A Progressive Approach to the Problem Of Foodborne Infections MAHFOUZ H. ZAKI, MD, DRPH, GEORGE S. MILLER, BS, MARY C. MCLAUGHLIN, MD, MPH, AND SIDNEY B. WEINBERG, MD
Abstract: Qualitative and quantitative bacteriological examinations of 100 samples of perishable foods from 39 retail stores were performed to determine the presence of bacterial contaminants and to explore the feasibility of establishing and utilizing microbiological standards in enforcement. Forty-six per cent of the samples had standard plate counts in excess of 100,000 per gram, 17 per cent showed coliform organisms in excess of 100 per gram, 20 per cent revealed the presence of Staphylococcus aureus and 2 per cent Clostridium perfringens. None of the shell fish samples grew Vibrio parahaemolyticus. The bacteriological findings are discussed in relation to pertinent variables and the use of microbiological standards for potentially hazardous foods is explored.
All 450 retail food establishments in a selected area of Western Suffolk County (New York) were subjected to comprehensive study, using a scoring system developed by the Food and Drug Administration. Initial inspections revealed 32 per cent as having one or more major violations. Follow-up inspections were performed to insure compliance and most violations were corrected within four weeks. Six months later all establishments were reinspected. The scoring system was found to have limited value. Half the establishments with major violations on initial inspection had major violations six months later as compared to less than a quarter of those with no initial major violation. (Am. J. Public Health 66:44 49, 1977)
It has been estimated that food poisoning ranks second only to the common cold as the most frequent cause of shortterm illness in this country. However, its short duration and mild symptoms in the majority of cases, coupled with extremely poor reporting, have hampered the implementation of intensive food protection programs. During 1974, 456 outbreaks of foodborne diseases, involving 15,489 persons, were reported to the Center for Disease Control in Atlanta, Georgia.1 The outbreaks were attributed to: food contamination by bacteria, (especially the various species of Salmonella and Shigella, Clostridium perfringens, and Vibrio parahaemolyticus), or by bacterial toxins (especially those of Staphylococcus aureus, Clostri-
whether at the county or national level, do not represent the actual incidence of foodborne illness. Traditionally, intensive sanitary inspection of food establishments and qualitative and quantitative bacteriological examinations of food items are usually performed only following the occurrence of outbreaks. The survey to be reported is a departure from routine procedures of most health agencies in that it included comprehensive sanitary inspection and bacteriological monitoring in the absence of known outbreaks. Its purpose was to explore the feasibility of using bacterial counts and a scoring system in routine inspections of food establishments.
diium botiulinum and Clostridium parabotulinum), chemical toxins (heavy metals, fish and mushroom toxins), and viral and parasitic infections.
Part I: Microbiological Studies
Among all cases of food poisoning with known etiology, bacterial contaminants are by far the most important etiologic agents, being responsible for 85 to 95 per cent of all cases. During 1975, 121 foodborne outbreaks, involving 588 persons, were reported to the Suffolk County Department of Health Services, New York. It is realized that these figures,
This aspect of the investigation deals with the microbiological contamination of certain perishable foods in supermarkets and retail food establishments. It was undertaken: 1. To determine the presence of certain bacterial contaminants in potentially hazardous foods and to explore reasons for such contamination; 2. To explore the practicality of utilizing microbiological standards in enforcement.
From the Suffolk County Department of Health Services, Hauppauge, NY, and the Downstate Medical Center, State University of New York, Brooklyn. Address reprint requests to Dr. M. H. Zaki, Director of Public Health, Suffolk County Department of Health Services, H. Lee Dennison Executive Office Building, Veterans Memorial Highway, Hauppauge, NY 11787. This paper, submitted to the Journal March 15, 1976, was revised and accepted for publication August 30, 1976. 44
Study Design and Procedures An area representative of Suffolk County and including adjacent sections of four townships was chosen for the investigation. All 450 retail food establishments-representing AJPH January, 1977, Vol. 67, No. 1
FOODBORNE INFECTIONS
about 10 per cent of the total in the County-were thoroughly inspected on two occasions separated by a six-month period. Violators had several interim repeat inspections. These establishments included restaurants, delicatessens, supermarkets, caterers, fish stores, and fast food service operations. Perishable food items encountered during a defined route of inspection on certain dates were sampled for bacteriological examination. A predetermined number of perishable foods were collected on 12 days during the initial inspection. Some of the foods were prepared in the restaurant or retail store; others were prepared by wholesale manufacturers and transported to the delicatessen or retail store for distribution. The investigators have no reason to suspect bias in the selection of days and foods sampled for microbiological study. The bacteriological examinations performed for all food samples included: 1. Standard plate count; 2. Coliform count; 3. Qualitative and quantitative testing for Staphylococcus aureus; In addition: 4. Meat products were examined for the presence of Clostridium perfringens and Salmonellae; and 5. Shellfish products for the presence of Vibrio parahaemolyticus. The total plate count measures that fraction of the bacterial population in the food sample which is capable of growing and producing visible colonies under the test conditions and during the test period. It is generally indicative of the presence of contaminated raw material, unsatisfactory sanitation, or unsuitable time/temperature conditions during processing or storage. The coliform organisms are widely distributed in nature; some such as Escherichia coli, are more specifically indicative of fecal contamination. Coliforms are killed by heat. Their presence in processed foods, therefore, indicates inadequate processing and/or post-processing contamination from workers or equipment.2 3 The reservoir of Staphylococcus aureus is man. The
presence of this organism in food signifies contamination from the skin or upper respiratory and gastrointestinal tracts of man. Large numbers of Staphylococcus aureus in food point to contamination from food handlers, inadequate sanitation and/or temperature control.
Study Findings One hundred perishable food samples, including salads, cold cuts, meat and meat products, poultry, fish products, custard and synthetic pastry and other miscellaneous items were collected from 39 food establishments. For the purpose of this study, a food was considered acceptable provided the total plate count did not exceed 100,000 per gram, the coliform and Staphylococcus aureus counts were not in excess of 100 per gram, and the product was otherwise free from pathogenic organisms and their toxic products. The plate counts in 46 samples were in excess of 100,000 per gram. Of the 100 samples examined, 20 revealed the presence of Staphylococcus aureus with 15 of these showing counts of 100 or more organisms per gram; and 17 samples had coliform counts in excess of 100 organisms per gram (Table 1). Clostridium perfringens were isolated from herring salad and sliced roast beef samples. None of the samples examined grew Salmonellae organisms or Vibrio parahaemolyticus. In some of the salad samples, particularly the shrimp and tuna fish, plate counts exceeding 100,000,000 per gram were noted and, in some, high coliform and Staphylococcus aureus counts were also observed. The same phenomenon was demonstrated in some of the cold cuts and prepared meats especially the ones outdated or offered for quick sale. High total plate counts were also found in many of the poultry samples. Table 2 shows the results of bacteriological examination of some of the highly contaminated food items. Bacteriological findings were studied in relation to various determinants, namely, the storage or display temper-
TABLE 1 Results of Microbiological Examination of 100 Food Samples Staphylococcus Plate Count
FoodsSampled
Salads ColdCuts Meat and Meat Products Poultry Products Fishand Shellfish Miscellaneous TOTAL
Coliform Organism < 100,000 100,000- 1,000,000+ < 100 100- 100,000+
16
7
7
10
2
9 9
1
2 53
1 11
17 6 6
31 13 12
7
2
5
1
2 1
12 9
1
3 35
6 83
1 14
0
32 10 13
Aureus 1- 100+ Total
4
1
12 7 3
6 80
5
4 3 4
40* 13 18*
3
12 10
1 15
100
7*
*One sample contained Clostridium perfringens "Total plate count was not performed on one sample containing cheese
AJPH January, 1977, Vol. 67, No. 1
45
ZAKI, ET AL. TABLE 2-Bacteriological Examination of Some Highly Contaminated Food Items Food Item
Salads Tuna Salad, Retail Mfd. coded 9/10/74 Tuna Salad Sandwich retail mfd. coded 9/17/74 Shrimp Salad, cm pd 9/27 Shrimp Salad, Retail mfd. Shrimp Salad, cm Shrimp Salad, cm 8/20 Cold Cuts Cotto Salami, Sliced, cm, pd 9/21 New England Sausage sliced cm, pd 8/23 Chopped Ham, sliced cm, pd 9/3 Meat and Meat Products Boiled Ham, sliced, cm Roast Beef, sliced, cm Fresh Italian Sausage, whole, cm Raw Pork Sausage, whole, retail mfd. Taco Meat Cake, retail mfd. Fish and Shellfish Sable (carp), smoked, cm Smoked Fish, cm Mahi-Mahi (dolphin meat), cm Poultry Products Chopped Chicken Liver, cm, pd 9/20 Chopped Chicken Liver, cm Miscellaneous Hors D'oeuvres, cm Dietary Frozen Dessert, cm Custard-filled Cookies, cm
Temp. oF.
Coliforms
Aureus
38
320,000
14,000
0
50
4,100,000
150,000
800
40
7,200,000
60
920
40 40
78,000,000
136,000,000
110,000 200
3,200
50
300,000,000+
100
0
P> 0.20). Salads which had acceptable bacterial counts had a 46
Staph Plate Count
mean interval of 6.3 days between manufacture and sampling while those with unacceptable counts had a mean of 5.5 days. The difference is not statistically significant (X2 = .09 0.80 > P > 0.70). In order to study the relationship between the bacterial counts and the results of sanitary inspection of food establishments, only those establishments with single samples or multiple consistent results were included. The bacterial counts of samples obtained from 10 establishments rated AJPH January, 1977, Vol. 67, No. 1
FOODBORNE INFECTIONS
satisfactory* did not differ significantly from those of 14 establishments rated unsatisfactory* (X2 = 0.7 0.50 > P > 0.40).
Discussion There is considerable interest in the establishment of microbiological standards for perishable foods. Although foods containing non-pathogenic bacteria which are processed under the Good Manufacturing Practice Regulations are not considered adulterated, studies reported by the Food and Drug Administration and other agencies indicate that, with a few exceptions, high microbial levels in processed foods are associated with low quality raw material and/or flaws in processing, storage, or distribution.4 In an attempt to promote quality control and in the interest of consumer protection, the Food and Drug Administration proposed, in 1972, the adoption of the following standards for ready-to-eat cream type pies: 1. Aerobic plate count (geometric mean) ' 50,000 per gram 2. Coliform count (geometric mean) ' 50 per gram In 1971, the City of New York passed a resolution establishing standards for potentially hazardous foods. This resolution bans the production, possession, or sale of potentially hazardous foods which contain bacteria in excess of: 1. 100 haemolytic Staphylococcus aureus per gram. 2. 100 coliform organisms per gram. 3. 100,000 bacteria per gram in the total plate count. The standard, in addition, precludes the presence of fecal coliforms, Salmonella, Shigella or other pathogenic micro-organisms. The State of New Jersey adopted standards similar to those of New York City. Other health agencies, including the State of New York and Suffolk County, have authorized the Commissioners of Health to establish microbiological standards for potentially hazardous foods. The wide variation in the microbiological levels in raw food and in the chance of contamination during the various processing procedures mandates that individual standards be established for the various types of food. For raw meat products, for example, the use of microbiological standards is somewhat controversial. Data reported by the Center for Disease Control in 1975 indicated that relatively few illnesses could be traced to the consumption of ground beef.5 In a recent outbreak of staphylococcal food poisoning investigated by the Suffolk County Department of Health Services, home cooked meat ravioli was incriminated. The frozen product was purchased from a local supermarket. Bacteriological examination was performed on the left-over food and on a store sample of ravioli bearing the same code number. While no staphylococci were detected in the cooked product, 800,000 Staphylococcus aureus organisms per gram were found in the raw meat ravioli obtained from the store. *As defined later in this article.
AJPH January, 1977, Vol. 67, No. 1
Laboratory limitations did not allow for the examination of the staphylococcal toxin in the cooked product. This outbreak and others, one of which is currently under investigation, tend to incriminate ground beef as the responsible vehicle. During the past two years, quantitative determination was made in 12 of the 16 outbreaks of staphylococcal food poisoning investigated by Suffolk County. In five of these, high counts of Staphylococcus aureus organisms (> 800,000 per gram) in suspect foods were accompanied by excessive total plate counts (1,000,000-12,000,000 per gram). In four outbreaks moderate staphylococcal counts (1200-150,000) did not correlate well with total plate counts while in the remaining three, low staphylococcal counts (100-960) were accompanied by relatively low total plate counts. These findings indicate that clinical disease due to Staphylococcus aureus enterotoxin can occur from food with very low counts. On occasion, in the presence of optimum conditions for growth and multiplication, staphylococci can multiply, produce enterotoxin, and then die off. Results of laboratory examinations were forwarded to the food establishments and those with unsatisfactory findings were asked to investigate their operation and to take corrective action. As a result, a large salad manufacturer supplying a chain of supermarkets and retail food outlets changed production time in order to meet actual orders rather than estimates and initiated routine bacteriological examinations of salads at various stages of production; four supermarket chains reviewed their food handling practices and contracted private laboratories to undertake full-line sampling while another, established a quality assurance program. In addition, a large restaurant chain eliminated commerciallymanufactured Mahi-Mahi (dolphin meat) from their menu as a result of extremely high total plate and coliform counts pending further investigation and corrective action; and a caterer changed his ordering practices and installed additional climate control systems.
Part II: Sanitary Inspections This aspect of the investigation was initiated to: 1. Establish guidelines for the frequency of sanitary inspections in order to more effectively utilize available manpower; 2. Test the practicality of the scoring system recommended by various health agencies.
Procedures For the sanitary inspection, a scoring system developed by the Food and Drug Administration and slightly modified by the New York State Health Department was used.6 County enforcement procedures were somewhat different from those recommended by FDA. The inspection included 44 items which were numerically scored. Weights of 1 and 2 represent minor violations such as cleanliness of non-food contact surfaces, lack of ther47
ZAKI, ET AL.
~ 47
mometers in storage facilities, reuse of single service articles, cleanliness and coverage of garbage containers, cleanliness of wash water and its proper temperature, etc. These violations play a minor role in foodborne illness. Major violations with a scoring weight of 4 or 5 relate to wholesomeness of food, source of food, temperature of potentially hazardous foods, water supply, hygienic practices and health status of personnel, etc., all of which have direct impact on disease transmission and are considered detrimental to public health.
Findings and Discussion
In the first round of inspections, 279 (62 per cent) of the 450 food establishments were given a satisfactory rating, meaning that they either had no violations (12, or 3 per cent) or that they had minor violations not directly affecting disease transmission or public health (267, or 59 per cent). One or more major violations were found in 171, (38 per cent) of the establishments. Of these, 5 (1 per cent) were immediately closed. Follow-up reinspections of the 171 establishments rated as unsatisfactory were made during the following 4-week period. Figure I shows the number and weight of the violations encountered at initial and subsequent inspections. Fifty-six per cent of all violations were
SECOND REINSPECTION
16 5 63i
FIRST RE INSPECTION
50
I130
ORIGINAL INSPECTION
23
W4
jfl
72
-J
139
I
3i
Conclusion The current survey indicates: 1. That certain potentially hazardous food items sold in supermarkets and other retail food establishments are highly contaminated, probably due to flaws in production, processing, handling, transportation and storage. 2. That there is an urgent need for the adoption of acceptable microbiological standards for potentially hazardous food items.
Ea189
TABLE 3-Scoring Range of 171 Retail Food Establishments Found Unsatisfactory
502
L
I 00
I
200
I
I
I
I
300
400
500
600
NUMBER OF VIOLATIONS FIGURE 1-Number of Violations of Different Types on Initial and Follow-up Inspections of 171 Food Establishments with One or More Major Violations on Initial Inspection. 48
corrected by the first reinspection and 84 per cent by the second reinspection. All 450 establishments were inspected again six months after the original inspection. Three hundred establishments (67 per cent) were found satisfactory while 150 (33 per cent) were unsatisfactory. It is of interest that 217 (78 per cent) of the 279 establishments rated as satisfactory in September 1974 were still satisfactory six months later. Of the 171 establishments rated as unsatisfactory on the original inspection, only 83 (48 per cent) were found satisfactory six months later. Thus the probability of finding an establishment with a satisfactory rating is substantially higher if the establishment was so rated on a previous occasion than if it was not so rated. In the interests of efficiency, the frequency of inspection could be adjusted according to the previous performance of the food establishment. Establishments rated as satisfactory on two consecutive semi-annual inspections might be inspected on an annual or semi-annual basis while those with major violations and repeat violators would require more frequent inspections. The numerical scoring system, previously alluded to, was found to be of little value in determining either the necessity for reinspection or the frequency of inspection. Fiftyfour per cent of the food establishments found to be unsatisfactory had numerical scores of 85 or over out of a possible 100 (Table 3). A further disadvantage of the scoring system is related to the fact that satisfactory achievement is traditionally measured by the height of the grade scores. Hence, it is often difficult to explain to a food operator, patron, or court of justice that high scores for food establishments may be accompanied by unsatisfactory conditions.
Numerical Score
Number Unsatisfactory
Per Cent Unsatisfactory
90-96
42 50 45 17 17
24.5 29.2 26.3
171
100.0
85-89 80-84 75-79
Abstract: Qualitative and quantitative bacteriological examinations of 100 samples of perishable foods from 39 retail stores were performed to determine the presence of bacterial contaminants and to explore the feasibility of establishing and utilizing microbiological standards in enforcement. Forty-six per cent of the samples had standard plate counts in excess of 100,000 per gram, 17 per cent showed coliform organisms in excess of 100 per gram, 20 per cent revealed the presence of Staphylococcus aureus and 2 per cent Clostridium perfringens. None of the shell fish samples grew Vibrio parahaemolyticus. The bacteriological findings are discussed in relation to pertinent variables and the use of microbiological standards for potentially hazardous foods is explored.
All 450 retail food establishments in a selected area of Western Suffolk County (New York) were subjected to comprehensive study, using a scoring system developed by the Food and Drug Administration. Initial inspections revealed 32 per cent as having one or more major violations. Follow-up inspections were performed to insure compliance and most violations were corrected within four weeks. Six months later all establishments were reinspected. The scoring system was found to have limited value. Half the establishments with major violations on initial inspection had major violations six months later as compared to less than a quarter of those with no initial major violation. (Am. J. Public Health 66:44 49, 1977)
It has been estimated that food poisoning ranks second only to the common cold as the most frequent cause of shortterm illness in this country. However, its short duration and mild symptoms in the majority of cases, coupled with extremely poor reporting, have hampered the implementation of intensive food protection programs. During 1974, 456 outbreaks of foodborne diseases, involving 15,489 persons, were reported to the Center for Disease Control in Atlanta, Georgia.1 The outbreaks were attributed to: food contamination by bacteria, (especially the various species of Salmonella and Shigella, Clostridium perfringens, and Vibrio parahaemolyticus), or by bacterial toxins (especially those of Staphylococcus aureus, Clostri-
whether at the county or national level, do not represent the actual incidence of foodborne illness. Traditionally, intensive sanitary inspection of food establishments and qualitative and quantitative bacteriological examinations of food items are usually performed only following the occurrence of outbreaks. The survey to be reported is a departure from routine procedures of most health agencies in that it included comprehensive sanitary inspection and bacteriological monitoring in the absence of known outbreaks. Its purpose was to explore the feasibility of using bacterial counts and a scoring system in routine inspections of food establishments.
diium botiulinum and Clostridium parabotulinum), chemical toxins (heavy metals, fish and mushroom toxins), and viral and parasitic infections.
Part I: Microbiological Studies
Among all cases of food poisoning with known etiology, bacterial contaminants are by far the most important etiologic agents, being responsible for 85 to 95 per cent of all cases. During 1975, 121 foodborne outbreaks, involving 588 persons, were reported to the Suffolk County Department of Health Services, New York. It is realized that these figures,
This aspect of the investigation deals with the microbiological contamination of certain perishable foods in supermarkets and retail food establishments. It was undertaken: 1. To determine the presence of certain bacterial contaminants in potentially hazardous foods and to explore reasons for such contamination; 2. To explore the practicality of utilizing microbiological standards in enforcement.
From the Suffolk County Department of Health Services, Hauppauge, NY, and the Downstate Medical Center, State University of New York, Brooklyn. Address reprint requests to Dr. M. H. Zaki, Director of Public Health, Suffolk County Department of Health Services, H. Lee Dennison Executive Office Building, Veterans Memorial Highway, Hauppauge, NY 11787. This paper, submitted to the Journal March 15, 1976, was revised and accepted for publication August 30, 1976. 44
Study Design and Procedures An area representative of Suffolk County and including adjacent sections of four townships was chosen for the investigation. All 450 retail food establishments-representing AJPH January, 1977, Vol. 67, No. 1
FOODBORNE INFECTIONS
about 10 per cent of the total in the County-were thoroughly inspected on two occasions separated by a six-month period. Violators had several interim repeat inspections. These establishments included restaurants, delicatessens, supermarkets, caterers, fish stores, and fast food service operations. Perishable food items encountered during a defined route of inspection on certain dates were sampled for bacteriological examination. A predetermined number of perishable foods were collected on 12 days during the initial inspection. Some of the foods were prepared in the restaurant or retail store; others were prepared by wholesale manufacturers and transported to the delicatessen or retail store for distribution. The investigators have no reason to suspect bias in the selection of days and foods sampled for microbiological study. The bacteriological examinations performed for all food samples included: 1. Standard plate count; 2. Coliform count; 3. Qualitative and quantitative testing for Staphylococcus aureus; In addition: 4. Meat products were examined for the presence of Clostridium perfringens and Salmonellae; and 5. Shellfish products for the presence of Vibrio parahaemolyticus. The total plate count measures that fraction of the bacterial population in the food sample which is capable of growing and producing visible colonies under the test conditions and during the test period. It is generally indicative of the presence of contaminated raw material, unsatisfactory sanitation, or unsuitable time/temperature conditions during processing or storage. The coliform organisms are widely distributed in nature; some such as Escherichia coli, are more specifically indicative of fecal contamination. Coliforms are killed by heat. Their presence in processed foods, therefore, indicates inadequate processing and/or post-processing contamination from workers or equipment.2 3 The reservoir of Staphylococcus aureus is man. The
presence of this organism in food signifies contamination from the skin or upper respiratory and gastrointestinal tracts of man. Large numbers of Staphylococcus aureus in food point to contamination from food handlers, inadequate sanitation and/or temperature control.
Study Findings One hundred perishable food samples, including salads, cold cuts, meat and meat products, poultry, fish products, custard and synthetic pastry and other miscellaneous items were collected from 39 food establishments. For the purpose of this study, a food was considered acceptable provided the total plate count did not exceed 100,000 per gram, the coliform and Staphylococcus aureus counts were not in excess of 100 per gram, and the product was otherwise free from pathogenic organisms and their toxic products. The plate counts in 46 samples were in excess of 100,000 per gram. Of the 100 samples examined, 20 revealed the presence of Staphylococcus aureus with 15 of these showing counts of 100 or more organisms per gram; and 17 samples had coliform counts in excess of 100 organisms per gram (Table 1). Clostridium perfringens were isolated from herring salad and sliced roast beef samples. None of the samples examined grew Salmonellae organisms or Vibrio parahaemolyticus. In some of the salad samples, particularly the shrimp and tuna fish, plate counts exceeding 100,000,000 per gram were noted and, in some, high coliform and Staphylococcus aureus counts were also observed. The same phenomenon was demonstrated in some of the cold cuts and prepared meats especially the ones outdated or offered for quick sale. High total plate counts were also found in many of the poultry samples. Table 2 shows the results of bacteriological examination of some of the highly contaminated food items. Bacteriological findings were studied in relation to various determinants, namely, the storage or display temper-
TABLE 1 Results of Microbiological Examination of 100 Food Samples Staphylococcus Plate Count
FoodsSampled
Salads ColdCuts Meat and Meat Products Poultry Products Fishand Shellfish Miscellaneous TOTAL
Coliform Organism < 100,000 100,000- 1,000,000+ < 100 100- 100,000+
16
7
7
10
2
9 9
1
2 53
1 11
17 6 6
31 13 12
7
2
5
1
2 1
12 9
1
3 35
6 83
1 14
0
32 10 13
Aureus 1- 100+ Total
4
1
12 7 3
6 80
5
4 3 4
40* 13 18*
3
12 10
1 15
100
7*
*One sample contained Clostridium perfringens "Total plate count was not performed on one sample containing cheese
AJPH January, 1977, Vol. 67, No. 1
45
ZAKI, ET AL. TABLE 2-Bacteriological Examination of Some Highly Contaminated Food Items Food Item
Salads Tuna Salad, Retail Mfd. coded 9/10/74 Tuna Salad Sandwich retail mfd. coded 9/17/74 Shrimp Salad, cm pd 9/27 Shrimp Salad, Retail mfd. Shrimp Salad, cm Shrimp Salad, cm 8/20 Cold Cuts Cotto Salami, Sliced, cm, pd 9/21 New England Sausage sliced cm, pd 8/23 Chopped Ham, sliced cm, pd 9/3 Meat and Meat Products Boiled Ham, sliced, cm Roast Beef, sliced, cm Fresh Italian Sausage, whole, cm Raw Pork Sausage, whole, retail mfd. Taco Meat Cake, retail mfd. Fish and Shellfish Sable (carp), smoked, cm Smoked Fish, cm Mahi-Mahi (dolphin meat), cm Poultry Products Chopped Chicken Liver, cm, pd 9/20 Chopped Chicken Liver, cm Miscellaneous Hors D'oeuvres, cm Dietary Frozen Dessert, cm Custard-filled Cookies, cm
Temp. oF.
Coliforms
Aureus
38
320,000
14,000
0
50
4,100,000
150,000
800
40
7,200,000
60
920
40 40
78,000,000
136,000,000
110,000 200
3,200
50
300,000,000+
100
0
P> 0.20). Salads which had acceptable bacterial counts had a 46
Staph Plate Count
mean interval of 6.3 days between manufacture and sampling while those with unacceptable counts had a mean of 5.5 days. The difference is not statistically significant (X2 = .09 0.80 > P > 0.70). In order to study the relationship between the bacterial counts and the results of sanitary inspection of food establishments, only those establishments with single samples or multiple consistent results were included. The bacterial counts of samples obtained from 10 establishments rated AJPH January, 1977, Vol. 67, No. 1
FOODBORNE INFECTIONS
satisfactory* did not differ significantly from those of 14 establishments rated unsatisfactory* (X2 = 0.7 0.50 > P > 0.40).
Discussion There is considerable interest in the establishment of microbiological standards for perishable foods. Although foods containing non-pathogenic bacteria which are processed under the Good Manufacturing Practice Regulations are not considered adulterated, studies reported by the Food and Drug Administration and other agencies indicate that, with a few exceptions, high microbial levels in processed foods are associated with low quality raw material and/or flaws in processing, storage, or distribution.4 In an attempt to promote quality control and in the interest of consumer protection, the Food and Drug Administration proposed, in 1972, the adoption of the following standards for ready-to-eat cream type pies: 1. Aerobic plate count (geometric mean) ' 50,000 per gram 2. Coliform count (geometric mean) ' 50 per gram In 1971, the City of New York passed a resolution establishing standards for potentially hazardous foods. This resolution bans the production, possession, or sale of potentially hazardous foods which contain bacteria in excess of: 1. 100 haemolytic Staphylococcus aureus per gram. 2. 100 coliform organisms per gram. 3. 100,000 bacteria per gram in the total plate count. The standard, in addition, precludes the presence of fecal coliforms, Salmonella, Shigella or other pathogenic micro-organisms. The State of New Jersey adopted standards similar to those of New York City. Other health agencies, including the State of New York and Suffolk County, have authorized the Commissioners of Health to establish microbiological standards for potentially hazardous foods. The wide variation in the microbiological levels in raw food and in the chance of contamination during the various processing procedures mandates that individual standards be established for the various types of food. For raw meat products, for example, the use of microbiological standards is somewhat controversial. Data reported by the Center for Disease Control in 1975 indicated that relatively few illnesses could be traced to the consumption of ground beef.5 In a recent outbreak of staphylococcal food poisoning investigated by the Suffolk County Department of Health Services, home cooked meat ravioli was incriminated. The frozen product was purchased from a local supermarket. Bacteriological examination was performed on the left-over food and on a store sample of ravioli bearing the same code number. While no staphylococci were detected in the cooked product, 800,000 Staphylococcus aureus organisms per gram were found in the raw meat ravioli obtained from the store. *As defined later in this article.
AJPH January, 1977, Vol. 67, No. 1
Laboratory limitations did not allow for the examination of the staphylococcal toxin in the cooked product. This outbreak and others, one of which is currently under investigation, tend to incriminate ground beef as the responsible vehicle. During the past two years, quantitative determination was made in 12 of the 16 outbreaks of staphylococcal food poisoning investigated by Suffolk County. In five of these, high counts of Staphylococcus aureus organisms (> 800,000 per gram) in suspect foods were accompanied by excessive total plate counts (1,000,000-12,000,000 per gram). In four outbreaks moderate staphylococcal counts (1200-150,000) did not correlate well with total plate counts while in the remaining three, low staphylococcal counts (100-960) were accompanied by relatively low total plate counts. These findings indicate that clinical disease due to Staphylococcus aureus enterotoxin can occur from food with very low counts. On occasion, in the presence of optimum conditions for growth and multiplication, staphylococci can multiply, produce enterotoxin, and then die off. Results of laboratory examinations were forwarded to the food establishments and those with unsatisfactory findings were asked to investigate their operation and to take corrective action. As a result, a large salad manufacturer supplying a chain of supermarkets and retail food outlets changed production time in order to meet actual orders rather than estimates and initiated routine bacteriological examinations of salads at various stages of production; four supermarket chains reviewed their food handling practices and contracted private laboratories to undertake full-line sampling while another, established a quality assurance program. In addition, a large restaurant chain eliminated commerciallymanufactured Mahi-Mahi (dolphin meat) from their menu as a result of extremely high total plate and coliform counts pending further investigation and corrective action; and a caterer changed his ordering practices and installed additional climate control systems.
Part II: Sanitary Inspections This aspect of the investigation was initiated to: 1. Establish guidelines for the frequency of sanitary inspections in order to more effectively utilize available manpower; 2. Test the practicality of the scoring system recommended by various health agencies.
Procedures For the sanitary inspection, a scoring system developed by the Food and Drug Administration and slightly modified by the New York State Health Department was used.6 County enforcement procedures were somewhat different from those recommended by FDA. The inspection included 44 items which were numerically scored. Weights of 1 and 2 represent minor violations such as cleanliness of non-food contact surfaces, lack of ther47
ZAKI, ET AL.
~ 47
mometers in storage facilities, reuse of single service articles, cleanliness and coverage of garbage containers, cleanliness of wash water and its proper temperature, etc. These violations play a minor role in foodborne illness. Major violations with a scoring weight of 4 or 5 relate to wholesomeness of food, source of food, temperature of potentially hazardous foods, water supply, hygienic practices and health status of personnel, etc., all of which have direct impact on disease transmission and are considered detrimental to public health.
Findings and Discussion
In the first round of inspections, 279 (62 per cent) of the 450 food establishments were given a satisfactory rating, meaning that they either had no violations (12, or 3 per cent) or that they had minor violations not directly affecting disease transmission or public health (267, or 59 per cent). One or more major violations were found in 171, (38 per cent) of the establishments. Of these, 5 (1 per cent) were immediately closed. Follow-up reinspections of the 171 establishments rated as unsatisfactory were made during the following 4-week period. Figure I shows the number and weight of the violations encountered at initial and subsequent inspections. Fifty-six per cent of all violations were
SECOND REINSPECTION
16 5 63i
FIRST RE INSPECTION
50
I130
ORIGINAL INSPECTION
23
W4
jfl
72
-J
139
I
3i
Conclusion The current survey indicates: 1. That certain potentially hazardous food items sold in supermarkets and other retail food establishments are highly contaminated, probably due to flaws in production, processing, handling, transportation and storage. 2. That there is an urgent need for the adoption of acceptable microbiological standards for potentially hazardous food items.
Ea189
TABLE 3-Scoring Range of 171 Retail Food Establishments Found Unsatisfactory
502
L
I 00
I
200
I
I
I
I
300
400
500
600
NUMBER OF VIOLATIONS FIGURE 1-Number of Violations of Different Types on Initial and Follow-up Inspections of 171 Food Establishments with One or More Major Violations on Initial Inspection. 48
corrected by the first reinspection and 84 per cent by the second reinspection. All 450 establishments were inspected again six months after the original inspection. Three hundred establishments (67 per cent) were found satisfactory while 150 (33 per cent) were unsatisfactory. It is of interest that 217 (78 per cent) of the 279 establishments rated as satisfactory in September 1974 were still satisfactory six months later. Of the 171 establishments rated as unsatisfactory on the original inspection, only 83 (48 per cent) were found satisfactory six months later. Thus the probability of finding an establishment with a satisfactory rating is substantially higher if the establishment was so rated on a previous occasion than if it was not so rated. In the interests of efficiency, the frequency of inspection could be adjusted according to the previous performance of the food establishment. Establishments rated as satisfactory on two consecutive semi-annual inspections might be inspected on an annual or semi-annual basis while those with major violations and repeat violators would require more frequent inspections. The numerical scoring system, previously alluded to, was found to be of little value in determining either the necessity for reinspection or the frequency of inspection. Fiftyfour per cent of the food establishments found to be unsatisfactory had numerical scores of 85 or over out of a possible 100 (Table 3). A further disadvantage of the scoring system is related to the fact that satisfactory achievement is traditionally measured by the height of the grade scores. Hence, it is often difficult to explain to a food operator, patron, or court of justice that high scores for food establishments may be accompanied by unsatisfactory conditions.
Numerical Score
Number Unsatisfactory
Per Cent Unsatisfactory
90-96
42 50 45 17 17
24.5 29.2 26.3
171
100.0
85-89 80-84 75-79
