Swaminathan, B. Molecular characterization of the gene encoding H antigen in Escherichia coli and development of a PCR restriction fragment length polymorphism test for identification of E. coli O157:H7 and O157:NM. J. Clin. Microbiol 1997, 35, 1066–1070.
  64. Johnson, JR; Delavari, P; Kuskowski, M; Stell, AL. Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J. Infect. Dis 2001, 183, 78–88, doi:10.1086/317656.
  65. Johnson, JR; Stell, AL. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis 2000, 181, 261–272, doi:10.1086/315217.
  66. Rahman, MA; Samad, MA; Rahman, MB; Kabir, SML. In vitro antibiotic sensitivity and therapeutic efficacy of experimental salmonellosis, colibacillosis and pasteurellosis in broiler chickens. Bangl. J. Vet. Med 2004, 2, 99–102.
  67. Cloud, SS; Rosenberger, JK; Fries, PA; Wilson, RA; Odor, EM. In vitro and in vivo characterization of avian Escherichia coli. I. Serotypes, metabolic activity, and antibiotic sensitivity. Avian Dis 1985, 29, 1084–1093, doi:10.2307/1590463.
  68. Irwin, RJ; McEwen, SA; Clarke, RC; Meek, AH. The prevalence of verocytotoxin-producing Escherichia coli and antimicrobial resistance patterns of nonverocytotoxin-producing Escherichia coli and Salmonella in Ontario broiler chickens. Can. J. Vet. Res 1989, 53, 411–418.
  69. Blanco, JE; Blanco, M; Mora, A; Blanco, J. Prevalence of bacterial resistance to quinolones and other antimicrobials among avian Escherichia coli strains isolated from septicemic and healthy chickens in Spain. J. Clin. Microbiol 1997, 35, 2184–2185.
  70. Bass, L; Liebert, CA; Lee, MD; Summers, AO; White, DG; Thayer, SG; Maurer, JJ. Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli. Antimicrob. Agents Chemother 1999, 43, 2925–2929.
  71. Li, XS; Wang, GQ; Du, XD; Cui, BA; Zhang, SM; Shen, JZ. Antimicrobial susceptibility and molecular detection of chloramphenicol and florfenicol resistance among Escherichia coli isolates from diseased chickens. J. Vet. Sci 2007, 8, 243–247, doi:10.4142/jvs.2007.8.3.243.
  72. Dubel, JR; Zink, DL; Kelley, LM; Naqi, SA; Renshaw, HW. Bacterial antibiotic resistance: frequency of gentamicin-resistant strains of Escherichia coli in the fecal microflora of commercial turkeys. Am. J. Vet. Res 1982, 43, 1786–1789.
  73. Allan, BJ; van den Hurk, JV; Potter, AA. Characterization of Escherichia coli isolated from cases of avian colibacillosis. Can. J. Vet. Res 1993, 57, 146–151.
  74. White, DG; Piddock, LJ; Maurer, JJ; Zhao, S; Ricci, V; Thayer, SG. Characterization of fluoroquinolone resistance among veterinary isolates of avian Escherichia coli. Antimicrob. Agents Chemother 2000, 44, 2897–2899, doi:10.1128/AAC.44.10.2897-2899.2000.
  75. van den Bogaard, AE; London, N; Driessen, C; Stobberingh, EE. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J. Antimicrob. Chemother 2001, 47, 763–771, doi:10.1093/jac/47.6.763.
  76. Zhao, S; White, DG; McDermott, PF; Friedman, S; English, L; Ayers, S; Meng, J; Maurer, JJ; Holland, R; Walker, RD. Identification and expression of cephamycinase blacmy genes in Escherichia coli and Salmonella isolated from food animals and ground meats. Antimicrob. Agents Chemother 2001, 45, 3647–3650, doi:10.1128/AAC.45.12.3647-3650.2001.
  77. Wooley, RE; Spears, KR; Brown, J; Nolan, LK; Dekich, MA. Characteristics of conjugative R plasmids from pathogenic avian Escherichia coli. Avian Dis 1992, 36, 348–352, doi:10.2307/1591510.
  78. Shivaprashad, HL. Pullorum disease and fowl typhoid. In Diseases of Poultry, 10th ed; Calnek, BW, Barnes, HJ, Beard, CW, McDoughald, LR, Saif, YM, Eds.; Iowa State University press: Ames, IA, USA, 1997; pp. 82–96.
  79. Minor, L. Bergey’s Manual of Systemic Bacteriology; Boone, R, Castenholz, W, Eds.; Williams & Wilkins: Philadelphia, PA, USA, 1984; pp. 427–458.
  80. Gast, RK. Paratyphoid Infections. In Diseases of Poultry, 10th ed; Calnek, BW, Barnes, HJ, Beard, CW, McDoughald, LR, Saif, YM, Eds.; Iowa State University press: Ames, IA, USA, 1997; pp. 97–121.
  81. Brito, JR; Xu, Y; Hinton, M; Pearson, GR. Pathological findings in the intestinal tract and liver of chicks after exposure to Salmonella serotypes Typhimurium or Kedougou. Br. Vet. J 1995, 151, 311–323, doi:10.1016/S0007-1935(95)80181-2.
  82. Berchieri, A, Jr; Murphy, CK; Marston, K; Barrow, PA. Observation on the persistence and vertical transmission Salmonella enterica serovars pullorum and gallinarum in chickens: Effect of bacterial and host genetic background. Avian Pathol 2001, 30, 221–231, doi:10.1080/03079450120054631.
  83. Shivaprasad, HL. Fowl typhoid and pullorum disease. Rev. Sci. Tech 2000, 19, 405–424.
  84. Christensen, JP. Phenotypic and genotypic characterization of Salmonella enterica serovar Gallinarum biovars gallinarum and pullorum in relation to typing and virulence. Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University: Copenhagen, Denmark, 1996.
  85. Hall, WJ; Legenhausen, DH; Macdonald, AD. Studies on fowl typhoid. 1. Nature and dissemination. Poult. Sci 1949, 28, 344–362, doi:10.3382/ps.0280344.
  86. Waltman, WD; Gast, RK; Mallinson, ET. Salmonellosis. In Isolation and Identification of Avian Pathogens, 5th ed. ed.; American Association of Avian Pathologists: Jacksonville, FL, USA, 2008; pp. 3–9.
  87. Henken, AM; Frankena, K; Goelema, JO; Graat, EAM; Noordhuizen, JPTM. Multivariate epidemiological approach to salmonellosis in broiler breeder flocks. Poult. Sci 1992, 71, 838–843, doi:10.3382/ps.0710838.
  88. Fris, C; van den Bos, J. A retrospective case-control study of risk factors associated with Salmonella enterica subsp. enterica serovar Enteritidis infections on Dutch broiler breeder farms. Avian Pathol 1995, 24, 255–272, doi:10.1080/03079459508419067.
  89. Oystein, A; Skov, MN; Chriel, M; Agger, JF; Bisgaard, M. A retrospective study on Salmonella infection in Danish broiler flocks. Prev. Vet. Med 1996, 26, 223–237, doi:10.1016/0167-5877(95)00549-8.
  90. Lahellec, C; Colin, P; Bennejean, G; Paquin, J; Guillerm, A; Debois, JC. Influence of resident Salmonella on contamination of broiler flocks. Poult. Sci 1986, 65, 2034–2039, doi:10.3382/ps.0652034.
  91. Baggesen, DL; Olsen, JE; Bisgaard, M. Plasmid profiles and phages types of Salmonella typhimurium isolated from successive flocks of chickens on three parent stock farms. Avian Pathol 1992, 21, 569–579, doi:10.1080/03079459208418878.
  92. Vaughn, JB; Williams, LP; LeBlanc, DR; Helsdon, HL; Taylor, C. Salmonella in a modern broiler operation: a longitudinal study. Am. J. Vet. Res 1974, 35, 737–741.
  93. Christensen, JP; Brown, DJ; Madsen, M; Olsen, JE; Bisgaard, M. Hatchery-borne Salmonella enterica serovar Tennessee infections in broilers. Avian Pathol 1997, 26, 155–168, doi:10.1080/03079459708419202.
  94. Davies, RH; Nicholas, RAJ; Mclaren, IM; Corkish, JD; Lanning, DG; Wray, C. Bacteriological and serological investigation of persistent Salmonella enteritidis infection in an integrated poultry organisation. Vet. Microbiol 1997, 58, 277–293, doi:10.1016/S0378-1135(97)00157-0.
  95. Martinetti, G; Altwegg, M. rRNA gene restriction patterns and plasmid analysis as a tool for typing Salmonella enteritidis. Res. Microbiol 1990, 141, 1151–1162, doi:10.1016/0923-2508(90)90088-8.
  96. Stubbs, AD; Hickman-Brenner, FW; Cameron, DN; Farmer, JJ, III. Differentiation of Salmonella enteritidis phage type 8 strains: evaluation of three additional phage typing systems, plasmid profiles, antibiotic susceptibility patterns, and biotyping. J. Clin. Microbiol 1994, 32, 199–201.
  97. Altwegg, M; Hinckman-Brenner, FW; Farmer, JJ, III. Ribosomal RNA gene patterns provide increased sensitivity for typing Salmonella typhi strains. J. Infect. Dis 1989, 160, 145–149, doi:10.1093/infdis/160.1.145.
  98. Esteban, E; Snipes, K; Hiird, D; Kasten, R; Kinde, H. Use of ribotyping for characterization of Salmonella serotypes. J. Clin. Microbiol 1993, 31, 233–237.
  99. Nastasi, A; Mammina, C; Villafrate, MR. rDNA fingerprinting as a tool in epidemiological analysis of Salmonella typhi infections. Epidemiol. Infect 1991, 107, 565–576, doi:10.1017/S0950268800049268.
  100. Usera, MA; Popovic, T; Bopp, CA; Stockbine, NA. Molecular subtyping of Salmonella enteritidis phage type 8 strain from the United States. J. Clin. Microbiol 1994, 32, 194–198.
  101. Olsen, JE; Skov, MN; Threlfall, EJ; Brown, DJ. Clonal lines of Salmonella enteritica serotype enteritidis documented by IS200-, ribo-, pulsed-field gel electrophoresis and RFLP typing. J. Med. Microbiol 1994, 40, 15–22, doi:10.1099/00222615-40-1-15.
  102. Thong, KL; Cheong, YM; Puthucheary, S; Koh, CL; Pang, T. Epidemiological analysis of sporadic Salmonella typhi isolates and those from outbreaks by pulsed-field gel electrophoresis. J. Clin. Microbiol 1994, 32, 1135–1141.
  103. Lapuz, R; Tani, H; Sasai, K; Shirota, K; Katoh, H; Baba, E. The role of roof rats (Rattus rattus) in the spread of Salmonella enteritidis and S. infantis contamination in layer farms in eastern Japan. Epidemiol Infect 2008, 136, 1235–1243.
  104. Barrow, PA; Berchieri, A, Jr; Al-Haddad, O. Serological response of chickens to infection with Salmonella gallinarum–Salmonella pullorum detected by enzyme linked immunosorbent assay. Avian Dis 1992, 36, 227–236, doi:10.2307/1591495.
  105. Bouzoubaa, K; Lemainguer, K; Bell, JG. Village chickens as a reservoir of Salmonella pullorum and Salmonella gallinarum in Morocco. Prev. Vet. Med 1992, 12, 95–100, doi:10.1016/0167-5877(92)90072-N.
  106. Bhattacharjee, PS; Kundu, RL; Mazumder, JU; Hossain, E; Miah, AH. A retrospective analysis of chicken diseases diagnosed at the Central Disease Investigation Laboratory, Dhaka, Bangladesh. Bangladesh Vet. Jr 1996, 30, 105–113.
  107. Begum, F; Khan, MSR; Choudhury, KA; Rahman, MM; Amin, MM. Studies on immune response of chickens to fowl typhoid vaccines. Bangladesh J. Microbiol 1993, 10, 51–56.
  108. Ghosh, SS. Incidence of pullorum disease in Nagaland. Indian Vet. J 1988, 65, 949–951.
  109. Kumur, A; Kaushik, RK. Investigation of fowl typhoid in Haryana State. Indian J. Poult. Sci 1988, 23, 104–106.
  110. Javed, T; Hameed, A. Prevalence of Salmonella carriers among broiler breeders in Pakistan. Veterinarski Arhiv 1989, 59, 185–191.
  111. Muneer, MA; Arshad, M; Sheikh, MA; Ahmad, MD. Identification of pullorum disease carriers using spot agglutination test. Pakistan Vet. J 1988, 8, 93–94.
  112. Jha, VC; Thakur, RP; Chand-Thakuri, K; Yadav, JN. Prevalence of salmonellosis in chickens in the eastern Nepal. Veterinary Review Kathmandu 1994, 9, 4–6.
  113. Fricker, CR. Isolation of Salmonella and Campylobacter. J. Appl. Bacteriol 1987, 63, 99–116, doi:10.1111/j.1365-2672.1987.tb02692.x.
  114. Okolo, MI. Bacterial drug resistance in meat animals: A review. Int. J. Zoonoses 1986, 13, 143–152.
  115. Vidon, DJ; Jacob, S; Ganzenmuller, M. Incidences of simple and transferable drug resistance in Escherichia coli and Salmonella isolated from various foods: Identification of a R plasmid in S. Saint-Paul. Ann. Microbiol 1978, 129, 155–159.
  116. O’Brien, TF; Hopkins, JD; Gilleece, ES; Mederios, AA; Kent, RL; lackburn, BO; Holmes, MB; Reardon, JP; Vergeront, JM; Schell, WL; Christenson, E; Bissett, ML; Morse, EV. Molecular epidemiology of antibiotic resistance in Salmonella from animals and human beings in the United States. N. Engl. J. Med 1982, 307, 1–6, doi:10.1056/NEJM198207013070101.
  117. Holmberg, SD; Osterholm, MT; Senger, KA; Cohen, ML. Drug-resistant Salmonella from animals fed antimicrobials. N. Engl. J. Med 1984, 311, 617–622, doi:10.1056/NEJM198409063111001.
  118. Poppe, C; Gyles, CL. Relation of plasmids to virulence and other properties of salmonellae from avian sources. Avian Dis 1987, 31, 844–854, doi:10.2307/1591041.
  119. Schuman, JD; Zottola, EA; Harlander, SK. Preliminary characterization of a food-borne multiple antibiotic resistant Salmonella typhimurium strain. Appl. Environ. Microbiol 1989, 55, 2344–2348.
  120. Salyers, AA; Whitt, DD. Antibiotics: mechanisms of action and mechanisms of bacterial resistance. In Bacterial Pathogenesis: A Molecular Approach; ASM Press: Washington, DC, USA, 1994; pp. 97–110.
  121. Poppe, C; McFadden, KA; Demczuk, WH. Drug resistance, plasmids, biotypes and susceptibility to bacteriophages of Salmonella isolated from poultry in Canada. Int. J. Food Microbiol 1996, 30, 325–344, doi:10.1016/0168-1605(96)00960-9.
  122. Wagner, J; Hahn, H. Increase of bacterial resistance in human medicine by resistance genes of bacteria from meat supplying animals. Berl. Munch. Tierarztl. Wochenschr 1999, 112, 380–384.
  123. Holmberg, SD; Osterholm, MT; Senger, KA; Cohen, ML. Drug-resistant Salmonella from animals fed antimicrobials. N. Eng. J. Med 1984, 311, 617–622, doi:10.1056/NEJM198409063111001.
  124. Gast, RK; Stephens, JF. Effects of kanamycin administration to poultry on the proliferation of drug-resistant Salmonella. Poult. Sci 1988, 67, 689–698, doi:10.3382/ps.0670689.
  125. Gast, RK; Stephens, JF; Foster, DN. Effects of kanamycin administration to poultry on the interspecies transmission of drug-resistant Salmonella. Poult. Sci 1988, 67, 699–706, doi:10.3382/ps.0670699.
  126. Dubel, JR; Zink, DL; Kelley, LM; Naqi, SA; Renshaw, HW. Bacterial antibiotic resistance: frequency of gentamicin-resistant strains of Escherichia coli in the faecal microflora of commercial turkeys. Am. J. Vet. Res 1982, 43, 1786–1789.
  127. Hirsh, DC; Ikeda, JS; Martin, LD; Kelley, BJ; Ghazikhanian, GY. R plasmid-mediated gentamicin resistance in salmonellae isolated from turkeys and their environment. Avian Dis 1983, 27, 766–772, doi:10.2307/1590320.
  128. Ekperigin, HE; Jang, S; McCapes, RH. Effective control of a gentamicin resistant Salmonella arizonae infection in turkey poults. Avian Dis 1983, 27, 822–829, doi:10.2307/1590326.
  129. Pacer, RE; Spika, JS; Thurmond, MC; Hargrett-Bean, N; Potter, ME. Prevalence of Salmonella and multiple antimicrobial-resistant Salmonella in California dairies. J. Am. Vet. Med. Assoc 1989, 195, 59–63.
  130. Poppe, C; Kolar, JJ; Demczuk, WHB; Harris, JE. Drug resistance and biochemical characteristics of Salmonella from Turkeys. Can. J. Vet. Res 1995, 59, 241–248.
  131. Oliveira, WF; Cardoso, WM; Salles, RPR; Romão, JM; Teixeira, RSC; Câmara, SR; Siqueira, AA; Marques, LCL. Initial identification and sensitivity to antimicrobial agents of Salmonella sp. isolated from poultry products in the state of Ceara, Brazil. Rev. Bras. Cienc. Avic 2006, 8, 193–199.
  132. Berrang, ME; Ladely, SR; Simmons, M; Fletcher, DL; Fedorka-Cray, PJ. Antimicrobial resistance patterns of Salmonella from retail chicken. Int. J. Poult. Sci 2006, 5, 351–354, doi:10.3923/ijps.2006.351.354.
  133. Parveen, S; Taabodi, M; Schwarz, JG; Oscar, TP; Harter-Dennis, J; White, DG. Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. J. Food Prot 2007, 70, 2466–2472.
  134. Sharma, M; Katock, RC. Deadly outbreak in chicks owing to Salmonella typhimurium. Indian J. Poult. Sci 1996, 31, 60–62.
  135. Herikstad, H; Hayes, P; Mokhtar, M; Fracaro, ML; Threlfall, EJ; Angulo, FJ. Emerging quinolone-resistant Salmonella in the United States. Emerg. Infect. Dis 1997, 3, 371–372, doi:10.3201/eid0303.970316.
  136. Manie, T; Khan, S; Brozel, VS; Veith, WJ; Gouws, PA. Antimicrobial resistance of bacteria isolated from slaughtered and retail chickens in South Africa. Lett. Appl. Microbiol 1998, 26, 253–258, doi:10.1046/j.1472-765X.1998.00312.x.
  137. Dho-Moulin, M; van den Bosch, JF; Girardeau, JP; Bree, A; Barat, T; Lafont, JP. Surface antigens from Escherichia coli O2 and O78 strains of avian origin. Infect. Immun 1990, 58, 740–745.
  138. Dozois, CM; Fairbrother, JM; Harel, J; Bosse, M. Pap-and pil-related DNA sequences and other virulence determinants associated with Escherichia coli isolated from septicemic chickens and turkeys. Infect. Immun 1992, 60, 2648–2656.
  139. van den Bosch, JF; Hendriks, JH; Gladigau, I; Willems, HM; Storm, PK; de Graaf, FK. Identification of F11 fimbriae on chicken Escherichia coli strains. Infect. Immun 1993, 61, 800–806.
  140. Pourbakhsh, SA; Dho-Moulin, M; Bree, A; Desautels, C; Martineau-Doize, B; Fairbrother, JM. Localization of the in vivo expression of P and F1 fimbriae in chickens experimentally inoculated with pathogenic Escherichia coli. Microb. Pathog 1997, 22, 331–341, doi:10.1006/mpat.1996.0116.
  141. Maurer, JJ; Lee, MD; Lobsinger, C; Brown, T; Maier, M; Thayer, SG. Molecular typing of avian Escherichia coli isolates by random amplification of polymorphic DNA. Avian Dis 1998, 42, 431–451, doi:10.2307/1592670.
  142. Foley, SL; Horne, SM; Giddings, CW; Robinson, M; Nolan, LK. Iss from a virulent avian Escherichia coli. Avian Dis 2000, 44, 185–191, doi:10.2307/1592523.
  143. Dho-Moulin, M; Fairbrother, JM. Avian pathogenic Escherichia coli (APEC). Vet. Res 1999, 30, 299–316.
  144. Ellis, MG; Arp, LH; Lamont, SJ. Serum resistance and virulence of Escherichia coli isolated from turkeys. Am. J. Vet. Res 1988, 49, 2034–2037.
  145. Pfaff-McDonough, SJ; Horne, SM; Giddings, CW; Ebert, JO; Doetkott, C; Smith, MH; Nolan, LK. Complement resistance-related traits among Escherichia coli isolates from apparently healthy birds and birds with colibacillosis. Avian Dis 2000, 44, 23–33, doi:10.2307/1592504.
  146. Lafont, JP; Dho, M; d'Hauteville, HM; Brée, A; Sansonetti, PJ. Presence and expression of aerobactin genes in virulent avian strains of Escherichia coli. Infect. Immun 1987, 55, 193–197.
  147. Reingold, J; Starr, N; Maurer, J; Lee, MD. Identification of a new Escherichia coli She haemolysin homolog in avian E. coli. Vet. Microbiol 1999, 66, 125–134, doi:10.1016/S0378-1135(98)00310-1.
  148. Provence, DL; Curtiss, R, III. Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect. Immun 1994, 62, 1369–1380.
  149. Bree, A; Dho, M; Lafont, JP. Comparative infectivity of axenic and specific pathogen free chickens of O2 E. coli strains with or without virulence factors. Avian Dis 1989, 33, 134–139, doi:10.2307/1591078.
  150. Emery, DA; Nagaraja, KV; Shaw, DP; Newman, JA; White, DG. Virulence factors of Escherichia coli associated with colisepticemia in chickens and turkeys. Avian Dis 1992, 36, 504–511, doi:10.2307/1591741.
  151. Blanco, JE; Blanco, M; Mora, A; Blanco, J. Production of toxins (enterotoxins, verotoxins, and necrotoxins) and colicins by Escherichia coli strains isolated from septicemic and healthy chickens: relationship with in vivo pathogenicity. J. Clin. Microbiol 1997, 35, 2953–2957.
  152. Parreira, VR; Yano, T. Cytotoxin produced by Escherichia coli isolated from chickens with swollen head syndrome (SHS). Vet. Microbiol 1998, 62, 111–119, doi:10.1016/S0378-1135(98)00197-7.
  153. Chaffer, M; Heller, ED; Schwartsburd, B. Relationship between resistance to complement, virulence and outer membrane protein patterns in pathogenic Escherichia coli O2 isolates. Vet. Microbiol 1999, 64, 323–332, doi:10.1016/S0378-1135(98)00278-8.
  154. Truscott, RB; Lopez-Alvarez, J; Pettit, JR. Studies of Escherichia coli infection in chickens. Can. J. comp. Med 1974, 38, 160–167.
  155. Hughes, LA; Bennett, M; Coffey, P; Elliott, J; Jones, TR; Jones, RC; Lahuerta-Marin, A; McNiffe, K; Norman, D; Williams, NJ; Chantrey, J. Risk factors for the occurrence of Escherichia coli virulence genes eae, stx1 and stx2 in wild bird populations. Epidemiol. Infect 2009, 137, 1574–82, doi:10.1017/S0950268809002507.
  156. Morley, AJ; Thomson, DK. Swollen-head syndrome in broiler chickens. Avian Dis 1984, 28, 238–243, doi:10.2307/1590147.
  157. Picault, JP; Giraud, P; Drouin, P; Guittet, M; Bennejean, G; Lamande, J; Toquin, D; Gueguen, C. Isolation of a TRTV-like virus from chickens with swollen-head syndrome. Vet. Rec 1987, 121, 135.
  158. Hafez, HM; Löhren, U. Swollen head syndrome: clinical observations and serology in West Germany. Deutsche Tierärztliche Wochenschrift 1990, 97, 322–324.
  159. Nakamura, K; Mase, M; Tanimura, N; Yamaguchi, S; Yuasa, N. Attempts to reproduce swollen head syndrome in specific pathogen-free chickens by inoculating with Escherichia coli and/or turkey rhinotracheitis virus. Avian Pathol 1998, 27, 21–27, doi:10.1080/03079459808419270.
  160. Georgiades, G; Iordanidis, P; Koumbati, M. Cases of swollen head syndrome in broiler chickens in Greece. Avian Dis 2001, 45, 745–750, doi:10.2307/1592922.
  161. Tsuji, T; Joya, JE; Honda, T; Miwatani, T. A heat-labile enterotoxin (LT) purified from chicken enterotoxigenic Escherichia coli is identical to porcine LT. FEMS Microbiol. Lett 1990, 55, 329–332.
  162. Akashi, N; Hitotsubashi, S; Yamanaka, H; Fujii, Y; Tsuji, T; Miyama, A; Joya, JE; Okamoto, K. Production of heat-stable enterotoxin II by chicken clinical isolates of Escherichia coli. FEMS Microbiol. Lett 1993, 109, 311–316.
  163. Dho-Moulin, M; Fairbrother, JM. Avian pathogenic Escherichia coli (APEC). Vet. Res 1999, 30, 299–316.
  164. Zanella, A; Alborali, GL; Bardotti, M; Candotti, P; Guadagnini, PF; Anna Martino, P; Stonfer, M. Severe Escherichia coli O111 septicemia and polyserositis in hens at the start of lay. Avian Pathol 2000, 29, 311–317, doi:10.1080/03079450050118430.
  165. Kariuki, S; Gilks, C; Kimari, J; Muyodi, J; Getty, B; Hart, CA. Carriage of potentially pathogenic Escherichia coli in chickens. Avian Dis 2002, 46, 721–724, doi:10.1637/0005-2086(2002)046[0721:COPPEC]2.0.CO;2.
  166. Guy, JS; Smith, LG; Breslin, JJ; Vaillancourt, JP; Barnes, HJ. High mortality and growth depression experimentally produced in young turkeys by dual infection with enteropathogenic Escherichia coli and turkey coronavirus. Avian Dis 2000, 44, 105–113, doi:10.2307/1592513.
  167. Bisgaard, M; Dam, A. Salpingitis in poultry. I. Prevalence, bacteriology and possible pathogenesis in broilers. Nordisk Veterinaermedicin 1980, 32, 361–368.
  168. Bisgaard, M; Dam, A. Salpingitis in poultry. I. Prevalence, bacteriology and possible pathogenesis in egg-laying chickens. Nordisk Veterina ermedicin 1981, 33, 81–89.
  169. Harry, EG. The survival of E. coli in the dust of poultry houses. Vet. Rec 1964, 76, 466–470.
  170. Goren, E. Colibacillose bij pluimvee: etiologie, pathologie en therapie. Tijdschrift voor Diergeneeskunde 1991, 116, 1122–1129.
  171. Norton, RA; Macklin, KS; McMurtrey, BL. The association of various isolates of Escherichia coli from the United States with induced cellulitis and colibacillosis in young broiler chickens. Avian Pathol 2000, 29, 571–574, doi:10.1080/03079450020016814.
  172. Leitner, G; Heller, ED. Colonization of Escherichia coli in young turkeys and chickens. Avian Dis 1992, 36, 211–220, doi:10.2307/1591493.
  173. Gross, WB. Electrocardiographic changes in Escherichia coli infected birds. Am. J. Vet. Res 1966, 27, 1427–1436.
  174. Dho-Moulin, M. Les Escherichia coli pathogènes des volailles. Annales de Médecine Vétérinair 1993, 137, 353–357.
  175. Humbert, F; Salvat, G. The risk of transmission of salmonellae in poultry farming: Detection and prevention in Europe. Rev. Sci. Tech 1997, 16, 83–90.
  176. Barrow, PA; Huggins, MB; Lovell, MA. Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect. Immun 1994, 62, 4602–4610.
  177. Barrow, PA. Salmonella control- past, present and future. Avian Pathol 1993, 22, 651–669, doi:10.1080/03079459308418954.
  178. Henderson, SC; Bounous, DI; Lee, MD. Early events in the pathogenesis of avian salmonellosis. Infect. Immun 1999, 67, 3580–3586.
  179. Lowry, VK; Tellez, GI; Nisbet, DJ; Garcia, G; Urquiza, O; Stanker, LH; Kogut, MH. Efficacy of Salmonella enteritidis-immune lymphokines on horizontal transmission of S. arizonae in turkeys and S. gallinarum in chickens. Int. J. Food Microbiol 1999, 48, 139–148, doi:10.1016/S0168-1605(99)00036-7.
  180. Gomis, SM; Watts, T; Riddell, C; Potter, AA; Allan, BJ. Experimental reproduction of Escherichia coli cellulitis and septicemia in broiler chickens. Avian Dis 1997, 41, 234–240, doi:10.2307/1592464.
  181. Gross, WB; Domermuth, CH. Colibacillosis. In Isolation and Identification of Avian Pathogens; Hitchner, SB, Domermuth, CH, Purchase, HG, Williams, JE, Eds.; Arnold Printing Corporation: New York, NY, USA, 1975; pp. 34–37.
  182. Leitner, G; Melamed, D; Drabkin, N; Heller, ED. An enzyme-linked immunosorbent assay for detection of antibodies against Escherichia coli: association between indirect hemagglutination test and survival. Avian Dis 1990, 34, 58–62, doi:10.2307/1591334.
  183. Bell, CJ; Finlay, DA; Clarke, HJ; Taylor, MJ; Ball, HJ. Development of a sandwich ELISA and comparison with PCR for the detection of F11 and F165 fimbriated Escherichia coli isolates from septicemic disease in farm animals. Vet. Microbiol 2002, 85, 251–257, doi:10.1016/S0378-1135(01)00514-4.
  184. Kles, V; Morin, M; Humbert, F; Lalande, F; Guittet, M; Bennejean, G. Serologic diagnosis of avian salmonelloses: Adjustment of an ELISA test using antigens adsorbed with the aid of anti-colibacillary sera. Zentralbl Veterinarmed B 1993, 40, 305–325.
  185. Szmolka, A; Kaszanyitzky, E; Nagy, B. Improved diagnostic and real-time PCR in rapid screening for Salmonella in the poultry food chain. Acta. Vet. Hung 2006, 54, 297–312, doi:10.1556/AVet.54.2006.3.1.
  186. Weinack, OM; Snoeyenbos, GH; Smyser, CF; Soerjadi, AS. Competitive exclusion intestinal colonization of Escherichia coli in chicks. Avian Dis 1981, 25, 696–705, doi:10.2307/1590000.
  187. La Ragione, RM; Casula, G; Cutting, SM; Woodward, MJ. Bacillus subtilis spores competitively exclude Escherichia coli O78:K80 in poultry. Vet. Microbiol 2001, 79, 133–142, doi:10.1016/S0378-1135(00)00350-3.
  188. Hofacre, CL; Johnson, AC; Kelly, BJ; Froyman, R. Effect of a commercial competitive exclusion culture on reduction of colonization of an antibiotic-resistant pathogenic Escherichia coli in day-old broiler chickens. Avian Dis 2002, 46, 198–202, doi:10.1637/0005-2086(2002)046[0198:EOACCE]2.0.CO;2.
  189. Kabir, SML; Rahman, MM; Rahman, MB; Hosain, MZ; Akand, MSI; Das, SK. Viability of probiotics in balancing intestinal flora and effecting histological changes of crop and caecal tissues of broilers. Biotechnology 2005, 4, 325–330, doi:10.3923/biotech.2005.325.330.
  190. Kabir, SML. The Role of probiotics in the poultry industry. Int. J. Mol. Sci 2009, 10, 3531–3546, doi:10.3390/ijms10083531.
  191. Melamed, D; Leitner, G; Heller, ED. A vaccine against avian colibacillosis based on ultrasonic inactivation of Escherichia coli. Avian Dis 1991, 35, 17–22, doi:10.2307/1591289.
  192. Heller, ED; Leitner, G; Drabkin, N; Melamed, D. Passive immunisation of chicks against Escherichia coli. Avian Pathol 1990, 19, 345–354, doi:10.1080/03079459008418685.
  193. Gyimah, JE; Panigrahy, B; Williams, JD. Immunogenicity of an Escherichia coli multivalent pilus vaccine in chickens. Avian Dis 1986, 30, 687–689, doi:10.2307/1590569.
  194. Pomery, BS; Nagaraja, KV. Fowl typhoid. In Diseases of Poultry, 9th ed; Calnek, BW, Barnes, HJ, Beard, CW, Reid, WM, Yoder, HW, Jr, Eds.; Wolfe publishing Ltd: London, UK, 1991; pp. 87–99.
  195. Christensen, JP; Skov, MN; Hinz, KH; Bisgaard, M. Salmonella enterica serovar Gallinarum biovar gallinarum in layers: epidemiological investigations of a recent outbreak in Denmark. Avian Pathol 1994, 23, 489–501, doi:10.1080/03079459408419019.
  196. Wray, C; Davies, RH; Corkish, JD. Enterobacteriaceae. In Poultry Diseases, 4th ed; Jordan, TW, Pattison, M, Eds.; W. B. Saunders: Philadelphia, PA, USA, 1996; pp. 9–43.
  197. Caya, F; Fairbrother, JM; Lessard, L; Quessy, S. Characterization of the risk to human health of pathogenic Escherichia coli isolates from chicken carcasses. J. Food Prot 1999, 62, 741–746.
  198. Czirók, E; Dho, M; Herpay, M; Gadó, I; Milch, H. Association of virulence markers with animal pathogenicity of Escherichia coli in different models. Acta Microbiol. Hungarica 1990, 37, 207–217.
  199. Chapman, PA; Siddons, CA; Gerdan Malo, AT; Harkin, MA. A 1-year study of Escherichia coli O157 in cattle, sheep, pigs and poultry. Epidemiol. Infect 1997, 119, 245–250, doi:10.1017/S0950268897007826.
  200. Stavric, S; Buchanan, B; Gleeson, TM. Intestinal colonization of young chicks with Escherichia coli O157:H7 and other verotoxin-producing serotypes. J. Appl. Bacteriol 1993, 74, 557–563.
  201. Doyle, MP; Schoeni, JL. Isolation of Escherichia coli O157:H7 from retail fresh meats and poultry. Appl. Environ. Microbiol 1987, 53, 2394–2396.
  202. Radu, S; Ling, OW; Rusul, G; Karim, MI; Nishibuchi, M. Detection of Escherichia coli O157:H7 by multiplex PCR and their characterization by plasmid profiling, antimicrobial resistance, RAPD and PWWFGE analyses. J. Microbiol. Methods 2001, 46, 131–139, doi:10.1016/S0167-7012(01)00269-X.
  203. Manges, AR; Smith, SP; Lau, BJ; Nuval, CJ; Eisenberg, JN; Dietrich, PS; Riley, LW. Retail meat consumption and the acquisition of antimicrobial resistant Escherichia coli causing urinary tract infections: A case-control study. Foodborne Pathog. Dis 2007, 4, 419–431, doi:10.1089/fpd.2007.0026.
  204. Yan, S; Pendrak, M; Abela-Ridder, B; Punderson, J; Fedorko, D; Foley, S. An overview of Salmonella typing public health perspectives. Clin. Applied Immunol. Rev 2003, 4, 189–204.
Table Table 1. ExPEC/APEC genes used in virulence genotyping*.

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Table 1. ExPEC/APEC genes used in virulence genotyping*.
GeneDescriptionReference
pTJ100-related genes
cvaC+Structural gene for the colicin V operon[50]
iroN±Catecholate siderophore receptor gene[51]
iss+Increased serum survival gene[52,53]
iucC±Involved in aerobactin synthesis[54,55]
iutA±Ferric aerobactin receptor gene; iron transport[55]
sitA±Putative iron transport gene[56]
traT+Outer membrane protein gene; surface exclusion; serum resistance[57,58]
tshTemperature-sensitive hemagglutinin gene[59]
Iron-Related
feoBGene which mediates ferric iron uptake[56]
ireAEncodes an iron-responsive element;[60]
putative sideropohore receptor gene
irp-2Iron repressible gene associated with yersiniabactin synthesis[61]
Toxins
hlyDTransport gene of the hemolysin operon[62]
Miscellaneous
fliC (H7)Produces-flagellin protein associated with the H7 antigen group[63]

*Descriptions of genes encoding components of certain adhesins (i.e., genes encoding parts of the P pilus, papA; papC; papEF; papG, including papG alleles I, II, and III; the S pilus, sfa and the gene encoding the S fimbrial tip, sfaS; the Type 1 fimbrial adhesin, fimH; the F1C fimbrial tip, focG; and other genes encoding portions of miscellaneous adhesins, iha; afa; gafD; and bmaE); toxins (cnf-1 and cdtB); protectins (kpsMT K1; kpsMT II; kpsMT III; and rfc); siderophores (fyuA); and other miscellaneous structures (ibeA; ompT; and PAI(CFT073), a fragment from archetypal UPEC strain CFT073) can be found in Johnson and co-workers [64]. Also, the description of papG allele I’ can be found in Johnson and Stell [65].+ These genes are listed as pTJ100-related, but they could also be listed as protectins.± These genes are listed as pTJ100-related, but they could also be listed with the iron-related genes.≠ These genes are listed as pTJ100-related, but they also could be listed in the miscellaneous group.

Table Table 2. A list of risk factors responsible for Salmonella contamination of broiler-chicken flocks.

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Table 2. A list of risk factors responsible for Salmonella contamination of broiler-chicken flocks.
Risk factorsReference
Inadequate level of hygiene[87,88]
Salmonella contamination of the previous flock with a persistence inside the house[89,90] [91]
Contaminated day-old chicks and feed[89,9294]
The farm structure (>3 houses on the farm)[89]
Wet and cold season[89]
Litter-beetle infestation of the house[91]
Table Table 3. A list of virulence factors contributing to the pathogenesis of avian colibacillosis.

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Table 3. A list of virulence factors contributing to the pathogenesis of avian colibacillosis.
Virulence facorsReference
F (type 1) and P fimbrial adhesins[137140]
Curli[141,142]
Factors contributing to adhesion, resistance to immunologic defense, survival in physiologic fluids, and cytotoxic effects[143]
Factors conferring resistance to serum and phagocytosis[138,140,144,145]
Aerobactin siderophores[138,146]
hylE, a hemolysin gene[147]
The tsh gene encoding temperature sensitive hemagglutinin[141,148]
K1 Capsular antigen[149]
Cytotoxins[150152]
Outer membrane proteins[153]
Coligenicity[151]
The heat-labile chick lethal toxin (CLT)[154]
Verotoxin-2 like toxin[152]
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