International Journal of Food Microbiology. 12 (1991) 9-16 © 1991 Elsevier Science Publishers B.V. 0168-1605/91/$03.50
9
FOOD 00361
Epidemiology of Campylobacterenteritis M.B. Skirrow Gloucester Public Health Laboratory, Gloucestershire Royal Hospital Gloucester, U.K (Received 6 July 1990; accepted 13 September 1990)
Campylobacter enteritis is the commonest form of infective diarrhoea in most developed countries of the world. In England and Wales laboratory reports indicate an annual incidence of about 85/100000, but the true rate is probably nearer 1100/100000. Measured costs run to many millions of pounds per year. Most infections are sporadic and believed to be foodborne; large outbreaks are infrequent and mostly due to the consumption of raw milk or unchlorinated water. Raw meats and animal products, notably broiler chickens, are the main source of campyiobacters in food. A case-control study in the U.S.A., where eating habits are similar to those in Europe, attributed about one-half of human Camp.vlobacter infections to the consumption of chickens. The production of Campylobacter-free chickens is not yet practicable, but considerable progress could be made to this end with sufficient motivation and resources from government and the poultry industry. Key words: Campylobacter: Diarrhoea; Poultry; Red meat; Milk
Introduction T h e first q u e s t i o n to be addressed is how big a health p r o b l e m is Campylobacter enteritis. T h e disease usually clears u p s p o n t a n e o u s l y after a few days a n d it is seldom d a n g e r o u s (Butzler a n d Oosterom, 1990), so does it m a t t e r all that m u c h ? M e a s u r e m e n t s of incidence a n d m o r b i d i t y show that it does. T h e second q u e s t i o n is how much of the p r o b l e m relates to food a n d the food industry. T h e answer is that moist of it does, so the subject is certainly relevant to this S y m p o s i u m .
Incidence W h e r e c a m p y i o b a c t e r s are looked for r o u t i n e l y in the stools of p a t i e n t s with diarrhoea, they are the most frequently identified pathogens. In E n g l a n d a n d Wales d u r i n g the past 10 years, Campylobacter isolations have exceeded those of Salmonella, even d u r i n g the recent surge of Salmonella enteritidis infection (Rowe, 1990). I n c i d e n c e figures are m u c h i n f l u e n c e d by the availability of diagnostic
Correspondence address: M.B. Skirrow, Gloucester Public Health Laboratory, Gloucestershire Royal Hospital, Gloucester GL] 3NN, U.K.
10 services and the sampling habits of doctors, so one must be careful when making comparisons. Annual rates of 85/100000 in England and Wales (PHLS Communicable Disease Surveillance Centre (CDSC), unpublished) and 60/100000 in Seattle, U.S.A. (Johnson and Nolan, 1985). are probably representative of Europe and North America. These figures are derived from reports of laboratory isolations, which clearly represent only a fraction of the true number of infections. N o b o d y knows what the ratio of reported to actual infections is, but estimates range from 1 in 10 to 1 in 100. A survey of diarrhoea in a single general practice in England (Kendall and Tanner, 1982) gave a projected incidence of 1100/100000. which suggests that the lower of these fractions is the more accurate. In England and Wales, annual Campylobacter isolations have increased four-fold over the last 10 years, but much of this increase is due to increased sampling rather than a true increase in infection (Skirrow, 1989). N o such increase has been observed in the U.S.A. Most of these reports are of sporadic infections or of small family outbreaks affecting only two or three people. Large outbreaks are uncommon and are almost always caused by the distribution of untreated water or milk. In the developed industrialised countries of Europe, North America and Australasia, Campylobacter enteritis affects people of all ages, but typically it has a bimodal distribution with peaks of incidence in children under the age of 4 years and in young adults (Skirrow, 1987). This secondary peak in young adults is not seen with Salmonella or Shigella infections. In developing countries exposure to infection is much greater, with the result that children become immune within the first 2 years or so of life: the disease is not seen in older children or adults. As commercially produced food plays only a small part in this scene, I shall not consider infection in developing countries further.
Seasonal trends Campylobacter enteritis in temperature zones is more c o m m o n in summer than in winter (Blaser et al., 1983). C D S C reports for England and Wales show a striking
15m
"olO. retO
"~5"
4-weekly periods Fig. 1. Seasonal pattern of campylobacter isolations in England and Wales for each of the 9 years, 1981-1989. Mean annual total 22200. (From Skirrow, 1990a.)
11 seasonal consistency (Skirrow, 1987); there is a sharp rise in May, with a peak in July and thereafter a gradual fall to winter levels in December (Fig. 1). The reasons for this pattern are unknown.
Costs
What all this illness means in terms of costs to society was shown starkly by Sockett and Pearson (1988) in a detailed survey of 53 patients with Campylobacter enteritis in England. Direct costs to government (health care, laboratory and environmental health investigation) and indirect costs to the individual and society (mainly lost productive output) amounted to £273 per patient. Thus in 1989 the cost of laboratory diagnosed cases alone amounted to nearly £9 million. In the same study the intangible cost of pain and suffering - - a recognised and legitimate factor - - amounted to as much again.
S o u r c e s and t r a n s m i s s i o n
Campylobacterjejuni and C. coli, the principal causes of Campylobacter enteritis, live in a wide range of animals, particularly birds, mainly as commensals but also as occasional enteric pathogens in the young of some species, notably lambs, calves and puppies (Blaser et al., 1983; Skirrow, 1990b). C. coli is particularly associated with pigs. Human beings are only transient hosts of campylobacters and are a relatively minor source of infection (Blaser et al., 1983). Thus animals form the principal reservoir of infection. Transmission can be direct or indirect. Direct transmisshgn from animals Those whose occupation brings them into close contact with animals or animal products, such as farmers, veterinarians, slaughterhouse workers, poultry processors and butchers, are at increased risk of infection. It appears that many of them become immune through regular exposure (Blaser et al., 1983). Members of the general public may become infected by contact with infected pets, usually in the form of a puppy or kitten with Campylobacter diarrhoea. Although these routes of transmission are well documented, they account for only a minority of infections. Indirect transmission is more important.
Indirect transmission from animals There are many potential routes of infection from animals to man, but basically there are three vehicles: water; milk; and animal meat, which is conveniently grouped under the headings poultry, red meat, and offal.
12
Water In view of the wide range of animals that carry campylobacters it is not surprising that the organisms are common in lakes, rivers and other natural deposits of surface water (Carter et al., 1987). A few sporadic infections arise from the casual or accidental consumption of untreated water, but major outbreaks of Campylobacter enteritis affecting several thousand people have been caused by the distribution of unchlorinated or inadequately treated water (Blaser et al.. 1983). Fortunatel\' such outbreaks are u n c o m m o n and water is probably more important as a source of infection for domestic stock. Campylobacters can survive for several weeks in cold water, including seawater, but for only a few days in water above 1 5 ° C (Blaser et al., 1980; Weber et al., 1987). Milk Milk is almost the only vehicle other than water to have caused major outbreaks of Camp.vlobacter enteritis (Blaser et al., 1983). Most outbreaks are caused by cows" milk, but goats' milk has also been implicated (Hutchinson et al., 1985). It is thought that faecal contamination, which is virtually impossible to avoid even in the best run dairy, is how campylobacters get into the milk. Surveys have shown that 4.5-5.9% of cows' milk samples may contain C. jejuni (Beumer et al., 1988; H u m p h r e y and Hart, 1988). Bovine Campylobacter mastitis provides another means of contamination; although u n c o m m o n it is difficult to detect, as campylobacters are shed into the milk in large numbers before the milk becomes obviously granular (Lander and Gill. 1980; Morgan et al., 1985). As with waterborne infection, it is only the raw or inadequately treated product that is a hazard. Conventional methods of pasteurization readily destroy campylobacters, which are more heat-sensitive than Escherichia coil (D'Aoust et al., 1988). Poultry Colonisation of poultry flocks is almost universal. Most broiler chickens sold in shops are contaminated with campylobacters (Blaser et al., 1983). Uneviscerated (New York dressed) birds may have Campylobacter counts of up to 2.4 x 10 7 per bird (Hood et ai., 1988). Normally processed fresh birds may have counts of up to 1.5 X 10 6 per bird, but fewer organisms survive on frozen birds owing to the damaging effect of freezing and thawing (Gill and Harris, 1984; Stern et al., 1985b). Red meat The process of slaughter and dressing of animals invariably results in the contamination of carcasses with gut flora. Campylobacters can be isolated from a high proportion of cattle, sheep and pig carcasses soon after slaughter (Lammerding et al., 1988), but conventional forced air chilling greatly reduces their number through surface drying (Oosterom et al., 1983). Less than 2% of retailed red meat samples were found to be contaminated in two large surveys (Turnbuil and Rose, 1982; Boiton et al., 1985), but rates of around 5% (Stern et al., 1985a) and 20% (Fricker and Park, 1989) have also been reported. These differences might be
13 explained in part by differences in methods, particularly if contamination was light and near the threshold of detection.
Offal Offal, such as liver, kidney and heart, is more commonly contaminated. There is clearly wide variation with such a variable product, but surveys have shown that 30-47% of such offal samples may be contaminated (Bolton et al.. 1985: Fricker and Park, 1989). It is notable that washing and salting pig intestines, as practised in Germany, does not eliminate campylobacters (Sticht-Groh, 1982).
Campylobacters in food readyfor consumption The presence of campylobacters in raw animal products is one thing: their presence in food that is ready for consumption is quite another. There are two ways in which the gap may be inadvertently bridged. The first is if the contaminated product is eaten raw or undercooked. Although campylobacters are destroyed by light conventional cooking (Gill and Harris, 1984), barbecue and fondue cooking may allow survival in the centre of the food and are known to carry an increased risk of infection (Oosterom et al., 1984; Mouton et al., 1982). Of the few foodborne outbreaks of Campylobacter enteritis that have been reported, undercooked poultry meat has featured significantly often, even though bacteriological proof has not always been obtained. An important difference from Salmonella food poisoning is that campylobacters do not multiply in meat at ambient temperatures. Their minimum growth temperature is about 30 ° C, and at higher temperatures they rapidly become overgrown by other bacteria. The second and probably more important way food becomes a vehicle of infection is by the passive transfer of campylobacters from heavily contaminated meat, such as poultry, to other 'innocent' foods in the kitchen. This is difficult to prove, but it is a logical hypothesis. As few as 500 bacteria are capable of causing infection (Robinson, 1981). Most people cook food adequately, but in a British survey less than one-third of respondents appreciated the need to handle raw meats separately from other foods (Ministry of Agriculture, Fisheries and Food, 1988). Campylobacters have been isolated from flies near pig and poultry units (Rosef and Kapperud, 1983), but there is no evidence that flies are a usual source of infection.
Prevention
Having listed the various sources of Campylobacter infection, we need to consider their relative importance in order to plan appropriate control measures. The proper treatment of water and milk supplies are obvious and highly effective measures that are generally well applied. Surprising as it may seem, there is only one major survey that assesses risk factors associated with foods. This was a case-control study from Seattle, U.S.A., where eating habits are similar to those in Europe (Harris et al., 1986a, b). Poultry, raw milk, raw or rare fish, shellfish, and mushrooms (low risk) were significantly
14 associated with infection, but poultry was the outstanding item. It was calculated that the consumption of chicken accounted for about one-half of all cases. Although much could be done to educate the public in good hygienic practice in the handling of raw poultry and other meats, the single most effective measure would be to eliminate or reduce Campylobacter contamination of poultry in shops. There are three possible lines of attack. (1) Prevention of infection in broiler flocks. As there is no evidence of vertical transmission (Shanker et al., 1986), infection is presumably introduced from extraneous sources sometime during the birds' short 6 - 7 week concentrated lives. Not all flocks become infected. Introduction of campylobacters on the boots of attendants, from small birds or rodents, and in water supplies have been suggested (Humphrey, 1989). Detailed work showing that infection may be introduced and perpetuated in broiler house water supply systems is of particular interest (Pearson et al., 1988): moreover, the application of intervention measures, albeit complex, greatly reduced colonisation in the flocks. (2) Reduction of cross-contamination during mass processing of broilers. The introduction of spray cooling instead of dip tank cooling and of machinery of improved design are examples of how cross-contamination can be reduced, but there is a limit to what can be achieved (Humphrey, 1989). Some cross-contamination is inevitable as long as heavily infected flocks continue to be submitted for processing. (3) Terminal disinfection of dressed birds. The use of disinfectants or acid rinsing of carcasses has not proved effective in concentrations that do not taint or spoil the meat (Humphrey, 1989). Irradiation is effective and it has the advantage of destroying other pathogens, but there are drawbacks, not least the removal of a motive for producing bacteriologically clean birds by means of good husbandry and hygiene. In summary, we must look for ways of reducing the intensity of colonisation of broiler flocks as the single most effective method of controlling human infection. Money and resources put to this end would be well spent even if the outlay is large. What is needed is sufficient motivation from government and the poultry industry.
References Beumer, R.R., Cruysen. J.J.M. and Birtantie, 1.R.K. (1988) The occurrence of Campylobacterjejuni in raw cows' milk. J. Appl. Bact. 65, 93-96. Blaser, M.J., Hardesty, H.L., Powers, B. and Wang, W.-L.L. (1980) Survival of Campylobacter fetus subsp, jejuni in biological milieus. J. Clin. Microbiol. 11,309-313. Blaser, M.J., Taylor, D.N. and Feldman, R.A. (1983) Epidemiologyof Campylobacterjejuni infections. Epidemiol. Rev. 5, 15"/-176. Bolton, F.J., Dawkins, H.C. and Hutchinson, D.N. (1985) Biotypes and serotypes of thermophilic campylobacters isolated from cattle, sheep and pig offal and other red meats, J. Hyg. Camb. 95, 1-6.
15 Butzler, J.-P. and Oosterom, J. (1990) Campylobacter: pathogenicity and significance in foods. Int. J. Food Microbiol. 12, 1-8. Carter, A.M.. Pacha, R.E.. Clark. G.W. and WilUams, E.A. (1987) Seasonal occurrence of Campylobacler spp. in surface waters and their correlation with standard indicator bacteria. Appl. Environ. Microbiol. 53. 523-526. D'Aoust, J.-Y., Park, C.E., Szabo, R.A., Todd, E.C.D., Emmons, D.B. and McKellar. R.C. (1988) Thermal inactivation of Campylobacter species, Yersinia enterocolitica, and haemorrhagic Escherwhia coil 0157/H7 in fluid milk. J. Dairy Sci. 71. 3230-3236. Fricker, C.R. and Park, R.W.A. (1989) A two-year study of the distribution of 'thermophilic" campylobacters in human, environmental and food samples from the Reading area with particular reference to toxin production and heat-stable serotype. J. Appl. Bact. 66, 477-490. Gill, C.O. and Harris. L.M. (1984) Hamburgers and broiler chickens as potential sources of human Campylobacter enteritis. J. Food Protect. 47, 96-99. Harris, N.V., Kimball, T., Weiss, N.S. and Nolan. C. (1986a) Dairy products, produce and other non-meat foods as possible sources of Campylobacterjejuni and Campylobacter coil enteritis. J. Food Protect. 49, 347-351. Harris, N.V., Weiss, N.S. and Nolan, C.M. (1986b) The role of poultry and meats in the etiology of Campylobacterjejuni/coli enteritis. Am. J. Publ. Health 76. 407-411. Hood, A.M., Pearson, A.D. and Shahamat, M. (1988) The extent of surface contamination of retailed chickens with Campylobacterjejuni serogroups. Epidemiol. Inf. 100, 17-25. Humphrey, T.J. (1989) Salmonella, Campylobacter and poultry: possible control measures. Abstr. Hyg. Commun. Dis. 64, R1-R8. Humphrey, T.J. and Hart, R.J.C. (1988) Campylobacter and salmonella contamination of unpasteurized cows' milk on sale to the public. J. Appl. Bact. 65, 463-467. Hutchinson, D.N., Bolton, F.J., JeUey, W.C.N., Mathews, W.G., Telford, D.R., Counter, D.E., Jessop, E.G. and Horsley, S.D. (1985) Campylobacter enteritis associated with consumption of raw goat's milk. Lancet i, 1037-1038. Johnson, K.E., Nolan, C.M. and the Campylobacter Laboratory Surveillance Group (1985) Communitywide surveillance of Campylobacterjejuni infection: evaluation of a laboratory-based method. Diagn. Microbiol. Infect. Dis. 3, 389-396. Kendall, E.J.C. and Tanner, E.1. (1982) Campylobacter enteritis in general practice. J. Hyg. Camb. 88, 155-163. Lammerding, A.M., Garcia, M.M., Mann, E.D., Robinson, Y., Dorward, W.J., Truscott, R.B. and Tittiger, F. (1988) Prevalence of Salmonella and thermophilic Campylobacter in fresh pork, beef, veal and poultry in Canada. J. Food Protect. 51, 47-52. Lander, K.P. and Gill, K.P.W. (1980) Experimental infection of the bovine udder with Campylobacter coli/jejuni. J. Hyg. Camb. 84, 421-428. Ministry of Agriculture, Fisheries and Food (1988) Food hygiene: report on a consumer survey. Her Majesty's Stationary Office, London. Morgan, G., Chadwick, P., Lander, K.P. and Gill, K.P.W. (1985) Camp.vlobacterjejuni mastitis in a cow: a zoonosis related incident. Vet. Rec. 176, 111. Mouton, R.P., Veltkamp, J.J., Lauwers, S. and Butzler. J.P. (1982) Analysis of a small outbreak of campylobacter infections with high morbidity. In: D.G. Newell (Ed.), Campylobacter: Epidemiology, Pathogenesis and Biochemistry, MTP Press, London, pp. 129-134. Oosterom, J., de Wilde. G.J.A.. Boer. E., de Blaauw. L.H. and Karman. H. (1983) Survival of Campylobacterjejuni during poultry processing and pig slaughtering. J. Food Protect. 46, 702-706. Oosterom, J., Den Uyl, C.H., Banffer, J.R.J. and Huisman, J. (1984) Epidemiological investigations on Campylobacterjejuni in households with a primary infection. J. Hyg. Camb. 93, 325-332. Pearson, A.D., Colweil, R.R., Rollins, D.M., Healing, T.D., Donaldson. J., Greenwood, M.H., Jump, E., Shahamat, M., Hooper. W.L. and Watkin-Jones, M. (1988) Prevention of C. jejuni transmission to broiler chicken by farm interventions. In: B. Kaijser and E. Faisen (Eds.), Campylobacter IV: Proceedings of the Fourth International Workshop on Campylobacter Infections, University of G~teborg, G~teborg, pp. 304-305. Robinson, D.A. (1981) Infective dose of Campylobacterjejuni in milk. Br. Med. J. 282, 1584.
16 Rosef, O. and Kapparud, G. (1983) House flies (Musca domestica) as possible vectors of Campylobacter fetus subsp, jejuni. Appl. Environ. Microbiol. 45, 381-383. Rowe, B. (1990) Recent problems with Salmonella enteritidis. Abstract 0-10, p. 34, The 14th International Symposium of the International Committee on Food Microbiology and Hygiene, Norwegian Food Research Institute, Oslo. Shanker, S., Lee, A. and Sorrelt, T.C. (1986) Campylobacter ./ejuni in broilers: the role of vertical transmission. J. Hyg. Camb. 96, 153-159. Skirrow, M.B. (1987) A demographic survey of campylobacter, salmonella and shigella infections in England. Epidemiol. Inf. 99, 647-657. Skirrow, M.B. (1989) Campylobacter perspectives. PHLS Microbiol. Digest. 6. 113-117. Skirrow, M.B. (1990a) Foodborne diseases and intoxications: Campylobacter. Lancet 336, 921-923. Skirrow, M.B. (1990b) Campylotmcter and Helicobacter infections of man and animals. In: T. Parker and L.H. Collier (Eds.), Topley and Wilson's Principles of Bacteriology, Virology and Immunity, 8th edn. Vol. 3, Edward Arnold, London, pp. 529-542. Sockett, P.N. and Pearson, A.D. (1988) Cost implications of human campyiobacter infections. In: B. Kaijser and E. Faisen (Eds.), Campylobacter IV: Proceedings of the Fourth International Workshop on Campylobacter Infections, University of G6teborg, G~teborg, pp. 261-264. Stern, N.J., Hernandez, M.P., Blankenship, L., Deibel, K.E., Doores, S., Doyle, M.P., Ng, H., Pierson, M.D., Solos, J.N., Sveum, W.H. and Westhoff, D.C. (1985a) Prevalence and distribution of Campylobacterjejuni and Campylobacter coli in retail meats. J. Food Protect. 48, 595-599. Stern, N.J., Rothenberg. P.J. and Stone, J.M. (1985b) Enumeration and reduction of Campylobacterjejuni in poultry and red meats. J. Food Protect. 48, 606-610. Sticht-Groh, V. (1982) Campylobacter in healthy slaughter pigs: a possible source of infection for man. Vet. Rec. 110, 104-106. Turnbull, P.C.B. and Rose, P. (1982) Campylobacterjejuni and salmonella in raw red meats. J. Hyg. Camb. 88, 29-37. Weber, G., Manafi, M. and Reisinger, H. (1987) Die Bedeutung von Yersinia enterocolitica und thermophilen Campylobactern f't~rdie Wasserhygiene. Zbl. Bakt. Hyg. B, 184, 501-514.
9
FOOD 00361
Epidemiology of Campylobacterenteritis M.B. Skirrow Gloucester Public Health Laboratory, Gloucestershire Royal Hospital Gloucester, U.K (Received 6 July 1990; accepted 13 September 1990)
Campylobacter enteritis is the commonest form of infective diarrhoea in most developed countries of the world. In England and Wales laboratory reports indicate an annual incidence of about 85/100000, but the true rate is probably nearer 1100/100000. Measured costs run to many millions of pounds per year. Most infections are sporadic and believed to be foodborne; large outbreaks are infrequent and mostly due to the consumption of raw milk or unchlorinated water. Raw meats and animal products, notably broiler chickens, are the main source of campyiobacters in food. A case-control study in the U.S.A., where eating habits are similar to those in Europe, attributed about one-half of human Camp.vlobacter infections to the consumption of chickens. The production of Campylobacter-free chickens is not yet practicable, but considerable progress could be made to this end with sufficient motivation and resources from government and the poultry industry. Key words: Campylobacter: Diarrhoea; Poultry; Red meat; Milk
Introduction T h e first q u e s t i o n to be addressed is how big a health p r o b l e m is Campylobacter enteritis. T h e disease usually clears u p s p o n t a n e o u s l y after a few days a n d it is seldom d a n g e r o u s (Butzler a n d Oosterom, 1990), so does it m a t t e r all that m u c h ? M e a s u r e m e n t s of incidence a n d m o r b i d i t y show that it does. T h e second q u e s t i o n is how much of the p r o b l e m relates to food a n d the food industry. T h e answer is that moist of it does, so the subject is certainly relevant to this S y m p o s i u m .
Incidence W h e r e c a m p y i o b a c t e r s are looked for r o u t i n e l y in the stools of p a t i e n t s with diarrhoea, they are the most frequently identified pathogens. In E n g l a n d a n d Wales d u r i n g the past 10 years, Campylobacter isolations have exceeded those of Salmonella, even d u r i n g the recent surge of Salmonella enteritidis infection (Rowe, 1990). I n c i d e n c e figures are m u c h i n f l u e n c e d by the availability of diagnostic
Correspondence address: M.B. Skirrow, Gloucester Public Health Laboratory, Gloucestershire Royal Hospital, Gloucester GL] 3NN, U.K.
10 services and the sampling habits of doctors, so one must be careful when making comparisons. Annual rates of 85/100000 in England and Wales (PHLS Communicable Disease Surveillance Centre (CDSC), unpublished) and 60/100000 in Seattle, U.S.A. (Johnson and Nolan, 1985). are probably representative of Europe and North America. These figures are derived from reports of laboratory isolations, which clearly represent only a fraction of the true number of infections. N o b o d y knows what the ratio of reported to actual infections is, but estimates range from 1 in 10 to 1 in 100. A survey of diarrhoea in a single general practice in England (Kendall and Tanner, 1982) gave a projected incidence of 1100/100000. which suggests that the lower of these fractions is the more accurate. In England and Wales, annual Campylobacter isolations have increased four-fold over the last 10 years, but much of this increase is due to increased sampling rather than a true increase in infection (Skirrow, 1989). N o such increase has been observed in the U.S.A. Most of these reports are of sporadic infections or of small family outbreaks affecting only two or three people. Large outbreaks are uncommon and are almost always caused by the distribution of untreated water or milk. In the developed industrialised countries of Europe, North America and Australasia, Campylobacter enteritis affects people of all ages, but typically it has a bimodal distribution with peaks of incidence in children under the age of 4 years and in young adults (Skirrow, 1987). This secondary peak in young adults is not seen with Salmonella or Shigella infections. In developing countries exposure to infection is much greater, with the result that children become immune within the first 2 years or so of life: the disease is not seen in older children or adults. As commercially produced food plays only a small part in this scene, I shall not consider infection in developing countries further.
Seasonal trends Campylobacter enteritis in temperature zones is more c o m m o n in summer than in winter (Blaser et al., 1983). C D S C reports for England and Wales show a striking
15m
"olO. retO
"~5"
4-weekly periods Fig. 1. Seasonal pattern of campylobacter isolations in England and Wales for each of the 9 years, 1981-1989. Mean annual total 22200. (From Skirrow, 1990a.)
11 seasonal consistency (Skirrow, 1987); there is a sharp rise in May, with a peak in July and thereafter a gradual fall to winter levels in December (Fig. 1). The reasons for this pattern are unknown.
Costs
What all this illness means in terms of costs to society was shown starkly by Sockett and Pearson (1988) in a detailed survey of 53 patients with Campylobacter enteritis in England. Direct costs to government (health care, laboratory and environmental health investigation) and indirect costs to the individual and society (mainly lost productive output) amounted to £273 per patient. Thus in 1989 the cost of laboratory diagnosed cases alone amounted to nearly £9 million. In the same study the intangible cost of pain and suffering - - a recognised and legitimate factor - - amounted to as much again.
S o u r c e s and t r a n s m i s s i o n
Campylobacterjejuni and C. coli, the principal causes of Campylobacter enteritis, live in a wide range of animals, particularly birds, mainly as commensals but also as occasional enteric pathogens in the young of some species, notably lambs, calves and puppies (Blaser et al., 1983; Skirrow, 1990b). C. coli is particularly associated with pigs. Human beings are only transient hosts of campylobacters and are a relatively minor source of infection (Blaser et al., 1983). Thus animals form the principal reservoir of infection. Transmission can be direct or indirect. Direct transmisshgn from animals Those whose occupation brings them into close contact with animals or animal products, such as farmers, veterinarians, slaughterhouse workers, poultry processors and butchers, are at increased risk of infection. It appears that many of them become immune through regular exposure (Blaser et al., 1983). Members of the general public may become infected by contact with infected pets, usually in the form of a puppy or kitten with Campylobacter diarrhoea. Although these routes of transmission are well documented, they account for only a minority of infections. Indirect transmission is more important.
Indirect transmission from animals There are many potential routes of infection from animals to man, but basically there are three vehicles: water; milk; and animal meat, which is conveniently grouped under the headings poultry, red meat, and offal.
12
Water In view of the wide range of animals that carry campylobacters it is not surprising that the organisms are common in lakes, rivers and other natural deposits of surface water (Carter et al., 1987). A few sporadic infections arise from the casual or accidental consumption of untreated water, but major outbreaks of Campylobacter enteritis affecting several thousand people have been caused by the distribution of unchlorinated or inadequately treated water (Blaser et al.. 1983). Fortunatel\' such outbreaks are u n c o m m o n and water is probably more important as a source of infection for domestic stock. Campylobacters can survive for several weeks in cold water, including seawater, but for only a few days in water above 1 5 ° C (Blaser et al., 1980; Weber et al., 1987). Milk Milk is almost the only vehicle other than water to have caused major outbreaks of Camp.vlobacter enteritis (Blaser et al., 1983). Most outbreaks are caused by cows" milk, but goats' milk has also been implicated (Hutchinson et al., 1985). It is thought that faecal contamination, which is virtually impossible to avoid even in the best run dairy, is how campylobacters get into the milk. Surveys have shown that 4.5-5.9% of cows' milk samples may contain C. jejuni (Beumer et al., 1988; H u m p h r e y and Hart, 1988). Bovine Campylobacter mastitis provides another means of contamination; although u n c o m m o n it is difficult to detect, as campylobacters are shed into the milk in large numbers before the milk becomes obviously granular (Lander and Gill. 1980; Morgan et al., 1985). As with waterborne infection, it is only the raw or inadequately treated product that is a hazard. Conventional methods of pasteurization readily destroy campylobacters, which are more heat-sensitive than Escherichia coil (D'Aoust et al., 1988). Poultry Colonisation of poultry flocks is almost universal. Most broiler chickens sold in shops are contaminated with campylobacters (Blaser et al., 1983). Uneviscerated (New York dressed) birds may have Campylobacter counts of up to 2.4 x 10 7 per bird (Hood et ai., 1988). Normally processed fresh birds may have counts of up to 1.5 X 10 6 per bird, but fewer organisms survive on frozen birds owing to the damaging effect of freezing and thawing (Gill and Harris, 1984; Stern et al., 1985b). Red meat The process of slaughter and dressing of animals invariably results in the contamination of carcasses with gut flora. Campylobacters can be isolated from a high proportion of cattle, sheep and pig carcasses soon after slaughter (Lammerding et al., 1988), but conventional forced air chilling greatly reduces their number through surface drying (Oosterom et al., 1983). Less than 2% of retailed red meat samples were found to be contaminated in two large surveys (Turnbuil and Rose, 1982; Boiton et al., 1985), but rates of around 5% (Stern et al., 1985a) and 20% (Fricker and Park, 1989) have also been reported. These differences might be
13 explained in part by differences in methods, particularly if contamination was light and near the threshold of detection.
Offal Offal, such as liver, kidney and heart, is more commonly contaminated. There is clearly wide variation with such a variable product, but surveys have shown that 30-47% of such offal samples may be contaminated (Bolton et al.. 1985: Fricker and Park, 1989). It is notable that washing and salting pig intestines, as practised in Germany, does not eliminate campylobacters (Sticht-Groh, 1982).
Campylobacters in food readyfor consumption The presence of campylobacters in raw animal products is one thing: their presence in food that is ready for consumption is quite another. There are two ways in which the gap may be inadvertently bridged. The first is if the contaminated product is eaten raw or undercooked. Although campylobacters are destroyed by light conventional cooking (Gill and Harris, 1984), barbecue and fondue cooking may allow survival in the centre of the food and are known to carry an increased risk of infection (Oosterom et al., 1984; Mouton et al., 1982). Of the few foodborne outbreaks of Campylobacter enteritis that have been reported, undercooked poultry meat has featured significantly often, even though bacteriological proof has not always been obtained. An important difference from Salmonella food poisoning is that campylobacters do not multiply in meat at ambient temperatures. Their minimum growth temperature is about 30 ° C, and at higher temperatures they rapidly become overgrown by other bacteria. The second and probably more important way food becomes a vehicle of infection is by the passive transfer of campylobacters from heavily contaminated meat, such as poultry, to other 'innocent' foods in the kitchen. This is difficult to prove, but it is a logical hypothesis. As few as 500 bacteria are capable of causing infection (Robinson, 1981). Most people cook food adequately, but in a British survey less than one-third of respondents appreciated the need to handle raw meats separately from other foods (Ministry of Agriculture, Fisheries and Food, 1988). Campylobacters have been isolated from flies near pig and poultry units (Rosef and Kapperud, 1983), but there is no evidence that flies are a usual source of infection.
Prevention
Having listed the various sources of Campylobacter infection, we need to consider their relative importance in order to plan appropriate control measures. The proper treatment of water and milk supplies are obvious and highly effective measures that are generally well applied. Surprising as it may seem, there is only one major survey that assesses risk factors associated with foods. This was a case-control study from Seattle, U.S.A., where eating habits are similar to those in Europe (Harris et al., 1986a, b). Poultry, raw milk, raw or rare fish, shellfish, and mushrooms (low risk) were significantly
14 associated with infection, but poultry was the outstanding item. It was calculated that the consumption of chicken accounted for about one-half of all cases. Although much could be done to educate the public in good hygienic practice in the handling of raw poultry and other meats, the single most effective measure would be to eliminate or reduce Campylobacter contamination of poultry in shops. There are three possible lines of attack. (1) Prevention of infection in broiler flocks. As there is no evidence of vertical transmission (Shanker et al., 1986), infection is presumably introduced from extraneous sources sometime during the birds' short 6 - 7 week concentrated lives. Not all flocks become infected. Introduction of campylobacters on the boots of attendants, from small birds or rodents, and in water supplies have been suggested (Humphrey, 1989). Detailed work showing that infection may be introduced and perpetuated in broiler house water supply systems is of particular interest (Pearson et al., 1988): moreover, the application of intervention measures, albeit complex, greatly reduced colonisation in the flocks. (2) Reduction of cross-contamination during mass processing of broilers. The introduction of spray cooling instead of dip tank cooling and of machinery of improved design are examples of how cross-contamination can be reduced, but there is a limit to what can be achieved (Humphrey, 1989). Some cross-contamination is inevitable as long as heavily infected flocks continue to be submitted for processing. (3) Terminal disinfection of dressed birds. The use of disinfectants or acid rinsing of carcasses has not proved effective in concentrations that do not taint or spoil the meat (Humphrey, 1989). Irradiation is effective and it has the advantage of destroying other pathogens, but there are drawbacks, not least the removal of a motive for producing bacteriologically clean birds by means of good husbandry and hygiene. In summary, we must look for ways of reducing the intensity of colonisation of broiler flocks as the single most effective method of controlling human infection. Money and resources put to this end would be well spent even if the outlay is large. What is needed is sufficient motivation from government and the poultry industry.
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