Bulletin of the World Health Organization, 65 (3): 397-406 (1987) © World Health Organization 1987

Infections associated with milk and dairy products in Europe and North America, 1980-85* J. C. M. SHARP1

Outbreaks of infection associated with milk and other dairy products in Europe and North Americafrom 1980 to 1985 are reviewed. Salmonella spp. and Campylobacter spp. were the most commonly identified etiological agents, while other infections of animal origin, in particular listeriosis and yersiniosis, were increasingly reported. Most infections were attributed to untreated cows' milk or cheese, but also increasingly to contaminated "heat-treated" products. Heat-treatment is highly effective in controlling foodborne disease, but may be insufficient if not complemented by high standards of hygiene throughout production and processing. Large community outbreaks of salmonellosis, listeriosis, and yersiniosis in Canada, Sweden, the United Kingdom, and the USA that were associated with contaminated "heat-treated" liquid milk, powdered milk, or cheese emphasize the vulnerability of dairy produce.

INTRODUCTION outbreaks of infections involving heat-treated dairy products. Disease eradication programmes have effectively Heat-treatment of milk and dairy products has controlled bovine tuberculosis and brucellosis in been widely practised for many years throughout many developed countries. Nevertheless, other Europe and North America. Nevertheless, untreated infections, such as salmonellosis, campylobacteri- milk products can still be obtained in most countries osis, listeriosis, and yersiniosis, which do not lend in these continents. For example, untreated cows' themselves so readily to veterinary control measures, milk can be purchased in many areas of France and continue to cause considerable human illness via Switzerland, in some rural districts in Hungary, contaminated milk and dairy products. The increase Ireland, and Poland, and through direct farm sales in in incidence of milkborne infections in the United Austria, England and Wales and the Netherlands. States of America in recent decades (1) has also been Special authorization to sell untreated milk may be observed in the United Kingdom (2-5). Furthermore, granted in Luxembourg and also in rural areas of in Canada over 300 incidents of milkborne disease, Sweden if it is difficult to obtain pasteurized supplies. mainly of bacterial origin, were recorded from 1973 While heat treatment is used generally throughout to 1982 (E. C. D. Todd, personal communication). southern Europe, there are considerable variations Although most episodes reported were associated within countries, depending on the availability of with untreated produce, there was an increase in local pasteurization facilities. In contrast, the sale of untreated dairy produce is totally prohibited in * Based on a paper presented to the Canadian Federal Food Directorate Seminar, November 1985, Ottawa, Canada. Denmark, Iceland, Norway and Yugoslavia, as is ' Consultant Epidemiologist, Communicable Diseases untreated cows' milk in Finland and Scotland. Raw (Scotland) Unit, Ruchill Hospital, Glasgow, G20 9NB, Scotland. milk can be sold under certain conditions in 20 of the 4797 -397 398 J. C. M. SHARP

Table 1. Infections associated with untreated cows' milk in Europe, 1980-85 Period Country Type of infection No. of outbreaks 1980-82 Scotland Salmonellosis 21 (1146) 1980-82 England and Wales Salmonellosis 40 (540) 1980-82 Scotland Campylobacteriosis 6 (278) 1980-82 England and Wales Campylobacteriosis 16 (976) 1981 Switzerland Campylobacteriosis 1 (500) 1981 England and Wales Corynebacterium ulcerans 1 (2) 1983-84 England and Wales Salmonellosis 19 (513) 1983-84 England and Wales Campylobacteriosis 6 (161) 1983-85 Scotland Campylobacteriosis 3 (25) 1983-85 Scotland Salmonellosis 15 (101) 1984 England and Wales "Streptococcus zooepidemicus" 1 (12) 1984 Italy Brucellosis 1 (23) 1985 England and Wales Salmonellosis 6 (54) 1985 England and Wales Campylobacteriosis 6 (178)

' Figures in parentheses indicate the total number of cases.

50 states in the USA and in seven of the 10 Canadian of untreated milk in Scotland decreased from 18% in provinces and territories, although untreated dairy 1970 to 4% in 1982, but paradoxically there was a products are not widely available. concomitant increase in the incidence of milkborne In this paper the reported incidence of infection infections. A cost-benefit study of one major associated with milk and other dairy produce in salmonella outbreak in 1981 (7) estimated a total Europe and North America from 1980 to 1985 is minimum cost at that time of £236 000 reviewed and the factors responsible for the (US$ 446 000)' and a maximum of £3 222 000 occurrence of outbreaks involving contaminated (US$ 6 154 000) with an average cost per patient of heat-treated products are discussed. £2637 (US$ 5036).a In August 1983, legislation was implemented in Scotland prohibiting the retail sale of untreated cows' milk, although temporary REVIEW OF REPORTED INFECTIONS exemptions were extended to several small dairies on islands where pasteurization facilities were not Cows' milk and products readily available. By 1985, only three such dairies remained, whose production represented less than Raw milk. With the exception of the United 0.005% of total milk sales in the country. In Kingdom, untreated liquid cows' milk has rarely been consequence, from 1983 to 1985, general community implicated as a vehicle of foodborne infection in outbreaks of milkborne infection were effectively Europe (Table 1). In 1981, Campylobacter enteritis controlled in Scotland, in marked contrast to the affected 500 persons attending a sports meeting in situation previously and to that elsewhere in the Switzerland (6), and in 1984 an outbreak of United Kingdom (8). However, localized outbreaks brucellosis was reported in a village community in of salmonellosis continued in dairy-farming com- Italy (S. Salmaso, personal communication). Other munities where farm-workers and their families than brucellosis, relatively little milkborne infection drank raw milk from their own herds, a practice not has been reported in southern Europe, but this almost affected by the 1983 legislation (9). certainly is due to underreporting in countries where In England and Wales, where the proportion of national surveillance programmes have not yet been untreated milk consumed has remained around 3% fully developed. for many years, outbreaks of salmonellosis, campylo- Within the United Kingdom, salmonellosis was a bacteriosis, and other milkborne infections have particular problem in Scotland throughout the 1970s continued to be reported (5). The most serious of and early 1980s (2, 4), with community outbreaks of milkborne Campylobacter enteritis also featuring a Calculated using the November-1981 exchange rate of from time to time. During this period the proportion £1=USS 1.91. MILK AND DAIRY PRODUCT INFECTIONS 399

Table 2. Infections associated with untreated cows' milk in North America, 1980-85

Period Country Type of infection No. of cases 1980 USA (Montana) Salmonellosis 105 1980 Canada (Alberta) Campylobacteriosis 27 1980-81 USA (Oregon) Campylobacteriosis 116 1980-81 USA (Washington) Salmonellosis 18 1980-82 Canada (Ontario) Salmonellosis > 127 1981 USA (Kansas) Campylobacteriosis 250 1981 USA (Minnesota) Campylobacteriosis 25 1981 USA (Georgia) Campylobacteriosis 50 1982 USA (Wisconsin) Campylobacteriosis 15 1983 USA (Pennsylvania) Campylobacteriosis 31 1983 USA (Pennsylvania) Campylobacteriosis 26 1983 USA (Arizona) Salmonellosis 12 1984 USA (California) Campylobacteriosis 12 1984 USA (Califomia) Campylobacteriosis 27 1984 Canada (British Columbia) Campylobacteriosis 9 1985 USA (California) Campylobacteriosis 23

these, in 1984, was due to "Streptococcus instances affecting groups, particularly school and zooepidemicus" and 12 persons were admitted to kindergarten classes, who had drunk untreated milk hospital, eight of whom died. In November 1985, while visiting farms. Outbreaks of salmonellosis were legislation was introduced in England and Wales also reported in Ontario in Canada (21) and in prohibiting the sale of untreated cows' milk in shops, Montana (22), Washington (23), and Arizona (24) in canteens, and other retail outlets, but unlike the the USA (Table 2). During 1980-82 in Canada, raw situation in Scotland, this did not affect the sale of milk was identified as the vehicle of infection in a untreated milk direct from dairy farms, including further 14 episodes of salmonellosis (affecting 59 local retail deliveries. persons), eight of campylobacteriosis (52 persons), Campylobacteriosis outbreaks have been reported three of yersiniosis (7 persons), and one of Q fever (1 in Canada (in Alberta and British Columbia) (10, 11) person) (E. C. D. Todd, personal communication). and in several locations in the USA (12-20), in many Also, Werner et al. (25) established a strong

Table 3. Infections associated with heat-treated cows' milk in Europe and North America, 1980-85 Period Country Type of infection No. of cases Comments 1980 England and Wales Campylobacteriosis 30 Unsterilized containers' 1982 USA (Tennessee inter alia) Yersiniosis 172 Fault not determined 1982 England and Wales Campylobacteriosis 400 Mixed with raw milk 1982 Scotland Campylobacteriosis 179 Failure to pasteurize 1983 USA (Massachusetts) Listeriosis 49 Large inoculum' 1983 England and Wales Salmonellosis 5 Post-treatment contamination 1984 USA (Kentucky) Salmonellosis 16 Inadequate pasteurization 1984 England and Wales Yersiniosis 2 Post-treatment contamination 1985 England Yersiniosis 3 Fault not determined 1985 USA (Illinois inter alia) Salmonellosis > 16 000 Contamination of cross-connecting pipe' 1985 Sweden Salmonellosis 153 Post-treatment contamination 1985 Guernsey, Channel Islands Salmonellosis 50 Inadequate pasteurization' 1985 USA (Kentucky) Staphylococcal enterotoxin 860 Contaminated chocolate milk

a Not firmly established. 4ao J. C. M. SHARP statistical association between the consumption of (3, 8), while contamination at a later stage of raw milk and endemic Salmonella dublin infection in preparation also caused minor outbreaks of staphylo- California. Finally, in Iowa, Warner et al. (26) coccal enterotoxin "food poisoning" (35). reported that 23% of 168 cases of campylobacteriosis during 1981-82 had drunk untreated milk. Cheese. Cheese, particularly when prepared from untreated cows' milk, was responsible for a wide "Heat-treated" milk. Outbreaks of infection range of infections (Table 4). Outbreaks of salmonel- implicating heat-treated milk have been reported in losis were reported in Canada (36), Finland (P. several countries (Table 3). Post-treatment contam- Pakkala, personal communication), and Switzerland ination of milk caused outbreaks of campylobacteri- (37), while enterotoxigenic E. coli enteritis from osis, salmonellosis, and yersiniosis in England and imported French cheese was reported in the Wales (3, 5, 27) (PHLS Communicable Disease Netherlands, Scandinavia, and the USA (38), and Surveillance Centre, unpublished report), as well as infection by "Streptococcus zooepidemicus" in New salmonellosis in Sweden (28). Also, in the USA Mexico, USA (39). Bacillary dysentery caused by contaminated pasteurized milk was responsible for Shigella sonnei, which affected numerous persons outbreaks of yersiniosis in Tennessee, Arkansas, and who had eaten various French cheeses purchased at a Mississippi (29), listeriosis in Massachusetts (30), sal- Paris airport in 1982, was reported by several monellosis in Illinois and adjacent states (31, 32), and Scandinavian countries through the early-warning staphylococcal enterotoxin "food poisoning" in system of the WHO Surveillance Programme for the Kentucky (33). Inadequate heat-treatment was Control of Foodborne Infections and Intoxications reported as the cause of salmonellosis in Guernsey, in Europe. During 1983-84 in Greece, 23 cases of Channel Islands (E. P. Lawrence, personal com- brucellosis were associated with consumption of a munication) and at a convent in Kentucky, USA (34). variety of fresh "home-made" cheeses (T. Stefanou, Other contaminated "heat-treated" products identi- personal communication). fied as vehicles of foodbome infection were cheese (associated with salmonellosis in Canada and Italy Cheddar cheese prepared from heat-treated milk and listeriosis in the USA) and powdered milk that had been contaminated in the pasteurizer of a (salmonellosis in the United Kingdom). cheese-making factory was responsible for salmonel- losis that affected over 2700 persons in the maritime Cream. Cream seldom featured as a vehicle of provinces of Canada in 1983-84 (40, 41). In 1985, foodborne disease. No episodes of any consequence one brand of "heat-treated" Mexican-style soft have been reported since 1974, when an outbreak of cheese was implicated in over 100 cases (including 40 salmonellosis affected over 500 persons in Sweden. deaths) of listeriosis in southern California, USA Several small-scale episodes of salmonellosis and (S. B. Werner, personal communication). Also, infection by Bacillus cereus and Escherichia coli cross-contamination of heat-treated mozzarella following consumption of untreated farm-produced cheese in a restaurant in Italy caused an outbreak of cream have been reported in the United Kingdom salmonellosis that affected over 100 persons (42).

Table 4. Infections associated with cows' milk cheese in Europe and North America, 1980-85 Period Country Type of infection No. of cases Type of cheese 1981 Italy Salmonellosis 100 Mozzarella' 1982 Canada (Ontario) Salmonellosis 8 "Oriental-type white", inter alia 1982 Scandinavia b Bacillary dysentery > 50 Brie, inter alis 1983 USA, Sweden, NetherlandsC Escherichia coli enteritis 350 Brie 1983 Finland Salmonellosis 35 "Farmhouse" 1983 USA (New Mexico) "Streptococcus zooepidemicus" 16 Home-made Queso blanco 1983 England and Wales Staphylococcal enterotoxin 2 Cheddar' 1983-84 Greece Brucellosis 23 "Home-made unripened" 1984 Canada (Maritime Provinces) Salmonellosis 2700 Cheddar 1985 USA (Califomia inter alia) Usteriosis - 100 Mexican-style' 1985 Switzeriand Salmonellosis 215 Vacherin

' "Heat-treated" product. bCheese purchased in France. ' Cheese imported from France. MILK AND DAIRY PRODUCT INFECTIONS 401

Butter. Butter seldom features as a vehicle of throat" associated with untreated goats' milk were foodborne infection, unless it contains also a raw recorded in Canada (46), the United Kingdom (3, 5, ingredient. For example, in Finland butter that 47), and the USA (45) (Table 5). In several instances, contained eggs caused two episodes of infection in the produce had been consumed by tourists during 1983-84: in one, staphylococcal "food poisoning" visits abroad, particularly to Mediterranean affected residents in an old persons' home; the second countries. of undetermined etiology, involved guests at a social Cheese made from contaminated, untreated function (P. Pakkala, personal communication). sheep's milk caused outbreaks of staphylococcal "food poisoning" in France and Scotland. In the Powdered milk French episode the source was traced to a shepherd who had made the cheese (48), whereas in Scotland Numerous cases of salmonellosis were identified the infection was of animal origin. Subsequent exam- throughout the United Kingdom during the latter ination of the remaining cheeses in Scotland revealed months of 1985, mainly affecting infants who had heavy contamination by staphylococcal organisms been fed a particular brand of powdered milk. The and enterotoxin, as well as numerous coliforms (F. J. same serotype (Salmonella ealing) was isolated from Bone, personal communication). various environmental and other samples of the product (43). DISCUSSION

Ice-cream Milk and dairy products are a valuable source of nutrition, but may harbour the following pathogens Outbreaks of infection associated with consump- or be exposed during production to contamination tion of ice-cream are relatively rare and have usually from various animal, environmental, or human been associated with "home-made" ices containing sources. eggs. In an outbreak of clinically severe salmonellosis involving eight persons at a farm in Wyoming, USA, -Pathogens of animal origin, the most important in 1982, a previously healthy 13-year-old boy died source, may be excreted in milk (Brucella, Campylo- (44). Furthermore, in 1984 in England, salmonellosis bacter, Coxiella, Listeria, Mycobacteria, Salmonella, affected 12 persons who had eaten "home-made" Staphylococcus, Streptococcus, and Toxoplasma ice-cream at a hotel (5). spp.) but, more commonly, contamination occurs during milking from the skin, particularly the teat (Staphylococcus and Streptococcus spp.), or from Goats' and sheep's milk faeces (Campylobacter, Escherichia, Salmonella, and Episodes of brucellosis, campylobacteriosis, sal- Yersinia spp.). monellosis, staphylococcal enterotoxin "food -Environmentally-acquired organisms include poisoning", and Corynebacterium ulcerans "sore Clostridium botulinum and Bacillus cereus, while

Table 5. Infections associated with goats' and sheep's milk products in Europe and North America, 1980-85 Period Country Type of infection No. of cases Product

1980 England and Wales - imported from Turkey Salmonellosis 6 Cheese 1981-83 England and Wales - imported from Sicily Brucellosis 2 Cheese and Jordan 1983 France Staphylococcal enterotoxin 20 Cheese' 1983 England and Wales Staphylococcal enterotoxin 2 Cheese 1983 England and Wales Corynebacterium ulcerans 1 Cheese 1983 Scotland - consumed in Canary Islands Brucellosis 1 Milk 1983 USA (Texas) - Mexican immigrants Brucellosis 30 + Cheese 1984 England and Wales Campylobacteriosis 3 Milk 1984 Scotland b Staphylococcal enterotoxin 19 Cheese' 1985 Scotlandb Staphylococcal enterotoxin 12 Cheese' 1985 Canada (British Columbia) Salmonellosis 5 Milk

' Sheep's milk. bBoth outbreaks were associated with the same hotel and farm of origin. 402 J. C. M. SHARP pathogens of human or animal origin may also cance are the many changes that took place over this contaminate equipment. Sewage effluents that con- period in dairying, such as more intensified animal taminate pastureland or animal drinking water have husbandry and production methods, a consequence caused outbreaks of milkborne salmonellosis (49). of advancing technology and economic pressures. In Environmental cross-contamination can occur in the United Kingdom, which has the largest dairy factories (37) or the kitchen (42). herds (average herd size 58.2 in 1984) in the European - Infections of human origin may be transmitted by Economic Community (EEC), followed by the direct contact (e.g., staphylococcal "food poison- Netherlands (42.3) and Denmark (28.4), the average ing"), via droplets (e.g., diphtheria and streptococcal number of cows per herd more than doubled between "sore-throat"), or by faecal spread (e.g., typhoid, 1965 and 1984. The traditional byre (cow-shed) has bacillary dysentery, and viral hepatitis). These, gradually been replaced by the milking parlour with however, have only occasionally been associated with cattle being "loose-housed" and this, together with milkborne disease in Europe and North America over the use of collecting yards, frequently results in faecal the last few decades, following improvements in soiling of animals prior to milking. The average standards of human health and in environmental number of cows per dairyman has also increased sanitation, along with the increasing use of closed markedly, with as many as 120 animals being systems for milk production. attended by one person in some of the largest dairies, thus minimizing the time available for attention to the Dairy products are excellent culture media for hygiene of individual animals. Modern milking bacteria, their high fat content protects micro- systems comprise pipe-lines and bulk collection organisms from gastric acid, while the fluid nature of tanks, and if one cow's milk is contaminated, the milk minimizes exposure time in the stomach. It has entire supply will readily become affected. Also, since been estimated that in milk as few as 500 cells of any faecal pathogens will be excreted in greater Campylobacter spp. (50) and in cheese 1-6 cells of numbers following the stresses of calving, an event Salmonella spp. (51) may be all that is required to followed by the period of optimum lactation, the cause human illness. Individuals with hypochlor- potential exposure of milk to contamination has hydria and/or who are immunocompromised are par- almost certainly increased in parallel with the above- ticularly vulnerable to infection, especially if they mentioned changes in the dairy industry. The smaller have consumed "health-promoting" foods, among herds and less intensified dairy farming in other EEC which raw milk features prominently. S. dublin, in countries, particularly those where a considerable particular, has a well known propensity for invasive- amount of untreated dairy produce is available in ness, severity of illness, and death among those whose rural areas, may also be a significant factor in health is compromised. The virulence associated with the absence of reported outbreaks of milkborne outbreaks of listeriosis (30) and the emergence of infection. multiple antibiotic-resistant strains of S. typhi- In contrast to liquid milk, cream features murium (22, 24), leading to further therapeutic infrequently in foodborne infections. Commercially- problems and fatalities, have also been observed in produced cream is virtually always heat-treated and recent years. has an excellent health record. Legislation relating to Heat-treatment is a highly effective method of the heat-treatment of cream and milk-based drinks preventing milkborne disease and this has been was introduced throughout the United Kingdom in emphasized by WHO (52). The implementation of November 1983, although this did little more than legislation in Scotland in 1983 prohibiting the sale of consolidate what had been almost universal practice untreated cows' milk resulted in the disappearance of for many years. general community outbreaks of milkborne infec- Cheese, particularly if prepared from untreated tion, in marked contrast to the previous years and to milk, has been associated with a wide range of elsewhere in the United Kingdom. The high annual infections. Unripened soft cheeses (e.g., Coulom- incidence (111 per 100 000) of milkborne salmonel- miers and cottage cheese), with their high moisture losis in Scotland, which has continued in dairy- content, offer optimum conditions for bacterial farming communities (9), should also be effectively survival and, if contaminated, pose a relatively controlled by measures introduced in September 1986 greater risk than matured cheeses, whose moisture to replace with pasteurized milk the provision of raw content can vary considerably from high (e.g., Brie milk as a payment benefit to farm-workers. and Camembert), to medium (e.g., Roquefort), to The increase in milkborne infection in Scotland low (e.g., Cheddar). In recent years matured cheeses, during the 1970s and early 1980s, despite the however, have featured more prominently in out- decreasing availability of untreated cows' milk, was breaks of infection than unripened soft cheeses. unexpected and can only partly be explained by Interestingly, Wood et al. (53) in Canada have improved surveillance. Probably of greater signifi- demonstrated the persistence of Salmonella spp. in MILK AND DAIRY PRODUCT INFECTIONS 403 naturally contaminated Cheddar cheese. In countries Fisheries for Scotland and have become increasingly where heat-treatment is practised, however, cheese is adopted throughout the United Kingdom and rarely implicated in foodborne disease, unless it is elsewhere. subsequently contaminated. Nevertheless, the exten- Proponents of untreated dairy produce have pro- sive outbreaks of salmonellosis in Canada and posed numerous arguments in its favour, citing its listeriosis in the USA indicate that there are no superior taste and greater nutritional and health- grounds for complacency. promoting properties compared with heat-treated Heat-treated dairy products, such as commercially counterparts. These claims are, however, unfounded produced butter, flavoured milks, and processed and have been refuted over the years. cheese, along with yoghurt and other fermented The following problems associated with pasteuriz- products (e.g., kefir), generally have a very good ation "failure", are, nevertheless, not unknown and record and have notably been absent as vehicles of can be attributed to a number of factors, which the foodborne infection, unless they contain also an dairy industry cannot afford to ignore if milkborne untreated ingredient such as egg or flavouring. infection is to be prevented: During the 1940s and 1950s outbreaks of illness -Spore-bearing organisms (e.g., B. cereus, a associated with powdered milk were invariably of common dairy contaminant, C. botulinum, and human origip1, such as streptococcal "sore throat", C. perfringens) readily survive pasteurization, typhoid, and ;viral hepatitis. However, from the 1960s although only occasionally have they featured as onwards, infections of animal origin predominated, etiological agents. and outbreaks of salmonellosis, in particular, were - Pre-formed heat-stable staphylococcal enterotoxin reported from several countries. Between 1970 and is not destroyed by pasteurization. 1978 the United States Department of Agriculture -Fleming et al. (30) have suggested that a large reported that 1.9% of samples of powdered milk inoculum of microorganisms, particularly those examined were contaminated with Salmonella spp. (e.g., Listeria spp.) able to exist intracellularly in (54). Contaminated powdered milk gives cause for milk, might permit their survival. Subsequent studies considerable concern in view of the vulnerability of by Bradshaw et al. (56) have demonstrated, however, infants, who form the largest consumer group. the efficacy of high-temperature short-time (HTST) However, a problem usually only arises if the pasteurization in destroying L. monocytogenes in reconstituted milk is incorrectly stored at ambient whole milk. temperature before use. -Failure to achieve proper pasteurization tempera- Today, ice-cream is more frequently prepared from tures or duration of heating (34). Incorrect tempera- vegetable rather than dairy fats, and is generally a safe tures may also inadvertently be used in plants that product unless mishandled at the point of sale or alternate between pasteurization of liquid milk and in the kitchen prior to consumption. In most the lower temperatures used in heat treatment for countries, legislation requires that the raw ingredients cheese-making. used in commercially produced ice-cream, whether of -Temporary breakdowns can occur, for example, animal or vegetable origin, are heat-treated to certain because of electrical failure during severe weather specified standards. conditions in winter (57). In a survey of goats' milk in England, Roberts (55) -Post-treatment contamination may arise from reported the isolation of S. aureus, E. coli and faulty equipment and/or human error. For example, occasionally Y. enterocolitica and Campylobacter pasteurized milk that was subsequently contaminated spp. from less than 10% of samples examined, while caused salmonellosis in Sweden (28), while contami- further work showed that B. cereus, S. aureus, nation in England produced outbreaks of campylo- Salmonella spp., and Yersinia spp. readily survived. bacteriosis, salmonellosis, and yersiniosis (3, 5, 43). Contamination was primarily due to poor hygiene Also, in the maritime provinces of Canada, untreated practices during production. In addition to infections milk that leaked into treated milk in the pasteurizer associated with goats' milk during 1980-85, episodes of a cheese factory, compounded by human error, oftoxoplasmosis and yersiniosis were also reported in caused salmonellosis (40,41). Furthermore, raw milk the USA in earlier years. Relatively few human inadvertently mixed with pasteurized resulted in cam- infections have been recorded implicating sheep milk pylobacteriosis at a school in England (27), while in products. Such products, usually untreated, have New York, USA, untreated chocolate syrup added to become increasingly popular in the United Kingdom, pasteurized milk produced an outbreak of yersiniosis in particular, where current dairy legislation applies in 1976 (58). to cows' milk only. In the absence of mandatory treatment, codes of practice for the hygienic Outbreaks associated with contaminated "heat- production of goats' and sheep's milk have been treated" milk products, when they do occur, are prepared by the Department of Agriculture and liable to be extensive, involving thousands of 404 J. C. M. SHARP

consumers (32, 41), and the resultant health and to maintain high standards throughout production, economic consequences can be enormous. processing, and distribution from farm to consumer Heat-treatment by itself, therefore, may be is of paramount importance. Any lowering of insufficient and must always be complemented by standards will undoubtedly result in contaminated good hygiene and correct operational practices. The supplies and outbreaks of infection, all of which are constant awareness by the dairy industry of the need totally preventable.

ACKNOWLEDGEMENTS

My thanks are due to Mr G. M. Paterson and Mr W. J. Reilly, Glasgow, Dr G. I. Forbes, Edinburgh, Dr E. C. D. Todd, Ottawa, and Dr E. H. Angus, Coquitlam, British Columbia, for their helpful advice in the preparation of this paper, to other colleagues elsewhere in the United Kingdom, Europe, and the USA for epidemiological and other information provided, and to Mrs Mary Graham and Mrs Suzanne Jardine for secretarial assistance.

RtSUMV

INFECTIONS ASSOCIEES AU LAIT ET AUX PRODUITS LAITIERS EN EUROPE ET EN AMERIQUE DU NORD DE 1980 A 1985

Dans beaucoup de pays developpes, les programmes episodes de brucellose, de campylobacteriose, de salmo- d'eradication ont permis de circonscrire de facon efficace la nellose, d'intoxications alimentaires par l'enterotoxine tuberculose et la brucellose bovines. Neanmoins, d'autres staphylococcique et d'infections de la gorge dues a Coryne- infections, telles que les salmonelloses, les campylobac- bacterium ulcerans se sont produits au Canada, aux Etats- terioses, les listerioses et les yersinioses, qui ne se pretent pas Unis, en France et au Royaume-Uni et ont et attribues a des aussi facilement a des mesures de contr6le veterinaire, produits a base de lait de chevre ou de brebis non traite continuent d'etre une cause importante de maladie et de qui, dans certains cas, avaient e consommes en dehors de mortalite chez l'homme. ces pays. Le present article passe en revue les flamb&es d'infections Des produits laitiers traites par la chaleur ont egalement associ6es au lait et aux produits laitiers qui ont ete signal6es e mis en cause dans plusieurs pays. La contamination du en Europe et en Am6rique du Nord, de 1980 a 1985. La lait de vache posterieurement au traitement a cause des plupart des cas etaient dus au lait de vache ou a des fromages flambees de listeriose, de salmonellose et de yersiniose aux non traites, bien que plusieurs pouss6es aient pu etre Etats-Unis, de campylobacteriose, de salmonellose et de attribu6es a des produits traites par la chaleur. yersiniose au Royaume-Uni, et de salmonellose en Suede. En Europe continentale, si l'on excepte une epidemie D'autre part, des epidemies de salmonellose qui se sont d'ent6rite a campylobacter, survenue en Suisse en 1981, et produites dans les iles Anglo-Normandes et aux Etats-Unis des cas de brucellose dans un village italien en 1984, peu ont e attribu&es a un traitement thermique inadequat. Des d'infections mettant en cause le lait de vache non traite ont fromages traites par la chaleur et contamines ont e a e observ&es au cours de cette periode. Par contre, au l'origine de cas de salmonellose au Canada et en Italie, ainsi Royaume-Uni, la salmonellose transmise par le lait a pose que de cas de listeriose aux Etats-Unis, tandis que du lait en un probleme particulier en Ecosse jusqu'en 1983, ann6e ou poudre contamine a e a l'origine d'une flamb&e de une legislation interdisant la vente au detail de lait de vache salmonellose au Royaume-Uni. non traite a ete mise en vigueur. En Amerique du Nord, de Le traitement thermique des produits laitiers est un nombreuses flamb&es de salmonellose et de campylobac- moyen de lutte tres efficace contre les infections d'origine teriose caus&es par le lait se sont produites, tant aux Etats- alimentaire; a lui seul, ce traitement peut toutefois etre Unis qu'au Canada. insuffisant si des normes d'hygiene rigoureuses et des La consommation de fromage contamine prepar6 a partir methodes de travail correctes ne sont pas appliquees a tous de lait de vache non traite s'est traduite par des cas de sal- les stades de la production, du traitement et de la distri- monellose au Canada, aux Etats-Unis, en Finlande et en bution. Tout abaissement du niveau des normes se traduira Suisse, ainsi que des infections a "Streptococcus zooepi- sans aucun doute par la mise en circulation de produits demicus" aux Etats-Unis. Des fromages frangais ont W contamines et par des flambees d'intoxications dont les l'origine de pouss&es de dysenterie bacillaire en Scandinavie consequences sanitaires et economiques risquent d'etre et d'intoxications a Escherichia coli enterotoxinogene aux considerables. Etats-Unis, aux Pays-Bas et en Scandinavie. De plus, des MILK AND DAIRY PRODUCT INFECTIONS 405

REFERENCES

1. BRYAN, F. L. Epidemiology of milkborne diseases. 20. BENDA, B. ET AL. Campylobacter outbreak associated Journal offood protection, 46: 637-649 (1983). with raw milk provided on a dairy tour. California 2. SHARP, J. C. M. ET AL. Milkborne salmonellosis in morbidity weekly report, No. 5, February 7 1986, p. 1. Scotland. Journal of infection, 2: 333-340 (1980). 21. Increasing incidence of Salmonella muenster in 3. GALBRAITH, N. S. ET AL. Communicable disease Ontario. Ontario disease surveillance report, 3 (13): associated with milk and dairy products in England and 141-142 (1982). Wales 195 1-1980. British medical journal, 284: 22. DAY, C. ET AL. Salmonellosis associated with raw 1761-1765 (1982). milk-Montana. Morbidity and mortality weekly 4. REILLY, W. J. ET AL. Milkborne salmonellosis in report, 30 (18): 211-218 (1981). Scotland 1980 to 1982. Veterinary record, 112: 578-580 23. ANDERSON, H. ET AL. Salmonella dublin associated with (1983). raw milk-Washington. Morbidity and mortality 5. BARRETr, N. J. Communicable disease associated with weekly report, 30 (30): 373-374 (1981). milk and dairy products in England & Wales: 24. TACKET, C. 0. ET AL. An outbreak of multiple drug- 1983-1984. Journal ofinfection, 12: 265-272 (1986). resistant Salmonella enteritis from raw milk. Journal of 6. STALDER, H. ET AL. [On the epidemiology of Campylo- the American Medical Association, 253: 2058-2060 bacter jejuni]. Schweizerische medizinische Wochen- (1985). schrift, 113: 245-249 (1983) (in German). 25. WERNER, S. B. ET AL. Salmonella dublin and raw milk 7. COHEN, D. R. ET AL. A cost-benefit study of milk- consumption-California. Morbidity and mortality borne salmonellosis. Journal of hygiene, 91: 17-23 weekly report, 33 (14): 196-198 (1984). (1983). 26. WARNER, D. P. ET AL. Epidemiologic study of 8. SHARP, J. C. M. ET AL. Pasteurisation and the control campylobacteriosis in Iowa cattle and the possible role of milkborne infection in Britain. British medical of unpasteurised milk as a vehicle of infection. journal, 291: 463-464 (1985). American journal of veterinary research, 47: 254-258 9. FORBES, G. I. ET AL. Milkborne salmonellosis affecting (1986). farming communities in Scotland. Communicable 27. Disease associated with milk and dairy products, 1982. diseases (Scotland) weekly report, 20 (26): 7-9 (1986). British medical journal, 288: 466-467 (1984). 10. McNAUGHTON, R. D. ET AL. Campylobacter enteritis 28. ANDERSSON, Y. ET AL. A milkborne outbreak in Sweden associated with the consumption of raw milk - in the summer of 1985. In: Proceedings of2nd World Alberta. Canada diseases weekly report, 7 (4): 20 Congress Foodborne Infections and Intoxications, (1981). Berlin, 26-30 May 1986. Vol. 1, pp. 290-293. 11. BATES, M. ET AL. Campylobacteriosis associated with 29. TACKET, C. 0. ET AL. A multistate outbreak of the consumption of raw milk - British Columbia. infections caused by Yersinia enterocolitica transmitted Canada diseases weekly report, 10 (40): 156-159 by pasteurised milk. Journal of the American Medical (1984). Association, 251: 483-486 (1984). 12. TERHUNE, C. ET AL. Raw-milk associated illness- 30. FLEMING, D. W. ET AL. Pasteurised milk as a vehicle of Oregon. Morbidity and mortality weekly report, 30 (8): infection in an outbreak of listeriosis. New England 90-91 (1981). journal of medicine, 312: 404-407 (1985). 13. BLESSING, D. J. ET AL. Campylobacter associated with 31. Update: Milk-borne salmonellosis- Illinois. Mor- raw milk consumption -Pennsylvania. Morbidity and bidity and mortality weekly report, 34 (15): 215-216 mortality weekly report, 32 (26): 337-344 (1983). (1985). 14. POTrER, M. E. ET AL. Human campylobacter infection 32. SUN, M. Desperately seeking salmonella in Illinois. associated with certified raw milk. Americanjournal of Science, 228: 829-830 (1985). epidemiology, 117: 475-483 (1983). 33. LECOS, C. W. A closer look at dairy safety. Dairy and 15. Campylobacter outbreak associated with certified raw food sanitation, 6: 240-242 (1985). milk products-California. Morbidity and mortality 34. ADAMS, D. ET AL. Salmonellosis from inadequately weekly report, 33 (39): 562 (1984). pasteurized milk-Kentucky. Morbidity and mortality 16. ONTIVEROS, M. L. ET AL. Campylobacter outbreak weekly report, 33 (36): 505-506 (1984). after consuming raw milk on a field trip to a dairy. 35. Disease attributed to dairy products. British medical California morbidity weekly report, No. 9, March 8 journal, 285: 1664 (1982). 1985, p. 1. 36. Presence of Salmonella muenster in Ontario cheese. 17. KORNBLATT, A. N. ET AL. Epidemiologic and Ontario disease surveillance report, 3 (13): 143 (1982). laboratory investigation of an outbreak of Campylo- 37. SADIK, C. ET AL. An epidemiological investigation bacter enteritis associated with raw milk. American following an infection by Salmonella typhimurium due journal ofepidemiology, 122: 884-889 (1985). to the ingestion of cheese made from raw milk. In: 18. KLEIN, B. S. ET AL. Campylobacter infection associated Proceedings of 2nd World Congress Foodborne with raw milk. Journal of the American Medical Infections and Intoxications, Berlin, 26-30 May 1986. Association, 225: 361-364 (1986). Vol. 1, pp. 280-282. 19. KORLATH, J. A. ET AL. A point-source outbreak of 38. MACDONALD, K. L. ET AL. A multistate outbreak of campylobacteriosis associated with consumption of raw gastrointestinal illness caused by enterotoxigenic milk. Journal of infectious diseases, 152: 592-596 Escherichia coli in imported semisoft cheese. Journal of (1985). infectious diseases, 151: 716-720 (1985). 406 J. C. M. SHARP

39. ESPINOSA, F. H. ET AL. Group C streptococcal Symposium on Staphylococci and Staphylococcal infections associated with eating homemade cheese- Infections, Warsaw, Poland, 26-30 June 1984. New Mexico. Morbidity and mortality weekly report, Stuttgart, Fischer Verlag, 1985, pp. 677-678. 32 (39): 510-516 (1983). 49. REILLY, W. J. ET AL. Human and animal salmonellosis 40. D'AOUST, J.-Y. ET AL. Salmonella typhimurium phage in Scotland associated with environmental con- type 10 from Cheddar cheese implicated in a major tamination. Veterinary record, 108: 553-555 (1981). Canadian foodborne outbreak. Journal of food 50. ROBINSON, D. A. Infective dose of Campylobacter protection, 48: 1062-1066 (1985). jejuni in milk. British medical journal, 282: 1584 41. TODD, E. C. D. A large outbreak in Canada of sal- (1981). monellosis from Cheddar cheese. In: Proceedings ofthe 51. D'AouST, J.-Y. Infective dose of Salmonella First International Congress on Food and Health, typhimurium in Cheddar cheese. American journal of Salsomaggiore Terme, Italy, 28-31 October 1985 (in epidemiology, 122: 717-720 (1985). press). 52. WHO Technical Report Series, No. 598, 1976 (Micro- 42. FELIP, G. DE & TOTI, L. [Foodborne diseases caused by biological aspects offood hygiene: report of a WHO Gram-negative microorganisms in milk products.] Expert Committee with the participation of FAO). Microbiologie-aliments-nutrition, 2: 251-256 53. WOOD, D. S. ET AL. Source and persistence of (1984) (in Italian). Salmonella muenster in naturally-contaminated 43. Communicable Disease Report, October to December Cheddar cheese. Journal offoodprotection, 47: 20-22 1985. Salmonellosis due to dried baby milk. (1984). Community medicine, 8 (3): 246 (1986). 54. EDITORIAL. Salmonellosis associated with consumption 44. TAYLOR, D. N. ET AL. An outbreak of salmonellosis of non-fat powdered milk-Oregon. Morbidity and associated with a fatality in a healthy child: a large dose mortality weekly report, 28 (11): 129-130 (1979). and severe illness. American journal of epidemiology, 55. ROBERTS, D. Microbiological aspects of goats' milk. A 119: 907-912 (1984). Public Health Laboratory Service survey. Journal of 45. PERKINS, P. ET AL. Brucellosis-Texas. Morbidity and hygiene, 94: 31-44 (1985). mortality weekly report, 32(42): 548-553 (1983). 56. BRADSHAW, N. G. ET AL. Thermal resistance of Listeria 46. JEssoP, J. H. ET AL. Outbreak of an unusual salmonella monocytogenes in milk. Journal offoodprotection, 48: serotype spread by goats' milk- British Columbia. 743-745 (1985). Canada diseases weekly report, 11 (52): 219-220 (1985). 57. PORTER, I. A. & REID, T. M. S. A milkborne outbreak 47. HUTCHINSON, D. N. ET AL. Campylobacter enteritis of campylobacter infection. Journal of hygiene, 84: associated with consumption of raw goats' milk. 415-419 (1980). Lancet, 1: 1037-1038 (1981). 58. BLACK, R. E. ET AL. Epidemic of Yersinia enterocolitica 48. DE BUYSER, M. L. ET AL. Contamination of ewe cheese infection due to contaminated chocolate milk. New with Staphylococcus aureus: study of an outbreak of Englandjournal of medicine, 298: 76-79 (1978). food poisoning. In: Proceedings of V International