THE JOURNAL OF I:\,FECTIOUS DISEASES. VOL. 137, :'1:0. 5 • MAY 1978 © 1978 by the University of Chicago. 0022-1899178/3705-0005S00.75
Virulence Factors of the Bacterial Cell Surface Frits 0rskov
From the International Escherichia and KLebsiella Center of the WorLd Health Organization, Copenhagen, Denmark
[8] have found that small, induced variations in the 0 polysaccharide have an influence on the virulence of gram-negative bacteria. Of the many known E. coli 0 groups (at the moment there are 163), only a few are highly prevalent in the normal human gut. By use of specific antisera to the 10 most common 0 groups, it is possible to determine the 0 group of about 50% of E. coli in the feces of humans. Studies indicate that the same 0 groups that are common in extraintestinal infections arc those frequently present in the normal gut (table 1). Some 0 groups have been associated with diarrhea due to enteropathogenic E. coli that occurs in infants, and other 0 groups with dysentery-like diarrhea (table 2). In cases of diarrhea of young animals that is caused by enterotoxigenic E. coli, certain 0 groups have been identified that are specific for piglets and others that are specific for calves. \Ve do not know what factors cause this apparent host and disease specificity or how they are related to pathogenicity [1]. There are so-called rough strains and smooth strains. Acute disease is related to the smooth strains. Some studies of urinary tract infections show that rough strains are found in asymptomatic chronic urinary tract infections. Hanson [2] has suggested that the smooth strains found in the first stage of disease mutate into rough strains and thus become less virulent. Strains that actually have a rough lipopolysaccharide may appear to be smooth on artificial media. This morphological smoothness on the plates is caused by a capsular polysaccharide that differs chemically and genetically from the lipopolysaccharide. The "hidden" rough character can be disclosed by heating the culture. Robbins et a1. [9] studied neonatal meningitis caused by E. coli and found that 85CJo of the strains contained KI capsular antigen. Although I O(:~ 15% of the strains were rough, those with a KI capsular antigen were invasive. The KI capsular polysaccharide is an a-2,9-linked N-acetyl neuraminic acid homopolymer that is structurally
Please address requests for reprints to Dr. Frits 0rskov, Statens Serurniustitut, Amager Boulevard 80, DK-2300 Copenhagen S, Denmark.
630
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
Bacterial surface structures are related to properties of virulence. Although these antigens can be associated with invasiveness, resistance to phagocytosis, and intestinal colonization, no single factor or antigen determines pathogenicity. Among the Enterobacteriaceae there are two categories of surface antigens, those composed of polysaccharide and those composed of protein. The polysaccharide antigens can be divided into the lipopolysaccharide 0 antigens and the capsular polysaccharide K antigens. The li popolysaccharides have three regions: (1) lipid A, (2) core oligosaccharide, and (3) O-specific polysaccharide. Lipid A is responsible for the toxic properties of the lipopolysaccharide and is probably similar in the different Enterobacteriaceae. The structure of the core polysaccharide (region II) present in enterobacteria varies, e.g., the same structure has been detected in all Salmonella, but four different ones have been found in Escherichia coli. The O-specific polysaccharide is characteristic of the smooth (S) form of Enterobacteriaceae. This polysaccharide is the chemical basis of the O-antigen specificity of gram-negative bacteria; the various () antigens are specified by the different sugars found in this O-specific side chain. Mutations affecting the synthesis of the O-specific side chain may result in rough (R) variants that give R specificity to the core polysaccharide [1]. Since R mutants are more easily phagocytized and more sensitive to bactericidal activities, they are less pathogenic and less virulent than S forms [2-6]. The specific 0 polysaccharide protects the bacterium against host resistance and is also responsible for the in vitro stability of bacterial suspensions. Although we believe that 0 antigens are important in pathogenicity, we do not have a simple explanation for the role of the different 0 antigens. Smith and Parsell [7] and Makela et a1.
Cell-Surjacc Virulence Factors
631
Table 1. Serogroups of 0 antigen of Escherichia coli isolated from humans with extraintestinal infections and from feces of healthy adults and children.
o serogroups*
Source Urinary tract infections
Septicemia
Other infections
Feces
*Since the prevalence rates were compiled from data of many different investigations, the 0 groups are listed numerically. tThe prevalent 0 groups listed here are characterized by having the same K antigen (K1) when isolated from patients with this disease.
identical to the capsule of group B Neisseria meningitidis. It is of interest that the same capsule confers virulence to two bacterial species. Most capsular polysaccharide K antigens are acidic; they are found in many Enterobacteriaceae, including E. coli, Klebsiella, and Salmonella. Eighty different K polysaccharides exist in E. coli. The K antigens of E. coli may be divided into two groups. One is similar to the capsular antigens of Klebsiella and is associated with 0 groups 08,09,020, and 0101. The second group is associated with several other common 0 groups (table 3). The first group is determined by a genetic locus close to that of histidine. It is interesting to note
Table 2. Identification of 0 groups, O:H types, and O:K:H types of Escherichia coli isolated from humans with in testinal infections [1] . Infection Infantile diarrhea Sporadic cases and outbreaks, mostly in institutions Diarrhea in ad ul ts and children Sporadic cases and outbreaks
Dysentery-like disease, sporadic cases and outbreaks
Classification of E. coli
o groups, O:H types, and
O:K:H types
Enteropathogenic
020,026,044,055,086,0111,0114,0119,0125, 0126,0127,0128,0142,0158
Enterotoxigenic
06:K15:H16, 08:K40:H9, 08:K25:H9, 011:H27, 015:H11, 020:H-, 025:K7:H42, 025:K98:H-, 027: H7, 078:Hll, 078:H12, 0128:H7, 0148:H28, 0149:H10,0159:H20
Enteroinvasive
028ac, 0112, 0124,0136,0143,0144,0152,0164
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
Neonatal meningitis'[
01,02,04,06,07, 08, 09, OIl, 022, 025, 062,075 01, 02, 04, 06, 07, 09, 011,018,022,025, 075 01,02,04,06,08,09, 011,021,062 01,06,07,016,018, 083 01, 02,04, 06, 07, 08, 018,025,045,075, 081
that the locus determining the structure of the O-specific polysaccharide is also close to the histidine locus. The remaining K antigens that are associated with several common 0 groups are genetically determined by a locus close to the serine A locus. Most common in this group of K antigens are KI, K2, K5, K12, and KI3. Because there are more than 80 such antigens and 163 0 groups, theoretically there may be a great number of combinations of the O-K serotypes. However, only a limited number of O-K combinations are common [1]. Not all E. coli have a capsular antigen, but strains associated with invasive disease usually do. The E. coli strains most frequently found in normal intestines also have capsules or belong to serotypes that are frequently encapsulated. The KI antigen is found in > 85% of the different serotypes isolated from human neonates with meningitis [9]. The KI antigen is also the most common K antigen present in E. coli organisms that cause septicemia or pyelonephritis and also in those in the intestinal tract of healthy persons [6,10-13]. Studies with mice and guinea pigs have demonstrated that a capsular variant is more virulent and less easily phagocytized than an acapsular variant of the same strain [6, 14, 15]. Generally, encapsulated serotypes are more frequently associated with invasive disease than uncapsulated serotypes, although there is no agreement on whether this characteristic is always associated with the amount of K polysaccharides [16, 17]. Cholanic acid or 1\1 antigens are genetically determined by loci different from those determining the two K antigen groups. The M antigens
~rskov
632
Table 3. Combinations of polysaccharide a and K surface antigens of Escherichia coli based on chemical and immunoelectrophoretic characterization [1] .
Occurrence
Material
Many 0 groups Neutral LPS and acidic capsular polysaccharide
Neu tral LPS and acidic capsular polysaccharide
o groups 08,
Neu tral LPS and acidic LPS
o groups 08,
Neutral LPS
Many 0 groups
09,0101, (020)
o line: cathodic, slow K line: anodic, fast
o line: cathodic, slow Kline: anodic, slow
o line:
cathodic, slow K line: anodic, slow
o line:
cathodic,
slow Many 0 groups
Acidic LPS
o line:
anodic,
slow Many 0 groups Acidic LPS and acidic capsular polysaccharide
NOTE.
LPS
o line: anodic, slow K line: anodic, fast
= lipopolysaccharide.
are common to most Enterobacteriaceae, and it is this antigen that causes the mucoid character of many Kl2 strains. Best examined of the surface antigens that have a protein nature are the flagellar antigens. We know of 60 different serological forms in E. coli. The fimbriae or pili antigens that are found in many Enterobacteriaceae constitute another group of protein antigens. These antigens have been divided into several types according to morphology and adhesive properties. Among the fimbriae antigens are the plasmid-determined K antigens (e.g., K88 and K99) that act as colonization factors in the small intestine in diarrheal diseases of piglets and calves. A similar antigen is seen in strains of E. coli from humans [18]. These colonization fimbriae or pili also hemagglutinate directly, and this reaction is resistant to mannose. The Kl2 strain used in genetic studies is rough, with deficient O-specific side chains on its lipopolysaccharide, and it has no capsular antigen; the serotype could be written O-:K-:H48. Under
References 1. 0rskov, 1., 0rskov, F., Jann, B., Jann, K. Serology, genetics and chemistry of 0 and K antigens of Escherichia coli. Bacteriol. Rev. 41 :667-710,1977. 2. Hanson, L. A. Host-parasite relationships in urinary tract infections. J. Infect. Dis. 127:726-730, 1973. 3. Howard, C. J., Glynn, A. A. Diphenylamine induced complement sensitivities and associated changes in antigenic structure of Escherichia coli. Immunology 21:951-955,1971. 4. OIling, S. Sensitivity of gram-negative bacilli to the serum bactericidal activity. A. Marker of the hostparasite relationship in acute and persisting infections. Scand. J. Infect. Dis. 9(Suppl. 10):1-40, 1977. 5. OIling, S., Hanson, L. A., Holmgren, J., Jodal, U., Lincoln, K., Lindberg, U. The bactericidal effect of normal human serum in E. coli strains from normals and from patients with urinary tract infections. Infection 1:24-28,1973. 6. Sjostcdt, S. Pathogenicity of certain serological types of B. coli. Acta Pathol. Microbiol, Scand. 63: 1-148, 1946. 7. Smith, H. W., Parsell, Z. The effect on virulence of converting the 0 antigen of Salmonella cholerae-suis from 6 27 to 6 17 by phage. J. Gen. Microbiol. 81:217224, 1974. 8. MakeHi, P. H., VaItonen, V. V., VaItonen, M. Role of 0 antigen (LPS) factors in the virulence of Salmonella. J. Infect. Dis. 128(Suppl.):S81-S85, 1973. 9. Robbins, J. B., McCracken, G. H., GotschIich, E. C., 0rsko\', F. 0rskov, I., Hanson, L. A. Escherichia coli Kl capsular polysaccharide associated with neonatal meningitis. ~. Engl. J. Med. 290: 1216-1220, 1974. 10. Cheasty, T., Gross, R. J., Rowe, B. Incidence of Kl antigen in Escherichia coli isolated from blood and cerebrospinal fluid of patients in United Kingdom. J. CIin. Pat hol. 30:945-947, 1977. II. Kaijser, B., Hanson, L. A., ]ocIa], U., Lidin-janson, G., Robbins, J. B. Frequency of F. coli K antigens in various forms of urinary tract infections in children. Lancet 1:663-664, 1977. 12. 0rskov, F., Biering Serensen, K. Escherichia coli serogroups in breast-fed and bottle-fed infants. Acta Pathol. Microbiol. Scand. [B] 83:25-30, 1975. 13. 0rskov, F., 0rskov, 1. Escherichia coli O:H serotypcs isolated from human blood. Acta Pathol. Microbiol. Scand. [B] 83:595-600, 1975.
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
09,0101, (020)
Immunoelectrophoretic properties
unusual culture conditions the Kl2 strain secretes a slime called cholanic acid. It appears that several of the recognized surface antigens play a role in virulence. Pathogenic strains of bacteria have to be defined by their antigenic structure as well as their fermentation reactions and other metabolic functions. I t is unlikely that the addition of a single factor could convert a nonpathogenic organism to a virulent strain.
633
Cell-Surface Virulence Factors
14. Kauffmann, F. Ueber neue thermolabile Korperantigene der Coli-Bak terien. Acta Pathol. Microbiol. Scand. 20:21-44, 1943. 15. Smith, T., Bryant, G. Studies on pathogenic R. coli from bovine sources. II. Mutations and their immunological significance. j. Exp. Med. 46: 133-140, 1927. 16. Howard, C. j., Glynn, A. A. The virulence for mice of strains of Escherichia coli related to the effects of K antigens on their resistance to phagocytosis and killing by complement. Immunology 20:767-777, 1971.
17. Ka ijser, B. E. coli 0 and K antigens and protective antibodies in relation to urinary tract infection. Doctoral (M.D.) dissertation, University of Coteborg, Coteborg, Sweden, 1972. 18. Evans, D. K, Silver, R. P., Evans, D. J., Chase, D. G .• Gorbach, S. L. Plasmid controlled colonization factors associated with virulence in Escherichia coli entcrotoxigenic for humans. Infec. Immun. 12:656-
667, 1975.
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
Virulence Factors of the Bacterial Cell Surface Frits 0rskov
From the International Escherichia and KLebsiella Center of the WorLd Health Organization, Copenhagen, Denmark
[8] have found that small, induced variations in the 0 polysaccharide have an influence on the virulence of gram-negative bacteria. Of the many known E. coli 0 groups (at the moment there are 163), only a few are highly prevalent in the normal human gut. By use of specific antisera to the 10 most common 0 groups, it is possible to determine the 0 group of about 50% of E. coli in the feces of humans. Studies indicate that the same 0 groups that are common in extraintestinal infections arc those frequently present in the normal gut (table 1). Some 0 groups have been associated with diarrhea due to enteropathogenic E. coli that occurs in infants, and other 0 groups with dysentery-like diarrhea (table 2). In cases of diarrhea of young animals that is caused by enterotoxigenic E. coli, certain 0 groups have been identified that are specific for piglets and others that are specific for calves. \Ve do not know what factors cause this apparent host and disease specificity or how they are related to pathogenicity [1]. There are so-called rough strains and smooth strains. Acute disease is related to the smooth strains. Some studies of urinary tract infections show that rough strains are found in asymptomatic chronic urinary tract infections. Hanson [2] has suggested that the smooth strains found in the first stage of disease mutate into rough strains and thus become less virulent. Strains that actually have a rough lipopolysaccharide may appear to be smooth on artificial media. This morphological smoothness on the plates is caused by a capsular polysaccharide that differs chemically and genetically from the lipopolysaccharide. The "hidden" rough character can be disclosed by heating the culture. Robbins et a1. [9] studied neonatal meningitis caused by E. coli and found that 85CJo of the strains contained KI capsular antigen. Although I O(:~ 15% of the strains were rough, those with a KI capsular antigen were invasive. The KI capsular polysaccharide is an a-2,9-linked N-acetyl neuraminic acid homopolymer that is structurally
Please address requests for reprints to Dr. Frits 0rskov, Statens Serurniustitut, Amager Boulevard 80, DK-2300 Copenhagen S, Denmark.
630
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
Bacterial surface structures are related to properties of virulence. Although these antigens can be associated with invasiveness, resistance to phagocytosis, and intestinal colonization, no single factor or antigen determines pathogenicity. Among the Enterobacteriaceae there are two categories of surface antigens, those composed of polysaccharide and those composed of protein. The polysaccharide antigens can be divided into the lipopolysaccharide 0 antigens and the capsular polysaccharide K antigens. The li popolysaccharides have three regions: (1) lipid A, (2) core oligosaccharide, and (3) O-specific polysaccharide. Lipid A is responsible for the toxic properties of the lipopolysaccharide and is probably similar in the different Enterobacteriaceae. The structure of the core polysaccharide (region II) present in enterobacteria varies, e.g., the same structure has been detected in all Salmonella, but four different ones have been found in Escherichia coli. The O-specific polysaccharide is characteristic of the smooth (S) form of Enterobacteriaceae. This polysaccharide is the chemical basis of the O-antigen specificity of gram-negative bacteria; the various () antigens are specified by the different sugars found in this O-specific side chain. Mutations affecting the synthesis of the O-specific side chain may result in rough (R) variants that give R specificity to the core polysaccharide [1]. Since R mutants are more easily phagocytized and more sensitive to bactericidal activities, they are less pathogenic and less virulent than S forms [2-6]. The specific 0 polysaccharide protects the bacterium against host resistance and is also responsible for the in vitro stability of bacterial suspensions. Although we believe that 0 antigens are important in pathogenicity, we do not have a simple explanation for the role of the different 0 antigens. Smith and Parsell [7] and Makela et a1.
Cell-Surjacc Virulence Factors
631
Table 1. Serogroups of 0 antigen of Escherichia coli isolated from humans with extraintestinal infections and from feces of healthy adults and children.
o serogroups*
Source Urinary tract infections
Septicemia
Other infections
Feces
*Since the prevalence rates were compiled from data of many different investigations, the 0 groups are listed numerically. tThe prevalent 0 groups listed here are characterized by having the same K antigen (K1) when isolated from patients with this disease.
identical to the capsule of group B Neisseria meningitidis. It is of interest that the same capsule confers virulence to two bacterial species. Most capsular polysaccharide K antigens are acidic; they are found in many Enterobacteriaceae, including E. coli, Klebsiella, and Salmonella. Eighty different K polysaccharides exist in E. coli. The K antigens of E. coli may be divided into two groups. One is similar to the capsular antigens of Klebsiella and is associated with 0 groups 08,09,020, and 0101. The second group is associated with several other common 0 groups (table 3). The first group is determined by a genetic locus close to that of histidine. It is interesting to note
Table 2. Identification of 0 groups, O:H types, and O:K:H types of Escherichia coli isolated from humans with in testinal infections [1] . Infection Infantile diarrhea Sporadic cases and outbreaks, mostly in institutions Diarrhea in ad ul ts and children Sporadic cases and outbreaks
Dysentery-like disease, sporadic cases and outbreaks
Classification of E. coli
o groups, O:H types, and
O:K:H types
Enteropathogenic
020,026,044,055,086,0111,0114,0119,0125, 0126,0127,0128,0142,0158
Enterotoxigenic
06:K15:H16, 08:K40:H9, 08:K25:H9, 011:H27, 015:H11, 020:H-, 025:K7:H42, 025:K98:H-, 027: H7, 078:Hll, 078:H12, 0128:H7, 0148:H28, 0149:H10,0159:H20
Enteroinvasive
028ac, 0112, 0124,0136,0143,0144,0152,0164
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
Neonatal meningitis'[
01,02,04,06,07, 08, 09, OIl, 022, 025, 062,075 01, 02, 04, 06, 07, 09, 011,018,022,025, 075 01,02,04,06,08,09, 011,021,062 01,06,07,016,018, 083 01, 02,04, 06, 07, 08, 018,025,045,075, 081
that the locus determining the structure of the O-specific polysaccharide is also close to the histidine locus. The remaining K antigens that are associated with several common 0 groups are genetically determined by a locus close to the serine A locus. Most common in this group of K antigens are KI, K2, K5, K12, and KI3. Because there are more than 80 such antigens and 163 0 groups, theoretically there may be a great number of combinations of the O-K serotypes. However, only a limited number of O-K combinations are common [1]. Not all E. coli have a capsular antigen, but strains associated with invasive disease usually do. The E. coli strains most frequently found in normal intestines also have capsules or belong to serotypes that are frequently encapsulated. The KI antigen is found in > 85% of the different serotypes isolated from human neonates with meningitis [9]. The KI antigen is also the most common K antigen present in E. coli organisms that cause septicemia or pyelonephritis and also in those in the intestinal tract of healthy persons [6,10-13]. Studies with mice and guinea pigs have demonstrated that a capsular variant is more virulent and less easily phagocytized than an acapsular variant of the same strain [6, 14, 15]. Generally, encapsulated serotypes are more frequently associated with invasive disease than uncapsulated serotypes, although there is no agreement on whether this characteristic is always associated with the amount of K polysaccharides [16, 17]. Cholanic acid or 1\1 antigens are genetically determined by loci different from those determining the two K antigen groups. The M antigens
~rskov
632
Table 3. Combinations of polysaccharide a and K surface antigens of Escherichia coli based on chemical and immunoelectrophoretic characterization [1] .
Occurrence
Material
Many 0 groups Neutral LPS and acidic capsular polysaccharide
Neu tral LPS and acidic capsular polysaccharide
o groups 08,
Neu tral LPS and acidic LPS
o groups 08,
Neutral LPS
Many 0 groups
09,0101, (020)
o line: cathodic, slow K line: anodic, fast
o line: cathodic, slow Kline: anodic, slow
o line:
cathodic, slow K line: anodic, slow
o line:
cathodic,
slow Many 0 groups
Acidic LPS
o line:
anodic,
slow Many 0 groups Acidic LPS and acidic capsular polysaccharide
NOTE.
LPS
o line: anodic, slow K line: anodic, fast
= lipopolysaccharide.
are common to most Enterobacteriaceae, and it is this antigen that causes the mucoid character of many Kl2 strains. Best examined of the surface antigens that have a protein nature are the flagellar antigens. We know of 60 different serological forms in E. coli. The fimbriae or pili antigens that are found in many Enterobacteriaceae constitute another group of protein antigens. These antigens have been divided into several types according to morphology and adhesive properties. Among the fimbriae antigens are the plasmid-determined K antigens (e.g., K88 and K99) that act as colonization factors in the small intestine in diarrheal diseases of piglets and calves. A similar antigen is seen in strains of E. coli from humans [18]. These colonization fimbriae or pili also hemagglutinate directly, and this reaction is resistant to mannose. The Kl2 strain used in genetic studies is rough, with deficient O-specific side chains on its lipopolysaccharide, and it has no capsular antigen; the serotype could be written O-:K-:H48. Under
References 1. 0rskov, 1., 0rskov, F., Jann, B., Jann, K. Serology, genetics and chemistry of 0 and K antigens of Escherichia coli. Bacteriol. Rev. 41 :667-710,1977. 2. Hanson, L. A. Host-parasite relationships in urinary tract infections. J. Infect. Dis. 127:726-730, 1973. 3. Howard, C. J., Glynn, A. A. Diphenylamine induced complement sensitivities and associated changes in antigenic structure of Escherichia coli. Immunology 21:951-955,1971. 4. OIling, S. Sensitivity of gram-negative bacilli to the serum bactericidal activity. A. Marker of the hostparasite relationship in acute and persisting infections. Scand. J. Infect. Dis. 9(Suppl. 10):1-40, 1977. 5. OIling, S., Hanson, L. A., Holmgren, J., Jodal, U., Lincoln, K., Lindberg, U. The bactericidal effect of normal human serum in E. coli strains from normals and from patients with urinary tract infections. Infection 1:24-28,1973. 6. Sjostcdt, S. Pathogenicity of certain serological types of B. coli. Acta Pathol. Microbiol, Scand. 63: 1-148, 1946. 7. Smith, H. W., Parsell, Z. The effect on virulence of converting the 0 antigen of Salmonella cholerae-suis from 6 27 to 6 17 by phage. J. Gen. Microbiol. 81:217224, 1974. 8. MakeHi, P. H., VaItonen, V. V., VaItonen, M. Role of 0 antigen (LPS) factors in the virulence of Salmonella. J. Infect. Dis. 128(Suppl.):S81-S85, 1973. 9. Robbins, J. B., McCracken, G. H., GotschIich, E. C., 0rsko\', F. 0rskov, I., Hanson, L. A. Escherichia coli Kl capsular polysaccharide associated with neonatal meningitis. ~. Engl. J. Med. 290: 1216-1220, 1974. 10. Cheasty, T., Gross, R. J., Rowe, B. Incidence of Kl antigen in Escherichia coli isolated from blood and cerebrospinal fluid of patients in United Kingdom. J. CIin. Pat hol. 30:945-947, 1977. II. Kaijser, B., Hanson, L. A., ]ocIa], U., Lidin-janson, G., Robbins, J. B. Frequency of F. coli K antigens in various forms of urinary tract infections in children. Lancet 1:663-664, 1977. 12. 0rskov, F., Biering Serensen, K. Escherichia coli serogroups in breast-fed and bottle-fed infants. Acta Pathol. Microbiol. Scand. [B] 83:25-30, 1975. 13. 0rskov, F., 0rskov, 1. Escherichia coli O:H serotypcs isolated from human blood. Acta Pathol. Microbiol. Scand. [B] 83:595-600, 1975.
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
09,0101, (020)
Immunoelectrophoretic properties
unusual culture conditions the Kl2 strain secretes a slime called cholanic acid. It appears that several of the recognized surface antigens play a role in virulence. Pathogenic strains of bacteria have to be defined by their antigenic structure as well as their fermentation reactions and other metabolic functions. I t is unlikely that the addition of a single factor could convert a nonpathogenic organism to a virulent strain.
633
Cell-Surface Virulence Factors
14. Kauffmann, F. Ueber neue thermolabile Korperantigene der Coli-Bak terien. Acta Pathol. Microbiol. Scand. 20:21-44, 1943. 15. Smith, T., Bryant, G. Studies on pathogenic R. coli from bovine sources. II. Mutations and their immunological significance. j. Exp. Med. 46: 133-140, 1927. 16. Howard, C. j., Glynn, A. A. The virulence for mice of strains of Escherichia coli related to the effects of K antigens on their resistance to phagocytosis and killing by complement. Immunology 20:767-777, 1971.
17. Ka ijser, B. E. coli 0 and K antigens and protective antibodies in relation to urinary tract infection. Doctoral (M.D.) dissertation, University of Coteborg, Coteborg, Sweden, 1972. 18. Evans, D. K, Silver, R. P., Evans, D. J., Chase, D. G .• Gorbach, S. L. Plasmid controlled colonization factors associated with virulence in Escherichia coli entcrotoxigenic for humans. Infec. Immun. 12:656-
667, 1975.
Downloaded from http://jid.oxfordjournals.org/ at Sheffield University on September 9, 2015
