Pathogenic Bacteria in Milk - A Review
P. C. VASAVADA
ABSTRACT
Pathogenic bacteria are transmissible
to humans through milk and milk prod-
ucts. Recently, attention is focused on
milk, cheese, and ice cream contaminated
with pathogenic bacteria, viz., Listeria
monocytogenes, Yersinia enterocolitica,
Campylobacter jejuni, and enteropatho-
genie Escbericbia colL This review pre-
sents information on characteristics of
these pathogens and illnesses caused by
them.
INTRODUCTION
Pathogenic bacteria in milk have been a
matter of public health concern since the early
days of the dairy industry. Many diseases such
as tuberculosis, brucellosis, diphtheria, scarlet
fever, Q-fever, and gastroenteritis are transmis-
sible via milk products. The potential threat of
pathogenic bacteria has been minimized and the
numbers of outbreaks involving milk and milk
products have steadily declined mainly due to
modern milk production practices which
emphasize sanitary measures, improved udder
health, herd inspections, proper cooling, care-
ful handling and storage of raw milk, and
almost universal use of pasteurization (31).
However, a recent flurry of well-publicized
outbreaks of salmonellosis (5, 13), listeriosis
(12, 24), campylobacteriosis (3, 8, 9, 61), and
yersiniosis (7, 25) has refocused our attention
on milkborne pathogens, especially the newly
emerging pathogens, such as Listeria rnonocyto-
genes, Campylobacter jejuni, Yersinia entero-
colitica, and enteropathogenic Escbericbia coli.
The main objective of this paper is to review
the problem of pathogenic bacteria in milk and
describe the major characteristics of these
bacteria and the illnesses caused by them.
Received December 28, 1987.
Accepted April 28, 1988.
1988 J Dairy Sci 71:2809--2816 2809
University of Wisconsin-River Falls
Animal and Food Science Department
River Falls 54022
DISCUSSION
Emerging Pathogens
The dairy industry is renewing its efforts to
promote a positive, healthful image of milk and
dairy products through advertisement campaigns
that claim "Milk: It does the body good". How-
ever, well-publicized disease outbreaks and
product recalls implicating milk, cheese, and ice
cream have caused concerns among consumers
regarding safety of the milk supply.
Investigations into the causes of these out-
breaks revealed several unique aspects of the
problem of pathogenic bacteria in milk:
1. In many instances, bacteria that either have
never been or were rarely known to have
been associated with milk were responsible
for the incident.
2. Use of contaminated raw materials or ingre-
dients, improper or insufficient processing,
and postprocessing contamination were
among the probable causes.
3. Quality control tests for detecting adequate
processing and apparent effectiveness of
pasteurization in killing all pathogens were
questioned.
4. Very little was known about the character-
istic, competitive ability of these pathogens
to survive and grow in milk and their mini-
mum infective dose.
The research community, regulatory agen-
cies, and the food industry responded by in-
creasing their efforts in generating much needed
new information regarding these pathogens.
Also, the need to communicate the information
to the dairy industry professionals became
essential. This symposium is one example of
such an effort.
Incidence of Pathogens
Pathogenic bacteria are defined as those
bacteria capable of causing disease, infection, or
intoxication in a susceptible host. Disease trans-
mission can be direct (i.e., when an animal
2810 VASAVADA

TABLE 1. Outbreaks of gastrointestinal illness associ- consume properly pasteurized milk. Despite
ated with raw milk and raw milk products. the potential public health hazard, raw milk
sale is legal in several states. Also, several
Year State Pathogen states are under pressure to reverse previous
legislation that limits the sale of raw milk
1980 Montana Salmonella typbimurium
(35).
1980 Vermont S. derby Recently, the US FDA has been asked by
1981 Washington S. dublin the US District Court for the District of Colum-
1981 Arizona Campylobacterjejuni bia to formulate a rule banning the sale of both
Michigan certified and noncertified raw milk and products
Minnesota C. jejuni, Salm onella (18). Over the past few years, pasteurized fluid
Oregon milk and milk products contaminated with
Kansas
pathogenic bacteria have been implicated as
1982 Wisconsin C. jejuni the causes of outbreaks of foodborne illness
1983 Pennsylvania C. jejuni (7, 13, 25) (Table 2). In addition, several well-
1984 California C. je]uni publicized incidents of dairy product recalls
have occurred as the direct result of product
contamination with pathogenic bacteria (14,
15, 16, 17) (Table 3).
disease is transmitted to man via milk) or As a result of outbreaks and recalls, the FDA
indirect (i.e., when man contaminates the milk, has increased the surveillance program designed
which is then consumed by another person). to detect contamination by pathogenic bacteria
Traditionally, raw or unpasteurized milk has in dairy plants and finished products (50, 52).
been a major vehicle for transmission of patho- Recent findings of the dairy plant inspections
gens. Several outbreaks of gastrointestinal ill- and check ratings by the FDA revealed that
ness associated with both certified and non- evidence of L. m o n o c y t o g e n e s contamination
certified raw milk and also certified milk prod- had increased from 9 ot 357 (2.5%) inspections
ucts have been reported (3, 4, 5, 6, 7, 8, 9, 10, in 1986 to 19 of 620 (3.1%) in 1987 (19)
27, 35, 61, 62, 74, 75)(Table 1). According to (Table 4). Of 47 plants in which there were
the Centers for Disease Control, raw milk drink- positive findings, FDA identified L. m o n o c y t o -
ers are 158 times more likely to contract illness g e n e s in finished products in 16 plants, L. in-
caused by S a l m o n e l l a d u b l i n than those who n o c u a in products in 3 plants, nonpathogenic

TABLE 2. Recent outbreaks associated with milk and milk products contaminated with pathogenic bacteria.

Date Location Product Pathogen

1976 New York Chocolate milk Yersinia enterocolitica

1982 Arkansas, Pasteurized milk !I. enterocolitica
Tennessee,
Mississippi
1983 Massachusetts Pasteurized milk Listeria monocytogenes
1985 Illinois Low fat milk Salmonella typbimurium
1985 California Mexican-style cheese L. monocytogenes
1985 Kentucky Chocolate milk Staphylococcus enterotoxin
1985 Linderkranz cheese L. monocytogenes
1986 Ohio French Brie cheese L. monocytogenes
1986 Arizona Mexican-style cheese L. monocytogenes
1987 Pennsylvania Ice cream L. monocytogenes

Journal of Dairy Science Vol. 71, No. 10, 1988

 SYMPOSIUM: PROBLEMS OF PATHOGENIC BACTERIA IN THE DAIRY INDUSTRY
TABLE 3. Major recalls of dairy products contamin-
ated with pathogenic bacteria.
Year Pathogen Product
1985 Sahnonella typbimurium Low fat milk
1986 Listeria monocytogenes Soft, Mexican-style
cheese, Linderkranz,
Brie
1986 L. monocytogenes Ice c r e a m ,
ice cream sand-
wiches,
ice cream bars
Y. enterocolitica in products of 21 plants,
Salmonella in products in 2 plants, Aero-
monas bydropbila in 3 plants, Pasteurella
hemolyticus in 1 plant, and enteropathogenic
E. coli in a product in 1 plant (19). According
to the FDA summary, L. monocytogenes was
detected in whole milk chocolate milk, and
whole and low fat milks; ice cream; ice milk
mix; and ice cream novelties including bars,
slices, drumsticks, ice cream rolls, and cups.
The incidence of pathogens in dairy foods is
not limited to domestic products only. Im-
ported soft cheeses also have been implicated
(16, 20). For example, in a 1986 survey of
imported Italian cheese, F D A found 21 of 74
(28.4%) samples were in violation and these
products were denied entry into the United
States. Of these products, two contained Listeria
species and tested positive for phosphatase
level indicative of inadequate pasteurization; 9
had E.coli levels exceeding 10,000 organisms/g;
6 had high phosphatase levels; and 2 had both
TABLE 4. Incidence of pathogens in 620 dairy plants
subjected to the FDA cheek rating - 1987.
Organism Plants
Listeria monocytogenes 19
Pathogenic and nonpathogenic
bacterial contamination 47
Yersinia spp.
(nonpathogenic) 21
Other 7 1.1
281 1
high phosphatase levels and E. coli levels ex-
ceeding 10,000 organisms/g (20).
Khayat et al. (48) surveyed coliforms and
Staphylococcus aureus in commercial cheese.
They found 54% o f cheeses contained 102 to
107 coliforms/g. Also, 5 o f 200 cheeses con-
tained >1000 coagulase-positive Stapb. aureus/
g.
Pathogens in Milk -- Historical Perspective
Because milk provides nutrients and near
neutral pH preferred b y many microorganisms,
it can serve as a growth medium for many
pathogenic and opportunistic microorganisms.
F o o d poisoning outbreaks and other illnesses
involving milk and milk products have been
reported since the beginning of the dairy indus-
try (Table 5).
Earlier, diseases such as tuberculosis, diph-
theria, and scarlet fever were commonly spread
through milk. The advent of tuberculin testing,
brucellosis eradication program, and mandatory
regulations requiring pasteurization led to a
dramatic decline in the incidence of milkborne
disease outbreaks.
From 1950 through the 1970's, several
disease outbreaks caused by pathogens in pro-
cessed milk and manufactured dairy products
were reported, e.g., Salmonella species in dried
milk products (2, 34), enteropathogenic E. coli
contamination in soft and semi-soft imported
cheese (32, 55, 76), and Staph. aureus in cheese
(1, 30, 45, 57, 83). The resulting industry-wide
surveillance programs and research dealing with
the behavior of these pathogens during the
manufacturing and storage of dairy products
TABLE 5. Pathogens in milk: food poisoning or
disease outbreaks involving milk and milk products.
Years Notable diseases or pathogens
(%) 1900--1940's Diphtheria, tuberculosis, brucellosis,
Q-fever, septic sore throat
3.1 1950-1975 Salmonellosis, Staphylococcus enter-
otoxin, brucellosis, Bacillus cereus,
7.6 enteropathogenic E. coil
1975--1986 Enteropathogenic E. coli, Yersinia
3.4 enterocolitica, Campylobacter jejuni,
Salmonella typhimurium, Listeria
monocytogenes
Journal of Dairy Science Vol. 71, No. 10, 1988
2 812
proved to be successful in managing the prob-
lem and reducing the hazard.
Today, however, several previously undetec-
ted pathogenic bacteria have been recognized
as potentially important agents of foodborne
illness associated with milk and milk products,
namely, L. monocytogenes, Y. enterocolitica,
C. jejuni, and enteropathogenic E. coli (0157:
H7). The remainder of this paper will summar-
ize the main characteristics of these organisms
and describe the illnesses caused by them.
Listeria monocytogenes. Listeria rnonocyto-
genes is a gram-positive, nonsporeforming, rod-
shaped organism with coccoid or diphtheroid
morphology. It is psychrotrophic and can grow
at temperatures from 3 to 45°C, optimally at
30 to 37°C. The organism forms bluish-green
colonies on trypticase soy agar (oblique illum-
ination) and shows characteristic tumbling
motility when grown in trypticase soy broth at
25°C. Listeria monocytogenes is weakly ~-
hemolytic on media containing blood. It grows
in a pH range of about 4.8 to 9.6 and is catalase
positive.
Listeria monocytogenes is distributed widely
in nature and has been isolated from a variety
of sources including soil, manure, leafy vege-
tables, raw beef, and poultry. It also has been
isolated from mastitic milk, improperly fermen-
ted silage, and from unpasteurized raw milk
(36, 42, 43, 44, 54, 79).
Listeriosis can manifest a variety of symp-
toms in humans, including meningitis, infec-
tious abortion, perinatal septicemia, and en-
cephalitis. Often, it is the cause of stillbirths
or deaths of infants soon after birth. Surviving
infants usually develop meningitis, which can
be fatal or result in permanent mental retarda-
tion (43, 63, 67).
Listeria rnonocytogenes is heat-sensitive and
is inactivated by pasteurization. However, there
is some concern that in the intracellular phase
(in leucocyte) it may survive conventional
pasteurization (38).
Yersinia enterocolitica. Yersinia enteroco-
litica is gram-negative, nonsporeforming, rod-
shaped bacterium. It is psychrotrophic and will
grow at temperatures from 0 to 450C, optimal-
ly at 22 to 29°C. Because Y. enterocolitica tol-
erates alkaline conditions, this characteristic is
used in its selection (23, 58, 65, 66, 78). On a
selective medium such as the Cefsulodin-lragas-
Journal of Dairy Science Vol. 71, No. 10, 1988
VASAVADA
an-Novobiocin agar or the Yersinia selective
agar, Y. enterocolitica forms characteristic
"bullseye" or "target" colonies (66, 78).
Yersinia enterocolitica is widely distributed
in nature. It has been isolated from foods of
animal origin, including milk and cheese, beef,
pork and lamb (28, 58, 64, 66, 73, 81). It also
is known to occur in waters of lakes, wells, and
streams (28).
Yersiniosis is characterized by gastroenter-
itis, mesenteric lymphadenitis, and terminal
ileitis. Often, yersiniosis symptoms mimic acute
appendicitis. Such was the case in the well-
known outbreak of yersiniosis in Oneida
County, NY in which several children were
subjected to unnecessary appendectomies after
drinking chocolate milk contaminated with IT.
enterocolitica (25). The outbreaks of yersiniosis
in the United States are primarily caused by Y.
enterocolitica serotype 0:8, whereas Y. entero-
cotitica serotype 0:3 is more prevalent in Europe
and Canada (66).
Although Y. enterocolitica and related
bacteria have frequently been isolated from raw
milk (58, 64, 78, 81), most isolates have been
recognized as nonpathogenic, "environmental"
strains. The organism is heat labile and is read-
ily inactivated by conventional pasteurization
( 4 1 , 6 9 , 70).
Campylobacter jejuni. Campylobacter jejuni
is a gram-negative nonsporeforming bacterium
with a characteristic S, gull, or comma-shaped
morphology. Under the phase-contrast micro-
scope, C. jejuni exhibits a characteristic darting,
"cork-screw" motility. The organism is micro-
aerophilic in nature and can be readily grown in
reduced oxygen atmosphere of 5% O~, 10%
CO2, and 85% N2 (37, 59, 68, 71). The organ-
ism grows at temperatures from 30 to 47°C,
optimally at 42°C. Campylobacter jejuni is
/3-hemolytic on media containing blood and is
catalase positive (37).
Campylobacter jejuni has been isolated from
feces of cattle, swine, sheep, goats, dogs, cats,
rabbits, and rodents (60, 68). It causes mastitis
in cows and has been isolated from raw milk
(39, 51, 59, 77, 80).
Campylobacter infections are more common
than cases of salmonellosis and shigellosis com-
bined (71). Symptoms of campylobacteriosis
include mild enteritis or sometimes severe
enterocolitis. Often the patient experiences
 SYMPOSIUM:PROBLEMSOF PATHOGENICBACTERIAIN THE DAIRY INDUSTRY
apparent recovery followed by relapse. Other
symptoms include nausea, abdominal cramps,
and bloody diarrhea (27, 37, 68).
Campylobacter jejuni is sensitive to heat,
drying, air (oxygen), and acidic pH. It is readily
inactivated by normal pasteurization (35, 60,
82).
Enteropatbogenic Escbericbia coli. The
presence of coliforms, particularly E. coli, in
foods indicates the possibility of pathogenic
contamination, polluted water supply, or a
breakdown in sanitation. Escbericbia coil is a
gram-negative, nonspreforming, rod-shaped
organism. Four groups of E. coE have been
recognized, namely, enteropathogenic, entero-
toxigenic, enteroinvasive, and colehemorrhagic
(49).
Escbericbia coli 0157:H7 is recognized as an
emerging pathogen. Several outbreaks involving
E. coli 0157:H7 have been reported (11, 32,
47, 55). The organism causes hemorrhagic
colitis or bloody diarrhea. This infection is
usually characterized by severe abdominal
cramps followed by watery and grossly bloody
stools (40, 56). Vomiting is common, but fever
is rare. The illness occasionally involves hemo-
lytic uremic syndrome (HUS), which is charac-
terized by serious kidney dysfunction with urea
in the blood.
Though E. coli 0157:H7 is often associated
with ground beef, recently it was implicated as
the cause of an outbreak in Ontario where
several kindergarten children suffered from an
illness after visiting a dairy farm were raw milk
was served (47). Some regulatory authorities
warn that the increased slaughtering and pro-
cessing of dairy cattle resulting from the dairy
diversion program may increase the potential
of E. coli 0157 :H7 contamination.
The significance of E. coli 0157:H7 as a
foodbase pathogen is not fully known. Investi-
gations are underway to develop effective and
sensitive methods for its detection and isolation.
The organism is heat labile and is readily in-
activated through cooking and proper pasteur-
ization.
Enterotoxienic E. coil 027:H20 is another
strain of E. coli that caused gastroenteritis asso-
ciated with eating imported Brie cheese (40, 49,
55). Several similar outbreaks occurred in the
United States and one in the Netherlands asso-
ciated with consumption of cheeses from France
(4O).
2813
Controlling Pathogenic Bacteria
Confronted with a recent flurry of food
poisoning outbreaks involving contaminated
milk and cheese and a rash of product recalls,
the dairy industry has taken several initiatives
to control pathogenic bacteria in milk and dairy
products. Emphasis is placed on keeping patho-
gens out of the plant, eliminating them through
proper processing, preventing postprocessing
contamination, and sanitation. Recent research
(53) indicates that commonly used dairy sani-
tizers, namely those containing chlorine and
iodine, acid anionic compounds, and quaternary
ammonium-based sanitizers, are effective
against S. typbimuriurn and L. rnonocytogenes.
Increased emphasis is focused on proper main-
tenance of eqipment, particularly the plates in
the HTST pasteurizer; use of clarifiers; use of
footbaths; and control of the plant environ-
ment (72). The Hazard Analysis and Critical
Control Point Program, specifically designed to
minimize the threat of pathogenic bacteria, is
also being reemphasized. Details of control
measures that can be used in dairy plants to
minimize the possibility of pathogens have been
published (21, 29, 33, 72).
SUMMARY
Pathogenic bacteria have occurred in milk
since the dairy industry began. Increased com-
mitment to research through dairy industry
associations, government regulatory agencies,
and universities continues to provide much
needed information regarding emerging patho-
gens. In addition to the pathogens discussed in
this paper, Aeromonas bydropbila also is note-
worthy. According to USDA scientists, food-
borne Aeromonas has the same virulent charac-
teristics as those found in clinical isolates and
should be considered pathogenic (22). Because
it is impossible to prevent contamination by
pathogens at all times, the dairy industry has to
implement newer knowledge in an effective
manner to minimize the threat of these patho-
gens. Research priorities for pathogens have
been identified, and much progress has been
made in diagnostic procedures and in under-
standing the mechanism of pathogenesis and
behavior of pathogens in milk and dairy prod-
ucts. Only through concerted effort of the in-
dustry, academic, and government institutions
can we successfully face the problem of "new"
and "emerging" pathogens.
Journal of Dairy Science Vol. 71, No. 10, 1988
2814 VASAVADA
ACKNOWLEDGMENTS
A contribution from the College of Agricul-
ture, University of Wisconsin-River Falls, and
University of Wisconsin-Extension.
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