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Campylobacter jejuni infection

Campylobacter jejuni infection

Campylobacter jejuni infection

Previous authors: M L VAN DER WALT

Current authors:
E DI GIANNATALE - Head of the Bacteriology Department and National Reference Laboratory of Campylobacter, Microbiologist, via Campo Boario, Teramo, 64100, Italy

GENERAL INTRODUCTION: AEROBIC/MICRO-AEROPHILIC, MOTILE, HELICAL/VIBROID GRAM-NEGATIVE BACTERIA

Introduction

Campylobacter jejuni is a common human pathogen and an important cause of diarrhoea worldwide.28, 77, 89 It is isolated frequently from the intestine of healthy animals and considered to be part of the normal intestinal flora. Birds and domestic ruminants play an integral role in the ecology of C. jejuni and may serve as a source of infection resulting in outbreaks of disease or sporadic cases in humans.34, 62 Poultry and cattle are the most important animal reservoirs. Infection in humans can be acquired via multiple routes, including direct contact with these animals, consumption of contaminated animal products, and environmental contamination such as water.17 Campylobacter jejuni alone, or in combination with other pathogens, may cause enteritis and diarrhoea in calves87 and sheep,83, 91 but its significance in such cases should be interpreted with care.64, 97 For many years it was considered to be the aetiological agent of ‘winter dysentery’ (caused by bovine coronavirus), characterized by profuse watery diarrhoea of sudden onset and short duration in adult cattle.57, 76 Campylobacter jejuni is also an occasional cause of mastitis in cattle41, 42, 52, 61 and abortion90 in cattle, sheep,20, 40, 92 goats5 and blesbok (Damaliscus dorcas).6

Aetiology

Campylobacter jejuni is micro-aerophilic and grows optimally in an atmosphere containing 5 per cent O2, 10 per cent CO2 and 85 per cent N2 and at 37-42°C. It is   unable to ferment or oxidize carbohydrates.   The organisms are slender, spirally curved, Gram-negative rods 0,2 - 0,8 μm wide and 0,5-6,0 μm long. They vary in morphology and may have an increased number of spirals or may be gull-wing-shaped, while coccoid forms occur in older cultures in response to deleterious conditions. The bacteria are motile, the movement being characteristically darting or corkscrew-like. Motility is caused by polar flagella at one or both ends of the organism51, 81 that propel it through viscous solutions, such as the mucus layer of the gastrointestinal tract.53

Campylobacter jejuni can survive in a moist environment for several weeks at 4 °C and maintain its metabolic activities39 but it tends to die more rapidly at ambient temperatures. It survives in bovine faeces for at least 20 days at 25 °C and for eight weeks at 4 °C.19 In cows’ milk or water C. jejuni survives for two to five weeks when kept at 4 °C.72, 94 The bacterium is sensitive to dehydration at room temperature,28 while freezing drastically reduces the number of organisms on meat.84 It does not proliferate below 30°C,68 perhaps due to the absence of cold shock proteins.39

The organism is inactivated by iodine udder washes within eight minutes and is rapidly killed by hydrochloric acid at pH 2,3.11 Campylobacters do not survive the temperatures of pasteurization:  inactivation in skimmed milk and beef cubes requires 50 seconds at 92 °C and 40 seconds at 95,7 °C, respectively.19

Epidemiology

The organism is widely distributed particularly in avian species, farm animals, pets such as dogs and cats, and humans. Food animals, especially poultry, are reservoirs of C. jejuni. Fifty to 80 per cent of cases of campylobacteriosis in humans are attributed to chickens as the source of infection.7, 22, 28, 65, 80

Campylobacter jejuni is shed in the faeces of both diarrhoeic and healthy animals.63, 70, 86 Faecal shedding by healthy animals is intermittent and only few organisms are shed. There appears to be no difference in the carrier rates between healthy cattle, horses, pigs and dogs. Carrier rates do vary within a species and between animals from different sources.69

Organisms are commonly present in the rumen of calves and less so in adult cattle. In healthy sheep C. jejuni is frequently carried in the intestinal tract.1, 79

Isolation levels are five times higher from fresh than from frozen tissue.   Refrigeration or frozen storage alone do not add a significant safety margin and therefore poultry contaminated with C. jejuni can cause infection if not properly handled and sufficiently cooked.10 In humans it is estimated that handling and consumption of broiler meat may account for 20 to 30 per cent of human cases of campylobacteriosis.22 Apart from chicken products, infection may follow consumption of untreated surface water, unpasteurized and incompletely cooked milk,37 and other contaminated food products such as meat from farm animals.24, 78 Carcasses of feedlot-fed cattle are more likely to be contaminated than those of pasture-fed cattle.27 Apart from milk no other dairy products act as a source of C. jejuni. 37

Flies may be important in the transmission of the bacterium, particularly to humans. On poultry and pig farms, 50 and 43 per cent respectively of Musca domestica may contain C. jejuni.73

Pathogenesis

Although C. jejuni mainly colonizes the gastrointestinal tract in animals, it may cross the intestinal epithelial barrier leading to bacteraemia.85 In pregnant animals C. jejuni may reach the gravid uterus, resulting in subsequent placentitis, foetal infection and abortion.14, 79

During a brief period of bacteraemia, which lasts no longer than 72 hours, organisms are disseminated to the mesenteric lymph nodes, gastrointestinal tract, gallbladder and spleen. Disappearance of the bacteraemia coincides with the appearance of circulating antibodies.88

The initial colonization of the entire intestinal tract by C. jejuni changes over time, and after 96 hours bacteria persist only in the ileum, caecum and colon. Lesions in calves develop mostly in the large intestine while in lambs they occur in the ileum.88 This intestinal localization is associated with scouring four to five days after infection,93 which also coincides with the development of severe oedema and inflammation in the colon. The inflammatory reaction is characterized by severe neutrophil infiltration, the development of microscopic ulcers, and focal goblet cell hyperplasia. The initial acute inflammatory reaction is followed by the infiltration of lymphocytes and macrophages.15, 93

In sheep the onset of the gastroenteritis can be precipitated by the stress of transport and a change in the diet.83

Different animal models have been developed to study the virulence and pathogenicity of C. jejuni.32 Studies on the mechanisms of virulence of C. jejuni showed that it is a unique pathogen, being able to execute N-linked glycosylation of more than 30 proteins related to colonization, adherence, and invasion. The cytolethal distending toxins (CdtA,B,C) contribute to the pathogenicity of C. jejuni.18 Host factors seem to play a major role in the pathogenesis of campylobacteriosis in humans.18

The organisms colonize the intestinal mucosal surface, adhere to and invade the epithelial cells48, 49 and the mucosa. After colonization, the bacteria multiply and produce toxins,58, 87 including an enterotoxin that is immunologically related to cholera toxin,43, 94 and other cytotoxic and cytolethal toxins.30, 44

Clinical signs

Cattle

Calves and older animals may suffer from an enteric syndrome.4 After an incubation period of one to three days, there is a rise in temperature to 41 °C and passage of dark, mucoid or haemorrhagic faeces70, 86 The diarrhoea may last up to 18 days. Experimental infections are self-limiting96 and the course of the disease is usually not longer than 20 days.87

Other syndromes in cattle associated with C. jejuni infections include abortion storms in late gestation, the birth of live but weak calves,90 and a varying degree of purulent mastitis.52

Sheep and goats

The morbidity in outbreaks of diarrhoea in fattening lambs may reach 30 per cent.83 In field outbreaks many ewes have mild diarrhoea before the first abortions occur. In an outbreak up to 10 per cent or more of the ewes may abort, and at the same time others may give birth to weak lambs.20 An abortion rate of 23.2 per cent in small ruminants has been reported in the USA,74, 99 where C. jejuni infection caused primarily by a highly virulent tetracycline-resistant C. jejuni clone has now replaced Campylobacter fetus subsp. fetus as an important cause of abortion in sheep.75

In goats, abortion may occur during late gestation. As in sheep, diarrhoea is seen in the does before or during the abortions.5

Pathology

Lesions in cattle suffering from the enteric syndrome occur primarily in the large intestine. Macroscopically the small intestine is flaccid and may contain fluid ingesta, whereas the large intestine has very fluid content containing strings of mucus and blood.87 The mesenteric lymph nodes are consistently enlarged.69, 86 In lambs the ileum is more commonly affected.

Bacteria occur close to the surface of the cells, sometimes in the lumen of crypts, and in the lamina propria surrounding the small blood vessels.3 In the ileum and the jejunum there is loss of superficial villar epithelium, stunting and fusion of villi, dilatation of crypts, thickening of the lamina propria, oedema and congestion and inflammatory cell infiltration of the mucosa,70 and prominent lymphoid hyperplasia.86 Scattered crypt abscesses occur, as well as excessive mucus production.88

In cattle that have aborted there is severe necrotizing placentitis and occasionally bronchopneumonia is present in the foetus.90

Ewes that abort suffer from severe purulent endometritis accompanied by vasculitis, and necropurulent placentitis. Bacterial colonies are present in the placenta.40 Aborted foetuses have severe purulent bronchopneumonia and multifocal hepatic necrosis (Figure 1).40

Diagnosis

Campylobacter jejuni is a labile organism and dies rapidly on exposure to air, heat and desiccation, and is also rapidly eliminated by putrefactive organisms. Specimens for diagnostic purposes should consist of fresh tissues, which must be placed in a transport medium such as Stuart’s or Amies’, kept cool, and should reach the laboratory as soon as possible.

Figure 1 Campylobacter jejuni infection: circular, umbilicated necrotic foci in the liver of an aborted ovine foetus. (By courtesy of Dr W. J. Hartley, Jaranga Zoo, Mosman, NSW, Australia)

For successful culture, prior filtering (pore size of 0,65 μm) and the use of commercially available selective media such as Campylobacter modified  Charcoal Cefoperazone Deoxycholate Agar (mCCDA),  Skirrow, Preston, Butzler, Blaser, Campy-BAP and others is recommended, and the organisms should be cultured in microaerophilic conditions. Preferential growth is also obtained if the cultures are incubated at the upper range of the optimal incubation temperature of 37 to 42 °C.81 After 48 hours of culture, the colonies are typically small (2 to 4 mm in diameter) and low-convex with entire edges. Swarming colonies may extend along the line of incubation when moist media are used. Colonies are further identified by biotyping.81

The identity of organisms may also be confirmed in tissue sections by immunofluorescent or immunoperoxidase techniques40 and by commercial latex agglutination tests.36 ELISA tests have also been applied successfully.29

When attempting the isolation of C. jejuni in live animals, it must be kept in mind that bacteraemia and faecal shedding of organisms may occur sporadically96 and that many animals are symptomless carriers. In fatal cases in cattle and sheep, organisms can be isolated from both normal and grossly inflamed intestinal mucosa.3, 83, 86 Organisms may be isolated from the gallbladder in chronically affected animals.87

In abortion storms, organisms may be isolated in pure culture and in large numbers from the placenta, as well as from the organs and stomach content of aborted foetuses.5, 6, 40, 90 Faecal cultures are of no help in the diagnosis of abortion, as C. jejuni can be isolated with the same frequency in infected herds from normal cows and from those that have aborted, as well as from normal calves and those with diarrhoea.90

Milk from cows with subclinical or mild mastitis due to infection with C. jejuni has an increased somatic cell count, and several strains of the bacterium, with different drug sensitivities, may be isolated from the affected milk of different animals on the same farm.61 Isolation of C. jejuni from milk is aided by the destruction of the lactoperoxidase system.9 Different strains of the organism may at the same time be isolated from the milk and the faeces of the same animal.41 Variable numbers of organisms are excreted from affected quarters for as long as 73 days after infection.50

Suspicious colonies of Campylobacter must be confirmed using different assays, including biochemical and molecular tests and matrix-assisted laser desorption/ionization (MALDI-TOF).8 Identification of C. jejuni   can be achieved by means of multiplex PCR74, 95 or real- time PCR methods.45, 46 In sheep a standard PCR has been used to detect C. jejuni directly in aborted foetal tissues and placentas.33

 Strains are differentiated by serotyping using heat-labile and heat-stable antigens,89 phage-typing, outer membrane protein-typing,12 pulsed field gel electrophoresis (PFGE) (Pulsenet USA), and multi locus sequence typing (MLST)21 that characterizes strains by their unique allelic profiles.59, 66 Strains of different pathogenicity may be identified in outbreaks,50 while serotypes also differ in pathogenicity and tropism.31, 40, 98 The first complete genome sequence of a C. jejuni strain was reported in 2001 for C. jejuni strain 11168.67 Currently whole-genome sequencing is used for C. jejuni typing.38, 54, 55

Differential diagnosis

Most cases of diarrhoea in cattle from which C. jejuni has been isolated in large numbers also yield other agents such as cryptosporidia, coccidia, rotavirus, coronavirus, enteropathogenic Escherichia coli, Salmonella serovars or nematodes. Clinical cases should in particular be differentiated from coccidiosis and paratyphoid.87

Control

No vaccines are commercially available to control C. jejuni infections in animals or birds, but an ovine C. fetus bacterin has been used in goats and sheep with good effect.5, 35

In general, most strains are susceptible to nitrofurans, gentamicin, and chloramphenicol.36 Multiple resistance to antibiotics may occur.16, 47 High resistance rates for quinolones, fluoroquinolones and tetracyclines have been reported in many countries but resistance to erythromycin and gentamicin in C. jejuni remains low.2, 25, 56, 100 An increased level of macrolide resistance is becoming a major public health concern in some countries in Europe and the USA.26

In sheep, abortions can be controlled by daily injections of erythromycin at a dosage of 4 mg/kg followed by an intramuscular injection of long-acting oxytetracycline.83 Orally administered chlortetracycline at a rate of 75 mg/kg per day for 14 days is also effective in controlling an outbreak of abortion.5

Permanent cure of intestinal infection appears to be difficult. In one report concerning the treatment of dogs with intestinal C. jejuni infection, both chloramphenicol and erythromycin failed to eliminate the infection, and the organism could again be isolated within nine days after discontinuation of treatment.60

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