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Avian Colibacillosis and Salmonellosis: A Closer Look at Epidemiology, Pathogenesis, Diagnosis, Control and Public Health Concerns

S. M. Lutful Kabir

International Journal of Environmental Research and Public Health · 2010 · Review · CC BY

doi:10.3390/ijerph7010089

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.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 18, 2026. Paragraph numbers are ours, so an answer can point at one.

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. 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. Avian salmonella infection may occur in poultry either acute or chronic form by one or more member of genus Salmonella, under the family Enterobacteriaceae. 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. Infectious bursal disease (IBD), mycoplasmosis, coccidiosis, Newcastle disease or infectious bronchitis, as well as nutritional deficiencies all predispose the birds to this disease. 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. The birds that survive from clinical disease when infected at a young stage may show few signs of infection but can become carriers.

At slaughter, resistant strains from the gut readily soil poultry carcasses and as a result poultry meats are often contaminated with multiresistant E. coli; likewise eggs become contaminated during laying. 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. 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.

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. Poultry meat is more popular in the consumer market because of advantages such as easy digestibility and acceptance by the majority of people. 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.

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. 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. 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%).

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. 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. 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. Moreover, rodents may be carriers of APEC and hence a source of contamination for the birds.

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. 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.

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. Other techniques such as ERIC–PCR and REP–PCR and random amplification of polymorphic DNA (RAPD)–PCR have been proposed as alternatives and used to characterize Escherichia coli isolates of avian origin. Other molecular techniques such as ribotyping and isoenzyme profile have also been used to evaluate the clonality of avian E. coli. 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. On the other hand, clonal relationships were found for O2:K1 isolates from humans and chickens and for O78 isolates from humans, cattle, sheep, pigs and chickens, 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, the isolates are very heterogenous, both in their pheno- and genotype. On the other hand, the prevalence of certain serotypes is linked with the geographical localisation of a flock.

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. 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, tetracyclines, chloramphenicol, sulfonamides, amino-glycosides and β-lactam antibiotics. Resistance to fluoroquinolones was reported within several years of the approval of this class of drugs for use in poultry. There is reason for concern that genes conferring resistance to extended-spectrum beta-lactams will emerge in avian pathogenic E. coli strains 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. Multiple antimicrobial resistance traits of avian pathogenic E. coli have also been associated with transmissible R-plasmids.

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. 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. In addition to S. gallinarum-pullorum, other salmonellae such as S. enteritidis, S. panama and S. dublin also belong to the serogroup D1. The various motile and non-host adapted highly invasive serotypes such as Salmonella enteritidis and Salmonella typhimurium are commonly referred to as paratyphoid salmonellae. 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.

Various routes of infection have been described. Oral route of infection represents the normal route of infection. 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. 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.

Although more than 2,300 serotypes of Salmonella have been identified, only about 10% of these have been isolated from poultry. 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. 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. 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. S. gallinarum can produce lesions in chicks, which are indistinguishable from those associated with pullorum disease. A certain percentage of chickens that survive from the initial infection become carriers with or without presence of clinical signs and pathological lesions. Crowding, malnutrition, and other stressful conditions as well as unsanitary surroundings can exacerbate mortality and performance losses due to salmonellosis, especially in young birds. 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, ribotyping, and PFGE have proved to be useful in discriminating isolates of Salmonella species. Lapuz et al. 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. They are mainly distributed in Latin America, the Middle East, the Indian subcontinent, Africa and perhaps other parts of the world. Salmonellosis has also been reported in many countries of South-East Asia including Bangladesh, India, Pakistan and Nepal. Fowl typhoid is common in both backyard chickens and in commercial poultry.

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. These mechanisms involve transfer of drug resistant genes by means of circular DNA plasmids such as R-factor, conjugative plasmid, or chromosomal elements. 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, the practice of dipping hatching eggs in solutions containing antimicrobial agents, routine inoculation of day-old poults with antibiotics and treatment of other animals and humans with antibiotics. Salmonella strains of avian origin are also often resistant to variety of antimicrobials approved for poultry including tetracycline, oxytetracycline, penicillin, aminoglycosides, sulfisoxazole and fluoroquinolones. On the other hand, Manie et al. found several strains of multiple antibiotic-resistant Salmonella strains in chicken.

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. 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. 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. Broilers may be affected by necrotic dermatitis, also known as cellulitis, characterized by a chronic inflammation of the subcutis on abdomen and thighs.

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%. Data on this disease are contradictory. Picault et al. and Hafez & Löhren considered SHS as a disease caused by avian pneumovirus (APV), usually followed by an opportunistic E. coli infection. Nakamura et al. 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., 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 and diarrhoea was experimentally induced after intramuscular inoculation of APEC. On the other hand, enteropathogenic E. coli (EPEC) were isolated from clinically healthy chickens. In turkeys, experimentally inoculated EPEC can only cause enteritis in combination with coronavirus.

Layers as well as broilers may suffer from acute or chronic salpingitis. Salpingitis can be the result of an ascending infection from the cloaca or an infection of the left abdominal airsac, although Bisgaard and Dam considered the latter possibility less likely than an ascending infection. Salpingitis can lead to the loss of egg-laying capacity. In the case of chronic salpingitis, the oviduct has a yellowish-gray, cheese-like content, with a concentric structure. 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.

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. This aerogenic route of infection is considered as the main origin of systemic colibacillosis or colisepticemia.

Septicemia also affects chickens of all ages, and is mainly described in broilers. It is the most prevalent form of colibacillosis, characterised by polyserositis. It causes depression, fever and often high mortality. Although its pathogenesis has not been elucidated, several routes of infection are possible: neonatal infections, infections through skin lesions, infection of the reproductive organs, of the respiratory tract and even infection per os. When E. coli reaches the vascular system, the internal organs and the heart are infected. The infection of the myocard causes heart failure. Septicemia occasionally also leads to synovitis and osteomyelitis and on rare occasions to panophthalmia. 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.

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.

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. 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. 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. 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. Pullorum disease manifests itself predominantly as an enteric disease of chickens, while fowl typhoid shows signs of septicemic disease. 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. S. gallinarum is extremely pathogenic to young broiler chicks.

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

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. Contamination from the intestines is rarely a problem, if fresh material is used and standard bacteriological procedures are applied. 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). 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. Another ELISA was based on fimbrial antigen. 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. Szmolka et al. 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.

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. 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), 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 and protecting the birds against mycoplasmas and viral diseases by vaccinations. Disease introduction must also be avoided 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. The housing climate must be kept optimal for bird density, humidity, ventilation, dust and ammonia.

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. However, Melamed et al. 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, 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.

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. Successful control programs can be achieved by developing good hygiene and management together with routine serological tests and slaughter policy. 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. 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. Wray et al. 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. Kabir et al. and Kabir 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.

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. Cherifi et al. 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.. 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. Although O157 verotoxigenic E. coli (VTEC) had been detected in broilers, 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. The study by Stavric et al. 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. 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. In addition, Manges et al. 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.

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.

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.

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.

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.

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    Jayaratne A Collins-Thompson DL Trevors JT Occurrence of aminoglycoside phosphotransferase subclass I and II structural genes among Enterobacteriaceae spp. isolated from meat samplesAppl. Microbiol. Biotechnol1990 33547552

    Not in our library10.1007/bf00172549

  14. 14.

    Turtura GC Massa S Chazvinizadeh H Antibiotic resistance among coliform bacteria isolated from carcasses of commercially slaughtered chickensInt. J. Food Microbiol1990 11351354

    Not in our library10.1016/0168-1605(90)90029-5

  15. 15.

    Lakhotia RL Stephens JF Drug resistance and R factors among enterobacteria isolated from eggsPoult. Sci1973 5219551962

    Not in our library10.3382/ps.0521955

  16. 16.

    van den Bogaard E London N Driessen C Stobberingh EE Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterersJ. Antimicrob. Chemother2001 47763771

    Not in our library10.1093/jac/47.6.763

  17. 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 1998J. Antimicrob. Chemother2001 47315321

    Not in our library10.1093/jac/47.3.315

  18. 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 BelgiumActa Clin. Belg2001 56180186

    Not in our library10.1179/acb.2001.028

  19. 19.

    Wybot I Wildemauwe C Godard C Bertrand S Collard JM Antimicrobial drug resistance in nontyphoid human Salmonella in Belgium: Trends for the period 2000–2002Acta Clin. Belg2004 59152160

    Not in our library10.1179/acb.2004.022

  20. 20.

    Mulder RW Hygiene during transport, slaughter and processingPoultry Meat Science Poultry Science Symposium SeriesRichardson RI Mead GC CABI PublishingOxford shire, UK1999 277285

    Not in our library

  21. 21.

    Yashoda KP Sachindra NM Sakhare PZ Rao DN Microbiological quality of broiler chicken carcasses processed hygienically in a small scale poultry processing unitJ. Food Qual2001 24249259

    Not in our library

  22. 22.

    Barnes HJ Gross WB ColibacillosisDiseases of Poultry10th edCalnek BW Barnes HJ Beard CW McDougald LR Saif YM Iowa State University PressAmes, IA, USA1997 131141

    Not in our library

  23. 23.

    La Ragione RM Woodward MJ Virulence factors of Escherichia coli serotypes associated with avian colisepticemiaRes. Vet. Sci2002 732735

    Not in our library10.1016/s0034-5288(02)00075-9

  24. 24.

    Gross WB Diseases due to Escherichia coli in poultryEscherichia coli in Domestic Animals and HumansGyles CL CAB International LibraryWallingford, UK1994 237260

    Not in our library

  25. 25.

    Chart H Smith HR La Ragione RM Woodward MJ An investigation into the pathogenic properties of Escherichia coli strains BLR, BL21, DH5α, and EQ1J. Appl. Microbiol2000 8910481058

    Not in our library10.1046/j.1365-2672.2000.01211.x

  26. 26.

    Rahman MA Samad MA Rahman MB Kabir SML Bacterio-pathological studies on salmonellosis, colibacillosis and pasteurellosis in natural and experimental infections in chickensBangl. J. Vet. Med2004 218

    Not in our library

  27. 27.

    Harry EG Hemsley LA The relationship between environmental contamination with septicemia strains of Escherichia coliVet. Rec1965 77241245

    Not in our library

  28. 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 septicemiaVet. Rec1965 773540

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  29. 29.

    Dho-Moulin M Fairbrother JM Avian pathogenic Escherichia coli (APEC)Vet. Res1999 30299316

    Not in our library

  30. 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 diseasesPoult. Sci1980 59205210

    Not in our library10.3382/ps.0590205

  31. 31.

    Rosenberger JK Fries PA Cloud SS Wilson RA In vitro and in vivo characterization of avian Escherichia coli. II. Factors associated with pathogenicityAvian Dis1985 2910941107

    Not in our library

  32. 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 erythrocytesAm. J. Vet. Res1992 53291293

    Not in our library

  33. 33.

    Pourbakhsh SA Boulianne M Martineau-Doizé B Dozois CM Desautels C Fairbrother JM Dynamics of Escherichia coli infection in experimentally inoculated chickensAvian Dis1997 41221233

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  34. 34.

    McGruder ED Moore GM Use of lipopolysaccharide (LPS) as a positive control for the evaluation of immunopotentiating drug candidates in experimental avian colibacillosis modelsRes. Vet. Sci1998 663337

    Not in our library10.1053/rvsc.1998.0237

  35. 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)–PCRVet. Microbiol2002 89323328

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  36. 36.

    Gilson E Clément JM Brutlag D Hofnung M A family of dispersed repetitive extragenic palindromic DNA sequences in Escherichia coliEMBO J1984 314171421

    Not in our library10.1002/j.1460-2075.1984.tb01986.x

  37. 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 enterobacteriaMol. Microbiol1991 5825834

    Not in our library10.1111/j.1365-2958.1991.tb00755.x

  38. 38.

    Welsh J McClelland M Fingerprinting genomes using PCR with arbitrary primersNucleic Acids Res1990 1872137218

    Not in our library10.1093/nar/18.24.7213

  39. 39.

    Chansiripornchai N Ramasoota P Sasipreyajan J Svenson SB Differentiation of avian Escherichia coli (APEC) isolates by random amplified polymorphic DNA (RAPD) analysisVet. Microbiol2001 807783

    Not in our library10.1016/s0378-1135(00)00380-1

  40. 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 reationAvian Dis2001 45173181

    Not in our library

  41. 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 analysisJ. Vet. Med. B Infect. Dis. Vet. Public Hlth2003 506369

    Not in our library10.1046/j.1439-0450.2003.00607.x

  42. 42.

    White DG Dho-moulin M Wilson RA Whittam TS Clonal relationships and variation in virulence among Escherichia coli strains of avian originMicrob. Pathog1993 14399409

    Not in our library10.1006/mpat.1993.1039

  43. 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 animalsInfect. Immun1986 51268276

    Not in our library10.1128/iai.51.1.268-276.1986

  44. 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 infectionsJ. Clin. Microbiol1994 3211971202

    Not in our library10.1128/jcm.32.5.1197-1202.1994

  45. 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 pathogenicityJ. Clin. Microbiol1997a 3529532957

    Not in our library10.1128/jcm.35.11.2953-2957.1997

  46. 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 reactionAvian Dis2001 45173181

    Not in our library

  47. 47.

    Ewers C Janßen T Kießling S Philipp HC Wieler LH Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultryVet. Microbiol2004 10491101

    Not in our library10.1016/j.vetmic.2004.09.008

  48. 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. Microbiol1998 61229235

    Not in our library10.1016/s0378-1135(98)00182-5

  49. 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 colibacillosisMicrobiology2005 15120972110

    Not in our library10.1099/mic.0.27499-0

  50. 50.

    Gilson L Mahanty HK Kolter R Four plasmid genes are required for colicin V synthesis, export, and immunityJ. Bacteriol1987 16924662470

    Not in our library10.1128/jb.169.6.2466-2470.1987

  51. 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 urineInfect. Immun1999 6753065314

    Not in our library10.1128/iai.67.10.5306-5314.1999

  52. 52.

    Binns MM Davies DL Hardy KG Cloned fragments of the plasmid ColV, I-K94 specifying virulence and serum resistanceNature1979 279778781

    Not in our library10.1038/279778a0

  53. 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 DNAMol. Gen. Genet1989 216287292

    Not in our library10.1007/bf00334367

  54. 54.

    de Lorenzo V Neilands JB Characterization of iucA and iucC genes of the aerobactin system of plasmid ColV-K30 in Escherichia coliJ. Bacteriol1986 167350355

    Not in our library10.1128/jb.167.1.350-355.1986

  55. 55.

    de Lorenzo V Bindereif A Paw BH Neilands JB Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12J. Bacteriol1986 165570578

    Not in our library10.1128/jb.165.2.570-578.1986

  56. 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 cellsInfect. Immun2003 7119191928

    Not in our library10.1128/iai.71.4.1919-1928.2003

  57. 57.

    Achtman M Kennedy N Skurray R Cell–cell interactions in conjugating Escherichia coli: Role of TraT protein in surface exclusionProc. Natl. Acad. Sci. USA1977 7451045108

    Not in our library10.1073/pnas.74.11.5104

  58. 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 coliInfect. Immun1980 28359367

    Not in our library10.1128/iai.28.2.359-367.1980

  59. 59.

    Provence DL Curtiss R III Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strainInfect. Immun1994 6213691380

    Not in our library10.1128/iai.62.4.1369-1380.1994

  60. 60.

    Russo TA Carlino UB Johnson JR Identification of a new iron-regulated virulence gene, ireA, in an extraintestinal pathogenic isolate of Escherichia coliInfect. Immun2001 6962096216

    Not in our library10.1128/iai.69.10.6209-6216.2001

  61. 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 humansInfect. Immun1998 66480485

    Not in our library10.1128/iai.66.2.480-485.1998

  62. 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 pathogenicityBacteria, Complement and the Phagocytic CellCabello FC Pruzzo C Springer-VerlagNew York, NY, USA1988 221229

    Not in our library

  63. 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:NMJ. Clin. Microbiol1997 3510661070

    Not in our library10.1128/jcm.35.5.1066-1070.1997

  64. 64.

    Johnson JR Delavari P Kuskowski M Stell AL Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coliJ. Infect. Dis2001 1837888

    Not in our library10.1086/317656

  65. 65.

    Johnson JR Stell AL Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromiseJ. Infect. Dis2000 181261272

    Not in our library10.1086/315217

  66. 66.

    Rahman MA Samad MA Rahman MB Kabir SML In vitro antibiotic sensitivity and therapeutic efficacy of experimental salmonellosis, colibacillosis and pasteurellosis in broiler chickensBangl. J. Vet. Med2004 299102

    Not in our library

  67. 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 sensitivityAvian Dis1985 2910841093

    Not in our library

  68. 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 chickensCan. J. Vet. Res1989 53411418

    Not in our library

  69. 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 SpainJ. Clin. Microbiol1997 3521842185

    Not in our library10.1128/jcm.35.8.2184-2185.1997

  70. 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 coliAntimicrob. Agents Chemother1999 4329252929

    Not in our library10.1128/aac.43.12.2925

  71. 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 chickensJ. Vet. Sci2007 8243247

    Not in our library10.4142/jvs.2007.8.3.243

  72. 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 turkeysAm. J. Vet. Res1982 4317861789

    Not in our library

  73. 73.

    Allan BJ van den Hurk JV Potter AA Characterization of Escherichia coli isolated from cases of avian colibacillosisCan. J. Vet. Res1993 57146151

    Not in our library

  74. 74.

    White DG Piddock LJ Maurer JJ Zhao S Ricci V Thayer SG Characterization of fluoroquinolone resistance among veterinary isolates of avian Escherichia coliAntimicrob. Agents Chemother2000 4428972899

    Not in our library10.1128/aac.44.10.2897-2899.2000

  75. 75.

    van den Bogaard AE London N Driessen C Stobberingh EE Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterersJ. Antimicrob. Chemother2001 47763771

    Not in our library10.1093/jac/47.6.763

  76. 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 meatsAntimicrob. Agents Chemother2001 4536473650

    Not in our library10.1128/aac.45.12.3647-3650.2001

  77. 77.

    Wooley RE Spears KR Brown J Nolan LK Dekich MA Characteristics of conjugative R plasmids from pathogenic avian Escherichia coliAvian Dis1992 36348352

    Not in our library

  78. 78.

    Shivaprashad HL Pullorum disease and fowl typhoidDiseases of Poultry10th edCalnek BW Barnes HJ Beard CW McDoughald LR Saif YM Iowa State University pressAmes, IA, USA1997 8296

    Not in our library

  79. 79.

    Minor L Bergey’s Manual of Systemic BacteriologyBoone R Castenholz W Williams & WilkinsPhiladelphia, PA, USA1984 427458

    Not in our library

  80. 80.

    Gast RK Paratyphoid InfectionsDiseases of Poultry10th edCalnek BW Barnes HJ Beard CW McDoughald LR Saif YM Iowa State University pressAmes, IA, USA1997 97121

    Not in our library

  81. 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 KedougouBr. Vet. J1995 151311323

    Not in our library10.1016/s0007-1935(95)80181-2

  82. 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 backgroundAvian Pathol2001 30221231

    Not in our library10.1080/03079450120054631

  83. 83.

    Shivaprasad HL Fowl typhoid and pullorum diseaseRev. Sci. Tech2000 19405424

    Not in our library10.20506/rst.19.2.1222

  84. 84.

    Christensen JP Phenotypic and genotypic characterization of Salmonella enterica serovar Gallinarum biovars gallinarum and pullorum in relation to typing and virulencePh.D. Thesis, Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University Copenhagen, Denmark1996

    Not in our library

  85. 85.

    Hall WJ Legenhausen DH Macdonald AD Studies on fowl typhoid. 1. Nature and disseminationPoult. Sci1949 28344362

    Not in our library

  86. 86.

    Waltman WD Gast RK Mallinson ET SalmonellosisIsolation and Identification of Avian Pathogens5th ed.American Association of Avian PathologistsJacksonville, FL, USA2008 39

    Not in our library

  87. 87.

    Henken AM Frankena K Goelema JO Graat EAM Noordhuizen JPTM Multivariate epidemiological approach to salmonellosis in broiler breeder flocksPoult. Sci1992 71838843

    Not in our library10.3382/ps.0710838

  88. 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 farmsAvian Pathol1995 24255272

    Not in our library10.1080/03079459508419067

  89. 89.

    Oystein A Skov MN Chriel M Agger JF Bisgaard M A retrospective study on Salmonella infection in Danish broiler flocksPrev. Vet. Med1996 26223237

    Not in our library

  90. 90.

    Lahellec C Colin P Bennejean G Paquin J Guillerm A Debois JC Influence of resident Salmonella on contamination of broiler flocksPoult. Sci1986 6520342039

    Not in our library10.3382/ps.0652034

  91. 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 farmsAvian Pathol1992 21569579

    Not in our library10.1080/03079459208418878

  92. 92.

    Vaughn JB Williams LP LeBlanc DR Helsdon HL Taylor C Salmonella in a modern broiler operation: a longitudinal studyAm. J. Vet. Res1974 35737741

    Not in our library

  93. 93.

    Christensen JP Brown DJ Madsen M Olsen JE Bisgaard M Hatchery-borne Salmonella enterica serovar Tennessee infections in broilersAvian Pathol1997 26155168

    Not in our library10.1080/03079459708419202

  94. 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 organisationVet. Microbiol1997 58277293

    Not in our library10.1016/s0378-1135(97)00157-0

  95. 95.

    Martinetti G Altwegg M rRNA gene restriction patterns and plasmid analysis as a tool for typing Salmonella enteritidisRes. Microbiol1990 14111511162

    Not in our library10.1016/0923-2508(90)90088-8

  96. 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 biotypingJ. Clin. Microbiol1994 32199201

    Not in our library10.1128/jcm.32.1.199-201.1994

  97. 97.

    Altwegg M Hinckman-Brenner FW Farmer JJ III Ribosomal RNA gene patterns provide increased sensitivity for typing Salmonella typhi strainsJ. Infect. Dis1989 160145149

    Not in our library10.1093/infdis/160.1.145

  98. 98.

    Esteban E Snipes K Hiird D Kasten R Kinde H Use of ribotyping for characterization of Salmonella serotypesJ. Clin. Microbiol1993 31233237

    Not in our library10.1128/jcm.31.2.233-237.1993

  99. 99.

    Nastasi A Mammina C Villafrate MR rDNA fingerprinting as a tool in epidemiological analysis of Salmonella typhi infectionsEpidemiol. Infect1991 107565576

    Not in our library10.1017/s0950268800049268

  100. 100.

    Usera MA Popovic T Bopp CA Stockbine NA Molecular subtyping of Salmonella enteritidis phage type 8 strain from the United StatesJ. Clin. Microbiol1994 32194198

    Not in our library10.1128/jcm.32.1.194-198.1994

  101. 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 typingJ. Med. Microbiol1994 401522

    Not in our library10.1099/00222615-40-1-15

  102. 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 electrophoresisJ. Clin. Microbiol1994 3211351141

    Not in our library10.1128/jcm.32.5.1135-1141.1994

  103. 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 JapanEpidemiol Infect2008 13612351243

    Not in our library10.1017/s095026880700948x

  104. 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 assayAvian Dis1992 36227236

    Not in our library

  105. 105.

    Bouzoubaa K Lemainguer K Bell JG Village chickens as a reservoir of Salmonella pullorum and Salmonella gallinarum in MoroccoPrev. Vet. Med1992 1295100

    Not in our library

  106. 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, BangladeshBangladesh Vet. Jr1996 30105113

    Not in our library

  107. 107.

    Begum F Khan MSR Choudhury KA Rahman MM Amin MM Studies on immune response of chickens to fowl typhoid vaccinesBangladesh J. Microbiol1993 105156

    Not in our library

  108. 108.

    Ghosh SS Incidence of pullorum disease in NagalandIndian Vet. J1988 65949951

    Not in our library

  109. 109.

    Kumur A Kaushik RK Investigation of fowl typhoid in Haryana StateIndian J. Poult. Sci1988 23104106

    Not in our library

  110. 110.

    Javed T Hameed A Prevalence of Salmonella carriers among broiler breeders in PakistanVeterinarski Arhiv1989 59185191

    Not in our library

  111. 111.

    Muneer MA Arshad M Sheikh MA Ahmad MD Identification of pullorum disease carriers using spot agglutination testPakistan Vet. J1988 89394

    Not in our library

  112. 112.

    Jha VC Thakur RP Chand-Thakuri K Yadav JN Prevalence of salmonellosis in chickens in the eastern NepalVeterinary Review Kathmandu1994 946

    Not in our library

  113. 113.

    Fricker CR Isolation of Salmonella and CampylobacterJ. Appl. Bacteriol1987 6399116

    Not in our library10.1111/j.1365-2672.1987.tb02692.x

  114. 114.

    Okolo MI Bacterial drug resistance in meat animals: A reviewInt. J. Zoonoses1986 13143152

    Not in our library

  115. 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-PaulAnn. Microbiol1978 129155159

    Not in our library

  116. 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 StatesN. Engl. J. Med1982 30716

    Not in our library10.1056/nejm198207013070101

  117. 117.

    Holmberg SD Osterholm MT Senger KA Cohen ML Drug-resistant Salmonella from animals fed antimicrobialsN. Engl. J. Med1984 311617622

    Not in our library10.1056/nejm198409063111001

  118. 118.

    Poppe C Gyles CL Relation of plasmids to virulence and other properties of salmonellae from avian sourcesAvian Dis1987 31844854

    Not in our library

  119. 119.

    Schuman JD Zottola EA Harlander SK Preliminary characterization of a food-borne multiple antibiotic resistant Salmonella typhimurium strainAppl. Environ. Microbiol1989 5523442348

    Not in our library10.1128/aem.55.9.2344-2348.1989

  120. 120.

    Salyers AA Whitt DD Antibiotics: mechanisms of action and mechanisms of bacterial resistanceBacterial Pathogenesis: A Molecular ApproachASM PressWashington, DC, USA1994 97110

    Not in our library

  121. 121.

    Poppe C McFadden KA Demczuk WH Drug resistance, plasmids, biotypes and susceptibility to bacteriophages of Salmonella isolated from poultry in CanadaInt. J. Food Microbiol1996 30325344

    Not in our library10.1016/0168-1605(96)00960-9

  122. 122.

    Wagner J Hahn H Increase of bacterial resistance in human medicine by resistance genes of bacteria from meat supplying animalsBerl. Munch. Tierarztl. Wochenschr1999 112380384

    Not in our library

  123. 123.

    Holmberg SD Osterholm MT Senger KA Cohen ML Drug-resistant Salmonella from animals fed antimicrobialsN. Eng. J. Med1984 311617622

    Not in our library10.1056/nejm198409063111001

  124. 124.

    Gast RK Stephens JF Effects of kanamycin administration to poultry on the proliferation of drug-resistant SalmonellaPoult. Sci1988 67689698

    Not in our library10.3382/ps.0670689

  125. 125.

    Gast RK Stephens JF Foster DN Effects of kanamycin administration to poultry on the interspecies transmission of drug-resistant SalmonellaPoult. Sci1988 67699706

    Not in our library10.3382/ps.0670699

  126. 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 turkeysAm. J. Vet. Res1982 4317861789

    Not in our library

  127. 127.

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  173. 173.

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  178. 178.

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  180. 180.

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    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 seraZentralbl Veterinarmed B1993 40305325

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    Not in our library

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    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 chickensAvian Dis2002 46198202

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    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 broilersBiotechnology2005 4325330

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  190. 190.
    The Role of Probiotics in the Poultry Industry · 2009
    No notice
  191. 191.

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    Not in our library

  192. 192.

    Heller ED Leitner G Drabkin N Melamed D Passive immunisation of chicks against Escherichia coliAvian Pathol1990 19345354

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  193. 193.

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    Not in our library

  194. 194.

    Pomery BS Nagaraja KV Fowl typhoidDiseases of Poultry9th edCalnek BW Barnes HJ Beard CW Reid WM Yoder HW Jr Wolfe publishing LtdLondon, UK1991 8799

    Not in our library

  195. 195.

    Christensen JP Skov MN Hinz KH Bisgaard M Salmonella enterica serovar Gallinarum biovar gallinarum in layers: epidemiological investigations of a recent outbreak in DenmarkAvian Pathol1994 23489501

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  196. 196.

    Wray C Davies RH Corkish JD EnterobacteriaceaePoultry Diseases4th edJordan TW Pattison M W. B. SaundersPhiladelphia, PA, USA1996 943

    Not in our library

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  200. 200.

    Stavric S Buchanan B Gleeson TM Intestinal colonization of young chicks with Escherichia coli O157:H7 and other verotoxin-producing serotypesJ. Appl. Bacteriol1993 74557563

    Not in our library

  201. 201.

    Doyle MP Schoeni JL Isolation of Escherichia coli O157:H7 from retail fresh meats and poultryAppl. Environ. Microbiol1987 5323942396

    Not in our library10.1128/aem.53.10.2394-2396.1987

  202. 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 analysesJ. Microbiol. Methods2001 46131139

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    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 studyFoodborne Pathog. Dis2007 4419431

    Not in our library10.1089/fpd.2007.0026

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    Yan S Pendrak M Abela-Ridder B Punderson J Fedorko D Foley S An overview of Salmonella typing public health perspectivesClin. Applied Immunol. Rev2003 4189204

    Not in our library

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