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Campylobacter: An Emerging Pathogen



M. Baserisalehi , N. Bahador and B.P. Kapadnis
 
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ABSTRACT

During the past decade Campylobacter has been shown to be responsible for enteritis in human and animal. The natural habitats of most Campylobacter species are the intestines of birds and other warm-blooded animals. These organisms may enter the environment, including drinking water, through the feces of animals, birds or infected humans. Campylobacter survive in aqueous environment for several weeks at temperature around 4°C and may enter the human food chain at slaughter of the animals. Although, many methods and media have been developed for detection of the Campylobacter from various samples, universally accepted methods and media are not available yet. Milk, mushrooms, hamburger, pork, shellfish and eggs are vehicles of Campylobacter however, most Campylobacter enteritis acquired by the consumption and handling of poultry. The sensitivity of Campylobacter to heat, acidic pH, food preservatives and irradiation must be considered as plus points to prevent of Campylobacter transmission to human beings. On the other hand, the antibiotic resistant character of Campylobacter is a negative point for control of Campylobacter infection in developed and developing countries. Campylobacter is usually causes a self-limited illness, but in more severe cases of gastroenteritis, antibiotics are usually begun before culture results are known. Nowadays, antibiotics such as erythromycin and ciprofloxacin have been recommended for treatment of campylobacteriosis however, resistance to these antibiotics has been rising.

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M. Baserisalehi , N. Bahador and B.P. Kapadnis , 2006. Campylobacter: An Emerging Pathogen. Research Journal of Microbiology, 1: 23-37.

DOI: 10.3923/jm.2006.23.37

URL: https://scialert.net/abstract/?doi=jm.2006.23.37

Biology of Campylobacter

In the beginning of the 20th century Vibrio fetus was found to be responsible for spontaneous abortions in cattle and sheep (Allos 2001). This organism unlike Vibrio species didn’t grow well under atmospheric oxygen tension and did not ferment sugars. In 1963 Sebald and Veron suggested the name Campylobacter for this organism to differentiate it from Vibrio species (Catteau, 1995). Campylobacters are microaerophilic, nonproteolytic, nonlipolytic and nonsaccharolytic, so they neither ferment nor oxidize carbohydrates. Hence, they obtain energy from oxidation of amino acids or tricarboxylic acids (Grau, 1991).

The genus Campylobacter contains 16 species and 6 subspecies (On, 2001), Many of these species have been implicated in human enteritis. But the most common cause of Campylobacter enteritis is 'thermophilic' campylobacters viz., Camp. jejuni, Camp. coli, Camp. lari and Camp. upsaliensis. The term 'thermophilic' for some species of Campylobacter is proposed not because of their ability to grow at high temperatures but to emphasize their inability to grow below 30°C. The optimum temperature and microaerophilic nature of thermophilic Campylobacter indicates that they arenot likely to be able grow outside of the mammalian gut. Thermophilic Campylobacter cannot grow in food or in water and therefore they should be considered 'food-borne' rather than 'food-poisoning' organisms (Stanley et al., 2003).

Camp. jejuni is the most commonly identified species (Nachamkin et al., 1992) and was formerly named Camp. fetus subsp. jejuni. It differs from the other species in that it is hippurate positive (Catteau, 1995). The other species of thermophilic Campylobacter such as Camp. coli and Camp. lari have also been associated with enteric disease in human (Barros-Velázequez et al., 1999) Nowadays Camp. hyointestinalis also identified as cause of enteric disease in cattle (Trachoo, 2003).

Gasteroenteritis caused by Campylobacter spp. has been recognized as one of the important public health problems in the developed countries (Chaveerach et al., 2002). Camp. jejuni, Camp. coli and Camp. lari are the most important pathogenic species of thermophilic campylobacters (Skirrow, 1994). Food is the most common vehicle for transmission of Campylobacter and some studies indicate that up to 70% of sporadic cases of campylobacteriosis were associated with eating chicken (Fang et al., 1991; Scott et al., 1998). Other identified food vehicles of campylobacters in developed countries include unpasteurized milk, undercooked meats, mushrooms, hamburger, cheese, pork, shellfish and eggs (Alterkruse et al., 1999). Several studies have revealed that 30-100% of poultry, 40% of cattle and 60-80% of swine carry campylobacters in their intestinal tract; hence, campylobacters are associated with foods of animal origin (Doyle, 1984). Household pets with diarrhea have often been shown to be the source of infection for man (Frost, 2001). Few hundred cells of Campylobacter can produce illness in babies; young children and debilitated people. Symptoms of the infection vary from mild (watery diaarea) to severe (bloody diarrhoea). Other symptoms are fever, nausea, abdominal cramps and (seldom) vomiting (Ketley, 1997).

Sources of Campylobacter

Most of the campylobacters grow at 37 and 42°C under microaerophilic conditions. These characters help pathogenic Campylobacter to grow in their natural habitat (intestine of warm-blooded birds and mammals). Poultry is the primary food vehicle for Campylobacter. Some studies indicate that up to 70% of sporadic cases of campylobacteriosis are associated with eating chicken. “Surveys by the USDA demonstrated that up to 88% of broiler chicken carcasses in the USA are contaminated with Campylobacter” (Anonymous, 1998). Inglis et al. (2004) reported that animal faeces are sources of a large number of Camp. lanienae and Camp. jejuni cells and suggested that Camp. lanienae may be pathogenic to cattle and that novel species of Campylobacter may occur within their GI tracts.

In general food, particularly the surface of meat could be contaminated with Camp. jejuni though contact with feces, but it should be noted that the Camp. jejuni do not multiply in food the temperature is lower than 30°C Although, Campylobacter survive at 4°C, these bacteria are sensitive to heat (Uradzinski et al., 1993). Therefore, pasteurization of milk and adequate cooking of meat will destroy this organism (Doyle, 1998).

Survival of Campylobacters in Environment

The morphology of Campylobacter spp. changes with age in culture media and varies from a spiral (predominant in young cultures) to coccoidal form (predominant in older cultures). The formation of these coccoidal forms may represent a physiological response of these bacteria to environmental stress including heat. The natural habitat of the campylobacters has been identified as the gut of human and animals. Therefore, this form of the campylobacters may provide a protective means to survive under adverse environmental conditions outside the intestinal tract of the animals (Smibert, 1978). Konkel et al. (1998) have reported the thermal stress response in Camp. jejuni due to the presence of 24 heat-shock proteins. Moore and Madden (2000) stated that presence of the heat-shock proteins in Camp. jejuni enable them to survive sublethal thermal shock, such as mild thermal processes or pasteurization.

Despite the susceptibility of Camp. jejuni to atmospheric oxygen and its inability to grow at ambient temperature, this bacterium has been isolated from natural aquatic environments including river water, ground water, coastal water and lake water (Hanninen et al., 1998). Stelzer et al. (1988) stated that wastewater could be considered as a source of Camp. jejuni. Bolton et al. (1987) observed that the river waters contain a variety of Campylobacter spp., which could be considered as a potential source of Camp. jejuni. Buswell et al. (1998) explained that Camp. jejuni collected from various aquatic systems and at various temperatures (4, 10, 22 and 37°C) could not grow on conventional media. Kusters et al. (1997) and Federighi et al. (1998) have reported that the exposure of Campylobacter isolates to an aquatic environment resulted in loss of their culturability.

Pickert and Botzenhart (1985) tested the survival of Camp. jejuni in drinking water, river water and sewage and reported that Camp. jejuni could only survive for a few days. This study showed that the concentration of oxygen or nutrients in the water did not affect the survival of Camp. jejuni. Maximal survival of Campylobacter spp. has been reported at low temperatures for four months (Rollins et al., 1986).

Isolation Techniques and Media

Isolation of campylobacters was not successful until 1972. In 1972 Dekeyser et al. isolated Campylobacter jejuni from faeces by culturing filtrate on a blood-thioglycolate agar medium containing bacitracin, polymyxin B sulfate, novobiocin and actidione.

In 1977 Skirrow isolate Campylobacter from faeces on a selective medium, this medium was blood agar supplemented with trimethoprim, polymyxin B and vancomycin. Blaser et al. (1979) developed the Campy-BAP medium. Another selective medium is Campylosel (Biomerieux), which comprises cefoperazone vancomycin and amphotericin B as selective agents. Bolton et al. (1982) developed the Preston medium, useful to isolate Campylobacter spp. from environmental samples. The efficiency of this medium for the isolation of Campylobacter was checked on various samples such as faeces and water. The results obtained indicated that some strains of Camp. coli were sensitive to polymyxin B (Barros-Velázquez et al., 1999).

Since blood is an expensive component and its quality is variable, Bolton et al. (1984) replaced it with charcoal. These authors described the Charcoal Cefoperazone Deoxycholate Agar medium (CCDA). Walmsley et al. (1989) isolated Camp. upsaliensis on both media CSM (Charcol-based selective medium) and SKM (Skirrow medium) without preliminary enrichment or filtration steps. In addition, Aspinall et al. (1993) formulated another blood-free selective medium viz., CAT (Cefoperazone, Amphotericin B, Teichoplanin) for the isolation of Campylobacter at 37°C. This medium contained cefoperazone, amphotericin B and teichoplanin as selective agents. CAT medium selected Camp. upsaliensis better than the CCDA medium (Byrne et al., 2001).

A most probable number method was developed for the enumeration of Campylobcters from environment samples based on Preston enrichment broth by Bolton et al. (1982). It was stated, “It is sometimes advisable to use an enrichment step for the isolation of Campylobacter spp. The enrichment step may increase the isolation rate of campylobacters, especially when the microbial load in the sample is low”. Tran (1998) devised a new blood-free enrichment broth (BFEB), which enabled Camp. jejuni strains to be isolated under aerobic conditions.

At first membrane-filtration techniques were designed for the isolation of Vibrio fetus (Camp. fetus) from cattle and later from human beings. Unlike many bacteria, campylobacters usually pass through 0.45 μm pore size filters. To perform this technique, 10% suspension of faeces was passed through the membrane-filter and the filtrate inoculated onto the plate containing selective medium (Barros-Velázquez et al., 1999).

Ribeiro et al. (1984) reported that the filters in Preston enrichment medium increased the isolation rate of Campylobacter. Another method that recommended by them was centrifugation of sample and further seeding of the bacterial sediment in selective medium.

In general, all conventional selective media for isolation of Campylobacter spp. incorporate different antibiotics as selective agents in order to achieve maximum isolation rates. However, unfortunately some strains of Campylobacter are sensitive to some of the antibiotics in the media (Corry et al., 1995). Thus for isolation of these strains a membrane filter method, which relies on the ability of Campylobacter and other bacteria, e.g., Helicobacter, to pass through a 0.45 or 0.65 μm pore size membrane filter, was recommended. Non-selective media may then be inoculated with the filtrate. However, variation in the different brands of membrane filters may lead to inconsistencies. In the results it has been considered that only 10% of these organisms to pass through the filter (Steele et al., 1984). It should also be noted that the membrane filter method depends on the ability of the motile bacteria small enough to pass through the pore of filter onto the non-selective growth medium, while some species with cell bodies too large or with specific growth requirements would not be isolated by this method (Engberg et al., 2000). On the other hand, Kulkarni et al. (2002) expressed that the combination of the current methods (filter technique and conventional technique) would not detect the unusual species of campylobacters.

Recently Baserisalehi et al. (2004a) recommended Kapadnis-Baseri device (KB device) and sample processing-Kapadnis Baseri medium (preT-KB method) (Baserisalehi et al., 2004b) for isolation of Campylobacter spp. from environmental samples without using antibiotics. The KB device was designed based on motility and activity of campylobactes at low temperature and enables to isolate and enumerate Campylobacter spp. from the environmental samples. The preT-KB method was recommended for selective isolation of Campylobacter spp. from environmental samples based on elimination of competing bacteria at the sample and culture levels. The preT minimizes most of the competing bacteria at the sample level and the KB medium without blood and antibiotic is selective and differential eliminate rest of the competing bacteria and differentiate Campylobacter from the other Gram negative bacteria at the culture level.

Incubation Conditions
The thermotolerant campylobacters viz., Camp. jejuni, Camp. coli, Camp. lari and Camp. upsaliensis grow well at 42-43°C. Although the optimum temperature for the growth thermophilic Campylobacter is 42-43°C, they can grow at 37°C but not below 30°C or above 47°C (Barros-Velázquez et al., 1999). All species of Campylobacter are strictly microaerophilic; i.e. they exhibit growth at low oxygen tension and oxygen acts as final electron acceptor during respiration process, but they do not tolerate the atmospheric oxygen concentration (21% v/v). Campylobacter spp. requires oxygen concentrations ranging from 5-10%. They also require 1-15% carbon dioxide concentration to grow (Barros-Velázquez et al., 1999). Several methods and commercial systems such as the Gas Generating Kits and the Campy-Pak system have been developed provide microaerophilic atmosphere anaerobic jar for growth of the organisms. Gas mixture containing (v/v) 15% carbon dioxide and 80% nitrogen and 5% oxygen is another technique to provide microaerophilic conditions for growth of the campylobacters during incubation. To provide microaerophilic conditions in anaerobic jar, air must be removed by vacuum technique and replaced it by gas mixture (Barros-Velázequez et al., 1999).

Effect of Temperature, Food Preservatives and Irradiation on Campylobacter

Campylobacters are more sensitive to heat than other Gram-negative pathogens (ICMSF, 1996). The effect of spraying chicken carcasses with water at different temperatures (20, 55 and 60°C) on survival of Camp. jejuni was investigated by Li et al. (2002). Their results indicated that the 55 and 60°C water spray treatments significantly reduced Campylobacter by more than 0.78 log cfu/carcass compared with the 20°C water spray treatment. However, with 50 ppm chlorine spray treatment at three different temperatures the reduction of Campylobacter population was not significantly different. The chilling process with 50 ppm chlorinated ice water at 4°C reduced more Camp. jejuni (approximately 1 log CFU/carcass) among the water spray treatments but did not result in greater reduction of Camp. jejuni among the chlorine spray treatments. In general, campylobacters are rapidly inactive by heating at 55°C and above (Anonymous, 2001).

Effect of food preservatives on survival of five strains of Camp. jejuni (Pen 2, 3, 6, 10 and 20) was studied by Uradzinski et al. (1993). Their results indicated that the chemical preservatives added to meat sample at concentrations usually used in meat processing affected in differential way the survival of different strains of Camp. jejuni. Campylobacter jejuni Pen 2 was resistant to all preservatives. Pen 3 and Pen 10 were sensitive to sodium nitrate and Pen 10 was also sensitive to sodium chloride. Camp. jejuni Pen 20 was sensitive to sodium chloride, but potassium nitrate, sodium ascorbate and Hamine stimulated growth of this strain. Kelana et al. (2003a) studied the effects of storage temperature (4, 22 and 30 °C), pH (4.0 to 8.5) and sodium chloride concentration (0.25 to 7.5% w/v) on the survival of Campylobacter jejuni ATCC 35921 in Mueller-Hinton broth under aerobic conditions. At comparable pH, Camp. jejuni cells die most rapidly at 30°C and most slowly at 4°C. At 4°C Camp. jejuni was sensitive to 2.5% NaCl concentration. However, the level of inactivation at this storage temperature was also significantly lower than that observed at 20 and 30°C. In an additional experiment they reported that the minimum, optimum and maximum temperatures for the growth of Camp. jejuni ATCC 35921 in solid media were found to be 30, 40 and 45°C, respectively. At optimum growth temperature, Camp. jejuni ATCC 35921 was able to grow well at pH 5.5 to 8.0 and in the presence of 1.70 to 1.75% NaCl. At its minimum growth temperature, however, Camp. jejuni ATCC 35921 could grow only at pHs 6.5 to 8.0 and the presence of 0.5% NaCl. L-Fucose, D-fucose and sodium desoxycholate were shown to inhibit the growth of Camp. jejuni (Kelana et al., 2003b). Campylobacter growth is inhibited in foods at less than pH 4.9 and above pH 9. They are rapidly inactivated in foods at pH <4.0 especially at above refrigeration temperatures. Campylobacters are sensitive to low water activity (dryness) but under certain refrigeration conditions can remain viable for several weeks (Anonyomus, 2001).

Growth and survival of Camp. jejuni and Camp. coli at different temperatures (-20, 4 and 25°C) on pieces of raw chicken and pork were investigated by Solow et al. (2003). In their experiment Campylobacter sp. (104 CFU cm-2) were inoculated on pieces of raw, irradiated chicken or pork skin and exposed to temperatures ranging from -20, 4 and 25°C under either microaerobic or aerobic conditions. Their results indicated that viable count over 48 h declined 2 or 3 log CFU cm-2 at -20°C and 1 to 2 log CFU cm-2 at 25°C regardless of skin type, species of Campylobacter, or level of oxygen. At 4°C there was no significant change in the number of Campylobacter over 48 h. At both 37 and 42°C, the number of viable Camylobacter increased significantly (2 to 3 CFU cm-2) under microaerophilic conditions but decreased significantly (2 to 3 log CFU cm-2) under aerobic conditions.

Chaveerach et al. (2002) evaluated the effect of organic acids on survival of Campylobacter spp. Ten strains of Campylobacter spp. were mixed with water of broiler feed separately and pH of the mixtures was adjusted to 4.0, 4.5, 5.0 and 5.5 by four acids viz., formic, acetic, propionic and hydrochloric acids. A combination of three organic acids was used in two different formulations ratios viz., formic: acetic: propionic in 1:2:3 and 1: 2: 5 proportion, at pH 4.0, 4.5, 5.0 and 5.5. The individual acids and their mixtures showed the strongest bactericidal effect on Campylobacter at pH 4.0 (the lowest pH tested). In contrast; at pH 5.0 and 5.5, the bactericidal activity of the four acids was low. The combination of organic acids showed a synergistic bactericidal activity at pH 4.5. The effect of the combined organic acids was stronger than the commercial products. Morphological cell changes were also studied by transmission electron microscope to determine the effect of the organic acids on the cell structure of Campylobacter. Some loss of outer membranes of the bacteria was found in treated groups. Therefore, based on their study, we can conclude that organic acids, individually or in combination, have a strong bactericidal effect on Campylobacter spp., their routine application to the water supply or in the feed of poultry farms could prevent or reduce Campylobacter transmission (Chaveerach et al., 2002).

Diker et al. (1987) investigated effect of three disinfectants on survival of Campylobacter jejuni isolated from poultry. In this study the bacteria were suspended in two-fold dilutions of ethyl alcohol, formalin and benzalkonium chloride and viable count determined at different time intervals (1 to 60 min). The results indicated that seventy percent ethyl alcohol and 2.5% of formalin killed all bacteria within one minute. Benzalkonium chloride (1:50.000) was effective against all bacteria within 5 min. Based on these results they concluded the recommended standard concentrations of disinfectants studied are adequate to destroy Camp. jejuni.

Campylobacters are more sensitive to gamma radiation than most vegetative Gram-negative bacteria including: Salmonella and E. coli with D values of about 0.12-0.32 KGy in chilled meat (Collins et al., 1996). Bhavsar et al. (2004) evaluated the effect of gamma radiation on survival of two strains of Camp. sputorum and Camp. coli in different food products. According to their report the effect of gamma radiation was dependent upon the medium in which the campylobacters were treated, e.g., the D10 value of Camp. sputorum was 2 KGy when it was in milk while 0.5-0.6 KGy when in meat. The D10 value of Camp. coli was 0.2-0.4 KGy when in meat, while 1.17 KGy when in milk. Based on these data they concluded that the effect of gamma radiation on the Campylobacter spp. varied with the type of food. These results were in accordance with those by Patterson (1995) who checked the sensitivity of Campylobacter spp. to gamma radiation, in poultry meat. These isolates were sensitive to 2.4 KGy, which is within the FDA limit of 3 KGy. Higher sensitivity of Camp. jejuni to UV light than other Gram-negative bacteria such as E. coli or Y. enterocolitica was also reported by Butler et al. (1987).

Plasmid Profile and Antimicrobial Susceptibility of Campylobacters

The probability of occurrence of plasmid in Campylobacter jejuni strain has been reported vary from 19to 53% (Bradbury et al., 1983) and many of them are R plasmids that are transmissible among Campylobacter spp. (Taylor, 1983; Tenover et al., 1985). Despite the importance of plasmids in virulence of numerous other pathogens, It is not confirmed that plasmids play role in the virulence of Campylobacvter or no. This paradigm is based on comparative study of the plasmid content and relative virulence of different Camp. jejuni strains in a guinea pig model of disease (Taylor et al., 1984).

Yao and Guerry (unpublished data) isolated two plasmids from Camp. jejuni strain 81-176, one of them is R plasmid that encodes tetracycline resistance and second one encodes proteins which display strong similarity to H. pylori proteins. Moreover, they reported that the mutation of two of these genes affect the virulence of Camp. jejuni 81-176 (Bacon et al., 2000). However, the presence of plasmids in clinical isolates of H. pylori did not have any correlation with their antibiotic resistance pattern (Dharmalingam et al., 2003).

Antimicrobial susceptibility of Camp. jejuni to antibiotics was studied by Tremblay et al. (2003). According to them all isolates were susceptible to ampicillin, gentamicin, meropenem and imipenem, with 90% minimal inhibitory concentrations of 4, 1, 0.12 and ≤0.06 μg mL-1, respectively. Three and two percent of the strains were, respectively, resistant and intermediate to ciprofloxacin. Thirty-four percent of the strains were resistant to tetracycline. There was a insignificant increase in resistance to ciprofloxacin and to tetracycline in recent years The percentage of intermediate and resistant MICs were, respectively, 12 and 1% for cefotaxime, 71 and 0% for erythromycin, all strains were β-lactamase negative. Lariviere et al. (1986) the majority of thermophilic Campylobacter spp. are resistant to most β-lactam antimicrobial agents. Therefore, patients suffering from acute Campylobacter enteritis are treated with erythromycin. Tetracycline is rarely used, because tetracycline resistance is plasmid mediated (Taylor et al., 1986). Resistant bacteria from animals can reach the human population by direct contact and also via food products of animal origin (Van den Bogaard et al., 2000). The consumption of poultry meat has been commonly associated with the development of Campylobacter enteritis (Deming et al., 1987). Resistance amongst broiler isolates of Campylobacter species may have implications in the treatment of poultry acquired Campylobacter infections.

In animals and humans, the use of antibiotics may cause an increase in the resistance of their endogenous flora. Intensive production of animals used as food sources for human such as broiler farming depends heavily on the usage of antimicrobial agents for both veterinary and growth promotion purposes (Van den Bogaard et al., 2000). However, Fallon et al. (2003), reported that the majority of Camp. jejuni strains isolated from poultry in Ireland were susceptible to antibiotics commonly used for human therapy, Camp. coli strains showed very low resistance levels and were susceptible to chloramphenicol, kanamycin, streptomycin, erythromycin, ciprofloxacin and nalidixic acid. Alfredson et al. (2003) have reported in southeast Queensland the incidence of thermophilic Campylobacter spp. resistant to erythromycin and tetracycline is low.

Regarding susceptibility of Campylobacter to antibiotics, there are no internationally accepted criteria of susceptibility testing break point assessment for Campylobacter spp. and no valid reference is available (Caprioli et al., 2000). Ciprofloxacin resistant strains of Camp. jejuni are reported isolates from United state, Finland, Spain and Thailand (Hankanen et al., 2003).

Skirrow et al. (1995) concerning erythromycin stated that this drug should be considered as the optimal drug for treatment of Campylobacter infections. It is because; the rate of resistance of Campylobacter to erythromycin is low. Erythromycin is cheap and unlike the fluoroquinolones and tetracyclines, it may be administered safely to children and pregnant women. However, currently isolation of erythromycin resistance strains of Campylobacter has also been reported (Tremblay et al., 2003). An investigation in India on antimicrobial susceptibility of thermophilic Campylobacter isolate from environmental samples (Baserisalehi et al., 2005) demonstrated high frequency of occurrence of ampicillin resistant Campylobacter spp. It was therefore, concluded that ampicillin could not be a drug of choice for treatment of Campylobacteriosis. Tetracycline and gentamicin were recommended as alternative treatment for Campylobacter gastroenteritis. However, ciprofloxacin was recommended as a drug of choice for treatment of Campylobacteriosis. Hence, based on foregoing evidences the authors concluded that in recommended as the geographical region of investigation, the ciprofloxacin is not yet a problem as it is in Styria, Austria.

Campylobacter Infections

The clinical symptoms of Campylobacter infection vary from a mild, watery diarrhea to severe bloody diarrhea. Although, diarrhea is prominent manifestation of campylobacteriosis, typical symptoms of Camp. jejuni infection could be fever, nausea, vomiting, abdominal pain, headache and muscle pain.. Majority of the campylobacteriosis cases are mild and do not require hospitalization and may be self-limited. However, Camp. jejuni infection can be severe and life threatening under certain conditions. Death is more common when other diseases e.g., cancer, liver disease and immuno-deficiency diseases are present (Allos et al., 1995).

Campylobacter jejuni is the cause of diarrhea/dysentery in children and it is often related to keeping pets, chicken meat consumption and untreated drinking water (Ali, 2003). Children under the age of five and young adults aged 15-29 are the age groups most frequently affected. The incubation period (the time between exposure and onset of the first symptom) is usually two to five days, but may occur in as few as 2 days or as long as 10 days after ingestion (CDC, 1996). Long-term consequences can sometimes result from a Campylobacter infection. Some people may develop a disease that affects the nerves of the body following campylobacteriosis. This disease is Guillain-Barré syndrome and it is the most common cause of acute generalized paralysis in the Western world. Usually it begins several weeks after the diarrheal illness caused by Campylobacter. It occurs when an immune system of the infected person makes antibodies against components of the Campylobacter and these antibodies attach to the components of the nerve cells. It is because some chemical components of the human nerve cells are similar to some chemical component of the bacteria.

Guillain-Barré syndrome begins in the feet and spreads up the body. Weakness is most important symptom of this disease and may lead to paralysis. Two therapies viz., intravenous immunoglobulin infusions and plasma exchange, may improve the rate of recovery in patients with Guillain-Barré syndrome. Miller Fisher Syndrome is another related neurological syndrome disease that can follow campylobacteriosis and is also caused by immunological disorder. In Miller Fisher syndrome, the nerves of the head are affected. Another chronic condition that could be associated with Campylobacter infection is an arthritis called Reiter's syndrome. This disease is a reactive arthritis and commonly affects joints such as the knees and the lower back (Allos, 1997).

Campylobacter may also cause appendicitis or infect the abdominal cavity (peritonitis), the heart (carditis), the central nervous system (meningitis), the gallbladder (cholecystitis) the urinary tract and the blood stream (Rees et al., 1995, Ang et al., 2001). Although Campylobacter jejuni is one of the major causes of bacterial diarrhea worldwide (Tauxe, 1992; Taylor, 1992), the details of its molecular pathogenesis are not well understood. Campylobacter jejuni produces a number of compounds, which may be related to its pathogenicity. These components are cell surface molecules, hemolysins and several cytotoxins (Smith, 1996; Ketley, 1997). Although, Campylobacter produce several cytotoxins, only the cytolethal-distending toxin that arrests eukaryotic cells at the G2 phase of the cell cycle (Whitehouse el al., 1998), has been characterized in detail. Several reports relevant to invasive factors of Campylobacter jejuni indicted that Camp. jejuni strains can invade intestinal epithelial cells in vitro (Grant et al., 1993; Oelschlaeger et al., 1993), although levels of invasion by different strains vary considerably (Tay et al., 1996). Camp. jejuni strain 81-176, originally isolated from a diarrheal outbreak associated with raw-milk consumption (Korlath et al., 1985), is one of the best-characterized strains of Camp. jejuni. This strain has been shown to cause an inflammatory diarrhea in two human feeding studies and to cause disease in experimental models using primates (Russell et al., 1989) and ferrets (Yao et al., 1997). Furthermore, Camp. jejuni strain 81-176 invades INT407 cells at levels higher than those of most other Camp. jejuni strains (Hu et al., 1999).

The Seasonality in Human Infection

Rates of human infection correlate with temporal and climatic factors. In many temperate countries there is a striking spring or summer peak (Nylen, 2002), while in tropical countries there is little seasonal variation. A high level of Campylobacter infections in tropical countries has been found during the rainy season (Taylor, 1992). Concerning Northern Europe, bacterial infections have been observed in summer (Walder and Forsgren,1982). Interestingly, the spring is mirrored in temperate regions of the southern hemisphere including New Zealand (Brieseman, 1990), Australia (Grau, 1991) and South Africa (Franco, 1988). Tauxe (1992) reported outbreaks caused by raw milk or contaminated water have a bimodal distribution with peaks in May and October. Stanley et al. (2003) suggested that the seasonality of human infections might be related to poultry and bovine reservoirs of Campylobacter.

Campylobacter in Developing Countries

In developing countries, Campylobacter species are responsible for childhood diarrhea. They are among the most common causes of diarrhea in travelers from developed nations. Remarkably, in many studies in the United States, Campylobacter infections were found to cause diarrheal disease >2-7 times as frequently of infections with Salmonella species, Shigella species, or Escherichia coli O157:H7 (Slutsker, 1997). National surveillance programs in developed countries monitor sporadic cases as well as outbreaks of human campylobacteriosis (Altekruse et al., 1999). However, national surveillance programs for campylobacteriosis generally do not exist in most developing countries despite the substantial burden of disease. Most data available on campylobacteriosis in developing countries were collected as a result of support provided by WHO to many laboratories in developing countries, including grants for epidemiological studies (Coker et al., 2000). The epidemiology of Campylobacter infections is quite different in developing countries than in the industrialized world. In tropical developing countries, Campylobacter infections are hyperendemic among young children, especially those <2 years. Asymptomatic infections occur commonly in both children and adults, whereas, in developed countries, asymptomatic Campylobacter infections are unusual. In addition, in developing countries, outbreaks of infection are uncommon and the illness lacks the marked seasonal nature observed in industrialized nations. Nevertheless, in both developed and developing countries, Campylobacter remains one of the most common bacterial causes of diarrhea. Although, very little information is available on the prevalence of Campylobacter in food (Varma et al., 2000) and the environment India, it has been isolated from clinical samples (Bhadra et al., 1989; Bichile et al., 1992). The most intriguing finding of these studies was the occurrence of Campylobacter spp. in adults as well as children suffering from acute gastroenteritis.

Conclusions

Campylobacter must be considered as transient contaminant on all kitchen surfaces and equipments used for processing raw food materials, especially poultry. Our knowledge is incomplete as to how campylobacters are transmitted, but the risk of transmission through properly heat-processed foods is probably very low. The existing reports of incidence of campylobacteriosis are based on laboratory and community based studies. Because of lack detection of the accurate information concerning Campylobacter infection is thought to be much higher than that of reported. Nowadays several research groups are developing rapid and high accuracy detection methods for Camp. jejuni. This will give new hopes for the food and animal production sectors to detect the source of infection in early stage. Although, a good detection method cannot be the only tool for elimination of the food infection, educational media can be used to increase the public awareness and understanding, which is the better tool for prevention of any foodborne illnesses.

REFERENCES
1:  Alfredson, D.A., R.J. Akhurst and V. Korolik, 2003. Antimicrobial resistance and genomic screening of clinical isolates of thermophilic Campylobacter spp. from South-East Queensland, Australia. J. Applied Microbiol., 94: 495-500.
Direct Link  |  

2:  Ali, A.M., A.H. Qureshi, S. Rafi, E. Roshan, I. Khan, A.M. Malik and S.A. Shahid, 2003. Frequency of Campylobacter jejuni in diarrhoea/dysentery in children in Rawalpindi and Islamabad. J. Pak. Med. Assoc., 53: 517-520.
PubMed  |  

3:  Allos, B.M. and M.J. Blaser, 1995. Campylobacter jejuni and the expanding spectrum of related infections. Clin. Infect. Dis., 20: 1092-1101.

4:  Allos, B.M., 1997. Association between Campylobacter jejuni infection and Guillain-Barre syndrome. J. Infect. Dis., 12: 125-128.

5:  Alterkruse, S.F., N.J. Stern, P.I. Fields and D.L. Swerdlow, 1999. Campylobacter jejuni an emerging food borne pathogen. Emerg. Infect. Dis., 5: 28-35.
CrossRef  |  PubMed  |  Direct Link  |  

6:  Ang, C.W., M.A. de Klerk, H.P. Endtz, B.C. Jacobs, J.D. Laman, F.G. van der Meche and P.A. van Doorn, 2001. Guillain-barre syndrome and miller fisher syndrome-associated Campylobacter jejuni lipopolysaccharides induce anti-GM1 and anti-GQ1b antibodies in rabbits. Infect. Immun., 69: 2462-2469.
CrossRef  |  Direct Link  |  

7:  Anonymous, 1998. Chicken: What you don't know can hurt you? Consumer Rep., 63: 12-18.

8:  Aspinall, S.T., D.R.A. Wareing, P.G. Hayward and D.N. Hutchinson, 1993. Selective medium for thermophilic campylobacters including Campylobacter upsaliensis. J. Clin. Pathol., 46: 829-831.

9:  Bacon, D.J., R.A. Alm, D.H. Burr, L. Hu and D.J. Kopecko et al., 2000. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immunity, 68: 4384-4390.
CrossRef  |  Direct Link  |  

10:  Barros-Velazquez, J., A. Jimenez-Tomas and G. Villa, 1999. Isolation and typing methods for the epidemiologic investigation of thermotolerant campylobacters. Int. Microbiol., 2: 217-226.

11:  Baserisalehi, M., N. Bahador and B.P. Kapadnis, 2004. A novel method for isolation of Campylobacter spp. from environmental samples, involving sample processing and blood and antibiotic free medium. J. Applied Microbiol., 97: 853-860.
Direct Link  |  

12:  Baserisalehi, M., N. Bahador, S.K. Agustine, A.Y. Al-Mahdi and B.P. Kapadnis, 2004. Enhanced recovery and isolation of Campylobacter sp. from water using a novel device. J. Applied Microbiol., 96: 664-670.

13:  Baserisalehi, M., A.Y. Al- Mahdi and B.P. Kapadnis, 2005. Antimicrobial susceptibility of thermophilic Campylobacter sp. isolated from environmental samples. Indian J. Med. Microbiol., 23: 48-51.

14:  Bhadra, L.K., H. Lior, S.K. Misra, S.C. Pal and G.B. Nair, 1989. Serotypes and biotypes of Campylobacter jejuni and Campylobacter coli from diverse sources in Calcutta. Indian J. Med. Res., 89: 225-228.

15:  Bhavsar, S.P., M. Baserisalehi and B.P. Kapadnis, 2004. Effect of gamma radiation on survival of campylobacters in various food samples. Indian J. Med. Microbiol., 22: 39-43.

16:  Bichile, L.S., K. Saraswati, U.R. Popat, S.A. Nanivadekar and L.P. Deodhar, 1992. Acute Campylobacter jejuni enteritis in 385 hospitalised patients. J. Assoc. Phys. India, 40: 164-166.

17:  Blaser, M.J., I.D. Berkowitz, M. LaForce, J. Cravens, L.B. Reller and W.L. Wang, 1979. Campylobacter enteritis: Clinical and epidemiologic features. Ann. Int. Med., 91: 179-185.

18:  Bolton, F.J. and L. Robertson, 1982. A selective medium for isolating Campylobacter jejuni/coli. J. Clin. Pathol., 35: 462-467.

19:  Bolton, F.J., P.M. Hinchliffe, D. Coates and L. Robertson, 1982. A most probable number method for estimating small numbers of campylobacters in water. J. Hyg., 89: 185-190.

20:  Bolton, F.J., D.N. Hutchinson and D. Coates, 1984. Blood-free selective medium for isolation of Campylobacter jejuni from feces. J. Clin. Microbiol., 19: 169-171.

21:  Bolton, F.J., D. Coates, D.N. Hutchinson and A.F. God-Free, 1987. A study of thermophilic campylobacters in a river system. J. Applied Bacteriol., 62: 167-176.

22:  Bradbury, W.C., A.M. Murray, J.N. Hennessy and J.L. Penner, 1983. Occurrence of plasmid DNA in serologically defined strains of Campylobacter jejuni and Campylobacter coli. Infect. Immun., 40: 460-463.

23:  Brieseman, M.A., 1990. A further study of the epidemiology of Campylobacter jejuni infections. N. Z. Med. J., 103: 207-209.

24:  Buswell, C.M., Y.M. Herlihy, L.M. Lawrence, J.T. McGuiggan, P.D. Marsh, C.W. Keevil and S.A. Leach, 1998. Extended survival and persistence of Campylobacter sp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and rRNA staining. Applied Environ. Microbiol., 64: 733-741.

25:  Butler, R.C., V. Lund and D.A. Carlson, 1987. Susceptibility of Campylobacter jejuni and Yersinia enterocolitica to UV irradiation. Applied Environ. Microbiol., 64: 733-741.

26:  Byrne, C., D. Doherty, A. Mooney, M. Byrne and D. Woodward et al., 2001. Basis of the superiority of cefoperazone amphotericin techoplanin for isolating Campylobacter upsaliensis from stools. J. Clin. Microbiol., 39: 2713-2716.
CrossRef  |  PubMed  |  

27:  Caprioli, A., L. Busani, J.L. Martel and R. Helmuth, 2000. Monitoring of antibiotic resistance in bacteria of animal origin: Epidemiological and microbiological metholologies. Int. J. Antimicrob. Agents, 14: 295-301.

28:  Chaveerach, P., D.A. Keuzenkamp, H.A. Urlings, L.J. Lipman and F. van Knapen, 2002. In vitro study on the effect of organic acids on Campylobacter jejuni/coli populations in mixtures of water and feed. Poult. Sci., 81: 621-628.
Direct Link  |  

29:  Coker, A.O., R.D. Isokpehi, B.N. Thomas, A.F. Fagbenro-Beyioku and S.A. Omilabu, 2000. Zoonotic infections in Nigeria: Overview from a medical perspective. Acta Trop., 37: 215-221.

30:  Collins, C.I., E.A. Murano and I.V. Wesley, 1996. Survival of Arcobacter butzleri and Campylobacter jejuni after irradiation treatment in vacuum-packaged ground pork. J. Food Prot., 59: 1164-1166.

31:  Corry, J.E., D.E. Post, P. Colin and M.J. Laisney, 1995. Culture media for the isolation of campylobacters. Int. J. Food Microbiol., 26: 43-76.

32:  Dekeyser, P., M. Gossuin-Detrain, J.P. Butzler and J. Sternon, 1972. Acute enteritis due to related vibrio: First positive stool cultures. J. Infect. Dis., 125: 390-392.

33:  Deming, M.S., R.V. Tauxe, P.A. Blake, S.E. Dixon and T.S. Jones et al., 1987. Campylobacter enteritis at a university transmission from eating chicken and from cats. Am. J. Epidemiol., 126: 526-534.

34:  Dharmalingam, S., U.A. Rao, G. Jayaraman and S.P. Thyagarajan, 2003. Relation ship of plasmid profile with the antibiotic sensitivity pattern of Helicobacter pylori isolates from peptic ulcer disease patients in Chennai. Indian J. Med. Microbiol., 21: 257-261.

35:  Diker, K.S., H. Yardimic and M. Arda, 1987. Effects of disinfectants on Campylobacter jejuni. Microbiol. Bull., 21: 86-90.

36:  Doyle, M.P., 1984. Association of Campylobacter jejuni with laving hens and eggs. Applied Environ. Microbiol., 47: 533-536.

37:  Engberg, J., S.L.W. On and C.S. Harrington, 2000. Efficient isolation of Campylobacter from stools. J. Clin. Microbiol., 38: 2798-2799.

38:  Fallon, R., N. O'Sullivan, M. Maher and C. Carrol, 2003. Antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolates from broiler chicken isolated at an Irish poultry processing plant. Lett. Applied Microbiol., 36: 277-281.

39:  Fang, G., V. Araujo and R.L. Guerrant, 1991. Enteric infections associated with exposure to animals or animal products. Infect. Disease Clin. North Am., 5: 681-701.
Direct Link  |  

40:  Federighi, M., J.L. Tholozan, J.M. Cappelier, J.P. Tissier and J.L. Jouve, 1998. Evidence of non-coccoid viable but non-culturable Camp. Jejuni cells in microcosm water by direct viable count, CTC-DAPI double staining and scanning electron microscopy. Food Microbiol., 15: 539-550.

41:  Forst, J.A., 2001. Current epidemiological issues in human campylobacteriosis. J. Applied Microbiol., 90: 85-95.

42:  Franco, D.A., 1988. Campylobacter species: Considerations for controlling a foodborne pathogen. J. Food Prot., 51: 145-153.

43:  Grant, C.C.R., M.E. Konkel, W.J. Cieplak and L.S. Tompkins, 1993. Role of flagella in adherence, internalization and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect. Immun., 61: 1764-1771.
PubMed  |  

44:  Hankanen, A., H.J. Somer, A. Siitonen, P. Huovinen and P. Kotilainen, 2003. Floroquinolone resistance in Campylobacter jejuni isolates in travelers returning to Finland: Association of ciprofloxacin resistance to travel destination. Emerg. Infect. Dis., 9: 267-270.

45:  Hanninen, M., L.M. Niskanen and L. Korhonen, 1998. Water as a reservoir for Campylobacter jejuni infection in cows studied by serotypingand Pulsed-field Gel Electrophoresis (PFGE). Zentralbl. Veterinarmed, 45: 37-42.

46:  Hu, L. and D.J. Kopecko, 1999. Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect. Immun., 67: 4171-4182.

47:  Inglis, G.D., L.D. Kalischuk and H.W. Busz, 2004. Chronic shedding of Campylobacter species in beef cattle. J. Applied Microbiol., 97: 410-412.

48:  Ketley, J.M., 1997. Pathogenesis of enteric infection by Campylobacter. Microbiology, 143: 5-21.
CrossRef  |  PubMed  |  Direct Link  |  

49:  Konkel, M.E., B.J. Kim, J.D. Klena, C.R. Young and R. Ziprin, 1998. Characterization of the thermal stress response of Campylobacter jejuni. Infect. Immun., 66: 3666-3672.

50:  Korlath, J.A., M.T. Osterholm, A. Judy, J.C. Forgang and R.A. Robinson, 1985. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J. Infect. Dis., 152: 592-596.

51:  Kulkarni, S.P., S. Lever, J.M.J. Logan, A.J. Lawson, J. Stanley and M.S. Shafi, 2002. Detection of Campylobacter species: A comparison of culture and polymerase chain reaction based methods. J. Clin. Pathol., 55: 749-753.

52:  Kusters, J.G., M.M. Gerrits, J.A.G. van Strijp and M.J.E. Vandenbroucke-Grauls, 1997. Coccoid forms of Helicobacter pylori are the morphologic manifestation of cell death. Infect. Immun., 65: 3672-3679.

53:  Lariviere, L.A., C.L. Gaudreau and F.F. Turgeon, 1986. Susceptibility of clinical isolates of Campylobacter jejuni to twenty-five antimicrobial agents. J. Antimicrob. Chemother., 18: 681-685.

54:  Li, Y., H. Yang and B.L. Swem, 2002. Effect of high temperature in side-outside spary on survival of Campylobacter jejuni attached to prechill chicken carcasses. Poult. Sci., 81: 1371-1377.

55:  Moore, J.E. and R.H. Madden, 2000. The effect of thermal stress on Campylobacter coli. Applied Microbiol., 89: 892-892.

56:  Nylen, G., F. Dunstan, S.R. Palmer, Y. Andersson and F. Bager et al., 2002. The seasonal distribution of Campylobacter infection in nine European countries and New Zealand. Epidemiol. Infect., 128: 383-390.

57:  Oelschlaeger, T.A., P. Guerry and D.J. Kopecko, 1993. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc. Natl. Acad. Sci. USA., 90: 6884-6888.

58:  On, S.L.W., 2001. Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: Current status, future prospects and immediate concerns. J. Applied Microbiol., 90: 1S-15S.
Direct Link  |  

59:  Patterson, M.F., 1995. Sensitivity of Campylobacter sp. to irradiation in poultry meat. Lett. Applied Microbiol., 20: 338-340.

60:  Pickert, A. and K. Botzenhart, 1985. Survival of Campylobacter jejuni in drinking water, river water and sewage. Zentralbl. Bakteriol. Mikrobiol. Hyg., 182: 49-57.

61:  Rees, J.H. and S.E. Soudain, 1995. Campylobacter jejuni infection and Guillain-Barre syndrome. N. Engl. J. Med., 333: 1374-1374.

62:  Ribeiro, C.D. and T.H. Price, 1984. The use of Preston enrichment broth for the isolation of thermophilic campylobacters from water. J. Hyg. (Lond.), 92: 45-51.

63:  Rollins, D.M. and R.R. Colwell, 1986. Viable but non-culturable stage of Camp. Jejuni and its role in survival in the aquatic environment. Applied Environ. Microbiol., 52: 531-538.

64:  Russell, R.G., M.J. Blaser, I. Sarmiento and J. Fox, 1989. Experimental Campylobacter jejuni infection in Macaca nemestrina. Infect. Immun., 57: 1438-1444.

65:  Skirrow, M.B., 1994. Disease due to Campylobacter, Helicobacter and related bacteria. J. Comp. Pathol., 111: 113-149.

66:  Slutsker, L.A., A.A. Ries, K.D. Greene, J.G. Wells, L. Hutwagner and P.M. Griffin, 1997. Escherichia coli O157:H7 diarrhea in the United States: Clinical and epidemiological features Ann. Int. Med., 126: 500-513.

67:  Smibert, R.M., 1978. The genus Campylobacter. Ann. Rev. Microbiol., 32: 673-709.
CrossRef  |  

68:  Smith, J.L., 1996. Determinants that may be involved in virulence and disease in Campylobacter jejuni. J. Food Safety, 16: 105-139.

69:  Solow, B.T., O.M. Cloak and I. Fratamicro, 2003. Effect of temperature on viability of Campylobacter jejuni and Campylobacter coli on raw chicken or pork skin. J. Food Prot., 66: 2023-2031.

70:  Stanley, K. and K. Jones, 2003. Cattle and sheep farms as reservoirs of Campylobacter. J. Applied Microbiol., 94: 104-113.

71:  Steele, T.W. and S.N. Mc Dermott, 1984. The use of membrane filters applied directly to the surface of agar plates for the isolation of Campylobacter jejuni from faeces. Pathology, 16: 263-265.

72:  Stelzer, W., H. Mochmann, U. Richter and H.J. Dobberkau, 1988. Characterization of Campylobacter jejuni and Campylobacter coli isolated from waste water. Zentralbl. Bakteriol. Microbiol. Hyg., 269: 188-196.

73:  Tay, S.T., S. Devi, S. Puthucheary and I. Kautner, 1996. In vitro demonstration of the invasive ability of campylobacters. Zentbl. Bakteriol., 283: 306-313.

74:  Taylor, D.E., 1983. Incidence of plasmid DNA in strains of Campylobacter jejuni isolated from stool specimens at 37 and 43EC. J. Infect. Dis., 47: 965-966.

75:  Taylor, D.E., R.S. Garner and B.J. Allan, 1983. Characterization of tetracycline resistance plasmids from Campylobacter jejuni and Campylobacter coli. Antimicrob. Agents Chemother., 24: 930-935.

76:  Taylor, D.E. and J.H. Bryner, 1984. Plasmid content and pathogenicity of Campylobacter jejuni and Campylobacter coli strains in the pregnant guinea pig model. Am. J. Vet. Res. 45: 2201-2202.

77:  Taylor, D.E., N. Chang, R.S. Garner, R. Sherburne and L. Muller, 1986. Incidence of antibiotic resistance and characterization of plasmids in Campylobacter jejuni strains from clinical sources in Alberts, Canada. Can. J. Microbiol., 32: 28-32.

78:  Tenover, F.C., S. Williams, K.P. Gordon, C. Nolan and J.I. Plorde, 1985. Survey of plasmids and resistance factors in Campylobacter jejuni and Campylobacter coli. Antimicrob. Agents Chemother, 27: 37-41.

79:  Trachoo, N., 2003. Campylobacter jejuni: An emerging pathogen Songklanakarin. J. Sci. Technol., 25: 141-157.

80:  Tran, T.T., 1998. A blood-free enrichment medium for growing Campylobacter sp. under aerobic conditions. Lett. Applied. Microbiol., 26: 145-148.

81:  Tremblay, C., C. Gaudreau and M. Lorange, 2003. Epidemiology and antimicrobial susceptibilities of 111 Campylobacter fetus subsp. fetus strains isolated in Quebec, Canada, from 1983 to 2000. J. Clin. Microbiol., 41: 463-466.

82:  Uradzinski, J. and J. Szteyn, 1993. Effect of preservatives on survival of Campylobacter jejuni in ground pork meat. Rocz Panstw Zaki Hig., 44: 392-402.

83:  Van de Bogaard, A.E. and E.E. Stobberingh, 2000. Epidemiology of resistance to antibiotics: Links between animals and humans. Int. J. Antimicrob. Agents, 14: 327-335.
CrossRef  |  PubMed  |  Direct Link  |  

84:  Varma, K.S., N. Jagadeesh, H.K. Mukhopadhyay and N. Dorairrajan, 2000. Incidence of Campylobacter jejuni in poultry and their carcasses. J. Food Sci. Technol., 37: 639-641.
Direct Link  |  

85:  Walmsley, S.L. and M.A. Karmali, 1989. Direct isolation of atypical thermophilic Campylobacter species from human feces on selective agar medium. J. Clin. Microbiol., 27: 668-670.

86:  Whitehouse, C.A., P.B. Balo, E.C. Pesci, D.L. Cottle, P.M. Mirabito and C.L. Pickett, 1998. Campylobacter jejuni cytolethal distending toxin causes a G2-phase cell cycle block. Infect. Immun., 66: 1934-1940.
Direct Link  |  

87:  Yao, R., D.H. Burr and P. Guerry, 1997. CheY-mediated modulation of Campylobacter jejuni virulence. Mol. Microbiol., 23: 1021-1031.

88:  Allos, B.M., 2001. Campylobacter jejuni infections: Update on emerging issues and trends. Clin. Infect. Dis., 32: 1201-1206.
CrossRef  |  Direct Link  |  

89:  Catteau, M., 1995. The Genus Campylobacter. In: Microbiological Control for Foods and Agricultural Products, Bourgeois, C.M. and J.Y. Leveau (Eds.). VCH Publishers, New York, pp: 325-334.

90:  CDC, 1996. Guidelines for confirmation of foodborne-disease outbreaks. MMWR, 45: 59-59.

91:  Doyle, M.E., 1998. Campylobacter-Chronic Effects. Food Research Institute, Madison.

92:  Grau, F.H., 1991. Campylobacter jejuni/coli. In: Foodborne Microorganisms of Public Health Significance, Buckle, K.A. (Ed.). 4th Edn., Australian Institute of Food Science and Technology, Australia, pp: 136-151.

93:  ICMSF, 1996. Microorganisms in Foods 6. Microbial Ecology of Food Commodities. Blackie, London, pp: 75-129.

94:  Kelana, L.C. and M.W. Griffiths, 2003. Growth of autobioluminescent Campylobacter jejuni in response to various environmental conditions. J. Food Prot., 66: 1190-1197.
Direct Link  |  

95:  Kelana, L.C. and M.W. Griffiths, 2003. Use of an autobioluminescent Campylobacter jejuni to monitor cell survival as a function of temperature, pH and sodium chloride. J. Food Prot., 66: 2032-2037.
Direct Link  |  

96:  Nachamkin, I., M.J. Blaser and L.S. Tomskins, 1992. Campylobacter jejuni Current Status and Future Trends. ASM, Washington, DC.

97:  Scott, E. and P. Sockett, 1998. How to Prevent Food Poisoning. John Wiley and Sons, New York.

98:  Skirrow, M.B., 1977. Campylobacter enteritis: A new disease. Br. Med. J., 2: 9-11.
CrossRef  |  Direct Link  |  

99:  Skirrow, M.B. and M.J. Blaser, 1995. Campylobacter jejuni. In: Infections of the Gastrointestinal Tract, Blaser, M.J., P.D. Smith, J.I. Ravdin, H.B. Greenberg and R.L. Guerrant (Eds.). Raven Press, New York, pp: 825-848.

100:  Tauxe, R.V., 1992. Epidemiology of Campylobacter jejuni Infections in the United States and other Industrialised Nations. In: Campylobacter jejuni. Current Status and Future Trends, Nachamkin, I., M.J. Blaser and L.S. Tompkins (Eds.). American Society for Microbiology, Washington, DC., pp: 9-19.

101:  Taylor, D.N., 1992. Campylobacter Infections in Developing Countries. In: Campylobacter jejuni, Current Status and Future Needs, Nachamkin, I., M.J. Blaser and L.S. Tompkins (Eds.). American Society for Microbiology, Washington, DC., pp: 20-30.

102:  Walder, M. and A. Forsgren, 1982. Acute Enteritis due to Campylobacter: An Epidemiological Study. In: Epidemiology, Pathogenesis and Biochemistry, Newell, D.G. (Ed.). MTP Press, Lancaster, pp: 14-15.

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