Epidemiology of Milk-Borne Diseases

Home , Listeriosis, Q fever, Shigellosis

637

FRANK L. BRYAN

Department of Health and Human Services. Public Health Service. Centers for Disease Control. Atlanta, Georgia 30333

(Received for pUblication November 22, 1982) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021

abundance of health hazards that were associated with in ABSTRACT gestion of raw milk in the early 1900s until the end of Secular trends in milk-borne diseases in the U.S.A. show World War n, Then, because most of the milk was pas numerous outbreaks associated with ingestion of raw milk in the teurized, outbreaks decreased dramatically. early 1900s until the end of World War II. Diseases common in Reports of experimental milk pasteurization were just this period, but no longer milk-borne, were typhoid fever, scarlet appearing in the public health literature in the early 1900s, fever, septic sore throat, diphtheria, tuberculosis, shigellosis, and but the process did not come into common use for many milk sickness. Milk-borne and milk-product-borne diseases rarely years thereafter. The first model milk ordinance recom reported somewhere in the world were botulism, Escherichia coli mended by the U.S. Public Health Service, for instance, enteritis, Pseudomonas aeruginosa enteritis, listeriosis, Clos was published in 1924 and a draft code followed in 1927. tridium periringens enteritis, Bacillus cereus gastroenteritis, Haverhill fever, Q fever, hepatitis A, poliomyelitis, toxoplas From that time on, pasteurization for milk was stressed na mosis, histamine intoxication and hypertension. After most milk tionally. Since 1950, there have been reports of only a few was pasteurized, outbreaks decreased dramatically. Milk-borne raw milk-associated outbreaks; but, such outbreaks still diseases of contemporary importance in the U.S.A. are salmonel occur, because some people prefer to drink raw milk. losis, campylobacteriosis, staphylococcal intoxication, brucel The percentage of reported outbreaks of milk-borne dis losis, and yersiniosis. These have usually been associated with in ease by decade is shown in Table I, Several trends stand gestion of raw milk, certified raw milk, home-made ice cream ouL During the period between the tum of the century and containing fresh eggs, dried milk, pasteurized milk which WilS 1940, typhoid fever was the major milk-borne disease. contaminated after heat processing, or either cheese made from Then after precipitous decline in two decades, no milk raw milk or cheese in which starter activity was inhibited during borne outbreaks of typhoid fever were reported during the its manufacture. sixties, the seventies, and early eighties, Streptococcal in fections (scarlet fever and septic sore throat) were the sec ond-most common cause of outbreaks reported during the first three decades of the 1900s, but such reports dwindled Throughout the years, epidemiologists, physicians and to extinction in the 1940s. Diphtheria, which accounted for sanitarians in the United States have expressed concern a smaller share, declined until reports ceased in 1946, about milk-borne and milk-product-borne diseases (8,31- As reports of outbreaks of these diseases waned, reports 40,54.58,115). Frequencies of reported outbreaks of of outbreaks of staphylococcal intoxication, nontyphoidal milk-borne and milk-product-borne disease during the salmonellosis and diseases of unknown etiology gathered 1900-1981 period are shown in Fig. 11. Secular trends in impetus. Milk products (ice cream, dry milk, and cheese) milk-borne (and milk-product-borne) diseases show the were the usual vehicles of these outbreaks. (The large number of outbreaks reported in 1956 was due to 27 out breaks of staphylococcal intoxication from dried milk.) IData in the Figure was extracted from the reviews by Trask (lIS). Salmonellosis and gastroenteritis of unknown etiology Armstrong. and Parran (8). reports from the U.S. Public Health Service. Office of Milk Investigations (l925-1936). Domestic Quaral!line Division. dominated the 1970s. In the last of the 1970s, campylobac Sanitation Section (1937-1939). State Relations Division, Sanitation Sec teriosis began to emerge as an important raw milk-borne tion (1940-1943). Engineering Division. Milk and Food Section (1944- disease. The large percentage of outbreaks of unknown 1946). Division of Sanitation, Milk and Food Branch (1947-1949); Na etiology reported in the last few decades, almost certainly tional Office of Vital Statistics-Reports by Dauer (31-40)-and surveil lance reports, reviews in Morbidity and Mortality Weekly Reports. and included undetected outbreaks of campylobacteriosis. The annual summaries about foodborne diseases by the Centerl s) for Disease relatively long gap between the report by Levy (75) and the Control (I961-198Jj (22). later reports reflects the difficulty to recover Campylobac-

JOURNAL OF FOOD PROTECTION. VOL. 46. JULY 1983 638 BRYAN

o Raw milk or cream 70 BI Certified raw milk Ili1 Milk, unspecified; most likely raw milk £Xl Pasteurized milk IDJ Oried (powdered) milk 51 Cheese 60 mMilk products. unspecified; malted milk; milk formula mHuman milk P»J Butter • Ice cream, eggs frequently added mJ Unknown Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 50

en CIl en ~ ....U 0 Q) 40 ..c E :::l 2

Year

10ata on specific vehicles, unavailable for the year 1950 20ata incomplete

Figure 1. Secular trends of milk-borne diseases by specific vehicle and year of occurrence, United States. ter jejuni until laboratory procedures improved and con for most of the ice cream-associated outbreaks (Fig. 1) dur cern about the problem was generated. ing the 1909 to 1925 period; staphylococcal intoxication predominated from 1930 through the 1950s. Of the remain The types of milk and milk products that were impli ing outbreaks, cheese and raw milk (including certified raw cated as vehicles of outbreaks of specific milk-borne dis milk) were often implicated as vehicles. The listing "milk, eases during the 1970s are shown in Table 2. Ice cream, unspecified" refers, most likely, to raw milk; but, the re usually homemade and containing eggs, was the vehicle of ported data do not so specify. The pasteurized milk and most of the outbreaks (usually of salmonellosis) reported chocolate milk were either improperly pasteurized or be during this period. Therefore, many of these should proba came contaminated after being pasteurized. [For informa bly be omitted from the list because they would be better tion on recent milk-borne diseases that have occurred in classified as egg-borne diseases. Typhoid fever accounted Canada, see data from the Health Protection Branch (4).]

JOURNAL OF FOOD PROTECTION, VOL. 46, JULY 1983 MILK-BORNE DISEASE 639

TABLE 1. Percent of reported milk-borne diseases by decade. 1900- 1910- 1920- 1930- 1940- 1950- 1960- 1970- 1980- Disease 1909 1919 1929 1939 1949 1959 1969 1979 1982

Arizonosis Botulism <1 1 Brucellosisa 8 4 9 1 Campylobacteriosis <1 3 40 Diphtheria 8 2 4 1 Escherichia coli diarrhea Haverhill fever <1 Hepatitis A <1 2 Histamine intoxication Iron intoxication

Milk sickness <1 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 Petroleum poisoning 2 Poliomyetitis <1 <1 <1 Pseudomonas aeruginosa infection infections 14 15 18 27 8 Toxoplasmosis Typhoid fever 78 80 68 50 17 3 Yersiniosis

alndividual cases not included, see Table 5.

MILK·BORNE DISEASES OF that of the 1971-1974 episode. This investigation impli CONTEMPORARY IMPORTANCE cated certified milk from the same dairy. Over 100 isola tions of Salmonella, including S. dublin, were made from Salmonellosis milk produced by the dairy, and several hundred isolations Milk-borne salmonelloses are common in those regions of Salmonella-including S. dublin-were made from cattle of the world in which milk is neither pasteurized nor in the dairy's herds (30). (Outbreaks of campylobacteriosis boiled. Many outbreaks of salmonelloses in the United also have been associated with milk from this dairy.) States from 1965 to the present that have been summarized Increased isolations of Salmonella newbrunswick led either in the professional literature or in official surveil epidemiologists to make epidemiologic associations be lance reports are listed in Table 3. Either, raw milk or cer tween ingestion of milk prepared from instantized dried tified raw milk has usually been the vehicle, but pas milk and 29 cases of salmonellosis (mostly infants) from teurized milk, powdered milk and Cheddar cheese have 17 states (28). The same serotype was isolated from three also been implicated. Marth (79) has reviewed salmonellae lots of the milk produced at a single processing plant. The and salmonelloses associated with milk and milk-products. milk was heated during processing, but without either ther Certified raw milk produced at a single large dairy was mostatic or time controls to ensure pasteurization. The ingested by 74 of 79 persons who became ill between April milk was then concentrated by a series of vacuum pan 1971 and March 1974 (70). Salmonella dublin was isolated evaporators before spray drying. The milk powder was from all of the ill persons, 37 of whom had underlying de then instantized (steam is applied to the powder and the bilitating conditions. Fifty-nine (75%) of these persons agglomerate is dried). Samples of the product taken at vari were hospitalized and 16 (20%) died. S. dublin was iso ous stages of processing indicated that the product most lated from a sample of raw milk from a California dairy likely became contaminated in the instantizer. This piece from which the ill persons obtained their milk, and sal of equipment had several rough-surface welded joints, monellae (but not S.dubUn) were isolated from cows of the numerous crevices and open seams, and contained numer dairy's herds. Milk from this same dairy was implicated as ous thin rods and divider plates. These all contributed to the vehicle in two other outbreaks in 1958 and in 1964. build-up of caked powder in areas inaccessible to cleaning. Investigation of a recurrence of S. dublin infections in The instantizer was wet-cleaned only weekly. California during 1977-1979, disclosed a pattern similar to An epidemiologic investigation of an outbreak of Sal-

JOURNAL OF FOOD PROTECTION. VOL. 46. JULY 1983 640 BRYAN

TABLE 2. Milk and Milk products reported as vehicles of disease outbreaks, 1970-1979. ,::: 0 .~ 0) u '" ,::: " 0 ':;i ell 0 ~ ,::: .~ .~ u .5 0 '6 '2 ';:: 0 ';;] -; ell u '-' '15 ,5 ..sl "0 .::1 0- '2 u '"or> '{ii'" '" « § 0 ,::: .::> ~ Product § >-. '".... ,::: '" .!l '8 0 ..<:i :S - .( iX:I ::c" !-< ~ ::2 ~ E-

Raw milk 3 2 7 Milk, unspecified 2 8 12 Certified milk 2 3 Pasteurized milk 2 2 Chocolate milk

3 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 Milk fonnula 1 Powdered milk 2 1 3 Butter 2 3 Whipped butter Whipped topping Cheese 10 14 Sour cream 1 Cheese puff Milk shake mix 2 2 Ice cream 26a 1" 12a 40a Unspecified, dairy product 1 2 Human milk 2 2 aEgg-borne rather than milk-borne in many outbreaks.

TABLE 3. Milk-borne arul milk-product-borne outbreaks of salmonellosis in the United States. 1965-1981. Year Product State Number of References cases Serotype

1965 Raw milk Washington 2 typhimurum (4) 1965-1966 Powdered milk Nationwide 29+ newbrunswick (29) 1967 Raw milk Washington 40+ typhimurum (53) 1971 Human milk Illinois I kottbus (74) 1971-1975 Certified raw milk California 44-1- dublin (70,124) 1975 ' 'Pasteurized milk Louisiana 43+ newport (15) 1977 Raw milk Kentucky 3 typhimurum (82) 1977 Human milk Maine 7 kottbus (99) 1977-1978 Certified milk California 57 dublin (30) 1978 ' 'Pasteurized milk' , Arizona 23+ typhimurum (46) 1979 Powdered milk Oregon 1+ agona, typhimurum (59) 1980 Cheddar cheese Colorado 339+ heidelberg (52) 1980-1981 Raw milk Washington 125 dublin (89) 1981 Certified raw milk California 1+ saint paul (20) 1981 Raw milk Montana 59 typhimurum (41 ) 1981 Raw milk 14 dublin (5)

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TABLE 4. Milk-borne and milk-product-borne outbreaks of campylobacteriosis in the United States . . ---~- ..-- ..-- ..-- .. --.--. Year Product State Number of References Cases 1946 Raw milk Illinois 357 (75) 1965 Raw milk Oregon I (67) 1976 Certified raw milk California 4 (110) 1978 Raw milk Colorado 3 (14) 1979 Grade A raw chocolate milk New Mexico 41 (30) 1980-81 Raw milk Oregon 52 ( 111) 1981 Raw Milk Kansas 60+ (114) 1981 Certified raw milk Georgia 50 (26) 1982 Certified raw milk California monella heidelberg infections, which affected at least 339 was either raw milk or certified raw milk. Three of the out

persons, showed statistically significant association be breaks affected farm families only. The other out Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 tween ill persons and their having eaten foods containing breaks were associated with milk that had been bottled in Cheddar cheese in Mexican-style restaurants (52). The dairies. cheese was from a single lot produced by a single man Between 1978 and 1980 in England and Wales, raw ufacturer. The milk used in the manufacture of the cheese milk was implicated in 14 documented outbreaks of cam had been held unrefrigerated for 3 d in insulated tanks be pylobacteriosis, which affected at least 3,553 persons fore it was pasteurized. The effectiveness of the pasteuriza (l00,109). In one of these outbreaks, 2,500 school chil tion process was not monitored. After pasteurization, the dren became ill during a 3-week period (69). milk was filtered; a violation of the U.S. Public Health The largest number-648-of cases in a common-source Service Milk Ordinance and Code, 1978 (118). Informa outbreak ever recorded in Scotland was caused by Cam tion on culturing, curd formation, and ripening was not re pylobacter transmitted by raw milk (122). In another Scot ported. tish outbreak, Campylabacter jejuni was isolated from In England and Wales from 1969 to 1976, either milk or stools of 148 patients, from 57 asymptomatic persons, and cream (usually raw) was implicated in 60 outbreaks of sal from a milk filter, during an investigation of an outbreak monelloses (117). Three percent of milk sold in England that followed ingestion of unpasteurized milk (91). and Wales did not receive a heat treatment. In Canada, an outbreak of campylobacteriosis that af In Scotland, where 10% of the milk is sold without heat fected 27 persons occurred at a camp. Raw milk purchased treatment, 29 milk-borne outbreaks of salmonelloses, af from a local dairy was found to be contaminated by Cam fecting at least 2,428 persons, occurred between 1970 and pylobacter (83). 1979 (103). During this period, one outbreak that affected A wide variety of warm-blooded vertebrates have been at least 700 persons was reported (104). Unpasteurized infected by C. jejuni. This organism has been isolated from milk was identified as the vehicle. the intestinal tract and feces of man, cattle, goats, sheep, Another outbreak of salmonellosis in which more than pigs, chickens and some wild birds. It has also been iso 500 persons were affected was reported from South Au lated from poultry meat, salt water and fresh water (46). stralia (102). Bottled, unpasteurized milk was implicated. Rapid cooling of milk should prevent growth of C. jejuni, In Trinidad, approximately 3,000 persons developed and either thorough cooking or pasteurization can be ex Salmonella derby gastroenteritis after they ingested one of pected to kill it. seven different brands of powdered milk, which had been packaged at a single processing plant on the island (1 23). Staphylococcal food poisoning Cows usually become infected with salmonellae from Raw milk from individual cows or goats has been impli either the feedstuffs they eat or from contaminated sources cated as a vehicle in numerous outbreaks of staphylococcal in their farm or barn environment. They also shed these or intoxication before the practices of rapid chilling of milk ganisms in their feces. Their udder or hide may become and pasteurization became common (JJ , 14,85). Pas contaminated with salmonellae when they wade in streams teurized milk that has become contaminated after being or lie on fecally-soiled litter or ground. Milk can become heat treated has been a vehicle on rare occasions (21,63). contaminated from such sources. Rapid chilling of raw Spray-dried milk has been the vehicle for staphylococcal milk inhibits multiplication of salmonellae, however, and enterotoxin at least two outbreaks (6,7). pasteurization by approved procedures kills large numbers Cheese has been a vehicle for staphylococcal enterotoxin of Salmonella. in several outbreaks (2,18,65,66,77,82,129). Staphylococci multiplied in the milk and elaborated en Campylobacteriosis terotoxin before fermentation commenced. Milk-borne campylobacteriosis has been reported in the Ice cream has also been implicated as a vehicle of United States, England and Wales, Scotland and Canada. staphylococcal enterotoxin in several outbreaks The outbreaks that have been reported in the United States (44,60,88,125). Usually, ice cream mix was contaminated are summarized in Table 4. The vehicle in all outbreaks at the time of preparation and the staphylococci multiplied

JOURNAL OF FOOD PROTECTION, VOL. 46, JULY 1983 642 BRYAN

TABLE 5. Cases of brucellosis associated with ingestion of domestic and foreign milk and milk-products (usually cheese) by year (23).

Year Total Cases related to unpasteurized milk or milk-products (cheese)

1971 171!190b 5 (2.9) 21 (12.3) 26 (\5.2) 1972 1791184 3 (1.7) 10 (5.6) 13 (7.3) 1973 166c 2 (1.2) 31 (18.7) 33 (19.9) 1974 235/246 7 (3.0) 14 (5.9) 21 (8.9) 1975 309 8 (2.6) 16 (5.2) 24 (7.8) 1976 271 6 (2.2) 18(6.6) 24 (8.8) 1977 232 4 (/.7) 11 (4.7) 15 (6.4) 1978 161 9 (5.6) 5 (3.1) 14 (8.7) 1979 212 10 (4.7) 28 (13.2) 38 (17.9) Total 1936/1971 54 154 208 (10.7) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 apercent of total case reports. bCases reports/total cases reported. cCase reports.

before and during the long period of cooling before the mix TABLE 6. Countries from which dairy products were processed froze. Butter has also been implicated as a vehicle that were vehicles of Brucella, 1971-1979 (23). (50,92,105,126). Country Number Staphylococcus aureus is frequently found on cows ud of cases ders and in their teat canals. It is a common cause of mas Mexico 115 titis. From these sources, staphylococci reach milk readily. United States 54 Milk and milk-products can also be contaminated by either Italy 12 hands or nasal discharges of dairy or processing plant Greece 5 workers. Staphylococci must multiply to produce sufficient Unspecified, Latin American countries 5 enterotoxin in foods to cause illness. Unspecified, European countries 3 India 2 Brucellosis Portugal 2 Milk-borne and milk-pro duct-borne brucellosis is a con Unspecified, Asian countries 2 Costa Rica tinuing problem in the United States. Table 5 summarizes France reports that implicated milk and milk-products as the most Germany probable sources of infection for approximately 10% of the Iran known cases during the period 1971-1978 (23). Most of Kenya the dairy product-associated cases have a history that in Tanzania cludes ingestion of milk products, usually raw goat-cheese, Thailand produced in other countries. The countries in which these Unspecified, Middle-East country products were produced are listed in Table 6. Examples of Total 208 outbreaks in which Mexican-prepared raw goat-cheese was implicated are described (16,48,106.128). school children became ill after they ingested raw milk Milk-producing animals-cattie, goats, sheep, and buf which had been held at room temperature in a home for faloes-can be reservoirs of brucellae. This organism has a about 4 h. propensity for localizing in the uteri of females that are An outbreak of yersiniosis was discovered in New York pregnant and in the mammary glands of lactating females. State during an investigation to uncover the reasons for an Thereby, infected animals can for years shed brucellae in unusually high incidence of appendectomies in children their milk. under 18 years old (12). The illness that caused the acute Milk can also become contaminated with brucellae syndrome suggestive of appendicitis was caused by Y. en through contact with infected organs or fomities or from terocolitica. Chocolate milk was the epidemiologically im excreta or dust. Brucellae are quite resistant to environ plicated vehicle. Chocolate syrup had been mixed and mental stress. They survive in raw milk several hours, and added to milk after pasteurization. in cheese several weeks, but usually not as long as a year. A report has been made of a Yersinia pseudotuberculosis They can survive in frozen products a few years. [See septicemia and post-diarrheal, hemolytic, uremic syn Bryan (19) for a review of Brucella and brucellosis.] drome in a I5-month old child (93). This child and his mother both became ill 1 d after they ingested goat's milk Yersiniosis that had not been pasteurized. Raw milk was suspected as a vehicle in an outbreak of Recently, Y. enterocolitica was responsible for an out Yersinia enterocolitica enteritis in Canada (42). Fifty-eight break affecting 148 persons from three states; most were

JOURNAL OF FOOD PROTECTION, VOL. 46, JULY 1983 MILK-BORNE DISEASE 643 hospitalized, 17 underwent appendectomies, one of these either milked cows or handled milk or milking equipment persons died. It was estimated that 857 cases may have oc and were considered as the source. curred. Pasteurized milk was the implicated vehicle; details Dried milk has also been implicated as a vehicle (1,94). about the source of contamination were discovered (73). Canned milk that had been opened and diluted the evening An investigation revealed that unsold milk was returned to before serving was responsible for three outbreaks that in the dairy and fed to hogs. At the hog farm, milk crates cluded 835 cases of tonsillitis and scarlet fever (l09). were stored on the ground down slope from hog pens. Crates were returned to the dairy and washed, but the Diphtheria washing failed to remove some of the mud in the triangular Before pasteurization became a common practice, many configurations on the undersurface of the crates. Aulisio et diphtheria epidemics were epidemiologically associated al. (10) hypothesized that the mud contaminated the bot with raw milk. These outbreaks have been summarized by tom of the milk containers when they were put into the various authors and reviewed by Bryan (19). In many of crates; tops of the containers could have been contaminated the outbreaks, implicated milk came from farms on which dairy workers were either carriers of Corynebacterium

during stacking. Animals are frequently infected with Y. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 enterocolitica. Water in streams, often contain this or diphtheriae or they suffered from clinical manifestations of ganisms. Milk can become contaminated from these diphtheria. In other outbreaks, implicated milk came from sources (68,120). cows that had superficial ulcers on their udders. Ice cream has also been implicated as a vehicle (19). No milk-borne outbreaks of diphtheria have been reported in the United States since 1948. MILK-BORNE DISEASES OF HISTORIAI, INTEREST Tuberculosis Typhoidfever Mycobacterium bovis can be transmitted by raw milk. Before the practice of pasteurization and at a time before The ingested organisms penetrate the orophamx and intes farm sanitation was commonplace, there were frequent re tine and give rise to lesions in the cervical lymph and ports of outbreaks of milk-borne typhoid fever. Reviews of mesenteric nodes. From these sites, they are diseminated to milk-borne typhoid fever outbreaks have been made bones and joints resulting in kyphosis, a condition in which (8,19,107,115). the afflicted are commonly called hunchbacks. In recent During investigations several sources of contamination years in the United States, the incidence of alimentary were found: persons who had typhoid fever, who were car tuberculosis has been low; however, in some other coun riers of Salmonella typhi or who nursed sick persons in tries, reports of this disease are much more common. their family either milked cows or handled milk or milk Strong circumstantial evidence has incriminated raw utensils or containers on milk-producing farms or in milk milk as a vehicle for transmitting M. bovis to man; out shops. Well water used to wash and rinse utensils and breaks have been reviewed (19). Factors that influence equipment was another source of contamination. Bottles transmission of M. bovis are: (a) incidence of infection in returned from homes of sick persons were suspected to be cows, (b) opportunities for contamination with M. bovis the sources of contamination on a few occasions. More re and the presence of and quantity of this organisms in milk, cently, in Trinidad, ice cream was implicated as a vehicle (c) whether or not milk is boiled or pasteurized and (d) the of S. typhi in an outbreak affecting 132 persons (106). milk-drinking habits of the populace. Large quantities of tubercle bacteria can readily reach milk of infected animals because both the mammary gland Streptococcal infections and the lungs discharge into the same canalicular system. Outbreaks of milk-borne scarlet fever and septic sore They can also reach milk from feces, which may dry upon throat were frequent in the United States (and no doubt, and cling to the udder, tailor flanks of cows. Contamina elsewhere) before pasteurization of milk became nearly tion can come also from infected udders and from air-borne universal. These outbreaks are reviewed (8,19,115). Sev organisms that have orginated in respiratory discharges. eral were traced to cows with either mastitis or lesions on Tuberculin testing and slaughter of reactors has almost their teats or udders. The cows usually acquired group A eradicated tuberculosis from dairy cows in the United streptococcal mastitis through contact with a human car States. So contamination of milk from animal sources is rier. Thereafter, they discharged large numbers of strep quite rare today. Furthermore, the pasteurization process tococci in their milk. If this milk was not pasteurized, out was initially designed to kill large numbers of M. bovis breaks resulted. (71). Outbreaks of scarlet fever and septic sore throat were also attributed to primary cases working at a farm or in Shigellosis milk shops and either milking cows or otherwise handling A few outbreaks of shigellosis have been associated with milk or milk equipment. For instance, milk was contami milk and cheese. These have been reviewed (19,107). The nated by a worker who, while suffering from an acute sore implicated milk or milk product was contaminated by a throat, bottled the milk and capped the bottles. In some human carrier, and the milk was frequently held for several outbreaks, persons who nursed sick persons in their family hours without refrigeration.

JOURNAL OF FOOD PROTECTION, VOL. 46, JULY 1983 644 BRYAN

Milk sickness was isolated from rectal swabs taken from 5 of 25 infants, Grazing animals have developed trembles as a result of from the pump and from the vessel in which the pump had eating leaves and stems of white snakeroot (Eupatorium been disinfected. rugosum) or rayless goldenrod (Aplopappus heterophyllus or lsocoma wrighii). Animals having this condition elimi Listeriosis nate tremetol ( a higher alcohol which is toxic to the liver) Foodborne transmission of listeriosis has not been con in their milk. Milk sickness is manifested by weakness, firmed in humans, but raw milk has been suspected to be prostration, loss of appetite, abdominal pain, nausea, vom a vehicle. For example, Potel (92) told about a woman iting, muscular tremors and coma. It is frequently fatal. who had drunk milk from a cow with atypical mastitis and Although, this disease is rare today, numerous cases and later gave birth to twins prematurely. The infants had mul deaths occurred among early settlers, particularly in the tiple tumors composed of granulation tissue, Listeria midwest, before land was cleared. Significant to the occur monocytogenes was isolated from the infants and from the rence was that cattle foraged wooded areas and were cow's milk. In several cases of listeriosis that occurred in

milked only sporadically (81). Halle, Germany, raw milk was suspected as the vehicle, Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 and in other cases, suspicion was cast on cream, sour milk, DISEASES RARELY REPORTED and cottage cheese (101). AS BEING MILK·BORNE Listeriosis has been observed in cattle; udder infections Botulism due to L. monocytogenes have been described, and this or Milk has been implicated as the vehicle in two outbreaks ganism has been found in milk. [See the review by Bryan of botulism involving 5 cases. Outbreaks of botulism have (19) for further discussion and references.] infrequently been traced to cheese (84). Seven cheese-as sociated outbreaks involving 21 cases, 9 of whom died, Clostridium perfringens enteritis have been reported in the United States (25,81). Cottage In 1933, a report incriminated Clostridium perfringens cheese was the vehicle in three outbreaks, cheese curd in as the cause of an outbreak of fever and flatulent diarrhea one, Neufchatel in one, Liederkranz cheese spread in one, in infants (87). Although, the syndrome is not typical of C. and an unspecified cheese in one. In 1974, an outbreak that perfringens enteritis, the hypothesis is interesting because affected 11 persons who ate a commercially-prepared, C. perfringens can readily reach milk and its spores can plastic-packaged, cheese spread containing dehydrated on survive pasteurization. The heat of pasteurization would ions was reported from Argentina (43). Yogurt has been heat-activate the spores and reduce populations of competi suspected of being a vehicle (5). tive organisms. Amino acids and growth factors necessary to sustain growth of C. perfringens are constituents of Escherichia coli enteritis milk, and this organism grows in milk causing a stormy Camembert and Brie cheese from France were vehicles fermentation. Refrigerated storage of heat-treated milk in an outbreak of diarrhea caused by Escherichia coli 0 would, however, prevent outgrowth of spores and multipli group 124, a non-lactose fermenter that reacted to Shigella cation of the vegetative cells. antiserium (116). More than 100 episodes-387 cases-were eventually traced to this source (78). A milk-borne out Bacillus cereus gastroenteritis break among children has been reported in the U.S.S.R. Milk and ice cream have been implicated as vehicles in (80). outbreaks of gastroenteritis caused by Bacillus cereus. [See Man and other animals shed large numbers of E. coli in Gilbert (61) for a more complete discussion of the role of their feces. These organisms have been recovered from the B. cereus as a foodborne pathogen and for references.] milk of apparently healthy animals, from those that had mastitis and from samples of milk and cheese in retail Haverhill fever stores. A few milk-borne outbreaks of Haverhill fever have been reported (90). In one outbreak, Streptobacillus monilifor mis, the etiologic agent of rat-bite fever, was isolated from Pseudomonas aeruginosa enteritis most of the cases and serum antibodies were demonstrated Pseudomonas aeruginosa, which produces a heat-labile in the other cases. All persons who were affected had enterotoxin, has, on rare occasions, been implicated as an drunk raw milk bottled from the same dairy. A cow in the etiologic agent of milk-borne disease. In an outbreak invol herd from which the implicated milk came had a healed le ving 409 cases, infants were severely affected and 9 died sion, suggestive of a rat-bite, on one teat. The outbreak (49). Contaminated pasteurized milk was epidemiologi ended after the dairy began to pasteurize its milk. cally implicated as the vehicle. During an investigation of the plant that had processed the milk, P. aeruginosa was Qfever recovered from a rag that had been used to wrap a pipe Coxiella burnetii is sometimes found in raw milk, and joint. Drippings from the rag fell into the pasteurized milk. some investigators have implicated raw milk as a vehicle In another outbreak, newborn infants vomited and had (19). Most of the evidence implicating milk as a vehicle, diarrhea after being fed human milk that had been obtained however, is the greater frequency that compliment-fixing by a breast-pump (113). The same strain of P. aeruginosa antibodies are found in the sera of persons who drank raw

JOURNAL OF FOOD PROTECTION. VOL. 46, JULY 1983 MILK-BORNE DISEASE 645 milk, than the frequency with which these antibodies are Histamine and tyramine in cheese are usually degraded found in the sera of persons who did not drink raw milk. in the body by monoamine oxidase. Certain drugs, how Epidemiologic evidence presented by Brown et al (17) ever, inhibit this enzyme. Persons who have taken one of suggested that ingestion of raw milk from infected cattle these drugs, have experienced attacks of hypertension resulted in a common-source outbreak; contact with ani shortly after ingestion of cheese; cerebrovacular accidents mals, farms, dust and insects were ruled out as possible have been reported (/3). routes of transmission. Ingestion of raw milk that con tained C. burnetii by human volunteers, however, has not Arsenic poisoning caused illness (51,73). In the summer of 1955, 12,131 children in western c. burnetii can survive vat-pasteurization at 61.7°C Japan were poisoned because they ingested arsenic-con (143°F) for 30 min; pasteurization at 62.8°C (l45°F) for 30 taminated dry milk. One-hundred-thirty of these children min or at 71. 7°C (161°F) for 15 sec is adequate to kill this died. The arsenic reached the milk from an inadequately organism. purified "sodium phosphate" stabilizer which was used in the manufacturing process. Fourteen years later, survivors Hepatitis A had a higher rate of physical and mental complaints than a Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 Just about any food that is handled by a person who is control group (127). shedding hepatitis A virus can become a vehicle for this or ganism. Raw milk from a small dairy was implicated in an ROLE OF MILK outbreak in Geiorgia (86). Cream used in a fruit salad and AND MILK PRODUCTS AS VEmCLES in sherry trifles (prepared by a pastry-cook who was in the incubation phase of hepatitis A) was the vehicle of another Raw milk outbreak (27). Microorganisms that reach a cow's teats can enter them through their openings and migrate to the interior. The Poliomyelitis types and numbers of microorganisms that invade the Raw milk-associated outbreaks of poliomyelitis have udder by this route vary from animal to animal and even been reported. [See Cliver (27) for a review.] In one of among the quarters of the same udder. Such invasion can these outbreaks, all cases had drunk milk from a small occur even in healthy animals. Micrococci, staphylococci, dairy. At this dairy, a 16-year old milker handled milk for streptococci and diphteroides usually predominate among 4 d while in the acute phase of poliomyelitis (72). the microbial flora of the teat and udder. Mastitis, an inflammitory disease of mammary tissue, Russian spring-summer encephalitis (Disphastic milk can lead to development of millions of pathogens in the in fever) fected quarter and the discharge of large numbers of them Ingestion of raw milk and of cheese made from raw milk to milk. Milk-borne pathogens that can cause mastitis, in from tick-infested sheep and goats has resulted in en clude, S. aureus, streptococci, E. coli, P. aeruginosa, C. cephalitis. Reports of this disease have been limited to the perfringens. streptococci, corynebacteria and mycobac U.S.S.R. (96). teria. Animals infected with other pathogens, such as Toxoplasmosis Brucella spp., C. burnetii and M. bovis, can shed them, The ingestion of raw milk from goats and cattle raises too, in milk. the possibility of transmission of Toxoplasma gondii; ani Microorganisms from soil, litter, feed, water, feces and mal-to-animal transmission by milk has been demonstrated other items in a farm environment commonly contaminate (57). A 7-month old child who had a history of being fed the surface of the udder and teats and the hair and skins of almost exclusively on raw goat's milk developed toxoplas cows and goats. From these sources they can get into milk mosis (98). Goat's milk is sometimes prescribed for infants during milking. Sporeformers such as B. cereus and C. who cannot tolerate cow's milk. perfringens can reach milk from soil and litter. Salmonel lae as weB as sporeformers can be transmitted to milk from Histamine intoxication and hypertension feed. Yersinia and Campylobacter may reach milk from Histamine is a powerful capillary dilator; it causes in contaminated water in streams and ponds. Salmonella, tense headaches, nausea, vomiting, facial flushing, burn Campy/obacter, Yersinia, enterococci, E. coli and C. per ing throat, thirst, swelling of lips, and urticaria. Histamine fringens can reach milk if feces of infected animals reach intoxication after ingestion of cheese has been reported milk either directly or from contaminated exteriors of (45,1 19). Histamine was suspected to be the cause of an cows. outbreak affecting 38 cases in persons who ate either Equipment used for milking, filtering, cooling, storing cheese crepes or onion soup on which cheese had been or distributing milk are also important sources of microor placed (24). Histamine can be formed in cheese when his ganisms. This situation is aggravated if the equipment is tidine, which is often found in cheese, is decarboxylated. not properly cleaned and sanitized after use. Milk residues Many Enterobacteriaceae, enterococci, and Lactobacillus left on equipment and utensil surfaces provide nutrients to casei produce decarbocylase. [This topic has been re support growth of many microorganisms, including patho viewed (19,97,121).] gens.

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Farm workers who either milk animals or handle milk, those organisms that reach raw milk may be found in the or milking or storage equipment, can contribute additional cheese. Brucellae that reach cheese and survive the cheese organisms to the milk. Such contamination has resulted in making process have caused several cases of brucellosis. numerous milk-borne outbreaks of typhoid fever, Salmonellae, also frequently reach milk, and they can diphtheria, septic sore throat, scarlet fever, shigellosis, grow during cheese making and persist during ripening of staphylococcal enterotoxicosis, hepatitis A and certain cheeses for 60 days or more. poliomyelitis. Slow acid production (low milling acidity) by a starter culture can allow staphylococci to grow and perhaps pro Certified milk duce enough entertoxin to cause disease if process temper Certified milk is raw milk which is produced under strict tures are favorable during curd formation. If the pH of the conditions that comply with standards of sanitation adopted curd is higher than normal (5.2-5.3), growth of by the American Association of Medical Milk Commis staphylococci can even continue during pressing, but sel sions (3). These procedures were originated in the early dom afterwards. Their numbers decline rapidly during ri

1800's to produce safe milk before pasteurization became pening. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/46/7/637/1656112/0362-028x-46_7_637.pdf by guest on 27 September 2021 common. In spite of these precautions, including produc E. coli hazards are of particular concern in soft and tion of milk with low bacterial counts, certified milk has semisoft surface-ripened cheeses. E. coli can multiply in been implicated as the vehicle in several milk-borne out soft and semisoft surface-ripened cheses when there is lack breaks throughout the years; including, the last few years. of acid production and low salt concentration in the interior during the early stage of ripening (56). Furthermore, this Pasteurized milk organism can grow on surfaces of these cheeses during the Pasteurization or more severe heat treatments applied to development of the mold matt, if temperatures are suffi raw milk is the only way to ensure that pathogens likely to ciently high (55). be present are killed and that the milk is safe. When pas C. botulium sometimes reaches milk because of soil or teurized milk has been implicated as a vehicle, further in dust contamination. It's spores survive pasteurization. C. vestigation has shown that there was either a process fail botulium can multiply 'in lightly salted cheeses that have ure or post-pasteurization contamination. Pasteurization, relatively high pH values (resulting from faulty starter cul more than improved dairy sanitation practices, has resulted ture activity) and a closed structure, which is conducive to in the dramatic decrease in milk-borne diseases during the anaerobiosis. past 35 years. Adequate heat treatment of milk and normal starter ac Ice cream tivity are the best preventives of cheese-borne disease out breaks. Prolonged ripening also results in a decrease in, When raw milk was frequently used to make ice cream, but not necessarily freedom from, pathogens. outbreaks were common. Eggs, not milk, have been the source of salmonellae in recent outbreaks of salmonellosis that have been transmitted by ice cream (63). Whatever REFERENCES their source, pathogens that are incorporated into ice cream can survive in the frozen product many months. 1. Allen, R. F., and Baer, L. S. 1944. Outbreak of septic sore throat Use of pasteurized milk in ice mixes, either omission of due to reconstituted powdered milk. J. Amer. Med. Assoc. eggs or use of pasteurized egg products in these mixes, and 124:1191-1193. 2. Allen, V. D., and W. D. Stovall. 1960. Laboratory aspects of rapid freezing of these mixes, minimize the possibility of staphylococcal food poisoning from Colby cheese. J. Milk Food ice cream becoming a vehicle of sufficient numbers of Technol. 23:271-274. pathogens to cause illness. 3. American Association of Medical Milk Commissions. 1976. Methods and standards for the production of certified milk. Amer. Dry milk Assoc. Med. Milk Commissions, Alpharetta, Georgia. 4. Anderson, H, W. and D. R. Peterson. 1965. Salmonella Dry milk has been the vehicle of outbreaks because (a) typhimurium infection traced to raw milk, Salmonella Surveillance it was not pasteurized before drying, (b) it was held at tem Rep. No. 49, Center for Disease Control, Atlanta. peratures that permitted the growth of S. aureus and the 5. Anderson, H .. J. Ballard, J. Lewis, J. Allard, B. J. Edmundson, production of entertoxin before drying, or (c) product ac and Centers for Disease Control. 1981. Salmonella dublin as cumulation and persistence of moisture in an instantizer, sociated with raw milk-Washington State. (u.S,) Morbidity Mor tality Week. Rept. 30:373-374. led to multiplication of salmonellae. Pasteurizing, hot 6. Anderson. P. H. R., and D. M. Stone. 1955. Staphylococcal food holding at not less than 65°C (149°F) in balance and surge poisoning associated with spray-dried milk. J. Hyg. 53:387-397. tanks, and cleaning equipment surfaces that contact the dry 7. Armijo, R., D. A. Henderson, R. Timothee, and H. B. Robinson. product to prevent product from accumulating in crevices 1957. Food poisoning outbreaks associated with spray-dried milk and dead ends, and to keep moisture from reaching the an epidemiologic study. Amer. J. Public Health, 47:1093-1100. 8, Armstrong, C, and T. Parran, Jr. 1927, Further studies on the im dried product, are essential to prevention of outbreaks as portance of milk and milk products as a factor in the causation of sociated with dried milk. outbreaks of disease in the United States. Public Health Rep. Supp\. No. 62:1-8: Cheese 9. Arnold, S. H., and W. D. Brown. 1978. Histamine (?) toxicity Unless, the milk used to make cheese is pasteurized, from fish products. Adv. Food Res. 24:113-154,

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62. Gunn, R. A. and G. Markakis. 1978. Salmonellosis associated with Hooper Foundation, UniVersity of California, San Francisco Medi homemade ice cream. An outbreak report and summary of out cal Center. breaks in the United States in 1966 to 1976. J. Amer. med. Assoc. 85. Minor, T. E. and E. H. Marth. 1976. Staphylococci and their sig 240: 1885-1886. niticance in foods. Elsevier Scientific Publishing Co., Tokyo. 63. Hacker. 1. F. 1939. Outbreak of Staphylococcus milk poisoning in 86. Murphy, W, J., L. M. Petrie, and S. D. Work. 1946. Outbreak of pasteurized milk. Amer. J. Public Health. 29:1247-1249. infectious hepatitis apparently milk-borne. Amer. J. Public Health. 64. Health Protection Branch. 1976-1981. Foodborne and waterborne 36: 169-173. disease in Canada. Annual summary 1973-1977. Health and Wel 87. Nelson, C. I. 1933. Flatulent diarrhea due to Clostridium welchii. fare Canada, Ottawa, Ontario. 1. Infect. Dis. 58:89-93. 65. Hendricks. S. L., R. A. Belknap, and W. J. Hausler, Jr. 1959. 88. New York State Department of Health. 1940. Gastroenteritis traced Staphylococcal food intoxication due to Cheddar cheese. 1. to homemade ice cream. Health News 17:104. Epidemiology. J. Milk Food TechnoL 22:313-317. 89. Nolan, C. M., H. W. Anderson, and D. E. T. Hoyt. 1981. Sal 66. Hobbs. B. C. 1964. Food poisoning: Observations on sources of monella surveillance pays off. Epi-Iog July/August 1981. Seattle salmonellae, Clostridium peifringens and staphylococci. Ann. Inst. King County Department of Public Health, Seattle. Pasteure Lille. 15:31-41. 90. Place, E. H., and L. E. Sutton, JI. 1934. Erythema Arthritcum 67. Holmes, M. A., W. Austin, W. Austin, and CDC. 1965. Vibrio epidemicum (Haverhill fever). Arch. Intern. Med. 54:659-684.

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