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AN EPIDEMIC OF APPENDICITIS AND PAROTITIS 
PROBABLY DUE TO STEPTOCOCCI CON- 
TAINED IN DAIRY PRODUCTS* 

Edward C. Rosenow and Stella I. Dunlap 

From the Memorial Institute for Infections Diseases, Chicago, and The Mayo Foundation, 

Rochester, Minnesota 

The occurrence of appendicitis in epidemic form, its seasonal 
prevalence, and its occurrence in several members of the same family 
have been noted repeatedly (Mantle, 1 Hood, 2 Martin, 3 Wahle, 4 Haim 5 
and Rostouzew 6 ). 

The epidemic of appendicitis and parotitis studied by us occurred 
at the Culver Military Academy, Culver, Ind. The study was 
made at the request of the superintendent of the academy, Lieut.- 
Col. L. R. Gignilliat, to whom we wish to express our appreciation for 
the opportunity and also to Dr. C. E. Reed for much aid in the work. 
From February 21 to March 5, 1915, a period of 12 days, there occurred 
8 cases of acute appendicitis ; 2 cadets developing appendicitis on the 
same day. Seven of the 8 patients were operated on and the diagnosis 
verified. All recovered. Only 7 cases developed during the rest of the 
school year — 2 in October, 1 in January, 3 in April, and 1 in May. 

Two cadets developed parotitis previous to the sudden outbreak of 
appendicitis ; 5 during the prevalence of appendicitis ; 27 during March 
and April, and 3 in May, making a total of 34 cases. From April 10 to 
18 there occurred an average of 1 new case a day and on April 25 
3 students developed the disease. During the epidemic of parotitis 3 
cadets developed appendicitis. The parotitis was not limited to the 
cadets, whose ages ranged from 15 to 19 years, but occurred in several 
older individuals as well. 

The occurrence, the character, the duration, and the complications 
of the parotitis were typical. The epidemics occurred without associated 
tonsillitis. The cases of appendicitis were so distributed among the 
population as to rule out the factor of trauma from violent exercise. 

* Received for publication October 30, 1915. 

1 Lancet, 1910, 2, p. 57. 

2 Ibid., 1, p. 1645. 

3 Miinchen. med. Wchnschr., 1912, 59, p. 2005. 

4 Ibid., p. 1438. 

6 Arch. f. klin. Chir., 1907, 82, p. 360. 

6 Mitt, a d. Grenzgeb. d. Med. u. Chir., 1906, 15, p. 564. 



384 Edward C. Rosenow and Stella I. Dunlap 

The total number of persons at the academy who ate in a common 
dining room of the same food was approximately 500. Of these, 430 
were cadets, ranging in age from 15 to 19 years; 30 were members of 
the faculty; 40 were helpers, having to do with the preparation and 
serving of the food, etc. The sanitary conditions, the refrigerating 
plant, the kitchen and dining-room, the quality of food served, the 
method of handling food, the mode of life as to exercise, etc., and the 
general physique and health of the cadets were all found to be excellent. 

The dairy products consumed were obtained from 4 independent 
sources. The milk and cream and the ice cream served at the mess 
were from a number of dairies directly under the supervision of the 
authorities at the academy. These dairies were kept in first-class con- 
dition, and the milk was cooled soon after milking, and refrigerated 
continuously until used. The butter, of first-grade quality, was an 
Indiana product from a neighboring town. The cheese was from 
southern Wisconsin. The ice cream served to many cadets at a neigh- 
boring shop was found to be prepared from unpasteurized cream 
obtained from local dairies under unsanitary surroundings and with 
deficient refrigeration. 

Since virulent streptococci have been isolated frequently from the 
udders of cows with mastitis, and even from normal udders in model 
dairies (Rosenow 9 ), and since epidemics of septic sore throat, scarlet 
fever, and typhoid fever have been traced to milk, the possibility that 
the outbreaks under consideration were due to bacteria in the dairy 
products had to be considered. Cultures and animal inoculations were 
therefore made of the milk, cream, butter, and cheese which were for 
general consumption at the mess, and of the ice cream which was con- 
sumed by the cadets at the neighboring shop. A similar study was also 
made of cultures obtained from the tonsils of cadets, of members of 
the corps who prepared and served the food, of members of the faculty, 
and of those that developed appendicitis. 

Tech nic 

The technic of making cultures and animal inoculations was similar to 
that described in connection with the production of appendicitis. 7 Material 
for the cultures in the cases of parotitis was obtained from Steno's duct of 
the involved gland by catheterization and from the tonsils. An attempt was 
made to obtain material from the depth, of the tonsils and not merely by 
swabbing the surface. The sediment of from 50 to 200 c.c. of milk and cream 
was used for the inoculations of the media. The butter and the cheese 

7 Jour. Infect. Dis., 1915, 16, p. 240. 



Epidemic Streptococcal Appendicitis and Parotitis 385 

(approximately 0.5 c.c), obtained in a sterile manner from the depth of a 
freshly cut surface of the original package, were emulsified in 2 c.c. of NaCl 
solution and then planted. 

The bacteriologic study consisted in the main of making blood-agar-plate 
cultures and inoculations of the material to be examined into a series of tall 
columns of ascites (10%) dextrose (0.2%) broth. These were incubated at 
37 C. over night; then the character of the growth on the plates was noted and 
smears of the cultures in broth were made; those cultures in which no bacilli 
or only a few were found, were used for intravenous injection into rabbits and 
dogs. The bacteria for these injections were suspended in salt solution so 
that 1 c.c. contained the growth from 15 c.c. of the broth culture. A portion 
of the suspension injected was again plated on blood agar. The animals, often 
injected in series with doses ranging from 1 to 6 c.c, were chloroformed 
usually in 48 hours, if they had not already died from the effects of the 
injection. The examinations were made as soon after death as possible. The 
organism responsible for the lesions was determined by culture and from 
sections. 

RESULTS OF INVESTIGATION 

Sections from 4 of the human appendices, all showed streptococci, 
some in almost pure growth. In the case of one patient cultures were 
made both from the tonsils and from the wall of the appendix. That 
from the tonsils showed a predominating number of short-chained, 
green-producing streptococci, a few hemolytic streptococci, and a 
moderate number of Micrococcus catarrhalis ; those from the wall of 
the appendix showed colon bacilli and green-producing streptococci. 
The culture in ascites dextrose broth from the tonsils of this patient 
was injected into 3 rabbits. All remained well and none showed lesions 
in the appendix. The growth from the appendix wall produced lesions 
in the appendix in 2 of 4 rabbits. 

The findings in the case of another patient further illustrate the 
results obtained: 

M., a cadet who developed symptoms of acute appendicitis on February 21, 
was operated upon on the following day and the acutely inflamed and edema- 
tous appendix removed. The lumen of this appendix was found to be very 
narrow and filled with bloody pus. There was no fecal concretion or other 
foreign body, and there were no constricting bands. The peritoneal coat was 
edematous and opaque and over the portion near the distal end was a thin 
fibrinous exudate. The mucous membrane was edematous and hemorrhagic 
throughout the larger portion, this condition extending well into the submu- 
cosa and the peritoneal coat. Sections showed an enormous number of strep- 
tococci within the lumen and within the infiltrated membrane (Figs. 1 and 2). 
Scattered diplococci were found also in the adjacent lymph follicles and in the 
peritoneal coat. In the lumen there were also a few gram-negative bacilli 
resembling colon bacilli, and what appeared to be fusiform bacilli. Cultures 
from a swab of the tonsils sent me by Dr. Reed 10 days after the operation, 
showed a predominating number of green-producing streptococci, a few colo- 



386 



Edward C. Rosenow and Stella I. Dunlap 



►■■; ^iffifiA 




Fig. 1. Section of the appendix in human appendicitis. Note the sloughinjr of the 
mucous membrane, the hemorrhagic and leukocytic infiltration in the lymph follicle, the 
mucous membrane, and the submucosa. Hematoxylin and eosin. X 75. 




Fig. 2. Streptococci in submucosa at a, shown in Fig. 1. Gram-Weigert. X 1200. 



Epidemic Streptococcal Appendicitis and Parotitis 387 

nies of hemolyzing streptococci, and a large number of colonies of Micrococcus 
catarrhalis. The broth culture revealed a pure growth of a short-chained strep- 
tococcus. Two rabbits were injected with the latter culture, one of which 
showed hyperemia and hemorrhages in the mucous membrane and the peritoneal 
coat of the appendix. It also showed a few hemorrhages in the tricuspid 
valve. The other rabbit showed only a slightly turbid joint fluid. Cultures 
from the blood of both on blood-agar plates disclosed pure growths of green- 
producing streptococci. The emulsion of one of the areas of hemorrhage in 
the peritoneal coat of the appendix showed many green colonies of streptococci. 
On June 4 cultures from the tonsils were made again. The tonsils were 
larger than normal but not badly infected. The culture in ascites dextrose 
broth was injected into one rabbit; it developed a number of small hemor- 
rhages in the appendix with hyperemia and edema, as well as a marked 
hemorrhagic edema of the parotid and associated lymph glands. There were 
also a number of hemorrhages in the muscles, particularly in the adductors 
of the thighs. The localization in the parotid is of interest, especially since 
this individual was the janitor in the hospital in which the patients with 
parotitis were treated and hence may be considered a possible carrier. 

TABLE 1 

Localization of Streptococci Following Intravenous Injection 



Sources of Streptococci 


Time of Experiments 


Animals 


Strains 


Percentage of 

Animals Showing 

Lesions in 




Appen- 
dix 


Paro- 
tid 


Tonsils 


Normal individuals 


Soon after epidemic of 
appendicitis (March) 

Soon after epidemic of 
parotitis (June) 


49 
30 


43 
30 


30 
6 


10 

20 




Individuals that had 
had appendicitis 


Soon after epidemic of 
appendicitis (March) 


19 


4 


47 





Dairy pr 


oducts 


Soon after epidemic of 
appendicitis (March) 

During epidemic of paro- 
titis (March and April) 

Soon after epidemic of 
parotitis (June) 


22 
28 
10 


9 
8 
6 


41 




9 
29 




30 


Steno's duct in parotitis 


During epidemie of paro- 
titis (March and April) 


19 


9 


15 


73 



Table 1 gives a summary of the results following intravenous injec- 
tion of streptococci isolated from tonsils, dairy products, and Steno's 
ducts. It is seen that the cultures obtained from the tonsils of normal 
individuals soon after the epidemic of appendicitis, and at the beginning 
of the epidemic of parotitis produced lesions of the appendix in 30%, 
and in the parotid gland in 10% of the animals injected. After the 
epidemic of parotitis, cultures made in exactly the same way produced 
lesions in the appendix in 6% and in the parotid in 20% of the animals 
injected. The lesions in the appendix here correspond with the average 



388 Edward C. Rosenow and Stella I. Dunlap 

incidence of lesions in the appendix (5%) following injection of stepto- 
cocci from a wide range of sources. 8 The cultures made soon after the 
epidemic of appendicitis from the tonsils in individuals who had had 
appendicitis produced this disease in 47% of the animals injected and 
no lesions in the parotid. Strains isolated from the dairy products soon 
after the epidemic of appendicitis, including cultures up to March 19, 
produced lesions in the appendix in 41%, and in the parotid in 9% of 
the animals injected; while during and soon after the epidemic of 
parotitis the strains failed to produce appendicitis, but produced paro- 
titis in 29 and 30%, respectively, of the animals injected. The strepto- 
cocci obtained from patients having parotitis during the epidemic pro- 
duced lesions in the appendix in 15%, and in the parotid in 73% of the 
animals injected. 

In this connection it should be noted that 4 of the 6 individuals 
whose tonsils were cultured and who had to do with the serving of 
food, including the waiter at the table at which 2 cadets developed 
appendicitis on the same day, showed streptococci having affinity for 
the appendix of rabbits. One of them is subject to repeated mild 
attacks of appendicitis. 

The average incidence of lesions in the various organs and the rate 
of mortality in animals injected with cultures from the tonsils or the 
throats of 46 normal individuals during March was 14 and 41%, 
respectively ; while during June they were only 8 and 33%, respectively. 
The evidence of infection in the tonsils was distinctly greater during 
March, altho none of the individuals complained of sore throat and in 
none was the inflammation acute. The occurrence of lesions was more 
frequent in the animals injected with cultures from distinctly infected 
tonsils (18%) than in animals injected with cultures from more normal 
tonsils, or normal throats (4) in which there had been a previous ton- 
sillectomy (10%). Likewise, there was a distinctly higher incidence of 
lesions and a greater rate of mortality following injection of streptococci 
from the dairy products during March and April (11 and 26%, respec- 
tively) than during June (8 and 10%, respectively). These findings 
suggest that the seasonal prevalence of streptococcal throat infections 
is largely due to an increase in infective power of the streptococci in 
tonsils and possibly in dairy products as well. 

It must not be supposed that the lesions in the appendix and the 
parotid are merely accidental. Cultures from the milk and the cream 
produced lesions in the appendix on March 6 and 19 while those 

8 Rosenow: Jour. Am. Med. Assn., 1915, 65, p. 1687. 



Epidemic Streptococcal Appendicitis and Parotitis 389 

injected on March 13, April 25, and June 4 failed entirely to produce 
lesions. In only one rabbit did the cultures from the milk and the 
cream produce parotitis (March 12). Cultures from the butter, made 
on March 5 and 13 and on April 9 and 25 and June 4 did not produce 
lesions in the appendix in rabbits, but did produce lesions in the parotid. 
Cultures from samples of butter obtained on April 9 showed a large 
number of 2 types of colonies of streptococci : the one produced distinct 
green colonies on blood agar ; the other produced smaller, grayish, ele- 
vated, round colonies surrounded by a narrow hazy zone of hemolysis. 
Injections of the mixture produced marked edema and hemorrhage of 
the parotid in 2 rabbits. Pure cultures from the latter (second culture) 
produced marked edema and hemorrhage of the parotid in 2 of 3 rab- 
bits. The strain which grew in pure culture in dextrose broth produced 
similar lesions in 2 rabbits, and after injection into Steno's duct in each 
of 3 dogs produced the swelling and cellular infiltration considered 
characteristic of mumps. (The results of the experiments with the 
organism from parotitis, which closely resembled the organism 
described by Herb, 9 will be detailed in a separate paper.) The cultures 
from the cream and the ice cream supplied at the neighboring shop 
produced marked lesions of the appendix in 2 rabbits injected March 
19, while cultures on two subsequent occasions after the plant was 
remodeled failed to produce either appendicitis or parotitis. Cul- 
tures from the cheese failed to produce either appendicitis or 
parotitis on March 15, but produced appendicitis on March 13, and 
parotitis on April 25 and on June 4. Cultures made May 7 and June 
4 from butter and ice cream from another source failed to produce 
either appendicitis or parotitis. Investigation showed that in the com- 
munities where the butter and the cheese were manufactured mumps 
was present in epidemic form during April and May — the time during 
which parotitis was so prevalent at the academy and during which there 
were found in the butter and the cheese streptococci having such marked 
affinity for the parotid gland. The possibility of infection of the butter 
and the cheese with these strains at the academy is excluded because 
the cultures were made from the original packages ; but whether these 
strains were from human sources or were from the udders of cows it is 
impossible to say. It might be said, however, that the fermentative 
powers of some of the strains having affinity for the appendix suggest 
the latter origin, while those of strains producing the parotitis suggest 
the former source. 

9 Arch. Int. Med., 1909, 4, p. 201. 



390 Edward C. Rosenow and Stella I. Dunlap 

The cultures from the dairy products showed a preponderance of 
non-hemolyzing, short-chain-producing streptococci, often in almost 
pure form and in enormous numbers. Slightly hemolyzing streptococci 
were found occasionally. All were of a relatively low grade of viru- 
lence, but those producing parotitis caused death more frequently than 
did those producing appendicitis. 

The importance of the streptococci contained in the dairy products 
as a possible source of infection for man is further shown by the fact 
that 6% of the animals injected showed ulcer of the stomach, 6% 
cholecystitis, 28% arthritis, 6% endocarditis, 20% myocarditis, and 
26% myositis. The high incidence of myositis and myocarditis, which 
occurred 2 and 5 times as often as they occur with streptococci from 
the tonsils, is of special interest and in accord with the findings of 
Rosenow and Moon, 10 who showed that streptococci from milk during 
an epidemic of sore throat had a marked affinity for the muscles in 
animals. 

The lesions other than those in the appendix and the parotid follow- 
ing injection of streptococci from the tonsils parallel very closely 
indeed those obtained previously by one of us 11 with streptococci from 
similar sources. It is realized of course that in man liability to infec- 
tion following ingestion of the streptococci is less than it is in animals 
following intravenous injection. Yet, that infection may occur must 
be conceded. 

The normal individuals during (10%), and immediately after 
(20%), the epidemic who harbored streptococci having elective affinity 
for the parotid in animals, must be regarded as carriers. 

It would appear, then, that these epidemics of appendicitis and paro- 
titis were due to streptococci contained in dairy products. This fact 
and the fact that milk is such an excellent culture medium make efficient 
pasteurization, or some other means of destroying the pathogenic bac- 
teria which may be present in milk, imperative in order that the public 
health may be safeguarded. 

10 Jour. Infect. Dis., 1915, 17, p. 69. 

11 Rosenow: Ibid., 1912, 11, p. 338.