Open Veterinary Journal, (2024), Vol. 14(8): 1733–1750

Review Article

10.5455/OVJ.2024.v14.i8.1

Campylobacteriosis: A rising threat in foodborne illnesses

Aswin Rafif Khairullah¹, Sheila Marty Yanestria², Mustofa Helmi Effendi^3*, Ikechukwu Benjamin Moses⁴, Muhammad Khaliim Jati Kusala¹, Kartika Afrida Fauzia^5,6, Siti Rani Ayuti⁷, Ima Fauziah¹, Otto Sahat Martua Silaen⁸, Katty Hendriana Priscilia Riwu⁹, Suhita Aryaloka¹⁰, Fidi Nur Aini Eka Puji Dameanti¹¹, Ricadonna Raissa¹², Abdullah Hasib¹³ and Abdul Hadi Furqoni¹⁴

¹Research Center for Veterinary Science, National Research and Innovation Agency (BRIN), Bogor, Indonesia

²Faculty of Veterinary Medicine, Universitas Wijaya Kusuma Surabaya, Surabaya, Indonesia

³Division of Veterinary Public Health, Faculty of Veterinary Medicine, Universitas Airlangga, Surabaya, Indonesia

⁴Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Nigeria

⁵Research Center for Preclinical and Clinical Medicine, National Research and Innovation Agency (BRIN), Bogor, Indonesia

⁶Department of Environmental and Preventive Medicine, Faculty of Medicine, Oita University, Yufu, Japan

⁷Faculty of Veterinary Medicine, Universitas Syiah Kuala, Banda Aceh, Indonesia

⁸Doctoral Program in Biomedical Science, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia

⁹Department of Veterinary Public Health, Faculty of Veterinary Medicine, Universitas Pendidikan Mandalika, Surabaya, Indonesia

¹⁰Master Program of Veterinary Agribusiness, Faculty of Veterinary Medicine, Universitas Airlangga, Surabaya, Indonesia

¹¹Microbiology and Immunology Laboratory, Faculty of Veterinary Medicine, Universitas Brawijaya, Malang, Indonesia

¹²Department of Pharmacology, Faculty of Veterinary Medicine, Universitas Brawijaya, Malang, Indonesia

¹³School of Agriculture and Food Sustainability, The University of Queensland, Gatton, Queensland 14Center for Biomedical Research, National Research and Innovation Agency (BRIN), Bogor, Indonesia

*Corresponding Author: Mustofa Helmi Effendi. Division of Veterinary Public Health, Faculty of Veterinary Medicine, Universitas Airlangga, Surabaya, Indonesia. Email: mhelmieffendi [at] gmail.com

Submitted: 17/05/2024 Accepted: 09/07/2024 Published: 31/08/2024

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ABSTRACT

Campylobacteriosis is a foodborne illness that is contracted by eating contaminated food, particularly animal products like meat from diseased animals or corpses tainted with harmful germs. The epidemiology of campylobacteriosis varies significantly between low-, middle-, and high-income countries. Campylobacter has a complicated and poorly known survival strategy for getting past host barriers and causing sickness in humans. The adaptability of Campylobacter to unfavorable environments and the host’s immune system seems to be one of the most crucial elements of intestinal colonization. A Campylobacter infection may result in fever, nausea, vomiting, and mild to severe bloody diarrhea in humans. Effective and rapid diagnosis of Campylobacter species infections in animal hosts is essential for both individual treatment and disease management at the farm level. According to the most recent meta-analysis research, the main risk factor for campylobacteriosis is travel, which is followed by eating undercooked chicken, being exposed to the environment, and coming into close contact with livestock. Campylobacter jejuni, and occasionally Campylobacter coli, are the primary causes of Campylobacter gastroenteritis, the most significant Campylobacter infection in humans for public health. The best antibiotic medications for eradicating and decreasing Campylobacter in feces are erythromycin, clarithromycin, or azithromycin. The best strategy to reduce the number of human infections caused by Campylobacter is to restrict the amount of contamination of the poultry flock and its products, even if the majority of infections are contracted through handling or ingestion of chicken.

Keywords: Campylobacter, Campylobacteriosis, Food, Poultry, Public health.

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Introduction

The zoonotic disease known as campylobacteriosis is brought on by bacteria belonging to the genus Campylobacter, which includes the species Campylobacter jejuni, Campylobacter coli, Campylobacter lari, and Campylobacter fetus (Facciolà et al., 2017). This is a foodborne illness that is contracted by eating contaminated food, particularly animal products like milk and meat from diseased animals or corpses tainted with harmful germs (Chlebicz and Śliżewska, 2018; Agumah et al., 2024). The number of instances of campylobacteriosis has surpassed that of classical enteric bacteria. The information indicates that the prevalence of Campylobacter infections has risen recently (Behailu et al., 2022). The incidence of this organism’s isolation from gastrointestinal infections is roughly three to four times higher than that of Salmonella or Escherichia coli (Epps et al., 2013; Yanestria et al., 2019; Ansharieta et al., 2021).

The digestive tracts of domestic animals, wild animals, and livestock serve as the organism’s reservoir (Johnson et al., 2017). Since the Campylobacter species that cause human gastroenteritis can grow at temperatures above 40ºC, they are categorized as temperature tolerant (Yanestria et al., 2024a). The two main variables that affect Campylobacter infection are transmission factors and body resistance. Human campylobacteriosis infections are mostly infrequent. The most common ways that these bacteria are spread are through the consumption of raw milk, drinking water, eating undercooked chicken and cattle meat, or coming into close contact with sick dogs or cats (Goddard et al., 2022). The range of germs that can induce an illness in an individual is between 500 and 10,000 cells (Kreling et al., 2020). Children are exposed to a lower infectious dosage than adults.

Foodborne Campylobacter infections are a human health problem that causes approximately 8.4% of global diarrhea cases (Igwaran and Okoh, 2019). One of the four primary causes of diarrheal illness worldwide is Campylobacter; diarrhea is the most prevalent foodborne illness, affecting 550 million people annually (Myintzaw et al., 2023). Campylobacteriosis symptoms include vomiting, fever, and bloody or watery diarrhea. In general, people over 75 years old and younger children (under 4) are more likely to have Campylobacter infections (Guo et al., 2023). Furthermore, patients with hemoglobinopathy, inflammatory bowel illness, and those with compromised immune systems are among the populations most at risk of contracting a Campylobacter infection (Igwaran and Okoh, 2019).

Compared to low-income countries, high-income countries have a higher risk of Campylobacter infection. A multitude of environmental factors present a significant risk of Campylobacter transmission to people in low-income countries, and eating poultry meat and poultry products is the main cause of outbreaks (El-Saadony et al., 2023). Worldwide incidences of campylobacteriosis are caused by 60%–80% of poultry meat and its by-products. Poultry meat from laying hens, turkeys, ostriches, ducks, and broilers is frequently consumed (Suzuki and Yamamoto, 2009). To lower product contamination and thus lower the incidence of human campylobacteriosis, intervention techniques to manage Campylobacter in hens must be prioritized as consumer demand for poultry meat and poultry products rises (Taha-Abdelaziz et al., 2023).

Campylobacter, especially in poultry, can spread quickly by the fecal-oral pathway from one animal to the entire flock in less than a week (Rawson et al., 2019). Once within the host body, these bacteria live in the intestines, which have the highest concentration of bacteria; the liver, deep muscles, spleen, thymus, and bursa of Fabricius have smaller concentrations of bacteria (Deng et al., 2020). Bacterial colonization results in serosal fluid leakage, inflammation, toxin production, invasion of host cells, and active secretion, all of which lead to epithelial diseases (O Cróinín and Backert, 2012). In humans, campylobacteriosis typically takes two to five days to incubate. Similar to the toxins produced by E. coli and cholera, this bacterium also produces enterotoxins (Wysok et al., 2022).

The yearly rise in instances of campylobacteriosis has raised concerns about the disease’s occurrence around the world, with major socioeconomic and public health ramifications. This review article aims to provide a comprehensive explanation of campylobacteriosis, starting from etiology, history, epidemiology, pathogenesis, virulence factors, diagnosis, clinical symptoms, transmission, public health importance, treatment, antibiotic resistance, control, and vaccination. Understanding the overview of campylobacteriosis is essential to implementing effective control measures.

Etiology

Organism description

Greek terms “campylos,” which means “curved,” and “baktron,” which means “rod,” are the sources of the word Campylobacter. Gram-negative bacteria belonging to the Campylobacteriaceae family are called Campylobacter species, and they do not produce spores (Wang et al., 2023). There are six subspecies and seventeen species in the genus Campylobacter. More advancements in taxonomic standards could lead to a more precise classification of Campylobacter species. The two species that are most frequently linked to human illness are C. jejuni and C. coli (Pölzler et al., 2018). More than 80% of human Campylobacter-related diseases are caused by C. jejuni, but up to 18.6% are caused by C. coli (Ammar et al., 2020). Additionally, C. fetus has been connected to human foodborne diseases.

Morphology and characteristics of Campylobacter bacteria

Certain gram-negative bacteria called Campylobacter species do not produce spores. These organisms range in size from 0.2 to 0.8 μm in width and 0.5 to 5 μm in length. They have a spiral shape, are curved, or are occasionally observed as straight rods (Epps et al., 2013). Campylobacter can be seen in short or occasionally large chains and can have shapes such as spiral, S, V, or comma (Mushi et al., 2014). Campylobacter cells begin to age and then become coccoid in shape. Possessing one or more flagella at one end, the cells exhibit remarkable motility. A phase contrast microscope can be used to observe the comma-shaped cells’ quick, darting movement (Frirdich et al., 2019).

Growth and survival characteristics of Campylobacter bacteria

Species of Campylobacter are delicate organisms. This organism is susceptible to irradiation, disinfectants, freezing, drying, heating (pasteurization/cooking), and acidic conditions (preservation) (Kim et al., 2021). Bacteria often do better at colder temperatures and struggle to thrive at room temperature (25°C). Campylobacter jejuni thrives in low-oxygen conditions, such as those with 5% O₂, 10% CO₂, and 85% N₂, and grows best at 37°C to 42°C (Kaakoush et al., 2007). The gut has evolved bacteria to have a single polar flagellum and a corkscrew form. These characteristics promote motility (Liu et al., 2018). It has been demonstrated that certain Campylobacter species can grow in viscous intestinal mucus under unfavorable circumstances, such as low nutrition availability, high temperature, freezing, or stationary phase (Ribardo et al., 2024). The cells undergo a form of transition in this condition, going from a motile spiral to a coccoid. This coccoid form’s nature and function are unknown. Due to its capacity to form a biofilm, C. jejuni can tolerate aerobic environments (Pokhrel et al., 2022).

History

There is a vast and varied range of bacteria in the Campylobacter genus. Theodor Escherich identified the first reported case of Campylobacter in 1886 when he observed non-culturable, helical-shaped bacteria in colonic mucosal stains linked to diarrhea in infants who perished from an outbreak of the disease thought to be “Cholera infantum” (Sheppard and Maiden, 2015). In 1906, Campylobacter or bacteria resembling Vibrio, were first isolated from the uterus of a sheep that had been aborted (Tresse et al., 2017). A similar pathogen, Vibrio fetus, was identified in 1912 from aborted bovine fetuses. After fifteen years, a different Vibrio pathogen called Vibrio jejuni was found in the feces of cows that had diarrhea (Epps et al., 2013). Vibrio coli was discovered in 1944 in pigs that had diarrhea.

For more than 40 years, it has been believed that Campylobacter causes animal illness, especially in 1938 when Campylobacter spp. was reported to be involved in foodborne illness outbreaks (Sockett and Rodgers, 2001). Due to the ingestion of tainted milk, a Vibrio jejuni-like virus was found in the blood of 13 outbreak victims. This outbreak resulted in acute diarrheal sickness in 357 prisoners at an Illinois state institution in the United States (Poly et al., 2019). To distinguish this bacterium from Vibrio spp., it was moved to the newly formed genus Campylobacter in 1963 because of its unique traits, which included low DNA base composition (low G+C concentration), microaerophilic development, and nonfermentative metabolism (O’Loughlin et al., 2015). The Greek word “kampyo’s” is the source of the genus name, which signifies bent or curled (Sheppard and Maiden, 2015).

The American bacteriologist Elisabeth King provided the first accurate description of the genus Campylobacter. King was determined to isolate these bacteria from feces and thought that the prevalence of Campylobacter was higher than the few cases that had been reported (Moore and Matsuda, 2002). Butzler was able to isolate Campylobacter from the feces of human patients who were experiencing diarrhea and elevated body temperatures in the early 1970s, thanks to the development of a unique filtration technique for the identification of this bacteria in veterinary medicine (Butzler, 2004). However, adding certain antimicrobial drugs, such as trimethoprim, polymyxin B, and vancomycin to the basic medium allowed for significant advancements in Campylobacter isolation (Bonnet et al., 2019).

Four distinct species of Campylobacter were identified by Veron and Chatelain in their 1973 comprehensive study on the taxonomy of microaerophilic vibrio-like organisms: C. coli, C. sputorum, C. fetal, and C. jejuni (Costa and Iraola, 2019). C. jejuni was not widely acknowledged as one of the most common causes of foodborne bacterial enteritis in people until the 1980s, around a century after it was initially discovered.

Public health importance

Campylobacter jejuni, and occasionally C. coli, are the primary causes of Campylobacter gastroenteritis, the most significant Campylobacter infection in humans for public health (Igwaran and Okoh, 2019). It is estimated that 80% of human Campylobacter infections are caused by chickens, which are the primary reservoir of Campylobacter spp. infections (Epps et al., 2013). Campylobacteriosis is thought to be carried asymptomatically by chickens. Most chicken flocks can become colonized by Campylobacter spp. (Yanestria et al., 2023). According to basic research conducted by the European Union, Campylobacter was found in 75.8% of broiler carcasses, 71.2% of a batch of broiler chickens’ cecal content contained Campylobacter, and 61.3% of chicken skin samples from retail settings had Campylobacter prevalence, with 18.6% of those samples having counts of more than 1000 CFU/g (Hue et al., 2010).

Despite the low severity of campylobacteriosis (0.03%), there are more instances of Campylobacter infection in humans (Facciolà et al., 2017). Remarkably, among foodborne microbes, Campylobacter infections are the most prevalent cause of death in humans. Patients with compromised immune systems, such as those with cancer, liver disease, and acquired immunodeficiency syndrome (AIDS), are susceptible to death from Campylobacter infections (Louwen et al., 2012). In most cases, campylobacteriosis is sporadic and self-limiting. The symptoms of Campylobacter-induced gastroenteritis include fever, headache, vomiting, cramping or pain in the abdomen, watery or often bloody diarrhea, and weight loss (Hsu et al., 2023).

A Campylobacter infection can result in post-infectious immune disorders like Guillain Barré syndrome (GBS), a neurological disorder characterized by flaccid paralysis and advanced weakness in the extremities. It can also cause reactive arthritis (RA), or inflammation of the joints, and paralysis of the respiratory muscles (Finsterer, 2022). Not only that, but this bacterial infection also results in Miller-Fisher syndrome (MFS), which manifests as visual abnormalities (ophthalmoplegia) and coulometer weakness (areflexia and ataxia) (Ang et al., 2001). Campylobacteriosis is hyperendemic in underdeveloped nations, and infections with Campylobacter are symptomatic, virtually exclusively occurring in young children and babies (Coker et al., 2002). In adults or older children, the signs of this infection are uncommon since subsequent infections may be asymptomatic.

It is interesting to note that developed and developing nations have very different campylobacteriosis epidemiologies. Due to the lack of national systems for the surveillance of Campylobacter infections, it is challenging to assess the prevalence of Campylobacter infections in underdeveloped nations, since Campylobacter is not the most common cause of bacterial foodborne diseases (Platts-Mills and Kosek, 2014). Research articles on Campylobacter isolation from various specimens are the primary source of information regarding the prevalence of Campylobacter infections in underdeveloped nations (Chala et al., 2021).

Epidemiology

The epidemiology of campylobacteriosis varies significantly between low-, middle-, and high-income countries. These variations are most likely due to variations in food habits, nutritional status, environmental cleanliness, climatic conditions, immune system status (especially among elderly people and children) diagnostic methods, and the availability of natural reservoirs (Sanchez et al., 2020). Campylobacter infections are hyperendemic in children under the age of two, with up to two cases per child in low- and middle-income countries (Kiarie et al., 2023). Most cases in children and adults are asymptomatic. Campylobacter infections without symptoms are uncommon in high-income nations, but the average lifetime frequency of infections is less than one (Pascoe et al., 2020). Children are typically more likely to have Campylobacter infections, which suggests that early exposure may result in the formation of protective immunity but later asymptomatic shedding (Samie et al., 2022).

The exact nature of the global incidence rate of Campylobacter outbreaks is largely unclear, and reports of their incidence differ between nations. The underreporting of Campylobacter infection cases, variations in reporting systems, challenges in diagnosis, and variations in surveillance in the event of an outbreak are among the factors contributing to the inaccurate incidence of campylobacteriosis outbreaks. Outbreaks of campylobacteriosis typically result from multiple humans contracting food- or water-borne diseases, and the majority of these outbreaks are caused by animals (Llarena and Kivistö, 2020). Despite the fact that many people rely on rivers and streams as their main supply of drinking water, environmental sources like these are typically the source of campylobacteriosis outbreaks in low-income nations (Whiley et al., 2013). Apart from their role in the spread of human diseases in low-income nations, water sources have also been linked to epidemics of campylobacteriosis in high-income nations including Finland (Suominen et al., 2024), Canada (Guy et al., 2018), Norway (Hyllestad et al., 2020), Denmark (Boysen et al., 2014), and New Zealand (Gilpin et al., 2020).

There have also been reports of Campylobacter infections and outbreaks in both high- and low-income nations that are caused by milk. Milk consumption is associated with outbreaks of campylobacteriosis in a number of countries, including the United States (Jaakkonen et al., 2020), Sweden (Artursson et al., 2018), Italy (Bianchini et al., 2014), China (Li et al., 2020), Japan (Ohno et al., 2023), India (Modi et al., 2015), and the Netherlands (Heuvelink et al., 2009). Apart from that, other countries that have recorded campylobacteriosis outbreaks due to the consumption of poultry meat are Canada (Hodges et al., 2019), Australia (Keerthirathne et al., 2022), British Columbia (Hakeem and Lu, 2021), Belgium (Gellynck et al., 2008), Denmark (Kuhn et al., 2018), England (Royden et al., 2021), Germany (Stingl et al., 2012), Poland (Szosland-Fałtyn et al., 2018), New Zealand (Sears et al., 2011), Norway (Llarena et al., 2022), Madagascar (Randremanana et al., 2014), Kenya (Mbai et al., 2022), Indonesia (Yanestria et al., 2024b), Malawi (Mason et al., 2013), Iceland (Stern et al., 2003), Estonia (Tedersoo et al., 2022), Guatemala (Benoit et al., 2014), and Peru (Harvey et al., 2003).

Humans are susceptible to campylobacteriosis due to a wide range of risk factors. According to the most recent meta-analysis research, the main risk factor for campylobacteriosis is travel, which is followed by eating undercooked chicken, being exposed to the environment, and coming into close contact with livestock (Facciolà et al., 2017).

Reports from the United Kingdom indicate that the occurrence of campylobacteriosis is linked to a seasonal increase in fly populations throughout the summer because of high temperatures and rainy weather that promote fly development (Nichols, 2005). This leads to the flies coming into touch with animal and human feces, which supports the theory that environmental factors cause the seasonal epidemics that are common in the summer (Penakalapati et al., 2017). It was also discovered that both conventional and organic environmental factors were linked to campylobacteriosis. According to a different Danish study, human campylobacteriosis incidence rose in tandem with environmental temperatures, with the biggest rise in incidence occurring between 13°C and 20°C (Patrick et al., 2004).

Pathogenesis

Research on the pathogenesis of Campylobacter is curiously typically conducted on C. jejuni. Campylobacter has a complicated and poorly known survival strategy for getting past host barriers and producing sickness in humans. It is thought that 350–10,000 cells are necessary for a Campylobacter infection, and the infectious dose frequently corresponds with the severity of the disease (Janssen et al., 2008). Immunocompromised individuals, the elderly, and children are the most common groups to contract Campylobacter infections (El-Tras et al., 2015).

Campylobacter must cross the stomach’s gastric acid barrier and the upper small intestine’s bile duct’s extremely alkaline secretions after consuming tainted food or drink (Facciolà et al., 2017). Pathogenic microorganisms like Campylobacter can survive and proliferate when the stomach acid barrier is disrupted. Thus, individuals who take proton pump inhibitors and antacids, or who have lowered stomach acidity, may be more susceptible to campylobacteriosis (Janssen et al., 2008).

Once Campylobacter enters the lower digestive tract, it targets the distal ileum and colon epithelial cells, causing severe inflammation and cell destruction; however, in chickens, the cecum is a crucial location for Campylobacter colonization (Pang et al., 2023). C. jejuni is the source of invasive inflammatory illness in affluent nations. However, Campylobacter is the cause of non-inflammatory watery diarrhea in underdeveloped nations (Coker et al., 2002). Chemotaxis and motility are thought to be necessary for Campylobacter host colonization, adhesion, and invasion (Elmi et al., 2021). These bacteria require iron uptake, bile salt and gastric acid resistance, and oxidative stress tolerance for growth and survival (Kreling et al., 2020). Toxins produced by bacteria mediate tissue damage and inflammatory reactions (Callahan et al., 2021).

Numerous parameters related to survival and virulence are thought to have a major role in the pathophysiology and induction of gastroenteritis caused by Campylobacter spp. It is thought that the clinical and epidemiological aspects of the illness have an impact on the molecular mechanisms of Campylobacter infection.

Virulence factors

The expression of virulence has been linked to a number of genes. Virulence genes implicated in colonization and adhesion include racR, flaA (flagellin A gene), dnaJ, and cadF (adhesin gene) (Hermans et al., 2011). The genes that cause invasion are virulence plasmid genes (ciaB, virB11), and (invasion-associated gene A (iamA) (Kovács et al., 2020). Virulence genes implicated in the synthesis of lipopolysaccharides are β-1,3-galactosyltransferases-encoding genes (cgtB and wlaN) (Guirado et al., 2020). Vital pathogenic virulence genes for the expression of cytotoxin synthesis are cdtC, cdtB, and cdtA, or cytoletal bloating toxins C, B, and A (Talukder et al., 2008). The adaptability of Campylobacter to unfavorable environments and the host’s immune system seems to be one of the most crucial elements of intestinal colonization. Under the influence of chemoattractants, organisms enter the intestinal environment through fecal-oral transfer and populate the intestinal tract (Parker et al., 2020). Additionally, the proximal digestive system contains a number of antimicrobial proteins, including beta-defensin gallinacin-6 (van Dijk et al., 2007). There has been a great deal of research done on the virulence traits of Campylobacter, as these traits affect how pathogenic the species is. The ability of the Campylobacter genus, particularly its pathogenic species like C. jejuni, to live and tolerate physiological stressors contributes to its pathogenicity. These bacteria have a variety of virulence factors.

Chemotaxis

Campylobacter uses a process known as chemotaxis, which facilitates directed movement toward or away from chemical stimuli (effectors/chemo ligands, which can be either repellent or attractant) in the environment, to adapt to different environments (Kreling et al., 2020). Transducer-like protein (Tlps), which has a methyl acceptor domain, and core signal transduction protein make up the chemotaxis system (Clark et al., 2019). Ligands binding to Tlps send signals to cytoplasmic chemotaxis proteins, which in turn trigger a signal transduction cascade leading to directed movement of the flagella (Zautner et al., 2012). Campylobacter can more easily participate in substrate-specific chemotaxis when transducer-like proteins are present. This is crucial for the pathogen’s capacity to adapt, grow its pathobiology, and invade the gastrointestinal tract (Chandrashekhar et al., 2017).

Flagellar motility

Campylobacter’s motility is crucial to its survival in the digestive tract under a variety of circumstances. The mobility of flagella allows Campylobacter species to locate favorable environments within their hosts (Baldvinsson et al., 2014). The human foodborne pathogen C. jejuni produces two structural flagellins, FlaA and FlaG, that are heavily glycosylated by nature (Radomska et al., 2017).

Oxygen tension and oxidative stress defense

Campylobacter is able to withstand a number of adverse environmental conditions, such as pH fluctuations, oxygen restriction in the cecum, oxidative stress, elevated osmotic pressure, and the presence of digestive fluids, such as bile salts, from penetrating the digestive system (Kim et al., 2021). Peroxide resistance regulators and Campylobacter oxidative stress regulators control the expression of genes linked to oxidative stress resistance (Kim et al., 2015).

Bile resistance

Bile salt resistance is another requirement for C. jejuni to successfully colonize (Lin et al., 2003). Deoxycholate disrupts the lipid bilayer of the cell membrane and causes the unfolding and aggregation of proteins in the bacterial cytoplasm, killing detergent-like bile acids like cholate and bacteria (Talukdar et al., 2022).

Adhesion

Numerous adhesins produced by Campylobacter, both separately and in combination, have the ability to affect or mediate the attachment of bacteria to various cell structures and hosts (Kreling et al., 2020). The Campylobacter adhesion protein to fibronectin (CadF), a 37 kDa protein that binds to the fibronectin ligand present in epithelial cells and is expressed by the CadF gene, the adhesin that has been the subject of the greatest research (Konkel et al., 2020).

Invasion

In addition to their ability to survive intracellularly, several species of Campylobacter are known to secrete invasion antigens (Cia), such as CiaB, CiaC, and CiaI (Lopes et al., 2021). These virulence factors are essential for the bacteria’s ability to infiltrate epithelial cells and populate the digestive system of their host (Callahan et al., 2021).

Cytolethal distending toxin

The cytolethal distention toxin is a toxin that functions similarly to DNase to generate DNA damage that stops cell division and starts apoptosis (Méndez-Olvera et al., 2016). Due to the toxin’s parasitic nature, intestinal crypts are destroyed, which results in diarrhea.

Clinical symptoms

In humans

The clinical manifestations of human C. jejuni and C. coli enteritis are identical and cannot be distinguished from severe bacterial diarrhea brought on by other infections, such as Salmonella enteritis (Kemper and Hensel, 2023). A Campylobacter infection may result in fever, nausea, vomiting, and mild to severe bloody diarrhea (Tracz et al., 2005).

Stomach ache may reoccur and linger for up to seven days. In addition to more severe and persistent abdominal discomfort and occasionally blood or mucus in the stool, campylobacteriosis sickness might start with abdominal cramps, myalgia, diarrhea, chills, fever, headache, and occasionally delirium (Huayanay et al., 2020). Patients experience a lower percentage of extra-intestinal infections and chronic infectious problems. Less than 1% of patients with C. jejuni infection have been reported to have bacteremia (Gallo et al., 2016). Meningitis and endocarditis are uncommon signs of infection with C. jejuni (Tsoni et al., 2013). Rare cases of C. jejuni infections presenting as cystitis, acute cholecystitis, pancreatitis, and septic abortion have been reported (Vaughan-Shaw et al., 2010).

Additionally, a number of autoimmune illnesses, including GBS and RA, have been related to campylobacteriosis (Malik et al., 2022). It is expected that one occurrence of these two serious late-onset campylobacteriosis problems occurs for every 2000 infections (El-Saadony et al., 2023). As postinfectious polyneuropathy, Campylobacter infection is acknowledged as the most often identified antecedent event in GBS (40%–60% of all cases) (Poropatich et al., 2010). Acute inflammatory demyelinating polyradiculo-neuropathy is the major lesion, resulting in flaccid paralysis. About 1% of people with Campylobacter enteritis develop RA (Ajene et al., 2013).

In food and farm animals

Warm-blooded mammals and companion birds have Campylobacter spp. in their intestines as a component of their gut microbiota (Kreling et al., 2020). Many animal species are susceptible to enteritis, abortion, and infertility due to Campylobacter species (Dai et al., 2020). The role of C. jejuni as a major pathogen in livestock remains unclear. Enteritis is a common condition in dogs, cats, lambs, mink, calves, and certain types of laboratory animals caused by C. jejuni and occasionally C. coli (Facciolà et al., 2017). In young animals, the clinical indications could be more severe. Calves typically have thick, slimy diarrhea, sometimes with blood stains, and may or may not have a fever (Hansson et al., 2021). The enzootic abortion caused by C. fetus and C. jejuni can result in late-term abortion, stillbirth, and poor lambs (Wolf-Jäckel et al., 2020). In sheep, endometritis and occasionally even death can occur after infection (Sanad et al., 2014). In the event of an outbreak in sheep, morbidity could reach 90%, although it typically falls between 5% and 50%. Sheep morbidity can lead to delayed lambing and decreased milk yield (van den Brom et al., 2020). It is typical to recover with immunity against reinfection. Sheep may carry an infection for an extended period of time and continue to excrete bacteria (Ogden et al., 2009).

Diagnosis

Effective and rapid diagnosis of Campylobacter species infections in animal hosts is essential for both individual treatment and disease management at the farm level. Furthermore, prompt detection aids in the appropriate surveillance and monitoring of Campylobacter infections, which may be dangerous for human health due to zoonotic transmission.

Isolation and identification

A common procedure in Campylobacter species identification, which employs a range of commercially available media, is to enrich the sample in a suitable broth, like Bolton broth, and then isolate it by plating it on a particular medium, like modified cefoperazone deoxycholate charcoal medium (Bojanić et al., 2019). In research laboratories, a range of biochemical assays is typically conducted after bacterial separation, such as urease expression, oxidase and catalase production, nitrate and nitrite reduction, H₂S synthesis, and hydrolysis of indoxyl acetate and hippurate (Sadek et al., 2023).

Immunological tests

Campylobacter diagnosis can be achieved by a variety of enzyme immunoassay techniques, including flow cytometry, quantitative immunofluorescence, and enzyme-linked immunosorbent assays (ELISA). However, ELISA is the most effective method since it targets many particular antigens on the microorganism’s surface (Ricke et al., 2019). It is possible to generate monoclonal and polyclonal antibodies to recognize particular pathogen epitopes. Moreover, antibodies can be altered, which frequently calls for the conjugation of several detection systems, like horseradish peroxidase, to boost the specificity and sensitivity of identifying various target epitopes (Hochel et al., 2007). It is significant to remember that immune-based detection methods can produce false-positive results even while they are somewhat sensitive to Campylobacter species. This has been noted when comparing conventional molecular and microbiological techniques with commercial equipment.

Molecular diagnosis

DNA or RNA sequences that are unique and extremely particular are found using technologies based on nucleic acids (Effendi et al., 2018; Wibisono et al., 2021). After that, these sequences can be separated, amplified, and shown on gel for molecular typing, identification, and quantitative analysis. DNA sequencing and polymerase chain reaction (PCR) provide quick, easy, and accurate identification of Campylobacter species while exposing their epidemiological traits (Yanestria et al., 2023). This approach also makes it possible for researchers to produce data that can be shared via web-based databases and utilized in phylogenetic analyses. This technology is known by two names, quantitative PCR (qPCR) and real-time PCR (Sails et al., 2003).

Differential diagnosis

The clinical manifestations of avian campylobacteriosis resemble those of other enteric infections, including rota virus, Salmonella, Shigella, E. coli 0157:H7, Yersinia, Clostridium difficile, and Entamoeba histolytica (Sadek et al., 2023).

Poultry

One of the primary ways that humans contract campylobacteriosis is through poultry, particularly from broiler chickens (Yanestria et al., 2024a). Furthermore, the chicken industry serves as a significant reservoir for additional Campylobacter species, including C. jejuni, C. lari, and C. upsaliensis (Skarp et al., 2016). Worldwide, the prevalence of campylobacteriosis and other Campylobacter infections is increased by both indigenous and imported broiler chickens (Carron et al., 2018). Additionally, Campylobacter can enter broiler chicken houses through vectors like flies, insects, or rodents, or it can travel through vehicles in the form of dust or aerosols. It can also be disseminated through excrement and be found everywhere in the environment, including surface water (Bahrndorff et al., 2013).

Domestic animals

In addition to a broad range of food products derived from animal groups, such as poultry, household animals (particularly cats and dogs) are the most common source of infection (Acke, 2018) and livestock are significant transmission vectors. Campylobacter bacteria can also be found in ruminant animals including cows, sheep, and goats (Hoque et al., 2021; Sanad et al., 2014; Cortés et al., 2006). Rather than in the rumen, Campylobacter bacteria are primarily located in the gut (duodenum, jejunum, and small and large intestine) (Chlebicz and Śliżewska, 2018). Therefore, there is a substantial danger of Campylobacter species transmission and spread when consuming meat from domestic animals or coming into touch with pets and companion animals.

Wildlife

Campylobacter species (particularly, C. jejuni and C. coli) are mostly commensals in birds, and they frequently invade the intestines in huge numbers (Hald et al., 2016). Wild animals can function as reservoirs in addition to acting as transmission vectors, such as wild birds (Olvera-Ramírez et al., 2023). It has been possible to isolate C. jejuni from wild birds, including pigeons, seagulls, geese, crows, ducks, and herons (Marotta et al., 2020). It is interesting to note that migrating birds have the ability to travel great distances and may provide novel genotypes of the Campylobacter species to various animals, including sheep, cattle, and broilers (Shad and Shad, 2019). Furthermore, wild birds congregate in metropolitan parks and recreation areas, particularly pigeons and crows. As a result, individuals with poor or neglected hygiene practices as well as children are more vulnerable to acquiring Campylobacter infections.

Water

According to a number of earlier studies, drinking water poses the greatest risk to the spread of campylobacteriosis (Ferrari et al., 2019; Whiley et al., 2013). The ability of Campylobacter to form a biofilm in the water pipes of broiler chicken houses contributes to the species’ increased growth and survival and is a key risk factor for colonization in chicken flocks (Pokhrel et al., 2022). Recent research conducted in Ireland found that on seven out of twenty farms, there were serious issues with getting rid of Campylobacter species colonies in water pipes following disinfection (Battersby et al., 2017). More people than any other documented enteric disease are at risk of contracting campylobacteriosis when they drink water from private wells as opposed to municipal surface water systems (Galanis et al., 2014). Another factor in the spread of Campylobacter is contaminated pet waste and wild bird droppings that pollute outdoor water sources (Pitkänen, 2013).

Other sources

Person-to-person transmission, whether by fomites or faecal-oral routes, is uncommon but has great potential and a propensity to spread. There is a documented 3% person-to-person transmission of campylobacteriosis in the United Kingdom (Wensley et al., 2020). The ingestion of raw milk derived from dairy cows has also been linked to numerous cases of campylobacteriosis outbreaks (An et al., 2018). Several other Campylobacter species, such as C. hyointestinalis, C. fetus, and C. ureolyticus, can also be found in unpasteurized milk (Koziel et al., 2012; Koziel et al., 2014; Grouteau et al., 2023). A genomic study of the milk revealed a considerable level of fecal contamination. Campylobacter infections can also be dangerously transmitted by insects such as flies, roaming animals, and chicken products (Royden et al., 2016; Frosth et al., 2020).

Treatment

The best antibiotic medications for eradicating and decreasing Campylobacter in feces are erythromycin, clarithromycin, or azithromycin (Wieczorek and Osek, 2013). If therapy was initiated prior to the third day after the onset of symptoms, there was a noticeable improvement. Research on children with C. jejuni-caused diarrhea revealed that early erythromycin treatment led to a significant improvement in symptoms (Munoz et al., 2022). Clinical experience and controlled research demonstrate that patients with high fever, bloody stools, diarrhea, and more than eight evacuations per day respond better to antibiotic treatment (Eiland and Jenkins, 2008).

Despite the lack of animal clinical efficacy trials, it has been reported that dogs and cats can recover from this illness when given erythromycin, the recommended medication for humans, three times a day for seven days at a dose of 11.1 to 15.5 mg/kg (Gibreel and Taylor, 2006). There is currently discussion about Campylobacter resistance to widely used antimicrobials in both veterinary and human situations.

In the past 20 years, there has been a noticeable rise in the amount of antibiotic resistance in bacteria isolated from humans, particularly to fluoroquinolones (Luangtongkum et al., 2009). This high level of resistance is still present today in many parts of the world. The first-choice medications for treating adult campylobacteriosis are those in the fluoroquinolone class (Portes et al., 2023). Global reports relate the approval of the use of these antimicrobials in poultry production to Campylobacter sp. infections that are resistant to fluoroquinolones (Zhao et al., 2010).

Rastall (2004) looked into alternate sources to antibiotics for the treatment of campylobacteriosis and discovered that probiotics (Lactobacillus acidophilus) combined with prebiotics (fructooligosaccharides and lactosucrose) had a positive impact on the balance of intestinal microflora, improved immune status, and aided in the recovery from campylobacteriosis infection. Following the usage of probiotics, pathogens are competitively excluded, resulting in this microflora balance.

Antibiotic resistance

In the US, 1% of C. jejuni strain isolates from infections in humans in 2010 had erythromycin resistance, compared to 43% for tetracycline and 22% for ciprofloxacin (Rodrigues et al., 2021). Almost the same data were reported in the same year about C. jejuni strain isolates from chicken flesh. In 2010, strains of C. jejuni recovered from chicken flesh in the European Union showed resistance to erythromycin in 2% of cases, tetracyclines in 21%, and fluoroquinolones in 52% of cases (Marotta et al., 2023). Antibiotic resistance in C. coli is higher than in C. jejuni in the US and Europe. The frequent use of veterinary antibiotics (enrofloxacin and danofloxacin) in the pharmacological treatment of chickens appears to be the root cause of the high level of resistance to fluoroquinolones (Cox and Popken, 2006). Consequently, the use of fluoroquinolones in chickens was outlawed in the US in 2005 (Price et al., 2007). Resistance to these antibiotics is uncommon in Australia, where the use of fluoroquinolones has not been allowed (Cheng et al., 2012). It is well recognized that travel, in both industrialized and developing nations, is often linked to fluoroquinolone-resistant illnesses. According to a recent study by Ghunaim et al. (2015), C. jejuni’s erythromycin resistance was comparatively low, accounting for just 8.6% of isolates, while ciprofloxacin resistance accounted for 63.2% of isolates. There have also been reports of high ciprofloxacin resistance in the United Arab Emirates, where 85.4% of isolates exhibited resistance (Sonnevend et al., 2006). Published ciprofloxacin resistance rates were 2% in Australia (Bell et al., 2022) and 40% lower in Poland (Jeżak and Kozajda, 2022).

Azithromycin, a macrolide, is typically the next line of treatment when resistance to these medications is established, yet resistance to this class of antibiotics has also been documented (Dai et al., 2020). The use of antibiotics indiscriminately at different points in the chicken production chain can contribute to the establishment of resistant forms of campylobacteriosis since the disease is spread through food consumption (Epps et al., 2013). Therapeutic options are limited due to the emergence of strains that are resistant to various medicines, including the antibiotics of choice for humans.

Control

The best strategy to reduce the number of human infections caused by Campylobacter is to restrict the amount of contamination of the poultry flock and its products, even if the majority of infections are contracted through the handling or consumption of chicken (Newell et al., 2011). A common way to stop Campylobacter infection outbreaks is to steer clear of unpasteurized milk (Facciolà et al., 2017; Tyasningsih et al., 2022). It is important to stress that those who are pregnant, have young children, are elderly, have weakened immune systems, are visiting low- or middle-income countries, or are campers should not drink unclean water (Asuming-Bediako et al., 2019).

Farm

Both domestic and wild animals, as well as the environment, frequently contract campylobacteriosis. As a result, it is critical to lessen the amount of contamination from these sources in chicken coops. It has been shown that using hygiene barriers at poultry house’s entrances, limiting the access of livestock workers, offering hand washing stations, putting in place boot dips, and using specific house boots and overshoes, are all beneficial practices (Wagenaar et al., 2006). One efficient way to stop the spread of contamination in slaughterhouses is to segregate Campylobacter-positive animals from negative animals and to kill Campylobacter-positive animals (Taha-Abdelaziz et al., 2023). It has been demonstrated that more frequent emptying and cleaning of water troughs lowers the chance of Campylobacter colonization in animals (Ellis-Iversen et al., 2009).

Food animals processing

Large concentrations of Campylobacter are found in the digestive tracts of chickens, and these bacteria have the ability to contaminate food products, the environment, and slaughterhouses (Kreling et al., 2020). At this stage, the amount of Campylobacter organisms is decreased by treatment with organic acids, UV radiation, and chemical dipping tanks for corpses (Szott et al., 2022). Reducing the amount of bacteria in the kitchen through heating, freezing, or radiation eliminates pathogens and lowers the degree of cross-contamination (Taha-Abdelaziz et al., 2023).

Home

The prevention of Campylobacter species infection depends on proper food preparation and consumption practices. It is possible to guarantee that temperatures high enough to destroy Campylobacter species organisms are reached by using a meat thermometer and properly cooking the meat (de Jong et al., 2012). After handling raw poultry or other meats, cutting boards and cutlery should be cleaned in hot, soapy water and used again to prepare other raw meals (Luber et al., 2006). Hand washing and the separation of raw and ready-to-eat food must be put into practice. Individuals experiencing acute diarrheal illness ought to refrain from handling and preparing food until the condition has resolved (Hatchette and Farina, 2011). Eating raw meat, unpasteurized dairy products and exposure to animals such as pets suffering from diarrhea should be avoided (Facciolà et al., 2017). Prior to eating, everyone should wash their hands, especially if they are handling pets or other animals (Taha-Abdelaziz et al., 2023).

Vaccination

The most effective control strategy is generally thought to be vaccination against Campylobacter. Numerous field and experimental investigations on sheep and experimental research on guinea pigs have shown the efficacy of vaccination (Burrough et al., 2010). However, there is limited cross-protection between strains or species, numerous strains of a species may be involved in the disease, and abortion can be induced by two or more separate species (C. fetus, C. jejuni, and C. coli) (Costa and Iraola, 2019). These factors make immunization complex. Therefore, even after using polyvalent vaccinations, vaccination may not offer full protection.

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Conclusion

The primary cause of the infectious disease, campylobacteriosis, is the Campylobacter species. Campylobacter is an emerging global foodborne bacterial pathogen attributed to the cause of foodborne diseases and death, resulting in enormous social and economic losses. Campylobacteriosis is particularly prevalent in the paediatric and elderly population. This illness is zoonotic, which means that eating certain foods can spread it from animals to people.

Campylobacter has been isolated from farm animals and foods of animal origin. Worldwide, poultry and their by-products remain the major cause of foodborne illnesses, especially campylobacteriosis. The prevention of Campylobacter species infection depends on proper food preparation and consumption practices. The consumption of undercooked poultry products and the contamination of carcasses and other food products continue to be an important public health concern. More challenging is the increasing incidence, emergence, and spread of antibiotic-resistant Campylobacter species which has further complicated and limited treatment options. In order to curtail and avert this challenging public health problem, it is imperative to establish strong measures that are directed towards its eradication, especially good hygienic practices during food handling. Efforts to curtail Campylobacter contamination in the food industry also need to become a more determined priority. To comprehensively understand the disease burden of campylobacteriosis, more research studies with multiple intervention within the “one health” approach are needed to evaluate the under-reporting of diarrhoea incidents at national and intercontinental levels by enhancing and encouraging local capacities for continuous disease surveillance and monitoring. Also, more research that will devise alternative strategies or new therapeutics against campylobacteriosis will also greatly help in turning the tide against this emerging foodborne and zoonotic disease.

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Acknowledgment

The authors thank Universitas Airlangga and Badan Riset dan Inovasi Nasional.

Authors’ contributions

ARK, IBM, and MKJK drafted the manuscript. SRA, MHE, FNAEPD, and SMY revised and edited the manuscript. OSMS, IF, AHF, and KHPR took part in preparing and critically checking this manuscript. AH, KAF, RR, and SA edited the references. All authors read and approved the final manuscript.

Funding

This study was funded in part by the Airlangga Article Review funding from Lembaga Penelitian dan Pengabdian Masyarakat Universitas Airlangga, Indonesia, in the fiscal year 2024, with grant number: 323/UN3.LPPM/PT.01.03/2024.

Conflict of interest

The authors declare that there is no conflict of interest.

Data availability

All references are open access, so data can be obtained from the online web.

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