CHAPTER XIX
Staphylococcal and Streptococcal Food Poisoning and Botulism
G. M. Dack, M. D.1
STAPHYLOCOCCAL FOOD POISONING
Experiences Before World War II
Staphylococcal food poisoning has probablyoccurred for hundreds of years. From the period of1870, when the occurrence of cocci in inflammatory processes was firstobserved, through thefirst three decades of the 20th century, the cause of these outbreakswas not generally recognizedbecause of the ubiquitous nature of the organism and the failure todemonstrate enterotoxin inimplicated foods as well as in cultures of Staphylococci isolatedfrom foods. Many outbreaks ofstaphylococcal food poisoning have falsely been ascribed to ptomainepoisoning or to productsfrom other bacteria which were toxic when injected parenterally intoanimals.
Staphylococcal food poisoning is not a reportable disease in our civilian populations, and usually only the large and spectacular outbreaks are reported. The disease has been common in armies. A good illustration of this occurred among the German troops in World War I.2 Although this outbreak was attributed to the bacillus Proteus vulgaris, it was obviously an outbreak of staphylococcal food poisoning since micrococci were found in the product upon bacteriologic examination and since the symptoms and epidemiologic features were characteristic of staphylococcal food poisoning. The following excerpts were translated from this report:
* * * Therefore Iam going to report in the following about an extensive sausagepoisoning outbreak (approximately2000 cases) which took place in the spring of 1918 during the siege ofVerdun and which could possibly have led tocatastrophical military consequences.
In the beginning of June 1918 all of a sudden mass outbreaks which had the appearance of acute gastro-enteritis and which, in some severe cases, were even increased to cholera nostras, spread among the troop surrounding Verdun; with a single blow, whole companies were disabled with the exception of just a few people, and within two days about 2000 men had been attacked. The symptoms were so severe in part of the troops that more
1Theauthor is indebtedto Maj. (later Lt. Col.) Everett B. Miller, VC, Office of the SurgeonGeneral, VeterinaryDivision, for his painstaking work in gathering the source materialused in this manuscript.
2Baerthlein,K.: Ueberausgedelhnte Wurstvergiftungen, bedingt durch Bacillus proteusvulgaris. München.med. Wchnschr. 69: 155-156, February 1922.
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than 200 sick people had to be transferred to field hospitals.Suspicion of food poisoning arose since, according tostatements by the sick people, severe illness set in 2-3 hours (with asmaller part of the sick 6-8 hours) after the ingestion of a certainsausage dish. Only those people among the fronttroops who had not partaken in the meal were spared, i. e. orderlies ofthe company who on the same day had goneback to headquarters to receive orders; or soldiers who for otherreasons had not eaten the sausages, and those partsof the troops who were in rest billets and had a different diet.However, it was surprising that among the troopsbehind the front, i. e. the corps butchers, who had eaten from the samesausages though two days earlier, no cases ofsickness were observed * * *.
Situation at the Beginning of WorldWar II
At the beginning of World War II, staphylococcalfood poisoning was recognized in publichealth laboratories, but it was not generally known to practicingphysicians. Many largeoutbreaks were reported in civilian defense establishments 3andin military establishments,including personnel in the Pentagon, as well as among troops in campsand in the field.4
Methods of control.-The control of staphylococcal food poisoning is concerned principally with the refrigeration of perishable foods which furnish a medium for the growth and enterotoxin production of Staphylococci. Where recurrent outbreaks have occurred,5 carriers have been sought among the foodllandlers because in some outbreaks enterotoxic strains of Staphylococci have been demonstrated in pyogenic lesions as well as in the noses and throats of carriers. Other control measures are concerned with scrupulous cleanliness, with particular attention being given to cutting boards and all kinds of cooking utensils.
Research.-Research should be directed towardpurification and isolation of the enterotoxin withthe hope that this approach will lead to a better method of assayingenterotoxin. If a good assaymethod were available, progress could be made in processing andprotecting foods fromstaphylococcal food poisoning. Investigation in this field isexpensive, and the problem involvessuch a wide segment of the food industry that no one industry can carrythis research load. TheArmed Forces and Government agencies should cooperate in this programto hasten the solutionof the problem.
Outbreaks During World War II
Staphylococcal food-poisoning outbreaks arecosmopolitan and have occurred among troops inall the war theaters, as well as on the homefronts. Sincestaphylococcal food poisoning is notgenerally reported even in the Army, there is no accurate informationas to its magnitude. Asurvey of the outbreaks of food poisoning reported in the Army in WorldWar II was tabulatedunder the following headings: Code, unit, location and date,epidemiology, case
3 Getting, V. A.,Rubenstein, A. D., and Foley, G. E.: Staphylococcus and StreptococcusCarriers: Sources of Food-borne Outbreaks in War Industry. Am. J. Pub.Health 34: 833-840, August 1944.
4 Williams, G. C.,Swift, S., Vollum, R. L., and Wilson, G. S.: Three Outbreaks ofStaphylococcal Food PoisoningDue to lce-Cream. Month. Bull. Min. Health & Emerg. Pub. HealthLab. Serv. 5:17-25, January1946.
5 See footnotes 2, p. 433, and 4.
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history, food, laboratory findings, remarks, and document. Underthis method of tabulation, 190outbreaks involving 22,364 cases were reported for all causes. In thistabulated summary, muchof the information was not available, and in some instances not eventhe number of cases wasreported. Of the 190 outbreaks reported, 76 were chosen in which theepidemiologic data,together with the laboratory findings, suggested staphylococcal foodpoisoning. These 76outbreaks involved 14,214 men. In addition to these 76 outbreaks, manyof the others may verywell have been staphylococcal food poisoning, but the informationavailable was inadequate toestablish them definitely as such. From a study of the data,staphylococcal food poisoning waswithout doubt the most important cause of the illnesses.
These 76 outbreaks of staphylococcal food poisoning occurred during the following months of the 4-year period from 1942 through 1945:
Month | Number of outbreaks |
January | 2 |
February | 6 |
March | 8 |
April | 6 |
May | 9 |
June | 12 |
July | 10 |
August | 2 |
September | 5 |
October | 7 |
November | 6 |
December | 3 |
More outbreaks occurred in each of the months May, June, and July than in the other months of the year. The seasonal incidence may have less meaning in view of the fact that Army personnel were scattered in many parts of the world where the prevailing temperatures differed for the separate geographic areas according to months. The inconstant and shifting Army populations in these different areas, together with the fact that the reported outbreaks probably are only a small part of the total, make this information unsuitable for statistical analysis. Furthermore, in many outbreaks epidemiologic and laboratory studies either were not done or were inadequate to permit the drawing of conclusions.
The number of outbreaks reached a peak in 1944 (41 of the 76 selected outbreaks). This number was far greater than reported in the two preceding years (5 and 8) and almost twice as great as reported for the following year (22). This yearly incidence is subject to the same variables mentioned for the seasonal incidence. Although the yearly average of the strength of the, Army reached a peak in 1944, there is not a direct relationship between the yearly number of outbreaks and the number of men at risk for that period. Furthermore, information disseminated through Army regulations, training manuals,
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and training courses may also have influenced recognition and reportingof outbreaks. 6 With thebetter understanding of the causes of staphylococcal food poisoning,more care may have beenutilized in the use of leftovers and in the provision for more adequaterefrigeration of perishablefoods, thus influencing the yearly incidence of the disease.
A list of foods involved in the staphylococcal food-poisoning outbreaks comprises some 43 different food items, the most common of which are as follows:
Foods involved | Number of outbreaks |
Bread pudding | 11 |
Ham | 9 |
Potato salad | 6 |
Rice pudding | 3 |
Ice cream | 3 |
Turkey | 3 |
Roast veal | 3 |
Ham salad | 2 |
Macaroni and chicken | 2 |
Ham sandwich | 2 |
Foods which were involved in 76 staphylococcal food-poisoning outbreaks comprising a total of 14,214 cases were as follows:
Food | Number of times | Food | Number of times |
Meat | Desserts | ||
Canned pork sausage | 1 | Rice pudding | 3 |
Canned corned beef or tongue | 1 | Ice cream | 3 |
Corned-beef stew | 1 | Bread pudding | 11 |
Frankfurters | 1 | Tapioca pudding | 1 |
Hamburger | 1 | Fruit pudding | 1 |
Roast veal | 2 | Pumpkin pie | 1 |
Ham salad | 2 | Cream filler of layer cake | 1 |
Beef | 1 | Peanut-butter pie | 1 |
Ham | 9 | Boston cream pie | 1 |
Roast beef | 1 | Vegetables | |
Liver-sausage sandwich | 1 | Canned corn | 1 |
Ham sandwich | 2 | Potato salad | 6 |
Ham omelet | 1 | Fried potatoes | 1 |
Hash | 1 | ||
Poultry | Miscellaneous | ||
Turkey | 3 | Turkey dressing | 1 |
Chicken a la king | 1 | Thanksgiving meal | 1 |
Chicken fricassee | 1 | Egg or roast-beef sandwiches | 1 |
Chicken salad | 1 | Macaroni salad | 1 |
Chicken pie | 1 | Cream | 1 |
Turkey a la king | 1 | Egg salad sandwich | 1 |
Creamed chicken | 1 | Vegetable soup | 1 |
Macaroni and chicken salad | 2 | Liver cheese | 1 |
Unknown | 1 |
6 (1)AR 40-205, 31Dec. 1942. (2) AR 40-210, 25 Apr. 1945.
(3) TM 8-227, 11 Oct.1946. (4)TM 8-210, 20 Mar.1942,
(5) TM 8-227, 17 Oct. 1941.
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Of the 76outbreaks, 21 were selected for which the data were most complete. Ofthese 21outbreaks, involving 5,370 men, 8 occurred in the European theater, 1in the Mediterraneantheater, 9 in the Zone of Interior, 1 aboard ship, and 2 in theCaribbean Defense Command. Ofthe 5,370 men ill, 1,059 were hospitalized. There was one death whichoccurred in a patienthospitalized with coronary heart disease. Of these 21 outbreaks, therewas I in which only 17men were involved, whereas the largest involved 1,637 men. The onset ofillnesses following theincriminated meals was reported as varying from 15 minutes to as longas 8 hours. In allinstances, the duration of illness varied from 6 to 48 hours and wasfollowed by weakness anddiarrhea which lasted as long as 48 hours. From 13 of the 21 outbreaks,laboratory studies weremade, and Staphylococci wereisolated from the incriminated foods.
In the 21 selected outbreaks, the time of onset following a specific meal and the symptoms of illness were typical of those which characterize staphylococcal food poisoning and set it apart from other types of gastrointestinal illnesses. The average period of onset of illness following a meal was slightly less than 3 hours. The symptoms included one or all of the following: Nausea, vomiting, abdominal cramping, and diarrhea. In severe cases, prostration occurred and the patients developed shock. Such cases were treated with fluids parenterally and made rapid recoveries. Fever or subnormal temperatures were rarely reported.
A history of the implicated food is given for 15 of these outbreaks, and in each of these the food stood for several hours at a warm temperature before being served. In two cases, the food item was stored in a warming oven for 7 hours before serving. One outbreak involving ham salad illustrates the folly of attempting to refrigerate large volumes of food. In this outbreak, ground ham was packed in 12-gallon containers and placed in the refrigerator. It is obvious that if the ham was warm when placed in such containers, it would require hours for the ground ham in the center of the container to reach refrigeration temperature. In two outbreaks, frozen ham was cooked and served the same day with no illnesses; the leftover portions were kept out of the refrigerator and served the following morning, causing severe illness. In 1 of these 2 outbreaks, 10 hours elapsed between servings.
Ice cream was involved in two outbreaks. A history of preparation was given in only one. In this incident, a portion of the mix was frozen in the hospital in which it was prepared and served to 30 to 40 people without causing any illnesses. The largest portion of the same mix, however, was kept at room temperature before it was frozen. There were 399 men made, ill from the later preparation of ice cream.
One of these 15outbreaks illustrates the thermostability of the enterotoxin. Thisoutbreakinvolved chicken pie in which the chicken was cooked and stored at roomtemperature for 16hours before being made into the pie which was served immediately aftercooking. Apparently,the cooking of the chicken pie did not destroy the enterotoxin whichwas probably formed duringthe 16-hour period in which the chicken was out of refrigeration.
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Summaryof Experiences
Staphylococcalfood poisoning frequently occurs in the Army. It is conceivable thatits untimelyappearance in troops may lose battles, as was pointed out in the caseof the Battle of Verdun inWorld War I. The incidence of staphylococcal food poisoning in WorldWar II is not known,since many outbreaks are not reported and since some of those reportedmay have been causedby Staphylococci but were not so classified because of insufficientdata. From the study of 190tabulated outbreaks involving 22,364 cases of illness, 76 outbreakswere selected wheresufficient data were available to classify them as staphylococcal foodpoisoning. The 76outbreaks involved 14,214 men. The illnesses usually appeared withinfrom 3 to 4 hoursfollowing a meal and were characterized by nausea, vomiting, diarrhea,and, in the acute cases,prostration.The acute symptoms lasted only a few hours, and in generalmen returned to dutywithin from 24 to 48 hours.The outbreaks of food poisoning due toStaphylococci were reportedfor all months of the year but were highest in the warm months, May,June, and July.
Forty-two different food items were involved comprising meat, poultry, desserts, vegetables, dairy products, and miscellaneous items. Of the 76 outbreaks attributed to Staphylococci, 21, for which the data were most complete, were selected for study. For 15 of these 21 outbreaks, a history of the handling of the implicated food was available, and in all cases the food had stood for several hours at a warm temperature before being served. The danger inherent in the use of leftovers was demonstrated repeatedly in the series of incidents under study. Examples were cited emphasizing (1) the length of time for enterotoxin production; (2) the failure to obtain rapid chilling in food refrigerated in large containers; and (3) an example of perishable food stored at room temperature and then cooked before serving, thus illustrating the thermostability of enterotoxin.
Although thedanger of staphylococcal food poisoning had been emphasized in Armyregulationsand other written communications in the Army, outbreaks continued tooccur. It is important thatinformation such as detailed here be made available to all personnelresponsible for handlingperishable foods.
STREPTOCOCCALFOOD POISONING
Outbreaks ofgastrointestinal illnesses caused by Streptococcus faecalishave been reported.7Human volunteers, who were fed large numbers of Str. faecaliswhich had been recently isolatedfrom implicated foods, developed illnesses identical to those describedin the outbreaks.Knowledge of this type of food poisoning is incomplete. In foodpoisoning attributable to Str.faecalis, the living organisms are responsible for illness and notpreformed toxins as instaphylococcal food poisoning or botulism.
7 Dack, G. M.: FoodPoisoning.Chicago: The University of Chicago Press, 1949.
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In outbreaksoccurring in the Army, little or no effort was made to look for Str.faecalis in theincriminated items of food.Several of the 190 outbreaks tabulated inthis series were suggestiveof Str. faecalis food poisoning. In only 1 of the 6 outbreakswas Str. faecalis demonstrated in theimplicated food. In the others, there were either no samples of thefood available or laboratorytests were not made.
These 6 outbreaks involved 1,015 men. Two were reported for the European theater, one from the Panama Canal Zone, and three from the Zone of Interior. The food items were turkey, lamb, canned meat and vegetable stew, canned creamed corn, veal dressing, and meat-hash sandwiches. The onset varied from 4 hours to 18 hours. The illnesses were usually mild, with little or no vomiting, and were characterized principally by abdominal cramps, nausea, and diarrhea. In general, recovery was complete in from 16 to 24 hours.
In all sixoutbreaks, perishable foods were kept out of refrigeration for varyingperiods of time.In the case of the turkey outbreak, 140 turkeys were cooked on anafternoon and evening withfacilities that accommodated 8 turkeys at a time. The followingmorning, the turkeys were slicedand placed in pans and stored in the refrigerator for 24 hours. Themeat was served at noon. Alpha-type streptococci were isolated from theturkey in this outbreak, which involved266 men. The lamb outbreak followed the use of leftover lamb that waskept out of refrigerationfor 24 hours. In the meat and vegetable stew outbreak, several of thecans contained gas, and thecontents were reported to have had a strong odor, when they wereopened. It was suggested thatone or two of the spoiled cans may have been used in preparing themeal. The outbreak traceableto creamed corn resulted from use of a product which had been left overfrom a previous meal.The veal dressing was prepared from chopped frankfurters left over froma meal 5 dayspreviously, stale bread, onions, cheese and macaroni left over from ameal 24 hours before, andscrambled eggs left over from breakfast of the day on which thedressing was prepared. A verypertinent remark for the last outbreak is made by the surgeon reportingit: "* * * so far as healthis concerned, food wastage is preferable, to food poisoning * * *." Themeat-hash sandwicheswere prepared a day previous to serving, although they wererefrigerated after preparation. Thereis no statement of the time required for the preparation and the lengthof time beforerefrigeration.
Str. faecalis food-poisoning outbreaks occur in the Army, although this type of food poisoning is not generally recognized. Laboratory and epidemiologic studies are necessary to establish the diagnosis.
In 6 selectedoutbreaks from the group of 190 studied, Str. faecalis wasconsidered the probableetiologic agent. In 5 of the 6 outbreaks, there was a definite historyof perishable food itemshaving been kept out of refrigeration for several hours.
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BOTULISM
There are records of civilian outbreaks of botulismin the United States and Canada dating backto 1899,8 and from then until 1918 the numberof outbreaks reported yearly varied from none toseven. However, beginning with 1918, when 16 outbreaks were reported,and following throughto include 1947, the annual number of outbreaks has varied from 3 to25, with an average of 13.9per year. The highest incidence of botulism from canned goods packed inthe United Statesoccurred in 1920 (6 outbreaks). Since 1925, with one possibleexception, no cases have occurredfrom commercially canned goods packed in the United States.The sharprise beginning in 1918may have been caused by the increase in preservation of foods becauseof the war. The publicityand better recognition of the disease after 1918 may explain why thenumber of outbreaks hasnot decreased since that time.
The control of botulism has been effectively developed by the canning industry in the United States. This disease occurred among only 23 men in the United States Army in World War II, with 9 deaths, giving a case fatality rate of 39 percent. The 23 cases were represented in 4 outbreaks. The first occurred from commercially canned beets packed in Australia in November 1942. In this outbreak, there were 16 cases and 7 deaths, with a case fatality rate of 44 percent. The other three incidents involved home-preserved products. In August 1944, an outbreak occurred in the European theater from home-canned ravioli which was sent to one of the enlisted men by his parents in the United States. There were 3 cases with 1 death. In January 1945, in the United States, a family had sent their son home-canned mushrooms, which caused 7 cases with 1 death among non-Army personnel as well as 1 nonfatal case in a soldier. The fourth outbreak, causing 3 cases with 1 death, occurred in April 1945 in Germany and was due to pickles and preserves found in a cellar of a home.
Since the Armyuses commercially canned products and the canning industry in theUnitedStates is keenly aware of the botulism hazard, there are norecommendations necessary in thisdirection. During World War II, the author evaluated a botulism hazardfrom dehydrated meats,and the industry and using agencies for these products were apprised ofthe hazard. Instructionswere issued for preventing botulism from the use of these products. Inrecent years, theQuartermaster Corps has been developing canned bread, which is anonsterile product, and thehazard involved has been investigated under experimental conditions, inthe author's laboratory.The specifications for the manufacture of canned bread have beenrigidly set to safeguard thisproduct from botulism. If new nonsterile items are introduced, thefoodpoisoning risk should beconsidered for each item and control measures instituted before theitem is placed in production.Since 3 of the 4 outbreaks were from home-preserved items consumed bysoldiers, in theory itmight
8 See footnote 7, p. 438.
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seem desirable to prohibit thesending of food items in which there may be a hazard frombotulism, but such selective regulation of items is obviously apractical impossibility. Data forUnited States Army personnel only indicate that in 3 of the 4 outbreaksantitoxin wasadministered to 6 cases, 1 of whom died, representing a case fatalityrate of 17 percent. Threeoutbreaks occurred between August 1944 and April 1945. In the otheroutbreak, which occurredin November 1942 in Australia, there were 16 cases with 7 deaths amongUnited States troops.No mention is made as to whether antitoxin was available or given, andthe case fatality rate was44 percent. The food was of Australian manufacture, and, prior to thearrival of United Statestroops, both New Zealand and Australia had done very little commercialcanning of foods. Underlend-lease agreement, these countries undertook to supply hugequantities of canned food toUnited States Armed Forces with resulting need for tremendous and rapidexpansion of theircanning industry. Despite assistance by technical experts from theUnited States, it wasinevitable that time would be required to bring productive methods to alevel equal to UnitedStates standards. Although the incidence of botulism in the UnitedStates Army is small, it issuggested that supplies of botulinus antitoxin be available to takecare of emergencies, such asthe occasional outbreaks reported here. Furthermore, thought should begiven to having availablea supply of antitoxin in the event that botulinus toxin is used as anagent in biologic warfare.
