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Human campylobacteriosis: A public health concern of global importance

Aboi Igwaran, Anthony Ifeanyi Okoh

Heliyon · 2019 · Review · CC BY

doi:10.1016/j.heliyon.2019.e02814

Abstract

outbreaks, prevention and treatment option, antibiotics resistance and control of antibiotics use.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 19, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Campylobacter belong to a distinct group of specialized bacteria designated rRNA superfamily VI of Class Proteobacteria. Campylobacter species are slender Gram-negative rod-shaped, spiral-shaped with single or pair of flagella. Some Campylobacter species have multiple flagella such as C. showae while some species are non-motile like C. gracilis. Campylobacter species are indole negative, oxidase positive, hippurate positive, catalase positive, nitrate positive and glucose utilization negative. Campylobacter species are closely related group of bacteria that principally colonise the gastrointestinal tracts of different animals. Campylobacter species are enormous significance due to the increase in number of species implicated in animals and human's infections. Since its first identification, the number of pathogenic Campylobacter species that causes animal and human infections are largely classified through phylogenetic means with few as 500–800 bacteria ingestion dose resulting to human disease. Nonetheless, report has shown that Campylobacter doses of 100 cells or less have been linked with human infections. The major infection caused by Campylobacter is mainly acute diarrhea and since 1977, Campylobacter species have been known as the major causative agent of acute diarrhea. Campylobacter species have also been reported to be implicated in various human systemic infections including septic thrombophlebitis, endocarditis, neonatal sepsis, pneumonia, bloodstream infections (BSIs), acute colitis of inflammatory bowel disease and acute appendicitis. Other major post-infections that significantly add to Campylobacter disease burden include severe demyelinating neuropathy, Guillain-Barré syndrome (GBS), sequelae and Miller-Fisher syndrome (MFS). Campylobacter species are also associated with series of gastrointestinal infections like colorectal cancer and Barrett's esophagus. In small group of patients, Campylobacter species have also been reported to be associated with extragastrointestinal infections such as brain abscesses, meningitis, lung infections, bacteremia and reactive arthritis.

Campylobacter is a significant zoonotic causes of bacterial food-borne infection and farm animals are the major reservoir of Campylobacter species and the major cause of campylobacteriosis. Worldwide, farm animals are also the major cause of both bacteria food poisoning and Campylobacter foodborne gastrointestinal infections. Campylobacter foodborne infection is a problem and an economic burden to human population which caused about 8.4% of the global diarrhea cases. Campylobacter foodborne infection is a global concern because of the emerging Campylobacter species involved in both human infections and Campylobacter foodborne outbreaks. Campylobacter foodborne outbreak is defined as Campylobacter infection that involve more than two or more persons as a result of consumption of Campylobacter contaminated foods. Majority of campylobacteriosis cases are not recognized as outbreaks rather as sporadic episode involving a single family group. Campylobacteriosis is a collective name of infections caused by pathogenic Campylobacter species and is characterized by fever, vomiting, watery or bloody diarrhea. In general, Campylobacter infections are predominantly common in certain age group such as children (below 4) and the aged (above 75). Other group of people at high risk of Campylobacter infections are immunocompromised individuals, hemoglobinopathies patients and those suffering from inflammatory bowel disease. In addition, the risks of Campylobacter infections are higher in high income nations than in low income nations. In low income nations, a number of environmental sources pose a high risks of human Campylobacter infections; and most outbreaks are caused by consumption of poultry meats and poultry products. Poultry meats include meats from laying hens, turkeys, ostriches, ducks and broilers, and poultry meats and it product cause about 60–80% of the global campylobacteriosis cases.

Campylobacter species

Campylobacter species are divided into Lior serotypes and penner serotypes and over 100 Lior serotypes and 600 penner serotypes have been reported. Among these Lior serotypes and penner serotypes, only the thermotolerant Campylobacter species have been reported to have clinical significance.

Pathogenic Campylobacter species

Worldwide, pathogenic Campylobacter species are responsible for the cause of over 400–500 million infections cases each year. Pathogenic Campylobacter species known to be implicated in human infections includes C. jejuni, C. concisus, C. rectus, C. hyointestinalis, C. insulaenigrae, C. sputorum, C. helveticus, C. lari, C. fetus, C. mucosalis, C. coli, C. upsaliensis and C. ureolyticus. These pathogenic Campylobacter species are grouped into major human enteric pathogens (C. jejuni, C. jejuni subsp. jejuni (Cjj), C. jejuni subsp. doyley (Cjd), C. coli and C. fetus); minor pathogens (C. concisus, C. upsaliensis, C. lari and C. hyointestinalis) and major veterinary pathogens (C. fetus subsp. venerealis (Cfv) and C. fetus subsp. fetus (Cff)).

C. jejuni

C. jejuni is a motile, microaerophilic, zoonotic, thermophilic bacterial considered as the leading cause of worldwide foodborne bacterial gastroenteritis. It's a member of the genus Campylobacter with polar flagella and helical morphology that is used for movement through viscous solutions including the mucus layer of the gastrointestinal tract. C. jejuni is the major enteric pathogen that displays significant strain-to-strain dissimilarities in their pathogenicity patterns. C. jejuni is the major species that caused infections than other pathogenic Campylobacter species and also the major Campylobacter species that regularly cause diarrhea in human. Infections caused by C. jejuni can develop into diverse severities such as mild and self-limiting diarrhea to hemorrhagic colitis and sometimes to meningitis and bacteremia. C. jejuni infections are also associated with many secondary complications such as autoimmune neuropathy, and inflammatory bowel disease (IBD). C. jejuni is the major Campylobacter species that cause disease in young people. C. jejuni infections can occur via various routes such as through direct contact with companion and farm animals or through waterborne or foodborne transmission. C. jejuni is a commensal bacterial of chickens which inhabit the chicken intestines at a level >106–108 CFU/g of chicken faeces and chickens are the main vector for human campylobacteriosis. C. jejuni consist of two subspecies; C. jejuni subsp. jejuni (Cjj) and C. jejuni subsp. doyley (Cjd). The main phenotypic feature generally used to differentiate Cjj from Cjd strain is the inability of C. jejuni subsp. doyley to reduce nitrate and also, Cjd is also associated with high susceptibility to cephalothin. Clinically, Cjd strain causes both enteritis and gastritis. C. jejuni subsp. jejuni (Cjj) is the main bacterial cause of enteroinvasive diarrhea and the major symptoms of C. jejuni infections include severe enteritis, severe abdominal cramps, fever and bloody diarrhea with mucus. In addition, C. jejuni has also been reported to be associated with immunoreactive complications like Miller-Fisher syndromes.

C. coli

Campylobacter coli is an S-shaped curved cell measuring about 0.2–0.5 micrometers long with a single flagellum. It's very similar to C. jejuni; and both bacteria cause inflammation of the intestine and diarrhea in humans. C. coli is the second most regularly reported Campylobacter species that causes human infections. C. coli is grouped into 3 clades (clade 1, 2 and 3). C. coli clade 1 includes most C. coli isolated from humans and farm animals. C. coli clade 1 causes most of human infections whereas infections cause by C. coli clade 2 and 3 are rare. In high income countries, report has shown that C. coli is the second most regular cause of campylobacteriosis. Also in high income countries, C. coli infections are usually sporadic and it show seasonal drifts with majority of the infections occurring in early fall or late summer. The clinical manifestations of C. coli infections include watery diarrhea, abdominal pain, vomiting, fever, inflammatory enterocolitis, malaise and nausea.

C. fetus

C. fetus is a curved cell, fastidious motile bacterial that majorly cause septic abortion in farm animals. C. fetus can cause infection in human and its infection can be acquired through direct contact with animals, through consumption of undercooked contaminated meat or through ingesting food or water contaminated by animal faeces. C. fetus is grouped into 3 subsp. which includes: C. fetus subsp. venerealis (Cfv), C. fetus subsp. testudinum (Cft) and C. fetus subsp. fetus (Cff). Cfv and Cff are associated with farm animal infections; while Cft has also been reported to be associated with human infection such as bacteremia. Cff and Cfv are categorized on the basis of their clinical manifestations and mechanisms of transmission. Cff caused abortion in infected sheep and cattle and it's an opportunistic human pathogen that largely infects immunecompromised patients. Cfv is reported to be cattle-restricted pathogen, but this species has been isolated from humans and most human infection caused by C. fetus strain is majorly caused by Cff. Some of the major reported symptoms of C. fetus infections include endocarditis, meningitis, septicemia, septic arthritis, peritonitis and cellulitis. C. fetus is sometimes responsible for human systemic infections like bloodstream infection in immunosuppressed and immunocompromised individuals, but infections are rare.

C. lari

Campylobacter lari was previously called Campylobacter laridis and is part of the thermotolerant Campylobacter species. C. lari is grouped into a genotypically and phenotypically diverse Campylobacter group that encompasses of the nalidixic-acid susceptible (NASC) group, nalidixic acid-resistant thermophilic Campylobacter, the urease-positive thermophilic Campylobacter and the urease-producing NASC. These aforementioned groups are all identified as variants of C. lari group. This C. lari group is made up of five Campylobacter species (C. subantarcticus, C. insulaenigrae, C. volucris, C. lari and C. peloridis) with other group of strains called UPTC and C. lari-like strains. Though, some of these strains formally identified as C. lari group were later classified as novel taxa such as C. volucris and C. peloridis. C. lari is a species within the genus Campylobacter and is grouped into two novel subsp. namely; C. lari subspe. concheus (Clc) and C. lari subsp. lari (Cll). In 1984, C. lari was first reported in immunocompromised patient and since then sporadic cases including water-borne C. lari outbreaks have been reported. C. lari has also been reported to be associated with enteritis, purulent pleurisy, bacteremia, urinary tract infection, reactive arthritis and prosthetic joint infection.

C. upsaliensis

Campylobacter upsaliensis is among the thermotolerant Campylobacter species and is mostly found in dogs and cats, regardless of whether the animal is sick or healthy. C. upsaliensis is the third most Campylobacter species after C. jejuni and C. coli. C. upsaliensis was named after the city it was first described and thereafter, reports have emerged globally associating this species as a human bacterial enteropathogen. C. upsaliensis is a well-known Campylobacter species that cause diarrhea in felines and canines. C. upsaliensis is well recognized as a clinically important emerging diarrhea pathogen in both pediatric and immunocompromised persons. It is one of the emerging Campylobacter species that is associated with human infections including Crohn's disease, neonatal infection, bacteremia, abscesses, meningitis and abortion. C. upsaliensis has also been reported to cause acute or chronic diarrhea in human and diarrhea in dogs though genetic studies have shown that Campylobacter strains isolated from dogs and human strains are different. In many nations, C. upsaliensis is the second reported Campylobacter species that cause infections in human after C. jejuni.

Other pathogenic Campylobacter species

Other pathogenic Campylobacter species implicated in human infections includes C. mucosalis, C. curvus, C. insulaenigrae, C. doylei, C. concisus, C. helveticus and C. rectus. Beside the well-known pathogenic species, other emerging species such as C. sputorum biovar sputorum, C. gracilis, C. ureolyticus, C. peloridis and C. showae, have also been reported to be implicated in causing human infections with some life-threatening complications in hospitalized patients. Some of these emerging Campylobacter species have also been isolated and detected in samples from the axillary nerve, soft tissue lesions, hepatic, lung, bone infections, the cerebrospinal, peritoneal fluid, genitalia, brain abscesses and thoracic empyema of hospitalized patients. In addition to these life-threatening complications caused by these emerging pathogens, there is a huge gap in tracing the connection between infection and source of human infection. Furthermore, even with the global incidence of Campylobacter species in causing infections, the knowledge of the epidemiology and pathogenesis are still incomplete.

Pathogenicity of Campylobacter species

Campylobacter species are of economic importance as they constantly cause foodborne infections due to diverse genes involved in its pathogenicity. Campylobacter pathogenicity is based on the virulence factors and these virulence factors are multi-factorial in nature and the ability of these bacteria to survival and resist physiological stress also contributes to its pathogenicity. The various virulence related mechanisms displayed by Campylobacter species includes invasive properties, oxidative stress defence, toxin production, iron acquisition and its ability to remain viable but non-culturable state. Campylobacter invasion, adherence and colonization also add to the pathogenicity of these groups of bacteria. Other virulence factors of Campylobacter include; secretion of some sets of proteins, translocation capabilities and flagella-mediated motility.

Motility and flagella

Motility is important for Campylobacter survival under diverse chemotactic conditions it comes across in the gastrointestinal tract. In some Campylobacter species, the motility system with the flagella involves a chemosensory system that steers flagella movement depending on the environmental conditions where these bacteria are found. Campylobacter chemotaxis and flagellin are the two important virulence factors that help lead these bacteria to its colonization site and also help in invading the host cell. Some of these Campylobacter motility virulence factors and their encoding genes are σ54 promoter regulates gene (flaB) and σ28 promoter regulates gene (flaA). The flaA gene appears to be significant for invasion, colonization of the host epithelial cells and adherence to the host gastrointestinal tracts. The flagellum is composed of structural extracellular filamentous components and a hook-basal body. The hook-basal body comprises of the following: (a) the surface localized hook, (b) the periplasmic rod and associated ring structures and (c) a base embedded in the cytoplasm and inner membrane of the cell. The hook-basal body is a complex component that is made up of a number of diverse proteins such as FliO, FlhA, FliG, FlhB, FliP, FliF, FliQ, FliR, FliY, FliM and FliN, FlgI, FlgH, FlgE, FliK, FlgE and FliK. The extracellular filament of the flagella is composed of multimers of the protein including flagellin protein (FlaA and FlaB), FlaA (coded by flaA gene), and FlaB (coded by flaB gene) which is the minor flagellin protein.

Chemotaxis

Chemotaxis is a method or system by which motile bacteria sense and move to the direction of more favourable conditions and several pathogenic bacteria uses this practice to invade their hosts. Campylobacter chemotaxis virulence factors involve in human infections includes chemotaxis proteins; Che A, B, R, V, W and Z encoded by cheA, cheB, cheR, cheV, cheW and cheZ genes, Methyl-accepting chemotaxis proteins encoded by tlp4, tlp and tlp1 genes, the CheY response regulator that is responsible for controlling flagella rotation encoded by cheY gene and Campylobacter energy taxis system proteins CetB (Aer2) and CetA (Tlp9) encoded by cetB and cetA gene.

Adhesion

Campylobacter adherence to epithelial cells of the host gastrointestinal tract is a precondition for its colonisation mediated by some adhesins on the bacterial surface. Campylobacter adhesion virulence factors includes outer membrane protein encoded by cadF gene, Campylobacter adhesion protein A encoded by capA gene, phospholipase A encoded by pldA gene, lipoprotein encoded by jlpA gene, periplasmic binding protein encoded by peb1A gene, fibronectin-like protein A encoded by flpA and Type IV secretion system encoded by virB11 gene. Campylobacter adhering to fibronectin F is another important Campylobacter virulence factor that enables these bacteria to bind to fibronectin which promotes the bacterium-host cell interactions and colonization. Other virulence genes in Campylobacter species reported to be linked with human infections responsible for expression of colonization and adherence include racR, dnaJ, docA and racR genes.

Toxin production

Campylobacter produce different type of cytotoxins and cytolethal distending toxin (CDT) is one of these toxins. CDT is a tripartite toxin that is made up of three subunits encoded by the cdtA, cdtB and cdtC genes. Cytolethal distending toxin activity is determined by these three cdt cluster genes. These three cdt cluster genes are all needed for these toxins to be active. The cdtA and C genes are heterodimeric toxin subunits responsible for toxin binding and internalization of the host cell while cdtB is the subunit which encodes for the toxic/active components of the toxin. Cytolethal distending toxins induce diarrhea in both humans and animals by intrusive with the division of cells in the intestinal crypts.

Invasion

Invasion is another virulence mechanism in Campylobacter that is carried out by the flagella which also function as an export apparatus in the secretion of non-flagella proteins during host invasion. There are many virulence genes that are involved in Campylobacter invasion mechanism and the products of these genes including flagellin C (flaC) and invasion antigens (cia) genes. These genes are transported into the host cell's cytoplasm with the aid of flagella secretion system which is vital for invasion and colonisation. The secretion of invasion antigens and invasion protein B (ciaB) are also important virulence proteins synthesized by Campylobacter species which help in the epithelial cells invasion and adhesion of the host gastrointestinal tract. Other important virulence genes and proteins synthesized by Campylobacter species including the 73-kDa protein involved in adhesion, the invasion antigen C protein involved in full invasion of INT-407 cells, invasion associated protein gene (iamA) implicated in invasion and virulence, the periplasmic protein HtrA responsible for full binding to the epithelial cells, the HtrA chaperone implicated in full folding of out outer membrane protein, the CiaI gene implicated in intracellular survival and pldA and hcp genes responsible for the expression of invasion.

Other virulence mechanism in Campylobacter species

Other virulence mechanism that adds to Campylobacter pathogenicity is the ability to obtain the necessary nutrient iron needed for its growth from the host body fluids and tissues. Sialyltransferases (cstII) activity also add to Campylobacter pathogenicity by providing lipooligosaccharide with a defensive barricade that help facilitates in the disruption of the epithelial cells which mimic the action of human ganglioside inducing diarrhea. The wlaN gene is implicated in lipopolysaccharide production. The spot gene is responsible for extreme control, the Kat A (catalase) responsible to convert H2O2 to H2O and O2, the cj0012c and cj1371 proteins genes implicated to protect against reactive oxygen species. The Peb4 chaperone is another virulence mechanism in Campylobacter that play a significant role in the exporting of proteins to the outer membrane. Other virulence genes responsible for stress response genes includes the cosR, cj1556, spoT, ppk1, csrA, nuoK and cprS and the cell surface modifications genes (waaF, pgp1 and peb4). All these aforementioned Campylobacter virulence-associated genes have all been reported to be implicated in human infections.

Campylobacter infections

Campylobacters are types of bacteria that majorly cause infections in the gastrointestinal tract. Campylobacter infections may be acquired through different means including consumption of unpasteurized milk, non-chlorinated/contaminated surface water and consumption of undercooked poultry or red meat. Campylobacter infections can also be acquired through direct contact with infected pets within the family environment. The clinical manifestations of Campylobacter infections are oftentimes impossible to differentiate from infections caused by Shigella and Salmonella. Campylobacter mechanisms of survival and infection is poorly understood but when colonized the ileum, jejunum and colon, it sometimes causes infection with or without symptoms. Fig. 1 is a schematic representation of the transmission cycle involve in Campylobacter infection.

Classification of Campylobacter infections

Campylobacter infection is a bacterial infection that commonly causes human gastroenteritis but infection can also occur outside the intestines. Campylobacter infections are classified into two categories namely; (i): Gastrointestinal infection (GI) and (ii): Extragastrointestinal infection.

Gastrointestinal infections

Gastrointestinal infection (GI) is the inflammation of the gastrointestinal tract involving both the small intestine and stomach. GI is generally characterized by diarrhea. Campylobacter is 1 of the 4 key global bacterial cause of gastrointestinal infections. It's also the major and regular cause of traveller's diarrhea and children diarrhea. Besides diarrhea, other gastrointestinal infections associated with different Campylobacter species are shown in Table 1.

Extragastrointestinal infections

Extragastrointestinal infections (EI) are infections outside the intestines but symptoms are associated with a problem within the intestine. Extragastrointestinal infections reported to be associated with Campylobacter infections includes reactive arthritis, GBS, bacteremia, septicaemia, septic arthritis, endocarditis, neonatal sepsis, osteomyelitis, and meningitis. In small number of cases, other extragastrointestinal post-infections associated with Campylobacter infections include severe neurological dysfunction, neurological disorders and a polio-like form of paralysis. Some Campylobacter species associated with extragastrointestinal infections are listed in Table 2.

Isolation and diognosis of Campylobacter infection

Isolation of Campylobacter species relied on culture-based methods which have helped to strongly ascertain its part in human infections. Campylobacter isolation involves a medium that uses antibiotics as selective agents. These antibiotics used differs from a single antibiotic including cefoperazone or cefazolin in modified CDA medium to a “cocktail” of polymixin B, trimethroprin and vancomycin found in Skirrow's medium. Campylobacter sensitivity to oxidizing radicals and O2 has led to the development of a number of selective media and selective agents for its isolation. Before the development of these culture media for Campylobacter isolation and detection, non-selective medium was previously used but the medium was less proper for isolation of campylobacters from environmental and animal samples. Owing to this problem, Bolton and Robertson in 1977 developed a selective Preston medium suitable for Campylobacter isolation from environmental and food samples. Several other selective broths and media latter developed for Campylobacter isolation includes Bolton broth, Preston broth and Campylobacter enrichment broth, modified charcoal cefoperazone deoxycholate agar (mCCDA), CampyFood agar (CFA) and broth, RAPID’Campylobacter agar, Campylobacter agar base (CAB) and Campylobacter Cefex agar. Campylobacter species are microaerobic, fastidious bacteria capable of growing in a temperature between 37 °C and 42 °C. Despite Campylobacter sensitivity to high temperature and low oxygen concentration, the actual procedures used by clinical laboratories in its isolation from human faecal specimens may vary in different countries. However, laboratory diagnosis of campylobacteriosis is usually carried out by culture-base technique or by rapid detection of Campylobacter antigen (Enzyme Immunoassay) in stool samples, body tissue or fluids of infected person to identify the genetic materials of this bacterial strain that shows similar symptoms with other bacteria pathogens.

Other method use for Campylobacter identification includes growth morphology, biochemical tests and some of these identification methods used are not unreliable. However, other molecular techniques have been designed as alternative and better diagnostic methods for identification. In 1992, application of polymerase chain reaction (PCR) was first used for specific detection of C. coli and C. jejuni, and PCR is widely used in the detection and identification of this bacterial to species level. In addition to PCR techniques, other molecular methods used for identification or detection of Campylobacter species include random amplified polymorphic DNA, whole-genome sequencing, matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF). Some of the challenges involved in Campylobacter isolation and identification includes difficult procedures for isolation and identification, suboptimal storage and loss of isolates during extensive freeze-thaw cycles which has raised concerns to the scientific community. Likewise, the presence of the “protective guard” in a community of multispecies biofilm could hide a wide range of emerging pathogenic Campylobacter species which can successfully “escape” adverse environments and regain its ability to cause infection when found in optimal conditions may lead to wrong results in the diagnosis process. Another serious challenge for public health concern in campylobacters identification and diagnosis is its ability to remain viable but nonculturable but retain its physiology and virulence ability. Lasstly, the laboratory diagnosis of Campylobacter infections caused by other pathogenic Campylobacter species except C. coli and C. jejuni is complex due to the challenging growth and identification processes of the several subsets of Campylobacter species.

Transmission routes of Campylobacter infection

Campylobacter species majorly colonized the intestine of poultry, European blackbirds, cattle, sheep, ostriches, cats, dogs and pigs. These bacteria are shed in the faeces of these animals into the environment. Campylobacter can also spread to person by direct contact to animals such as pets, with dog owners at high risk of Campylobacter infection. Beside pets, other domestic animals such as cattle are also regularly colonized by Campylobacter species and persons working with these animals are also at high risk of Campylobacter infection. Other sets of people at high risk of campylobacteriosis include farms and abattoirs workers who sometimes do not practice hand-washing and food safety habits. However, identification and understanding the transmission routes of Campylobacter infections is crucial for its prevention and control. The common and major route/pathways of campylobacteriosis includes through faecal-oral routes, through consumption of contaminated undercooked meats or through consumption of contaminated food/water. Fig. 2 is a schematic illustration of overview of the transmission routes of Campylobacter infection.

Milk as a route of Campylobacter transmission

Worldwide, there is a rise in the consumption of unpasteurized milk as a result of its health benefits compared to pasteurized milk. Despites the health benefits in the consumption of unpasteurized milk, there is a great concern to the health risk its pose to human. Milk is a white liquid and a nutrient-rich food produced in the mammary glands of mammals. It's a source of protein, dietary fats and minerals (calcium and magnesium) for growth particularly in children. Milk is consumed either unpasteurized or pasteurized and mammals that produced milk for human consumption includes sheep, buffalo, goats, cows, yak and camel and the highest proportions of commercially produced milks are from cows. Milk is considered germ-free when secreted in the alveoli of the udder. Fresh milk drawn from animals naturally possess a short lived antibacterial system that display ‘germicidal’ or ‘bacteriostatic’ properties but bacterial growth is inevitable after sometimes except it undergoes heat treatment or freezing. Milk is a good substrate for bacteria growth and it's reported to be among the major transmission routes for Campylobacter to humans. Milk is natural foods that has no protection against external contamination and can easily be contaminated when separated from it source. Milk contamination generally occurs from environmental sources such as water, grass, milking equipments, feed, air, teat apex, soil and other sources. It's believed that the occurrence of Campylobacter species in raw milk samples is from faecal contamination. Campylobacter species have been detected in cow milk ( et al., 2017), and different Campylobacter species that have been detected in milk samples from different mammals including C. Jejuni detected in buffalo and cow milk and C. coli identified in cow milk. Campylobacter species have also been detected in bulk tank milk where these milks are stored, and Campylobacter species reported to have been detected from milk samples from the bulk tank include C. lari, C. jejuni and C. coli. Globally, several cases of illness and deaths have been reported to occur via consumption of contaminated raw milk and its products, and in many countries, milk-borne pathogens are of public health concern.

Meat as a route of Camplobacter transmission

Worldwide, consumption of meats is steadily increasing and meats are sometimes contaminated with microorganisms but bacteria contaminations may sometimes occur from animal microbiota, equipment surfaces and water. The bacteria from animal's microbiota that majorly contaminate meats include pathogenic Salmonella and Campylobacter species and these two bacteria species are majorly responsible for human gastroenteritis as a result of consumption of contaminated undercooked meat. Campylobacter contamination remains the major cause of bacterial food-borne infection and the major reservoir of these bacteria species are poultry. Infections caused by poultry consumption represents about 50–70% of the global Campylobacter infections cases, and poultry is define as meats from chicken, turkey, duck and goose. Beside poultry, Campylobacter species have also been detected in other meat typss such as pork and beef, mutton and in camel, lamb and chevon. Campylobacter species that have been isolated and detected in meat samples include C. coli and C. jejuni identified in poultry meat, C. coli, C. lari, C. jejuni and C. fetus detected in mutton samples, and C. jejuni and C. coli detected in pork, beef and lamb. Isolation and detection of these bacteria species from meats samples position them as one of the major transmission route.

Water as a route of Campylobacter transmission

Worldwide, access to safe drinking water is one of the targets goals, but report from regular analysis of water samples have showed that unsafe drinking water remain the number eight leading risk factor for human disease. Studies have also showed that improved water sources including public taps/standpipes, protected dug wells, boreholes and protected springs are not automatically free of faecal contamination. In high income countries, water is sometimes contaminated through faulty pumps and pipes while in low income countries, majority of the people rely mostly on streams, lakes and other surface water sources for food preparation, washing clothes, drinking and these water are usually contaminated by human and animal faeces exacerbating the possibility of waterborne infections. Though, some environmental sources used for recreational purposes are often overlooked as a route of disease transmission. Water is an important route of Campylobacter transmission to humans resulting to waterborne infections and waterborne infections can involve several persons. Besides, Campylobacter infection via consumption of contaminated food/tap water, other water sources including dug well water have been reported to be implicated in Campylobacter outbreaks. Some of the reported pathogenic Campylobacter species detected in water samples from beach and river include C. coli, C. jejuni and C. lari. Other water sources where these bacteria have also been isolated includes ponds, streams, lakes, children's paddling pool, groundwater and seawater.

Epidemiological information of Campylobacter outbreaks

The reports in the incidences of Campylobacter outbreaks differs among countries and the true nature of the global occurrence rate is largely unknown. The reasons for lack of true incidences rate of Campylobacter outbreaks includes underreporting of Campylobacter infection cases, differences in the reporting systems, difficulties with diagnosis and differences in surveillance in case of outbreaks. Campylobacter outbreaks are usually either from waterborne or foodborne infection involving several persons, and majority of Campylobacter outbreaks are usually from animal origin. Although, in low income countries, Campylobacter outbreaks are majorly from environmental sources such as streams and river where many people depend on these water bodies as their major drinking water source. Beside involvement of water sources in human infection in low income countries, water sources have also been reported to be implicated in Campylobacter outbreaks in high income countries such as Norway, New Zealand, Canada, Finland and Denmark. Campylobacter milk borne infection and outbreaks have also been reported in several high and low income countries. Some of the countries with records of campylobacteriosis outbreaks including the Netherlands, Israel, China, Japan, India, Sweden, Mexico and the United States. Also, other nations where there have been records of Campylobacter outbreaks includes Canada, British Columbia, Australia, the United Kingdom, Belgium, Denmark, Germany, Norway, Poland, New Zealand, Madagascar, Malawi, Kenya, Iceland and Estonia, Guatemala and Peru. Fig. 3 is a map showing records of some reported cases of Campylobacter outbreaks in some countries of the world.

Prevention and treatment of Campylobacter infections

Prevention of Campylobacter infections can be directly applied to humans by different ways including sewage sanitary conditions, provision of portable water, vaccine usage, public awareness concerning the significance of pasteurization of milk, proper cooking of food from animal origins and the use of therapeutics in case of infections. Prevention of Campylobacter infections can also be directed on animals by phage treatment, probiotics, prebiotics, and by improved biosecurity such as the provision of good water quality at farm level and also by monitoring the regular use of antibiotics in animal husbandry. Another vital preventive measure that will help lower the level of these bacteria is the withholding of feed from poultry for about 12 h before slaughter. Campylobacter infections are sometimes self-limiting but in most cases fluid and electrolyte replacement are major supportive measures for the treatment of this infection. Beside fluid and electrolyte replacement, antibiotics are used when symptoms pesist and antibiotics treatments are most effective when started within three days after onset of illness. Nonetheless, antibiotics are regularly used in Campylobacter infected patients with diarrhea, high fever or patients with other severe illness like weakened immune systems, AIDS, thalassemia, and hypogammaglobulinemia. Antibiotics drugs of choice for the treatment of campylobacteriosis includes fluoroquinolones, aminoglycosides, tetracycline, macrolides, betalactams and erythromycin. Other useful alternative antibiotics drugs of choice include ciprofloxacin, vancomycin and quinolones.

Antibiotic resistance

Antibiotics use for the treatment of campylobacteriosis is significant for patients with prolonged or severe infections. Campylobacter resistance to vital antibiotics used in the treatments of Campylobacter infections is an emerging global burden and Campylobacter resistance to drugs of choice may limit the treatment options. The global spread of antibiotic-resistant Campylobacter strains is a contineous process due to the regular use of antibiotics in animal husbandary and this is a problem of public health concern. Other problems that add to the spread of Campylobacter resistance includes inability to completely remove these antibiotic-resistant bacteria during wastewater treatment process, inproper dumping of humans and animals waste into waterbodies and inappropriate preparation of food from animal origin. Antibiotic resistant bacteria is a global problem assocaited with increased healthcare cost, prolonged infections with a greater risk of hospitalization and high mortality risk and rate. Molecular detection of antibiotic resistance genes in Campylobacter species have helped in determining the resistance genes in Campylobacter species from animals and environmental origin. Molecular detection of antimicrobial resistance genes in Campylobacter originating from foods and water samples is a major public health concern of global importance. Some of the resistance genes detected in Campylobacter species includes quinolone resistance-genes (gyrA, gyrB and parC), FQ-resistant (parE), β-lactamase (blaOXA-61 and blaOX-184), tetracycline resistance genes (tetA, tetB, tetM, tetO and tetS), aminoglycoside resistance genes (aphA and aadE) and erythromycin resistance gene (ermB). Antibiotics resistance genes in Campylobacter are either acquired by spontaneous mutations or through horizontal gene transfer via transduction, conjugation and transformation. Other resistance mechanisms developed by Campylobacter against antimicrobials include genetic mutation, point mutation, decreased in membrane permeability due to MOMP and rRNA methylases. Resistance-nodulation-cell division efflux system, modification of ribosomal target sites and weakening of the interaction of the macrocyclic ring and the tunnel wall of the ribosome are also essential resistance mechanism developed in Campylobacter. Fig. 4 is a schematic illustration of the patterns implicated in the spread of antibiotic resistance genes.

Control of antibiotic use

The emergence of antibiotic-resistant Campylobacter strains has rise markedly in both developing and developed countries suggesting the use of antibiotics in animal husbandry as the source of the accelerating trend. Several countries have policy in the control of antibiotics use in animal production. However, multiples countries do not have policy in the control of antibiotics use for animal production. In addition, grain-based feeds and water are mostly supplemented with antibiotics and other drugs for animal production. In some countries that practise indiscriminate use of antimicrobial in animal production, new regulatory policy should be place on the use of antibiotic in animal husbandry for non-therapeutic reasons such as promoting weight gains of birds or improving feed efficiency. Owing to the increase in antibiotic-resistant Campylobacter strains, vaccine development is important and vaccination of birds against Campylobacter could help eradicate Campylobacter from birds and reduce the rate of incidence of human infections. Vaccine would also help to reduce high cost of post-harvest treatments. Nevertheless, the cost of Campylobacter infections treatment to public health systems is high thus the main motivation towards developing a Campylobacter vaccine would be to reduce the high costs of treatment associated with campylobacteriosis, enhance food safety and reduce potential human health risks. Presently, there are no vaccines approved by any global governing authority to prevent Campylobacter infections. Vaccine approaches against Campylobacter infections are restricted by lacking in comprehension of its association with post-infectious syndromes, antigenic diversity, protective epitopes and its pathogenesis.

Conclusions

Worldwide, outbreaks of campylobacteriosis have been increasing and the major routes of transmission of these bacteria to human is generally believed to be through consumption of contaminated foods. The development of rapid Kits for Campylobacter detection and quantification in foods from animal origin will be essential for the prevention of Campylobacter infections. Campylobacter infections are majorly treated with antibiotics and the actions of these antibiotics have been compromised and this call for the development of new vaccines that will help to control the regular use of antibiotics in animal husbandry. In addition, regular domestic hygiene will also help to prevent Campylobacter infections. The production of new and effective antibiotic for better treatment of campylobacteriosis will as well help in the reduction of antibiotic-resistant Campylobacter strain and the spread of antibiotics resistant genes.

Author contribution statement

All authors listed have significantly contributed to the development and the writing of this article.

Funding statement

This work was supported by the South African Medical Research Council.

Competing interest statement

The authors declare no conflict of interest.

Additional information

No additional information is available for this paper.

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    Gilliss D., Cronquist A.B., Cartter M., Tobin-D’Angelo M., Blythe D., Smith K., Lathrop S., Zansky S., Cieslak P.R., Dunn J., Holt K.G., Lance S., Crim S.M., Henao O.L., Patrick M., Griffin P.M., Tauxe R.V. Incidence and trends of infection with pathogens transmitted commonly through food-foodborne diseases active surveillance network, 10 U.S. sites, 1996–2012. MMWR Morb. Mortal. Wkly. Rep. 2013;62:283-287.

    Not in our library

  86. 86.

    Gölz G., Kittler S., Malakauskas M., Alter T. Survival of Campylobacter in the food chain and the environment. Curr. Clin. Microbiol. Rep. 2018;1–9.

    Not in our library

  87. 87.

    Golden N.J., Acheson D.W. Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect. Immun. 2002;70:1761-1771.

    Not in our library10.1128/iai.70.4.1761-1771.2002

  88. 88.

    Goni M.D., Muhammad J., Goje M., Abatcha M.G., Bitrus A.A., Abbas M.A. Campylobacter in dogs and cats; its detection and public health significance: a Review. Adv. Anim. Vet. Sci. 2017;5(6):239-248.

    Not in our library

  89. 89.

    Gras L.M., Smid J.H., Wagenaar J.A., Koene M.G.J., Havelaar A.H., Friesema I.H.M., French N.P., Flemming C., Galson J.D., Graziani C., Busani L. Increased risk for Campylobacter jejuni and C. coli infection of pet origin in dog owners and evidence for genetic association between strains causing infection in humans and their pets. Epidemiol. Infect. 2013;141(12):2526-2535.

    Not in our library10.1017/s0950268813000356

  90. 90.

    Grant A.J., Maskell D.J., Holmes M.A. Phylogenetic Analyses and Antimicrobial Resistance Profiles of Campylobacter Spp. From Diarrhoea Patients and Chickens in Botswana. 2018.

    Not in our library10.1371/journal.pone.0194481

  91. 91.

    Grzybowska-Chlebowczyk U., Kalita B., Flak-Wancerz A., Jasielska M., Więcek S., Wojcieszyn M., Horowska-Ziaja S., Chlebowczyk W., Woś H. Clinical course of Campylobacter infections in children. Pediatr. Pol. 2013;88(4):329-334.

    Not in our library

  92. 92.

    Guarino A., Ashkenazi S., Gendrel D., Vecchio A.L., Shamir R., Szajewska H. European society for pediatric gastroenterology, hepatology, and nutrition/European society for pediatric infectious diseases evidence-based guidelines for the management of acute gastroenteritis in children in Europe. J. Pediatr. Gastroenterol. Nutr. 2014;59(1):132-152.

    Not in our library10.1097/mpg.0000000000000375

  93. 93.

    Guzman-Herrador B., Carlander A., Ethelberg S., de Blasio B.F., Kuusi M., Lund V., Löfdahl M., MacDonald E., Nichols G., Schönning C., Sudre B. Waterborne outbreaks in the Nordic countries, 1998 to 2012. Eurosurveillance. 2015;20(24):21160.

    Not in our library10.2807/1560-7917.es2015.20.24.21160

  94. 94.

    Haddock G., Mullin M., MacCallum A., Sherry A., Tetley L., Watson E., Dagleish M., Smith D.G., Everest P. Campylobacter jejuni 81-176 forms distinct microcolonies on in vitro-infected human small intestinal tissue prior to biofilm formation. Microbiology. 2010;156(10):3079-3084.

    Not in our library10.1099/mic.0.039867-0

  95. 95.

    Hansson I., Sandberg M., Habib I., Lowman R., Olsson E.E. Knowledge gaps in control of Campylobacter for prevention of campylobacteriosis. Transbound. Emerg. Dis. 2018;65:30-48.

    Not in our library10.1111/tbed.12870

  96. 96.

    Hamer R., Chen P.Y., Armitage J.P., Reinert G., Deane C.M. Deciphering chemotaxis pathways using cross species comparisons. BMC Syst. Biol. 2010;4(1):3.

    Not in our library10.1186/1752-0509-4-3

  97. 97.

    Hartley-Tassell L.E., Day C.J., Semchenko E.A., Tram G., Calderon-Gomez L.I., Klipic Z., Barry A.M., Lam A.K., McGuckin M.A., Korolik V. A peculiar case of Campylobacter jejuni attenuated aspartate chemosensory mutant, able to cause pathology and inflammation in avian and murine model animals. Sci. Rep. 2018;8(1):12594.

    Not in our library10.1038/s41598-018-30604-5

  98. 98.

    Hasman H., Saputra D., Sicheritz-Ponten T., Lund O., Svendsen C.A., Frimodt-Møller N., Aarestrup F.M. Rapid whole-genome sequencing for detection and characterization of microorganisms directly from clinical samples. J. Clin. Microbiol. 2014;52:139-146.

    Not in our library10.1128/jcm.02452-13

  99. 99.

    Hati S., Gawai K., Sreeja V. Food borne pathogens: a threat to dairy industry. Res. Rev.: J. Dairy Sci. Technol. 2018;4(1):28-36.

    Not in our library

  100. 100.

    Hauri A.M., Just M., McFarland S., Schweigmann A., Schlez K., Krahn J. Campylobacteriosis outbreaks in the state of Hesse, Germany, 2005–2011: raw milk yet again. DMW (Dtsch. Med. Wochenschr.). 2013;138:357-361.

    Not in our library10.1055/s-0032-1332884

  101. 101.

    Henry R., Schang C., Chandrasena G.I., Deletic A., Edmunds M., Jovanovic D., Kolotelo P., Schmidt J., Williamson R., McCarthy D. Environmental monitoring of waterborne Campylobacter: evaluation of the Australian standard and a hybrid extraction-free MPN-PCR method. Front. Microbiol. 2015;6:4.

    Not in our library10.3389/fmicb.2015.00074

  102. 102.

    Heredia N., García S. Animals as sources of food-borne pathogens: a review. Animal Nutr. 2018.

    Not in our library10.1016/j.aninu.2018.04.006

  103. 103.
  104. 104.

    Hernandez L., Green P. Extraintestinal manifestations of celiac disease. Curr. Gastroenterol. Rep. 2006;8(6):383-389.

    Not in our library10.1007/s11894-006-0023-7

  105. 105.

    Hendrixson D.R. A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol. Microbiol. 2006;61:1646-1659.

    Not in our library10.1111/j.1365-2958.2006.05336.x

  106. 106.

    Hofreuter D., Tsai J., Watson R.O., Novik V., Altman B., Benitez M., Clark C., Perbost C., Jarvie T., Du L., Galán J.E. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 2006;74(8):4694-4707.

    Not in our library10.1128/iai.00210-06

  107. 107.

    Hsieh Y.-H., Sulaiman I.M., Holban A.M., Grumezescu A.M. Chapter 5 - campylobacteriosis: an emerging infectious foodborne disease. Foodborne Dis. 2018;119-155.

    Not in our library

  108. 108.

    Hudson A., King N., Lake R., Cressey P. Risk profile: Campylobacter jejuni/coli in raw Milk. ESR (Eur. Surg. Res.). 2014;1-77.

    Not in our library

  109. 109.

    Hur K., Lee E., Kang J., Lee Y. Campylobacter fetus peritonitis in a patient with continuous ambulatory peritoneal dialysis: a first case report in Korea. Ann. Clin. Microbiol. 2018;21(1):20-22.

    Not in our library

  110. 110.

    Hurd S., Patrick M., Hatch J., Clogher P., Wymore K., Cronquist A.B., Segler S., Robinson T., Hanna S., Fitzgerald G.S.C. Clinical laboratory practices for the isolation and identification of Campylobacter in foodborne diseases active surveillance network (FoodNet) Sites: baseline information for understanding changes in surveillance data. Clin. Infect. Dis. 2012;54:440-445.

    Not in our library10.1093/cid/cis245

  111. 111.

    Hussain I., Mahmood M.S., Akhtar M., Khan A. Prevalence of Campylobacter species in meat, milk and other food commodities in Pakistan. Food Microbiol. 2007;24(3):219-222.

    Not in our library10.1016/j.fm.2006.06.001

  112. 112.

    Iglesias-Torrens Y., Miro E., Guirado P., Llovet T., Muñoz C., Cerdà-Cuéllar M., Madrid C., Balsalobre C., Navarro F. Population structure, antimicrobial resistance, and virulence-associated genes in Campylobacter jejuni isolated from three ecological niches: gastroenteritis patients, broilers, and wild birds. Front. Microbiol. 2018;9:1676.

    Not in our library10.3389/fmicb.2018.01676

  113. 113.

    Iraola G., Pérez R., Betancor L., Marandino A., Morsella C., Méndez A., Paolicchi F., Piccirillo A., Tomás G., Velilla A., Calleros L. A novel real-time PCR assay for quantitative detection of Campylobacter fetus based on ribosomal sequences. BMC Vet. Res. 2016;12(1):286.

    Not in our library10.1186/s12917-016-0913-3

  114. 114.

    Iraola G., Forster S.C., Kumar N., Lehours P., Bekal S., García-Peña F.J., Paolicchi F., Morsella C., Hotzel H., Hsueh P.R., Vidal A. Distinct Campylobacter fetus lineages adapted as livestock pathogens and human pathobionts in the intestinal microbiota. Nat. Commun. 2017;8(1):1367.

    Not in our library10.1038/s41467-017-01449-9

  115. 115.

    Irena J., Katrine B., Line V., Helge L., Tore F., Raisa H. A Large Waterborne Outbreak of Campylobacteriosis in Norway: the Need to Focus on Distribution System Safety. 2008.

    Not in our library10.1186/1471-2334-8-128

  116. 116.

    Jagannathan A., Penn C., Ketley J.M., Konkel M.E. Motility in Campylobacter. Molecular and Cellular Biology. 2005;331-347.

    Not in our library

  117. 117.

    Jain D., Prasad K.N., Sinha S., Husain N. Differences in virulence attributes between cytolethal distending toxin positive and negative Campylobacter jejuni strains. J. Med. Microbiol. 2008;l57:267-277.

    Not in our library10.1099/jmm.0.47317-0

  118. 118.

    Jaime A.L., Joan S., Lee B., Nancy S., Sydney M.H., Eleanor L., Roshan R., Laurene M. Campylobacter upsaliensis: another pathogen for consideration in the United States. Clin. Infect. Dis. 2002;34(11):59-60.

    Not in our library10.1086/340266

  119. 119.

    Jakopanec I., Borgen K., Vold L., Lund H., Forseth T., Hannula R., Nygård K. A large waterborne outbreak of campylobacteriosis in Norway: the need to focus on distribution system safety. BMC Infect. Dis. 2008;8(1):128.

    Not in our library10.1186/1471-2334-8-128

  120. 120.

    Jamshidi A., Bassami M.R., Farkhondeh T. Isolation and identification of Campylobacter spp. and Campylobacter coli from poultry carcasses by conventional culture method and multiplex PCR in Mashhad, Iran. Iran. J. Vet. Res. 2008;9(2):132-137.

    Not in our library

  121. 121.

    Jin S., Joe A., Lynett J., Hani E.K., Sherman P., Chan V.L. JlpA, a novel surfaceexposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol. Microbiol. 2001;39:1225-1236.

    Not in our library10.1111/j.1365-2958.2001.02294.x

  122. 122.

    Johnson T.J., Shank J.M., Johnson J.G. Current and potential treatments for reducing Campylobacter colonization in animal hosts and disease in humans. Front. Microbiol. 2017;8:1-14.

    Not in our library10.3389/fmicb.2017.00487

  123. 123.

    Johansson C., Nilsson A., Kaden R., Rautelin H. Campylobacter coli clade 3 isolates induce rapid cell death in vitro. Appl. Environ. Microbiol. 2018;2993.

    Not in our library10.1128/aem.02993-18

  124. 124.

    Kaakoush N.O., Baar C., MacKichan J., Schmidt P., Fox E.M., Schuster S.C., Mendz G.L. Insights into the molecular basis of the microaerophily of three Campylobacterales: a comparative study. Antonie Leeuwenhoek. 2009;96(4):545.

    Not in our library10.1007/s10482-009-9370-3

  125. 125.

    Kaakoush N.O., Castaño-Rodríguez N., Mitchell H.M., Man S.M. Global epidemiology of Campylobacter infection. Clin. Microbiol. Rev. 2015;28:687-720.

    Not in our library10.1128/cmr.00006-15

  126. 126.

    Kale A., Phansopa C., Suwannachart C., Craven C.J., Rafferty J.B., Kelly D.J. The virulence factor PEB4 (CJ0596) and the periplasmic protein Cj1289 are two structurally related SurA-like chaperones in the human pathogen Campylobacter jejuni. J. Biol. Chem. 2011;286:21254-21265.

    Not in our library10.1074/jbc.m111.220442

  127. 127.

    Kashappanavar S., Nair A., Vanitha H., Mathew B., Baskaran S., Sudheesh L., Menon V. Comparison of five different enrichment broth-agar combinations for the isolation of Campylobacter jejuni. Int. J. Livestock Res. 2018;8:102-112.

    Not in our library

  128. 128.

    Keegan V.A., Majowicz S.E., Pearl D.L., Marshall B.J., Sittler N., Knowles L., Wilson J.B. Epidemiology of enteric disease in C-EnterNet’s pilot site-Waterloo region, Ontario, 1990 to 2004. Can. J. Infect Dis. Med. Microbiol. 2009;20(3):79-87.

    Not in our library10.1155/2009/978784

  129. 129.

    Kemp R., Leatherbarrow A.J.H., Williams N.J., Hart C.A., Clough H.E., Turner J., Wright E.J., French N.P. Prevalence and genetic diversity of Campylobacter spp. in environmental water samples from a 100-square-kilometer predominantly dairy farming area. Appl. Environ. Microbiol. 2005;71(4):1876-1882.

    Not in our library10.1128/aem.71.4.1876-1882.2005

  130. 130.

    Kennedy M., Villar R., Vugia D.J., Rabatsky-Her T., Farley M.M., Pass M., Smith K., Smith P., Cieslak P.R., Imhoff B., Griffin P.M. Hospitalizations and deaths due to Salmonella infections, FoodNet, 1996-1999. Clin. Infect. Dis. 2004;38(3):142-148.

    Not in our library10.1086/381580

  131. 131.

    Ketley J.M. Virulence of Campylobacter species: a molecular genetic approach. J. Med. Microbiol. 1995;42:312-327.

    Not in our library10.1099/00222615-42-5-312

  132. 132.

    Khan I.U., Hill S., Nowak E., Palmer M.E., Jarjanazi H., Lee D.Y., Mueller M., Schop R., Weir S., Irwin A.M., Winter J. Investigation of the prevalence of thermophilic Campylobacter species at Lake Simcoe recreational beaches. Inland Waters. 2013;3(1):93-104.

    Not in our library

  133. 133.

    Khan J.R., Bakar K.S. Spatial risk distribution and determinants of E. coli contamination in household drinking water: a case study of Bangladesh. Int. J. Environ. Health Res. 2019;1-16.

    Not in our library10.1080/09603123.2019.1593328

  134. 134.

    Kienesberger S., Sprenger H., Wolfgruber S., Halwachs B., Thallinger G.G., Perez-Perez G.I., Blaser M.J., Zechner E.L., Gorkiewicz G. Comparative genome analysis of Campylobacter fetus subspecies revealed horizontally acquired genetic elements important for virulence and niche specificity. PLoS One. 2014;9(1):85491.

    Not in our library10.1371/journal.pone.0085491

  135. 135.

    Koneman E.W., Allen S.D., Janda W.M., Schreckenberger P.C., Winn W.C. Diagnostic Microbiology. The Nonfermentative Gram-Negative Bacilli. 1997;253-320.

    Not in our library

  136. 136.

    Konkel M.E., Klena J.D., Rivera-Amill V., Monteville M.R., Biswas D., Raphael B., Mickelson J. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J. Bacteriol. 2004;186:3296-3303.

    Not in our library10.1128/jb.186.11.3296-3303.2004

  137. 137.

    Konkel M.E., Larson C.L., Flanagan R.C. Campylobacter jejuni FlpA binds fibronectin and is required for maximal host cell adherence. J. Bacteriol. 2010;192(1):68-76.

    Not in our library10.1128/jb.00969-09

  138. 138.

    Korsak D., Maćkiw E., Rożynek E., Żyłowska M. Prevalence of Campylobacter species in retail chicken, Turkey, pork, and beef meat in Poland between 2009 and 2013. J. Food Prot. 2015;78:1024-1028.

    Not in our library10.4315/0362-028x.jfp-14-353

  139. 139.

    Kubota K., Kasuga F., Iwasaki E., Inagaki S., Sakurai Y., Komatsu M., Toyofuku H., Angulo F.J., Scallan E., Morikawa K. Estimating the burden of acute gastroenteritis and foodborne illness caused by Campylobacter, Salmonella, and Vibrio parahaemolyticus by using population based telephone survey data, Miyagi Prefecture, Japan, 2005 to 2006. J. Food Prot. 2011;74(10):1592-1598.

    Not in our library10.4315/0362-028x.jfp-10-387

  140. 140.

    Kuhn K.G., Falkenhorst G., Emborg H.D., Ceper T., Torpdahl M., Krogfelt K.A., Ethelberg S., Mølbak K. Epidemiological and serological investigation of a waterborne Campylobacter jejuni outbreak in a Danish town. Epidemiol. Infect. 2017;145(4):701-709.

    Not in our library10.1017/s0950268816002788

  141. 141.

    Kuijper E.J., Stevens S., Imamura T., De Wever B., Claas E.C. Genotypic identification of erythromycin-resistant Campylobacter isolates as Helicobacter species and analysis of resistance mechanism. J. Clin. Microbiol. 2003;41:3732-3736.

    Not in our library10.1128/jcm.41.8.3732-3736.2003

  142. 142.

    Kumar A., Drozd M., Pina-Mimbela R., Xu X., Helmy Y.A., Antwi J., Fuchs J.R., Nislow C., Templeton J., Blackall P.J., Rajashekara G. Novel anti-Campylobacter compounds identified using high throughput screening of a pre-selected enriched small molecules library. Front. Microbiol. 2016;7:405.

    Not in our library10.3389/fmicb.2016.00405

  143. 143.

    Kuwabara S., Yuki N. Axonal Guillain-Barre syndrome: concepts and controversies. Lancet Neurol. 2013;12(12):1180-1188.

    Not in our library10.1016/s1474-4422(13)70215-1

  144. 144.

    Kuusi M., Klemets P., Miettinen I., Laaksonen I., Sarkkinen H., Hänninen M.L., Rautelin H., Kela E., Nuorti J.P. An outbreak of gastroenteritis from a non-chlorinated community water supply. J. Epidemiol. Community Health. 2004;58(4):273-277.

    Not in our library10.1136/jech.2003.009928

  145. 145.

    Lagler H., Kiesewetter B., Raderer M. Infection with multidrug-resistant Campylobacter coli mimicking recurrence of carcinoid syndrome: a case report of a neuroendocrine tumor patient with repeated diarrhea. BMC Infect. Dis. 2016;16:409.

    Not in our library10.1186/s12879-016-1743-4

  146. 146.

    Lahti E., Löfdahl M., Ågren J., Hansson I., Olsson E.E. Confirmation of a campylobacteriosis outbreak associated with chicken liver pâté using PFGE and WGS. Zoonoses Publ. Health. 2017;64:14-20.

    Not in our library10.1111/zph.12272

  147. 147.

    Lund M., Jensen J.D. A real options approach to biotechnology investment policy-the case of developing a Campylobacter vaccine to poultry. Prev. Vet. Med. 2016;128:58-69.

    Not in our library10.1016/j.prevetmed.2016.04.006

  148. 148.

    Larson C.L., Shah D.H., Dhillon A.S. Campylobacter jejuni invade chicken LMH cells inefficiently and stimulate differential expression of the chicken CXCLi1 and CXCLi2 cytokines. Microbiology. 2008;154:3835-3847.

    Not in our library10.1099/mic.0.2008/021279-0

  149. 149.
  150. 150.

    Lertsethtakarn P., Ottemann K.M., Hendrixson D.R. Motility and chemotaxis in Campylobacter and Helicobacter. Annu. Rev. Microbiol. 2011;65:389-410.

    Not in our library10.1146/annurev-micro-090110-102908

  151. 151.
  152. 152.
  153. 153.

    Liu J., Platts-Mills J.A., Juma J., Kabir F., Nkeze J., Okoi C., Operario D.J., Uddin J., Ahmed S., Alonso P.L., Antonio M. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: a reanalysis of the GEMS case-control study. The Lancet. 2016;388(10051):1291-1301.

    Not in our library10.1016/s0140-6736(16)31529-x

  154. 154.

    Liu K.C., Jinneman K.C., Neal-McKinney J., Wu W.H., Rice D.H. Simultaneous identification of Campylobacter jejuni, Campylobacter coli, and Campylobacter lari with smart cycler-based multiplex quantitative polymerase chain reaction. Foodb. Pathog. Dis. 2017;14:371-378.

    Not in our library10.1089/fpd.2016.2245

  155. 155.

    Liu F., Ma R., Wang Y., Zhang L. The clinical importance of Campylobacter concisus and other human hosted Campylobacter species. Front. Cell. Infect. Microbiol. 2018;8:243.

    Not in our library10.3389/fcimb.2018.00243

  156. 156.

    Llarena A.K., Taboada E., Rossi M. Whole-genome sequencing in epidemiology of Campylobacter jejuni infections. J. Clin. Microbiol. 2017;55(5):1269-1275.

    Not in our library10.1128/jcm.00017-17

  157. 157.

    Loshaj-Shala A., Regazzoni L., Daci A., Orioli M., Brezovska K., Panovska A.P., Beretta G., Suturkova L. Guillain Barré syndrome (GBS): new insights in the molecular mimicry between C. jejuni and human peripheral nerve (HPN) proteins. J. Neuroimmunol. 2015;289:168-176.

    Not in our library10.1016/j.jneuroim.2015.11.005

  158. 158.

    Luangtongkum T., Jeon B., Han J., Plummer P., Logue C.M., Zhang Q. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 2009;4(2):189-200.

    Not in our library10.2217/17460913.4.2.189

  159. 159.

    Magana M., Chatzipanagiotou S., Burriel A.R., Ioannidis A. Inquiring into the gaps of Campylobacter surveillance methods. Vet. Sci. 2017;4(3):36.

    Not in our library10.3390/vetsci4030036

  160. 160.

    Man S.M. The clinical importance of emerging Campylobacter species. Nat. Rev. Gastroenterol. Hepatol. 2011;8(12):669-685.

    Not in our library10.1038/nrgastro.2011.191

  161. 161.

    Marchant J., Wren B., Ketley J. Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. Trends Microbiol. 2002;10:155-159.

    Not in our library10.1016/s0966-842x(02)02323-5

  162. 162.
  163. 163.

    Martinot M., Jaulhac B., Moog R., De Martino S., Kehrli P., Monteil H., Piemont Y. Campylobacter lari bacteremia. Clin. Microbiol. Infect. 2001;7(2):96-97.

    Not in our library10.1046/j.1469-0691.2001.00212.x

  164. 164.

    Martinez I., Mateo E., Churruca E., Girbau C., Alonso R., Fernandez-Astorga A. Detection of cdtA, cdtB, and cdtC genes in Campylobacter jejuni by multiplex PCR. Int. J. Med. Microbiol. 2006;296(1):45-48.

    Not in our library10.1016/j.ijmm.2005.08.003

  165. 165.
  166. 166.

    Maziero M.T., de Oliveira T.C. Effect of refrigeration and frozen storage on the Campylobacter jejuni recovery from naturally contaminated broiler carcasses. Braz. J. Microbiol. 2010;41:501-505.

    Not in our library10.1590/s1517-838220100002000034

  167. 167.

    Mezher Z., Saccares S., Marcianò R., De Santis P., Rodas E.M.F., De Angelis V., Condoleo R. Occurrence of Campylobacter spp. in poultry meat at retail and processing plants’ levels in Central Italy. Ital. J. Food Saf. 2016;5(1).

    Not in our library10.4081/ijfs.2016.5495

  168. 168.

    Miller W.G., Yee E., Chapman M.H., Smith T.P., Bono J.L., Huynh S., Parker C.T., Vandamme P., Luong K., Korlach J. Comparative genomics of the Campylobacter lari group. Gen. Biol. Evol. 2014;6(12):3252-3266.

    Not in our library10.1093/gbe/evu249

  169. 169.

    Modi S., Brahmbhatt M.N., Chatur Y.A., Nayak J.B. Prevalence of Campylobacter species in milk and milk products, their virulence gene profile and antibiogram. Vet. World. 2015;8(1):1-3.

    Not in our library10.14202/vetworld.2015.1-8

  170. 170.

    Moore J.E., Corcoran D., Dooley J.S., Fanning S., Lucey B., Matsuda M., McDowell D.A., Mégraud F., Millar B.C., O’Mahony R., O’Riordan L. Campylobacter. Vet. Res. 2005;36(3):351-382.

    Not in our library10.1051/vetres:2005012

  171. 171.

    Morishita S., Fujiwara H., Murota H., Maeda Y., Hara A., Horii T. Bloodstream infection caused by Campylobacter lari. J. Infect. Chemother. 2013;19(2):333-337.

    Not in our library10.1007/s10156-012-0471-y

  172. 172.

    Mossong J., Mughini-Gras L., Penny C., Devaux A., Olinger C., Losch S., Cauchie H.M., Van Pelt W., Ragimbeau C. Human campylobacteriosis in Luxembourg, 2010-2013: a case-control study combined with Multilocus sequence typing for source attribution and risk factor analysis. Sci. Rep. 2016;6:20939.

    Not in our library10.1038/srep20939

  173. 173.

    Moyane J.N., Jideani A.I.O., Aiyegoro O.A. Antibiotics usage in food producing animals in South Africa and impact on human: antibiotic resistance. Afr. J. Microbiol. Res. 2013;7:2990-2997.

    Not in our library

  174. 174.

    Mshelia G.D., Amin J.D., Woldehiwet Z., Murray R.D., Egwu G.O. Epidemiology of bovine venereal campylobacteriosis: geographic distribution and recent advances in molecular diagnostic techniques. Reprod. Domest. Anim. 2010;45(5):221-230.

    Not in our library10.1111/j.1439-0531.2009.01546.x

  175. 175.

    Mukherjee P., Ramamurthy T., Bhattacharya M.K., Rajendran K., Mukhopadhyay A.K. Campylobacter jejuni in hospitalized patients with diarrhea, Kolkata, India. Emerg. Infect. Dis. 2013;19(17):1155-1156.

    Not in our library10.3201/eid1907.121278

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    Mungai E.A., Behravesh C.B., Gould L.H. Increased outbreaks associated with nonpasteurized milk, United States, 2007-2012. Emerg. Infect. Dis. 2015;21(1):119-122.

    Not in our library10.3201/eid2101.140447

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    Neeta P.N., Prashanth N., Shivaswamy M.S., Mallapur M.D. A study on awareness regarding milk borne diseases in an urban community of Karnataka. Int. J. Med. Sci. Public Health. 2014;3(9):1093-1100.

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    Newell D.G., Mughini-Gras L., Kalupahana R.S., Wagenaa J.A. Campylobacter epidemiology-sources and routes of transmission for human infection. Camp. Featu. Detect. Prevent. Foodbor. Dis. 2017;85-110.

    Not in our library

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    Nielsen E.M., Fussing V., Engberg J., Nielsen N.L., Neimann J. Most Campylobacter subtypes from sporadic infections can be found in retail poultry products and food animals. Epidemiol. Infect. 2006;134(4):758-767.

    Not in our library10.1017/s0950268805005509

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    Nielsen H.L., Ejlertsen T., Engberg J., Nielsen H. High incidence of Campylobacter concisusin gastroenteritis in North Jutland, Denmark: a population-based study. Clin. Microbiol. Infect. 2013;19(5):445-450.

    Not in our library10.1111/j.1469-0691.2012.03852.x

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    Nisar M., Mushtaq M.H., Shehzad W., Hussain A., Nasar M., Nagaraja K.V., Goyal S.M. Occurrence of Campylobacter in retail meat in Lahore, Pakistan. Acta Trop. 2018;185:42-45.

    Not in our library10.1016/j.actatropica.2018.04.030

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    Nishiguchi S., Sekine I., Kuroda S., Sato M., Kitagawa I. Myositis Ossificans of the hip due to pyogenic arthritis caused by Campylobacter fetus Subspecies fetus. Intern. Med. 2017;56(8):967-972.

    Not in our library10.2169/internalmedicine.56.7906

  183. 183.

    O’Callaghan T.F., Sugrue I., Hill C., Ross R.P., Stanton C. Nutritional aspects of raw milk: a beneficial or hazardous food choice. Raw Milk. 2019;127-148.

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    Oh E., Chui L., Bae J., Li V., Ma A., Mutschall S.K., Taboada E.N., McMullen L.M., Jeon B. Frequent implication of multistress-tolerant Campylobacter jejuni in human infections. Emerg. Infect. Dis. 2018;24:1037.

    Not in our library10.3201/eid2406.171587

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    O'Reilly C.E., Jaron P., Ochieng B., Nyaguara A., Tate J.E., Parsons M.B., Bopp C.A., Williams K.A., Vinjé J., Blanton E., Wannemuehler K.A. Risk factors for death among children less than 5 years old hospitalized with diarrhea in rural western Kenya, 2005-2007: a cohort study. PLoS Med. 2012;9:1001256.

    Not in our library10.1371/journal.pmed.1001256

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    Oliver S.P., Jayarao B.M., Almeida R.A. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodb. Pathog. Dis. 2005;2(2):115-129.

    Not in our library10.1089/fpd.2005.2.115

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    On S.L. Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: current status, future prospects and immediate concerns. J. Appl. Microbiol. 2001;90(6):1-15.

    Not in our library10.1046/j.1365-2672.2001.01349.x

  188. 188.

    On S.L.W. Isolation, identification and subtyping of Campylobacter: where to from here? J. Microbiol. Methods. 2013;95(1):3-7.

    Not in our library10.1016/j.mimet.2013.06.011

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    Oyofo B.A., Thornton S.A., Burr D.H., Trust T.J., Pavlovskis O.R., Guerry P. Specific detection of Campylobacter jejuni and Campylobacter coli by using polymerase chain reaction. J. Clin. Microbiol. 1992;30(10):2613-2619.

    Not in our library10.1128/jcm.30.10.2613-2619.1992

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    Pacanowski J., Lalande V., Lacombe K., Boudraa C., Lesprit P., Legrand P., Trystram D., Kassis N., Arlet G., Mainardi J.L., Doucet-Populaire F. Campylobacter bacteremia: clinical features and factors associated with fatal outcome. Clin. Infect. Dis. 2008;47(6):790-796.

    Not in our library10.1086/591530

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    Pal M. Campylobacter jejuni: an emerging foodborne pathogen of global significance. J. Exp. Food Chem. 2017;3(3):1-4.

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    Parker C.T., Miller W.G., Horn S.T., Lastovica A.J. Common genomic features of Campylobacter jejuni subsp. doylei strains distinguish them from C. jejuni subsp. jejuni. BMC Microbiol. 2007;7(1):50.

    Not in our library10.1186/1471-2180-7-50

  193. 193.

    Patel R. A moldy application of MALDI: MALDI-ToF mass spectrometry for fungal identification. J. Fungi. 2019;5(1):4.

    Not in our library10.3390/jof5010004

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    Patrick M.E., Gilbert M.J., Blaser M.J., Tauxe R.V., Wagenaar J.A., Fitzgerald C. Human infections with new subspecies of Campylobacter fetus. Emerg. Infect. Dis. 2013;19(10):1678.

    Not in our library10.3201/eid1910.130883

  195. 195.

    Pérez-Boto D., López-Portolés J., Simón C., Valdezate S., Echeita M. Study of the molecular mechanisms involved in high-level macrolide resistance of Spanish Campylobacter jejuni and Campylobacter coli strains. J. Antimic. Chem. 2010;65(10):2083-2088.

    Not in our library10.1093/jac/dkq268

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    Piddock L.J., Ricci V., Pumbwe L., Everett M.J., Griggs D.J. Fluoroquinolone resistance in Campylobacter species from man and animals: detection of mutations in topoisomerase genes. J. Antimic. Chem. 2003;51(1):19-26.

    Not in our library10.1093/jac/dkg033

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    Pitkänen T. Review of Campylobacter species in drinking and environmental waters. J. Microbiol. Methods. 2013;95(1):39-47.

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    Platts-Mills J.A., Kosek M. Update on the burden of Campylobacter in developing countries. Curr. Opin. Infect. Dis. 2014;27(5):444.

    Not in our library10.1097/qco.0000000000000091

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    Poly F., Guerry P. Pathogenesis of Campylobacter. Curr. Opin. Gastroenterol. 2008;24:27-31.

    Not in our library10.1097/mog.0b013e3282f1dcb1

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    Prescott L.M., Harley J.P., Klein D.A. Campylobacter. Microbiology. 2005;430-433.

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    Premarathne J.M.K.J.K., Satharasinghe D.A., Huat J.T.Y., Basri D.F., Rukayadi Y., Nakaguchi Y., Nishibuchi M., Radu S. Impact of human Campylobacter infections in Southeast Asia: the contribution of the poultry sector. Crit. Rev. Food Sci. Nutr. 2017;57(18):3971-3986.

    Not in our library10.1080/10408398.2016.1266297

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    Prouzet-Mauléon V., Labadi L., Bouges N., Ménard A., Mégraud F. Arcobacter butzleri: underestimated enteropathogen. Emerg. Infect. Dis. 2006;12(2):30.

    Not in our library10.3201/eid1202.050570

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    Quigley L., O’Sullivan O., Stanton C., Beresford T.P., Ross P.R., Fitzgerald G.F., Paul D.C. The complex microbiota of raw milk. FEMS Microbiol. Rev. 2013;37(5):664-698.

    Not in our library10.1111/1574-6976.12030

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    Rahimi E., Ameri M., Kazemeini H.R. Prevalence and antimicrobial resistance of Campylobacter species isolated from raw camel, beef, lamb, and goat meat in Iran. Foodb. Pathog. Dis. 2010;7(4):443-447.

    Not in our library10.1089/fpd.2009.0421

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    Rahimi E., Sepehri S., Momtaz H. Prevalence of Campylobacter species in milk and dairy products in Iran. Revue de Méd. Vétér. 2013;164(5):283-288.

    Not in our library

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    Rahman G., Price L., Rabanes H.G., Hilsabeck R. Implications of Foodborne Bacteria on Human Health: Isolation and Antibiotic Resistance of Salmonella enterica and Campylobater Spp. On Retail Chicken Sold in California. 2018.

    Not in our library

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    Randremanana R.V., Randrianirina F., Sabatier P., Rakotonirina H.C., Randriamanantena A., Razanajatovo I.M., Ratovoson R., Richard V. Campylobacter infection in a cohort of rural children in Moramanga, Madagascar. BMC Infect. Dis. 2014;14(372):1-9.

    Not in our library10.1186/1471-2334-14-372

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    Ravel A., Pintar K., Nesbitt A., Pollari F. Non food-related risk factors of campylobacteriosis in Canada: a matched case-control study. BMC Public Health. 2016;16:1-12.

    Not in our library10.1186/s12889-016-3679-4

  209. 209.

    Reddy S., Zishiri O.T. Detection and prevalence of antimicrobial resistance genes in Campylobacter spp. isolated from chickens and humans. Onderstepoort J. Vet. Res. 2017;84(1):1-6.

    Not in our library10.4102/ojvr.v84i1.1411

  210. 210.

    Riddle M.S., Guerry P. Status of vaccine research and development for Campylobacter jejuni. Vaccine. 2016;34(26):2903-2906.

    Not in our library10.1016/j.vaccine.2016.02.080

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    Rosner B.M., Schielke A., Didelot X., Kops F., Breidenbach J., Willrich N., Gölz G., Alter T., Stingl K., Josenhans C., Suerbaum S. A combined case-control and molecular source attribution study of human Campylobacter infections in Germany, 2011-2014. Sci. Rep. 2017;7:1-12.

    Not in our library10.1038/s41598-017-05227-x

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    Rollins D.M., Joseph S.W. Pathogenic Microbiology-Fall. Enterococcus Summary. 2000;424.

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    Sadkowska-Todys M., Kucharczyk B. Campylobacteriosis in Poland in 2012. Przegl. Epidemiol. 2014;68(2):239-241.

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    Sails A.D., Bolton F.J., Fox A.J., Wareing D.R.A., Greenway D.L.A. Detection of Campylobacter jejuni and Campylobacter coli in environmental waters by PCR enzyme-linked immunosorbent assay. Appl. Environ. Microbiol. 2002;68(3):1319-1324.

    Not in our library10.1128/aem.68.3.1319-1324.2002

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    Scallan E., Hoekstra R.M., Mahon B.E., Jones T.F., Griffin P.M. An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol. Infect. 2015;143(13):2795-2804.

    Not in our library10.1017/s0950268814003185

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    Sears A., Baker M.G., Wilson N., Marshall J., Muellner P., Campbell D.M., Lake R.J., French N.P. Marked campylobacteriosis decline after interventions aimed at poultry, New Zealand. Emerg. Infect. Dis. 2011;17(6):1007.

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    Seguino A., Chintoan-Uta C., Smith S.H., Shaw D.J. Public health significance of Campylobacter spp. colonisation of wild game pheasants (Phasianus colchicus) in Scotland. Food Microbiol. 2018;74:163-0170.

    Not in our library10.1016/j.fm.2018.04.002

  221. 221.

    Seliwiorstow T., Baré J., Verhaegen B., Uyttendaele M., De Zutter L. Evaluation of a new chromogenic medium for direct enumeration of Campylobacter in poultry meat samples. J. Food Prot. 2014;77:2111-2114.

    Not in our library10.4315/0362-028x.jfp-14-237

  222. 222.

    Seliwiorstow T., Baré J., Van Damme I., Uyttendaele M., De Zutter L. Campylobacter carcass contamination throughout the slaughter process of Campylobacter-positive broiler batches. Int. J. Food Microbiol. 2015;194:25-31.

    Not in our library10.1016/j.ijfoodmicro.2014.11.004

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    Sharma K.P., Chattopadhyay U.K., Naskar K. Prevalence of Campylobacter species in raw meat samples sold in open markets of Kolkata city. Int. J. Agric. Environ. Biotechnol. 2016;9(4):535-539.

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    Schürch A.C., Arredondo-Alonso S., Willems R.J.L., Goering R.V. Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene–based approaches. Clin. Microbiol. Infect. 2018;24(4):350-354.

    Not in our library10.1016/j.cmi.2017.12.016

  225. 225.

    Schulze F., H€anel I., Borrmann E. Formation of cytotoxins by enteric Campylobacter in humans and animals. Zentralblatt Bakteriol. 1998;288:225-236.

    Not in our library10.1016/s0934-8840(98)80045-5

  226. 226.

    Shane S.M. Campylobacter infection of commercial poultry. Revue Scientifique et Technique-Office Intern. des Epizoot. 2000;19(2):376-385.

    Not in our library10.20506/rst.19.2.1224

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    Shawky H.M., Kamel N.M., Farghaly E.M., Samir A. Isolation and molecular characterization of Campylobacter spp. in newly hatched poultry in Egypt. J. Global Biosci. 2015;4(5):2087-2091.

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    Silva J., Leite D., Fernandes M., Mena C., Gibbs P.A., Teixeira P. Campylobacter spp. as a foodborne pathogen: a review. Front. Microbiol. 2011;2:1-12.

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    Skarp C.P.A., Hänninen M.L., Rautelin H.I.K. Campylobacteriosis: the role of poultry meat. Clin. Microbiol. Infect. 2016;22(2):103-109.

    Not in our library10.1016/j.cmi.2015.11.019

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    Skirrow M.B. Campylobacter enteritis: a “new” disease. Br. Med. J. 1977;2:9-11.

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    Steens A., Eriksen H.M., Blystad H. What are the most important infectious diseases among those 65 years: a comprehensive analysis on notifiable diseases, Norway, 1993-2011. BMC Infect. Dis. 2014;14(57):1-9.

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    Steinhauserova I., Fojtikova K., Klimes J. The incidence and PCR detection of Campylobacter upsaliensis in dogs and cats. Lett. Appl. Microbiol. 2000;31(3):209-212.

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    Stuart T.L., Sandhu J., Stirling R., Corder J., Ellis A., Misa P., Goh S., Wong B., Martiquet P., Hoang L., Galanis E. Campylobacteriosis outbreak associated with ingestion of mud during a mountain bike race. Epidemiol. Infect. 2010;138(12):1695-1703.

    Not in our library10.1017/s095026881000049x

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    Sugrue I., Tobin C., Ross R.P., Stanton C., Hill C. Foodborne pathogens and zoonotic diseases. Raw Milk. 2019;259-272.

    Not in our library

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    Swierczewski B.E., Odundo E.A., Koech M.C., Ndonye J.N., Kirera R.K., Odhiambo C.P., Cheruiyot E.K., Shaffer D.N., Ombogo A.N., Oaks E.V. Enteric pathogen surveillance in a case-control study of acute diarrhea in Kisii Town, Kenya. J. Med. Microbiol. 2013;62(11):1774-1776.

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    Szosland-Fałtyn A., Bartodziejska B., Królasik J., Paziak-Domańska B., Korsak D., Chmiela M. The prevalence of Campylobacter species in Polish poultry meat. Pol. J. Microbiol. 2018;67(1):117-120.

    Not in our library10.5604/01.3001.0011.6152

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    Taheri N., Fällman M., Wai S.N., Fahlgren A. Accumulation of virulence-associated proteins in Campylobacter jejuni Outer Membrane Vesicles at human body temperature. J. Proteomics. 2019;195:33-40.

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    Tam C.C., Rodrigues L.C., Viviani L., Dodds J.P., Evans M.R., Hunter P.R., Gray J.J., Letley L.H., Rait G., Tompkins D.S., O’Brien S.J. Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut. 2012;61:69-77.

    Not in our library10.1136/gut.2011.238386

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    Taylor P., D'Cruz P., Noronha E., Scholarios D. The experience of work in India's domestic call centre industry. Int. J. Hum. Resour. Manag. 2013;24(2):436-452.

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    Thomas C.D. Pilot study for the development of a new Campylobacter selective medium at 37°C using aztreonam. J. Clin. Pathol. 2005;58:413-416.

    Not in our library10.1136/jcp.2004.019042

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    Thompson R.A., Monis P. Giardia from genome to proteome. Adv. Parasitol. 2012;78:57-95.

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    Tribble D.R., Baqar S., Scott D.A., Oplinger M.L., Trespalacios F., Rollins D., Walker R.I., Clements J.D., Walz S., Gibbs P., Burg E.F.I., Moran A.P., Applebee L., Bourdeois A.L. Assessment of the duration of protection in Campylobacter jejuni experimental infection in humans. Infect. Immun. 2010;78(4):1750-1759.

    Not in our library10.1128/iai.01021-09

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    Unicomb L.E., Fullerton K.E., Kirk M.D., Stafford R.J. Outbreaks of campylobacteriosis in Australia, 2001 to 2006. Foodb. Pathog. Dis. 2009;6(10):1241-1250.

    Not in our library10.1089/fpd.2009.0300

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    Vacheyrou M., Normand A.C., Guyot P., Cassagne C., Piarroux R., Bouton Y. Cultivable microbial communities in raw cow milk and potential transfers from stables of sixteen French farms. Foodb. Pathog. Dis. 2011;6(10):1241-1250.

    Not in our library10.1016/j.ijfoodmicro.2011.02.033

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    van Vliet A.H.M., Ketley J.M. Pathogenesis of enteric Campylobacter infection. J. Appl. Microbiol. 2001;90:45-56.

    Not in our library10.1046/j.1365-2672.2001.01353.x

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    Vihavainen E., Lundstrom H.S., Susiluoto T., Koort J., Paulin L., Auvinen P., Bjorkroth J. Role of broiler carcasses and processing plant air in contamination of modified-atmosphere-packaged broiler products with psychrotrophic lactic acid bacteria. Appl. Environ. Microbiol. 2007;73:1136-1145.

    Not in our library10.1128/aem.01644-06

  248. 248.

    Wagenaar J.A., van Bergen M.A., Blaser M.J., Tauxe R.V., Newell D.G., van Putten J.P. Campylobacter fetus infections in humans: exposure and disease. Clin. Infect. Dis. 2014;58(11):1579-1586.

    Not in our library10.1093/cid/ciu085

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    Wang Y., Zhang M., Deng F., Shen Z., Wu C., Zhang J., Zhang Q., Shen J. Emergence of multidrug-resistant Campylobacter species isolates with a horizontally acquired rRNA methylase. Antimicrob. Agents Chemother. 2014;58(9):5405-5412.

    Not in our library10.1128/aac.03039-14

  250. 250.

    Walsh T.J., Roilides E., Rex J.H., McGinnis M.R. Mucormycosis. Trop. Med. Infect. Dis. 2011;3:597-602.

    Not in our library

  251. 251.

    Wei B., Kang M., Jang H.-K. Evaluation of potassium clavulanate supplementation of Bolton broth for enrichment and detection of Campylobacter from chicken. PLoS One. 2018;13(10):1-13.

    Not in our library10.1371/journal.pone.0205324

  252. 252.

    Wei B., Kang M. Molecular basis of macrolide resistance in Campylobacter strains isolated from poultry in South Korea. BioMed Res. Int. 2018;1–9.

    Not in our library10.1155/2018/4526576

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    Weinberger M., Lerner L., Valinsky L., Moran-Gilad J., Nissan I., Agmon V., Peretz C. Increased incidence of Campylobacter spp. Infection and high rates among children. Israel Emerg. Infect. Dis. 2013;19(11):1828.

    Not in our library10.3201/eid1911.120900

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    Werno A.M., Klena J.D., Shaw G.M., Murdoch D.R. Fatal case of Campylobacter lari prosthetic joint infection and bacteremia in an immunocompetent patient. J. Clin. Microbiol. 2002;40(3):1053-1055.

    Not in our library10.1128/jcm.40.3.1053-1055.2002

  255. 255.

    Westermarck E. Chronic diarrhea in dogs: what do we actually know about it? Top. Companion Anim. Med. 2016;31(2):78-84.

    Not in our library10.1053/j.tcam.2016.03.001

  256. 256.

    WHO. The Global View of Campylobacteriosis: Report of an Expert Consultation. Utrecht, Netherlands 9-11 July 2012. Who Rep. 57. 2013.

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  257. 257.

    WHO. WHO Estimates of the Global Burden of Foodborne Diseases: Foodborne Disease Burden Epidemiology Reference Group 2007-2015. 2018.

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  258. 258.
  259. 259.

    Wieczorek K., Denis E., Osek J. Comparative analysis of antimicrobial resistance and genetic diversity of Campylobacter from broilers slaughtered in Poland. Int. J. Food Microbiol. 2015;210:24-32.

    Not in our library10.1016/j.ijfoodmicro.2015.06.006

  260. 260.

    Wieczorek K.A., Wołkowicz T., Osek J. Antimicrobial resistance and virulence-associated traits of Campylobacter jejuni isolated from poultry food chain and humans with diarrhea. Front. Microbiol. 2018;9:1508.

    Not in our library10.3389/fmicb.2018.01508

  261. 261.

    Wilkinson D.A., O’Donnell A.J., Akhter R.N., Fayaz A., Mack H.J., Rogers L.E., Biggs P.J., French N.P., Midwinter A.C. Updating the genomic taxonomy and epidemiology of Campylobacter hyointestinalis. Sci. Rep. 2018;8(1):2393.

    Not in our library10.1038/s41598-018-20889-x

  262. 262.
  263. 263.

    Wong T.L., Hollis L., Cornelius A., Nicol C., Cook R., Hudson J.A. Prevalence, numbers, and subtypes of Campylobacter jejuni and Campylobacter coli in uncooked retail meat samples. J. Food Prot. 2007;70(3):566-573.

    Not in our library10.4315/0362-028x-70.3.566

  264. 264.

    Wood T.K., Knabel S.J., Kwan B.W. Bacterial persister cell formation and dormancy. Appl. Environ. Microbiol. 2013;79:7116-7121.

    Not in our library10.1128/aem.02636-13

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    Zaidi M.B., Campos F.D., Estrada-Garcia T., Gutierrez F., Leon M., Chim R., Calva J.J. Burden and transmission of zoonotic foodborne disease in a rural community in Mexico. Clin. Infect. Dis. 2012;55(1):51-60.

    Not in our library10.1093/cid/cis300

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