637 Journal of Food Protection. Vol. 46. No.7 Pages 637-649 (July 1983) Copyright©. International Association 01 Milk. Food. and Environmental Sanitarians Epidemiology of Milk-Borne Diseases 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 80 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 30 20 10 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 <I Q fever Salmonellosis 3 2 7 21 28 41 50 Shigellosis 2 4 3 Staphylococcal intoxication 8 26 50 30 5 Streptococcal 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.