S. V. Androsova, A. E. Vydrevich, A. S. Karataeva (Moscow)

On the Effect of Heat Treatment of Food Products on the Survival of bac. coli and bac. proteus in Them

Food Department of the Erisman Institute of Sanitation and Hygiene
Head: Professor A. V. Reisler

The extraordinary growth in the USSR’s need for public catering, and the exceptionally rapid expansion of the network of factory kitchens and large and small dining halls associated with it, make it necessary to study food preparation processes from a sanitary standpoint and to examine their effect on the quality of the finished product.

During their passage from the point of initial procurement to the factory kitchen or dining hall, and their subsequent processing into food, products may be subject to continuous contamination. This is facilitated by the still insufficient qualifications of the personnel responsible and the lack of sanitary training among public catering workers. It is known that contamination of food products is accompanied by heavy microbial contamination; the microorganisms involved may include both specific pathogenic microbes and saprophytes, which are constant companions of all contamination, organic decomposition, and putrefaction.

There is a widespread belief that, however heavily contaminated a food product, prepared dish, or semifinished product may be, it need only be placed in an oven or on a stove, even for a short time, to kill and destroy all the microorganisms that have entered it, since heat treatment eliminates any danger from contamination occurring during culinary preparation. Cases of illness associated with the consumption of prepared dishes are therefore often attributed to bacterial contamination of the product after heat treatment. However, individual food-poisoning incidents that occurred in Moscow in 1933 showed that a large proportion were bacteriological in nature and that many of these were caused not by specific pathogens but by saprophytes—bacteria of the coli and proteus groups present in contaminated food products. Such agents cause food poisoning in a number of countries, as well as in our own. Recently published data by Bekenfeld¹ indicate that, of 55 cases of meat poisoning observed in Germany in 1929 and 1930, pathogenic agents were found in only 40; in the remaining cases, the illnesses were caused by so-called saprophytes, which had permeated the meat throughout.

The discovery of bacteria of the coli and proteus groups among the causative agents in the poisonings of 1933 once again demonstrated convincingly that these incidents depended on the sanitary condition of factory kitchens and dining halls and on the technological processes used to prepare food in them. This prompted a series of major measures that brought about a considerable improvement in sanitary conditions at public catering establishments. The same circumstances led the Food Department of the Erisman Institute to investigate whether heat treatment of food products in hot-food preparation areas—that is, keeping a dish in an oven or on a stove—really guarantees its almost complete freedom from microorganisms.

To answer this question, it was first necessary to study the temperatures at which food products undergo heat treatment and the sanitary conditions both in the hot-food preparation area and during the preceding culinary preparation of the dishes.

Observation of work in the hot-food preparation areas of factory kitchens reveals a striking difference between the working conditions of the day and night shifts. Whereas the day shift works under conditions of normal labor productivity, the night shift is extremely overloaded with work—

¹ Ergebnisse der Bakterioskopie von Fleischwaren. Ztr. f. Untersuchung der Lebensmittel, June 1934.

…—each worker on the night shift has more items to process than a worker on the day shift. This results in food being processed with extreme haste on the night shift and in shorter frying, baking, boiling, and other cooking times; the time dishes spend over the heat is reduced to nearly half that on the day shift. Thus, cutlets are fried for approximately 14–16 minutes during the day, but only 8–10 minutes at night. Mass production and the need for speed lead to trays being hurriedly filled with prepared items, which are crushed and broken. The small quantity of fat allotted for frying is reduced still further by defective trays: the fat leaks onto the stove, producing smoke, hindering the work, and distracting attention from the food being fried. Day-shift workers, not being overburdened, select sound trays, load them more carefully with prepared items, and pay closer attention to the processes taking place on the stove and in the oven. It would, of course, be a mistake to assume that all is entirely well in the hot-food departments during the day shift: stoves are far from always in good working order, and their surfaces are not always evenly heated. As on the night shift, trays are constantly moved about on the stove, sometimes onto strongly heated areas and sometimes onto weakly heated ones; and cooks, in order to brown a dish more thoroughly and thus give it the outward appearance of having been well heated, surreptitiously pour oil beneath the trays.

Because staff do not always exercise strict economy in their use of fat, and sometimes because supplies are interrupted, fat runs short. The dish is then fried on the stove with some water added—that is, it is more nearly boiled—and in the oven it is often merely dried on the surface. In general, frying and baking methods and techniques are extremely variable, depending on the time available to the cook, the supply of fat, the heat of the stove or oven, and, finally, the workers’ qualifications. Unfortunately, there are at present very few adequately qualified first-category cooks; they usually occupy supervisory positions, while the entire process of food preparation is frequently entrusted to insufficiently knowledgeable workers.

We obtained data on the temperatures at which certain dishes most commonly served in public catering are prepared by first questioning a qualified, experienced cook and then checking the information through extensive observations of the preparation of these dishes in factory kitchens. We first considered the temperatures inside the oven when a small number of dishes were prepared by one cook and when food was prepared on a mass scale. In the first case, that is, when one cook was working, the oven temperature at the moment a frying pan was placed or a tray slid inside ranged from 180° to 200°, very rarely reaching 250°C, and remained at these levels for the entire time the dish was in the oven. When food was prepared on a mass scale by an entire team of cooks, however, the oven temperature fluctuated continuously and fell each time the door was repeatedly opened by a worker checking whether a dish in the oven was ready, removing a finished dish, or placing new trays in the space thus freed. The decrease in temperature varied according to how long the oven door remained open; at times it fell to 120° or below. The oven temperature also varied considerably with the load: the greater the load, the lower the temperature. Thus, throughout its time in the oven, the dish was continuously subjected to temperature fluctuations. The larger the team, the more poorly qualified workers it included and the more often the oven doors were opened, the greater the temperature fluctuations.

When observing the heating of the stove surface, we found in every case that the heat varied throughout the frying or boiling process and that different areas of the stove surface were heated unevenly, even in its central parts.

We then attempted to measure the temperature inside the dish throughout the entire period of heat treatment by means of a thermometer inserted into it. For these measurements, we selected the simplest meat and vegetarian dishes most commonly served in public catering, both those consisting of a single product and those combining different products—stuffed dishes, casseroles, zrazy, and so forth. Readings from the thermometer inserted into the food very rarely exceeded 90°C, the highest temperatures being recorded inside the muscle of un…

…of a large common fish near the backbone, while readings inside the muscle of fish boiling in a pan were higher than in fish being fried. Continuing our observations, initially only of the temperatures of dishes heat-treated on the stovetop, we obtained a series of similar temperature-rise curves: immediately after the thermometer was inserted, the temperature remained low for several minutes, then rose sharply and, upon reaching a certain level, either rose no further throughout the heat treatment or increased very slowly and only slightly. The heights of the temperature curves varied considerably and depended on a number of conditions: the thickness of the piece, the moisture content of the dish, whether its composition was uniform or combined, and so forth. Vegetable and moist fillings caused the temperature of the dish to be lower. Red fish, which requires careful heat treatment because of its delicate flesh and the effect of prolonged boiling on its flavor, gave thermometer readings of 48–60°C, depending on the thickness of the piece, its position on the stove, the amount of water in the pan, and the intensity and duration of boiling. Common fish, which does not require such careful heat treatment, reached a maximum temperature of 68–72°C in large specimens. The same fish, when boiled, gave thermometer readings of 80–90°C.

Mixed dishes (dishes with fillings) with high moisture content and considerable thickness are ordinarily placed in the oven either at the very beginning of heat treatment or after brief frying on the stovetop. Heat treatment in the oven, i.e., baking, takes longer than frying on the stovetop and produces different temperatures inside the baked dish depending on a number of the factors already mentioned. Despite the lengthy time the food spent in the oven (30–50 minutes or more), we never observed a high temperature inside it. Cabbage rolls with pearl barley porridge reached a maximum temperature of 64–73°C after 20 minutes in the oven; the maximum temperature was usually reached after 11–12 minutes, so that the product was exposed to the high temperature for only 8–9 minutes. Cabbage rolls with rice, baked under the same conditions, reached 65–70°C, rising at the same rate. A pasta casserole left in the oven for 25 minutes reached only 58–64°C. Our numerical results are summarized in Table 1.

Table 1

Results of temperature measurements inside dishes during heat treatment at a factory kitchen

¹ Thickness of the piece: 2–2.5 cm.

Thus, on the basis of a series of temperature measurements in the hot-food preparation departments of central kitchens, we concluded that the temperature inside dishes subjected to various forms of heat treatment is far from always high; that thermometer readings are rather low in moist, composite dishes and in large, thick pieces; and that maximum temperatures in dishes are reached only after they have spent some time on the stove or in the oven and are maintained, on average, for no more than one-third of the total heat-treatment time. Taking into account the extremely wide variations in the duration of heat treatment of dishes noted earlier, which sometimes falls to extremely low values, these measurements further strengthened our doubts as to whether the heat treatment currently applied to food in public catering establishments guarantees the destruction of microorganisms present in the raw ingredients.

To test our conclusions experimentally, we attempted to reproduce culinary preparation under laboratory conditions by frying and baking semifinished products brought from the central kitchen after inoculating them with cultures of bac. coli and bac. proteus isolated from various food products submitted to our institute for investigation in connection with outbreaks of gastrointestinal disease. These strains had previously been studied morphologically and biochemically. Their heat resistance was first tested in broth cultures, after which the survival of certain strains in food products was examined under heat-treatment conditions approximating those of central kitchens as closely as possible.

To determine the heat resistance of the strains in broth cultures, 24-hour cultures were prepared in test tubes containing approximately \(5\ \text{cm}^3\) of ordinary meat-peptone broth. The tubes were heated for 5 minutes in a water bath at \(60\text{–}65^\circ\text{C}\), since the literature indicates that coli bacilli and proteus ordinarily die at these temperatures and heating times; moreover, these temperatures are frequently encountered during the normal heat treatment of food in production. The temperature was measured with a thermometer in a control tube containing broth. Under these experimental conditions, only 10 strains survived. These strains, which proved to be the most heat-resistant, were studied further in broth at higher temperatures and over longer storage periods.

Of the 5 strains in the b. coli group, strain No. 13 proved the most heat-resistant, withstanding \(85^\circ\text{C}\) for 5 minutes; strain No. 1 withstood \(65^\circ\text{C}\) for 15 minutes, and strain No. 7, \(65^\circ\text{C}\) for 10 minutes; strains No. 5 and No. 28 died under these conditions. The strains in the b. proteus group proved less resistant: strain No. 8 withstood \(60^\circ\text{C}\) for 15 minutes, and strain No. 29, \(65^\circ\text{C}\) for 5 minutes. The latter strain should also be classed among the more heat-resistant in this group, since in the course of our experiments it withstood \(60^\circ\text{C}\) for 20 minutes and \(75^\circ\text{C}\) for 5 minutes; the remaining strains in the b. proteus group died under these conditions. It should be noted that at the temperatures specified, the duration of heat exposure has the greatest inhibitory effect: for example, strain No. 1 of the b. coli group withstood \(60\text{–}65^\circ\text{C}\) for 15 minutes but died when exposed to \(60^\circ\text{C}\) for 20 minutes.

This series of experiments showed that different strains of coli bacilli and proteus vary in heat resistance: ordinarily they did not survive temperatures above \(60\text{–}65^\circ\text{C}\) when heated for 5 minutes, but some strains withstood these temperatures for 15–20 minutes.

In view of the possibility that a product might be contaminated with both types of microbe, for the experiments on food products we selected both the most resistant strains of b. coli (No. 13) and b. proteus (No. 29) and ordinary, less resistant strains of b. coli (No. 5) and b. proteus (No. 8 and No. 22). The products selected were those most commonly used in public catering establishments. The temperatures and treatment times applied were the same as those ordinarily observed during temperature measurements made while food was being prepared in production.

The experiments were conducted as follows: pieces of fish were selected to be approximately equal in size, and standard cutlets and baked dishes were obtained from the central kitchen. Suspensions prepared to a standard concentration from 24-hour cultures, containing 5 million and 5 thousand microbes per \(1\ \text{cm}^3\), were used to inoculate the samples. A syringe was used to introduce \(0.5\ \text{cm}^3\) into each food sample: into an incision in the muscle tissue near the backbone in the pieces of fish, and into a break in the cutlets and baked dishes by injection into the center. The inoculated sites were marked, and the food was fried in a small quantity of fat in a pan placed on an asbestos mesh over a gas burner. The duration of frying on each side ...

…was 5 minutes, or 10 minutes in all. For dishes baked in an oven, an appropriate temperature was used. During frying, the temperature on each side was measured with a thermometer inserted into the center of the specimen. After frying, samples from the marked inoculated sites were cultured in enrichment media: meat-peptone broth, Eijkman medium, directly on solid Endo medium, and in the condensation water on agar slants. The isolated strains were examined for identity with the original culture, which, as mentioned above, had previously been studied thoroughly in morphological and biochemical terms.

The results of the experiments are presented in Table 2.

Table 2

Survival of b. coli and b. proteus in food products at different temperatures and heating times

Twenty-four experiments were performed with fish, 12 each with b. coli and b. proteus. Of the 12 experiments with b. coli, six were conducted with strain No. 13 and six with strain No. 5. The internal temperature during frying on one side ranged from 25 to 35°, and during frying on the second side from 55 to 75°C. In specimens inoculated with b. proteus, the temperatures ranged from 25 to 36° and from 50 to 70°C, respectively. The following results were obtained: of the six experiments with b. coli strain No. 13, the organism survived in three; the least resistant strain, No. 5, survived in only one experiment at a low temperature (55°). B. proteus survived in only one instance, at 50–55°C; in all other cases it died.

Fifteen experiments were conducted with meat cutlets inoculated with the same microorganisms.

The temperature inside the cutlets also ranged from 25 to 30°C during frying on the first side and from 60 to 65°C during frying on the second side. The results were as follows: b. coli strain No. 13 survived in 3 of 4 cases, strain No. 5 in only 1 of 4 cases, while b. proteus died in all experiments.

Sixteen experiments were conducted with barley and semolina cutlets, and in all of them all the microbes died, even at temperatures of 50–58°C.

In 28 experiments with potato cutlets, the temperature inside the cutlets varied as follows: during frying on the first side, from 30 to [[unclear: temperature]]° in experiments with b. coli and from 25 to 35°C in experiments with b. proteus; during frying on the second side, from 53 to 60° in experiments with b. coli and 78° in experiments with b. proteus. In these experiments, b. coli No. 15 survived in only 1 of 7 experiments, whereas b. coli No. 13 survived in 3 of 7.

Interesting results were obtained in 12 experiments with potato casserole—6 each with b. coli and b. proteus contamination. These experiments confirmed the particular importance of the oven temperature. When the oven temperature was 180°C and the temperature inside the casserole was 58–60°C, all the microbes survived: b. coli Nos. 13 and 5 and b. proteus. When the oven temperature reached 200°C and the temperature inside the casserole reached 68°C, only the heat-resistant strain No. 13 survived; all the other microbes died. At an oven temperature of 240°C and an internal casserole temperature of 81°C, all the introduced microbes died.

Summarizing the data obtained on the survival of b. coli and b. proteus at different temperatures during the cooking of food products, the following conclusions may be drawn:

1. The same strains of the intestinal bacillus and proteus exhibit varying heat resistance during the processing of food, associated with their biological characteristics. The heat resistance of strains fluctuates over the course of an experiment even in broth cultures. Alongside strains of ordinary heat resistance, strains with increased heat resistance are frequently encountered, particularly among intestinal bacilli.

2. Further study of this subject should clarify the effects on bacterial survival not only of increased temperature but also of the chemical and physicochemical properties of the product: heat capacity, thermal conductivity, pH, salt composition, and the colloidal state of the material.

3. If fish or meat is contaminated with intestinal bacilli and proteus, these microbes, including strains with low resistance, may survive at the temperatures ordinarily used to fry prepared foods in public catering establishments. Consequently, when raw ingredients are heavily contaminated with bacteria, intestinal bacilli and proteus may well survive in the finished dish.

4. The duration of heat treatment of food on the stove and in the oven should be increased; further research is needed to determine the appropriate duration. The oven temperature should be above 200°C and should not fluctuate.

5. The workload standards for hot-food kitchens must be urgently revised, with particular attention to the unacceptable shortening of heat-treatment times observed during night shifts.