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)
ABSTRACT
Secular trends in milk-borne diseases in the U.S.A. show
numerous outbreaks associated with ingestion of raw milk in the
early 1900s until the end of World War II. Diseases common in
this period, but no longer milk-borne, were typhoid fever, scarlet
fever, septic sore throat, diphtheria, tuberculosis, shigellosis, and
milk sickness. Milk-borne and milk-product-borne diseases rarely
reported somewhere in the world were botulism, Escherichia coli
enteritis, Pseudomonas aeruginosa enteritis, listeriosis, Clos-
tridium periringens enteritis, Bacillus cereus gastroenteritis,
Haverhill fever, Q fever, hepatitis A, poliomyelitis, toxoplas-
mosis, histamine intoxication and hypertension. After most milk
was pasteurized, outbreaks decreased dramatically. Milk-borne
diseases of contemporary importance in the U.S.A. are salmonel-
losis, campylobacteriosis, staphylococcal intoxication, brucel-
losis, and yersiniosis. These have usually been associated with in-
gestion of raw milk, certified raw milk, home-made ice cream
containing fresh eggs, dried milk, pasteurized milk which WilS
contaminated after heat processing, or either cheese made from
raw milk or cheese in which starter activity was inhibited during
its manufacture.
Throughout the years, epidemiologists, physicians and
sanitarians in the United States have expressed concern
about milk-borne and milk-product-borne diseases (8,31-
40,54.58,115). Frequencies of reported outbreaks of
milk-borne and milk-product-borne disease during the
1900-1981 period are shown in Fig. 11. Secular trends in
milk-borne (and milk-product-borne) diseases show the
IData in the Figure was extracted from the reviews by Trask (lIS).
Armstrong. and Parran (8). reports from the U.S. Public Health Service.
Office of Milk Investigations (l925-1936). Domestic Quaral!line Division.
Sanitation Section (1937-1939). State Relations Division, Sanitation Sec-
tion (1940-1943). Engineering Division. Milk and Food Section (1944-
1946). Division of Sanitation, Milk and Food Branch (1947-1949); Na-
tional Office of Vital Statistics-Reports by Dauer (31-40)-and surveil-
lance reports, reviews in Morbidity and Mortality Weekly Reports. and
annual summaries about foodborne diseases by the Centerl s) for Disease
Control (I961-198Jj (22).
JOURNAL OF FOOD PROTECTION. VOL. 46. JULY 1983
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abundance of health hazards that were associated with in-
gestion of raw milk in the early 1900s until the end of
World War n, Then, because most of the milk was pas-
teurized, outbreaks decreased dramatically.
Reports of experimental milk pasteurization were just
appearing in the public health literature in the early 1900s,
but the process did not come into common use for many
years thereafter. The first model milk ordinance recom-
mended by the U.S. Public Health Service, for instance,
was published in 1924 and a draft code followed in 1927.
From that time on, pasteurization for milk was stressed na-
tionally. Since 1950, there have been reports of only a few
raw milk-associated outbreaks; but, such outbreaks still
occur, because some people prefer to drink raw milk.
The percentage of reported outbreaks of milk-borne dis-
ease by decade is shown in Table I, Several trends stand
ouL During the period between the tum of the century and
1940, typhoid fever was the major milk-borne disease.
Then after precipitous decline in two decades, no milk-
borne outbreaks of typhoid fever were reported during the
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
to extinction in the 1940s. Diphtheria, which accounted for
a smaller share, declined until reports ceased in 1946,
As reports of outbreaks of these diseases waned, reports
of outbreaks of staphylococcal intoxication, nontyphoidal
salmonellosis and diseases of unknown etiology gathered
impetus. Milk products (ice cream, dry milk, and cheese)
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.)
Salmonellosis and gastroenteritis of unknown etiology
dominated the 1970s. In the last of the 1970s, campylobac-
teriosis began to emerge as an important raw milk-borne
disease. The large percentage of outbreaks of unknown
etiology reported in the last few decades, almost certainly
included undetected outbreaks of campylobacteriosis. The
relatively long gap between the report by Levy (75) and the
later reports reflects the difficulty to recover Campylobac-
638 BRYAN

80

o Raw milk or cream

BI Certified raw milk
70
Ili1 Milk, unspecified; most likely raw milk
£Xl Pasteurized milk
IDJ Oried (powdered) milk
51 Cheese
60 m Milk products. unspecified; malted
milk; milk formula
m Human milk
P»J Butter
• Ice cream, eggs frequently added
mJ Unknown

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

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

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0)
,:::
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0 .~
~ ell
,:::
0
.~

.5 0
'6 '2 u
';;]
.~
-;
u
';::
<l c'-' '"
0
'1'"5 .s ell
,:::
t>
..sl
<l
"u0
0 :9'"
.::1
'"....
'"or> '"
'{ii
.9
'" «en § 0-
8
,5
g
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Product § >-. .~ 0
:S
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,::: '" ::> .::> '80-
~ §-
<l .~ .!l 0

~
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E
-;
..<:i
0-
"'"8 ~
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0- x e ,:::
-'Ci ~
"l
g
"l U" ~'"
v
>- .(
1:
iX:I ::c" 0
!-< ~ ::2 ,g ~ E-

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

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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 26 a 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)

JOURNAL OF FOOD PROTECTION, VOL. 46, JULY 1983

 MILK-BORNE DISEASE 641

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-

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tween ill persons and their having eaten foods containing
Cheddar cheese in Mexican-style restaurants (52). The
cheese was from a single lot produced by a single man-
ufacturer. The milk used in the manufacture of the cheese
had been held unrefrigerated for 3 d in insulated tanks be-
fore it was pasteurized. The effectiveness of the pasteuriza-
tion process was not monitored. After pasteurization, the
milk was filtered; a violation of the U.S. Public Health
Service Milk Ordinance and Code, 1978 (118). Informa-
tion on culturing, curd formation, and ripening was not re-
ported.
In England and Wales from 1969 to 1976, either milk or
cream (usually raw) was implicated in 60 outbreaks of sal-
monelloses (117). Three percent of milk sold in England
and Wales did not receive a heat treatment.
In Scotland, where 10% of the milk is sold without heat
treatment, 29 milk-borne outbreaks of salmonelloses, af-
fecting at least 2,428 persons, occurred between 1970 and
1979 (103). During this period, one outbreak that affected
at least 700 persons was reported (104). Unpasteurized
milk was identified as the vehicle.
Another outbreak of salmonellosis in which more than
500 persons were affected was reported from South Au-
stralia (102). Bottled, unpasteurized milk was implicated.
In Trinidad, approximately 3,000 persons developed
Salmonella derby gastroenteritis after they ingested one of
seven different brands of powdered milk, which had been
packaged at a single processing plant on the island (123).
Cows usually become infected with salmonellae from
either the feedstuffs they eat or from contaminated sources
in their farm or barn environment. They also shed these or-
ganisms in their feces. Their udder or hide may become
contaminated with salmonellae when they wade in streams
or lie on fecally-soiled litter or ground. Milk can become
contaminated from such sources. Rapid chilling of raw
milk inhibits multiplication of salmonellae, however, and
pasteurization by approved procedures kills large numbers
of Salmonella.
Campylobacteriosis
Milk-borne campylobacteriosis has been reported in the
United States, England and Wales, Scotland and Canada.
The outbreaks that have been reported in the United States
are summarized in Table 4. The vehicle in all outbreaks
breaks were associated with milk that had been bottled in
dairies.
Between 1978 and 1980 in England and Wales, raw
milk was implicated in 14 documented outbreaks of cam-
pylobacteriosis, which affected at least 3,553 persons
(l00,109). In one of these outbreaks, 2,500 school chil-
dren became ill during a 3-week period (69).
The largest number-648-of cases in a common-source
outbreak ever recorded in Scotland was caused by Cam-
pylobacter transmitted by raw milk (122). In another Scot-
tish outbreak, Campylabacter jejuni was isolated from
stools of 148 patients, from 57 asymptomatic persons, and
from a milk filter, during an investigation of an outbreak
that followed ingestion of unpasteurized milk (91).
In Canada, an outbreak of campylobacteriosis that af-
fected 27 persons occurred at a camp. Raw milk purchased
from a local dairy was found to be contaminated by Cam-
pylobacter (83).
A wide variety of warm-blooded vertebrates have been
infected by C. jejuni. This organism has been isolated from
the intestinal tract and feces of man, cattle, goats, sheep,
pigs, chickens and some wild birds. It has also been iso-
lated from poultry meat, salt water and fresh water (46).
Rapid cooling of milk should prevent growth of C. jejuni,
and either thorough cooking or pasteurization can be ex-
pected to kill it.
Staphylococcal food poisoning
Raw milk from individual cows or goats has been impli-
cated as a vehicle in numerous outbreaks of staphylococcal
intoxication before the practices of rapid chilling of milk
and pasteurization became common (JJ , 14,85). Pas-
teurized milk that has become contaminated after being
heat treated has been a vehicle on rare occasions (21,63).
Spray-dried milk has been the vehicle for staphylococcal
enterotoxin at least two outbreaks (6,7).
Cheese has been a vehicle for staphylococcal enterotoxin
in several outbreaks (2,18,65,66,77,82,129).
Staphylococci multiplied in the milk and elaborated en-
terotoxin before fermentation commenced.
Ice cream has also been implicated as a vehicle of
staphylococcal enterotoxin in several outbreaks
(44,60,88,125). Usually, ice cream mix was contaminated
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)

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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
hospitalized, 17 underwent appendectomies, one of these
persons died. It was estimated that 857 cases may have oc-
curred. Pasteurized milk was the implicated vehicle; details
about the source of contamination were discovered (73).
An investigation revealed that unsold milk was returned to
the dairy and fed to hogs. At the hog farm, milk crates
were stored on the ground down slope from hog pens.
Crates were returned to the dairy and washed, but the
washing failed to remove some of the mud in the triangular
configurations on the undersurface of the crates. Aulisio et
al. (10) hypothesized that the mud contaminated the bot-
tom of the milk containers when they were put into the
crates; tops of the containers could have been contaminated
during stacking. Animals are frequently infected with Y.
enterocolitica. Water in streams, often contain this or-
ganisms. Milk can become contaminated from these
sources (68,120).
MILK-BORNE DISEASES OF HISTORIAI, INTEREST
Typhoidfever
Before the practice of pasteurization and at a time before
farm sanitation was commonplace, there were frequent re-
ports of outbreaks of milk-borne typhoid fever. Reviews of
milk-borne typhoid fever outbreaks have been made
(8,19,107,115).
During investigations several sources of contamination
were found: persons who had typhoid fever, who were car-
riers of Salmonella typhi or who nursed sick persons in
their family either milked cows or handled milk or milk
utensils or containers on milk-producing farms or in milk
shops. Well water used to wash and rinse utensils and
equipment was another source of contamination. Bottles
returned from homes of sick persons were suspected to be
the sources of contamination on a few occasions. More re-
cently, in Trinidad, ice cream was implicated as a vehicle
of S. typhi in an outbreak affecting 132 persons (106).
Streptococcal infections
Outbreaks of milk-borne scarlet fever and septic sore
throat were frequent in the United States (and no doubt,
elsewhere) before pasteurization of milk became nearly
universal. These outbreaks are reviewed (8,19,115). Sev-
eral were traced to cows with either mastitis or lesions on
their teats or udders. The cows usually acquired group A
streptococcal mastitis through contact with a human car-
rier. Thereafter, they discharged large numbers of strep-
tococci in their milk. If this milk was not pasteurized, out-
breaks resulted.
Outbreaks of scarlet fever and septic sore throat were
also attributed to primary cases working at a farm or in
milk shops and either milking cows or otherwise handling
milk or milk equipment. For instance, milk was contami-
nated by a worker who, while suffering from an acute sore
throat, bottled the milk and capped the bottles. In some
outbreaks, persons who nursed sick persons in their family
JOURNAL OF FOOD PROTECTION, VOL. 46, JULY 1983
643
either milked cows or handled milk or milking equipment
and were considered as the source.
Dried milk has also been implicated as a vehicle (1,94).
Canned milk that had been opened and diluted the evening
before serving was responsible for three outbreaks that in-
cluded 835 cases of tonsillitis and scarlet fever (l09).
Diphtheria
Before pasteurization became a common practice, many
diphtheria epidemics were epidemiologically associated
with raw milk. These outbreaks have been summarized by
various authors and reviewed by Bryan (19). In many of
the outbreaks, implicated milk came from farms on which
dairy workers were either carriers of Corynebacterium
diphtheriae or they suffered from clinical manifestations of
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diphtheria. In other outbreaks, implicated milk came from
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.
Tuberculosis
Mycobacterium bovis can be transmitted by raw milk.
The ingested organisms penetrate the orophamx and intes-
tine and give rise to lesions in the cervical lymph and
mesenteric nodes. From these sites, they are diseminated to
bones and joints resulting in kyphosis, a condition in which
the afflicted are commonly called hunchbacks. In recent
years in the United States, the incidence of alimentary
tuberculosis has been low; however, in some other coun-
tries, reports of this disease are much more common.
Strong circumstantial evidence has incriminated raw
milk as a vehicle for transmitting M. bovis to man; out-
breaks have been reviewed (19). Factors that influence
transmission of M. bovis are: (a) incidence of infection in
cows, (b) opportunities for contamination with M. bovis
and the presence of and quantity of this organisms in milk,
(c) whether or not milk is boiled or pasteurized and (d) the
milk-drinking habits of the populace.
Large quantities of tubercle bacteria can readily reach
milk of infected animals because both the mammary gland
and the lungs discharge into the same canalicular system.
They can also reach milk from feces, which may dry upon
and cling to the udder, tailor flanks of cows. Contamina-
tion can come also from infected udders and from air-borne
organisms that have orginated in respiratory discharges.
Tuberculin testing and slaughter of reactors has almost
eradicated tuberculosis from dairy cows in the United
States. So contamination of milk from animal sources is
quite rare today. Furthermore, the pasteurization process
was initially designed to kill large numbers of M. bovis
(71).
Shigellosis
A few outbreaks of shigellosis have been associated with
milk and cheese. These have been reviewed (19,107). The
implicated milk or milk product was contaminated by a
human carrier, and the milk was frequently held for several
hours without refrigeration.
644 BRYAN
Milk sickness
Grazing animals have developed trembles as a result of
eating leaves and stems of white snakeroot (Eupatorium
rugosum) or rayless goldenrod (Aplopappus heterophyllus
or lsocoma wrighii). Animals having this condition elimi-
nate tremetol ( a higher alcohol which is toxic to the liver)
in their milk. Milk sickness is manifested by weakness,
prostration, loss of appetite, abdominal pain, nausea, vom-
iting, muscular tremors and coma. It is frequently fatal.
Although, this disease is rare today, numerous cases and
deaths occurred among early settlers, particularly in the
midwest, before land was cleared. Significant to the occur-
rence was that cattle foraged wooded areas and were
milked only sporadically (81).
DISEASES RARELY REPORTED
AS BEING MILK·BORNE
Botulism
Milk has been implicated as the vehicle in two outbreaks
of botulism involving 5 cases. Outbreaks of botulism have
infrequently been traced to cheese (84). Seven cheese-as-
sociated outbreaks involving 21 cases, 9 of whom died,
have been reported in the United States (25,81). Cottage
cheese was the vehicle in three outbreaks, cheese curd in
one, Neufchatel in one, Liederkranz cheese spread in one,
and an unspecified cheese in one. In 1974, an outbreak that
affected 11 persons who ate a commercially-prepared,
plastic-packaged, cheese spread containing dehydrated on-
ions was reported from Argentina (43). Yogurt has been
suspected of being a vehicle (5).
Escherichia coli enteritis
Camembert and Brie cheese from France were vehicles
in an outbreak of diarrhea caused by Escherichia coli 0
group 124, a non-lactose fermenter that reacted to Shigella
antiserium (116). More than 100 episodes-387 cases-were
eventually traced to this source (78). A milk-borne out-
break among children has been reported in the U.S.S.R.
(80).
Man and other animals shed large numbers of E. coli in
their feces. These organisms have been recovered from the
milk of apparently healthy animals, from those that had
mastitis and from samples of milk and cheese in retail
stores.
Pseudomonas aeruginosa enteritis
Pseudomonas aeruginosa, which produces a heat-labile
enterotoxin, has, on rare occasions, been implicated as an
etiologic agent of milk-borne disease. In an outbreak invol-
ving 409 cases, infants were severely affected and 9 died
(49). Contaminated pasteurized milk was epidemiologi-
cally implicated as the vehicle. During an investigation of
the plant that had processed the milk, P. aeruginosa was
recovered from a rag that had been used to wrap a pipe
joint. Drippings from the rag fell into the pasteurized milk.
In another outbreak, newborn infants vomited and had
diarrhea after being fed human milk that had been obtained
by a breast-pump (113). The same strain of P. aeruginosa
JOURNAL OF FOOD PROTECTION. VOL. 46, JULY 1983
was isolated from rectal swabs taken from 5 of 25 infants,
from the pump and from the vessel in which the pump had
been disinfected.
Listeriosis
Foodborne transmission of listeriosis has not been con-
firmed in humans, but raw milk has been suspected to be
a vehicle. For example, Potel (92) told about a woman
who had drunk milk from a cow with atypical mastitis and
later gave birth to twins prematurely. The infants had mul-
tiple tumors composed of granulation tissue, Listeria
monocytogenes was isolated from the infants and from the
cow's milk. In several cases of listeriosis that occurred in
Halle, Germany, raw milk was suspected as the vehicle,
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and in other cases, suspicion was cast on cream, sour milk,
and cottage cheese (101).
Listeriosis has been observed in cattle; udder infections
due to L. monocytogenes have been described, and this or-
ganism has been found in milk. [See the review by Bryan
(19) for further discussion and references.]
Clostridium perfringens enteritis
In 1933, a report incriminated Clostridium perfringens
as the cause of an outbreak of fever and flatulent diarrhea
in infants (87). Although, the syndrome is not typical of C.
perfringens enteritis, the hypothesis is interesting because
C. perfringens can readily reach milk and its spores can
survive pasteurization. The heat of pasteurization would
heat-activate the spores and reduce populations of competi-
tive organisms. Amino acids and growth factors necessary
to sustain growth of C. perfringens are constituents of
milk, and this organism grows in milk causing a stormy
fermentation. Refrigerated storage of heat-treated milk
would, however, prevent outgrowth of spores and multipli-
cation of the vegetative cells.
Bacillus cereus gastroenteritis
Milk and ice cream have been implicated as vehicles in
outbreaks of gastroenteritis caused by Bacillus cereus. [See
Gilbert (61) for a more complete discussion of the role of
B. cereus as a foodborne pathogen and for references.]
Haverhill fever
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
most of the cases and serum antibodies were demonstrated
in the other cases. All persons who were affected had
drunk raw milk bottled from the same dairy. A cow in the
herd from which the implicated milk came had a healed le-
sion, suggestive of a rat-bite, on one teat. The outbreak
ended after the dairy began to pasteurize its milk.
Qfever
Coxiella burnetii is sometimes found in raw milk, and
some investigators have implicated raw milk as a vehicle
(19). Most of the evidence implicating milk as a vehicle,
however, is the greater frequency that compliment-fixing
antibodies are found in the sera of persons who drank raw
 MILK-BORNE DISEASE
milk, than the frequency with which these antibodies are
found in the sera of persons who did not drink raw milk.
Epidemiologic evidence presented by Brown et al (17)
suggested that ingestion of raw milk from infected cattle
resulted in a common-source outbreak; contact with ani-
mals, farms, dust and insects were ruled out as possible
routes of transmission. Ingestion of raw milk that con-
tained C. burnetii by human volunteers, however, has not
caused illness (51,73).
c. burnetii can survive vat-pasteurization at 61.7°C
(143°F) for 30 min; pasteurization at 62.8°C (l45°F) for 30
min or at 71. 7°C (161°F) for 15 sec is adequate to kill this
organism.
Hepatitis A
Just about any food that is handled by a person who is
shedding hepatitis A virus can become a vehicle for this or-
ganism. Raw milk from a small dairy was implicated in an
outbreak in Geiorgia (86). Cream used in a fruit salad and
in sherry trifles (prepared by a pastry-cook who was in the
incubation phase of hepatitis A) was the vehicle of another
outbreak (27).
Poliomyelitis
Raw milk-associated outbreaks of poliomyelitis have
been reported. [See Cliver (27) for a review.] In one of
these outbreaks, all cases had drunk milk from a small
dairy. At this dairy, a 16-year old milker handled milk for
4 d while in the acute phase of poliomyelitis (72).
Russian spring-summer encephalitis (Disphastic milk
fever)
Ingestion of raw milk and of cheese made from raw milk
from tick-infested sheep and goats has resulted in en-
cephalitis. Reports of this disease have been limited to the
U.S.S.R. (96).
Toxoplasmosis
The ingestion of raw milk from goats and cattle raises
the possibility of transmission of Toxoplasma gondii; ani-
mal-to-animal transmission by milk has been demonstrated
(57). A 7-month old child who had a history of being fed
almost exclusively on raw goat's milk developed toxoplas-
mosis (98). Goat's milk is sometimes prescribed for infants
who cannot tolerate cow's milk.
Histamine intoxication and hypertension
Histamine is a powerful capillary dilator; it causes in-
tense headaches, nausea, vomiting, facial flushing, burn-
ing throat, thirst, swelling of lips, and urticaria. Histamine
intoxication after ingestion of cheese has been reported
(45,1 19). Histamine was suspected to be the cause of an
outbreak affecting 38 cases in persons who ate either
cheese crepes or onion soup on which cheese had been
placed (24). Histamine can be formed in cheese when his-
tidine, which is often found in cheese, is decarboxylated.
Many Enterobacteriaceae, enterococci, and Lactobacillus
casei produce decarbocylase. [This topic has been re-
viewed (19,97,121).]
JOURNAL OF FOOD PROTECTION, VOL. 46. JULY 1983
645
Histamine and tyramine in cheese are usually degraded
in the body by monoamine oxidase. Certain drugs, how-
ever, inhibit this enzyme. Persons who have taken one of
these drugs, have experienced attacks of hypertension
shortly after ingestion of cheese; cerebrovacular accidents
have been reported (/3).
Arsenic poisoning
In the summer of 1955, 12,131 children in western
Japan were poisoned because they ingested arsenic-con-
taminated dry milk. One-hundred-thirty of these children
died. The arsenic reached the milk from an inadequately
purified "sodium phosphate" stabilizer which was used in
the manufacturing process. Fourteen years later, survivors
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had a higher rate of physical and mental complaints than a
control group (127).
ROLE OF MILK
AND MILK PRODUCTS AS VEmCLES
Raw milk
Microorganisms that reach a cow's teats can enter them
through their openings and migrate to the interior. The
types and numbers of microorganisms that invade the
udder by this route vary from animal to animal and even
among the quarters of the same udder. Such invasion can
occur even in healthy animals. Micrococci, staphylococci,
streptococci and diphteroides usually predominate among
the microbial flora of the teat and udder.
Mastitis, an inflammitory disease of mammary tissue,
can lead to development of millions of pathogens in the in-
fected quarter and the discharge of large numbers of them
to milk. Milk-borne pathogens that can cause mastitis, in-
clude, S. aureus, streptococci, E. coli, P. aeruginosa, C.
perfringens. streptococci, corynebacteria and mycobac-
teria. Animals infected with other pathogens, such as
Brucella spp., C. burnetii and M. bovis, can shed them,
too, in milk.
Microorganisms from soil, litter, feed, water, feces and
other items in a farm environment commonly contaminate
the surface of the udder and teats and the hair and skins of
cows and goats. From these sources they can get into milk
during milking. Sporeformers such as B. cereus and C.
perfringens can reach milk from soil and litter. Salmonel-
lae as weB as sporeformers can be transmitted to milk from
feed. Yersinia and Campylobacter may reach milk from
contaminated water in streams and ponds. Salmonella,
Campy/obacter, Yersinia, enterococci, E. coli and C. per-
fringens can reach milk if feces of infected animals reach
milk either directly or from contaminated exteriors of
cows.
Equipment used for milking, filtering, cooling, storing
or distributing milk are also important sources of microor-
ganisms. This situation is aggravated if the equipment is
not properly cleaned and sanitized after use. Milk residues
left on equipment and utensil surfaces provide nutrients to
support growth of many microorganisms, including patho-
gens.
646 BRYAN
Farm workers who either milk animals or handle milk,
or milking or storage equipment, can contribute additional
organisms to the milk. Such contamination has resulted in
numerous milk-borne outbreaks of typhoid fever,
diphtheria, septic sore throat, scarlet fever, shigellosis,
staphylococcal enterotoxicosis, hepatitis A and
poliomyelitis.
Certified milk
Certified milk is raw milk which is produced under strict
conditions that comply with standards of sanitation adopted
by the American Association of Medical Milk Commis-
sions (3). These procedures were originated in the early
1800's to produce safe milk before pasteurization became
common. In spite of these precautions, including produc-
tion of milk with low bacterial counts, certified milk has
been implicated as the vehicle in several milk-borne out-
breaks throughout the years; including, the last few years.
Pasteurized milk
Pasteurization or more severe heat treatments applied to
raw milk is the only way to ensure that pathogens likely to
be present are killed and that the milk is safe. When pas-
teurized milk has been implicated as a vehicle, further in-
vestigation has shown that there was either a process fail-
ure or post-pasteurization contamination. Pasteurization,
more than improved dairy sanitation practices, has resulted
in the dramatic decrease in milk-borne diseases during the
past 35 years.
Ice cream
When raw milk was frequently used to make ice cream,
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
their source, pathogens that are incorporated into ice cream
can survive in the frozen product many months.
Use of pasteurized milk in ice mixes, either omission of
eggs or use of pasteurized egg products in these mixes, and
rapid freezing of these mixes, minimize the possibility of
ice cream becoming a vehicle of sufficient numbers of
pathogens to cause illness.
Dry milk
Dry milk has been the vehicle of outbreaks because (a)
it was not pasteurized before drying, (b) it was held at tem-
peratures that permitted the growth of S. aureus and the
production of entertoxin before drying, or (c) product ac-
cumulation and persistence of moisture in an instantizer,
led to multiplication of salmonellae. Pasteurizing, hot
holding at not less than 65°C (149°F) in balance and surge
tanks, and cleaning equipment surfaces that contact the dry
product to prevent product from accumulating in crevices
and dead ends, and to keep moisture from reaching the
dried product, are essential to prevention of outbreaks as-
sociated with dried milk.
Cheese
Unless, the milk used to make cheese is pasteurized,
JOURNAL OF FOOD PROTECTION. VOL. 46, JULY 1983
those organisms that reach raw milk may be found in the
cheese. Brucellae that reach cheese and survive the cheese
making process have caused several cases of brucellosis.
Salmonellae, also frequently reach milk, and they can
grow during cheese making and persist during ripening of
certain cheeses for 60 days or more.
Slow acid production (low milling acidity) by a starter
culture can allow staphylococci to grow and perhaps pro-
duce enough entertoxin to cause disease if process temper-
tures are favorable during curd formation. If the pH of the
curd is higher than normal (5.2-5.3), growth of
staphylococci can even continue during pressing, but sel-
dom afterwards. Their numbers decline rapidly during ri-
pening.
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E. coli hazards are of particular concern in soft and
semisoft surface-ripened cheeses. E. coli can multiply in
soft and semisoft surface-ripened cheses when there is lack
of acid production and low salt concentration in the interior
during the early stage of ripening (56). Furthermore, this
organism can grow on surfaces of these cheeses during the
development of the mold matt, if temperatures are suffi-
ciently high (55).
C. botulium sometimes reaches milk because of soil or
dust contamination. It's spores survive pasteurization. C.
botulium can multiply 'in lightly salted cheeses that have
relatively high pH values (resulting from faulty starter cul-
ture activity) and a closed structure, which is conducive to
anaerobiosis.
Adequate heat treatment of milk and normal starter ac-
tivity are the best preventives of cheese-borne disease out-
breaks. Prolonged ripening also results in a decrease in,
but not necessarily freedom from, pathogens.
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