476 Modern Food Microbiology
6. possess growth requirements and a growth rate equaling or exceeding that of the pathogen
7. have a die-off rate that at least parallels that of the pathogen and ideally persists slightly longer
than the pathogen of concern (Figure 20–1)
8. be absent from foods that are free of the pathogen except perhaps at certain minimum numbers
These criteria apply to most, if not all, foods that may be vehicles of foodborne pathogens, regardless
of their source to the foods. In the historical use of safety indicators, however, the pathogens of concern
were assumed to be of intestinal origin, resulting from either direct or indirect fecal contamination.
Thus, such sanitary indicators were used historically to detect fecal contamination of waters and
thereby the possible presence of intestinal pathogens. The first fecal indicator was Escherichia coli.
When the concept of fecal indicators was applied to food safety, some additional criteria were stressed,
and those suggested by Buttiaux and Mossel in 1961
11 are still valid:
1. Ideally, the bacteria selected should demonstrate specificity, occurring only in intestinal environments.
2. They should occur in very high numbers in feces so as to be encountered in high dilutions.
3. They should possess a high resistance to the extraenteral environment, the pollution of which is
to be assessed.
4. They should permit relatively easy and fully reliable detection even when present in very low
numbers.
Following the practice of employing E. coli as an indicator of fecal pollution of waters, other organisms
were suggested for the same purpose, and most are covered below.
Coliforms
While attempting to isolate the etiologic agent of cholera in 1885, Escherich
24 isolated and studied
the organism that is now E. coli. It was originally named Bacterium coli commune because it was
present in the stools of each patient he examined. Schardinger
77 was the first to suggest the use of this
organism as an index of fecal pollution because it could be isolated and identified more readily than
individual waterborne pathogens. A test for this organism as a measure of drinking water potability
was suggested in 1895 by T. Smith.
82 This marked the beginning of the use of coliforms as indicators
of pathogens in water, a practice that has been extended to foods.
Species/Strains
In a practical sense, coliforms are Gram-negative asporogeneous rods that ferment lactose within
48 hours and produce dark colonies with a metallic sheen on Endo-type agar.
4 By and large, coliforms
are represented by four or five genera of the family Enterobacteriaceae: Citrobacter, Enterobacter,
Escherichia, and Klebsiella. Since the relatively new genus Raoultella was formerly a part of Klebsiella,
it could represent the fifth coliform genus. Occasional strains of Arizona hinshawii and Hafnia alvei
ferment lactose but generally not within 48 hours, and some Pantoea agglomerans strains are lactose
positive within 48 hours.
Since E. coli is more indicative of fecal pollution than the other genera and species noted (especially E. aerogenes), it is often desirable to determine its incidence in a coliform population. The
IMViC formula is the classic method used, where I = indole production, M = methyl red reaction,
6. possess growth requirements and a growth rate equaling or exceeding that of the pathogen
7. have a die-off rate that at least parallels that of the pathogen and ideally persists slightly longer
than the pathogen of concern (Figure 20–1)
8. be absent from foods that are free of the pathogen except perhaps at certain minimum numbers
These criteria apply to most, if not all, foods that may be vehicles of foodborne pathogens, regardless
of their source to the foods. In the historical use of safety indicators, however, the pathogens of concern
were assumed to be of intestinal origin, resulting from either direct or indirect fecal contamination.
Thus, such sanitary indicators were used historically to detect fecal contamination of waters and
thereby the possible presence of intestinal pathogens. The first fecal indicator was Escherichia coli.
When the concept of fecal indicators was applied to food safety, some additional criteria were stressed,
and those suggested by Buttiaux and Mossel in 1961
11 are still valid:
1. Ideally, the bacteria selected should demonstrate specificity, occurring only in intestinal environments.
2. They should occur in very high numbers in feces so as to be encountered in high dilutions.
3. They should possess a high resistance to the extraenteral environment, the pollution of which is
to be assessed.
4. They should permit relatively easy and fully reliable detection even when present in very low
numbers.
Following the practice of employing E. coli as an indicator of fecal pollution of waters, other organisms
were suggested for the same purpose, and most are covered below.
Coliforms
While attempting to isolate the etiologic agent of cholera in 1885, Escherich
24 isolated and studied
the organism that is now E. coli. It was originally named Bacterium coli commune because it was
present in the stools of each patient he examined. Schardinger
77 was the first to suggest the use of this
organism as an index of fecal pollution because it could be isolated and identified more readily than
individual waterborne pathogens. A test for this organism as a measure of drinking water potability
was suggested in 1895 by T. Smith.
82 This marked the beginning of the use of coliforms as indicators
of pathogens in water, a practice that has been extended to foods.
Species/Strains
In a practical sense, coliforms are Gram-negative asporogeneous rods that ferment lactose within
48 hours and produce dark colonies with a metallic sheen on Endo-type agar.
4 By and large, coliforms
are represented by four or five genera of the family Enterobacteriaceae: Citrobacter, Enterobacter,
Escherichia, and Klebsiella. Since the relatively new genus Raoultella was formerly a part of Klebsiella,
it could represent the fifth coliform genus. Occasional strains of Arizona hinshawii and Hafnia alvei
ferment lactose but generally not within 48 hours, and some Pantoea agglomerans strains are lactose
positive within 48 hours.
Since E. coli is more indicative of fecal pollution than the other genera and species noted (especially E. aerogenes), it is often desirable to determine its incidence in a coliform population. The
IMViC formula is the classic method used, where I = indole production, M = methyl red reaction,