Distribution of Human Commensal Escherichia coli Phylogenetic Groups

Most Escherichia coli infections other than gastrointestinal infections are believed to originate from human fecal flora, and the term “extraintestinal pathogenic Escherichia coli” (ExPEC) was introduced to describe these E. coli strains (13). However, there is an enormous diversity of strains within the species E. coli, making it difficult to clearly identify the potential ExPEC strains among the gut E. coli isolates from healthy people by any simple measure.

One categorization of E. coli isolates that is frequently determined is the phylogenetic group. E. coli strains generally fall into one of four phylogenetic groups—A, B1, B2, and D—and early studies using multilocus enzyme electrophoresis (MLEE) indicated that isolates from human feces are not equally distributed between the groups, with group A predominant, whereas among ExPEC strains, groups B2 and D predominate (see reference 13 and references therein). A subsequent study using a triplex PCR to determine phylogenetic group (1) found a predominance of groups A and B1 (2), and it has become common for authors to state that phylogenetic groups A and B1 “predominate” among commensal E. coli strains.

We have used the same multiplex assay to test 68 distinct E. coli strains recovered from the feces of healthy adults who had not taken antibiotics in the preceding 6 months and found a substantial underrepresentation of the B1 type at 7.4% of isolates (Table 1). This led us to reexamine published data on the distribution of phylogenetic groups among human commensal E. coli isolates. Only data sets that used either a single isolate per individual or a single representative of strains identified by extensive characterization of multiple isolates from the same sample were included, and the total number of isolates listed is 1,889. Specific features of the populations from which samples were collected are listed in the table as footnotes. Comparison of the results of different studies reveals considerable variation in which phylogenetic group is most often encountered, and there is no clear trend toward an excess abundance of groups A and B1 relative to B2 and D. Indeed, B1 is overrepresented (measured as greater than 25% of isolates) in only 5 of the 25 studies listed and is underrepresented in the total at 17.9%. Phylogenetic group A, which currently includes isolates that give no signal with the triplex PCR and may represent distinct types (17), is overrepresented in 16 of 25 studies and in the global total (32.0%). However, phylogenetic group B2 is also overrepresented in 11 studies, including the largest study, which examined 530 isolates. Overall, 29.4% of the total isolates were from group B2.

TABLE 1.

Distribution of phylogenetic groups in commensal E. coli isolates from human feces

Location	No. of isolates analyzeda	Phylogenetic group								Reference
		Incidence (no. of isolates)				% of isolates
		A	B1	B2	D	A	B1	B2	D
United States, Sweden	27	12	2	7	6	44.5	7.4	25.9	22.2	1
Paris, France	56	34	7	6	9	61	12.5	10.5	16	2
Olib and Silba, Croatia	57	20	18	11	8	35	32	19	14	2
Dogon, Mali	55	13	32	1	9	24	58	2	16	2
Michigan	88	18	11	42	17	20.5	12.5	47.7	19.3	19
Franceb	25	12	3	5	5	48	12	20	20	7
Tokyo, Japanc	61	17	0	27	17	28	0	44	28	12
Franced	24	6	5	7	6	25	21	29	25	18
Paris, France	27	8	3	10	6	29.6	11.1	37.1	22.2	3
Brest, France	21	3	5	7	6	14.3	23.8	33.3	28.6	3
Brittany, Francee	25	6	6	8	5	24	24	32	20	3
Brittany, Francef	25	8	7	4	6	32	28	16	24	3
French Guyana	93	59	19	3	12	63.4	20.4	3.2	12.9	3
Cotonou, Benin	46	23	15	8	0	50	32.6	17.4	0	3
Bogota, Colombia	28	16	1	7	4	57.1	3.6	25	14.3	3
Minnesotag	71	11	13	38	9	15	18	54	13	15
Canberra, Australia	77	15	9	35	18	19.5	12.4	45.1	22.9	4
Madrid, Spain	38	19	7	4	8	50	18	11	21	6
Swedenh	149	43	16	69	21	29	11	46	14	11
Swedeni	61	28	12	11	10	46	20	18	16	10
Spain	50	10	17	9	14	20	34	18	28	14
United Statesj	530	119	90	191	130	22	17	36	25	5
Spaink	67	37	12	7	11	55	18	10	16	8
Spain	120	40	23	20	37	33	19	17	31	9
Sydney, Australia	68	27	5	19	17	39.7	7.4	27.9	25.0	This study
Global total	1,889	604	338	556	391	32.0	17.9	29.4	20.7

^aWhere >1 isolate per subject was used, prior identification of strains had been undertaken.

^bHospital staff.

^cHospital food court staff.

^dPregnant women.

^eBank and insurance workers.

^fPig farmers.

^gNewly admitted inpatients with no evidence of acute infection.

^hInfants 0 to 12 months old.

ⁱSchoolgirls aged 7 to 16 years.

^jSix hundred twenty-two subjects were newly admitted hospital patients, for whom disease status is unknown. The remaining 100 subjects were vegetarians, all from Minnesota and Wisconsin.

^kSubjects had suspected acute cystitis.

The combined data from these 1,889 strains thus reveal that groups A and B2 are both somewhat more abundant (32.0% and 29.4% of the total, respectively) than B1 or D (17.9% and 20.7% of the total, respectively) in human feces, and a similar conclusion has recently been drawn by others (16). While both geographic and temporal variation as well as specific features of the populations used may have influenced the outcome of the various studies, the differences could also simply be a reflection of the enormous overall diversity in the E. coli species pool.