Campylobacter infection of commercial poultry - OIE

Rev. sci. tech. Off. int. Epiz., 2000,19 (2), 376-395

Campylobacter infection of commercial poultry S.M. Shane

Department of Epidemiology and Community Health, School of Veterinary Medicine, Louisiana State University, Baton Rouge, Louisiana 70803, United States of America

Summary Campylobacter jejuni, a widespread food-borne pathogen is responsible for enteritis in the populations of both industrialised and developing nations and is acquired by consumption of contaminated water, milk and food products. Contaminated poultry meat is regarded as an important source of campylobacteriosis, with both commercial broiler and turkey growing flocks infected at two to three weeks of age by direct and indirect horizontal exposure. Non-chlorinated water is regarded as a vehicle of infection, followed by rapid intraflock dissemination. Intensification in the poultry industry has contributed to the increased prevalence rates on carcasses associated with increased stocking density and mechanised processing which are inherent to the high efficiency dictated by a competitive market. Currently, pre- and post-harvest control measures may ameliorate the problem of Campylobacter infection in consumers. Refrigerated storage and transport of red meat and poultry, appropriate handling and food preparation, and thorough cooking reduce the possibility of food-borne infection. In view of the world-wide distribution of C. jejuni infection and the multiplicity of sources, including non-pasteurised milk and contaminated water, it is inappropriate to impose trade restrictions on poultry meat based on the detection of Campylobacters.

Keywords Avian diseases - Campylobacter coli - Campylobacter jejuni - Food-borne infection -Post-harvest control - Poultry - Pre-harvest control - Prevalence.

Introduction Campylobacter is responsible for food-borne enteric infection among consumers world-wide (32, 196). The infection may be acquired by consumption of non-chlorinated, contaminated surface water or water from wells (97) , unpasteurized milk (181) , and consumption of undercooked poultry (153) or red meat (172). In addition, campylobacteriosis may be acquired by direct contact with infected human shedders in the family environment. Nosocomial infection occurs and cases of congenital transmission are rarely documented. Campylobacteriosis in children is often acquired from immature diarrhoeic pets (31).

In the context of international trade, the ubiquitous nature of Campylobacter jejuni and the multiple reservoirs and sources of infection mitigate against impeding trade on the basis of contamination. Establishing an import barrier against poultry or red meat contaminated with Campylobacter would be

unjustified. Invoking sanitary and phytosanitary measures would be blatantly protectionist and inconsistent with the rules of the World Trade Organization (100).

The characteristics of the thermophilic Campylobacter spp. of food-bome significance are reviewed in relation to isolation and identification, epidemiology in poultry and human populations, and current and future methods of control.

Isolation and identification of thermophilic Campylobacter spy. The genus Campylobacter was established in the early 1970s (193) , based on morphological and biochemical characteristics including serological typing (26). Subsequent developments in molecular biology have facilitated revision of the genus and differentiation from Helicobacter and Arcobacter (187).

Rev. sci. tech. Off. int. Epiz., 19 (2) 377

The three thermophilic Campylobacter species of human health significance, C. jejuni, C. coli and C. lari, require selective media, incubation at 42°C and a microaerobic environment comprising a low level of oxygen (5% to 10%) and elevated carbon dioxide ( 1 % to 10%). Methods of specimen collection to avoid desiccation, and subsequent culture and identification are reviewed in laboratory manuals (159). The three thermophilic species of Campylobacter can be differentiated by biochemical characteristics (167) and hydrogen sulphide production (105) . The Penner serotyping scheme is based on heat-stable antigens derived from surface lipopolysaccharides (135) . The alternative Lior serotyping scheme using heat-labile H antigens (106) is practical under laboratory conditions to differentiate among C. jejuni isolates derived from flocks and patients (131).

The relative efficiency of ten alternative methods to distinguish among Campylobacter isolates in epidemiological investigations was based on extensive studies undertaken at the United States Centers for Disease Control and Prevention, Atlanta (132) . Techniques included Penner and Lior serotyping, multilocus enzyme electrophoresis, deoxyribonucleic acid (DNA) restriction endonuclease analysis, phage typing, plasmid analysis and ribotyping. Serotyping was determined to be the most discriminating phenotypic method, but all the procedures required specialised laboratory equipment and trained technicians consistent with reference centres. Pulse field gel electrophoresis is frequently applied to distinguish C. jejuni from C. coli and in molecular epidemiological studies (201) . Flagella typing using restriction fragment length polymorphism (RFLP) analysis can discriminate among isolates and is regarded as a practical typing method for epidemiological investigations (124). Highly sensitive polymerase chain reaction (PCR) procedures are being developed to detect C. jejuni in food products (199) . This has specific implications for regulations which impose a zero tolerance for C. jejuni on imported poultry, since the high sensitivity of this technique will detect the organism at extremely low prevalence. In a study conducted in Switzerland, Campylobacter was detected in 4% of a series of 231 litter samples using conventional microbiology, compared to 6 8 % detection using PCR (175). In a trial conducted on faecal samples derived from hospitalised patients with enteric infections, the sensitivity and specificity of the PCR procedure as compared to conventional culture was determined to be 9 1 % and 97% respectively (192). Alternative methods of detection and identification of Campylobacter include immunomagnetic separation and identification of pathogen-specific ions by mass spectrometry (114).

Campylobacter jejuni and C. coli produce a cytotonic toxin which has immunological similarities to cholera toxin (109). This toxin is probably responsible for the diarrhoea associated with submucosal oedema noted in three- to four-day-old chickens inoculated with C. jejuni isolated from diarrhoeic

patients (151). The cytotoxin produced by toxigenic strains of C. jejuni is dose dependent and is not neutralised by shiga-toxin immune serum. The toxin is regarded as a unique compound, lethal to HeLa and CHO cells (63) and chicken embryos (111) .

In vitro assays involving adhesion and cytotoxicity have demonstrated that C. jejuni isolates from surface water are less pathogenic than strains derived from diarrhoeic patients (126) . Pathogenic isolates are thought to develop the ability to colonise and to produce toxin as a result of passage in a susceptible host. This hypothesis was confirmed using a neonatal mouse model to demonstrate increased virulence following successive passage of C. jejuni isolates in chicks (150).

Epidemiology of Campylobacter jejuni infection in commercial poultry Infection of commercial poultry, including ducks (93) , broilers (140) , turkeys (2), egg production flocks (55) and parent breeding stock (161) with thermophilic Campylobacter spp. is widespread (155) . Of the three species, C. jejuni predominates, with C. coli and C. lari infrequently recovered from the intestinal tract of poultry. A review lists forty-eight reports of isolations from five species of poultry in thirty countries from 1981 to 1990 (153) .

Experimental infection may induce mortality and transient diarrhoea in chicks following infection at one-day-old with a known enteroinvasive and pathogenic strain of C. jejuni (149). Subsequent exposure to the organism results in colonisation of the intestinal tract resulting in either watery droppings (125) or the absence of clinical signs (194) . Neonatal infection with pathogenic strains of C. jejuni possessing virulence factors may produce focal hepatic necrosis and distention of the jejunum (39) or focal haemorrhage (194) . Generally, flocks infected with C. jejuni show no clinical abnormality.

Oral infection results in colonisation of the distal jejunum, caecum and cloaca (39), with the organism located in the mucosal film. An outer membrane protein component, with a molecular weight of 69 kDa, is associated with colonisation (118) . Campylobacter jejuni is attracted to L-fucose, a terminal sugar of the glycoprotein constituent of mucin (74). Infected broiler flocks excrete C. jejuni from the second or third week during the growing cycle (1). Prevalence rates among flocks vary, with values ranging from 17% to 9 0 % in surveys conducted between 1984 and 1996, as documented in Table I.

378 Rev. sci. tech. Off. int. Epiz., 19 (2)

Table ! Prevalence rate of commercial broiler flocks infected with Campylobacter jejuni

Authors Country Prevalence rate (%) Reference

Prescott and Gellner (1984) Canada 48 140 Altmeyer et al. (1985) Germany 54 11 Engvall et al. (1986) Sweden 17 51 Pokamunski et al. (1986) Israel 31 138 Evans(1992) England 50 52 Kapperud et al. (1993) Norway 18 92 Humphrey et al. (1993) England 76 77 Jacobs-Reitsma et al. (1994) The Netherlands 82 83 Stern et al. (1995) United States of America 90 173 Berndtson et al. (1996) Sweden 27 24 Pearson et al. (1996) England 36 134 Van de Giessen et al. (1996) The Netherlands 57 189

Seasonal differences in prevalence rate can be detected, with higher recovery during summer compared to winter in Norway (90), the Netherlands (82), Sweden (24) and Yugoslavia (13), which is reflected in corresponding levels of contamination on processed broiler carcasses (198) . Generally, intraflock transmission is rapid following introduction of infection. A field study showed an infection rate, based on cloacal isolation, increasing from 2% on the tenth day of the growing cycle to 8 0 % on the twentieth day and persisting until the eightieth day (57) . Data from commercial broiler processing plants in Israel confirm prevalence rates within flocks ranging from 5 8 % to 100% of representative birds selected at slaughter. These field surveys are supported by the results of experimental infection which show rapid horizontal transmission of C. jejuni among contacts ( 1 2 0 , 1 6 3 , 1 6 2 ) .

Appropriate pre-harvest control is dependent on an understanding of the reservoirs of infection, mechanisms of transmission to flocks and the interaction of C. jejuni with the host and commercial housing.

Contaminated water has been demonstrated to be a source of infection for flocks (146). Non-chlorinated water supplied to broilers has been implicated as a vehicle of transmission in Sweden (51) , England (133) and Norway (92) . The occurrence of viable but 'non-culturable' C. jejuni in surface water may be significant in introducing infection onto farms (146). Open water receptacles, including troughs and suspended drinkers, contribute to intraflock dissemination of C. jejuni infection (168). This observation is based on experimental studies demonstrating rapid horizontal spread of C. jejuni, with recovery of the organism from the oral cavity (120, 162).

Wild birds are a potential source of C. jejuni, with a 10% recovery rate from 445 cases representing 13 orders (205) . Species most likely to introduce infection into commercial

poultry flocks include passeriformes (11 , 62) and columbiforrnes (205) . Anseriformes (107) may contaminate surface water used to supply flocks (129).

Insects (90), and especially darkling beetles (82) (Alphatobius diaperinus) and houseflies (Musca domestica) (13, 198) may transmit C. jejuni. The role of houseflies in transmitting C. jejuni infection has been demonstrated under controlled conditions (156).

Rodents may serve as reservoirs of C. jejuni (13, 24) , although recent surveys in the United States of America (USA) have not detected C. jejuni in trapped rats and mice on farms with infected flocks (62, 86) . The role of rodents in introducing or perpetuating infection in successive broiler flocks with appropriate inter-cycle decontamination has not been defined.

The presence of domestic livestock on broiler farms has been implicated as a risk factor in infection of flocks with C. jejuni (13, 92 , 189). Recent studies, applying flagellin-A gene RFLP assays, have demonstrated a commonality among isolates obtained from the intestinal tract of broilers, houseflies, boots of farm personnel and cattle (174). Indirect mechanical transmission of C. jejuni from cattle resident on a farm to successive broiler flocks, by farm personnel, wild birds, vermin, rodents and domestic pets is possible in the absence of appropriate biosecurity procedures and facilities to exclude wildlife.

Feed is not regarded as a source of infection because of the low moisture content and water activity below 0.8, which is inconsistent with survival of C. jejuni (47). Broiler feed, which is generally pelleted, is subjected to pasteurisation temperatures expected to destroy C. jejuni (77). Surveys have consistently failed to show the presence of C. jejuni in broiler feed delivered to farms ( 1 3 , 5 1 , 9 3 ) . Isolation of C. jejuni from

http://passeriform.es


feed in pans and troughs within a house has been documented (103). This is attributed to contamination by regurgitation, or introduction of litter or faeces into receptacles.

Fomites may be responsible for indirect mechanical transmission of C. jejuni, as determined by field surveys (13) . Movement of personnel and equipment between breeder, broiler and turkey growing farms, associated with modern integrated production, may contribute to introduction of infection if clothing, boots and equipment are contaminated with moist faecal material from a flock excreting C. jejuni. Abiotic transmission is facilitated on multi-age farms or where units are in close proximity.

As C. jejuni is intolerant to desiccation (108) , recovery from broiler litter is limited to substrate with a water activity value exceeding 0.85. Contaminated litter has been implicated in infection of flocks of broilers (57, 137) and turkeys (1). Campylobacter jejuni has been recovered inconsistently from the substrate of flocks excreting the organism (62). This suggests that litter is not a suitable medium for survey of C. jejuni infection in broiler flocks. The ability of contaminated litter to transmit C. jejuni under controlled experimental conditions was confirmed using Horsfall isolator units (120). The recovery of the organism from litter is a function of the water activity value of the litter, stocking density, techniques used to collect and transport samples, and methods of enrichment and isolation (159).

The results of numerous field studies generally disfavour the acceptance of vertical transmission of C. jejuni from breeding flocks to progeny via the egg under practical conditions (153). A survey of eggs derived from commercial egg-producing flocks, known to be faecal excretors of C. jejuni, failed to yield the organism from the shell surface or from homogenates of yolk or albumen. Contamination of the surface of shells with a faecal suspension of C. jejuni (1.4 x 1 0 s colony forming units [CFU]/g) resulted in shell penetration in 3/70 eggs and recovery from the contents of only 1/70 eggs (157) . This study confirmed previous investigations which demonstrated that shell membranes serve as an effective barrier to penetration of C. jejuni from the shell to albumen (46). A concurrent study showed that survival of C. jejuni in albumen was limited to six hours. The organism could not be recovered from dead-in-shell embryos, or from the intestinal tracts of neonatal specific-pathogen-free chicks derived from eggs experimentally contaminated with C. jejuni (125).

Turkey poults, brooded in an isolator unit, remained free of C. jejuni for twenty-one days, in contrast to commercially reared birds which excreted the organism by the fifteenth day, concurrently with the recovery of C. jejuni from the drinking water of the birds (2). Both cross-sectional and longitudinal studies of commercial egg-producing flocks and broilers in

Sweden failed to demonstrate C. jejuni excretors in day-old chicks. The organism was recovered from the faeces of the laying-strain pullets at five weeks, but broilers remained free of infection through to slaughter at five weeks of age (103). Consistent with field experience, studies in Sweden showed that chicks derived from sixteen broiler flocks were free of C. jejuni at placement. In the case of eight flocks, excretion of the organism commenced at three weeks and persisted until slaughter at six weeks (51). A survey conducted in Australia failed to detect C. jejuni in 185/187 eggs derived from a breeder flock with a 74% prevalence of faecal excretion. Fourteen placements of broilers, derived from breeders known to be infected, were free of C. jejuni during a six-week growing cycle (161) . In a parallel laboratory study, C. jejuni could not be recovered from 162 chicks hatched from eggs contaminated with a suspension of C. jejuni, suggesting that vertical transmission was unlikely under commercial conditions.

Field studies in Yugoslavia confirmed the observations made previously in Australia. Broiler chicks derived from known infected parent flocks (60% to 8 0 % prevalence) were free of infection at day old but excreted C. jejuni when sampled at twenty-one days (13). A longitudinal study conducted in the Netherlands (188) demonstrated C. jejuni infection in one broiler flock, but C. jejuni was absent in six subsequent placements. Evidence against vertical transmission was predicated by the fact that parent flocks in the Netherlands are frequently infected (81) and that broiler placements are derived from eggs delivered to hatcheries from a large number of parent flocks (188). Freedom from infection in successive flocks was attributed to thorough intercycle decontamination. In a concurrent study, C. jejuni was isolated from seven consecutive broiler flocks. Penner serotyping and random amplification polymorphic DNA-typing denoted identical C. jejuni isolates, suggesting a common source of infection or residual infection in the poultry house.

Recently, the results of a number of investigations based on more sensitive assays for C. jejuni using molecular biological techniques have again raised the question of vertical transmission. Applying a DNA hybridisation procedure, investigators in Japan were able to demonstrate C. jejuni infection in day-old broiler chicks at the time of placement and over the following three-week period. Conventional microbiological assays with enrichment failed to detect the organism in cloacal swabs (38) .

A recent study applying DNA sequencing of the variable region of the flagella antigen fla A gene confirmed that C. jejuni isolates from a breeder flock and the broiler progeny of this flock were identical (40). The fact that the farms were separated by a distance of 30 km suggests congenital infection, either vertically through the egg, or associated with infection during incubation, handling or delivery.


Previous studies have demonstrated the susceptibility of day-old chicks to infection with C. jejuni (149) , especially by the intra-cloacal route (39). Horizontal transmission occurred rapidly among chicks in the hatching trays of commercial incubators and also in chick delivery boxes. Attempts at culture showed that two of fifteen samples of the water in the humidity pans in the hatcher were contaminated with C. jejuni. Given the high rate of air displacement by fans in hatchers, C. jejuni introduced into the environment of an incubator may be disseminated rapidly among the hatchlings. It was previously noted that a small proportion of eggs yield C. jejuni following experimental infection (46). Faecally soiled eggs, especially with damaged shells, which are subjected to incomplete decontamination by either disinfectant solutions or fumigants may introduce C. jejuni into incubators and the hatchery environment. This may result in infection of chicks at the time of pipping and thereafter, as the hatch is subjected to 37°C and 70% relative humidity for the holding period which frequently exceeds twelve hours, conditions which are conducive to survival of C. jejuni.

The recent series of DNA-based assays should be extended to define the mechanisms relating to possible vertical infection. To confirm this route of infection, the identification of a common serotype in parent flocks, eggs and progeny is required. The presence of the same gene for a flagella antigen, in both parent stock and progeny does not necessarily eliminate congenital infection through exposure in the hatchery environment, independently of direct vertical transmission through the egg.

Evaluating the results of field studies on commercial flocks, including a large number of prevalence surveys and laboratory experiments, the following conclusions are relevant to the epidemiology of C. jejuni infection in breeders, broilers and growing turkeys:

- Campylobacter jejuni is prevalent in all types of commercial flocks in all regions of the world where poultry is raised and where surveys have been conducted

- although the organism is sensitive to desiccation, intensive systems of production, especially in integrated operations, facilitate transmission to both floor and cage-housed flocks

- the major reservoirs of infection include the intestinal tracts of mature breeding flocks, commercial broilers and turkeys and replacement pullet flocks over three weeks of age

- the known routes of abiotic transmission include non-chlorinated surface water or water from wells, faecally contaminated clothing, footwear and equipment and exposure of a young flock to a contaminated environment

- rodents, vermin, insects, wild birds, domestic livestock and companion animals may serve as reservoirs or sources of infection

- conventional methods of sampling, followed by enrichment and culture may not be capable of isolating viable but non-culturable C. jejuni. Sophisticated DNA-based

techniques will, in the future, contribute to a greater understanding of the molecular epidemiology of C. jejuni infection at the commercial flock level.

Contamination of poultry meat with Campylobacter The high prevalence of Campylobacter on poultry meat and derived products is of significance to consumers (8). Records of the occurrence of C. jejuni and the less frequently isolated species of Campylobacter (C. coli, C. lari and C. fetus) during the period 1980 to 1990 are documented in a review of forty-two publications concerning seventeen countries and five poultry species (153).

Live broilers (128) , turkeys (206) and ducks (93) are delivered to processing plants with high levels of faecal contamination (195). A study conducted in the USA confirmed that 2 0 % of live broilers yielded C. jejuni from cloacal swabs obtained at the time of delivery to two plants (86). Unwashed transport coops may contribute to surface contamination of plumage and feet (71) , resulting in recovery rates of 8 0 % to 100% from the caecum for clinically healthy broiler flocks (195).

The practice in the USA of withholding feed from broiler flocks for periods of 6 h to 10 h to reduce contamination of carcasses with ingesta during evisceration, may exacerbate the introduction of C. jejuni contamination into plants via the crop. The recovery of the organism increased from 2 5 % of 360 crops before feed withdrawal, to 6 2 % at the time of harvesting. During an eight-hour period, levels of C. jejuni in the caeca of the subject birds remained constant (34). Subsequent studies using a fluorescent dye gavaged into the crop confirmed the extent of dissemination of ingesta among carcasses and the eviscerating environment (65, 66) . Surveys conducted at three processing plants demonstrated cross contamination of carcasses during defeathering and evisceration, but a decrease in level of C. jejuni on the skin surface associated with scalding and immersion chilling (79). On-line washing of turkey carcasses with chlorinated water reduced levels of contamination (2).

A recent study of whole, processed packed and refrigerated carcasses and portions at point of sale yielded a Campylobacter recovery rate of 2 6 % . The products were derived from five countries of the European Union (EU) with similar methods of flock management and processing (185). The values recorded in the study in Belgium are generally in agreement with surveys which yielded a 2 8 % recovery rate in a survey conducted in Germany (15). Higher levels of C. jejuni were documented in a study in the USA using enrichment culture of samples derived from whole carcasses offered for sale. Recovery ranged from a low of 7% in December, to 97% in June and July, with an average annual rate of 6 4 % among

Rev. sci. tech. Off. int. Epiz.. 19 (2) 381

the thirty samples examined by whole carcass wash (198) . Previous surveys over the period from 1980 to 1988 to quantify the levels of C. jejuni contamination on broiler carcasses reveal a generally high rate of recovery ranging from 14% to 8 8 % , with an unweighted mean of 57% (Table II).

The recovery rate from carcasses may be influenced by the proportion of flocks infected, the degree of intraflock colonisation, seasonal and climatic factors, configuration and operation of immersion tanks and processing plant equipment, chlorination and chemical treatment of water and carcasses and microbiological techniques used for sampling, isolation and identification.

Quantification of the level of Campylobacter on carcasses, portions and derived products can be influenced by handling and storage (130) . Freeze-thaw and heat stress injury following exposure to disinfectants or acids can lower recovery of C. jejuni, unless appropriate enrichment and isolation techniques are applied.

Campylobacter jejuni is relatively tolerant to freezing (64) . A reduction of 0.5 to 2.0 log was recorded over a two-week period on broiler carcasses held at - 2 0 ° C , with inoculation levels of 1 0 3 to 1 0 5 CFU/g. Viability of C. jejuni persisted on drumsticks contaminated at a level of 4.8 x 1 0 3 CFU/cm 2 , for an extreme shelf life of ten days at both 9°C and - 1 2 ° C . At -20°C , the level of C. jejuni declined from 9.9 x 1 0 2 CFU/cm 2

to 4.5 x 10 CFU/cm 2 in seven days, but persisted through the twenty-sixth week of storage with a terminal level of 0.2 x 10 CFU/cm 2 (203) .

Campylobacter jejuni survived for up to twenty-eight days in vacuum-packed processed turkey rolls and hams held at 4°C (143). A statistically significant decrease was reported in the level of C. jejuni over time, and differences in viability were recorded among three isolates. The organism survived in sliced turkey roll under carbon dioxide enriched packaging for eighteen days at 4°C, confirming that processed poultry products may serve as a vehicle for infection.

Campylobacter jejuni infection on whole broiler carcasses is sensitive to cooking for 90 minutes at 190°C when subjected to moderately high levels of contamination corresponding to 1 0 3 CFU/carcass. Some recontamination from mishandling of cooked carcasses was demonstrated when an inoculum of 1 0 6 CFU was applied (59).

The potential of C. jejuni contamination of carcasses to be disseminated over hands and work surfaces was demonstrated in institutional kitchens surveyed in England (42). The organism was recovered from 8 8 % of chilled and 10% of frozen broiler carcasses respectively, and from the kitchen environment (34%) and hands (4%) during preparation of chicken. In contrast, the environment was free of contamination before processing and after cleaning. A variety of Skirrow biotypes were identified on the carcasses which were recovered from hands and the kitchen environment. Similar results were obtained in the Netherlands where extensive cross contamination was demonstrated in a structured trial simulating transfer of C. jejuni from carcasses to work surfaces, raw vegetables and cooked products (43) .

Commercial table eggs In contrast to the high prevalence of C. jejuni infection on poultry meat, extensive surveys have failed to demonstrate the potential pathogen in table eggs destined for consumption. Commercial hens known to be faecal shedders of C. jejuni did not produce infected eggs using conventional microbiological detection (157). A parallel study did not detect C. jejuni in 276 eggs derived from twenty-three farms in the State of New York (17). A survey conducted in two commercial egg processing plants did not demonstrate C. jejuni in eggs, derived products or from samples of water collected from the overflow of the egg washer (78). The investigators were able to detect C. jejuni from experimentally inoculated control specimens.

Table II Recovery rate of Campylobacter jejuni from broiler carcasses

Authors Country Recovery (%) Reference number

Chowdhury et al. (1984) India 63 36 Dawkins et al. (1984) United Kingdom 88 42 Rosei et al. (1984) Norway 14 147 Stern et al. (1984) United States of America 30 171 Harris et al. (1986) United States of America 56 67 Juven and Rogol (1986) Israel 70 87 Humphrey and Lanning (1987) United Kingdom 54 75 Hood et al. (1988) United Kingdom 48 70 Lammerding et al. (1988) Canada 38 99 DeBoerand Hahne (1990) The Netherlands 61 43

382 Rev. sci. tech. Off. int. Epiz, 19 (2)

Based on epidemiological studies involving numerous outbreaks of campylobacteriosis, eggs have not been identified as a primary source of infection. Accordingly, regulations aimed at preventing international movement of eggs on the basis of potential Campylobacter infection would be unjustified.

The relation between poultry and campylobacteriosis in humans Incidence of Campylobacter infection in humans The United States Department of Health, Centers for Disease Control and Prevention has recently completed an extensive survey of food-bome disease in the USA (117) . Figures were collected from ten national and regional databases including the Food-bome Disease Active Surveillance Network ('Food Net') established in 1996. An estimate of the incidence of campylobacteriosis in 1998 was based on active surveillance among a population of 20 million. The incidence rate from 1996 to 1997, of 24/100,000 was extrapolated to the entire population of the USA following application of a multiplication factor of thirty-eight to represent the proportion of non-reported to diagnosed cases. The total estimated number of cases in the USA exceeded 2.5 million, with 13,000 hospital admissions and 124 deaths in 1997. Campylobacteriosis represented 14.2% of all diagnosed food-borne infections including bacterial, viral, protozoal and metazoal aetiologies, and exceeded paratyphoid salmonellosis (9.7%) in incidence. The most recent compilation of data on food-borne Campylobacter infections in the USA updates previous reports on occurrence and causation of outbreaks covering the period from 1973 to 1992 (20, 2 1 , 179). The campylobacteriosis incidence rate in the USA of 1,020/100,000 population, estimated in 1992 (176) , is strongly supported by the latest, more structured evaluation.

The differential between diagnosed and non-reported cases of campylobacteriosis complicates estimates of economic losses associated with infection. Based on incidence rates and hospital records pertaining to the mid-1980s, the direct and indirect cost of the disease ranges from US$700 million to US$1,400 million (121). A comparative value of US$150 million was estimated for the United Kingdom (UK), based on an incidence rate of 1,100/100,000 and prevailing medical costs in that nation (166).

Epidemiology of Campylobacter infection in humans A recent review of C. jejuni infection as a food-borne disease, provides a perspective of the history, epidemiology and prevalence of the condition in human populations (10), supplementing information contained in earlier reviews (136, 1 5 4 , 1 7 7 ) . Campylobacter jejuni is responsible for over 9 5 % of

the diagnosed cases of campylobacteriosis, whilst C. coli and G lari are occasionally isolated from cases of haemorrhagic enteritis in industrialised countries which maintain appropriate surveillance systems (179) . Campylobacter coli represented 19% of the isolates in a survey in Portugal (35) , 1 1 % in Singapore (101) and 3 5 % in Yugoslavia, with a predominance of this species from patients in rural areas (139).

Following the first recognised cases of enteritis attributed to 'related vibrios' in 1952 (94), an association was recognised between infection and either the consumption of contaminated food products of animal origin or direct contact with livestock. Stmctured investigations were later facilitated by pivotal advances in isolation, culture and identification of the 'related vibrios' from faeces (44). By the late 1970s, Campylobacter enteritis was recognised as an emerging food-borne disease (165). At this early stage in the understanding of the disease, the recognised risk factors included close contact with domestic flocks or processing of poultry, handling diarrhoeic companion animals or foreign travel by residents of urban areas of industrialised countries in the northern hemisphere (142) .

The first documented outbreak of campylobacteriosis which was directly attributed to consumption of chickens occurred in the Netherlands among a group of cadets who experienced an 8 0 % attack rate (28). Subsequent surveys confirmed the high prevalence of C. jejuni in the faeces of patients and on the carcasses of broilers and turkeys (61, 127). The introduction of serotyping schemes (106 , 135) and biotyping (105) facilitated epidemiological studies (110) to establish relationships between sporadic outbreaks in communities and consumption of processed poultry in Australia (160) , the UK (85), the Netherlands (18), Yugoslavia (13) and Germany (200).

Campylobacteriosis may be regarded as an occupational infection of processing plant workers (60) . A single outbreak was documented in a poultry abattoir in Sweden, affecting thirty-seven workers of whom 7 1 % were young, untrained temporary summer labourers (37). A comparison of titres in a survey in the UK revealed that 27% to 6 8 % of workers in poultry and red meat plants demonstrated antibodies to C. jejuni compared to 3% among field labourers (84). A survey conducted in Italy confirmed antibody titres to G jejuni in 12% of abattoir workers, compared to 2% in a cohort of blood donors (113).

Young adults, and specifically male college students (123) , demonstrate high incidence rates for Campylobacter infection, approaching 15/100,000 during the mid-1980s (178). An outbreak at the University of Victoria, British Columbia, Canada, in the autumn of 1984, involved an attack rate of 30%. among 1,076 students. Salads and fried chicken were implicated as vehicles, with evidence of mishandling and


improper storage, preparation and serving of food (4). A subsequent case control study conducted at the University of Georgia, USA, identified the consumption of undercooked and raw chicken and contact with a cat as risk factors for infection (odds ratio: 9) , resulting in an overall C. jejuni isolation rate of 24 /10 ,000 students per academic quarter of fifty days (45).

Contact with raw chicken during food preparation is regarded as a significant risk factor for campylobacteriosis among consumers (72, 91) . Raw poultry carcasses and portions and seepage during thawing frequently contaminate hands, storage areas, work surfaces and utensils, leading to transfer of C. jejuni to salads and other non-cooked foods. Improper and unhygienic procedures during storage and preparation (29, 68) contribute to outbreaks of campylobacteriosis in catering and institutional units (9) and also in domestic kitchens. Educational initiatives undertaken by the Food Safety and Inspection Service of the United States Department of Agriculture (USDA) address the safe handling of poultry meat (184).

Children are at risk of campylobacteriosis, based on age-prevalence data. An incidence rate of 36 /100 ,000 was determined for infants in the USA in 1997 (14). Reports from various countries confirm the susceptibility of children, including Taipei China (102) , the USA (180) , Mexico (186) , Chile (54), Guatemala (41), Peru (122) , Singapore (101) , Portugal (35), Israel (152) , Liberia (119) , Nigeria (3), South Africa (144) and Bangladesh (25). The high rates recorded in surveys conducted in non-industrialised countries reflect deficiencies in sanitation, hygiene, housing, consumption of unchlorinated water, unpasteurised milk and non-refrigerated food, and contact with domestic livestock including free-ranging chickens (116). In industrialised countries, contact with diarrhoeic pets, food-borne infection and direct contact transmission have been reported to occur in day-care centres employing suboptimal procedures for food handling and hygiene (19).

Immunosuppressed patients, including those infected with human immunodeficiency vims (HIV), are extremely susceptible to campylobacteriosis, especially when concurrent exposure to opportunistic fungal and protozoal pathogens occurs (23) . Isolation rates of C. jejuni increase with age. Data for the period 1982-1986 in the USA confirm a rise from 1/10 5 in the age range 40-45 to 5 / 1 0 5 in the 60-65 year cohort. The frequency of isolation of C. jejuni from blood increases exponentially with age (180).

Antibiotic resistance The isolation of antibiotic resistant strains of Campylobacter from poultry represents an emerging public health problem. Plasmid-mediated resistance to tetracycline was demonstrated in Canada in 1983. The studies revealed a close relationship

between isolates from humans and domestic animals (182) . The occurrence of erythromycin resistant strains of C. jejuni was documented in Israel, using the agar dilution technique which was considered superior to the less sensitive disc susceptibility method (145). A survey of the antibiotic sensitivity of twenty-one C. jejuni isolates from healthy chickens in Canada showed resistance to sulphonamides and bacitracin (both intrinsic), streptomycin, tetracycline and penicillin G (27) . The isolates were all susceptible to erythromycin, kanamycin and ampicillin.

The mechanisms of antibiotic resistance in Campylobacter, and the prevalence of resistant strains was comprehensively reviewed during the late 1980s (183) . Campylobacter jejuni strains were noted to be highly susceptible to quinolones, but plasmid-mediated resistance to tetracyclines and aminoglycosides (in the case of C. coli) was documented.

A significant paper confirming a parallel increase in quinolone resistance of C. jejuni isolates from human patients and from poultry was attributed to the extensive use of enrofloxacin in the production of broilers in the Netherlands. During the period between 1982 and 1989, quinolone resistance in human isolates increased from 0% to 11.5%. During the same period, poultry isolates increased in resistance from 0.5% to 14% (50). In contrast, a survey in Sweden showed no increase in resistance to antibiotics used therapeutically for gastroenteritis among isolates of C. jejuni from patients during the period 1978 to 1988. In 1989, 14% of Campylobacter isolates were resistant to quinolones, with corresponding values of 7.3% and 12.4% for erythromycin and doxycycline, respectively (164) .

A study on quinolone resistance of species of Campylobacter derived from poultry abattoir effluent arid sewage plants was conducted in the Netherlands in 1995. Of the isolates derived from the poultry plant outflow, 2 8 % were resistant to quinolones. In contrast, 1 1 % to 18% of isolates from a sewage treatment plant were resistant to quinolones. A second plant receiving effluent from various sources, including a poultry abattoir, yielded 17% to 3 3 % quinolone resistant Campylobacter (95). The difference between the Netherlands and Sweden with respect to prevalence of quinolone resistance was attributed to the patterns of drug use in poultry in the respective countries.

During the period from 1990 to 1994, a study in Spain demonstrated that resistance to quinolones increased from 4 5 % to 8 8 % of C. jejuni isolates obtained from patients. During the same period, the proportion of isolates resistant to chloramphenicol, amoxycillin and tetracycline remained constant (148).

Quinolone resistance in Campylobacter involves a single point mutation around residues Ser 83 and Asp 87, located near the N terminus of the gyrase A subunit (197). Inappropriate and


excessive administration of antibiotics, including quinolones, to poultry is regarded as a major source of drug resistant C. jejuni. In the USA, where quinolones have been licensed for restricted therapy of poultry since 1995, under strict veterinary supervision and employing the 'principles of prudent use' of the Food and Drug Administration, ciprofloxacin resistant C. jejuni can be recovered from processed broilers (10) .

Autoimmune conditions following campylobacteriosis During the 1990s, epidemiologists confirmed a relationship between infection with C. jejuni and post-recovery autoimmune conditions. These include Guillain-Barré syndrome (GBS) (88), Fisher's syndrome, a variant of GBS (96), and Reiter's syndrome, a non-purulent reactive arthritis (48).

Guillain-Barré syndrome is an acute neuro-muscular paralysis associated with an inflammatory demyelinating polyneuropathy. Following an increase in anecdotal reports on the possible relationship between C. jejuni infection and subsequent GBS (22), surveillance studies established a serological basis for the association (7). A case-control study determined a significantly higher antibody titre in patients with GBS, compared to fifty-five controls (odds ratio: 12.5 with a 9 5 % confidence interval of 0.6 to 33) in five centres in the USA during the summer months of 1983 to 1990. Similar results were obtained from a field study conducted in the north of the People's Republic of China, which showed a statistically significant difference (P = 0.001) in C. jejuni titre in patients with GBS (66%), compared to controls (16%) (69). Microbiological studies have confirmed the presence of C. jejuni in patients at the time of onset of GBS (5). According to estimates, 3 0 % to 4 0 % of GBS cases are preceded by C. jejuni infection, and one case of GBS follows 1,050 infections (6). The lipopolysaccharides of C. jejuni and specifically the 0:19 serotype are thought to stimulate an inappropriate immune response to the gangliosides GM1 and GDlb incorporated in the myelin sheath of peripheral nerves. This mechanism may be common to infection with Epstein-Barr virus, cytomegalovirus and Mycoplasma pneumoniae, which are also associated with GBS (80).

The annual economic impact of GBS in the USA was calculated to be US$0.2 to US$1.8 billion on the basis of 3,000 to 10,000 reported cases. Between 500 and 3,500 cases of GBS were assumed to be initiated by C. jejuni infection (33).

Reactive arthritis and associated conjunctivitis and stomatitis occur following C. jejuni infection in patients demonstrating HLA-B27 antigen (191). No reports have been published on the incidence or cost of autoimmune arthroses following food-borne C. jejuni infection.

Reduction of Campylobacter jejuni contamination in poultry meat Pre-harvest control of Campylobacter The amelioration of C. jejuni contamination must be based on control during both the pre-harvest and processing components of the chain of production.

If confirmation is obtained that vertical transmission of campylobacteriosis can occur from parent flock to broiler progeny, the implementation of programmes to limit the introduction of infection into grandparent and parent level breeder flocks will be necessary. Intensification of biosecurity to suppress Salmonella should also reduce exposure to Campylobacter, as many of the mechanisms of transmission are common to the two organisms. The biosecurity precautions appropriate to breeding farms have been reviewed (158) and incorporate both structural and operational procedures. Poultry houses should be designed and constructed to eliminate the entry of rodents and wild birds which are reservoirs of infection. Showering of personnel, provision of clean clothing and footwear, and placement of disinfectant boot dips, are basic procedures which can reduce the probability of introduction of infection.

Although feed is not regarded as an important vehicle for Campylobacter, pelletisation with heat pasteurisation and the addition of organic acids will effectively eliminate infection in feed.

The introduction of mechanical egg collection eliminates the need to use nest litter which is often associated with faecal contamination of shells. Frequent collection of eggs using a mechanical installation with self-cleaning belts, followed by decontamination after collection using either formalin fumigation or a phenolic disinfectant, will reduce the probability of mechanical transmission of Campylobacter.

Since breeding stock is intrinsically valuable, with each female potentially capable of producing 130 broiler chicks, expenditure on competitive inhibition cultures is justified. As water has been demonstrated to be an important source of Campylobacter, chlorination of the central supply at a level of 2 ppm to 3 ppm is strongly recommended (146). Removal of the biofilm in water supply lines using frequent cycles of flushing will reduce the potential for infection. Recent studies implicating domestic livestock, including cattle, as reservoirs of infection, suggests that farms should be securely fenced to exclude food animal and companion species.


The hatchery is a potential link in the chain of transmission from breeder flock to broilers, and accordingly, intensification of biosecurity procedures and decontamination should be emphasised in a control programme appropriate for an integrated poultry producer (158) .

Litter additives, including sodium bisulphate (112) , acidify the upper 5 cm to 10 cm of substrate and may reduce exposure to Campylobacter by eliminating sporadic introduction of low grade infection by defects in biosecurity. Field trials of sodium bisulphate, added to litter at 2 kg to 3 kg/10 m 2 , delayed the onset of infection in flocks, compared to controls on untreated litter. Litter treatment did not prevent infection in thirty-five-day-old broilers which were assayed at processing (56). Intensifying biosecurity will reduce but not eliminate the possibility of introduction of infection (190).

Applying competitive exclusion cultures, immunological adjuvants and stimulants, and dietary supplements can reduce the prevalence and intensity of Campylobacter colonisation in broilers under controlled laboratory conditions (16). Trials with undefined caecal cultures have confirmed the studies on the 'Nurmi effect' (141) and subsequent work conducted in the USA (169) and the UK (76) in which inhibition of colonisation, but not absolute eradication of Campylobacter, could be achieved. The weight of literature suggests that competitive inhibition is a more effective mechanism against Salmonella than Campylobacter ( 1 0 4 , 1 7 0 ) .

Rearing broilers on plastic mesh to eliminate the possibility of coprophagy offers some potential in eliminating food-borne intestinal pathogens. Technical, financial and animal welfare restraints limit the possibility of applying off-litter growing as a means of eliminating Campylobacter infection in commercial broilers.

Currently, no vaccines are available for commercial control of Campylobacter in live parent stock or progeny. Although studies have been undertaken on the immunology and molecular biology of Campylobacter jejuni, products which are both effective and economically feasible have yet to be developed.

Post-harvest control of Campylobacter Procedures to reduce the amount of Campylobacter infection entering processing plants on live broilers should be implemented. Thorough disinfection of coops and transport modules will reduce interflock contamination which may occur with partial flock depletion programmes.

Since introduction of mandated hazard analysis and critical control point (HACCP) programmes in the USA to reduce microbiological contamination of poultry and red meat, a significant decrease has occurred in contamination of carcasses with Salmonella (115) .

This decrease is largely attributable to an increase in water utilisation for overflow of scalders, immersion chillers and improved 'inside-outside' spray washers. Concurrently, most processing plants have increased the levels of chlorine in immersion tanks and spray washers to achieve a reduction in Salmonella recovery from 2 0 % of carcasses to a national average of 10% to 12%. Initial surveys conducted by the USDA Food Safety and Inspection Service and individual companies suggest that methods to reduce Salmonella contamination have not resulted in a corresponding decrease in the recovery of Campylobacter, which remains at high levels.

Immersion scalding is associated with a reduction in the level of C. jejuni on broiler carcasses providing the temperature of the water is maintained above 50°C at a pH range of 8 to 9. Additional reduction in the level of C. jejuni can be achieved by adding a quaternary ammonium disinfectant to water used for scalding, at a level of 50 ppm to 100 ppm (73). Concurrent studies showed that a reduction in the number of C. jejuni from 80 to 100 organisms/ml is possible, but with no effect on carcass contamination (75).

The introduction of an antimicrobial additive into 'inside-outside' bird washers can reduce the level of Salmonella on carcasses, and presumably also decrease C. jejuni levels. Trials conducted in the USA show that 0 .5% cetylpyridinium chloride, 10% trisodium phosphate, 5% sodium bisulphate and 2% lactic acid are active against Salmonella when applied at a temperature of 35°C and a pressure of 4 0 0 kPa for 60 seconds. Of the range of chemicals, 0 .5% cetylpyridinium chloride was the most effective (202) . Trisodium phosphate is widely used as an antimicrobial rinse and is approved for application in poultry plants in the USA. Statistically significant reduction in the recovery rate of C. jejuni from carcasses has been documented under practical conditions. Application of trisodium phosphate in a commercial carcass washer (level not stated but presumed to be 10%) reduced Campylobacter levels from a prewash rate of 7 8 % of carcasses examined to 4 6 % . By comparison, Salmonella levels were reduced from 3 0 % to 1% and Escherichia coli from 9 6 % to 1%, confirming the greater susceptibility of these organisms to trisodium phosphate compared to Campylobacter (49). Previous studies on disinfectants have demonstrated the efficacy of 0.5% lactic and acetic acids, and chlorine at 100 ppm (204) . Recent studies have focused on practical aspects of application and evaluation under operating conditions at line speeds exceeding 9,000 birds per hour. Chemical treatment is subject to approval by regulatory authorities in the USA and the EU. Registration requires data demonstrating the absence of either mutagenic or toxic effects of chemicals and to ensure that at practical levels, equipment is protected from damage and that organoleptic properties of poultry products are not compromised (153).


Gamma irradiation ('cold pasteurisation') is an effective

method of eliminating C. jejuni from poultry meat and

products (89). Experiments have established D 1 0 values of

0.3 kGy for C. jejuni, suggesting that a 2 kGy dose would

effect a six log reduction in levels of C. jejuni (98). The

literature on ionising radiation in relation to poultry

supports the finding of the joint Food and Agriculture

Organization/International Atomic Energy Agency/World

Health Organization Committee, which established a 10 kGy

level to eliminate Salmonella and other bacterial food-borne

pathogens in poultry meat.

A petition to the Food and Drug Administration of the USA to

amend the appropriate regulation (21 CFR 179.26) to allow

irradiation of poultry products was filed in late 1986.

Following approval by this agency, in 1990, the USDA Food

Safety and Inspection Service developed specific regulations

relating to procedures, controls and labelling to allow for

irradiation at a level ranging from 1.5 kGy to a maximum dose

of 3.0 kGy. Irradiation of poultry meat is not approved for use

in all countries.

Feasibility studies on cobalt 6 0 isotope irradiation

demonstrated the need to invest US$2 to US$4 million in a

free standing plant which could irradiate poultry and other

food products at a cost ranging from US$0.05 to US$0.1

per kg, depending on volume of utilisation, the interest rate

and local factors (30). The development of electron beam

technology will facilitate the adoption of 'cold pasteurisation',

since the elimination of isotopes and the lower capital cost of

an installation may represent a more acceptable alternative for

poultry producers.

Despite adverse publicity by opponents of food irradiation, no

evidence suggests a widespread consumer rejection of

irradiated poultry (58). Trials conducted at the University of

Georgia confirmed that education is an important motivator

to accept 'cold pasteurised' breast and thigh portions. Over

8 0 % of informed consumers accepted that 'cold

pasteurisation' reduced the risk of food-borne infection. Half

the subjects were willing to pay a 5% premium for treated

product. Current information relating to food preservation

using ionising radiation including packaging, and the

sensitivity of bacteria including Campylobacter have been

extensively reviewed (12, 53) . Acceptance of 'cold

pasteurisation' by both producers and consumers will be a

necessary requirement for the widespread use of this

technology. Establishing that poultry meat subjected to

ionising radiation is both wholesome, nutritious and free of

bacterial food-borne pathogens will encourage the

commercialisation of the process.

At present, Campylobacter contamination of poultry products

can be ameliorated by a combination of pre- and post-harvest

procedures. Poultry products should be stored and

transported at a temperature of 4°C or lower to prevent

proliferation of Campylobacter and other food-borne bacterial

pathogens. Appropriate precautions in handling and

preparation of raw poultry, decontamination of utensils and

work surfaces, and thorough cooking in accordance with

health codes should reduce the risk to consumers.

Significance for international trade Campylobacter jejuni and C. coli are widely distributed among

commercial broiler, turkey and commercial egg-producing

flocks in all countries where commercial poultry industries

operate. The frequency of recovery of Campylobacter from

broiler and turkey carcasses and portions is a function of

diagnostic intensity. Commercial table eggs are not involved

in transmission of Campylobacter infections from caged flocks

to consumers. In view of the widespread distribution of

Campylobacter infection in foods derived from mammalian

livestock and poultry, and the presence of the organism in

untreated water, imposition of trade restrictions on poultry

meat following recovery of C. jejuni or C. coli would be

inappropriate.

Infection à Campylobacter chez les volailles commerciales S.M.Shane

Résumé Campylobacter jejuni, largement répandu et transmis par les aliments, est à l'origine de cas d'entérite chez l'homme dans les pays développés et en développement. L'infection survient après consommation d'eau, de lait ou d'aliments contaminés. La viande de volaille contaminée est considérée comme une source importante de campylobactériose ; les poulets de chair et les dindes issus de l'élevage industriel s'infectent par exposition horizontale directe et


indirecte à l'âge de deux ou trois semaines. L'eau non chlorée est considérée comme une source de contamination, celle-ci se disséminant ensuite rapidement au sein de l'élevage. L'intensification de l'aviculture industrielle entraîne une présence accrue de la bactérie dans les carcasses, du fait de l'accroissement des capacités de stockage et de l'automatisation des processus de transformation, indispensables pour atteindre l'efficacité optimale requise par un marché de plus en plus concurrentiel. Actuellement, des mesures prophylactiques avant et après abattage peuvent contribuer à protéger le consommateur contre l'infection à Campylobacter. Le stockage et le transport réfrigérés des viandes rouges et des volailles, la manipulation et la préparation d'aliments dans des conditions appropriées ainsi qu'une cuisson suffisante permettent de réduire les risques d'intoxication alimentaire. Compte tenu de la répartition mondiale de l'infection à C. jejuni et de la multiplicité des sources de contamination, y compris le lait non pasteurisé et l'eau, il serait vain d'imposer des restrictions aux échanges de viande de volailles sur la base de la détection de Campylobacters.

Mots-clés Campylobacter coli - Campylobacter jejuni - Maladies aviaires - Prévalence - Prévention après abattage - Prévention avant abattage - Toxi-infection alimentaire - Volailles.

Infección por Campylobacter de aves de corral de explotaciones comerciales

S.M.Shane

Resumen

La infección por Campylobacter jejuni, organismo transmitido por vía alimentaria, se contrae por consumo de agua, leche o alimentos contaminados y da lugar a brotes de enteritis entre las poblaciones de países tanto industrializados como en desarrollo. La contaminación de aves, que afecta sobre todo a los pollos asaderos y pavos de dos a tres semanas de edad de las explotaciones comerciales, infectados por exposición horizontal directa o indirecta, se considera una importante fuente de campilobacteriosis. Se piensa que el agua no clorada constituye un importante vehículo de la infección, que después se propaga rápidamente en el interior de las bandadas. La intensificación de la producción avícola, asociada a la mayor densidad de almacenamiento y a la mecanización de los sistemas productivos inherentes al elevado rendimiento que exige un mercado muy competitivo, han contribuido a elevar las tasas de prevalencia en las aves. En las circunstancias actuales, la aplicación de medidas de control previas y posteriores al sacrificio puede paliar el problema que supone la infección por Campylobacter para los consumidores. El transporte y almacenamiento de carne roja y aves de corral en instalaciones refrigeradas, la manipulación y preparación correctas de los alimentos y su cocción completa reducen las probabilidades de infección alimentaria. Habida cuenta de la distribución mundial que presenta la

388 Rev. sci. tech. Off. int. Epiz, 19 (2)

in fecc ión por C. jejuni y de la mul t ip l ic idad de fuentes (entre ellas la leche no pasteur izada y el agua contaminada) , no resulta ind icado imponer barreras comerc ia les a las aves basadas en la de tecc ión de Campylobacter.

Palabras clave Aves de corral - Campylobacter coli - Campylobacter jejuni - Control posterior al sacrificio - Control previo al sacrificio - Enfermedades aviares - Infección alimentaria -Prevalencia.

References

1. Acuff G.R., Vanderzant C., Gardner F.A. & Golan FA. (1982). - Examination of turkey eggs, poults and brooder house facilities for Campylobacter jejuni. J. Food Protec., 45, 1279-1281.

2. Acuff G.R., Vanderzant C , Hanna M.O., Ehlers J.G., Golan F.A. & Gardner F.A. (1986). - Prevalence of Campylobacter jejuni in turkey carcass processing and further processing of turkey products. J. Food Protec., 49, 712-717.

3. Alabi S.A., Coker O., Dosunmu-Ogunbi O. & Odugbemi T. (1988). - Biotype and serogroup distribution of Campylobacter isolates from children in Nigeria. J. clin. Microbiol, 24, 856-858.

4. Allen A.B. (1985). - Outbreak of campylobacteriosis in a large educational institution - British Columbia. J . Food Protee, 48, 458.

5. Alios B.M. (1997). - Association between Campylobacter infection and Guillain-Barré syndrome. J. inject. Dis., 176 (Suppl. 2), 125-128.

6. Alios B.M. (1998). - Campylobacter jejuni infection as a cause of the Guillain-Barré syndrome. Inject. Dis. Clin. N. Am., 12 (1), 173-184.

7. Alios B.M., Ilyas A.A., Koski C.L., Vriesendorp F., Cook S.D., Mithen F.A. & Blaser M.J. (1993). - Serological evidence of previous Campylobacter jejuni infection in patients with the Guillain-Barré syndrome. Ann. internal Med., 118, 947-953.

8. Altekruse S.F., Hunt J.M., Tollefson L.K. & Madden J.M. (1994). - Food and animal sources of human Campylobacter jejuni infection. J . Am. vet. med. Assoc., 204, 57-61.

9. Altekruse S.F., Cohen M.L. & Swerdlow D.L. (1997). -Emerging foodborne diseases. Emerg. inject. Dis., 3, 285-294.

10. Altekruse S.F., Stem N.J., Fields P.I. & Swerdlow D.L. (1999). - Campylobacter jejuni - an emerging foodborne pathogen. Emerg. infect. Dis., 5, 28-35.

11. Altmeyer M., Krabisch P. & Dom P. (1985). - Zum vorkommen and zur Verbreitung von Campylobacter jejuni/coli in der jungmastgeflugel - production. 1 Mitteilung. Dtsch. tierärztl. Wochenschr., 92, 456-459.

12. Andrews L.S., Ahmedna M., Grodner R.M., Liuzzo J.A., Murano P.S., Murano E.A., Rao R.M., Shane S. & Wilson P.W. (1998). - Food preservation using ionizing radiation. Rev. Environ. Contam. Toxicol, 154, 1-53.

13. Annan-Prah A. & Janc M. (1988). - The mode of spread of Campylobacter jejuni/coli to broiler flocks. J. vet. Med., 35, 11-18.

14. Anon. (1998). - Incidence of foodbome illnesses - FoodNet, 1997. Morb. Mort. weekly Rep., 47 (37), 782-786.

15. Atanassova V., Altemeir J . , Kruse K.P. &Dolzinski B. (1998). - The detection of Salmonella and C. jejuni/coli in fresh poultry. Fleischwirtschaft, 78, 364-366.

16. Bailey J.S. (1993). - Control of Salmonella and Campylobacter in poultry production. A summary of work at Russell Research Center. Poult. Sci., 72, 1169-1173.

17. Baker R.C., Paredes M.D.C. & Qureshi R.A. (1986). -Prevalence of Campylobacter jejuni in eggs and poultry meat in New York State. Poult. Sci., 66, 1766-1770.

18. Banffer J.R.J. (1985). - Biotypes and serotypes of Campylobacter jejuni and Campylobacter coli strains isolated from patients, pigs, and chickens in the region of Rotterdam. J. Injection, 10, 277-281.

19. Bartlett A.V., Moore M., Gary G.W., Starko K.M., Erben J.J. & Meredith B.A. (1985). - Diarrheal illness among infants and toddlers in day care centers. I. Epidemiology and pathogens. J . Pediatr., 107, 495-502.

20. Bean N.H., Griffin P.M., GouldingJ.S. & Ivey C.B. (1990). -Foodbome disease outbreaks, 5-year summary, 1983-1987. J. Food Protee, 53, 711-728.


21. Bean N.H., Goulding J.S., Lao C. & Angulo F.J. (1996). -Surveillance for foodborne-disease outbreaks - United States, 1988-1992. Morb. Mort. weekly Rep., 45, 1-66.

22. Beenen L.F.M. & Scholten H.G. (1990). - Het Guillain-Barré-syndroom na een Campylobacter jejuni-enteritis. Ned. Tijdschrift Geneeskde., 134, 1010-1012.

23. Bernard E., Roger P.M., Carles D., Bonaldi V., Fournier J.P. & Dellamonica P. (1989). - Diarrhea and Campylobacter infections in patients infected with the human immunodeficiency virus. J. infect. Dis., 159, 143-144.

24. Bemdtson E., Emanuelson U., Engvall A. & Danielsson-Tham M.-L. (1996). - A 1-year epidemiological study of Campylobacters in 18 Swedish chicken farms. Prev. vet. Med., 26, 167-185.

25. Blaser M.J., LaForce F.M., Wilson N.A. & Wang W.-L. (1980). - Reservoirs for human campylobacteriosis. J . inject. Dis., 141 (5), 665-669.

26. Bolton F.J., Holt A.V. & Hutchinson D.N. (1984). -Campylobacter biotyping scheme of epidemiological value. J. clin. Pathol., 37, 677-681.

27. Bradbury W.C. & Munroe D.L.G. (1985). - Occurrence of plasmids and antibiotic resistance among Campylobacter jejuni and Campylobacter coli isolated from healthy and diarrheic animals. J. din. Microbiol., 22, 339-346.

28. Brouwer R., Mertens M.J.A., Siem T.H. & KatchakiJ. (1979). - An explosive outbreak of Campylobacter enteritis in soldiers. Antonie Van Leeuwenhoek, 45, 517-519.

29. Brown P., Kidd D., Riordan T. & Barrell R.A. (1988). - An outbreak of food-borne Campylobacter jejuni infection and the possible role of cross-contamination. J . Infection, 17, 171-176.

30. Brynjolfsson A. (1987). - Costs of irradiating foods. In Handbook for conducting feasibility studies (J. Sivinski, ed.). International Consultive Group on Food Irradiation, Vienna, 37-70.

31. Bumens A.P., Angeloz-Wick B. & Nicolet J . (1992). -Comparison of Campylobacter rates in diarrheic and healthy pet animals. J. vet. Med., 39, 175-180.

32. Butzler J.-P. & Oosterom J . (1991). - Campylobacter: pathogenicity and significance in foods. Int. J. Food Microbiol, 12, 1-8.

33. Buzby J.C. & Roberts J . (1998). - Estimated annual costs of Campylobacter-associated Guillain-Barré syndrome. Agricultural Economic Report 756. United States Department of Agriculture, Washington, DC, 29 pp.

34. Byrd J.A., Corrier D.E., Hume M.E., Bailey R.H., Hargis B.M. & Stanker L.H. (1998). - Effect of feed withdrawal on the incidence of Salmonella and Campylobacter in the crops and ceca of market age broiler chickens. In Proc. International Symposium on food-borne salmonella in poultry (R.K. Gast & C.L. Hofacre, eds), 25-26 July, Baltimore, Maryland. American Association of Avian Pathologists, Kennett Square, Pennsylvania, 299.

35. Cabrita J . , Pires I., Vlaes L., Coignau H., Levy J . , Goosens H., Goncalves A.P., de Mol P. & Butzler J.P. (1992). -Campylobacter enteritis in Portugal: epidemiological features and biological markers. Eur. J . Epidemiol, 8 (1), 22-26.

36. Chowdhury S., Nair G.B. & Pal S.C. (1984). - Occurrence of Campylobacter jejuni in country chicken in Calcutta. Indian

J. med. Res., 79, 171-173.

37. Christenson B., Ringner A., Blucher C , Billaudelle H., Gundtoft K.N., Erikson G. & Bottiger M. (1983). - An outbreak of Campylobacter enteritis among the staff of a poultry abattoir in Sweden. Scand.j. inject. Dis., 15,167-172.

38. Chuma T., Yanada T., Yano K., Okamoto K. & Yugi H. (1994). - A survey of Campylobacter jejuni in broilers from assignment to slaughter using DNA-DNA hybridization.

J. vet. med. Sci., 56, 697-700.

39. Clark A.G. & Bueschkens D.H. (1988). - Horizontal spread of human and poultry-derived strains of Campylobacter jejuni among broiler chickens held in incubators and shipping boxes. J . Food Protec, 51, 438-441.

40. Cox N.A., Stem N.J., Hiett K.L. & Berang M.E. (1999). -Campylobacter passage from hen to offspring through the egg. In Proc. 34th National Meeting on poultry health and processing, 20-22 October, Ocean City, Maryland. Delmarva Poultry Industry Inc., Georgetown, Delaware, 6-7.

41 . Cruz R.J., Bartlett AV. & Mendez H. (1994). - Infection, diarrhea, and dysentry caused by Shigella .species and Campylobacter jejuni among Guatemalan rural children. Pediatr. inject. Dis. J., 13, 216-223.

42. Dawkins H.C., Bolton F.J. & Hutchinson D.N. (1984). - A study of the spread of Campylobacter jejuni in four large kitchens. J . Hyg. (London), 92, 357-364.

43. DeBoer E. & Hahné M. (1990). - Cross-contamination with Campylobacter jejuni and Salmonella spp. from raw chicken products during food preparation. J . Food Protec., 53, 1067-1068.

44. Dekeyser P., Gossuin-Detrain M., Butzler J.P. & Sternon J . (1972). - Acute enteritis due to related vibrio: first positive stool culture. J. inject. Dis., 125, 390-392.

45. Deming M.S., Tauxe R.V., Blake P.A., Dixon S.E., Fowler B.S., Jones T.S., Lockamy F.A., Patton CM. & Sikes R.O. (1987). - Campylobacter enteritis at a university: transmission from eating chicken and from cats. Am. J . Epidemiol, 126, 526-534.

46. Doyle M.P. (1984). - Association of Campylobacter jejuni with laying hens and eggs. Appl. environ. Microbiol., 47, 533-536.

47. Doyle M.P. & Roman D.J. (1982). - Sensitivity of Campylobacter jejuni to drying. J. Food Protee, 45, 507-510.

48. Edmonds J . (1984). - Reactive arthritis. N.Z. med. J., 14, 81-88.

http://Geneesh.de


49. Elfstrum J.T. (1998). - Continuous on-line reprocessing trials with trisodium phosphate as an antimicrobial rinse. In Proc. National Meeting on poultry health and processing, 21-23 October, Ocean City, Maryland. Delmarva Poultry Industry Inc., Georgetown, Delaware, 133-142.

50. Endiz H.P., Ruijs G.J., van Klingeren B., Jansen W.H., van der Reyden T. & Mouton R.P. (1991). - Quinolone resistance in Campylobacter isolated from man and poultry following introduction of fluoroquinolones in veterinary medicine. J . antimicr. Chemother., 27, 199-208.

51. Engvall A., Bergqvist A., Sandstedt K. & Danielsson-Tham M.-L. (1986). - Colonization of broilers with Campylobacter in conventional broiler-chicken flocks. Acta vet. scand., 27, 540-547.

52. Evans S.J. (1992).-Introduction and spread of thermophilic Campylobacters in broiler flocks. Vet. Rec., 131, 574-576.

53. Farkas J . (1998). - Irradiation as a method for decontaminating food. A review. Int. J. Food Microbiol., 10, 189-204.

54. Fernandez H., Kahler K., Salazar R. & Rios M.A. (1994). -Prevalence of thermotolerant species of Campylobacter and their biotypes in children and domestic birds and dogs in southern Chile. Rev. Inst. Med. trop. S. Paulo, 36, 433-436.

55. Figueroa G., Hidalgo H., Troncosco M., Rosende S. & Soto V. (1983). - Campylobacter jejuni in broilers, hens, and eggs in developing countries. In Campylobacter II (A.D. Pearson, M.B. Skirrow, B. Rows, J.R. Davies & D.M. Jones, eds). London Public Health Laboratory Service, London, 161-162.

56. Fleniken J.M. & Shane S.M. (2000). - Evaluation of sodium bisulphate litter additive for pre-harvest suppression of Campylobacter infection in broilers. J. appl. Poult. Res. (in press).

57. Genigeorgis C., Hassuneh M. &r Collins P. (1986). -Campylobacter jejuni infection on poultry farms and its effect on poultry meat contamination during slaughtering. J . Food Protec, 49, 895-903.

58. Giddings G.G. & Marcotte M. (1991). - Poultry irradiation for hygiene/safety and market-life enhancement. Food Rev. Int., 7, 259-282.

59. Gill C.O. & Harris L.M. (1984). - Hamburgers and broiler chickens as potential sources of human Campylobacter enteritis. J . Food Protee, 47, 96-99.

60. Grados O., Bravo N., Butzler J.P. & Ventura G. (1983). -Campylobacter infection: an occupational disease risk in chicken handlers. In Campylobacter II (A.D. Pearson, M.B. Skirrow, B. Rowe, J.R. Davies & D.M. Jones, eds). London Public Health Laboratory Service, London, 162.

61. Grant I.H., Richardson N.J. & Bokkenheuser V.D. (1980). -Broiler chickens as potential source of Campylobacter infectious in humans. J. din. Microbiol, 11, 508-510.

62. Gregory E., Barnhart H., Dreesen D.N., Stem N. & Com J.L. (1997). - Epidemiological study of Campylobacter spp. in broilers: source, time of colonization, and prevalence. Avian Dis., 41 , 890-898.

63. Guerrant R.L., Wanke CA., Penne R.A., Barrett L.J., Lima A.A.M. & O'Brien A.D. (1987). - Production of a unique cytotoxin by Campylobacter jejuni. Infect. Immun., 55, 2526-2530.

64. Hanninen M.-L. (1981). - Survival of Campylobacter jejuni/coli in ground refrigerated and in ground frozen beef liver and in frozen broiler carcasses. Acta vet. scand., 22, 566-577.

65. Hargis B.M., Caldwell D.J., Brewer R.L., Corrier D.E. & DeLoach J.R. (1995). - Evaluation of the chicken crop as a source of Salmonella contamination for broiler carcasses. Poult. Sci., 74, 1548-1552.

66. Hargis B.M., Byrd J.A. & Caldwell D.J. (1999). -Opportunities for meeting present and emerging standards for fecal and ingesta contamination. In Proc. 34th National Meeting on poultry health and processing, 20-22 October, Ocean City, Maryland. Delmarva Poultry Industry Inc., Georgetown, Delaware, 67-76.

67. Harris N.V., Thompson D., Martin D.C. & Nolan CM. (1986). - A survey of Campylobacter and other bacterial contaminants of pre-market chicken and retail poultry and meats, King County, Washington. Am. J. public Hlth, 76,401-406.

68. Hayek L.J. & Cruickshank J.G. (1977). - Campylobacter enteritis. Br. med. J . , 2, 1219.

69. Ho T.N., Mishu B., Li C.Y., Gao C.Y., Cornblath D.R., Griffin J.N., Asbury A.K., Blaser M.J. & McKhann G.M. (1995). - Guillain-Barré syndrome in northern China. Relationship to Campylobacter jejuni infection and anti-glycolipid antibodies. Brain, 118, 597-605.

70. Hood A.M., Pearson A.D. & Shahamat M. (1988). - The extent of surface contamination of retailed chicken with Campylobacter jejuni serogroups. Epidemiol. Inject, 100, 17-25.

71. Hoop R. & Ehrsam H. (1987). - Ein Beitrag zur Epidemiologie von Campylobacter jejuni und Campylobacter coli in der Hühnermast. Schweizer Arch. Tierheilkd., 129, 193-203.

72. Hopkins R.S. & Scott A.S. (1983). - Handling raw chicken as a source for sporadic Campylobacter jejuni infections. J . inject. Dis., 148, 770.

73. Hudson W.R. & Mead G.C. (1987). - Factors affecting the survival of Campylobacter jejuni in relation to immersion scalding of poultry. Vet. Rec., 121, 225-277.

74. Hugdahl M.B., Beery J.T. & Doyle M.P. (1988). -Chemotactic behavior of Campylobacter jejuni. Inject. Immun., 56, 1560-1566.


75. Humphrey T.J. & Lanning D.G. (1987). - Salmonella and Campylobacter contamination of broiler chicken carcasses and scald tank water: the influence of water pH. J. appl. Bacteriol, 63, 21-25.

76. Humphrey T.J., Lanning D.G. & Mead G.C. (1989). -Inhibition of Campylobacter jejuni in vitro by broiler chicken cecal contents. Vet. Rec., 125, 272-273.

77. Humphrey T.J., Henley A. & Lanning D.G. (1993). - The colonization of broiler chickens with Campylobacter jejuni. Some epidemiological investigations. Epidemiol. Infect., 110, 601-607.

78. Izat A.L. & Gardner F.A. (1988). - Incidence of Campylobacter jejuni in processed egg products. Poult. Sci., 67, 1431-1435.

79. Izat A.L., Gardner F.A., Denton J.H. & Golan F.A. (1988). -Incidence and level of Campylobacter jejuni in broiler processing. Poult. Sci., 67, 1568-1572.

80. Jacobs B.C., Rothbarth P.H., van der Meche F.G., Herbrink P., Schmitz P.I., de Klerk M.A. & van Doom A. (1998). - The spectrum of antecedent infections in Guillain-Barré syndrome: a case-control study. Neurology, 51, 1110-1115.

81. Jacobs-Reitsma W.F. (1995). - Campylobacter bacteria in breeder flocks. Avian Dis., 39, 355-359.

82. Jacobs-Reitsma W.F. (1997). - Aspects of epidemiology of Campylobacter in poultry. Vet. Q., 19, 113-117.

83. Jacobs-Reitsma W.F., Bolder N.M. & Mulder R.W.A.W. (1994). - Cecal carriage of Campylobacter and Salmonella in Dutch broiler flocks at slaughter: a one year study. Poult. Sci., 73, 1260-1266.

84. Jones D.M. & Robinson D.A. (1981). - Occupational exposure to Campylobacter jejuni infection. Lancet, i, 440-441.

85. Jones D.M., Abbot J.D., Painter J.M. & Sutcliffe E.M. (1984). - A comparison of biotypes and serotypes of Campylobacter sp. isolated from patients with enteritis and from animal and environmental sources. J. Infection, 9, 51-58.

86. Jones F.T., Axtell R.C., Rives D.V., Scheidler S.E., Tarver F.R. Jr, Walker R.L. & Wineland M.J. (1991). - A survey of Campylobacter jejuni contamination in modem production and processing systems. J. Food Protec., 54, 259-262.

87. Juven B.J. & Rogol M. (1986). - Incidence of Campylobacter jejuni and Campylobacter coli serogroups in a chicken processing factory. J. Food Protee, 49, 290-292.

88. Kaldor J . & Speed B.R. (1984). - Guillain-Barré syndrome and Campylobacter jejuni: a serological study. Br. med. J., 288, 1867-1870.

89. Kamplemacher E.H. (1983). - Irradiation for control of Salmonella and other pathogens in poultry and fresh meats. Food Technol, 37, 117.

90. Kapperud G. & Rosef D. (1983). - Serotyping and biotyping of thermophilic Campylobacters from man and animals in Norway. In Campylobacter 11 (A.D. Pearson, M.B. Skirrow, B. Rowe, J.R. Davies & D.M. Jones, eds). London Public Health Laboratory Service, London, 98-99.

91. Kapperud G., Skjerve E., Bean N.H., Ostroff S.M. & Lassen J . (1992). - Risk factors for sporadic Campylobacter infections: results of a case-control study in Southeastern Norway. J . clin. Microbiol., 30, 3117-3121.

92. Kapperud G., Skjerve E., Vik L., Hauge K., Lysaker A., Aalmen I., Ostroff S.M. & Potter M. (1993). -Epidemiological investigation of risk factors for Campylobacter colonization in Norwegian broiler flocks. Epidemiol. Infect, 111, 245-255.

93. Kasrazadeh M. & Genigeorgis C. (1987). - Origin and prevalence of Campylobacter jejuni in ducks and duck meat at the farm and processing plant level. J . Food Protee, 50, 321-326.

94. King E. (1957). - Human infections with Vibrio fetus and a closely related vibrio. J . infect. Dis., 101, 119-128.

95. Koenraad R.P., Jacobs-Reitsma W.F., van der Laan T., Beumer R.R. & Rombouts F.M. (1995). - Antibiotic susceptibility of Campylobacter isolates from sewage and poultry abattoir drain water. Epidemiol. Infect., 115, 475-483.

96. Kohler A., de Torrente A. & Inderwildi B. (1988). - Fisher's syndrome associated with Campylobacter jejuni infection. Eur. Neurol, 28, 150-151.

97. Kramer M.H., Herwaldt B.L., Craun G.F., Calderon R.L. & Juranek D.D. (1996). - Surveillance for waterbome-disease outbreaks - United States, 1993-1994. Morb. Mort, weekly Rep., 12 (45), 1-33.

98. Lambert J.D. & Maxcy R.B. (1984). - Effect of gamma radiation on Campylobacter jejuni. J. Food Sci., 49, 665-667.

99. Lammerding A.M., Garcia M.M., Mann E.D., Robinson Y., Dorward R.B., Truscott R.B. & Tittiger F. (1988). -Prevalence of Salmonella and thermophilic Campylobacter in fresh pork, beef, veal, and poultry in Canada. J . Food Protee, 51, 47-52.

100. Leonard R.E. (1996). - Safe food, environment compliments global trade. Nutrition Week Community Nutrition Institute, Washington, DC, 4-5.

101. Lim Y.S. & Tay L. (1992). - A one-year study of enteric Campylobacter infections in Singapore. J. trop. Med. Hyg., 95, 119-123.

102. Lin C.W. & Cheng K.S. (1998). - Incidence and clinical manifestations of Campylobacter enteritis in central Taiwan. Chung Hua I Hsueh Tsa Chih (Taipei), 61, 339-345.

103. Lindblom G.-B., Sjorgren E. & Kaijser B. (1986). - Natural Campylobacter colonization in chickens raised under different environmental conditions. J. Hyg., 96, 385-391.

104. Line J.E., Bailey J.S., Cox N.A., Stem N.J. & Tompkins T. (1998). - Effect of yeast-supplemented feed on Salmonella and Campylobacter populations in broilers. Poult. Sci., 77, 405-410.


105. Lior H. (1984). - New, extended biotyping scheme for Campylobacter jejuni, Campylobacter coli, and Campylobacter lundis. J, clin. Microbiol, 25, 2030-2031.

106. Lior H., Woodward D.L, Edgar J.A., Laroche L.J. & Gill P. (1982). - Serotyping of Campylobacter jejuni by slide agglutination based on heat-labile antigenic factors. J . clin. Microbiol, 15, 761-768.

107. Luechtefeld N.A.W., Blaser M.S., Reller L.B. & Wang W.-L.L. (1980). - Isolation of Campylobacter fetus subsp. jejuni from migratory waterfowl. J. din. Microbiol., 12, 406-408.

108. Luechtefeld N.W., Wang W.-L.L, Blaser M.J. & Reller L.B. (1981). - Evaluation of transport and storage techniques for isolation of Campylobacter fetus subsp. jejuni from turkey cecal specimens. J. clin. Microbiol, 13, 438-443.

109. McCardell B.A., Madden J.M. & Lee E.C. (1984). -Campylobacter jejuni and Campylobacter coli production of a cytotonic toxin immunologically similar to cholera toxin. J. Food Protec., 47, 943-949.

110. McMyne P.M.S., Penner J.L., Mathias R.G., Black W.A. & Hennessy J.N. (1982). - Serotyping of Campylobacter jejuni isolated from sporadic cases and outbreaks in British Columbia. J. clin. Microbiol, 16, 281-285.

111. Mahajan S. & Rodgers F.G. (1989). - Virulence of Campylobacter jejuni for chicken embryos. J. clin. Microbiol., 27, 1377-1379.

112. Malone G.W. (1998). - Future of poultry litter treatments. In Proc. National Meeting on poultry health and processing, 21-23 October, Ocean City, Maryland. Delmarva Poultry Industry Inc., Georgetown, Delaware, 49-51.

113. Mancinelli S., Riccardi F., Santi A.L., Palombi L. & Marazzi M.C. (1988). - Campylobacter jejuni infections in slaughterhouse workers. Bol. Ist. seiroter, milan., 67, 363-368.

114. Mandrell R.E. & Wachtel M.R. (1999). - Novel detection techniques for human pathogens that contaminate poultry. Curr. Opin. Biotechnol., 10, 273-278.

115. Marion J.E. (1999). - Industry perspective on microbial food safety in poultry. In Proc. National Meeting on poultry health and processing, 20-22 October, Ocean City, Maryland. Delmarva Poultry Industry Inc., Georgetown, Delaware, 1-2.

116. Marquis G.S., Ventura G., Gilman R.H., Porras E., Miranda E., Carbajal L. & Pentafiel M. (1990). - Fecal contamination of shantytown toddlers in households with non-corralled poultry. Lima, Peru. Am. J . public Hlth, 80, 146-149.

117. Mead P.S., Slutsker L , Dietz V., McCaig L.F., Bresee J.S., Shapiro C , Griffin P.M. & Tauxe R.V. (1999). -Food-related illness and death in the United States. Emerg. infect. Dis., 5, 607-625.

118. Meinersman R.J., Stern N.J. & Blankenship L.C. (1990), -Antigenic differences in congenic chickens - colonizing and noncolonizing strains of Campylobacter jejuni. Curr. Microbiol, 21, 17-21.

119. Molbak K. & Hojlyng N. (1988). - High prevalence of Campylobacter excretors among Liberian children related to environmental conditions. Epidemiol. Infect., 100, 227-237.

120. Montrose M.S., Shane S.M. & Harrington K.S. (1985).-Role of litter in the transmission of Campylobacter jejuni. Avian Dis., 29, 392-399.

121. Morrison R.M. & Roberts T. (1985). - Potential public health benefits of irradiating fresh chicken, pork and beef. In Food irradiation: new perspectives on a controversial technology. A review of technical, public health and economic considerations. Hearing on Federal Food Irradiation Development and Control Act. Committee of Agriculture. United States House of Representatives, Washington, DC, Serial No. 99-14, 1038-1064.

122. Murga H., Huicho L. & Guevara G. (1993). - Acute diarrhoea and Campylobacter in Peruvian children: a clinical and epidemiologic approach. J. trop. Pediatr., 39, 338-341.

123. Murray B.J. (1985). - Campylobacter enteritis in college students. College Hlth, 33, 147-149.

124. Nachamkin I., Bohachick K. & Patton CM. (1993). -Flagellin gene typing of Campylobacter jejuni by restriction fragment length polymorphism analysis. J . din. Microbiol., 31 , 1531-1536.

125. Neil S.D., Campbell J.N. & Greene J.H. (1984). -Campylobacter species in broiler chickens. Avian Pathol, 13, 777-785.

126. Newell D.G., McBride H., Saunders F., Dehele Y. & Pearson A.D. (1985). - The virulence of clinical and environmental isolates of Campylobacter jejuni. J. Hyg. (Camb.), 94, 45-54.

127. Norkrans G. & Svedhem A. (1982). - Epidemiological aspects of Campylobacter jejuni enteritis. J. Hyg. (London), 89, 163-170.

128. Oosterom J . , DeWilde G.J.A., DeBoer E., DeBlaauw L.H. &r Karman H. (1983). - Survival of Campylobacter jejuni during poultry processing and pig slaughtering. J. Food Protee, 46, 702-706.

129. Pacha R.E., Clark G.W., Williams E.A. & Carter A.M. (1988). - Migratory birds of central Washington as reservoirs of Campylobacter jejuni. Can. J. Microbiol, 34, 80-82.

130. Palumbo S. (1986). - Campylobacter jejuni in foods: its occurrence, isolation from foods and injury. J. Food Protee, 49, 161-166.

131. Patton C.M., Barret T.J. & Morris G.K. (1985). -Comparison of the Penner and Lior methods for serotyping Campylobacter spp. J . din. Microbiol, 22, 558-565.

132. Patton C.M., Wachsmuth I.K., Evins G.M., Kielbauch J.A., Plikaytis B.D., Troup N., Tompkins L.N. & Lior H. (1991). -Evaluation of 10 methods to distinguish epidemic-associated Campylobacter strains. J . clin. Microbiol, 29, 680-688.


133. Pearson A.D., Greenwood M., Healing T.D., Rollins D., Shahamut M., Donaldson J . & Colwell R.R. (1993). -Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl. environ. Microbiol., 59, 987-996.

134. Pearson A.D., Greenwood M.H., Feltham R.K.A., Healing T.D., Donaldson J . , Jones D.M. & Colwell R. (1996). - Microbial ecology of Campylobacter jejuni in a United Kingdom chicken supply chain: intermittent common source, vertical transmission, and amplification by flock propogation. Appl, environ. Microbiol, 62 (12), 4614-4620.

135. Penner J.L., Hennessy J.N. & Congi R.V. (1983). -Serotyping of Campylobacter jejuni and Campylobacter coli on the basis of thermostable antigens. Eur. J. clin. Microbiol, 2, 378-383.

136. Petersen K.E. & James W.O. (1988). - Agents, vehicles, and causal inference in bacterial foodborne disease outbreaks: 82 reports (1986-1995). J . Am. vet. med. Assoc., 212, 1874-1881.

137. Pokamunsky S., Horn M., Kass N., Borojovich E. & Rogol M. (1984). - The incidence of Campylobacter in poultry flocks in northern Israel. Refuah Vet., 41, 80-84.

138. Pokamunski S., Kass N., Borochovich E., Marantz B. & Rogol M. (1986). - Incidence of Campylobacter spp. in broiler flocks monitored from hatching to slaughter. Avian Pathol, 15, 83-92.

139. Popovic-Uroic T. (1989). - Campylobacter jejuni and Campylobacter coli diarrhoea in rural and urban populations in Yugoslavia. Epidemiol. Inject., 102, 59-67.

140. Prescott J.F. & Gelmer O.S. (1984). - Intestinal carriage of Campylobacter jejuni and Salmonella by chicken flocks at slaughter. Can. J. comp. Med., 48, 329-331.

141. Rantala M. & Nurmi E. (1973). - Prevention of the growth of Salmonella infantis in chicks by the flora of the alimentary tract of chickens. Br. Poult. Sci., 14, 627-630.

142. Reinthaller F.F., Feierl G., Stunzner D. & Marth E. (1998). -Diarrhea in returning Austrian tourists: epidemiology, etiology, and cost-analysis. J. Travel Med., 5, 65-72.

143. Reynolds G. & Draughton F.A. (1987). - Campylobacter jejuni in vacuum packaged processed turkey. J. Food Protec., 50, 300-304.

144. Richardson N.J., Koomhof HJ. , Bokkenheuser V.D., Mayet Z. & Rosen E.U. (1983). - Age related susceptibility to Campylobacter jejuni infection in a high prevalence population. Arch. Dis. Child., 58, 616-619.

145. Rogol M. & Michael J . (1984). - Detection of resistant isolates of Campylobacter jejuni by the disc susceptibility method. Eur. J. clin. Microbiol. inject. Dis., 3, 40-42.

146. Rollins D.M. (1991). - Potential for reduction in colonization of poultry by Campylobacter from environmental sources. In Colonization control of human bacterial enteropathogens in poultry (L.C. Blankenship, J.S. Bailey, N.A. Cox, S.E. Craven, R.J. Meinersmann & N.J. Stem, eds). Academic Press, San Diego, California, 47-56.

147. Rosef O., Gondrosen B. & Kapperud G. (1984). -Campylobacter jejuni and Campylobacter coli as surface contaminants of fresh and frozen poultry carcasses. Int. J. Food Microbiol, 1, 205-215.

148. Ruiz J . , Goni P., Marco F., Gallardo F., Mirelis B., Jimenez De Anta T. & Vila J . (1998). - Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyr A gene mutations in quinolone-resistant clinical isolates. Microbiol Immunol, 42, 223-226.

149. Ruiz-Palacios G.M., Escamilla E. & Torres N. (1981). -Experimental Campylobacter diarrhea in chickens. Inject. Immun., 34, 250-255.

150. Sang F.C., Shane S.M., Yogasundram K., Hagstad H.V. & Kearney M.T. (1989). - Enhancement of Campylobacter jejuni virulence by serial passage in chicks. Avian Dis., 33, 425-430.

151. Sanyal S.C., Islam K.M.N., Neogy P.K.B., Islam M., Speelman P. & Huq M.I. (1984). - Campylobacter jejuni diarrhea model in infant chickens. Inject. Immun., 43, 931-936.

152. Schwartz D., Melamed I., Cohen D., Konforti N. & Goldhar J . (1990). - ELISA for Campylobacter jejuni antibodies in Israeli children with diarrhea and in healthy soldiers. Isr. J . med. Sci., 26, 319-324.

153. Shane S.M. (1992). - The significance of Campylobacter jejuni infection in poultry: a review. Avian Pathol, 21, 189-213.

154. Shane S.M. (1994). - Campylobacteriosis. In Handbook of zoonoses, 2nd Ed. (G.N. Beran & J.H. Steele, eds). CRC Press, Boca Raton, Florida, 311-320.

155. Shane S.M. (1997). - Campylobacteriosis. In Diseases of poultry, 10th Ed. (B.W. Calnek with H.J. Barnes, C.W. Beard, L.R. McDougald & Y.M. Saif, eds). Iowa State University Press, Ames, Iowa, 236-245.

156. Shane S.M., Montrose M.S. & Harrington K.S. (1985). -Transmission of Campylobacter jejuni by the housefly (Musca domestica). Avian Dis., 29 (2), 384-391.

157. Shane S.M., Gifford D.H. & Yogasundram K. (1986). -Campylobacter jejuni contamination of eggs. Vet. Res. Commun., 10, 487-492.

158. Shane S.M., Halvorson D., Villegus P. & Wayes D. (eds) (1995). - Biosecurity in the poultry industry. American Association of Avian Pathologists, Kennett Square, Pennsylvania, 120 pp.

159. Shane S.M. & Harrington K.S. (1998). - Campylobacteriosis. In A laboratory manual for the isolation and identification of avian pathogens (D.E. Swayne.J.R. Glisson, M.N. Jackwood, J.E. Pearson & W.M. Reed, eds). American Association of Avian Pathologists, Kennett Square, Pennsylvania, 35-39.

160. Shanker S., Rosenfield J.A., Davey G.R. & Sorrell T.C. (1982). - Campylobacter jejuni: incidence in processed broilers and biotype distribution in human and broiler isolates. Appi, environ. Microbiol, 43, 1219-1220.


161. Shanker S., Lee A. & Sorrell T.C. (1986). - Campylobacter jejuni in broilers: the role of vertical transmission. J. Hyg., 96, 153-159.

162. Shanker S., Lee A. & Sorrell T.C. (1990). - Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiol. Inject., 104, 101-110.

163. Shanker S., Lee A. & Sorrell T.C. (1998). - Experimental colonization of broiler chicks with Campylobacter jejuni. Epidemiol. Inject, 100, 27-34.

164. Sjogren E., Kaijser B. & Werner M. (1992). - Antimicrobial susceptibilities of Campylobacter jejuni and Campylobacter coli isolated in Sweden: a 10-year follow-up report. Antimicrob. Agents Chemother., 36, 2847-2849.

165. Skirrow M.B. (1977). - Campylobacter enteritis: a 'new' disease. Br. med.J., 2, 9-11.

166. Skirrow M.B. (1990). - Campylobacter. Lancet, 336,

921-923.

167. Skirrow M.B. & Benjamin J . (1980). - 1001 Campylobacters: cultural characteristics of intestinal Campylobacters from man and animals. J. Hyg. (London), 85, 427-442.

168. Smitherman R.E., Genigeorges C. & Farber T.B. (1984). -Preliminary observations on the occurrence of Campylobacter jejuni at four California chicken ranches. J. Food Protec., 47, 293-298.

169. Soerjadi-Liem A.S., Snoeynbos G.H. & Weinack O.M. (1983). - Comparative studies on competitive exclusion of three isolates of Campylobacter fetus subsp. jejuni in chickens by native gut microflora. Avian Dis., 28, 139-146.

170. Stem N.J. (1994). - Mucosal competitive exclusion to diminish colonization of chickens by Campylobacter jejuni. Poult. Sci., 73, 402-407.

171. Stem N.J., Green S.S., Thaker N., Krout D.J. & Chiu J . (1984). - Recovery of Campylobacter jejuni from fresh and frozen meat and poultry collected at slaughter. J. Food Protec., 47, 372-374.

172. Stem N.J., Hernandez M.P., Blakenship L., Deibel K.E., Doores S., Doyle M.P., Ng H., Pierson M.D., Sofos J.N., Sveum W.H. & Westhof D.C. (1985). - Prevalence and distribution of Campylobacter jejuni and Campylobacter coli in retail meats. J. Food Protee, 48, 595-599.

173. Stern N.J., Clavero M.R.S., Bailey J.S., Cox N.A. & Robach M.C. (1995). - Campylobacter spp. in broilers on the farm and after transport. Poult Sci., 74, 937-941.

174. Stem N.J., Myszewski M.A., Barnhart H.M. & Dreesen D.W. (1997). - Flagellin A gene restriction fragment length polymorphism patterns of Campylobacter spp. isolates from broiler production sources. Avian Dis., 41 , 899-905.

175. Studer E., Luthy J . & Hubner P. (1999). - Study of the presence of Campylobacter jejuni and C. coli in sand samples from four Swiss chicken farms. Res. Microbiol., 150, 213-219.

176. Tauxe R.V. (1992). - Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In Campylobacter jejuni, current status and future trends (I. Nachamkin, M.J. Blaser & L. Tomkins, eds). American Society of Microbiology, Washington, DC, 9-19.

177. Tauxe R.V. (1997). - Emerging foodborne diseases: an evolving public health challenge. Emerg. Foodborne Dis., 3, 425-434.

178. Tauxe R.V., Deming M.S. & Blake P.A. (1985). -Campylobacter jejuni infections on college campuses; a national survey. Am. J. public Hlth, 75, 659-660.

179. Tauxe R.V., Pegues D.A. & Hargrett-Bean N. (1987). -Campylobacter infections: the emerging national pattern. Am. J. public Hlth, 77, 1219-1221.

180. Tauxe R.V., Hargrett-Bean N., Patton CM. & Wachsmuth I.K. (1988). - Campylobacter isolates in the United States, 1982-1986. Morb. Mort, weekly Rep., 37 (SS2), 1-13.

181. Taylor D.N., Porter B.W., Williams C.A., Miller H.G., Bopp C.A. & Blake P.A. (1982). - Campylobacter enteritis: a large outbreak traced to commercial raw milk. Western J. Med., 137, 365-369.

182. Taylor D.E., Gamer R.S. & Allan B.J. (1983). -Characterization of tetracycline resistance plasmids from Campylobacter jejuni and Campylobacter coli. Antimicrob. Agents Chemother., 24, 930-935.

183. Taylor D.E. & Courvalin P. (1988). - Mechanisms of antibiotic resistance in Campylobacter species. Antimicrob. Agents Chemother., 32, 1107-1112.

184. United States Department of Agriculture (USDA) (1997). -Campylobacter: questions and answers. USDA, Food Safety and Inspection Service, Consumer Education and Information, Washington, DC, 6 pp.

185. Uyttendaele M., DeTroy P. & Debevere J . (1999). -Incidence of Salmonella, Campylobacter jejuni, Campylobacter coli, and Listeria monocytogenes in poultry carcasses and different types of poultry products for sale on the Belgian retail market. J . Food Protee, 62, 735-740.

186. Valdespino-Gomaz J.L., Garcia-Garcia M.L., Del Rio-Zolezzi A., Giono-Cerezo S., Salcedo-Alvarez R.A. & Sepulveda-Amor J . (1994). - Epidemiology and etiology of infectious diarrheas. The case of Mexico. Rev. latinoam. Microbiol, 36, 307-324.

187. Vandamme P., Falsen E., Rossau R., Hoste B., Segers P., Tytgat R. & DeLey J . (1991). - Revision of Campylobacter, Helicobacter, and Wolinella taxonomy: emendation of generic descriptions and proposal of Arcobacter gen. nov. Int. J . syst. Bacterìol, 41 , 88-103.

188. Van de Giessen A., Mazurier S.-I., Jacobs-Reitsma W., Jansen W., Berkers P., Ritmeester W. & Wemars K. (1992). - Study on the epidemiology and control of Campylobacter jejuni in poultry broiler flocks. Appl, environ. Microbiol, 58, 1913-1917.

Rev. sci. tech. Off. int. Epiz, 19 (2) 395

189. Van de Giessen A.W., Bloemberg B.P.M., Ritmeester N.S. & Tilburg J.J.H.C. (1996). - Epidemiological study on risk factors and risk reducing measures for Campylobacter infection in Dutch broiler flocks. Epidemiol. Inject., 117, 245-250.

190. Van de Giessen A.W., Tilburg J.J . , Ritmeester W.S. & van der Plas J . (1998). - Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiol. Inject., 121, 57-66.

191. Van de Putte L.B.A., Berden J.H.M., Boerbooms A.M.T., Muller W.H., Rasker J.J. , Reynvaan-Groendijk A. & van der Linden S.M.J.P. (1980). - Reactive arthritis after Campylobacter jejuni enteritis. J. Rheumatol., 7, 531-535.

192. Vanniasinkam T., Lanser J.A. & Barton M.D. (1999). - PCR for the detection of Campylobacter spp. in clinical specimens. Lett appl. Microbiol, 28, 52-56.

193. Véron M. & Chatelain R. (1973). - Taxonomic study of the genus Campylobacter Sebald and Véron and designation of the neotype strain for the type species Campylobacter fetus (Smith and Taylor) Sebald and Véron. Int. J. syst. Bacteriol, 23, 122-134.

194. Welkos S.L. (1984). - Experimental gastroenteritis in newly-hatched chicks injected with Campylobacter jejuni. J. med. Microbiol, 18, 233-248.

195. Wempe J.M., Genigeorgis C.A., Farver T.B. & Yusufu H.I. (1983). - Prevalence of Campylobacter jejuni in two California chicken processing plants. Appl. environ. Bacteriol, 45, 355-359.

196. White P.L., Baker A.R. & James W.O. (1997). - Strategies to control Salmonella and Campylobacter in raw poultry products. In Contamination of animal products: prevention and risks for public health (A.S. Ahl & P. Sutmoller, eds). Rev. sci. tech. Off. int. Epiz., 16 (2), 525-541.

197. Wiedemann B. & Heisig P. (1994). - Mechanisms of quinolone resistance. Injection, 22 (Suppl. 2), 73-79.

199. Winters D.K., O'Leary A.E. & Slavik M.F. (1998). -Polymerase chain reaction for rapid detection of Campylobacter jejuni in artificially contaminated foods. Lett, appl. Microbiol, 27, 163-167.

200. Wokatsch R. & Bockemuhl J . (1987). - Sero- and biotyping of Campylobacter strains originating from men and slaughterhouse animals in the area of Hamburg. Fed. Rep. of Germany. In Campylobacter IV (B. Kaijser & E. Falsen, eds). University of Gothenburg, Gothenburg, Sweden, 312.

201. Yan W., Chang N. & Taylor D.E. (1991). - Pulsed field gel electrophoresis of Campylobacter jejuni and Campylobacter coli genomic DNA and its epidemiologic application. J . inject. Dis., 163, 1068-1072.

202. Yang Z., Li Y. & Slavik M. (1998). - Use of antimicrobial spray applied with an inside-outside bird washer to reduce bacterial contamination on prechilled chicken carcasses. J. Food Protec., 61, 829-832.

203. Yogasundram K. & Shane S.M. (1986). - The viability of Campylobacter jejuni on refrigerated chicken drumsticks. Vet Res. Commun., 10, 479-486.

204. Yogasundram K., Shane S.M., Grodner R.M., Lambremont E.M. & Smith R.E. (1987). - Decontamination of Campylobacter jejuni on chicken drumsticks using chemicals and radiation. Vet Res. Commun., 11, 31-40.

205. Yogasundram K., Shane S.M. & Harrington K.S. (1989). -Prevalence of Campylobacter jejuni in selected domestic and wild birds in Louisiana. Avian Dis., 33, 664-667.

206. Yusufu H.I., Genigeorgis C , Farver T.B. & Wempe J.M. (1983). - Prevalence of Campylobacter jejuni at different sampling sites in two California turkey processing plants. J. Food Protec., 46, 868-872.

198. Willis W.L. & Murray C. (1997). - Campylobacter jejuni seasonal recovery observations of retail market broilers. Poult Sci., 76, 314-317.

Documents

Campylobacter infection of commercial poultry - OIE