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rarely. (2) In many, though not all, of the cases of
parat>^hoid meat poisoning it has been demonstrated
that the meat concerned has been derived from an
animal slaughtered while ailing {notgeschlachtet, to use
the expressive German term). There seems reason
to believe that in such an animal, ''killed to save its
life," the specific paratyphoid germ is present as an
infection before death. Milk also has caused para-
typhoid poisoning and in certain of these cases has been
found to be derived from a cow suffering from enteritis
or some other disorder. (3) There is evidence that
originally wholesome food may become infected with
paratyphoid bacilli during the process of preparation or
serving in precisely the same way that it may become
infected with t>^hoid bacilli; the handling of the food
by a paratyphoid-carrier is commonly responsible for
this. In a few instances the disease is passed on from
case to case, but this mode of infection seems exceedingly
rare and is not nearly so frequent as "contact" infection
in typhoid. (4) The majority of parat>^hoid outbreaks




FOOD-BORNE PATHOGENIC BACTERIA 63

are associated with the use of uncooked or partly cooked
food. A selective action is often manifested, those
persons who have eaten the incriminated food substance
raw or imperfectly cooked being most seriously affected,
while those who have partaken of the same food after
cooking remain exempt.

The discovery of the •'* «*'x^"^"^*k^

connection of paraty- ^< m*''^^'^ *^ *»4

phoid baciUi with meat ,\ v' j ^ V^^ ' v *
poisoning dates from /^^ '"^''^\''" ^ ' iJL,**Ji "
the investigation by * - i*-*-*^. - Jt i\ v#
Gartner,^ in 1888, of a
meat poisoning out-
break in Frankenhau-

sen, a small town in , -^ ^ ^ ,

Germany. This epi- V *J^^V.

demic was traced to the ^ **"

use of meat from a cow ^^^- ^ - Bacillus enkritidis, Gartner;

, 111 pure culture; Van Ermengem prepara-

that was slaughtered ^j^^ (Kolle and Wassermann.)

because she was ill with

a severe enteritis. Fifty-eight persons were affected in
varying grades of severity; the attack resulted fatally in
one young workman who ate about eight hundred grams
of raw meat. Gartner isolated from the spleen of the
fatal case and also from the flesh and intestines of the
cow a bacillus to which he gave the name B. enteritidis.
Inoculation experiments showed it to be pathogenic
for a number of animal species. Bacilli with similar
characters have since been isolated in a number of
other meat poisoning epidemics in Germany, Belgium,
France, and England. One well-studied instance of

■ Breslau aerztl. Ztschr., X (1888), 249.



64 FOOD POISONING

food poisoning due to the paratyphoid bacillus has
been reported in the United States.'

The bacteria of the paratyphoid group are closely
related to the true typhoid bacillus, but differ from the
latter organism in being able to ferment glucose with
gas production. They are more highly pathogenic for
the lower animals than is the typhoid bacillus, but
apparently somewhat less pathogenic for man. Most
types of paratyphoid bacilli found in food poisoning
produce more or less rapidly a considerable amount of
alkali, and, if they are inoculated into milk containing
a few drops of litmus, the milk after a time becomes
a deep blue color. Several distinct varieties of para-
typhoid bacilli have been discovered. The main
differences shown by these varieties are agglutinative
differences. That is, the blood serum of an animal that
has been inoculated with a particular culture or strain
will agglutinate that strain and also other strains isolated
from certain other meat poisoning epidemics, but will
not agglutinate certain culturally similar paratyphoid
bacteria found in connection with yet other outbreaks.
Except in this single matter of agglutination reaction,
no constant distinction between these varieties has been
demonstrated. The clinical features of the infections
produced in man and in the higher animals by the dif-
ferent varieties seem to be very similar if not identical.

The bacillus discovered by Gartner {loc. cit.) and
known as B. enteritidis or Gartner's bacillus is commonly
taken as the type of one of the agglutinative varieties.
Bacilli with all the characters of Gartner's bacillus have
been found in meat poisoning epidemics in various

• Bernstein and Fish, Jojir. Amcr. Med. Assoc, LXVI (1916), 167.



FOOD-BORNE PATHOGENIC BACTERIA 65

places in Belgium and Gcniian\'. Mayer' has compiled
a list of forty-eight food poisoning outbreaks occurring
between 1888 and 1911 and attributed to B. enlerilidis
Gartner. These outbreaks comprised approximately two
thousand cases and twenty deaths. In twenty-three
of the forty-eight outbreaks the meat was derived from
animals known to be ill at the time, or shortly before,
they were slaughtered. Sausage and chopped meat of
undetermined origin were responsible for eleven of the
remaining twenty-five outbreaks. Two of the B. enter-
///(/i5 outbreaks were attributed to Vanille Pudding; one,
to potato salad.

In other food poisoning outbreaks a bacillus is found
which is culturally similar to the Gartner bacillus, but
refuses to agglutinate with the Gartner bacillus serum.
Its cultural and agglutination reactions are almost, if
not quite, identical with those of the bacilli found in
human cases of paratyphoid fever which have no known
connection with food poisoning. Mayer^ gives a list of
seventy-seven outbreaks of food poisoning (1893-1911)
in which organisms variously designated as ^'B. para-
typhosus B" or as ^'^B. suipestifer'' were held to be
responsible. The total number of cases (two thousand)
and deaths (twenty) is about the same as ascribed to
B. enleritidis. According to Mayer's tabulation meat
from animals definitely known to be ailing is less com-
monly implicated in this type (ten in seventy-seven)
than in B. enterilidis outbreaks (twenty-three in forty-
eight). Sausage and chopped meat of unknown origin,
however, were connected with eighteen outbreaks.

^Deutsche Viertelj.f. offenlL Ges., XLV (1913), 58-59.
^Op. cit., pp. 60-62.



66 FOOD POISONING

The bacillus named B. suipestifer was formerly
believed to be the cause of hog cholera, but it is now
thought to be merely a secondary invader in this disease ;
it is identical with the bacillus called B. paratypho-
sus B in its cultural and to a large extent in its agglutina-
tive behavior, but is regarded by some investigators as
separable from the latter on the basis of particularly
delicate discriminatory tests. Bainbridge, Savage, and
other English investigators consider indeed that the
true food poisoning cases should be ascribed to B. sui-
pestifer and would restrict the term B. paratyphosus
to those bacteria causing *'an illness clinically indistin-
guishable from typhoid fever." German investigators,
on the other hand, regard B. suipestifer and B. para-
typhosus B as identical. My own investigations* indicate
that there is a real distinction between these two types.

Bearing directly on this question is the discussion
concerning the distribution of the food poisoning bacilli
in nature. Most investigators in Germany, where the
majority of food poisoning outbreaks have occurred,
or at least have been bacteriologically studied, are of
the opinion that B. suipestifer (the same in their opinion
as B. paratyphosus B) is much more widely distributed
than B. enteritidis and that it occurs, especially in certain
regions, as in the southern part of the German Empire,
quite commonly in the intestinal tract of healthy human
beings. Such paratyphoid-carriers, it is supposed, may
contaminate food through handling or preparation
just as typhoid-carriers are known to do. A number
of outbreaks in which contamination of food during
preparation is thought to have occurred have been

^ Jour. Infect. Dis., XX (1917), 457.



FOOD-BORNE PATHOGENIC BACTERIA 67

reported by Jacobitz and Kayser' (vermicelli), Reinhold-
(fish), and others. Reinhold notes that in one outbreak
several persons who had nursed those who were ill
became ill themselves, indicating possible contact
infection. In another outbreak also reported by Rein-
hold it was observed that those who partook of the
infected food, in this case dried codfish, on the first
day were not so severely affected as those who ate what
was left over on the second day. A bacillus belonging
to the paratyphoid group was isolated from the stools
of patients, but not from the dried codfish. These
facts were interpreted as signifying that the fish had
become infected in the process of preparation and that
the bacilli multiplied in the food while it was standing.
There seems no doubt that certain cases of paraty-
phoid food poisoning are caused by contamination of
the food during preparation and are, sometimes at
least, due to infection by human carriers. The bacilli
in such cases are usually (according to many German
investigators) or always (according to most English
bacteriologists) of the B. suipestifer type. Other cases
are due to pathogenic bacteria derived from diseased
animals, and these bacteria are often, possibly always,
of a slightly different character (B. enteritidis Gartner).
It is still unsettled whether both types of food poisoning
bacteria are always associated with disease processes
of man or animals, or whether they are organisms of
wide distribution which may at times acquire pathogenic
properties. In certain regions, as in North Germany
and England, such bacteria are rarely, if ever, found

^ Centralbl. f. Bakl., I Orig., LIII (1910), 377.
^Cor.-Bl.f. schweiz. Aerzte, XLII (1912), 2S1 and 332.



68 FOOD POISONING

except in connection with delinite cases of disease.
In parts of Southwest Germany, on the other hand, they
are said to occur with extraordinary frequency in the
intestines of healthy men and animals. Savage' believes
that there is some confusion on this subject owing to the
existence of saprophytic bacteria which he calls "Para-
gaertner" forms and which bear a close resemblance
to the "true" Gartner bacilli. They can be distin-
guished from the latter only by an extended series of
tests. The bacilli of this group show remarkable
variability, and in the opinion of some investigators
"mutations" sometimes occur which lead to the trans-
formation of one type into another.^

In spite of the present uncertainty regarding the
relationship and significance of the varieties observed,
a few facts emerge plainly from the confusion: (i) The
majority of meat poisoning outbreaks that have been
bacterially studied in recent years have been traceable
to one or another member of this group and not to
"ptomain poisoning." (2) Bacteria of the paratyphoid
cnteritidis group that are culturally alike but agglutina-
tively dissimilar can, when taken in with the food, give rise
to identical clinical symptoms in man. (3) Food poison-
ing bacteria of this group, when derived directly from
diseased animals, seem more likely to be of the Gartner
type {B. enteritidis) than of the B. suipestifer type.

Toxin production. — The problem of the production
of toxin by the bacteria of this group and the possible
relation of the toxin to food poisoning has been much

^ Jour. Hyg., XII (1912), i.

^ Sec Sobernheim and Scligmann, Cciilralbl. f. Bakl., Rcf., Bcilage,
L (1911), 134.



FOOD-BORNE PATHOGENIC BACTERIA 69

discussed. Broth cultures in which the hving bacilH
have been destroyed by heat or from which they have
been removed by filtration contain a soluble poison.
When this germ-free broth is injected into mice,
guinea-pigs, or rabbits, the animals die from the effects.
Practically nothing is known about the nature of the
poisonous substances concerned, except that they are
heat-resistant. They are probably not to be classed with
the so-called true toxins generated by the diphtheria
and tetanus bacilli, since there is no evidence that they
give rise to antibodies when injected into susceptible
animals. In the opinion of some investigators the
formation of these toxic bodies by the paralyphoid-
enteritidis bacilli in meat and other protein foodstuffs
is responsible for certain outbreaks and also for some
of the phenomena of food poisoning, the rapid develop-
ment of symptoms being regarded as due to the ingested
poisons, whereas the later manifestations are considered
those of a true infection. Opposed to this view is the fact
that well-cooked food has proved distinctly less liable to
cause food poisoning than raw or imperfectly cooked food.
A large proportion of the recorded meat poisoning
outbreaks are significantly due to sausages made from
raw meat and to meat pies, puddings, and jellies. This
is most likely because the heat used in cooking such
foods is insufiicient to produce germicidal results. In
milk-borne epidemics also it is noteworthy that the users
of raw milk are the ones affected. For example, respect-
ing an extensive B. enteritidls outbreak in and about
Newcastle, England, it is stated:

In no instance was a person who had used only boiled milk
known to have been affected. Thus in one family, consisting of



70 FOOD POISONING

husband, wife, and wife's mother, the two women drank a small
quantity of raw milk from the farm, at the most a tumblerful,
and both were taken ill about twelve hours later. The husband,
on the other hand, habitually drank a pint a day, but always
boiled. He followed his usual custom on this occasion, and was
unaffected.'

When in addition it is taken into consideration that
the ordinary roasting or broihng of a piece of meat is
often not sufficient to produce a germicidal temperature
throughout, the argument that a heat-resistant toxin
is present in such cases is not conclusive. It must be
remembered also that in some outbreaks those persons
consuming raw or partly cooked meat have been affected
while at the same time others eating well-cooked meat
from the same animal have remained exempt; this
would seem to indicate the destruction of living bacilli
by heat, since the toxic substances formed by these
organisms are heat-resistant. The view that a definite
infection occurs, is favored, too, by the fact that the
blood-serum of affected persons so frequently has an
agglutinative action upon the paratyphoid bacillus.
This would not be the case if the symptoms were due
to toxic substances alone. Altogether the role of toxins
formed by B. enteritidis and its allies in food outside
the body cannot be said to be established. The avail-
able evidence points to infection as the main, if not the
sole, way in which the bacilli of this group are harmful.

Sources of injection. — The main sources of enteritidis-
suipestifer infection are: (i) diseased domestic animals,
the infected flesh or milk of which is used for food;
(2) infection of food by human carriers during the process

' Report Med. Officer of Heallh (Newcastle-upon-Tyne, 19 13).



FOOD-BORNE PATHOGENIC BACTERIA



71



of preparation or serving. To these may be added a
third possibility: (3) contamination of food with bacteria
of this group which arc inhabitants of the normal animal
intestine. Considering these in order:

I. Diseased animals: The majority of the meat
poisoning outbreaks are caused by meat derived from
pigs or cattle. Table III gives the figures for a number
of British' and German^ epidemics.

TABLE III*













Belonging to




B.


:>}TERITIDIS


B. SUIPESTIFER


This Group but
Undifferen-












tiated




British


German


Total


British


German


Total


British


Pig


I


I


2


3


5


8


4


Ox or cow . .


3


9


12


2


3


5


5


Calf





7


7


2




4





Korse




I


I



I

I






I
I


1
I




Chickens . . .









* It must be noted that origin of the food from a diseased animal was not definitely
proved in all the cases cited. Some of these cases should possibly be classed under
human contamination (2).

Occasional outbreaks have also been attributed to in-
fection through eating rabbit, sheep, goose, fish, shrimp,
and oysters. Especially noteworthy is the relative
rarity of infection from the meat of the sheep.

More definite information is needed respecting the
pathological conditions caused by these bacteria in
animals and the relation of such conditions to sub-
sequent human mfection. A rather remarkable problem
is presented by the relation of B. suipestifer to hog
cholera. This bacillus, although not now considered

' Compiled from Savage, Report of Local Gov't Board, 1913.

* Mayer, Deutsche Viertelj.f. djjentl. Gcs., XLV (1913), 8.



72 FOOD POISONING

the causal agent of hog cholera, is very commonly
associated with the disease as an accessory or secondary
invader, and is frequently found in the internal organs
of swine after death. It might be supposed that in
regions where hog cholera is prevalent human infections
would be more common than in other districts, but this
seems not to be the case. No connection has ever
been demonstrated between outbreaks of hog cholera —
in which B. suipestifer is known to be abundantly
distributed — and so-called B. suipestifer infections in
man.

Suppurative processes in cattle, and especially in
calves, have given rise to poisoning from the use of the
meat or milk of the infected animals. It has been often
demonstrated that bacteria of the enteritidis-suipestifer
group are associated with inflammation of the udder
in cows and with a variety of septicemic conditions in
cattle and other domestic animals as well as with
manifestations of intestinal disturbances ("calf diar-
rhea," etc.).' The frequency with which poisoning has
occurred through the use of the meat of "emergency-
slaughtered" animals has been already mentioned.
K. F. Meyer^ has reported an instance of accidental
infection in a laboratory worker caused by handling
a bottle of sterilized milk that had been artificially
contaminated with a pure culture of B. enteriiidis for
experimental purposes. The strain responsible for the

' Although not directly connected with the cjuestion of food poison-
ing, it is of interest to note that certain diseases of birds have been
traced to infection with members of this group of bacteria. In a few
cases, as in several epidemics among parrots in Paris and elsewhere,
the infection has" been communicated to man by contact.

''Jour. Infect. Dis., XIX (1916), 700.



FOOD-BORNE PATHOGENIC BACTERIA 73

infection had been isolated from the heart blood of a
calf that had succumbed to infectious diarrhea.

2. Human contamination: In a certain number of
parat>T3hoid food infections there is some evidence that
the food was originally derived from a healthy animal
and became infected from human sources during the
process of preparation. In addition to the instances
already mentioned (Reinhold et al., p. 67) the Ware-
ham (England, 19 10) epidemic' was considered by the
investigators to be due to infection of meat pies by a
cook who was later proved to be a carrier of paratyphoid
bacilli. The evidence in this case, however, is not
altogether conclusive. Soderbaum^ mentions a milk-
borne paratyphoid epidemic occurring in Kristiania
which was ascribed to infection of the milk by a woman
milker. Sacquepee and Bellot^ report an interesting
paratyphoid outbreak involving nineteen out of two
hundred and fifty men in a military corps. The patients
fell ill on different dates between June 14 and June 21.

It was found that an assistant cook who had been in the
kitchen for several months had been attacked a Uttle before the
epidemic explosion by some slight malady which was not definitely
diagnosed. He had been admitted to the hospital and was
discharged convalescent. The cook, on being recalled and
quarantined, stated that some days before June 10 he was indis-
posed with headache and anorexia. He had nevertheless con-
tinued his service in the kitchen B. paratyphosus B

{B. suipestijer) was repeatedly found in his stools in August,
September, and October In all probability, therefore, the

' R. Trommsdorff, L. Rajchmann, and A. E. Porter, Jour. Ilyg.,
XI (1911), 89.

^ Hygiea, LXXY (igis), i.

J Progres med., 3d series, XXVI (1910), 25.



74 FOOD POISONING

outbreak was due to food contaminated by a paratyphoid-carrier
who had passed through an abortive attack of the fever.'

Bainbridge and Dudfield'' describe an outbreak of acute
gastro-enteritis occurring in a boarding-house; it was
found that no one article of food had been eaten by all
the persons affected, and there were other reasons for
supposing the outbreak to be due to miscellaneous food
contamination by a servant who was a carrier.

There is, therefore, ground for believing that occa-
sional contamination of food may be brought about
by bacteria of this group derived from human sources.
It is not clear, however, how frequent this source of
infection is, compared to infection originating in diseased
animals. It must be admitted, too, that English investi-
gators are disposed to look upon outbreaks similar to
those just described as infections with B. paratypho-
sus B, an organism which they would distinguish from
the "true" food poisoning bacilli, B. enteritidis and
B. suipestifer.

3. Miscellaneous contaminations: Some investiga-
tors, especially certain German writers, regard the bacilli
of the paratyphoid group as so widely distributed
in nature that any attempt to control the spread of
infection is like fighting windmills. According to this
view the bacilli occur commonly in our everyday sur-
roundings and thence make their way rather frequently
into a variety of foodstuffs. Various German investi-
gators have reported the presence of paratyphoid bacilli
in the intestinal contents of apparently normal swine,
cattle, rats, and mice and more rarely of other animals,

' Ledingham and Arkwright, T/ie Carrier Problem in Infectious
Diseases, pp. 152-53.

'Jottr. Hyg., XI (1911), 24.



FOOD-BORNE PATHOGENIC BACTERIA 75

in water and ice, in German sausage and chopped meat,
and in the bodies of apparently healthy men. To what
extent their alleged ubiquity is due to mistaken bacterial
identification, as claimed by some English investigators,
remains to be proved. There is no doubt that in some
quarters exaggerated notions have prevailed respecting
a wide distribution of the true paratyphoid bacteria.
Savage and others believe that the hypothesis that food
poisoning outbreaks are derived from ordinary fecal
infection of food is quite unfounded. It is pointed out
that there is good evidence of the frequent occurrence
of intestinal bacteria in such food as sausages and
chopped meat, and that consequently, if paratyphoid
infections could occur through ordinary contamination
with intestinal bacteria not connected with any specific
animal infection, food poisoning outbreaks should be
exceedingly common instead of — ^as is the case — -com-
paratively rare.

At the present tirtie even those who maintain that
these bacilli are of common occurrence admit that their
abundance is more marked in some regions than in
others. Southwest Germany, for example, seems to
harbor paratyphoid bacilli in relatively large numbers.
Possibly local differences in distribution may account
for the discrepancies in the published findings of German
and British investigators.

A special case is presented by the relation of these
bacilli to rats and mice. Among the large number of
bacteria of the paratyphoid group is the so-called
Danysz bacillus, an organism quite pathogenic for
rodents, and now and again used in various forms as a
"rat virus" for purposes of rodent extermination.
Several outbreaks of food poisoning in man have been



76 FOOD POISONING

attributed on more or less cogent evidence to food
contamination by one of these viruses either directly
by accident, as in the case described by Shibayama,' in
which cakes prepared for rats were eaten by men, or
indirectly through food contaminated by mice or rats
that had been infected with the virus/ The use of
such viruses has not proved of very great practical value
in the destruction of rodents, and is open to serious
sanitary objections, since the animals after apparent
recovery can continue to carry the bacilli of the virus
and to distribute them on or near food substances.

It seems possible that rats and mice may become
infected with certain bacteria of this group without
human intervention, and that these infected animals
may be the means of contaminating foodstuffs and so
causing outbreaks of food poisoning. Proof of the


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